Volume 12 - 2024 | https://doi.org/10.3389/fchem.2024.1436389 Bioluminescent high-throughput screening (HTS) assays based largely on the activity of firefly (FLuc) are widely utilised in research and drug discovery we quantify the luciferase-based real-life HTS assay interference from biologically and environmentally relevant metal ions ubiquitously present in buffers and as contaminants in plastics and compound libraries We also provide insights into the cross-effects of metal ions and other key experimental and biological reagents (e.g. and glutathione) to inform HTS assay design A total of 21 ions were screened in three robust HTS assays (“SC” assays) based on the luminescence of FLuc Three newly optimised HEPES buffer variants (“H” assays) were developed for direct luciferase comparison Interference in bioluminescent signal generation was quantified by calculating the IC50 values from concentration-dependent experiments for selected highly active and relevant metal ions Metal ion inhibition mechanisms were probed by variations in specific reagents and the sequence of addition and buffer composition we revealed a significant impact of metal ions’ salts on luciferase-mediated bioluminescence even at biologically and environmentally relevant concentrations The extent of signal interference largely aligned with the Irving–Williams series of metal ion–ligand affinities (Cu > Zn > Fe > Mn > Ca > Mg) supporting previous reports on metal ion-dependent FLuc inhibition the absolute magnitude and relative extent of signal reduction by metal ions’ salts differed between SC and H assays and between luciferases suggesting a complex network of metal ions’ interactions with enzymes The diversity of the tested conditions and variability of responses provided insights into potential interference mechanisms and synergies that may exacerbate or alleviate interference The beneficial influence of EDTA and the impact of glutathione on bioluminescence readout were pinpointed Given the ubiquity of metal ions in analysed samples the causative role in false-positive generation in drug discovery and the wide breadth of luciferase-based assays used in screening awareness and quantification of metal influence are crucial for developing assay validation protocols and ensuring reliable screening data ultimately increasing the critical robustness of bioluminescence-based HTS assays Scheme 1. Mechanism of bioluminescence for D-luciferin (FLuc substrate), coelenterazine (RLuc substrate), and furimazine (NLuc substrate). Adopted from the study by Kaskova et al. (2016) Despite some work on the ionic interference with FLuc-mediated bioluminescence the studies regarding the impact of metal ions on their bioluminescence are limited no comprehensive bioluminescence interference studies in HTS-format assays in the context of screening interference were performed for any of the three enzymatic detection systems it is crucial to determine the influence of metal ions on bioluminescence-based assays using FLuc In this work, various metal ion salts were tested in specific concentration ranges and underwent experimental bioluminescence-based HTS assay conditions established previously (https://www.eu-openscreen.eu/services/bioprofiling-assays.html); three new HEPES buffer variants of those assays were also included to enable more direct comparison between luciferases The main objective of this research was to pinpoint possible interfering metal ion salts that could impair bioluminescence-based HTS assays involving FLuc Identifying these interfering metal ions will enable research workers to prevent compromised interpretations and optimise the design of bioluminescence-based HTS assays ultimately increasing their robustness and saving time and resources by minimising false-positives in early stages of drug discovery Milli-Q water was used to prepare all aqueous solutions All salts available from commercial sources were of analytical grade Iron(III) chloride hexahydrate (# 236489) iron(II) sulphate heptahydrate (#215422) manganese(II) sulphate monohydrate (#M7899) copper(I) tetrafluoroborate (# 677892) and Trizma base (# T6066) were obtained from Sigma-Aldrich Sodium chloride (# 54447) was from Warchem Calcium nitrate tetrahydrate was from Chmes Caesium carbonate (# C2160) was from TCI Potassium tetrachloroplatinate(II) (# 11396315) zinc nitrate hexahydrate (# 10036103) aluminium nitrate nonahydrate (# 15269686) copper(II) nitrate trihydrate (#10124790) nickel(II) nitrate hexahydrate (# 10401651) and sodium nitrate (# 11904281) were from ThermoScientific Acros Potassium carbonate (# 427465708) and sodium sulphate (# 118078707) were from Chempur Ammonium iron(II) sulphate hexahydrate (# 10087291) cobalt(II) nitrate hexahydrate (# 10529380) and lithium nitrate (# 10568620) were from Fisher Chemical Cadmium nitrate tetrahydrate (# 11351579) and gallium nitrate monohydrate (# ALF-032116-14) were from Alfa Aesar PBS (# 10010-015) and EDTA (# AM9260G) were from Thermo Fisher Scientific Glycine (# GLN001) and ATP (# ATP007) were from BioShop Canada BSA (# 160069) was from MP Biomedicals NaOH (# 810981424) was obtained from POCH Positive controls for the luciferases activity assays are as follows: PT-C124 {3-[5-(2-fluorophenyl)-1,2,4-oxadiazol-3-yl]benzoic acid} (VWR # BIOV9421-10) and N-benzyl-p-toluenesulfonamide BTS (VWR # J64910 Luciferase enzymes for the activity assays were as follows: the firefly enzyme (Promega # E1701) and Renilla enzyme (RayBiotech # RB-15-0003P-50) The substrates for the activity assays were beetle luciferin (Promega # E1603) and coelenterazine (Promega # S2001) All bioluminescent signal generation experiments were performed in 384-well plate formats The assay plates used were the LUMITRAC 384 (#781075) white from Greiner Bio-One Multidrop Combi (Thermo Fisher) non-contact dispenser was used to add solutions of enzymes and substrate to the assay multi-well plates Measurements of bioluminescent signal generation in the corresponding buffers were recorded with a CLARIOStar (BMG Labtech) plate reader The pH measurements were carried out in vials with a Mettler Toledo™ FiveEasy FP20 pH metre Abbreviations used throughout the text are listed alphabetically: N-benzyl-p-toluenesulfonamide (BTS) half maximal inhibitory concentration (IC50) Ataluren (3-[5-(2-fluorophenyl)-1,2,4-oxadiazol-3-yl]benzoic acid (PTC-124) All metal salts were abbreviated to their corresponding metal ion (e.g. For several salts containing both the same metal ion and oxidation state (e.g. The following abbreviations have been used for the corresponding salts: AgNO3 The negative controls had the same %DMSO as the corresponding positive controls (0.04% for FLuc luminescent signal was measured using a CLARIOStar plate reader Final experimental conditions for each luciferase activity assay the luminescent signal was measured using a CLARIOStar plate reader and RLuc activity assays were carried out in screening conditions (SC) and in HEPES conditions (H) for 0.01 and 5 mM of the final metal ion salt concentrations The data were analysed with KNIME software and RLuc activity assays were carried out both in SC and in H with at least 11 concentrations of metal ion salts in the range 0.16–20 mM as the final concentrations Every concentration of each metal was tested in triplicates on the same plate if no top or bottom plateau was observed in the IC50 curve additional experiments were performed for extended concentration ranges and relative %INHIBITION values were combined on one figure for IC50 curve fitting The data were analysed with KNIME software (see below) and bottom of plateau) and 1 mM were chosen as the final concentrations Several pre-incubation tests were carried out with the same SC final conditions but with different orders of addition and longer incubation time (30 min instead of 10 min) ATP + M then S: FLuc assay with the subsequent addition of substrate and enzyme to a 30-min pre-incubated solution of ATP + metal E + M then S: addition of a solution of substrate (+ATP in the case of FLuc) to a 30-min pre-incubated solution of metal + enzyme S + M then E: subsequent addition of enzyme (and ATP in the case of FLuc assay) to a 30-min pre-incubated solution of substrate + metal (grey columns) EDTA testing was carried out in SC for NLuc with the final concentrations 0 and 0.5 mM and for RLuc with 0.25 and 0.5 mM Corresponding EDTA concentrations for the EDTA–enzyme and EDTA–substrate solutions to be added to the well for NLuc were 4x (5 µL) and 2x (10 µL) whereas the corresponding EDTA concentrations for the EDTA–enzyme and EDTA–substrate solutions to be added to the well for RLuc were 2x (5 µL) and 1x (10 µL) GSH testing was carried out with the final concentrations of 0 Corresponding GSH concentrations for the GSH–enzyme and GSH–substrate solutions to be added to the well were 4x (5 µL) and 2x (10 µL) KNIME pipeline was generated and applied for the analysis of the results The raw data files (one txt file per plate) were read and matched with plate template followed by calculation of averages and standard deviation of controls and compound wells and Z′ factor values for each plate generating one dataset for all the tested plates Automatic outlier removal was used for detecting control outliers for plates with Z′ factor values below 0.5 The plates for which removal of the outliers did not lead to improvement of the Z′ factor (higher than 0.5) or the algorithm was detecting more than two outliers were retested The raw data values were normalised to positive and negative controls for each plate to calculate percent inhibition (% INHIBITION = (1-(x- μp)/(μn–μp))* 100%) Z' = 1- (3*(SDp + SDn)/(μn - μp)) signal to background ratio (S/B = μn/μp) variance coefficient (CV = SD of population/mean *100%) percent normalised bioluminescent signal (% N_VALUE = (x/μn)*100) and normalised bioluminescence signal change (% N_SCh = (x - μn)/μn*100) where x represents the readout VALUE of the well μp represents the mean of the positive controls μn represents the mean of the negative controls SDn represents the standard deviation of the negative controls and SDp represents the standard deviation of the positive controls for each tested assay plate The heatmap of % INHIBITION was then generated for each plate in order to identify plate effects or signal distribution patterns a validation plate (no metal ions added) was run for each assay under the screening conditions All raw data as well as platemaps and calculated QC parameters are provided in Supplementary Tables 1, 2 spreadsheet files attached in the Supplementary Material second sets of aliquots were added to the same vials to reach a final concentration of 5 mM for all salts (except Zn in SC RLuc buffer These experiments were performed in triplicates Concentrations (mM) of each metal ion at their respective addition steps (x To 5 mL of 100 mM HEPES buffer, aqueous stock solutions of metal ion salts (0.2 M, Ag, Cu(II), Fe(II)-1, Fe(II)-2, Fe(III), and Zn) were added in four incremental steps into the same vial. The volume added at each step was equal to the volume required to achieve the concentration as indicated in Table 2 (x1 with the final addition leading to the concentration of 5 mM The pH was measured upon stirring before and after each addition and the experiment was repeated in triplicates The highest Z’ factor value of 0.88 was observed for the NLuc assay in HEPES (H) conditions vs the assays in SC exhibited slightly higher Z’ factor values (respectively Each condition for a given type of experiment was performed in triplicate on the same plate but every sample is prepared independently and each experiment type was performed on a different day All of this confirms the robustness of the assays and the lack of position-dependent artefacts enabling reliable data generation independent of the plate design 26 salts of 21 different biologically and environmentally relevant metal ions were selected Most of the salts were in the form of highly soluble nitrates and tin(II) (Sn (II)) as chlorides; iron(II) (Fe(II)-1 and 3) and sodium (Na-3) as sulphates; potassium (K-2) and cesium (Cs(I)) as carbonates; and copper(I) (Cu(I)) as a tetrafluoroborate In order to get insight into the ionic strength and/or anionic effects three different salts of sodium (sodium nitrate,Na-1; sodium chloride two different salts of potassium (potassium nitrate and three different salts of iron(II) (ammonium iron(II) sulphate hexahydrate The aqueous solutions of three of the selected metal ions (Fe(II) and they needed to be prepared freshly every time and used immediately after dissolution in water/buffer Fe(III) tends to form various water insoluble oxides that precipitate out of the solution in time and/or at higher concentrations leading to a change in effective metal concentration that cannot be easily estimated Fe(II) and Cu(I) are also particularly susceptible to oxidation even in air and so they needed to be handled with care and just for short periods of time In addition to having high oxidation susceptibility most of the widely available Cu(I) salts remain rather insoluble in aqueous solutions the acetonitrile Cu(I) complex was used as a source of Cu(I) The salt is relatively stable in the solid form and is highly soluble in acetonitrile that stabilizes the Cu(I) state After subsequent dilution of acetonitrile stock solutions of Cu(I) in water the ion becomes highly susceptible to oxidation (and partial or total ligand exchange to water can occur); therefore Cu(I) aqueous solutions were freshly prepared every time and measured immediately after addition to the reaction buffer with lower but statistically significant quenching effect (between 71.2% and 90.8% of residual signal) noticeable for Al Normalised bioluminescent signal in the presence of three different concentrations (0.01 white) of metal ion salts in optimised luciferase activity assays of (A) FLuc SC (10 µM substrate and pH 7.5) (C) NLuc SC (10 µM substrate PBS pH 7.4 0.75% 0.1% BSA) (D) NLuc H (100 mM HEPES Positive controls (red) used are PTC-124 (1 µM) The negative controls (green) had the same %DMSO as the corresponding positive controls.Each condition for a given type of experiment was performed n = 3 on the same plate but every sample was prepared independently and each experiment type was performed on a different day Normalisation of the bioluminescent signal was carried out against the negative control output of the corresponding bioluminescent assay plate Statistical two-tailed Student’s t-test (95% confidence) was carried out between a given sample and the corresponding negative control The samples were deemed statistically different from the negative control for p < 0.05 and were marked with black “*.” Summary of the effect of metal ion salts on bioluminescent signal (residual % signal after the addition of metal 0%: full quenching) in screening buffer and in HEPES buffer for FLuc For NLuc and RLuc assays in SC (Table 3; Figures 2C, E respectively) little to no effect was observed for any of the metal ions at 0.01 mM with the exception of Ag in the NLuc assay Very similar trends (and similar types of metal ions) were observed for both at higher concentrations with almost complete quenching observed for Ag and Pt(II) at 1 mM and 5 mM concentrations and Ga(II) quenching in the NLuc SC assay was less pronounced than that in the RLuc one and the effect was even more clearly visible at 5 mM concentration for Pb(II) (only 6% residual signal in RLuc vs 44.2% in NLuc) and especially Ca(II) (19.5% in RLuc vs In analogous assays with NLuc and RLuc, but in HEPES buffer conditions (Table 4; Figure 2C vs. Figure 2D for NLuc; Figure 2E vs. Figure 2F for RLuc) SC at even 5 mM concentrations is observed for Sn(II) on RLuc and NLuc and for Ca(II) in the RLuc H assay is observed in the RLuc assay for Ga at 1 mM (no quenching in SC vs only 10.6% residual signal remaining in H) the opposite effects of changing the buffer from SC to H when comparing both luciferases are observed for Cd and Co(II) (weakened for NLuc but more pronounced for RLuc) as well as Pb(II) (weakened for RLuc but exacerbated for NLuc) IC50 values from the curve fitting for each luciferase activity assay in SC and in H including Sn(II) in particular for all assays but FLuc in SC 100% inhibition was not achieved even at the highest concentrations leading to an inadequate fit and no reliable IC50 estimation In the case of Ag and Cu(I) salts in the FLuc H assay the inhibition was very significant even at the highest concentration leading to the lack of reliable IC50 fit but clearly indicating that the value of that parameter lies below 0.1 µM Further examination of the IC50 and the curves largely confirms qualitative observations from the initial screen the influence of metal ions is more pronounced in FLuc assays with the following order of the strength of inhibition according to IC50 values (the lower the IC50 value Cu(I) (0.01 µM) > Cu(II) (0.07 µM) > Zn (0.88 µM) > Cd (1.21 µM) > Fe(II)-3 (2.73 µM) and Pb(II) (2.74 µM) > Ga (11 µM) > Fe(II)-1 and Fe(III) (all between 22–24 µM) > Co(II) (31 µM) > Pt(II) (40 µM) The IC50 values in the SC conditions for the FLuc assay are in the same order of magnitudes for Fe(III) and Pt(II); only slightly higher (weaker inhibition) for Ag (0.24 µM in SC); one order of magnitude higher for Co(II) and Fe(II)-2; two orders of magnitude higher for Fe(II)-3 and Cd; more than three orders of magnitude larger for Zn and Cu(II); and over 10,000 times larger for Cu(I) only Ag in the SC buffer has an IC50 value below 10 µM (4.5 µM); Ag in the H buffer and Cu(I) and Cu(II) in both H and SC buffers exhibit IC50 values between 22 µM and 56 μM with the rest of the metal ions’ IC50 being above 100 µM in both H and SC and Sn(II) in both SC and H and Pb(II) in SC conditions the strongest inhibition is seen for Cu(II) ions in the H condition (7.79 µM) with Cu(I) and all iron salts in the H buffer and Ag in both H and SC being within the 18–68 µM range and Sn(II) in both buffers have all shown IC50 values of above 1 mM higher inhibition can be found generally in the H conditions with Ag being approximately 2 times less inhibiting in SC than in H and Zn salts having one order of magnitude higher IC50 values in SC than H Co(II) (688 µM in SC) and Pt(II) (350 µM in SC vs 723 µM in H) are the only metal ions with higher inhibitory effect in SC than in H for RLuc assays a handful of the most potent and biologically relevant metal ions were selected to further investigate the nature of the potential interference of metal ions with bioluminescent signal generation in luciferase activity assays This included Ag (highest potency across the board) and high abundance in environment as well as impurity) and Zn due to its biological and environmental ubiquity All of the experiments below will therefore involve only these selected metal ions Result of pH titration experiments (with standard deviations n = 3) of various metal ions in SC conditions and in H conditions for different concentrations (see Table 2 for concentrations of x the addition of the first aliquot did not change the pH significantly apart from Zn (2.5 mM led to a decrease in pH from 6.89 to 5.39) whereas 5-mM solutions of all the metals led to a comparable drop of 1–1.5 pH units in the case of Ag and Fe(II)-2 (to 5.97–5.75); almost two pH units drop for Zn (to 5.05); and a dramatic drop to pH 3.53 mM for Cu(II) and 3.29 mM for Fe(III) Similarly, little to no decrease in the pH was observed with the addition of the first metal aliquot to the SC RLuc buffer (50 mM Tris-HCl, 12.5 mM KH2PO4, 125 mM NaCl, 0.25 mM EDTA, 0.1% BSA, and 0.3 M sodium ascorbate; Table 1) apart from Zn (drop from 7.03 to 6.54 for 5 mM solution and then 5.84 for 10 mM solution) the pH of the solution for all of the metals ranged between 6.37 (for Fe(III)) and 6.92 (for Ag) In case of the NLuc screening buffer (Table 1; PBS 0.75% × 0.1% BSA) no change in the pH was observed even for 5-mM concentration of Ag Initial addition of Cu(II) (20 µM) did not change the pH the pH dropped to 4.89.5 mM of Fe(II)-1 whereas Fe(II)-2 solution had a pH of 6.73 at 2.5-mM concentration and 6.28 at 5-mM Fe(III) induced most dramatic changes with pH 5.74 (2.5 mM) and 2.71 (5 mM) the addition of 5 mM of Zn to NLuc SC led to a pH of 5.55 metal ion salts were also pre-incubated with ATP as a potentially reactive and yet critical element of the buffer Four different concentrations of the salts (for Ag(I) in FLuc only three concentrations) were selected based on IC50 experiments including 1 mM (same for all the salts) the concentration near the IC50 value itself and one lower and one higher than that (respectively closer to concentrations inducing the lower and upper limit responses in the IC50 curve for a given assay) Normalised percentage of bioluminescent signal for (A) FLuc and (C) RLuc assays for different pre-incubations FLuc assay with subsequent addition of substrate and enzyme to a 30-min pre-incubated solution of ATP + metal salt (white dashed) Addition of a solution of substrate (+ATP in the case of FLuc) to a 30-min pre-incubated solution of metal salt + enzyme (black) Subsequent addition of enzyme (and ATP in the case of FLuc assay) to a 30-min pre-incubated solution of substrate + metal (grey) Positive controls used are PTC-124 (1 µM) The negative controls had the same %DMSO as the corresponding positive controls Normalisation of the bioluminescent signal was carried out against the negative control output given for each independent pre-incubation condition Statistical two-tailed Student’s t-test (95% confidence) was carried out between a given sample and the corresponding negative control both at the same pre-incubation conditions a pre-incubation of Ag with enzyme leads to almost complete quenching (no signal) for even the lowest Ag concentration whereas ATP or substrate pre-incubation with Ag salt leads to higher signal than that without pre-incubation (so weakens its quenching effect) A somewhat similar but weaker effect has been observed for Fe(III) at IC50 concentration of 4.7 µM and also above (20 µM) and for high Zn concentrations (1 mM and 1.25 mM) in case of Fe(II)-1 salt at lower concentrations (25 μM and 75 µM) pre-incubation with substrate first leads to maintaining of the level of quenching observed when no pre-incubation is applied (same as for IC50 value in pure SC buffer) whereas enzyme or ATP-pre-incubation causes higher signal (weaker quenching) than that without pre-incubation The effect is reversed for 0.5-mM concentration at which near-complete quenching is observed for enzyme pre-incubation with least quenching (most residual signal) at ATP pre-incubation For both NLuc and RLuc exposed to Ag salt or Zn salt pre-incubation of metal ion salt with enzyme leads to lower bioluminescent signal (stronger signal quenching) than pre-incubation with the substrate The same is true for NLuc with Fe(II)-1 and Fe(III) the order of pre-incubation seems to have little to no effect on Fe(II)-1-induced quenching with less residual signal (stronger quenching) for Fe(III) at higher concentrations Cu(II) presence quenches the signal more strongly (lower residual signal) in case of pre-incubation with a substrate with much lower (or even none) quenching observed when pre-incubated with an enzyme first Normalised percentage of bioluminescent signal for (A) NLuc and (B) RLuc assays with the original EDTA concentration in screening conditions (black; 0 mM for NLuc and 0.25 mM for RLuc) and the same EDTA concentration as in FLuc assay screening conditions (grey; 0.5 mM) Normalisation of the bioluminescent signal was carried out against the negative control output given by the original screening conditions (lowest EDTA concentration) of the corresponding bioluminescent assay plate Statistical two-tailed Student’s t-test (95% confidence) was carried out between a given sample (at a given EDTA concentration) and the negative control at lowest EDTA concentration The samples were deemed statistically different from blank for p < 0.05 and were marked with black “*.” 0.5-mM EDTA slightly increases the bioluminescent signal for all samples with Ag at 68 μM and 200 µM concentrations and Cu(II) at 132 µM concentrations (all near the IC50 values of the original SC assay) being the most affected (the largest increase in bioluminescent signal in the presence of EDTA) and (C) RLuc assays with 0 mM (black columns) and 2 mM (black columns) concentration of glutathione (GSH) Normalisation of the bioluminescent signal was carried out against the negative control output given by the original screening conditions (lowest GSH concentration) of the corresponding bioluminescent assay plate Statistical two-tailed Student’s t-test (95% confidence) was carried out between a given sample (at a given GSH concentration) and the negative control at lowest GSH concentration presents a statistically significant increase in activity with 0.2-mM GSH and even more with 2-mM GSH leads to the weakening of inhibition of RLuc by all of the tested metals with the effect being most pronounced for Ag and Cu(II) Screening and subsequent investigations have been performed for a broad panel of environmentally and biologically relevant metal ions and their concentration ranges (Sigel and Sigel, 2000; Maret, 2016; Shamsollahi and Partovinia, 2019; Adams et al., 2020) increasing the significance of any observed metal ion-induced quenching of bioluminescent signals These effects could arise from various processes including direct interaction with a luciferase enzyme interference with substrate binding or turnover substrate and reactants’ sequestration or alterations in the chemical environment required for the bioluminescent reaction As all of those processes are broadly dependent on the same type of affinities of metal ions to various ligands such as amino acid residues on enzymes discerning these mechanisms remains challenging Diverse experimental designs discussed above allowed quantifying the effects and providing insights into the role of reactants and buffer components in metal-mediated interference with luciferase-driven bioluminescent signal generation Nearly all tested metal ions’ salts led to statistically significant reduction of bioluminescent signal of the FLuc system even at 1-mM concentration Alkali metal ions salts showed the weakest inhibition that is relatively independent of the FLuc assay buffers (similar for both SC and H) which might suggest a non-specific quenching mechanism (e.g. their ubiquitous presence in buffers and biological as well as environmental samples often at well into millimolar concentrations can have a significant effect on bioluminescent readout and requires careful consideration supporting direct metal ion–enzyme interaction as a cause of inhibition observed in our experiments leading to a change in the stability of the light-emitting oxyluciferin product still exhibits the strongest inhibition when pre-incubated with FLuc substrate-metal ion pre-incubation leads to stronger quenching than ATP-metal ion pre-incubation This supports previously reported hypothesis that apart from direct enzyme–metal ion interaction FeSO4 can also reduce bioluminescent signal through the precipitation of D-luciferin substrate NLuc and RLuc that do not require ATP and both use similar substrate types that are displayed relatively higher tolerance to metal ion interference with fewer metal ion salts exhibiting significant inhibitory effects at low concentrations and most IC50 values oscillating in the higher micromolar to millimolar range Higher FLuc sensitivity is particularly visible when comparing low metal-affinity HEPES-based assay variants that were designed to minimise buffer–metal binding and the buffer variability between different luciferases (HEPES buffer has been shown to have negligible binding to metal ions; however each of those assays still differ by the additives that came out essential to ensure sufficient assay quality) all active metal ion salts tested exhibited from two (Fe(II) salts in RLuc H vs FLuc H assay) to over thousand times (Cu(I) for NLuc H vs FLuc H assay) higher IC50 values (lower inhibition) for NLuc H and RLuc H assays than in the FLuc H one The variability in inhibition efficiency is much smaller between NLuc and RLuc (only up to 10 times the difference) with NLuc being generally more resistant than RLuc This is in line with the fact that NLuc is a bioengineered version of natural RLuc The exceptionally stronger inhibition of NLuc than RLuc in the H assay by Zn and Pt(II) might stem from the differential presence of ascorbate in the RLuc H assay which is a known and highly potent Zn ionophore (i.e. binds strongly to Zn2+ and potentially also to chemically similar Cd2+ and Pt2+ ions depleting the effective concentration of “free” metal ions in the RLuc H assay) With limited insights into the mechanism of NLuc and RLuc activity and regulation (Liu and Escher, 1999; Loening et al. 2006; Schenkmayerova et al., 2023; Nemergut et al. 2023) the mechanism of metal ion interference with RLuc- and NLuc-mediated bioluminescence is very poorly studied Pre-incubation experiments described in this manuscript for NLuc SC and RLuc SC assay conditions shed some light on this process pre-incubation of NLuc and RLuc with Ag and Zn and RLuc with Fe(II) led to more pronounced quenching indicating direct metal–enzyme interaction Reversed effects observed for pre-incubation of furimazine (NLuc substrate) with Cu(II) and coelenterazine (RLuc substrate) with Cu(II) and Fe(III) suggest substrate interaction or sequestration by those metals The nature and composition of the buffer system played a crucial role in modulating the extent of metal ion interference observed in the bioluminescent assays by binding/precipitation and lowering of effective availability of metal ions for interaction with luciferase/substrate/reactants was used to unify the buffering system across all luciferases; however some additives (like BSA for NLuc and RLuc and MgSO4 for FLuc) could not be eliminated as they turned out to be essential to ensure sufficient luciferase activity and quality and robustness of the assays (Z′ factor and signal-to-background ratios above recommended thresholds) Certain metal ions, especially Cu(II) and Fe(III) at millimolar concentration, led to substantial pH decrease in SC buffers and especially in FLuc assay, potentially disrupting the optimal pH range for FLuc activity (Schenkmayerova et al., 2023) and demonstrating superior buffering capacity of HEPES buffering systems together with simpler buffer composition and higher sensitivity of all enzymes to metal ion effects in the HEPES buffer such as direct enzyme inhibition or substrate interference may be more prominent drivers of metal ion-induced quenching in this system together with the fact that Zn and Cu(II) IC50 values for FLuc and RLuc (bot not NLuc) drastically increase when moving from simpler H to TRIS and EDTA-containing SC conditions points at those chelators as key protective additives of analysed luciferase buffer systems These findings collectively highlight the importance of considering buffer composition and potential interactions between buffer components and metal ions when evaluating their impact on bioluminescent assays we screened comprehensive and diverse panel of metal ion interferents highlighting their significant influence on bioluminescence-based high-throughput screening (HTS) assays involving firefly luciferase (FLuc) It is noteworthy that the observed quenching effects occurred within biologically and environmentally relevant concentration ranges of metal ions underscoring a significant impact on HTS campaigns and the subsequent interpretation of screening data The susceptibility to metal ion-induced quenching varied among the three luciferase systems with FLuc exhibiting the highest sensitivity This variability and differential effects of buffer compositions and GSH highlight the complexity of the underlying mechanisms The findings have important implications for the design and interpretation of bioluminescence-based HTS assays emphasising the need for rigorous assay validation protocols and potentially incorporating mitigating strategies such as the use of chelators or alternative luciferase systems depending on the anticipated metal ion composition of the samples or compound libraries we reported a panel of three pairs of high-quality HTS assays for the activity of each of the three luciferases and often complementary sensitivities to different metal ions This allows future users to select an assay that is best suited to the type of anticipated metal contamination the FLuc HEPES assay serves as a wide-spectrum metal ion detection assay with sub-micromolar sensitivity for quality control of samples/compound libraries and for hit validation to flag possible metal-induced false-positives By elucidating the influence of metal ions on these widely used bioluminescent reporter systems and providing a set of new high-quality HTS assays for the activity of the three most commonly used luciferases we contribute to the ongoing efforts to enhance the robustness and interpretability of HTS campaigns in drug discovery and biological research The original contributions presented in the study are included in the article/Supplementary Material; further enquiries can be directed to the corresponding author The author(s) declare that financial support was received for the research The authors acknowledge the financial support of the Foundation for Polish Science (FNP) for the Homing (grant no POIR.04.04.00-00-441F/17-00 (FC the National Science Centre of Poland (NCN) for the Sonata (grant no 2017/26/D/NZ1/01234 (MK the European Union for the grant iCare—Integrated assessment and advanced characterisation neuro-nanotoxicity (no HORIZON-CL4-2022-DIGITAL-EMERGING-01 (DK and the Polish Ministry of Science and Higher Education (previously MNiSW (decision no DIR/WK/2018/06)) for involvement in the joint international project entitled European Infrastructure of Open Screening Platforms of Chemical Biology European Research Infrastructure Consortium (POL-OPENSCREEN The authors are also pleased to recognise the expert support and access to the Centre for Chemical Biology (ERIC) infrastructure at IBCH PAS supported by the Ministry of Science and Higher Education (decision no DIR/WK/2018/06) The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fchem.2024.1436389/full#supplementary-material Bioavailability assessment of metals in freshwater environments: a historical review PubMed Abstract | CrossRef Full Text | Google Scholar Intracellular ionic strength sensing using nanoluc PubMed Abstract | CrossRef Full Text | Google Scholar Auld, D. 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This oceanfront apartment with a wraparound balcony and sweeping view of the Atlantic Ocean was purchased for $3.4 million in 2006 by Daniyar Kesikbaev the brother of then-Kazakh President Nursultan Nazarbaev became part of a rancorous lawsuit in the United States between Bolat and his ex-wife That dispute also involved millions of dollars in Manhattan real estate as well as what Bolat’s lawyer described as “over $50 million” worth of jewelry purchased with his client’s money The Real Deal, a real estate industry site, reported shortly after the sale that the apartment had been on the market since the previous fall around a year after Kesikbaev transferred ownership to Bolat The fight over the Florida apartment was not the only property dispute for Bolat Nazarbaev in the Miami area he sued a developer for alleged breach of contract over a balcony he claimed was insufficiently private His complaint stated that Bolat paid a $1.2 million deposit for an apartment that the developer indicated would feature “private” balconies. In reality, the balcony for the apartment he planned to purchase “was not private at all,” the complaint said “The privacy of the balcony is particularly important for the buyer in this case. Bolat Nazarbayev is the brother of the President of Kazakhstan. A private balcony is necessary for security reasons,” the Courthouse News Service cited the complaint as saying Bolat requested that the developer return his deposit and court records indicate the two sides reached a confidential settlement When it was last sold, the Margo Way mansion, located in a cul-de-sac in one of the wealthiest postal codes in the United States, was reportedly among the most expensive homes sold in state history The purchaser was hidden behind an anonymous company Initial press speculation suggested a Russian oligarch was behind the purchase federal court suggest that the home purchase was funded by Bolat Nazarbaev the brother of former Kazakh President Nursultan Nazarbaev just a few months after Bolat became embroiled in a bitter legal fight with his ex-wife over ownership of several Manhattan properties A proposed settlement submitted by Bolat’s lawyer in New York State Supreme Court in March 2014 stated that his client would relinquish any claim against Kurmangalieva relating to the property “located at 2 Margo Way New Jersey.” Court papers filed as part of the lawsuit identified 2 Margo Way as the residence where Kesikbaev and Kurmangalieva lived New Jersey property records show that the property has not been sold since the anonymous New Jersey-incorporated company bought it for $20 million in 2012 Precisely where the money for the home purchase came from remains unclear But in a February 2014 e-mail to Kurmangalieva’s U.S Bolat Nazarbaev’s attorney wrote that “we believe” the New Jersey property “was purchased with Mr Nazarbayev’s money” and estimated its value as more than $20 million attorney John Snyder also indicated that Bolat Nazarbaev had acquired more than $50 million in jewelry that Kurmangalieva was holding onto Nazarbayev has agreed to release claims against your clients relating to jewelry that Ms Kurmangaliyeva has appropriated for herself valued in excess of $50 million,” Snyder wrote Kurmangalieva has been listed as an executive or shareholder in several Kazakh companies Kesikbaev married the daughter of Malaysia’s prime minister a seller of expensive Hermes handbags in New York sued Kurmangalieva after she refused to pay a bill of more than $400,000 for the bags she had purchased Kurmangalieva at one point threatened the seller telling her in a phone call: “You know who my son is He is the son-in-law of the prime minister of Malaysia Do you know what we can do to you and your family Kurmangalieva and Bolat Nazarbaev have a son together: Khanbolat Nazarbaev Nazarbaev’s New York lawyer from the lawsuit told RFE/RL that he no longer represented Nazarbaev and did not know how to contact him E-mails sent to Nazarbaev-linked investment companies in Almaty and to a charity he heads went unanswered as of publication A message sent to a WhatsApp number for Kurmangalieva was opened and read but was not responded to Kesikbaev did not respond to a Facebook message seeking comment Property records show that more than a decade ago, the owner of the 215-237 block on Baker Street was a company called Farmont Baker Street Limited That record is part of a larger backstory of the property, which was the focus of an exposé by the anti-corruption watchdog Global Witness published in July 2015 then-Kazakh President Nursultan Nazarbaev’s former son-in-law The properties were acquired between 2008 and 2010 by four British-registered companies that either share a common parent — a shell company in the British Virgin Islands — or a direct corporate lineage according to Global Witness and property and corporate registry records reviewed by RFE/RL Among the strongest evidence tying the property to Rakhat Aliev is the extensive overlap among directors between these companies and others directly owned by Aliev prior to his death But documents obtained by RFE/RL and first published by the London-based organization SourceMaterial show that as of 2015 the owner was a British Virgin Islands shell company called Farmont Investors Corporation Corporate documents showed Farmont Investors was ultimately controlled by Nurali Aliev’s mother Darigha Nazarbaeva -- the former wife of Rakhat Aliev and the elder daughter of Nazarbaev Not long after the publication of the Global Witness report ownership of the Baker Street property was switched to another company According to SourceMaterial this appeared to be an effort to avoid new regulations aimed at cutting down on corrupt money flowing into British real estate E-mails sent to the London law firm that has represented Nazarbaeva were not responded to prior to publication An e-mail seeking comment from a public relations agency that Nazarbaeva and Aliev have used in the past went unanswered as of publication SourceMaterial said that Nazarbaeva’s lawyers declined to answer detailed questions about the Baker Street property’s ownership Documents reviewed by RFE/RL suggest that the new ownership structure under Landmark Network continues to have multiple ties to Darigha including overlapping officers who worked for her deceased ex-husband The Global Witness report helped lead to an investigation by the National Crime Agency and so-called “unexplained wealth orders” targeting properties owned by Nurali and Darigha but rather others in the London area that shared several past corporate owners and directors — and linked back to Nurali Aliev and Darigha a British court rejected the crime agency’s arguments that the properties were acquired by Rakhat Aliev prior to his death as a way to launder money is perched on a south-facing hillside plot overlooking the Mediterranean Sea in one of Cannes’ most exclusive neighborhoods Many of the houses in the neighborhood are hidden behind high walls and appear to have bodyguards and security cameras the last time the property changed owners was in January 2008 when a company called Khanika purchased it for 22.9 million euros ($34 million) Khanika’s ownership structure or beneficial owners could not be determined though a company with a similar name appears in court records in nearby Monaco and a Monaco-based bank appeared to provide financing for the transaction A real estate brochure published in August 2020 described the property as fulfilling “all the criteria corresponding to the mythology of the Riviera: a historical past illustrious owners and an inordinate splendor The property was one of several that Bolat Nazarbaev and his ex-wife Maira battled over in a bitter U.S lawsuit that grew out of their divorce in the early 2010s court records indicate a settlement was reached sometime in 2014 though it is unclear what kind of agreement was reached concerning the Cannes property The court records also suggest the property was at one point owned by a trust registered in the name of the couple’s son the nephew of former Kazakh President Nursultan Nazarbaev Khanbolat was 9 years old when his parents divorced it was not clear if the property was still for sale When RFE/RL journalists photographed the house in September Laundry was visible hanging to dry in the courtyard and several open windows could be seen on the house 41 Reeves Mews were purchased together in 2007 for 25.8 million pounds ($50.9 million) by a shell company called Merix International Ventures 41 Upper Grosvenor had been vacant for about seven years which triggered both annoyance and curiosity in the neighborhood was bought in August 2007 for 11.9 million pounds ($24.4 million) by a company in Luxembourg owned by Kulibaev was bought later that year by a Luxembourg-registered company called Lynn Properties for 8.35 million pounds ($16.9 million) the four properties are effectively part of a single unit According to a 2015 lawsuit filed in British court by a real estate investor who claimed he had been jilted out of millions of dollars Merix International Ventures was a wholly-owned subsidiary of a British Virgin Islands company called Kipros whose ultimate beneficial owner was Kulibaev That’s backed up by corporate registry documents all four properties -- the two Upper Grosvenor and the two Reeves Mews properties -- belonged to Kulibaev through Merix and the Luxembourg-incorporated Vitala Investment Holding located in a historic building in Manhattan’s famed Wall Street district were also caught up in the legal fight between Bolat Nazarbaev and his ex-wife had used his stepfather’s money to buy the two apartments some six years earlier as an investment for Bolat Daniyar took possession of them for himself and his mother apartment 702 was sold by Kesikbaev in 2011 for $940,000 was sold by Bolat for an undisclosed price in 2016 Perched on a southern-facing hillside overlooking Spain’s Mediterranean coast the sprawling property known locally as Can Juncadella was first developed by a Spanish industrialist around the end of World War II It was later bought by a Japanese company that operated a school on the grounds \nThe property was sold in 2007 and since then it has become a regular source of legal controversy the estate is widely believed to belong to former Kazakh President Nursultan Nazarbaev himself a theory referenced in a November 2012 court ruling in the nearby town of Blanes The mansion is “said to be the property of the President of the Republic of Kazakhstan,” the ruling stated Unconfirmed news reports said Nazarbaev himself attended a party at the property Nazarbaev’s press secretary did not answer repeated phone calls made over several days by RFE/RL An e-mail sent to the main office for the Nur Otan political party The assertion of Kazakh ownership is backed up in corporate filings a company registered in Barcelona called Flinder Data acquired the property for an unknown price Flinder Data was owned by a Dutch-incorporated company called Faltain which was in turn owned by another entity called Steppe Unity Cooperative Steppe Unity is owned in part by Timur Kulibaev one of Kazakhstan’s wealthiest men and husband of the former Kazakh president’s daughter Flinder Data’s registered agent is Olga Aristova who served in the same role for several companies linked to Kulibaev Aristova was preceded in her role at Flinder by a Kazakh named Assylbek Karibaev who worked for a subsidiary of KazMunayGas who also headed the country’s sovereign-wealth fund and controls the country’s largest bank by assets A London law firm that has represented Kulibaev for many years did not respond to e-mails seeking comment E-mails sent to the charitable foundations that Dinara Kulibaeva heads in Switzerland and Kazakhstan also went unanswered Much of the paper trail regarding the Spanish property’s ownership stems from court battles over environmental permits A local environmental group called SOS Lloret tried to block the expansion of the buildings on the property in the early 2010s saying the property was located in a sensitive The Catalonian regional legislature also joined the fray passing an ultimately unsuccessful measure to halt the expansion the property’s owners sought to block access to a section of public road that ran close to the estate but environmental groups won a series of rulings in local courts the region’s highest court dismissed an appeal by Flinder while the fight over the road played out in courts the property’s owners aggressively tried to block people from walking on the road erecting menacing signs and loudspeakers that blared warnings They told RFE/RL that some of the loudspeakers also broadcast sounds of gunfire -- an apparent attempt to frighten locals the Chateau de Bellerive was for many years owned by Sadruddin Aga Khan the former UN diplomat and jet-setting global celebrity known for his philanthropic work the lakeside property was purchased by Dinara Kulibaeva the daughter of former Kazakh President Nursultan Nazarbaev,for 62 million Swiss francs ($63.8 million) Kulibaeva expanded her lakeside holdings in January 2020 when she purchased an adjoining tract of land totalling about 1.5 hectares for 44 million Swiss francs ($49.3 million) which includes a smaller house -- a historical building reportedly once owned by a 19th-century French military commander -- was acquired from an extended member of the Sadruddin family The Swiss magazine Bilan last year ranked Kulibaeva as Switzerland’s 59th wealthiest person the Hotel Corso is owned by a Czech-registered company called Kalma II whose daughter is married to the son of Timur and Dinara Kulibaev the company Kalma II is headquartered at the same address as the hotel The company’s stated activities include “hospitality activities residential and nonresidential premises and cosmetic services.” Katranova is a general director of a company called Vostochnoye Rudoupravlenie the largest producer and supplier of specialized minerals used by several oil- and gas-producing companies in Kazakhstan and the former Soviet Union She has held positions in several other major companies in Kazakhstan which is a subsidiary of the state-owned railroad Kazakhstan Temir Zholy The hotel appeared to not be open when visited by RFE/RL reporters in September Waiters working in cafes and restaurants nearby said the hotel had not been operational in recent memory E-mails sent by RFE/RL to three Kazakh companies on whose boards Katranova sits No one answered the main office phone at Hotel Corso on two separate days The hotel was acquired by a Czech-registered company owned by Boranbaev in April 2000 four months after the purchase of Villa Ahlan has reregistered several times since its founding in 1999 Initially described as “rental of flats and nonresidential premises without providing other than basic services associated with the lease of flats and nonresidential premises,” the company’s declared activities were changed in 2014 to “operation of nongovernmental medical facilities in the scope of physiatry and balneology” -- the medical study of therapeutic baths The company also added as its declared activities “washing and personal goods.” Another listed executive with the company is Zelina Katranova whose daughter is married to another of Nazarbaev grandsons Czech corporate records show Mingon-II is linked to several other non-Czech companies including KazMunayGas-Service and Razvedka Dobycha KazMunayGas both of which are subsidiaries of Kazakh state-owned oil and gas giant KazMunayGas is a shareholder and former top executive in KazMunayGas the building known as Myslivna used to be a popular cafe known as the Jagerhaus according to historical postcards from the time employees of the Czech Interior Ministry came to vacation and take medicinal baths The entire property was sold by the Interior Ministry in 2017 to a company registered in the Czech Republic located in the municipality of Karlovy Vary The property was initially listed for auction at 41.4 million Czech crowns ($1.8 million) but ended up being sold below the advertised price in November 2016 holds executive positions in several Czech-registered companies that belong to Boranbaev who is related to Nazarbaev by marriage: his daughter married Nazarbaev’s grandson was equally owned by two Dutch-registered firms whose parent companies link directly back to Timur Kulibaev ADNTS Holdings’ only owner is ADNTS Investments registered in Singapore as a private company The director of this company is a Singaporean man who is also listed as a secretary in Steppe Capital a Singaporean company whose only shareholder is Kulibaev linked to the Spanish hillside estate that has been identified as belonging to Kulibaev Dostyk Holdings’ only shareholder is Steppe Unity Cooperatief which is also registered in Amsterdam and is a subsidiary of Kulibaev’s Steppe Capital Dostyk Holdings exited its ownership of Margotrade in November Margotrade’s new 50 percent owner is a Kazakh company which was incorporated in October and is owned by two Kulibaev companies when RFE/RL reporters visited the Karlovy Vary property with peeling paint and overgrown shrubbery Though a car was parked next to the property’s outbuilding no one answered when RFE/RL reporters tried to enter the grounds ringing a gate bell and calling out to see if anyone was present The London law firm that has represented Kulibaev for many years RFE/RL also left a voice mail with Kulibaev’s lawyer at the same firm Located in one of the most expensive districts on Geneva’s outskirts the lakeshore property drew the attention of Swiss authorities when Kulibaeva sought to purchase it Swiss regulations restrict some investments by foreigners; a local magistrate ultimately approved the purchase in 2009 According to a 2013 investigation by Swiss public broadcaster RTS, Kulibaeva had to seek permission from the Swiss government to acquire the property because its area exceeded the ceiling of 3,000 square meters set for citizens of non-European countries The magistrate who allowed the purchase to go forward cited likely visits by her husband "The frequent stays of her husband...as well as those of her father which published an excerpt of the decision "The importance of the receptions that Madame Kulibayeva would have to organize as well as the special security measures that would be required as a result also justify the acquisition of a building characterized by the size of its surface.” In a 2016 interview with a Swiss business magazine who previously had lived in eastern Switzerland near the lakeside town of Lugano which Forbes magazine at the time estimated at $2.4 billion This is neither a goal nor a source of pride,” Kulibaeva said Boranbaev is the father of a Kazakh woman who was the wife of former Kazakh President Nursultan Nazarbaev’s grandson The property is located within Wentworth Estate a 700-hectare location southwest of London that was once part of a grand country estate in the family of the royal duke of Wellington The estate itself is a collection of gentle hills and leafy roads that is now best known as home to the Wentworth Club U.K. property records show Boranbaev bought his property there in November 2014 through a New Zealand-incorporated company he controlled the location has gained notoriety for the luxuriously priced homes but also for the British and foreign notables who have lived there at one time or another The list includes former Chilean dictator Augusto Pinochet the late Russian oligarch and Kremlin confidant Boris Berezovsky The husband of Boranbaev’s daughter, Alima, was Aisultan Nazarbaev, one of Nazarbaev’s grandsons and the son of Darigha Nazarbaeva. He was found dead in London in August 2020. According to preliminary conclusions by British authorities, the cause of death was cardiac arrest. The Financial Times reported earlier this month that an autopsy listed the cause as toxicity from cocaine Aisultan had said publicly that he battled drug addiction When Boranbaev bought the property in 2014 The owner of an interior-design studio listed on the property’s planning records gave an interview in 2016 discussing her firm’s work on what she called the “Pinehurst Project.” But she did not reveal the identity or nationality of the client “On a project like this, the sky is the limit, and what I like about our clients is that they are incredibly mature about what they want,” the designer, Charu Gandhi, was quoted as saying “These are not people who stumbled into having this lifestyle Gandhi’s studio did not respond to an e-mail seeking comment on its work for Boranbaev E-mails sent by RFE/RL to the Almaty soccer club that Boranbaev owns An e-mail sent to a Gmail account that Boranbaev is known to use also went unanswered Bolat Nazarbaev — the younger brother of former Kazakh President Nursultan Nazarbaev — and his then-wife Maira Kurmangalieva purchased the unit in a building overlooking Manhattan’s famed Central Park The couple divorced three years later and the apartment became central to a bitter and public legal fight that played out in New York courts and the city’s tabloids as Bolat accused Kurmangalieva and his stepson (her son) of fraudulently taking ownership of the unit Bolat is listed as a shareholder or head of numerous Kazakh companies operating in a range of sectors The couple ultimately settled their lawsuit and Bolat regained sole ownership of the unit in 2014 He sold it two years later for a reported $17.9 million The sports center near Karlovy Vary sits on various plots of land that were bought from various owners between 2010 and 2012 The entire property is owned by a company whose only shareholder is Boranbaev Boranbaev also owns several sport and fitness centers The mansion at Sunninghill Park was long known as the family home for Prince Andrew who was given the property in 1986 as a wedding gift by his mother The royal couple divorced in 1996 and the house was sold in 2007 for 3 million pounds above the asking price to a company in Luxembourg called Unity Assets Corporation The property ended up sitting unoccupied for several years much to the consternation of neighbors and historic preservationists In 2016, Kulibaev tore down the property and moved forward with plans for a newer residence RFE/RL also left a voice mail with Kulibaev’s lawyer that went unanswered as of publication Two of the three properties -- on Denewood Road and Bishops Avenue respectively -- were purchased by shell companies in 2008; the third Britain’s National Crime Agency (NCA) argued in court filings that “the properties were acquired as a means of laundering the proceeds of unlawful conduct by Mr Aliev was a prominent and powerful Kazakh who built a fortune in banking, oil, media, and other industries, and held several prominent government positions, including deputy chairman of the state security service known as the KNB former Kazakh President Nursultan Nazarbaev’s elder daughter Five months after his death, in a report about Kazakh investments in British real estate, the London corruption watchdog Global Witness described Aliev as allegedly having “used his position as the former deputy head of the country’s secret police to amass a vast business empire.” A British judge overturned all three orders in April 2020 ruling that the agency\'s “assumption” that the money to buy the three properties came from Rakhat Aliev “as a means of laundering his money” was unreliable "It is frustrating and disappointing that she has had to take this action to fight these draconian proceedings and clear her name,” a spokesman for Nazarbaeva said in a statement in April after the court issued its ruling Representatives for Nazarbaeva and Nurali Aliev told the U.K court that the funding for two of the homes was linked to Nurbank one of Kazakhstan’s largest private lenders Nurali Aliev bought the Hampstead Mansion on London’s “billionaire’s row” with money that came “principally” from a $65 million loan from Nurbank while Nazarbaeva bought the Manresa Road property using proceeds from the sale of her shares in the Kazakh lender An e-mail seeking comment from a public relations agency that Nazarbaeva and Aliev have used in the past also went unanswered as of publication Rakhat exited the bank’s ownership in 2007 after which both Nurali Aliev and Nazarbaeva became Nurbank shareholders At the time of Nurali’s purchase of the Hampstead Mansion Nurbank was “ultimately controlled” by the mother-and-son duo Nurali was elected chairman of the Nurbank board in October 2007 Nazarbaeva was elected to the board at the same time court that she bought the Denewood Road property located in a leafy suburb of northern London using the proceeds of shares in the Kazakh sugar producer Kant that she sold They said that Rakhat Aliev had transferred these shares to her in connection with their divorce in 2007 and that “unlike other assets then held by [Aliev] in Kazakhstan,” Kazakh authorities did not identify them as “being any part of his suspected proceeds of crime.” Her representatives told the court that she was an independently successful businesswoman and “one of many entrepreneurial individuals who capitalized on the economic reforms in Kazakhstan at this time,” including in the sugar industry They said that records related to her business trading “sugar and cigarettes” in the years following the Soviet collapse could not be found despite “significant efforts” to do so But Nazarbaeva estimates that this business potentially brought her as much as $45 million between 1992 and 1995 The Czech-registered company Mignon-II purchased the Villa Ahlan hotel in December 1999 -- the first of two hotel purchases by the company Czech media reported that the hotel belonged to Boranbaev and noted that then-Kazakh President Nursultan Nazarbaev was a regular visitor to Karlovy Vary even speculating that Nazarbaev was a part owner of the hotel Records do not indicate any ownership role for Nazarbaev Nazarbaev stayed at Villa Ahlan during a 2002 visit to Karlovy Vary, Russia’s state-run news agency RIA Novosti cited the municipality’s press service as saying at the time. The report noted that the hotel’s owners were “citizens of Kazakhstan,” but did not identify them Former Ukrainian President Leonid Kuchma, who was known as a friend of Nazarbaev, stayed at the Villa Ahlan in 2005 the property on Lake Lugano housed a famed 19th-century building known as Villa Galli popular among generations of Lugano locals for a luxury restaurant Pacolli’s construction company, Mabatex In 2008, Pacolli publicly revealed the ownership of the property where La Romantica was housed, saying that he owned three neighboring buildings for whom he said he was the official representative Pacolli denied that he had purchased La Romantica “on behalf of third parties” and threatened legal action against those who suggested this was the case “no member of the family of President Nazarbaev is or ever has been the owner” of La Romantica or Stott Limited Despite public outcry from historic preservationists Pacolli demolished the aging La Romantica in 2013 the developer has been fighting with local authorities over zoning permits The land is now home to a tennis club and three nondescript office buildings An investigation by Swiss journalists published in 2010, meanwhile, found that Stott Limited was 50 percent owned by another company, Transasian Oil, headed by an Indian businessman and partner of Timur Kulibaev whose name appears on several Kulibaev-owned companies Transasian Oil loaned Stott more than 10 million Swiss francs ($12.4 million) according to the investigation by Swiss public broadcaster RTS and received the Villa Galli property as collateral The debt pledge on the property totaled 8.5 million Swiss francs ($10.5 million) making Transasian Oil the ultimate owner of Villa Galli In a 2015 report on the threat facing Switzerland from money laundering and terrorism Swiss Federal Police detailed an example of a scheme in which an unnamed Swiss property is purchased under circumstances that raise suspicions While the scheme does not name the people or companies involved it closely mirrors details in the RTS investigation and publicly known information about the Villa Galli property and the individuals it has been linked to the person identified as “Suspect A” in the Swiss Federal Police scheme is described as someone “accused of having benefited from his position as a manager in the national oil company of an oil-producing country to enrich himself illegally.” This person’s money “would have passed through different companies to finally be used by a front man to acquire property in Switzerland,” the document states the company resembling Stott gains ownership of the property using a loan of 8.55 million Swiss francs from a company resembling Transasian Oil that is ultimately controlled by someone who has been “a confidant and front man” of “Suspect A” for “many years.” The mortgage note for the historic building is then held by the company resembling Transasian Oil as collateral for the loan that the firm resembling Stott uses to buy the property Asked whether the property cited in the scheme in the 2015 report was the La Romantica building Swiss Federal Police spokeswoman Katrin Schmitter said: “We are subject to official secrecy and cannot comment on specific cases.” that the examples “described in our reports are generally based on real-life cases.” The federal police report also echoes the real-life case of Kulibaev who was investigated by the Swiss Attorney-General’s Office for possible money laundering The probe was dropped in 2013 after authorities said they found no evidence of wrongdoing The report states that the allegations against “Suspect A” are determined to be “unfounded” and the proceedings dropped due to “lack of evidence as to the criminal origin of the assets.” the property cited in the scheme is “demolished” amid media reports that “Suspect A” and “an acquaintance and presumed accomplice” intend “to replace it with a luxury hotel.” RFE/RL also left a voice mail with Kulibaev’s lawyer Pacolli’s longtime representative in Lugano said Stott Ltd Behget Pacolli” and “Stott is the 100 percent owner” of the La Romantica property The representative said the purchase of properties more than a decade ago and the construction of a luxury hotel now planned for the former location of La Romantica “There [was] no working relationship with Mr.Kulibaev at all!” she said in her e-mail She did not respond to a follow-up e-mail seeking further details of when Pacolli gained control of Stott and the discrepancy with Pacolli’s earlier public statements about the ownership of the Villa Galli properties Swiss journalists also reported that Dinara Kulibaeva lived in a nearby villa between January 2007 and December 2009 which they said she rented from Pacolli for a reported 50,000 Swiss francs ($57,000) annually Pacolli’s representative confirmed that his villa in Lugano was rented at one point for an unspecified 12-month period to the Kulibaev family “while their son and nephew were visiting the American school in Lugano and for that period of time the two students were living in the villa.” the tenancy has been terminated,” she told RFE/RL The Nazarbaev Family’s Opulent Offshore Real Estate Empire GENEVA – In the gentle dawn of Switzerland’s late summer Lake Geneva’s ripples lap against the properties on the eastern shore in the suburb of Anières Some of the buildings are understated in their wealth with slate shingles or mansard roofs or Corinthian columns Some have gazebos on manicured lawns looking west to the Jura Mountains or docks where motorboats and kayaks are parked Many have gates and surveillance cameras to protect from curious passersby 399 Route D’Hermance: a 3,200-square-meter three-level villa with a butterfly staircase In an area known for having some of the most expensive housing in the region the daughter of Kazakhstan’s longtime ruler who are among Kazakhstan’s wealthiest people purchased the villa in 2009 for a reported $75 million And they are among several immediate and extended relatives of Nazarbaev who own lavish real estate in the West relatives of Nazarbaev have purchased hundreds of millions of dollars in posh real estate in Europe and the United States a string of high-end properties on luxurious lakesides and overlooking the azure waters of Spain’s Costa Brava A new RFE/RL investigation provides the most comprehensive overview to date of the properties in this sprawling real estate network linked to Nazarbaev’s relatives The findings are not an exhaustive record of every foreign property owned by a relative of the former Kazakh president who was officially granted the title “Leader of the Nation” in 2010 and currently serves as chairman of the country’s powerful Security Council and heads its ruling political party But they offer an unprecedented window into the scale of the real estate investments by Nazarbaev’s relatives and how many in close proximity to Kazakhstan’s ruling family ended up with luxury assets in exclusive locations RFE/RL identified at least $785 million in European and U.S real estate purchases made by Nazarbaev’s family members and their in-laws in six countries over a 20-year span This figure includes a handful of properties that have since been sold including multimillion-dollar apartments in the United States bought by Nazarbaev’s brother It does not include a sprawling Spanish estate owned by Kulibaev for which a purchase price could not be found These acquisitions have been funded by the vast fortunes Nazarbaev’s relatives have amassed in the oil-rich nation’s energy while at various times also serving in official government posts Nazarbaev’s patronage is widely seen as crucial to the wealth built by his relatives who have repeatedly and vehemently insisted they are successful businesspeople independent of their family and political connections who has been dogged for years by accusations that his wealth mainly from his work in the oil-and-gas industry The Financial Times on December 2 said it had uncovered a secret scheme that allegedly channeled tens of millions of dollars from contracts related to a massive gas pipeline to China to Kulibaev His lawyers denied specifics of the report to the Financial Times and did not respond to queries from RFE/RL Several of these properties documented by RFE/RL have been the subject of legal challenges and British freezing orders on three London residences that were later overturned by a court The investments in pricey foreign properties also come against the backdrop of the country’s overall increase in national wealth since the Soviet collapse This increased prosperity has lifted livelihoods for many average Kazakhs -- but it has also helped the politically connected elite transform into jet-setting tycoons and fodder for newspaper gossip pages And with 80-year-old Nazarbaev in his twilight will succeed him when he fully departs from Kazakh politics -- and what might happen to the fortunes of those closest to him The political economy that Nazarbaev has built it’s built on one man,” said Kate Mallinson a London-based consultant and researcher of Central Asian politics His relatives and closest allies have “hedged the bets on the future not knowing what will happen -- and so they’ve had to put assets outside the country,” Mallinson told RFE/RL the head of Kazakhstan’s oldest and largest human-rights organization said “it is hard to separate the government from the [Nazarbaev] family” and “hard to say how it will be in Kazakhstan” after Nazarbaev dies “You cannot rely on protection from the rule of law when you live in such political systems,” Zhovtis said 41-42 Upper Grosvenor Street; 41-42 Reeves Mews RFE/RL journalists report the news in 23 countries where a free press is banned by the government or not fully established We provide what many people cannot get locally: uncensored news RFE/RL is registered with the IRS as a private Congress through the United States Agency for Global Media (USAGM) as a private grantee RFE/RL's editorial independence is protected by U.S Independent journalism at the University of Twente The Institute of Electrical and Electronics Engineers (IEEE) has featured Pep Canyelles Pericas as their Engineer of the Week especially because I’m still relatively junior in my career,’ says the University of Twente scientist Canyelles Pericas: ‘It brings a lot of visibility and recognition for my work but it helps if people know what I’m up to It’s nice to be acknowledged for my research and it has helped me to reconnect with a lot of people from my network We have to wait and see how much it will bring in the long run but I think it’s important to engage with the general public and explain what you do in language that everyone understands As scientists we are often paid from public funds and it’s important to show what we do with the funding.’ ‘An engineer of the week should be an IEEE member with a variety of backgrounds and expertise I focus a lot on tech transfer in between academia and industry The Institute of Electrical and Electronics Engineers (IEEE) is the world's largest association of technical professionals with more than more than 396,000 members in over 160 countries around the world Its objectives are the educational and technical advancement of electrical and electronic engineering computer engineering and similar disciplines ‘To align the space between industry and academia. I enjoy working at the university and I’m thankful to MESA+ for their support in exploring my potential. I want to bridge the gap no matter on which side I end up. Ultimately, I want to work on technologies that can be applied fast and be of use to people.’ David Fernandez Rivas heeft woensdagavond een prijs in de wacht gesleept. Zowel de vakjury als het publiek viel voor de bezieling van de universitair docent van de UT en bekroonden hem met de Prins Friso Ingenieursprijs 2021. David Fernandez Rivas won a prize on Wednesday night. Both the professional jury and the public fell for the inspiration of the UT associate professor and awarded him with the Prins Friso Ingenieursprijs 2021 (Prince Friso Engineering Prize). UT-atletiekvereniging Kronos loopt als titelverdediger van het algemeen klassement warm voor de alternatieve Batavierenrace. De ambities zijn wat minder hooggespannen dan de vorige jaren, maar de hoop is er op een klassieke Bata-atmosfeer. Ondanks de kritiek van universiteiten zet de Europese Commissie het plan door: Horizon Europe moet ook ingezet kunnen worden voor militaire toepassingen (dual use). Vooral bedrijven moeten daarvan profiteren. Vanaf september 2026 gaan studenten in het hoger onderwijs 2.694 euro collegegeld per jaar betalen. Dat is een stijging van bijna honderd euro. Reden daarvoor is de relatief hoge inflatie van afgelopen jaar. With the magazine ROOTS we want to connect students and companies. We do this by bringing stories of starters on the labor market. They talk about living and working in the region. We also publish advertorials. In this way, companies come into the spotlight of students and students get an idea of the life that awaits them and what opportunities there are in the region. LEA BELIAEVA BANDER | Barcelona First published: November 27, 2023 05:10 PM Christmas has descended upon Catalonia, a perfect time to learn about Catalan holiday traditions such as eating turrons (nougats), placing the caganer (pooping figurine) in nativity scenes, or feeding the Tió de Nadal (Christmas log). And all of these things can be found in Christmas markets all over Catalonia.  This is the oldest Christmas market in Catalonia, open every Christmas since 1786. This year it will have 200 stalls dedicated to decorations, ornaments, nativity scenes, Christmas trees and more, making it the largest of its kind in the world, according to organizers.  Nadal al Port, Port Vell Christmas Market  Nadal al Port, located in the harbor area of Port Vell, is one of the newest Christmas markets in Barcelona, having only been inaugurated in 2018. Located right by the water on the Moll de la Fusta, visitors can enjoy a local gastronomy market, take a ride on the Ferris Wheel, see Christmas light shows and installations, or even try the 400m2 ice rink.       This market is another traditional Christmas Market in Barcelona, dating back to 1877 when street vendors would set up stalls to sell their goods. Today visitors can buy Christmas presents, decorations and food in over 100 stalls.   For Art Nouveau fans, there are two events that cannot be missed this year.   The first is the Sagrada Familia Christmas Market, located by the Nativity Facade of the famous Gaudí cathedral. Inaugurated in 1962, it has 150 stalls, that, according to the organizers, have "everything you need to celebrate Christmas at home.".   A short walk from that Christmas Market, there’s the Christmas Garden at the Sant Pau Art Nouveau Site (Recinte Modernista de Sant Pau). For the third year in a row, the old hospital is bathed in Christmas lights and other audiovisual installations. The Sant Pau Site also includes an ice rink.  For residents and visitors who are interested in alternative Christmas markets in Barcelona, there are various great options:   For the past 15 years, an old closed-down German toy factory, Antiga Fàbrica Lehmann, located in L'Esquerra d'Eixample, has been a creative hub for local designers and artists, and every year the cobblestone-clad patio of the factory is transformed into a Christmas Market, where visitors can buy handcrafted goods like jewellery, ceramics, clothing, artwork, as well as books and food.  Another alternative Christmas market is the Market for Sustainable Consumption and Social and Solidary Economy, held in the center of the city, ion Pl. Catalunya.  A total of fifty small businesses and organizations will sell craft products, clothing, books, food and other small gift items all produced with sustainability and solidarity in mind.  The new edition of the Christmas Market of Caldes de Montbui will be held from December 5th to 10th, with more stalls and family activities in the historic center of the town. The highlight of the event a thermal soup cooked in the biggest pot in all of Catalonia, which can hold 1,600 liters of soup. There will also be dozens of stalls selling food, Christmas products and antiques.  Not strictly Christmas themed, the market sets out to recreate medival life through workshops, shows, theatre and music for visitors of all ages. The fair will also include stalls with locally produced products such as food, jewelry, herbs and decorations.   This is one of the most popular events for children. Mura is located in the Bages region and, during the weeks before Christmas up until after the New Year, the Tió de Nadal logs invade the streets of the town. Christmas and Torró Fair in Cardedeu  The fair dates back to 1272, according to organizers in the town located in northern Catalonia. The centerpiece of the fair is the torró, a traditional Christmas sweet, which will be sold in most of the stalls. Other items include gifts, handcrafted goods, nativity scenes and Christmas decorations.   The Fair of Santa Llúcia de Canyelles is held on December 2nd and 3rd. There are more than 350 stalls, exhibitions, children's programs and other activites between 9 am and 9 pm.  The characteristic wooden stalls of the Girona Christmas Market have once again filled the Independence Square in the heart of the city. In most of the stalls, visitors can buy handcrafted goods such as Christmas decorations, ceramics and other gifts, as well as a huge selection of locally produced foods.   The tiny town of Espinelves, located in north-central Catalonia just outside Vic, holds an annual Christmas tree market, the Fira d'Alvet. Vendors sell locally grown trees and Christmas decorations. Aditionally, the fair features around a hundred stalls selling hand-made crafts and food.  From December 8 to 10, the Olot Nativity Scene Fair will take place in the Esteve Ferrer square, with dozens of wooden stalls where artisans will exhibit and sell figurines and sculptures. The Plaça Major will host the Christmas Market Km. 0, where you will find gift products made by local producers.  The city of Lleida doesn't just have one, but two Christmas markets.  Located in the center of the commercial hub of the city, the Santa Llúcia Market, offers a variety of Christmas-related goods such as decorations, nativity scenes and trees.  The other market, the Lleida Christmas Market, is located next to the main Cathedral. Here, visitors can buy handcrafted products and foods from 25 different stalls.  Tarragona’s Rambla Nova will be packed with traditional wooden house stalls this season, selling Christmas decorations, trees, small presents, and typical Christmas sweets such as xurros, waffles and chocolate.    Get the day's biggest stories right to your phone Metrics details A Publisher Correction to this article was published on 25 April 2018 This article has been updated β-cell proliferation is a rare event in adult pancreatic islets To study the replication-related β-cell biology we designed a replicating β-cells sorting system for gene expression experiments Replicating β-cells were identified by EdU incorporation and purified by flow cytometry For β-cell separation islet cells were sorted by size granularity and Newport Green fluorescence emission that was combined with emitted fluorescence for EdU-labelled replicating cells sorting The purity of the resulting sorted populations was evaluated by insulin staining and EdU for β-cell identification and for replicating cells Total RNA was isolated from purified cell-sorted populations for gene expression analysis Cell sorting of dispersed islet cells resulted in 96.2% purity for insulin positivity in the collected β-cell fraction and 100% efficiency of the EdU-based cell separation RNA integrity was similar between FACS-sorted replicating and quiescent β-cells Global transcriptome analysis of replicating vs quiescent β-cells showed the expected enrichment of categories related to cell division and DNA replication key genes in the spindle check-point were the most upregulated genes in replicating β-cells This work provides a method that allows for the isolation of replicating β-cells a very scarce population in adult pancreatic islets Pancreatic β-cells are the unique cell type in the body that produces and secretes insulin in response to small variations in blood glucose levels to tightly control systemic glucose homeostasis Β-cell mass reduction is a central event in the development of type 1 and type 2 diabetes and β-cell regeneration is a potential curative treatment of the disease Despite the advantages provided by this system its use is restricted to the study of β-cell replication in mouse islets we sought to develop a method for replicating β-cells sorting based on EdU incorporation suitable for global gene expression analysis and applicable to most of experimental designs and animal species FELASA guidelines and recommendations for the use of laboratory animals were followed (European and local government guidelines) and animal procedures were reviewed and approved by the Animal Research Committee of the University of Barcelona (identification number: DAAM 7082) Isolated islets were hand-picked under a stereomicroscope two or three times until a population of pure islets was obtained Islets were cultured in RPMI 1640 (Sigma Immunochemicals USA) supplemented with 100 U/ml penicillin and 100 mg/ml streptomycin containing 10% heat-inactivated foetal bovine serum (FBS) at 37 °C in a humidified atmosphere with 5% CO2 USA) were added into the culture medium at final concentration of 10 µM For the analysis of continuous labelling with EdU islets were cultured in 5.5 mM or 22.2 mM glucose with or without EdU for 7 and 14 days Culture medium was replaced on a daily basis and BrdU was added to the islets for the last 24 h of culture islets were cultured in 5.5 mM glucose with EdU overnight starting on the day of isolation Dispersed islet cells were washed once with PBS and incubated with 25 µM NG at 37 °C for 30 min EdU labelling was performed by means of the Click-iT® EdU Alexa Fluor®647 Flow cytometry Assay Kit (Invitrogen cells were fixed in 2% paraformaldehyde–PBS at room temperature (RT) for 15 min. and washed once with 1% BSA-PBS before mild permeabilization with a saponin-based reagent for additional 15 min The click reaction buffer was prepared following the manufacturer’s instructions and added to the washed cells for 30 min labelled cells were washed twice with FACS buffer (PBS 0.5%BSA) and transferred into 35 µm nylon mesh cell strainer caped-tubes (BD biosciences 400 units of RNasin plus RNase inhibitor (Promega) were added to the buffer or solution used in each step from the cell fixation with PFA until cell sorting Unstained cells and FMO (fluorescence minus one) were used as negative control in each experiment and served as autofluorescence control Sorting was done using a Beckman-Coulter MoFlo Astrios cell sorter equipped with a 100-μm flow tip and operated at a sheath pressure of 25 psi The laser illumination power was set to 150 mW for NG excitation at 488 nm and to 100 mW for Alexa 647 excitation at 640 nm and 671/30 nm for EdU Alexa 647 fluorescence cells were filtered through a 35 μm strainer to eliminate all remaining cell clumps doublets are excluded by using pulse processing (FSC-H vs FSC-A) followed by the exclusion of debris gating on a two physical parameter dot plot (FSC/SSC) Mitotic and post-mitotic cell subpopulations were selected as EdU+ or EdU- respectively An average sorting rate of 200 events per second was maintained Sorted cells were collected in 150 μl of PKD buffer (Qiagen) Cultured islets were fixed overnight in 4% paraformaldehyde-PBS at 4 °C sectioned and immunostained after deparaffinization and rehydration For EdU detection in cultured islets the click chemistry-based Click-iT EdU assay (Click-iT® EdU Alexa Fluor® 594 Imaging Kit; Molecular Probes Life Technologies) was used according to the manufacturer’s instructions sections were permeabilized with saponin and incubated with the Click-iT reaction cocktail for 1 h at room temperature This labelling method was combined with insulin immunofluorescence Β-cell purity in sorted populations was determined by insulin and c-peptide immunofluorescence as follows Sorted populations were directly collected in 1% BSA-PBS washed twice with PBS and incubated overnight with the rabbit anti-insulin antibody (1/100) or mouse-anti c-peptide antibody (1/50 Abcam) diluted in 1% BSA-PBS + 0.3% triton Donkey anti-rabbit Alexafluor-488 labelled antibody (1/400) was used for β-cell visualization Cells were loaded into the haemocytometer for counting At least 200 cells were counted for each sorted population The experiment was replicated 8 times with islets isolated from 8 different rats Total RNA was extracted with RNeasy FFPE kit (Qiagen UK) according to manufacturer’s instructions with the following variation Sorted cells were directly collected in PKD buffer immediately treated with 200 μg/ml proteinase K (Qiagen) at 56 °C for 3 h with continuous shaking This modification significantly increased the RNA extraction yield mRNA was linearly amplified with the Arcturus® RiboAmp® HS PLUS RNA Amplification Kit (Arcturus USA) or Complete Whole Transcriptome Amplification Kit (Sigma WTA2) following the manufacturer’s protocol RNA quality was assessed by using the Agilent RNA Nano kit in the Bioanalyzer 2100 (Agilent Technologies Results are expressed as means ± SEM for 4–8 independent experiments. Statistical analysis were performed using GraphPad Prism 6 software, and differences among means were evaluated using the Student’s paired t test with p < 0.05 considered significant. The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request. Continuous labelling of islets with EdU ex vivo Rat pancreatic islets were cultured at 5.5 or 22.2 mM glucose in the presence or absence of 10 µM EdU 10 µM BrdU was added into the culture medium for the last 24 h (A,B) β-cell replication (BrdU incorporation) and (C,D) β-cell apoptosis (TUNEL) of islets exposed to EdU for 7 days (A,C) or 14 days (B,D) (E) Representative image of EdU and insulin staining on islets cultured for 7 (top) or 14 days (bottom) at 22.2 mM glucose with continuous EdU labelling (F) Quantification of β-cells positive for EdU Efficiency of replicating and quiescent β-cell sorting (A) Replicating and quiescent β-cells were sorted after gating on SSC-Ahi/FSC-Ahi (R2) and FSC-Ahi/NG-Ahi (R9) for β-cell population and EdU647+ (R5) and EdU647− (R4) for replicating and quiescent cells (B) To assess the purity of each cell population Mitotic β-cell population is illustrated as a composite of pictures from 4 different fields to show a representative number of cells Insets framed in red show replicating (top) and quiescent (bottom) β-cells at higher magnification The number of cells collected per rat pancreas ranged from 760 to 1200 cells in the proliferative β-cell fraction and from 4 × 104 to 6 × 104 cells in the quiescent β-cell fraction RNA was isolated from replicating and quiescent β-cell fractions RNA extraction from the quiescent β-cell fraction that consisted of approximately 2 × 104 cells whereas for the replicating fraction with ≈1000 cells the collected RNA yielded ~5 ng of RNA (~5 pg of RNA/cell) Similar results were obtained in the RNA extraction from 1000 quiescent β-cells excluding the possibility that replicating β-cells had lower content of RNAs the efficiency of RNA extraction correlated with the number of cells in the fraction Gene expression of replicating β-cells (A) Ct values of housekeeping genes used as endogenous controls amplified in replicating (empty) and quiescent β-cells (hashed) Values are represented as median [IQR] of n = 6 (B) Differential expression of cell-cycle related genes and insulin in replicating over quiescent β-cells In order to confirm the purity of the collected fractions a panel of pancreatic cell types and proliferation markers were analysed in both fractions keratin 20 (krt20) and pecam1 were undetectable in our samples indicating the absence of contaminating acinar duct or endothelial cells (data not shown) mRNAs encoding for glucagon (gcn) and somatostatin (sst) were detected in 2 out of 11 samples from both fractions and pancreatic polypeptide (ppy) in 6 out of 11 vimentin the major cytoskeletal component of mesenchymal cells was detectable in both β-cell fractions and levels of expression in the replicating β-cell fraction were doubled compared to the quiescent β-cell fraction a marker for the epithelial to mesenchymal transition (EMT) was undetectable Genetic programme of replicating β-cells Selection according to p-value < 0.001 and absolute linear fold change > 2 Q: quiescent β-cells; R: replicating β-cells (B) EnrichR analysis of most changing genes Relevant and significantly enriched gene sets from Biocarta KEGG and Reactome data bases are represented in the bar-plot (C) Gene Set Enrichment Analysis showing selected Rat Gene Ontology data sets enriched in the replicating β-cells compared to the quiescent β-cells (D) Quantitative RT-PCR determination of mRNA levels of selected genes from the top regulated transcripts unveiled in the gene array The genes most significantly upregulated in replicating β-cells are mainly involved in the control of G2-M phases of the cell-cycle (Table 2 and Fig. 4D) the Slc16a1 gene that encodes for the Monocarboxilate transporter 1 which conveys pyruvate and lactate through the plasma membrane and its expression is negligible in mature β-cells was significantly upregulated in replicating β-cells This study reports a method for the purification of replicating and quiescent pancreatic β-cells for downstream gene expression analysis This technique is based on the incorporation of EdU to the replicating DNA strands during the S phase of the cell cycle and makes it compatible with diverse experimental designs and animal species In the present study we have determined the effects of long-term EdU exposure on β-cell replication and survival We show that β-cell replication and viability are unaffected in cultured islets exposed to 10 μM of EdU for 7 days; whereas longer exposure has a negative impact on β-cell survival which compromises RNA isolation from fixed cells the inclusion of a protein digestion step in the RNA extraction protocol with the addition of Proteinase K in the cell lysis buffer significantly improved the quality and yield of the RNA granularity and NG labelling resulted in pure β-cell preparations amylase and keratin 20 RNAs were undetectable in β-cell preparations non β-cell pancreatic islet hormones (glucagon somatostatin and pancreatic polypeptide) RNAs were detectable in some samples indicating that contamination with endocrine non β-cells was not completely avoided replicating β-cells could incur in inappropriate insulin release in response to glucose levels Further work will reveal whether the genetic program of cycling β-cells is completely restored in daughter cells after mitosis we present a method that allows for the isolation of replicating β-cells even in situations where they are very scarce We anticipate that it will be particularly useful for the study of β-cell replication of human islets in which replicating β-cells are infrequent we expect this method to have a broad applicability in the study of β-cell proliferation in the context of diabetes and β-cell regeneration A correction to this article has been published and is linked from the HTML and PDF versions of this paper Beta-cell replication is the primary mechanism subserving the postnatal expansion of beta-cell mass in humans Significant human beta-cell turnover is limited to the first three decades of life as determined by in vivo thymidine analog incorporation and radiocarbon dating Dynamics of beta-cell mass in the growing rat pancreas Estimation with a simple mathematical model Linear correlation between beta-cell mass and body weight throughout the lifespan in Lewis rats: role of beta-cell hyperplasia and hypertrophy reduced duct cell plasticity and impaired β-cell mass regeneration in middle-aged rats A transgenic mouse marking live replicating cells reveals in vivo transcriptional program of proliferation A chemical method for fast and sensitive detection of DNA synthesis in vivo Cell type specific applicability of 5-ethynyl-2′-deoxyuridine (EdU) for dynamic proliferation assessment in flow cytometry Adenoviral overproduction of interleukin-1 receptor antagonist increases beta cell replication and mass in syngeneically transplanted islets Identification and purification of functional human beta-cells by a new specific zinc-fluorescent probe Adenoviral overexpression of interleukin-1 receptor antagonist protein increases beta-cell replication in rat pancreatic islets Gastrin induces ductal cell dedifferentiation and beta-cell neogenesis after 90% pancreatectomy Controlling the false discovery rate: a practical and powerful approach to multiple testing Journal of the Royal Statistical Society Series B 1 Orchestrating high-throughput genomic analysis with Bioconductor limma powers differential expression analyses for RNA-sequencing and microarray studies Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool Mouse beta cell proliferation is inhibited by thymidine analogue labelling Autofluorescence-activated cell sorting of pancreatic islet cells: purification of insulin-containing B-cells according to glucose-induced changes in cellular redox state B and D cells and for the isolation of coupled cells from isolated rat islets Preparation of rat islet B-cell-enriched fractions by light-scatter flow cytometry Beta cells can be generated from endogenous progenitors in injured adult mouse pancreas Proliferation of sorted human and rat beta cells Gene expression analysis of in vivo fluorescent cells and MCM proteins: Markers of proliferation in the diagnosis of breast cancer Combined modulation of polycomb and trithorax genes rejuvenates β cell replication Bmi-1 regulates the Ink4a/Arf locus to control pancreatic beta-cell proliferation Transcriptional control at regulatory checkpoints by histone deacetylases: molecular connections between cancer and chromatin The effect of formaldehyde fixation on RNA: optimization of formaldehyde adduct removal The forkhead transcription factor Foxo1 links insulin signaling to Pdx1 regulation of pancreatic beta cell growth Long live FOXO: unraveling the role of FOXO proteins in aging and longevity Reduced Insulin Production Relieves Endoplasmic Reticulum Stress and Induces β Cell Proliferation Insulin demand regulates β cell number via the unfolded protein response Insulin Signaling Regulates the FoxM1/PLK1/CENP-A Pathway to Promote Adaptive Pancreatic β Cell Proliferation Activation of FoxM1 Revitalizes the Replicative Potential of Aged β-Cells in Male Mice and Enhances Insulin Secretion The FoxM1 transcription factor is required to maintain pancreatic beta-cell mass Overexpression of monocarboxylate transporter-1 (SLC16A1) in mouse pancreatic β-cells leads to relative hyperinsulinism during exercise β-cell-specific gene repression: a mechanism to protect against inappropriate or maladjusted insulin secretion Download references This work was supported by grants from the Catalan Diabetes Association (NT) Carlos III Health Institute (ISCIII) PI17/00108 co-funded by FEDER funds/European Regional Development Fund (ERDF)-“a Way to Build Europe” (EM) and by CIBERDEM which is a project of ISCIII The authors thank the CRG Genomics and Bioinformatics facilities Maria de Lluc Canyelles and Claudia Fernández contributed equally to this work The Barcelona Institute of Science and Technology and UPF obtained and analysed the data and contributed to discussion conceived the method design and wrote the manuscript All authors reviewed the final version of the manuscript The authors declare that they have no competing interests Download citation DOI: https://doi.org/10.1038/s41598-017-17776-2 Anyone you share the following link with will be able to read this content: a shareable link is not currently available for this article Sign up for the Nature Briefing newsletter — what matters in science Metrics details Circulating tumour cells (CTCs) are rare tumour cells found in the circulatory system of certain cancer patients The clinical and functional significance of CTCs is still under investigation Protein profiling of CTCs would complement the recent advances in enumeration transcriptomic and genomic characterization of these rare cells and help define their characteristics Here we describe a microfluidic western blot for an eight-plex protein panel for individual CTCs derived from estrogen receptor-positive (ER+) breast cancer patients The precision handling and analysis reveals a capacity to assay sparingly available patient-derived CTCs a biophysical CTC phenotype more lysis-resistant than breast cancer cell lines a capacity to report protein expression on a per CTC basis and two statistically distinct GAPDH subpopulations within the patient-derived CTCs Targeted single-CTC proteomics with the capacity for archivable multiplexed protein analysis offers a unique complementary taxonomy for understanding CTC biology and ascertaining clinical impact Direct measurement of multiple proteins in single-CTCs comprises a critical complement to single-CTC transcriptomic and genomic studies the current format of the single-cell western blot requires 1000s of cells to account for cell losses when settling into the microwells single-cell resolution western blot (scWB) to measure a panel of proteins in single CTCs isolated from patients with primary estrogen receptor-positive (ER+) breast cancer The rare-cell scWB quantifies multiple surface and intracellular signalling proteins—in each individual CTC—allowing estimates of biological protein expression variation among CTCs as compared with a quantitative threshold for technical variation that we establish We show that the rare-cell scWB is compatible with established CTC isolation tools thus successfully analysing CTC populations with as few as two starting cells In a pilot study of ER+ metastatic breast cancer patient-derived CTCs we observe a lysis–hardy CTC phenotype and the unique capacity to normalize target protein expression by the number of CTCs analysed per assay The rare-cell scWB offers a new approach to examining CTCs with relevance spanning from understanding CTC biology to monitoring an individual’s response to therapy Putative CTCs are visually identified using Hoescht 33342 nuclear stain and each identified CTC is micropipetted (under microscopy) into a 50 μm diameter microwell (micrographs in inset) Step iii: after the seating of one CTC into one microwell single-cell western blotting proceeds as in-microwell chemical CTC lysis covalent immobilization of proteins to the gel (photo-blotting) and in-gel immunoprobing Step iv: single-CTC lysate is analysed by western blotting and rounds of immunoprobing support the multiplexing of 12 proteins with expression is compared among patient-derived CTCs and to spiked cell line validation studies 25 μm (for the cell micrographs) and 250 μm (the separation micrographs) After spiking the cancer cells into healthy blood the samples were purified in the same manner as patient-derived CTCs (a) Fluorescence micrographs and intensity plots from rare-cell scWB handling and analysis of healthy blood samples each spiked with a cancer subtype: EGFR+(BT-20) Negative controls include analysis of WBCs only and blank microwells (that is Protein panel comprises the following: control and housekeeping proteins (GAPDH and β-tubulin) (b) Comparative protein expression for each cancer cell (BT-20: n=27; SK-BR-3: n=27; MCF7: n=35) Protein expression is graphed using a log-scale Ranked oncoprotein expression for each cell line agrees with cancer subtype Less than 1% of total protein signal is attributable to CD45 rare-cell scWB analyses of pure WBC populations reported only CD45 and GAPDH signal with no measurable signal from any cancer-specific protein target thus establishing co-expression of CD45 and GAPDH and negative cancer marker response as selective for WBCs When microwells were empty in the spiked cancer cell studies (‘blank’ wells) the rare-cell scWB did not detect CD45 or GAPDH In assessing potential ‘cross-talk’ between proximal microwells we did not observe detectable protein in empty microwells proximal to cancer marker-positive cell-laden microwells with the exception of low-level EpCAM background the validation study suggests that (i) the cancer markers are selective for putative cancer cells (as expected from the literature) and (ii) the protein panel allows the rare-cell scWB to distinguish between cancer cells and WBCs As is relevant to emerging clinical indicators of prognosis the observation corroborates the utility of the rare-cell scWB to capture both single CTCs and perhaps also CTCs associated with other cells (although association mechanisms are not currently understood) The primary molecular classification marker exhibited higher variability than other classification markers in two of the cancer cell lines (HER2: σSK-BR-32=2.08 × 1012 EpCAM expression in MCF7 and BT-20 cells had a wider distribution than that observed in the SK-BR-3 cell lines (σMCF72=3.00 × 1011; σSK-BR-32=1.80 × 1010; σBT-202=2.72 × 1011) For surface proteins known to be minimally or not expressed in each cancer subtype we observed minimal variability in expression among each population (for example numerous and even unexpected relationships may be identified by deeper profiling such as that provided by 8- to 12-plex scWB analysis of cancer cells Micrographs of rare-cell scWB of patient-derived CTCs in representative cases where CD45 was not detected (CD45−) We extended the lysis duration and elevated the lysis buffer temperature (that is Na-DOC at 0.5% and lysis buffer duration of 20–25 s at 60–65 °C) The increased temperature aids in reducing the CMC we observed successful lysis and separations of CTCs from Patients 5 The number of CTCs counted after immunostaining did not match to the number of CTCs analysed by rare-cell scWB as each measurement was performed on a unique blood fraction with no guarantee of a matched number of CTCs in each The rare-cell scWB was suitable for protein analysis of CTCs from patients with both low (Patient 6) and high (Patient 10) CTC counts the stringent lysis conditions were applied rare-cell scWB analyses of patient-derived CTCs from Patients 5–11 (a) Expression for each protein marker and each patient-derived CTC, with comparison with CD45 levels from scWB analyses of pure WBC controls. (b) CVs for protein expression (AUC) from the patient-derived CTCs. Dashed line indicates the threshold in protein expression variation established using GFP-expressing MCF7 cells (see Supplementary Fig. 3) (c) Biaxial plots report protein expression for all markers for each patient-derived CTC from Patients 5 (n=6) Protein target expression was normalized by microwell occupancy, which was one CTC per microwell with the rare-cell handling workflow described. We attribute the observed CTC-to-CTC variation in protein expression levels to biological differences, as all protein panel targets had variability that exceeded the technical variation cutoff (Fig. 4b) we observed a wider distribution among the CTCs as compared with the ER+ MCF7 cells (σCTC2=4.33 × 1012 This CTC EpCAM expression heterogeneity underscores the challenge for immunocapture-based enrichment the patient-derived CTCs exhibited a larger CV than the MCF7 cells suggesting that the patient-derived CTCs have higher variation in GAPDH (CVCTC=123% in ER protein expression the patient-derived CTCs exhibited a narrower distribution than the MCF7 cells (σCTC2=8.20 × 109 these findings point to potential limitations of using cancer cell lines as models for patient-derived CTCs To further contextualize CTC-to-CTC variation in protein expression, we compared each patient-derived CTC with all other patient-derived CTCs for Patients 5, 6 and 10 (Fig. 4c) In contrast to the cell line spiking experiments with patient-derived CTCs we observed low variability in GAPDH expression between Patients 5 we observed high CVs for panCK (CVP5=110% CVP10=71% In accordance with our breast cancer cell line observations the ER+ breast cancer patient-derived CTCs also exhibited correlation between ERK and GAPDH (rCTCs=0.579 P<0.01; n=20) and between the pairs ERK with β-tubulin (rCTCs=0.691 P<0.01; n=20) and EpCAM with β-tubulin (rCTCs=0.6 Among the patient-derived CTCs, we detected no statistically significant outlier CTCs (F-test)—with regards to exceptionally high or low protein expression—when target expression was normalized to the number of CTCs analysed in each scWB (that is, one CTC analysed per microwell). However, the GAPDH expression suggests two distinct CTC sub-populations (Fig. 4c) which was confirmed with a F-test comparing a one-population model and a two-subpopulation model for the data resulting in an F-statistic of 3.89 and a P-value of 0.035 (degrees of freedom: (1,4)) thus suggesting two possible populations of GAPDH expression The scWB leverages short distances and timescales to rapidly complete lysis PAGE and protein blotting of proteins in single CTCs The careful control of sample and analysis affords the unique option to forgo normalization by protein housekeeping proteins and directly assign protein levels on a per CTC basis Important to longitudinal studies, the scWB is archivable30 which allows later-date profiling of new targets of interest with previously analysed single-CTC lysates CTC lysates are covalently immobilized to the PA gel layer on the scWB device a stable linkage compatible with long-term storage for retrospective CTC analysis Although chemical fixation of CTCs also yields biospecimens suitable for long-term storage and retrospective studies cell fixation is incompatible with stripping procedures and suffers from several pre-analytical variables including the following: epitope disfigurement during fixation especially changes in posttranslational modifications loss of antigenicity owing to over- and under-fixation analytical variables including target cross-reactivity with moderate specificity antibodies lab-to-lab variation and qualitative but not quantitative analyses Although the rare-cell scWB requires further long-term storage performance characterization and larger-scale patient studies the targeted proteomics tool introduced here presents a promising approach to multiplexed archival protein analysis of single CTCs with direct relevance to longitudinal studies the microfluidic form factor of the assay may find utility in low-resource settings especially with further engineering integration of the cell purification and handling fluidics The cell line and CTC experiments used an 8%T PA gel with arrays of 50 μm diameter and 60 μm-deep microwells All PA gels were chemically polymerized with 0.08% APS and 0.08% TEMED A separate SU-8 master was created to fabricate the PDMS mesofluidic insert used to localize large volumes (∼700 μl) of enriched cells over the microwell array in the PA gel layer The insert dimensions were 37.5 mm × 50 mm with an opening comprising the volume reservoir of 20 mm × 30 mm PDMS polymer base and curing agent were mixed (ratio 10:1) poured over the insert master and cured for 2 h at 70 °C we acquired healthy donor blood and spiked with cell lines representing three major breast cancer subtypes: triple-negative (BT-20) MCF7 and SK-BR-3 cells were obtained from the American Type Culture Collection and authenticated using short tandem repeat analysis (Promega) All cell lines tested negative for mycoplasma BT-20 (ER−/PR−/HER2−) was maintained in Eagle’s minimal essential medium supplemented with 1% penicillin/streptomycin and 10% FBS MCF7 (ER+/PR−/HER2−) was maintained in RPMI 1640 supplemented with 1% penicillin/streptomycin 0.01 mg ml−1 insulin (Invitrogen) and 10% FBS SK-BR-3 (ER−/PR−/HER2+) was maintained in McCoy’s 5A supplemented with 1% penicillin/streptomycin and 10% FBS was obtained from the American Type Culture Collection and authenticated using short tandem repeat analysis (Promega) The cell line was maintained in RPMI 1640 supplemented with 1% penicillin/streptomycin All cell lines were cultured in an incubator held at 37 °C under 5% CO2 and tested for mycoplasma contamination Twelve patients with advanced breast cancer were recruited according to a protocol approved by the Institutional Review Board (Stanford IRB 350–Panel 3–Protocol 5630) from the Department of Oncology at the Stanford School of Medicine stored at room temperature and processed within 5 h after collection The microfluidic device was first primed with PBS the diluted blood sample was processed through the Vortex HT chip (8 ml min−1) followed by a wash step with PBS to remove contaminating red blood cells and WBCs (8 ml min−1) Stopping the flow dissipates the vortices and releases the cancer cells from the microscale reservoirs for direct deposition on the top surface of the scWB platform The enriched volume was ∼300 μl and was contained by a mesofluidic PDMS insert that sits atop the scWB 300–600 cells from 1 cell line were spiked into 1 ml healthy donor blood and processed using the Vortex chip the cells isolated in the vortices were directly collected into the mesofluidic PDMS insert seated on top of the scWB PA gel for cell positioning into microwells For both cell line spiking and patient-derived cell experiments a volume of blood was reserved for subsequent red blood cell lysis to perform control experiments with WBCs WBCs were prepared by lysing the red blood cells with Buffer EL (Qiagen) 0.5 ml of whole blood was combined with 2.5 ml of Buffer EL (Qiagen) The tube was inverted several times and incubated for 10–15 min at room temperature After centrifugation at 228 g for 5 min at room temperature The pellet was re-suspended with 2.5 ml of Buffer EL and the process repeated the WBCs were washed once with 1 ml of Buffer EL The scWB assay can be completed within ∼20 h Primary antibodies and fold dilutions against GAPDH (1:20 goat polyclonal antibody (pAb); SAB2500450 Sigma) were the immunoprobes in both breast cancer cell lines (BT-20 MCF7 and SK-BR-3) and patient-derived CTCs Abcam) followed by anti-goat AlexaFluor 555-conjugated secondary antibody (A21432 Secondary antibodies to goat IgG pre-labelled with AlexaFluor 488 and 555 (A11055 and A21432) mouse IgG pre-labelled with AlexaFluor 488 and rabbit IgG pre-labelled with AlexaFluor 488 A31572 and A31573) were used as prepared by the vendor (Invitrogen) All secondary antibodies were applied as a 1:20 dilution Flow cytometry analysis was performed on MCF7 cells to ascertain the effects of enzymatic detachment on the EpCAM antigen MCF7 cells were detached from tissue culture plates either by trypsin-EDTA (0.25% Gibco 25200072) or by EDTA alone (Ultrapure 0.5 M EDTA Gibco 15575020 diluted in PBS to 5 mM) Half the cells were labelled with anti-EpCAM–AlexaFluor488 (mouse eBioscience) and half were labelled with mouse IgG AlexaFluor488 (A21202) as an isotype control 2 × 106 cells were resuspended in 100 μl of 3% BSA (Sigma A2058) in PBS containing antibody at a concentration of 1 μg ml−1 and incubated over ice for 30 min then resuspended in resuspension buffer (1% BSA Cells were analysed on a Guava flow cytometer (Millipore) A total of 10,000 events were collected per sample four samples per experimental group (n=4) and data were compiled and analysed using FlowJo software SK-BR-3 (n=34 and n=30) and MCF7 (n=42 and 40) The null hypothesis that the GAPDH protein expression distributions are equivalent across the technical replicates was supported Cells with similar (<5% variation) GFP AUC were binned and considered a homogeneous GFP-expressing sample with a 1.27–3.37% difference in AUC from the lowest and highest GFP AUC of each bin observed The technical variation cutoff was defined as 3 s.d above the average CV of protein expression (for a 99.7% confidence interval) Quantification of protein PAGE and probing used in-house MATLAB scripts as described in Kang et al.29 Band widths were characterized by Gaussian curve fitting in MATLAB (R2014b Curve Fitting Toolbox) if the Gaussian had a R2-value>0.7 the integrated intensity for the region of interest was calculated Multiple statistical analyses were performed to compare protein distribution To determine significance between the different protein CVs observed we performed a t-test statistic and used a permutation test to determine the P-values The Levene’s test was used to determine non-equivalence of the variance between the markers for each cell line (BT-20 To classify a group of CTCs as a sub-population based on GAPDH expression in Patient 5 an F-test for model selection was performed Model 1 assumed one population exists and model 2 assumed two sub-populations exist The F-test compares the two models with the null hypothesis considering the data follows model 1 instead of model 2 To detect correlation in protein expression between proteins, a Spearman’s rank correlation was performed, as the correlation of protein expression between two proteins was expected to be monotonic but not necessarily linear. Two proteins in the panel were sequentially paired (Supplementary Table 3) to determine possible correlations Only correlations with a P-value ⩽0.01 were considered significant The authors declare that all the data are available within the article file and its Supplementary Information or from the corresponding author upon reasonable request Profiling protein expression in circulating tumour cells using microfluidic western blotting Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations Significance of circulating tumor cells detected by the cellsearch system in patients with metastatic breast colorectal and prostate cancer Isolating highly enriched populations of circulating epithelial cells and other rare cells from blood using a magnetic sweeper device Isolation of rare circulating tumour cells in cancer patients by microchip technology Size-selective collection of circulating tumor cells using Vortex technology Membrane microfilter device for selective capture electrolysis and genomic analysis of human circulating tumor cells Circulating tumor cells predict survival in early average-to-high risk breast cancer patients Changes in circulating tumor cell detection in patients with localized breast cancer before and after surgery mRNA and microRNA expression profiles in circulating tumor cells and primary tumors of metastatic breast cancer patients Whole-exome sequencing of circulating tumor cells provides a window into metastatic prostate cancer Single cell mutational analysis of PIK3CA in circulating tumor cells and metastases in breast cancer reveals heterogeneity and mutation persistence in cultured disseminated tumor cells from bone marrow Correlation between protein and mRNA abundance in yeast Protein pathway and complex clustering of correlated mRNA and protein expression analyses in Saccharomyces cerevisiae Global analysis of protein expression in yeast Proteogenomic characterization of human colon and rectal cancer multiplexed analysis of proteins in microliter quantities of blood Single-cell codetection of metabolic activity and genetic mutations from rare circulating tumor cells EPISPOT assay: detection of viable DTCs/CTCs in solid tumor patients Functional analysis of single cells identifies a rare subset of circulating tumor cells with malignant traits Androgen receptor expression in circulating tumour cells from castration-resistant prostate cancer patients treated with novel endocrine agents Essential Cytometry Methods Academic Press (2009) with an assessment of Tyramide signal amplification multispectral imaging and multiplex analysis Circulating tumor cells: advances in isolation and analysis Seventeen-colour flow cytometry: unravelling the immune system Truncated p110 ERBB2 induces mammary epithelial cell migration invasion and orthotopic xenograft formation and is associated with loss of phosphorylated STAT5 Toward analysis of proteins in single cells: a quantitative approach employing isobaric tags with MALDI mass spectrometry realized with a microfluidic platform An open letter to our readers on the use of antibodies Single-cell western blotting after whole-cell imaging to assess cancer chemotherapeutic response Classification of large circulating tumor cells isolated with ultra-high throughput microfluidic Vortex technology Circulating tumor cells (CTCs) in metastatic breast cancer (MBC): prognosis drug resistance and phenotypic characterization Determination of HER2 status using both serum HER2 levels and circulating tumor cells in patients with recurrent breast cancer whose primary tumor was HER2 negative or of unknown HER2 status Targeting the phosphoinositide-3 (PI3) kinase pathway in breast cancer Roles of the Raf/MEK/ERK pathway in cell growth malignant transformation and drug resistance Overexpression of the proto-oncogene/translation factor 4E in breast-carcinoma cell lines mTOR inhibition induces upstream receptor tyrosine kinase signaling and activates Akt PI3K/AKT/mTOR inhibitors in patients with breast and gynecologic malignancies harboring PIK3CA mutations Deregulation of glycolysis in cancer: glyceraldehyde-3-phosphate dehydrogenase as a therapeutic target Quantitative high-resolution genomic analysis of single cancer cells Circulating tumor cell clusters are oligoclonal precursors of breast cancer metastasis Multiplex flow cytometry barcoding and antibody arrays identify surface antigen profiles of primary and metastatic colon cancer cell lines EpCAM: Structure and function in health and disease Overcoming technical variation and biological variation in quantitative proteomics Microfluidic single-cell whole-transcriptome sequencing Heterogeneity of estrogen receptor expression in circulating tumor cells from metastatic breast cancer patients Rapid phenotypic and genomic change in response to therapeutic pressure in prostate cancer inferred by high content analysis of single circulating tumor cells KI-67 and AR by immunohistochemical analysis in breast cancer cell lines A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes Choosing the right cell line for breast cancer research Epidermal growth factor receptor (EGFR)-targeted immunoliposomes mediate specific and efficient drug delivery to EGFR- and EGFRvIII-overexpressing tumor cells Mixed micelles of triton x‐100 and sodium dodecyl sulfate and their interaction with polymers Interactions between sodium dodecylsulphate and Triton X-100: molecular properties and kinetics investigations Epidermal growth factor-like repeats mediate lateral and reciprocal interactions of Ep-CAM molecules in homophilic adhesions The dynamic structure of the estrogen receptor Mass cytometry: technique for real time single cell multitarget immunoassay based on inductively coupled plasma time-of-flight mass spectrometry marker-free isolation of circulating tumor cells from blood samples Albumin and mammalian cell culture: Implications for biotechnology applications Ex vivo culture of circulating breast tumor cells for individualized testing of drug susceptibility Tumour heterogeneity and cancer cell plasticity Stem cell and epithelial-mesenchymal transition markers are frequently overexpressed in circulating tumor cells of metastatic breast cancer patients Circulating tumor cells from patients with advanced prostate and breast cancer display both epithelial and mesenchymal markers Tumor metastasis: mechanistic insights and clinical challenges Download references We thank the breast cancer patients and healthy donors who generously consented to provide the blood samples necessary for this study M.D.) who assisted with patient recruitment The research reported in this publication was supported in part by the US National Institutes of Health and the National Cancer Institute (R21CA183679 to A.E.H.) the National Institute of Biomedical Imaging and Bioengineering (R21EB019880 to A.E.H.) and the Office of the Director's New Innovator program (DP2OD007294 to A.E.H.) with a Diversity Supplement (to E.S.) a CIRM Predoctoral Fellowship and Obra Social `la Caixa' Fellowship (to E.R.C.) and a National Science Foundation Graduate Research Fellowship (to T.A.D. UC Berkeley Biomolecular Nanotechnology Center (BNC) provided support for device fabrication The UC Berkeley–UCSF Graduate Program in Bioengineering performed single-CTC western blottings and analysis performed fluorescence-activated cell sorting-based validation experiments purified protein control experiments and experiments for scWB benchmarking against fluorescence imaging coordinated patient recruitment and healthy blood samples collection designed software for fluorescence quantitation has financial interest in intellectual property related to the device and assay described here and may benefit from royalties from licensing has financial interest in commercialization efforts have financial interests in Vortex Biosciences All other authors declare no competing financial interest Supplementary Figures and Supplementary Tables (PDF 925 kb) Download citation Sorry, a shareable link is not currently available for this article. 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MusicInnovation& Creativity12.13.14June 2025BarcelonaProgrammeTicketsSónar+DPractical infoPlaylistsPartnersBack25/09/2023You can now watch the Piromusical at La Mercè 2023 plus explore the full playlist On the evening of Monday 25th of September Sónar closed its 30th anniversary celebrations by providing the soundtrack for the closing ceremony of La Mercè in Barcelona drawing the curtain on the city's biggest annual celebration The creative team at Pirotècnia Igual (Canyelles) studied the soundtrack provided by Sónar for over a month in order to decide which effects to combine with each moment depending on the rhythm and intensity of the music The team then spent  over 20 days developing the spectacle which involved over 1,300kg of pyrotechnic material spread across 700 installations over 15,000 discharges were fired during the show accurate to within a hundredth of a second the opening notes of Ryuichi Sakamoto's ‘Chasm’ rang out a piece chosen especially by Sónar to pay tribute to the legendary Japanese composer The show lasted 30 minutes and featured five segments of music mixed and mastered by Phran a DJ and producer who’s a regular performer at Sónar The soundtrack took the audience on a global journey through sounds and rhythms from all five continents: a cross-cultural journey and a giant celebration featuring classic tracks from some of the most legendary names in modern music From Rosalía and Bad Gyal to Daft Punk and Pet Shop Boys And from Björk and Aphex Twin to Miss Kittin and Jeff Mills Just some of the artists from the history of the festival that were shared with over 100,000 people who attended the show plus the 1 million spectators who followed it live on TV3 Listen to all 52 tracks in their entirety in the playlist for the Piromusical de La Mercè 2023 ya Now available via the Sónar Spotify account Stray beyond Barcelona and you’ll find that Catalonia has some delightful spots for the adventurous boater hoping to make the most out of the Med Tucked beneath a wooded hill and an old castle Blanes (pictured below) is a pleasant fishing and yacht harbour a welcome change after cruising up the mostly flat coastline from Barcelona The town has good beaches and an intriguing ruined palace The cliffs start rising immediately beyond Blanes and a procession of headlands stretches away to the distant corner of Catalonia which make the Costa Brava so enticing from the sea Many smaller calas can only be reached by boat and you anchor in such piercingly clear water that plunging overboard is irresistible Three miles from Blanes you skirt the packed resort of Lloret de Mar before the coast turns wild again past a string of inlets Cala Gran is delightful and then you reach the tiny club marina at Canyelles Tucked under a wooded cliff near a dazzling beach Cala Canyelles has a narrow gap into a shallow pool where locals moor stern-to the jetties visiting boats up to about 35ft can squeeze into the first section behind the breakwater but in settled weather you can anchor off the beach Beyond Point Garbí is an impressive sweeping bay where a long mole protects the relaxed pleasure-seeking marina at Sant Feliu de Guíxols the winding village-style marina of Port d’Aro is set between a wooded park and a halcyon beach Port d’Aro is a safe place to winter and has good facilities for getting work done Look out for your first newsletter in your inbox soon We help you navigate a myriad of possibilities Sign up for our newsletter for the best of the city By entering your email address you agree to our Terms of Use and Privacy Policy and consent to receive emails from Time Out about news Sign up for our email to enjoy your city without spending a thing (as well as some options when you’re feeling flush) Our newsletter hand-delivers the best bits to your inbox Sign up to unlock our digital magazines and also receive the latest news By entering your email address you agree to our Terms of Use and Privacy Policy and consent to receive emails from Time Out about news, events, offers and partner promotions. Girona Who says beachside dining is strictly for summertime these are our top beachy stops after a long day at the beach or even on a sunny winter afternoon.  Thanks for subscribing! Look out for your first newsletter in your inbox soon! twitterinstagramAbout us Contact us Time Out Worldwide General view of the exit of Barcelona on the Avinguda Meridiana with the neighbourhood of Vallbona to the right of the bridge and Ciutat Meridiana and Torre Baró to the left. © Myriam Meloni i Arnau Bach a photographic project by Myriam Meloni and Arnau Bach we see the Barcelona behind the ring roads The Barcelona of the Rec Comtal irrigation canal and the old Ribes road The Barcelona that every train commuter relates to the image More than drawing closer to the farthest Barcelona the photographs welcome us to the city’s first neighbourhoods Myriam Meloni and Arnau Bach offer a profound contemporary photographic portrait – verging on the ethnographic – of the four border neighbourhoods in the far north of the city: “The primary interest is to photographically portray the limits of Barcelona and Nou Barris is the district furthest from the centre” the four neighbourhoods that mark the city limits and lend them a name are Canyelles if you get sidetracked while walking through the thick forests or up the really steep slopes which entailed not only photographing the main characters in the great little stories told in Linde Co-author Myriam Meloni explains the approach she adopted when exploring the neighbourhoods and their people: “First we went to the residents’ associations because they have the most connection with the social fabric of each neighbourhood but from there we try not to be bound to be spokespeople for their demands which would undoubtedly provide us with a more complete and Esperanza went from living in a shack in the neighbourhood of El Carmel to living in a flat in Canyelles The longstanding president of the Ciutat Meridiana Residents’ Association these neighbourhoods have been home to people from very different backgrounds and with fairly low economic means are the three neighbourhoods with the lowest average family income in the city Vallbona and Torre Baró do not amass even 5,000 residents The latter neighbourhood also has a population density of 28,000 people per square kilometre although far from the population density of the neighbourhood La Florida which ranks the highest in Europe with more than 74,000 inhabitants per square kilometre The houses are also different depending on the neighbourhood In Torre Baró and Vallbona many self-built In Canyelles and Ciutat Meridiana there is a profusion of warren-type many of which lack decent living conditions Past (and present) of neighbourhood struggle Filiberto Bravo is an institution in Ciutat Meridiana Longstanding president of its residents’ association his legacy of neighbourhood struggle is an encyclopaedia open to anyone who talks to him: “Filiberto’s vision of the neighbourhood is one of togetherness and social struggle but the possible vision of Ciutat Meridiana held by a woman who has recently migrated from a small town in Morocco is a sense of freedom” having a close-knit community that cares for one another but at the same time does not interfere in each other’s lives is critical for personal development in freedom” Bellvitge on the northern border of Barcelona as one of the testimonials presented in Linde notes it is also class dignity: “When they proposed we come to live in Canyelles […] At night I could only think of the flat – Esperanza lived with her family in a shack in El Carmel – of how it was made but for me it was a palace… And it still is.” Although denouncing social injustice has helped keep the feeling of attachment alive among its residents after so many generations lapsing into showing Ciutat Meridiana just as Evictionville and the x of the equation was already resolved by Candel in Els altres Catalans [The Other Catalans]: “In reality It is the sad fate of their status as a low proletariat.” In Linde the exploration of reality of four of Barcelona’s poorest neighbourhoods seeks to express itself through beauty and eschewing drama it moves away from the constant historicist examinations that are made of the now thirteen “nou barris” [new neighbourhoods] the realities of the four neighbourhoods portrayed in the book are woven together in a narratively richer whole “but in Linde it was not our intention to speak of the other objectively but to afford a glimpse within a much more complex reality” When a journalist has to cover a story about precariousness they should always be attuned to the signal that warns of the danger of yielding to the romanticisation of poverty Stories of precariousness are passed on orally by the person concerned; the journalist listens to them internalises them and contextualises them (or they should); then they portray that story they publish it for the scrutiny and judgment of public opinion neither with the publication nor with the payment received by the journalist but continues to be the unique and current reality of that person and their environment The great balancing act entails telling the story in a manner that is mindful of otherness and that is only achieved over time and through an honest relationship with the sources among other things: “The main idea was to decipher and understand the day-to-day life of these neighbourhoods which end up being the fringes of the fringes when they are not and should not be considered as such Beyond the economic reality and the historical institutional neglect of these neighbourhoods there is another factor that explains how the distinctive characteristics of their residents are structured and how the feeling of attachment has been ignited here: all four are recent neighbourhoods built in many cases by the actual residents who still reside in them who inherited the homes that their parents built four walls and a roof were raised at night so that the wardens couldn’t demolish the construction It is not the only example of neighbourhoods built home by home by their own residents: Huertas Clavería tells us in his Barrios de Barcelona [Barcelona’s Neighbourhoods] how the residents provided some rudimentary steps to spare the residents the slopes in Torre Baró Another example: during the hijacking of bus line 47 in May 1978 (which served to demonstrate to the city council that the bus could climb the slopes of these neighbourhoods) too steep for the Pegaso Monotral steered by the bus driver Manuel Vital people continue to make small improvements in these neighbourhoods without asking for permission or pardon: “Here the feeling of attachment is very different from that of a neighbourhood that was built centuries ago by people already forgotten and whose history has been lost” Many were built by their owners in the mid-20th century Until the Congost bridge was built in 2005 Only a goat path connected it with the adjacent neighbourhoods of Torre Baró and Ciutat Meridiana someone prepares what is needed and in a couple of days children are already playing soccer young people will adapt it to rehearse urban music choreographies: “The legislation is the same as in the rest of the city Nor do they need to direct thousands of tourists each day.” Myriam Meloni rounds off the reflection: “There every piece of public space has been allocated a use It ends up being a matter of economic interest each piece of city has a huge potential for economic revenue; but not here” The centralist and productive conception of here and there is blurred in these neighbourhoods Candel was referring to this type of peripheral neighbourhoods with his famous Donde la ciudad cambia su nombre [Where the City Changes Its Name] and while it is true that the residents (including the photographer who has spent a bit more than a year in these neighbourhoods as read in the previous paragraph) say “go to Barcelona” when they are already in it (something that also happens in the neighbourhoods that centuries ago were independent towns) the historical aspiration of the residents of Canyelles Vallbona and Ciutat Meridiana is to overcome this otherness and be treated just like the rest of Barcelona Giving new meaning to sometimes monstrous spaces The relationship with nature is much closer at these latitudes of the city the last vestiges of the Rec Comtal irrigation canal are still used by young people to go for a dip and the last vegetable gardens in the city also lie in this area In Linde we become acquainted with the story of Rosita a wild boar that roams the area: “When I call her” “she always comes to me and we spend time together Blas works the land and has raised animals the landscape changes in a few hundred metres From the mountain surroundings we enter the hub of roads (C-17 the city’s quintessential non-place that has been reappropriated by its residents Ciutat Meridiana and Vallbona they have learned to live next to the mountains they have still had more to learn to live hemmed-in between piles of concrete The entry road links to Barcelona to the north have marked the life of these neighbourhoods separating them from the rest of the city and from each other motorway entries and exits and columns of implausible diameters to hold it all together ooze through the hovels the little vegetable gardens and the waste grounds of Barcelona’s northernmost neighbourhoods The photographs of these landscapes featured in Linde convey that overwhelming sense of insignificance of human measure in the presence of such architectural abominations Two members of the dance troupe La Virgen del Quincho named in honour of a very popular virgin in Ecuador who rehearse every Sunday on wasteland in Ciutat Meridiana The Ciutat Meridiana sloping lift connects to Torre Baró suburban train station and Ciutat Meridiana's line 11 metro station.  © Myriam Meloni i Arnau Bach Many of the residents who use these non-places to meet up come from realities in which many people had to live in miniscule places such that all social life took place on the street many of the flats in Canyelles and Ciutat Meridiana are tiny and are still inhabited by lots of people so to a certain extent they are not only reproducing customs but also they are still adapting to the circumstances “This also occurs in the Raval neighbourhood Occupation of the public space is a very cultural thing It is a reappropriation of space without too much press The residents of these neighbourhoods have given a new meaning to the non-place meeting up with their families and friends In short: “The space outside homes is given new meaning turning it into something to be shared by the community” Under tons of cement and countless cars that travel in and out and cross the city limits in a frenzy of movement at ground level and availing of the shade under the bridges And they are dressed in regional costumes that they have been sewing for weeks from being there so long and having made the place their own they have also internalised the constant and piercing noise of rolling tyres and rattling engines Subscribe to our newsletter to keep up to date with Barcelona Metròpolis' new developments spicy sobrasada sausage spread generously on to sweet toast and marmalade will always seem disappointing It’s just one of Mallorca’s many delicacies and it’s served at a new five-star hotel that has opened in Santanyi in the southeast of the island."},"children":[]}]},{"name":"paragraph","children":[{"name":"text","attributes":{"value":"Thanks to its peaceful lifestyle and picturesque surroundings Santanyi has been attracting increasing international interest And the arrival of Can Ferrereta means that the town is now a serious player in the luxury holiday market."},"children":[]}]},{"name":"paragraph","children":[{"name":"text","attributes":{"value":"The hotel which is full of intriguing historical touches is on the site of a Mallorcan stately home thought to have been built in the 17th and 18th centuries An ornate stone pathway leads you through the entrance; it was"},"children":[]},{"name":"paywall","children":[{"name":"text","attributes":{"value":" originally a passage for horses and other animals past an iron sculpture by the Catalan artist Josep Riera i Aragó that resembles an aeroplane propeller."},"children":[]}]}]},{"name":"paywall","children":[{"name":"image","attributes":{"id":"6318cbe6-3233-4013-8e2d-310631760292","display":"primary","caption":"The hotel’s Ocre restaurant","title":"Can Ferrereta Mallorca","credits":"ARTURO+LAUREN","url":"https://www.thetimes.com/imageserver/image/%2Fmethode%2Ftimes%2Fprod%2Fweb%2Fbin%2F112ea6dc-c39b-11eb-a26e-4c086490cfe1.jpg?crop=5804%2C3869%2C0%2C0","ratio":"1500:1000","relativeHorizontalOffset":0,"relativeVerticalOffset":0,"relativeWidth":0.9649210307564422,"relativeHeight":1},"children":[]},{"name":"paragraph","children":[{"name":"text","children":[],"attributes":{"value":"Art is a theme: the hotel is bursting with works including a quarter-tonne bronze sculpture by Jaume Plensa next to the hotel’s 25m outdoor swimming pool and there’s even an original Miró in my bedroom."}}]},{"name":"paragraph","children":[{"name":"text","children":[],"attributes":{"value":"The grandeur of the building is complemented by friendly welcoming touches; the idea was to create the feeling of staying with (rather extravagant) relatives tells me."}}]},{"name":"ad","children":[]},{"name":"paragraph","children":[{"name":"text","children":[],"attributes":{"value":"Can Ferrereta forms part of an independent portfolio (which includes Sant Francesc a hotel in a 19th-century neoclassical mansion in Palma) run by their eldest son I speak to Soldevila Jr in the hotel’s cosy library which has shelves stuffed with books on style wine and travel."}}]},{"name":"paragraph","children":[{"name":"text","children":[],"attributes":{"value":"Can Ferrereta The plot had remained in the same family for centuries until the Soldevila Ferrers came across it in 2018 a big restoration job was needed and Bastidas Architecture was given the task of preserving the building’s characterful features such as the stone arches and wooden beams."}}]},{"name":"paragraph","children":[{"name":"text","children":[],"attributes":{"value":"Even the new parts of the hotel such as the annexe that houses 12 private suites replicate the style of the original manor; the spa imitates the structure and layout of a Mallorcan barn typical of the agriculture of the region while the pool’s showers are in a recreated"}},{"name":"italic","children":[{"name":"text","children":[],"attributes":{"value":" barraca de roter"}}]},{"name":"text","children":[],"attributes":{"value":" a traditional stone hut for shepherds."}}]},{"name":"paragraph","children":[{"name":"text","children":[],"attributes":{"value":"According to Gerard Bastidas shade is just as important as light in Mallorcan buildings which are designed to protect you from the sun Light and shadow influenced the interior design as well “The property’s natural light has very romantic moments but it is also limited in some spaces,” explains Carla Navas from the Barcelona-based interior design studio Wit “We wanted to keep that chiaroscuro feeling when you walk around.”"}}]},{"name":"inlineAd1","children":[]},{"name":"paragraph","children":[{"name":"text","children":[],"attributes":{"value":"They have succeeded are known for the ochre colour of the buildings The colour lends its name to Can Ferrereta’s restaurant where the chef Alvar Albaladejo serves dishes incorporating traditional Balearic produce such as tap de corti paprika mahones cheese and purple safarnaria carrots."}}]},{"name":"paragraph","children":[{"name":"text","children":[],"attributes":{"value":"Wit has furnished the interior with items by international and home-grown brands from Mogg and Carl Hansen to Blasco and Lo de Manuela Woven rope contrasts with soft linen upholstery while rustic wooden tables and seats bring a warm touch against the sandstone sourced from the local quarry."}}]},{"name":"paragraph","children":[{"name":"text","children":[],"attributes":{"value":"Leaving to explore the town a remnant of the city walls built in the 16th century to defend against Ottoman and Moorish invaders who coveted this town and its gateway position to the island Santanyi’s location is no less desirable today although for rather different reasons — it’s 45 minutes by car from Palma airport and a short drive from beaches such as Cala Santanyi Germans have been coming to Santanyi for years and not just on holiday drawn by the laid-back Mallorcan way of life arrived here in the mid-1990s and has been running his restaurant serving seasonal Mediterranean dishes such as"}},{"name":"italic","children":[{"name":"text","children":[],"attributes":{"value":" llengua amb taperes "}}]},{"name":"text","children":[],"attributes":{"value":"(beef tongue with capers) and "}},{"name":"italic","children":[{"name":"text","children":[],"attributes":{"value":"frit mallorqui "}}]},{"name":"text","children":[],"attributes":{"value":"(the island’s traditional stew made with pork or lamb)."}}]},{"name":"inlineAd2","children":[]},{"name":"paragraph","children":[{"name":"text","children":[],"attributes":{"value":"Another reputed restaurateur in town was born in Germany and raised in Mallorca from the age of two Five years ago he opened his stylish establishment Laudat — a charming spot for lunch or dinner with a romantic patio filled with lemon trees."}}]},{"name":"paragraph","children":[{"name":"text","children":[],"attributes":{"value":"Laudat works with the local winery Armero i Adrover to produce a range of bespoke house wines — I try the white made with a combination of prensal blanc and giro ros grapes which nicely complements my sea bass fillet with caramelised fennel Judit and her team serve tapas and decadent deserts."}}]},{"name":"image","attributes":{"id":"d2ab9afd-d86f-4843-b351-a376fe1fa608","display":"fullwidth","caption":"The market at Santanyi","title":"market in Santanyi Spain","credits":"ALAMY","url":"https://www.thetimes.com/imageserver/image/%2Fmethode%2Ftimes%2Fprod%2Fweb%2Fbin%2F65e8a42a-c39b-11eb-a26e-4c086490cfe1.jpg?crop=6000%2C4000%2C0%2C0","ratio":"1500:1000","relativeHorizontalOffset":0,"relativeVerticalOffset":0,"relativeWidth":1,"relativeHeight":1},"children":[]},{"name":"paragraph","children":[{"name":"text","children":[],"attributes":{"value":"Santanyi particularly comes to life on Wednesdays and Saturdays when its street market attracts crowds from neighbouring regions to browse summery dresses There are fresh fruit and vegetables in the Plaça Major next to the 18th-century Sant Andreu church preserves and olive oils."}}]},{"name":"paragraph","children":[{"name":"text","children":[],"attributes":{"value":"The bakery Panaderia Lozano tempts with savoury "}},{"name":"italic","children":[{"name":"text","children":[],"attributes":{"value":"panades"}}]},{"name":"text","children":[],"attributes":{"value":" stuffed with meat as well as traditional pastries and cakes such as "}},{"name":"italic","children":[{"name":"text","children":[],"attributes":{"value":"lazos"}}]},{"name":"text","children":[],"attributes":{"value":" (twists of pastry with cream or chocolate) "}},{"name":"italic","children":[{"name":"text","children":[],"attributes":{"value":"xuxos"}}]},{"name":"text","children":[],"attributes":{"value":" (fried Ramón Canyelles produces contemporary clay homeware and sells more traditional earthenware Across town I get an early peek at Terra Origens a new concept store and café spread across three floors scheduled to open this summer as a place to eat and shop; local artisans will also run workshops on pottery and weaving."}}]},{"name":"inlineAd3","children":[]},{"name":"paragraph","children":[{"name":"text","children":[],"attributes":{"value":"At dusk an enchanting luminosity envelops Santanyi as the sun begins to set and everything glows No wonder so many have been drawn here and so many have stayed And I have the bonus of that sausage breakfast at Can Ferrereta to look forward to."}}]},{"name":"paragraph","children":[{"name":"italic","children":[{"name":"text","children":[],"attributes":{"value":"Agnish Ray was a guest of Can Ferrereta B&B doubles from £272 ("}},{"name":"link","children":[{"name":"text","children":[],"attributes":{"value":"hotelcanferrereta.com"}}],"attributes":{"href":"https://www.hotelcanferrereta.com/en/"}},{"name":"text","children":[],"attributes":{"value":") Fly to Palma"}}]}]},{"name":"heading3","children":[{"name":"text","children":[],"attributes":{"value":"Three new buzzing hotels in the Balearics"}}]},{"name":"image","attributes":{"id":"e3a45cf2-0a32-4323-9e86-1d027a7806d6","display":"primary","caption":"Casa Pacha Formentera","title":"CASA PACHA","credits":null,"url":"https://www.thetimes.com/imageserver/image/%2Fmethode%2Ftimes%2Fprod%2Fweb%2Fbin%2Fb1264294-c39b-11eb-a26e-4c086490cfe1.jpg?crop=3000%2C2000%2C0%2C0","ratio":"1500:1000","relativeHorizontalOffset":0,"relativeVerticalOffset":0,"relativeWidth":1,"relativeHeight":1},"children":[]},{"name":"paragraph","children":[{"name":"bold","children":[{"name":"text","children":[],"attributes":{"value":"Casa Pacha Formentera"}}]},{"name":"break","children":[]},{"name":"text","children":[],"attributes":{"value":"Laid-back is the word for the style of luxury taking over the Balearics this summer which means that the nightlife and leisure group Pacha is embracing all things barefoot with this new addition in Formentera so expect ravishing sea views from the rooms The interiors have been decked out by the Ibiza-based designer Patricia Galdón as well as a few 1960s touches evoking the vintage spirit of Pacha lifestyle "}},{"name":"bold","children":[{"name":"break","children":[]},{"name":"text","children":[],"attributes":{"value":"Details "}}]},{"name":"text","children":[],"attributes":{"value":"B&B doubles from £414 ("}},{"name":"link","children":[{"name":"text","children":[],"attributes":{"value":"casapacha.com"}}],"attributes":{"href":"https://www.casapacha.com/"}},{"name":"text","children":[],"attributes":{"value":") Fly to Ibiza"}}]},{"name":"image","attributes":{"id":"19bcf222-df7c-43db-a482-a9aeeaba08df","display":"primary","caption":"Cristine Bedfor Menorca","credits":"DANIEL SCÝFER","url":"https://www.thetimes.com/imageserver/image/%2Fmethode%2Ftimes%2Fprod%2Fweb%2Fbin%2Fd1b2dd88-c39b-11eb-a26e-4c086490cfe1.jpg?crop=5906%2C3937%2C0%2C0","ratio":"1500:1000","relativeHorizontalOffset":0,"relativeVerticalOffset":0,"relativeWidth":1,"relativeHeight":0.8889139760668322},"children":[]},{"name":"paragraph","children":[{"name":"bold","children":[{"name":"text","children":[],"attributes":{"value":"Cristine Bedfor Menorca"}}]},{"name":"break","children":[]},{"name":"text","children":[],"attributes":{"value":"The novice hoteliers Cristina Lozano and Daniel Entrecanales have just opened their debut property a colourful 21-bedroom guesthouse in the heart of Menorca’s capital A fictitious persona invented by the owners gives the hotel its name You’re encouraged to think of her as the perfect hostess in which you can enjoy candlelit dinners and a sparkling pool The interiors are designed by Lorenzo Castillo where this new 20-acre resort opens in July from a yoga platform with sea views to CrossFit cryotherapy and even snorkelling meditation much of it grown on the hotel’s organic farm Tuck into seasonal island specialities such as tomato entrecôte prepared by Israel’s celebrity chef Eyal Shani before heading down to the Live Cave at the waterfront for cocktails and music from visiting artists."}},{"name":"bold","children":[{"name":"break","children":[]},{"name":"text","children":[],"attributes":{"value":"Details "}}]},{"name":"text","children":[],"attributes":{"value":"B&B doubles from £933 ("}},{"name":"link","children":[{"name":"text","children":[],"attributes":{"value":"sixsenses.com"}}],"attributes":{"href":"https://www.sixsenses.com/en/resorts/ibiza"}},{"name":"text","children":[],"attributes":{"value":") Fly to Ibiza"}}]},{"name":"inlineAd4","children":[]},{"name":"paragraph","children":[{"name":"bold","children":[{"name":"text","children":[],"attributes":{"value":"International travel restrictions are in place expert advice and inspiration for 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the"},"children":[]}]}]},"summary({\"maxCharCount\":145})":{"type":"json","json":[{"name":"paragraph","children":[{"name":"text","attributes":{"value":"There is no excuse for missing a polo match in Sotogrande as each game is announced on the vintage signs that dot the tree-lined avenues of this"},"children":[]}]}]},"summary({\"maxCharCount\":160})":{"type":"json","json":[{"name":"paragraph","children":[{"name":"text","attributes":{"value":"There is no excuse for missing a polo match in Sotogrande as each game is announced on the vintage signs that dot the tree-lined avenues of this grand private"},"children":[]}]}]},"summary({\"maxCharCount\":175})":{"type":"json","json":[{"name":"paragraph","children":[{"name":"text","attributes":{"value":"There is no excuse for missing a polo match in Sotogrande as each game is announced on the vintage signs that dot the tree-lined avenues of this grand private estate on"},"children":[]}]}]},"summary({\"maxCharCount\":225})":{"type":"json","json":[{"name":"paragraph","children":[{"name":"text","attributes":{"value":"There is no excuse for missing a polo match in Sotogrande as each game is announced on the vintage signs that dot the tree-lined avenues of this grand private estate on Spain’s Cadiz coast."},"children":[]}]},{"name":"paragraph","children":[{"name":"text","attributes":{"value":"Matches are family affairs It’s just one of Mallorca’s many delicacies and it’s served at a new five-star hotel that has opened in Santanyi in the southeast of the island Thanks to its peaceful lifestyle and picturesque surroundings And the arrival of Can Ferrereta means that the town is now a serious player in the luxury holiday market An ornate stone pathway leads you through the entrance; it was originally a passage for horses and other animals past an iron sculpture by the Catalan artist Josep Riera i Aragó that resembles an aeroplane propeller The hotel’s Ocre restaurantARTURO+LAURENArt is a theme: the hotel is bursting with works and there’s even an original Miró in my bedroom The grandeur of the building is complemented by friendly by which time its ownership was divided across several family members The nearby Es Pontas sea archALAMYHaving fallen into disuse for several decades while the pool’s showers are in a recreated barraca de roter “We wanted to keep that chiaroscuro feeling when you walk around.” One of Can Ferrereta’s junior suitesMallorca’s southern towns mahones cheese and purple safarnaria carrots Wit has furnished the interior with items by international and home-grown brands where you can see wild olive forests and wetlands Cala LlombardsGETTY IMAGESYou are likely to hear more German spoken here than Spanish or Mallorqui serving seasonal Mediterranean dishes such as llengua amb taperes (beef tongue with capers) and frit mallorqui (the island’s traditional stew Laudat — a charming spot for lunch or dinner with a romantic patio filled with lemon trees Laudat works with the local winery Armero i Adrover to produce a range of bespoke house wines — I try the white Judit and her team serve tapas and decadent deserts The market at SantanyiALAMYSantanyi particularly comes to life on Wednesdays and Saturdays The bakery Panaderia Lozano tempts with savoury panades stuffed with meat as well as traditional pastries and cakes such as lazos (twists of pastry with cream or chocolate) custard-filled eclairs) and ensaimadas (circular doughy treats) You’ll do well for ceramic and handicraft gifts too scheduled to open this summer as a place to eat and shop; local artisans will also run workshops on pottery and weaving At dusk an enchanting luminosity envelops Santanyi as the sun begins to set and everything glows And I have the bonus of that sausage breakfast at Can Ferrereta to look forward to Agnish Ray was a guest of Can Ferrereta. B&B doubles from £272 (hotelcanferrereta.com) International travel restrictions are in place. Check gov.uk for more information Follow Times Travel on Instagram and Twitter and sign up for our weekly Travel newsletter for all the latest articles expert advice and inspiration for your next trip The Local Europe ABVästmannagatan 43113 25 StockholmSweden Barcelona recently announced that it will ban smoking on all of its 10 city beaches from July this year This means there will be a total of five kilometres of smoke-free sand in Spain's second-largest city Barcelona decided to ban smoking on four of its main beaches between May 29th and September 12th as a trial run and this year has extended the ban all year round to all its beaches while many others have taken to social media to express their anger at the rule As well as being horrible to find between your toes when sunbathing or when your kids are building a sandcastle cigarette butts are harmful to the environment and marine life A discarded cigarette butt is made of over 97 percent cellulose acetate and contains 4,000+ chemical toxins discarded cigarette butts are just half the issue which on Spain's crowded beaches can affect the health and well-being of many others around Barcelona is of course not the only Spanish city to have banned smoking on its public beaches We take a look at which other beaches across the country have put a stop to it many of Catalonia's beaches have banned smoking Catalonia became the first region to designate a 'smoke-free' beach when the town of L’Escala introduced the rule back in 2006 it has been extended to a total of 19 beaches in the region The region of Galicia has the most smoke-free beaches in Spain with a whopping 187 ocean and river beaches imposing the ban These include 70 beaches in the province of A Coruña Some of the most popular and well-known beaches that are free from tobacco include Santa Cristina in Oleiros Asturias designated smoke-free beaches for the first time in 2019 and now has 14 smoke-free beaches The list currently includes Playa de Misiego El Puntal y Miami in Villaviciosa and Playa de Los Quebrantos in Soto del Barco Please log in here to leave a comment Marina Fabic and Faye Mallia are organising a holiday with a difference where participants can learn the secrets of Spanish gastronomy while trying their hand at preparing traditional recipes What better place to indulge in a culinary vacation than Catalonia are organising a unique foodie visit to Spain – including cheese tastings and vineyard visits as well as fun cooking classes with talented chefs and while enjoying the architecture of Barcelona and Costa Brava seaside Participants will be able to discover the exquisite and typical dishes of the area the famous miniature canapés known as pintxos some of the best wines in the world and an avant-garde cuisine the group will prepare regional cuisine recipes such as the paella catalan and visit traditional markets and places to enjoy genuine Spanish gastronomy The group will be hosted at a seaside villa perched in the coastal town of Roses many restaurants and the fishing port that sells its fresh catches of fish daily The villa offers the perfect location for a pleasant coastal walk while a two-minute stroll from the house leads to Almadrava sandy cove and onto the rugged coast on a path to Canyelles Petites beach and further on to the larger town and beaches of Roses Food at the villa will be in the hand of a local chef who will focus on Mediterranean cuisine – foodies will also be able to enjoy several Michelin star restaurants lying in the middle of the gastronomic belt of Spain and touted by foodies as one of the best restaurant in the world bars and terraces all offer splendid panoramic views and the cuisine of Girona cold roast vegetables and the xató (escarola lettuce with anchovies and cod) the group will prepare regional cuisine recipes such as the paella catalan and visit traditional markets and places to enjoy genuine Spanish gastronomy The combination of mountain and sea also reaches the kitchen in the form of chicken with spiny lobster or rabbit with snails stews and rice dishes are other tasty recipes the crema catalana (a kind of custard with caramelised sugar) and fresh cheese with honey (mel i mató) are outstanding The best wines for this menu belong to the Ampurdán-Costa Brava Denomination of Origin Wine lovers will enjoy many cooperatives and vineyards in the area The Mediterranean character of Roses is reflected in the products of the land In Roses begins the Wine Route DO Empordà This constitutes the main focus of winemaking in the Empordà providing an essential yardstick with which to discover and understand DO Empordà wineries while exploring the zone with the highest density of vineyards and wineries that may be visited Roses’ fishermen cooked suquet de peix a simple dish of freshly-caught fish boiled with potatoes this recipe has experienced an evolution and has been enriched with the incorporation of typically Mediterranean products The holiday will also help the group become acquainted with some of the different regions in Spain through its most popular appetisers desserts and main courses – the world-famous tapas paella from Valencia and Andalusian gazpacho cakes and pastries from Galicia and others a good part of the province of Girona as well as Cadaqués or Port de la Selva can be toured Empuries preserves important Greek remains while at Figueres the Dalí Theatre-Museum offers tribute to the master of surrealism declared a historic-artistic site and Girona with its walled town known as La Força Vella are some of the many other possibilities offered by this Catalan region There will also be visits to traditional Catalan markets attractive cities and natural environments And of course you’ll enjoy the dishes you yourself have cooked along with other typical delicacies from Spain’s gastronomic culture For more information send an e-mail to Creative Holidays Malta on info@creativeholidaysmalta.com please register for free or log in to your account.