Researchers have suspected for some time that the link between our gut and brain plays a role in the development of Parkinson's disease
"Supplementation of riboflavin and/or biotin is likely to be beneficial in a subset of Parkinson's disease patients, in which gut dysbiosis plays pivotal roles," Nagoya University medical researcher Hiroshi Nishiwaki and colleagues wrote in their paper published in May 2024
The neurodegenerative disease impacts almost 10 million people globally, who at best can hope for therapies that slow and alleviate symptoms
Symptoms typically begin with constipation and sleep problems
up to 20 years before progressing into dementia and the debilitating loss of muscle control
Previous research found people with Parkinson's disease also experience changes in their microbiome long before other signs appear
Analyzing fecal samples from 94 patients with Parkinson's disease and 73 relatively healthy controls in Japan
Nishiwaki and team compared their results with data from China
While different groups of bacteria were involved in the different countries examined
they all influenced pathways that synthesize B vitamins in the body
The researchers found the changes in gut bacteria communities were associated with a decrease in riboflavin and biotin in people with Parkinson's disease
Nishiwaki and colleagues then showed the lack of B vitamins was linked to a decrease in short-chain fatty acids (SCFAs) and polyamines: molecules that help create a healthy mucus layer in the intestines
"Deficiencies in polyamines and SCFAs could lead to thinning of the intestinal mucus layer, increasing intestinal permeability, both of which have been observed in Parkinson's disease," Nishiwaki explains
They suspect the weakened protective layer exposes the intestinal nervous system to more of the toxins we now encounter more regularly. These include cleaning chemicals, pesticides
Such toxins lead to the overproduction of α-synuclein fibrils – molecules known to amass in dopamine-producing cells in the substantia nigra part of our brains
eventually leading to the more debilitating motor and dementia symptoms of Parkinson's
A 2003 study found high doses of riboflavin can assist in recovering some motor functions in patients who also eliminated red meat from their diets
So it's possible that high doses of vitamin B may prevent some of the damage
This all suggests ensuring patients have healthy gut microbiomes may also prove protective, as would reducing the toxic pollutants in our environment
with such a complicated chain of events involved in Parkinson's disease
not all patients likely experience the same causes
so each individual would need to be assessed
"We could perform gut microbiota analysis on patients or conduct fecal metabolite analysis," explains Nishiwak
we could identify individuals with specific deficiencies and administer oral riboflavin and biotin supplements to those with decreased levels
potentially creating an effective treatment."
This research was published in npj Parkinson's Disease
An earlier version of this article was published in June 2024
Metrics details
We aimed to identify gut microbial features in Parkinson’s disease (PD) across countries by meta-analyzing our fecal shotgun sequencing dataset of 94 PD patients and 73 controls in Japan with five previously reported datasets from USA
GC-MS and LC-MS/MS assays were established to quantify fecal short-chain fatty acids (SCFAs) and fecal polyamines
α-Diversity was increased in PD across six datasets
Taxonomic analysis showed that species Akkermansia muciniphila was increased in PD
while species Roseburia intestinalis and Faecalibacterium prausnitzii were decreased in PD
Pathway analysis showed that genes in the biosyntheses of riboflavin and biotin were markedly decreased in PD after adjusting for confounding factors
Five out of six categories in carbohydrate-active enzymes (CAZymes) were decreased in PD
Metabolomic analysis of our fecal samples revealed that fecal SCFAs and polyamines were significantly decreased in PD
Genes in the riboflavin and biotin biosyntheses were positively correlated with the fecal concentrations of SCFAs and polyamines
Bacteria that accounted for the decreased riboflavin biosynthesis in Japan
and Germany were different from those in China1
different bacteria accounted for decreased biotin biosynthesis in the two country groups
We postulate that decreased SCFAs and polyamines reduce the intestinal mucus layer
which subsequently facilitates the formation of abnormal α-synuclein fibrils in the intestinal neural plexus in PD
implying that ~50% of PD patients may follow this hypothesis
Marked difference in gut microbiota across countries makes it difficult to identify causally associated intestinal bacteria and bacterial genes in PD patients
We here performed shotgun-seq of fecal samples of 94 PD patients and 73 controls
and meta-analyzed our dataset with five previously reported datasets to identify bacterial taxa
and pathways that were specifically changed in PD across countries
Decreased genes in fecal riboflavin and biotin biosyntheses were positively correlated with the decreased fecal SCFAs and polyamines
different bacterial species were responsible for the decreased genes in fecal riboflavin and biotin biosyntheses in different countries
a Left panel: PCoA plot of bacterial species in PD and controls in six countries with Bray–Curtis dissimilarity
Circles and triangles indicate controls and PD
Right panel: PCoA plot showing the center of gravity and the standard error of the overall compositions of bacterial species in six datasets in PD and controls with Bray–Curtis dissimilarity
b Forest plot of α-diversities of bacterial species in six datasets
FEM and REM represent fixed and random effect models
The square sizes represent the number of samples
Diamonds represent the mean and 95% confidence interval
P-values of FEM and REM and I2 are indicated
c The cumulative frequency plots of the relative abundance at the species level in six datasets
The number of identified bacterial species in controls and PD in each dataset is indicated by a small circle at the end of the curve
Orange and blue symbols represent increased and decreased CAZymes in PD
Violin plots of (a) short-chain fatty acids
and (d) polyamines in feces in controls and PD
Concentrations are indicated by mg per g of freeze-dried fecal sample (mg/g FD)
Median and interquartile range are indicated
The sample sizes were 92 (PD) and 72 (controls) for acetate
91 (PD) and 70 (controls) for lactate and succinate
and 86 (PD) and 66 (controls) for polyamines
P-values were calculated by the Wilcoxon rank sum test
Enzymes are indicated by EC numbers in squares
Metabolites are indicated in green letters and open circles
KEGG pathways are indicated by round squares
Arrows indicate decreased or increased in PD
Significant and non-significant changes are indicated by thick and thin arrows
Forest plots of six datasets are indicated for the four significantly changed enzymes
A right upper heatmap indicates the Spearman’s rank correlation coefficients between the four significantly changed enzymes and fecal SCFAs/polyamines
a Heatmap showing the difference of the fractional CPMs between PD and controls of five most influential bacteria in each dataset
b Forest plots of Faecalibacterium prausnitzii and Phocaeicola vulgatus in six datasets
Supplementation of riboflavin to compensate for decreased riboflavin production by gut microbiota may be beneficial in PD patients
concentrations of fecal polyamines may not be simply represented in plasma polyamines
it is interesting to note that decreased spermine is a shared feature between plasma and feces in PD
decreased riboflavin may lead to decreased polyamines through decreased vitamin B6
biotin may affect the SCFA and polyamine biosyntheses by serving as an essential cofactor
biotin-dependent enzymes have not been extensively analyzed to date
and we do not know which enzyme(s) become defective in the absence of biotin
our analysis showed that the decreases of distinct sets of bacteria in PD in different countries led to a decrease of an identical pathway
which poses another burden in the meta-analysis and the systematic review of gut microbiota at the genus and species levels
these pathways were either up- or down-regulated without any statistical significance
Solid arrows indicate the associations observed in the current study
Broken arrows indicate speculations based on previous reports
The sizes of the bacterial symbols represent the effects on biotin and riboflavin biosynthesis
in which gut dysbiosis plays pivotal roles in PD
We recruited 94 patients with idiopathic PD and their 73 healthy spouses who lived together from September 2015 to February 2018
Each PD patient was diagnosed according to the Movement Disorder Society’s (MDS) PD criteria
We also excluded subjects who claimed to have taken antibiotics in the last four weeks
The protocol was partially modified to use Lysing Matrix E Beads (MP Biomedicals
USA) with FastPrep-24 5G (MP Biomedicals) for three cycles at 6.0 m/s for 60 s instead of vortex mixing
Sequencing libraries were generated using NEBNext Ultra DNA Library Prep Kit for Illumina (NEB
USA) according to manufacturer’s protocols
and index codes were added to attribute sequencing fragments to each sample
The library quality was assessed using TapeStation (Agilent
Metagenomic sequencing was conducted using the HiSeq 2500 sequencing platform
HiSeq Rapid SBS Kit v2 and HiSeq PE Rapid Cluster Kit v2 (Illumina
USA) to obtain 3 Gbp per sample by 2 × 150 bp paired end-reads
The total numbers of subjects including our own dataset were 813 PD patients and 558 controls
The average read counts per sample ranged from about nine to sixty million reads
The number of mapped reads per contig was normalized to CPM
because a single EC number 2.1.1.43 constituted 25% or more of total CPM in 96 out of 156 samples (61.5%)
the disease state (PD or control) was set to a covariate and the differences in bacterial abundances across datasets were set to batch effects
PCoA was plotted with the function of vegdist in vegan (version 2.6-4) on R 4.2.3 using Bray–Curtis dissimilarity as a distance measurement and with the function of cmdscale in stats (version 3.6.2) on R 4.2.3
PERMANOVA was performed with the function of adonis2 in vegan (version 2.6-4) on R 4.2.3
a taxon or a CAZyme was considered to be significant when false-discovery rate (q-value) by Benjamini–Hochberg method for both FEM and REM was less than 0.05
that were significantly different between controls and PD in meta-analysis
The difference between the USA and Japan was set to a random effect in the MaAsLin2 analysis
The total number of samples analyzed with MaAsLin2 was 851 due to lack of the metadata
P-values between controls and PD were normalized by the Benjamini–Hochberg method for each analysis of 73 EC numbers
Statistical significance was set to q-value < 0.05
p-value of each pathway in each dataset was first calculated by GSEA
An integrated p-value was then calculated for each pathway
In the analysis of a KEGG pathway that was decreased in PD
actual p-value was used when the pathway was decreased in PD in a dataset
but p-value was set to 1.00 when the pathway was increased in PD in a dataset
In the analysis of a KEGG pathway that was increased in PD
a similar rule was applied in an opposite way
A significance threshold of q-value by Benjamini–Hochberg method was set to 0.05
We previously established a GC-MS-based method to quantify fecal SCFA levels22
20 mg of FD feces was mixed with 1000 µL of 5 mmol/L NaOH and 300 µL of H2O
The mixture was shaken vigorously with zirconia beads for 10 min and centrifuged at 13,200 × g for 20 min at 4°C
The supernatant (333 µL) was mixed with 200 µL of H2O
50 µL hexanoic-6,6,6-d3 acid solution (internal standard)
The resulting solution was then mixed for 1 min
and centrifuged at 1900 × g for 5 min at room temperature
Quantitative analysis was performed using an Agilent 7890A GC equipped with an Agilent 5975 inert mass spectrometer (Agilent Technologies)
The precisions for all SCFA quantifications were less than 8.4% relative standard deviation (RSD)
20 mg of FD feces was mixed with 400 μL of H2O
10 μL of sulfosalicylic acid solution (1 mg/μL)
and an internal standard solution (hexanoic-6,6,6-d3 acid)
The mixture was shaken vigorously with zirconia beads for 10 min and centrifuged at 13,200 × g for 20 min at 4 °C
The supernatant was then mixed with 20 μL of 6 mol/L HCl and 2 ml μL of diethyl ether
and the upper layer was transferred into a new glass test tube
The sample was dried by nitrogen gas at 40 °C
The residue was dissolved in 300 μL diethyl ether
After adding 20 μL N-tert-butyldimethylsilyl imidazole
the derivatization reaction was performed at 60 °C for 30 min
the solution was analyzed using GC-MS as described above
The precisions for quantifications of lactate and succinate were less than 16% RSD and 2% RSD
after derivatization using N-(9-fluorenylmeth-oxycarbonyloxy) succinimide
which was composed of an Agilent 1200 infinity LC coupled with an Agilent 6430 Triple Quadrupole LC/MS System (Agilent Technologies)
1,6-diaminohexane was used as an internal standard
The precisions for all polyamine quantifications were less than 4.9% RSD
In order to examine the bacterial origins of nine significantly decreased EC numbers in “riboflavin metabolism” and “biotin metabolism”
we calculated a fractional CPM contributed by each bacterium for each EC number
the median of fractional CPMs in controls was subtracted from the median of fractional CPMs in PD to calculate ΔfCPM
We assumed that a bacterium with the most negative ΔfCPM mostly accounted for the decreased EC number in a specific dataset
the averaged ΔfCPMs were sorted in ascending order and the top five bacteria were selected
Relative abundances of intestinal bacteria were analyzed by the Wilcoxon rank sum test for unmatched pairs with the mannwhitneyu functionality of scipy.stat on Python 3.11.2
the significance threshold for p-value after Bonferroni correction was set to less than 0.05 for both FEM and REM and the significance threshold of I2 was set to less than 40%
the significance threshold for q-value by Benjamini–Hochberg method was set to less than 0.05 for both FEM and REM
the significance threshold for q-values by Benjamini–Hochberg method was set to less than 0.05
Sequence data of our dataset are available at the DNA Data Bank of Japan (DDBJ) under the accession number of DRA016410
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Idiopathic Parkinson’s disease: possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen
Vagotomy and subsequent risk of Parkinson’s disease
Intestinal Dysbiosis and Lowered Serum Lipopolysaccharide-Binding Protein in Parkinson’s Disease
Progression of Parkinson’s disease is associated with gut dysbiosis: Two-year follow-up study
Short chain fatty acids and gut microbiota differ between patients with Parkinson’s disease and age-matched controls
Meta-Analysis of Gut Dysbiosis in Parkinson’s Disease
Short chain fatty acids-producing and mucin-degrading intestinal bacteria predict the progression of early Parkinson’s disease
Gut microbiota are related to Parkinson’s disease and clinical phenotype
Gut microbiota in Parkinson’s disease: Temporal stability and relations to disease progression
Functional implications of microbial and viral gut metagenome changes in early stage L-DOPA-naive Parkinson’s disease patients
Gut metagenomics-derived genes as potential biomarkers of Parkinson’s disease
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Association of Fecal and Plasma Levels of Short-Chain Fatty Acids With Gut Microbiota and Clinical Severity in Patients With Parkinson Disease
Oral and gut dysbiosis leads to functional alterations in Parkinson’s disease
Metagenomics of Parkinson’s disease implicates the gut microbiome in multiple disease mechanisms
Integrated Multi-Cohort Analysis of the Parkinson’s Disease Gut Metagenome
Metagenomics of the Gut Microbiome in Parkinson’s Disease: Prodromal Changes
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Multivariable association discovery in population-scale meta-omics studies
Freeze-drying enables homogeneous and stable sample preparation for determination of fecal short-chain fatty acids
Ueyama, J. et al. Effects of Pesticide Intake on Gut Microbiota and Metabolites in Healthy Adults. Int. J. Environ. Res. Public Health 20, https://doi.org/10.3390/ijerph20010213 (2022)
The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of Pathway/Genome Databases
Gut microbiome alpha-diversity is not a marker of Parkinson’s disease and multiple sclerosis
A predictive index for health status using species-level gut microbiome profiling
Riboflavin Has Neuroprotective Potential: Focus on Parkinson’s Disease and Migraine
High doses of riboflavin and the elimination of dietary red meat promote the recovery of some motor functions in Parkinson’s disease patients
Riboflavin Supplementation in Patients with Crohn’s Disease [the RISE-UP study]
Regulation of immunological and inflammatory functions by biotin
High doses of biotin in chronic progressive multiple sclerosis: a pilot study
Targeting demyelination and virtual hypoxia with high-dose biotin as a treatment for progressive multiple sclerosis
A metabolic profile of polyamines in parkinson disease: A promising biomarker
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A New Mechanism of Biological Energy Coupling
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Riboflavin Bioenriched Soymilk Alleviates Oxidative Stress Mediated Liver Injury
and Gut Microbiota Modification in B(2) Depletion-Repletion Mice
Riboflavin Supplementation Promotes Butyrate Production in the Absence of Gross Compositional Changes in the Gut Microbiota
Two interconnected B vitamins: riboflavin and pyridoxine
Riboflavin Is an Important Determinant of Vitamin B-6 Status in Healthy Adults
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and Tomomi Yamada at the Nagoya University Graduate School of Medicine for their technical assistance
We also acknowledge Division for Medical Research Engineering
Nagoya University Graduate School of Medicine for their technical support on shotgun metagenomic analysis
and Yusuke Okuno at the Nagoya City University Graduate School of Medicinal Sciences
This study was supported by Grants-in-Aid from the Japan Society for the Promotion of Science (JP22K17343 to H.N.
JP23H02794 to K.O.); the Ministry of Health
Labour and Welfare of Japan (23FC1014 to K.O.); the Japan Agency for Medical Research and Development (JP22ek0109488 to K.O.)
and the National Center of Neurology and Psychiatry (5-6 to K.O.)
Center for Neurological Diseases and Cancer
Nagoya University Graduate School of Medicine
Department of Pathophysiological Laboratory Sciences
Chubu University College of Life and Health Sciences
HN performed bioinformatic analyses with the help of H.M
All authors critically revised and approved the manuscript
The authors declare no competing interests
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations
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It was April 23, 2011, a balmy and beautiful Petaluma spring day with temperatures in the mid-60’s, and Marcelo Aguero was competing in a tennis match at the Petaluma Valley Athletic Club, according to an account in the Petaluma Argus-Courier (https://www.petaluma360.com/article/news/grateful-cardiac-patient-thanks-for-saving-my-life/) As fate would have it
Aguero collapsed in the middle of the match
Aguero told the Petaluma Argus-Courier.
Aguero recovered and was out of the hospital by May 3
This week he was introduced as the new President and CEO of wine and spirits importer and supplier Kobrand Wine & Spirits
Aguero’s first day on the job will be September 9
Aguero takes over for the retiring President and CEO Robert T
who will be on the Management Committee of Kopf Family Enterprises
the umbrella organization that includes Kobrand.
DeRoose and representatives from Jackson Family Wines and Kobrand for comment were unsuccessful.
a 52 year-old graduate of the University of Washington
comes to Kobrand with over 30 years of experience in the wine industry
including the last 20 years with Jackson Family Wines
rising to Executive Vice President for Marketing and Direct to Consumer Sales before taking the top job at Kobrand
He also held leadership positions as the Senior Vice President and General Manager at Santa Rosa
the distributor owned by Jackson Family Wines
Aguero was first hired by Jackson Family Wines in 2002 as its Northwest Regional Manager.
Aguero served as the Executive Sponsor for the Diversity
and Inclusion program at Jackson Family Wines
The Seattle native born to parents from Buenos Aires
Argentina regularly speaks on issues of diversity
including as recently as this year’s Unified Wine & Grape Symposium
He becomes the first person of color to lead Kobrand in the company’s 80-year history.
It is with a figurative big heart that Aguero has pursued a career as a wine industry executive
“The one thing that I appreciate about Marcelo is that he's a no-nonsense guy,” said Eric Mummert
who worked with Aguero at Regal Wine Company from 2012-15 and recently left a position at Southern Glazer’s Wine & Spirits
The worst bosses are the ones that don't have a sense of humor or who have a big ego
that colors one's sense of purpose and how one deals with people.
He would be someone who I would work for again if he called me.”
Mummert expects Aguero will thrive in his new job immediately.
“Every good CEO should work in every different department to understand what is required to run a company and he's done all of that,” Mummer said
“I can't imagine of a better candidate for the job
He has the management skills.”
The career promotions and the latest job almost didn’t happen for the ambitious Aguero if the quick-thinking Giacomini hadn’t administered CPR immediately on the tennis court in 2011
Giacomini’s wife fetched a portable automated external defibrillator from the club
Aguero’s doctor said that starting the defibrillator was key and preserved all his brain function
is playing tennis again and thriving professionally.
DeRoose retires after 41 years with Kobrand
including the last 15 as its President and CEO
He came up through the Kobrand ranks and saw the company through international and domestic economic trauma.
“When we think of the cycles we have gone through
other cycles that were tough in the industry that required flexibility and execution to get through those tough times
Bob led Kobrand through those tough times,” said Dennis Cakebread co-owner and Chairman of the Board of the eponymous Cakebread Cellars
What I would observe is that it is so unusual in the alcohol distribution businesses to have a relationship that long
We've had a great relationship with Bob and Bob’s predecessors
We go back to when he was the Estates Group manager and district manager
I thought it was a good choice when they made him President
he's continued to do the same thing and remained data focused.”
Kopf with headquarters in New York City’s Empire State Building
Kobrand was bequeath to his three daughters
The company is now headquartered in Purchase
less than three miles from the Connecticut border.
The Kobrand portfolio currently holds over 80 brands and producers of wine
Producers include France’s Louis Jadot
Italy’s Tenuta San Guido (producers of Sassicaia)
Domaine Carneros and Mullan Road Cellars.
The Kobrand Portfolio is distributed by Republic National Distributing Company in 38 states.
“If you look at the portfolio and the brands they represent
that speaks to a lot of things and it also speaks for their ability to work with so many different cultures,” Cakebread said
“We are proud to be part of their portfolio.”
10 minutes by taxi from Nishiwakishi Station on the JR Kakogawa line
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Researchers have suspected for some time that the link between our gut and brain plays a role in the development of Parkinson's disease
"Supplementation of riboflavin and/or biotin is likely to be beneficial in a subset of Parkinson's disease patients, in which gut dysbiosis plays pivotal roles," Nagoya University medical researcher Hiroshi Nishiwaki and colleagues write in their published paper
While different groups of bacteria were involved in the different countries examined, they all influenced pathways that synthesize B vitamins in the body. The researchers found the changes in gut bacteria communities were associated with a decrease in riboflavin and biotin in people with Parkinson's disease
BAUM made its debut as a global skin beauty brand in the prestige category
It focuses on the “power of trees” that have been harmonizing with the changing environment since ancient times
while promoting the initiatives to solve social issues and reduce environmental impact under the Shiseido’s philosophy “BEAUTY INNOVATIONS FOR A BETTER WORLD.” Three years after its conceptualization
it was launched as a skin & mind care brand under the theme of “coexistence with trees.” What are the thoughts of the project team that endeavored to balance a sustainability mindset and the beauty business and then tackled the new unconventional challenge of using wood for cosmetics packaging to embody the theme
We talked with three members: Ayami Nishiwaki
Motoki Okoshi responsible for the outer packaging design at Global Innovation Center
―Could you talk about the background of launching BAUM
As symbolized in the phrase “itadakimasu (thank you for the meal or offering),” maintaining a sense of awe and gratitude towards nature and living by efficiently circulating the limited resources in this island nation are deeply engrained elements of Japanese culture
We started brand value development with that stance
we ultimately decided to use the idea of ”coexistence with trees.” Trees are familiar materials for Japanese culture and symbolize the circulation of resources
We think them the best motif to represent what a prestige brand should look like in the coming age
―I heard that your team focused on “a sense of familiarity upon use” as the consumers’ motive for selecting products while being aware of sustainability
―BAUM has been realized through solid building of the brand story that “consumers’ rich experience is organically connected with the context of being sustainable.” Am I right
―What kind of experience is the “skin & mind care” that BAUM touts
―Could you talk about the package design next
How did you incorporate the themes like “sustainability” and “trees”
―You use upcycled wood from Karimoku Furniture for packaging
―There aren’t many cases of using wood for cosmetics packaging
―Had refill design been planned from the beginning as a means to create a sustainable brand
―What were the difficulties in producing actual packages
How did you feel about the reactions of customers and society in general
―It was the passion of all the members that realized this unprecedented project through repeated trial and error
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Those high-risk stunts apparently performed by Lucy Liu were really done by Michiko Nishiwaki
She has been a stunt double for some big names in Hollywood as well as a fight choreographer
After just missing being cast in Mortal Kombat
Michiko decided to add stuntwoman to her resume
She performed all the high-risk stunts in Kill Bill: Vol
so in Japan being a woman in a muscle competition was positively a revolution
Michiko Nishiwaki was able to find a gym and began training with weights in a quest to balance out her proportions and symmetry
Michiko became the first female bodybuilding and powerlifting champion in Japan and held these titles for three consecutive years
She opened three fitness clubs with her brother to capitalize on her competition success
Being known as an expert in strength training
she also did executive personal training and made connections with the elite of Japan
Michiko forever changed the stereotype of the submissive and docile Japanese woman by becoming a strong role model for all
Michiko’s acting career began in 1985 in Hong Kong
Her first leading role was in the film My Lucky Stars
Her performance caught the attention of Jackie Chan and Sammo Hung and soon she appeared with many of the best-known martial arts stars
Michiko appeared in dozens of these genre films and then
she had no problem learning to portray a martial arts expert on film
which also included learning weapons training
Michiko realized she could make use of her own gymnastic training like Jackie Chan
whose background helped him develop a unique
She eventually found herself in demand doing stunts as well as appearing as an actress and was quickly typecast
playing villains in most of her Hong Kong films
Michiko was brought to my attention by movie director Oliver Stone
I scheduled a shoot with her in my studio for the Weider magazines
Michiko is so popular around the world that I have seen my photos of her published all over the internet on sites devoted to martial arts
She was not only a pioneer in the world of muscle & physique but an admirable role model in how she was able to capitalize on her athletic success and develop a career in movies
Michiko Nishiwaki married and subsequently moved to Moorpark
Having Michiko living close to Los Angeles gave me the chance to bring her to my studio to do photos for Muscle & Fitness
I consider the images I created with her to be a significant addition to my photo archives
and I’m happy to share them with magazine readers of the current era
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Metrics details
which functions as a t-SNARE component of the syntaxin18 complex
is localized on the ER membrane and regulates retrograde transport from Golgi to the ER
which generally releases pro-apoptotic proteins from Bcl2-mediated inhibition
Previously we reported that retinal photoreceptors undergo BNip1-dependent apoptosis in zebrafish β-snap1 mutants
we investigated physiological roles of BNip1-dependent photoreceptor apoptosis
we examined the spatio-temporal profile of photoreceptor apoptosis in β-snap1 mutants
and found that apoptosis occurs only during a small developmental window
in which an apical photoreceptive membrane structure
Transient expression of β-SNAP1 during this OS growing period prevents photoreceptor apoptosis in β-snap1 mutants
enabling cone to survive until at least 21 dpf
These observations suggest that BNip1-mediated apoptosis is linked to excessive activation of vesicular transport associated with rapid growth of the OS
which inhibits protein transport to the OS
rescued photoreceptor apoptosis in β-snap1 mutants
which inhibits protein synthesis via the mTOR pathway
also rescued photoreceptor apoptosis in β-snap1 mutants
These data suggest that BNip1 performs risk assessment to detect excessive vesicular transport in photoreceptors
These genes encode proteins with great functional diversity
scaffolding of the apical photoreceptive membrane organelle known as the outer segment (OS)
and transport of proteins to the OS through the connecting cilium
it remains to be seen how dysfunction of these proteins triggers photoreceptor cell death
After fusion of retrogradely transported vesicles on the ER membrane
the syntaxin-18 cis-SNARE complex is generated
This complex is normally disassembled by SNAP and NSF
the syntaxin-18 cis-SNARE complex fails to be disassembled for lack of β-SNAP activity
A possible mechanism underlying BNip1-dependent apoptosis is that BNip1 pro-apoptotic activity is suppressed by intramolecular binding of the N-terminal coiled-coil domain to the BH3 domain in the monomeric state; however
when BNip1 forms the syntaxin-18 cis-SNARE complex
BNip1 monitors reduction of β-SNAP activity and activates apoptosis when β-SNAP activity is decreased
rescued photoreceptor apoptosis in coa mutants
These data suggest that BNip1 performs risk assessment that detects excessive activation of vesicular transport in photoreceptors
Bcl2-ER significantly rescues photoreceptor apoptosis in coa mutants
EGFP-tagged Bcl2-ER was generated by replacement of the Bcl2 TM domain with a BNip1 TM domain
(B) Retinas injected with mRNA encoding ER-mKO (magenta) and either mRNA encoding EGFP-tagged Bcl2
Fluorescent images shown in squares of upper panels
and their green and magenta channels (middle panels)
Bottom histograms indicate spatial profiles of EGFP and mKO signals along the line shown in the middle panels
the spatial profile of EGFP-tagged Bcl2-ER signals correlates with that of ER-mKO signals
whereas EGFP-tagged Bcl2 signals are not correlated
(C) Retinas injected with mRNA encoding MT-mKO (magenta) and either mRNA encoding EGFP-tagged Bcl2
peaks of EGFP-tagged Bcl2-ER signals do not match those of MT-mKO signals
whereas EGFP-tagged Bcl2 signals are broader than MT-mKO signals
(D) Retinas of wild-type and coa mutant embryos combined with transgenic lines Tg[hs:mCherry-tagged Bcl2] or Tg[hs:mCherry-tagged Bcl2-ER]
Tg+ and Tg− indicate transgenic and non-transgenic embryos
Green color indicates zpr1 antibody signals
INL and photoreceptor cell layer (PCL) are shown
Right two columns indicate higher magnification of the PCL shown in the left two columns
The interface between pigmented epithelium (PE) and the neural retina is shown as a white
Arrowheads indicate rescued photoreceptors
Scale: 50 μm (left two columns) and 10 μm (right two columns)
(E) Percentage of zpr1-positive area relative to total retinal area
increase the zpr1-positive fraction in coa mutants
Bcl2-ER effectively rescues photoreceptor apoptosis in coa mutants
Two-way ANOVA with the Tukey multiple comparison test
apoptotic activity of BNip1 is activated on the ER membrane and overexpression of Bcl2 on the ER membrane effectively suppresses its apoptotic activity
suggesting that Bcl2-ER is specifically located on the ER membrane
These observations support the current model that lack of β-SNAP activity causes accumulation of the syntaxin-18 cis-SNARE complex
which facilitates the interaction between the BNip1 BH3 domain and Bcl2 on the ER membrane in coa mutant photoreceptors
Apoptosis occurs during OS growth stages from 60 to 96 hpf
(A) Whole mount retinas of zebrafish transgenic embryos
labelled with anti-red opsin antibody (magenta)
Green and magenta colors indicate rod and cone photoreceptor OSs
The OS appears at 60 hpf and progressively increases in size until 96 hpf
(B) Whole mount retinas of zebrafish transgenic embryos
labelled with zpr1 antibody (green) and TUNEL (magenta)
Upper and lower panels indicate wild-type and the coa mutant genetic background
a few TUNEL-positive cells were observed at each stage
spread to the entire retina by 84 hpf and disappear by 96 hpf
The lack of zpr1 and XP-GFP signals in coa mutants at 96 hpf suggest that almost all photoreceptors are eliminated by 96 hpf
almost all photoreceptors undergo apoptosis from 60 to 96 hpf
(C) Sectioned images of the photoreceptor cell layer labelled with anti-green opsin antibody (green) at 3
(D) Green cone OS size measured using section images shown in (C)
The green cone OS increases linearly from 3 to 5 dpf
One-way ANOVA with the Tukey multiple comparison test
(E) Sectioned images of the photoreceptor cell layer labelled with fluorescent signals of Tg[XlaRho:XP-GFP] (green) at 3.5
The cone photoreceptor cell layer is counterstained with zpr1 antibody (blue)
(F) Rod OS size measured using section at 3.5
The rod OS initially increases until 4.5 dpf
is maintained as a plateau from 4.5 to 8.5 dpf
and again starts to grow after 8.5 until 28 dpf
One-way ANOVA with Dunnett’s multiple comparison test
rod and cone apoptosis occur in coa mutants during their initial OS growth from 2 to 4 dpf
β-SNAP1 activity after 48 hpf is required for photoreceptor survival at 84 hpf
(A) Experimental design and results of heat-shock promoter-driven β-SNAP1 overexpression in coa mutants
Zebrafish embryos were injected with a DNA construct that expresses mCherry-tagged β-SNAP1 under control of the heat-shock promoter
Heat-shock treatment of injected embryos was performed at 36
and photoreceptor apoptosis was examined at 84 hpf
Green or grey circles indicate rescue results for cone survival
control embryos and coa mutant embryos injected with a DNA construct encoding hs:mCherry-β-SNAP1 at the one-cell stage and heat-shocked four times at 36/48/60/72 hpf
Cone and rod survival was confirmed by labeling with zpr1 antibody (magenta) and fluorescent signals of Tg[XlaRho:XP-GFP] (green)
Three or four heat-shock treatments effectively
rescued photoreceptor degeneration in coa mutants
(C) Percent zpr1-positive area relative to total retinal area
Blue and red bars indicate wild-type and coa mutant embryos injected with DNA encoding hs:mCherry-β-SNAP1
Cone apoptosis was rescued by heat shock treatment at 36/48/60/72 hpf and 48/60/72 hpf
which shows an equivalent rescue level to wild type
(D) Percent XP-GFP-positive area relative to the total area of the photoreceptor cell layer
Rod apoptosis was rescued by heat shock treatment at 36/48/60/72 hpf and 48/60/72 hpf
Two-way ANOVA with Sidak’s multiple comparison test
β-SNAP1 overexpression from 36 to 132 hpf is enough to maintain cones until 21 dpf but not rods in coa mutants
(A) Experimental design of β-SNAP1 overexpression in coa mutants
Heat treatments were applied at 12-h intervals from 36 to 132 hpf (red arrows)
Green or grey circles indicate rescue results of cone survival and stage of analysis
The blue arrow indicates the critical period for β-SNAP1-dependent cone survival
(B) Retinas of coa; Tg[XlaRho:XP-GFP]; Tg[hs:mCherry-β-SNAP1] embryos or larvae that were heat-shocked from 36 to 132 hpf
Wild-type with Tg[hs:mCherry-β-SNAP1] and coa mutant without Tg[hs:mCherry-β-SNAP1] are positive and negative controls
Cone photoreceptors and rod OS were visualized by labeling with zpr1 antibody (green) and GFP signals from Tg[XlaRho:XP:GFP] (magenta)
In coa mutants with Tg[hs:mCherry-β-SNAP1]
photoreceptors were maintained until 21 dpf
(C) Percentage of zpr1-positive area relative to total retinal area
There was no significant difference in cone survival between wild-type embryos with/without Tg[hs:mCherry-β-SNAP1] and coa mutant embryos with Tg[hs:mCherry-β-SNAP1] at 6
the fraction of surviving cones in coa mutants with Tg[hs:mCherry-β-SNAP1] started to decrease although it was still significantly higher than that of coa mutants
surviving cones markedly decreased in coa mutants with Tg[hs:mCherry-β-SNAP1] in a similar level to coa mutants
(D) Higher magnification of photoreceptor cell layers indicated by squares of panel (B)
The rod OS is increased in wild type during development
the rod OS in coa mutants was similar to that of wild type at 6 dpf
(E) Percentage of XP-GFP-positive area relative to total area of the photoreceptor cell layer
the XP-GFP-positive fraction increases progressively during development
in coa mutant embryos with Tg[hs:mCherry-β-SNAP1]
the fraction is similar to that of wild type at 6 dpf
significantly decreased after 10 dpf and became 0% at 28 dpf
rod degeneration after 6 dpf is consistent with our model that BNip1-dependent photoreceptor apoptosis is linked to the OS growing period
or β-SNAP2 is ectopically expressed in photoreceptors at later stages in coa mutants in compensation for loss of β-SNAP1 and prevents cone photoreceptor apoptosis
cone photoreceptors survive after 6 dpf in the absence of SNAP activity in zebrafish
these data suggest that BNip1-mediated photoreceptor apoptosis is specifically activated during the OS growth period
Photoreceptor apoptosis and neuronal regeneration in coa mutants with overexpression of β-SNAP1 during the OS growth period
(A) TUNEL of wild-type and coa mutant retinas with overexpression of β-SNAP1 during the initial OS growth period
Yellow and red circles indicate TUNEL signals in photoreceptors of central retinas and retinal CMZ
Higher magnification images of all TUNEL signals indicated by white squares are shown in the right side
(B) The number of TUNEL-positive cells per 10,000 μm2 in photoreceptors and CMZs of 21-dpf
wild-type siblings and coa mutants with overexpression of β-SNAP1 during the OS growth period
TUNEL density is slightly increased in rescued coa mutant photoreceptors
but does not differ significantly from that of wild-type siblings
TUNEL density in the CMZ is significantly higher in coa mutants than in wild-type siblings
(C) Anti-PCNA antibody labeling of wild-type and coa mutants with overexpression of β-SNAP1 during the initial OS growth period
Arrowheads and arrows indicate rod progenitor cells and reprogrammed proliferative Müller cells
the number of reprogrammed proliferative Müller cells was increased in the central retina
In coa mutants with overexpression of β-SNAP1 during the initial OS growth period (bottom)
the number of rod progenitor cells is markedly increased in the central retina; however
reprogrammed proliferative Müller cells were only observed in the peripheral retina and not in the central retina
(D) The number of PCNA-positive cells per section
In coa mutants with overexpression of β-SNAP1 during the initial OS growth period
numbers of proliferative Müller cells in both the CMZ (red bars) and the central retina (purple bars) were similar to that of wild type
Rod progenitors in the CMZ were not significantly different from those of wild type (blue bars)
rod progenitors in the central retina were twice as numerous as in wild type (green bars)
Müller cells are not reprogrammed for neuronal regeneration
but rod progenitors markedly increase in central retinas of coa mutants with overexpression of β-SNAP1 during the initial OS growth period
but non-significant increase in apoptotic cell density in the surviving photoreceptor cell layer in coa mutants with overexpression of β-SNAP1 during the initial OS growth period at 21 dpf; however
this subtle increase of apoptotic cell density may trigger proliferation of rod progenitor cells
Blockade of intracellular vesicular transport rescues photoreceptor apoptosis in coa mutants
(A) Retinas of 3.5 dpf wild-type and coa mutant embryos injected with standard MO
Cone photoreceptors and rod OSs were visualized by labeling with zpr1 antibody (green) and fluorescent signals from Tg[XlaRho:XP-GFP] (magenta)
In coa mutant retinas injected with either MO-ift88 or MO-kif3b
cone photoreceptor degeneration was partially inhibited
(B) Percentage of zpr1-positive area relative to total retinal area in wild-type and coa mutant embryos injected with standard MO and MO-ift88
MO-itf88 significantly rescued photoreceptor apoptosis in coa mutants
(C) Percentage of zpr1-positive area relative to total retinal area in wild-type and coa mutant embryos injected with standard MO and MO-kif3b
MO-kib3b significantly rescued photoreceptor apoptosis in coa mutants
(D) Retinas of 3.5 dpf wild-type and coa mutant embryos treated with DMSO or rapamycin
Lower panels indicate higher magnification of squares in upper panels
The outline of the photoreceptor cell layer (white dotted lines) was visualized by labeling with zpr1 (green) and phalloidin (magenta)
In coa mutant retinas treated with rapamycin
the size of photoreceptor cell layer increased
(E) Percentage of the photoreceptor cell layer relative to total retinal area in wild-type and coa mutant embryos treated with DMSO and rapamycin
Rapamycin treatment significantly recovers the size of photoreceptor cell layer in coa mutants
Since reduction of protein synthesis in the ER is likely to decrease vesicular transport to the OS
these data suggest that decreased vesicular transport from the ER to the OS suppresses photoreceptor apoptosis in coa mutants
These data support the possibility that excessive activation of vesicular transport activates BNip1 proapoptotic activity
The alternative spliced form of xbp-1 and increased chop1 mRNA expression were observed only in tunicamycin-treated embryos
(B) The ratio of the spliced form relative to the non-spliced form of xbp-1 mRNA
We carried out three independent sets of PCR reactions for wild type
The same set of PCR reactions are connected with the line
The difference of coa mutant heads relative to wild-type heads
and Tunicamycin-relative to DMSO-treated embryos in xbp1 spliced/non-spliced mRNA ratio were evaluated by Ratio paired t-test
There was no significant difference between wild type and coa mutants
(C) Ratio of chop1 mRNA relative to ef1α mRNA
and Tunicamycin-relative to DMSO-treated embryos in chop1 mRNA expression were evaluated by Ratio paired t-test
The role of BNip1-mediated apoptosis in photoreceptors
(A) The current model for molecular mechanism of BNip1-dependent apoptosis
BNip1 proapoptotic activity is inhibited by intra-moleculer interaction between N-terminal coiled-coil domain and BH3 domain
BNip1 interacts with other components of the syntaxin-18 complex (Syntaxin18
Sec22b) through their SNARE domain and forms cis-SNARE complex
in which BNip1 BH3 domain is activated to interact with anti-apoptotic Bcl2
leading to the activation of Bax-dependent apoptosis
syntaxin-18 cis-SNARE complex is normally disassembled by SNAP and NSF
syntaxin-18 cis-SNARE complex is abnormally accumulated on ER membrane
which subsequently allows BNip1 to interact with Bcl2
(B) A model for physiological significance of BNip1-mediated apoptosis in photoreceptor differentiation and survival
When intracellular vesicular transport is arrested
subsequently triggering the ER stress response (Right panel)
when intracellular vesicular transport is abnormally activated
vesicular fusion events increase on target membranes along the secretory pathway
Such excessive fusion events may trap SNAP molecules
which reduces the relative contribution of SNAP to vesicular fusion on the ER membrane
the syntaxin-18 cis-SNARE complex accumulates and the BNip1-dependent apoptotic pathway is activated (Left panel)
Blockade of ciliary transport functions of Ift88 or Kib3b inhibits BNip1-dependent apoptosis
BNip1 may cooperate with the ER stress response to maintain appropriate levels of vesicular transport in photoreceptors
both cones and rods undergo apoptosis in β-snap1 mutants during their initial OS growth period from 2 to 4 dpf
Although there is a second expansion phase of the rod OS
it is likely that the initial expansion of the rod OS is enough to trigger rod apoptosis in β-snap1 mutants
to determine the critical period of β-SNAP activity for photoreceptor survival
we overexpressed β-SNAP1 during different time windows in β-snap1 mutants using the heat shock promoter
Transient expression of β-SNAP1 from 36 to 132 hpf is enough to prevent cone and rod apoptosis in coa mutants at 6 dpf
Since overexpressed β-SNAP1 protein can be maintained at least for 24 hpf after heat-shock treatment
it is likely that cones are maintained in the absence of β-SNAP activity after 6 dpf
rods failed to be maintained in the absence of β-SNAP after 6 dpf
probably because rod OS genesis is still active from 8.5 to 28 dpf
These data suggest that BNip1-dependent apoptosis is associated with OS growth of rod and cone photoreceptors
All zebrafish experiments were performed in accordance with the Animal Care and Use Program of Okinawa Institute of Science and Technology Graduate School (OIST)
which is based on the Guide for the Care and Use of Laboratory Animals by the National Research Council of the National Academies and has been accredited by the Association for Assessment and Accreditation of Laboratory Animal Care (AAALAC International)
All experimental protocols were approved by the OIST Institutional Animal Care and Use Committee
TUNEL was performed using an In Situ Cell Death Detection Kit (Roche)
Rhodamine-conjugated phalloidin (Invitrogen
R415) at 0.66 μM was applied to visualize actin filaments on cryosections labelled with zpr1 antibody
Images were scanned using a confocal laser scanning microscope (Carl Zeiss
BNip1 is localized in the ER membrane via its C-terminal TM domain2
we replaced the Bcl2 TM domain with a BNip1 TM domain
EGFP or mCherry was fused to their N-termini
To confirm that Bcl2-ER is localized in the ER
we injected mRNA encoding EGFP-Bcl2-ER (200 ng/μL) with mRNA encoding monomeric Kusabira Orange (mKO)-tagged ER retention peptides (ER-mKO) (200 ng/μL)
We also injected mRNA encoding EGFP-Bcl2-ER (200 ng/μL) with mRNA encoding mKO-tagged mitochondrial-located peptides (MT-mKO) (400 ng/μL)
We also generated DNA constructs expressing mCherry-Bcl2 and mCherry-Bcl2-ER under control of the heat shock promoter
We established zebrafish transgenic lines Tg[hs:mCherry-tagged Bcl2] and Tg[hs:mCherry-tagged Bcl2-ER]
Morpholino was dissolved in water at 250 μM for MO-ift88
and injected into wild-type embryos at the one-cell stage
In accordance with a previous report36
wild-type and coa mutant embryos were treated with rapamycin (LC laboratories
Photoreceptor survival was evaluated with rhodamine-conjugated phalloidin labeling
the photoreceptor cell layer was outlined and its size was determined
Means and standard deviations were calculated
Statistical analysis was done using two-way ANOVA with the Tukey multiple comparison test
Total RNA was prepared from 2.5-dpf wild-type and coa mutant embryos
Complementary DNA strands were synthesized from total RNA using 3′RACE System for Rapid Amplification of cDNA Ends (Invitrogen
Cat#18373-027) and used as a template for semi-quantitative PCR
and ef1α cDNAs were amplified with TaKaRa Ex Taq (TaKaRa Biochemicals)
ER stress-induced wild-type samples were obtained by treatment with Tunicamycin (Nacalai code 35638-74
Amounts were quantified using ImageJ (NIH)
Statistical analysis employed two-tailed Ratio paired t-tests
Molecular genetics and emerging therapies for retinitis pigmentosa: Basic research and clinical perspectives
The BH3-only SNARE BNip1 mediates photoreceptor apoptosis in response to vesicular fusion defects
a family of NSF attachment proteins involved in intracellular membrane fusion in animals and yeast
SNAP family of NSF attachment proteins includes a brain-specific isoform
A fusion protein required for vesicle-mediated transport in both mammalian cells and yeast
The mechanisms of vesicle budding and fusion
Adenovirus E1B 19 kDa and Bcl-2 proteins interact with a common set of cellular proteins
Involvement of BNIP1 in apoptosis and endoplasmic reticulum membrane fusion
Functional identification of the apoptosis effector BH3 domain in cellular protein BNIP1
The unfolded protein response and cell fate control
Intraflagellar transport genes are essential for differentiation and survival of vertebrate sensory neurons
Kinesin-2 family in vertebrate ciliogenesis
Mutation of DNA primase causes extensive apoptosis of retinal neurons through the activation of DNA damage checkpoint and tumor suppressor p53
The role of subunit assembly in peripherin-2 targeting to rod photoreceptor disk membranes and retinitis pigmentosa
The 1D4 antibody labels outer segments of long double cone but not rod photoreceptors in zebrafish
Early onset of phenotype and cell patterning in the embryonic zebrafish retina
The development of photoreceptors in the zebrafish
Cloning and characterization of six zebrafish photoreceptor opsin cDNAs and immunolocalization of their corresponding proteins
Targeted effects of retinoic acid signaling upon photoreceptor development in zebrafish
Retinoic acid alters photoreceptor development in vivo
Late-stage neuronal progenitors in the retina are radial Muller glia that function as retinal stem cells
Stem cells in the teleost retina: Persistent neurogenesis and injury-induced regeneration
Genetic evidence for selective transport of opsin and arrestin by kinesin-II in mammalian photoreceptors
is essential for vertebrate photoreceptor assembly and maintenance
A transgenic zebrafish model for monitoring xbp1 splicing and endoplasmic reticulum stress in vivo
Transgenic zebrafish model to study translational control mediated by upstream open reading frame of human chop gene
Comparison of topographical patterns of ganglion and photoreceptor cell differentiation in the retina of the zebrafish
How variable clones build an invariant retina
Cone photoreceptor types in zebrafish are generated by symmetric terminal divisions of dedicated precursors
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TNFalpha induces muller glia to transition from non-proliferative gliosis to a regenerative response in mutant zebrafish presenting chronic photoreceptor degeneration
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Mamoru Fujiwara supported genotyping and histology experiments
This work was supported by a grant from OIST to I.M
Okinawa Institute of Science and Technology Graduate University
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DOI: https://doi.org/10.1038/s41598-020-74360-x
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Volume 8 - 2021 | https://doi.org/10.3389/fmed.2021.812370
The mean percentage change in newly started clinical trials for diseases other than COVID-19 between each month in 2019 and the corresponding month in 2020 was −7.5%
with the maximum of −57.3% observed between April 2019 and April 2020
the mean percentage change of reported results for each month in 2019 and 2020 was −5.1%
with the maximum of −27.4% observed in July 2020
The activity of clinical trials was decreased as the number of COVID-19 patients was increased
and a statistically negative correlation was observed between the prevalence of COVID-19 and the percentage decrease in the number of clinical trials stared or reported results
decreases were observed in the latter half of 2020 compared with the same period during the previous year
A considerable decline in non-COVID-19 activity for all indicators regarding clinical developments was suggested during the first wave of the COVID-19 pandemic
It is important to recognize the situation and continue to make efforts to conduct clinical trials for both COVID-19 and no-COVID-19 for new medical developments in the future
Crucial clinical trials are being conducted internationally
which can lead to new drug applications in each participating country or region
medical development for non-COVID-19 is also important
this study mainly focused on clinical trials for non-COVID-19
The number of clinical trials for diseases other than COVID-19 was calculated by subtracting the number of clinical trials for COVID-19 (entering “COVID-19 OR SARS-CoV-2” in the “Condition or disease” field) from the number of all clinical trials
Monthly data regarding reported results were extracted by specifying the date using “Results First Posted” in the advanced search
studies labeled with the status “Completed” were identified as completed clinical trials with results
The total number of COVID-19 cases was obtained from the website “Worldometer Coronavirus” (9)
The total number of COVID-19 cases at the end of the previous month was used to examine the impact on clinical research activities during that month
extracted from the cumulative graph of total cases by country
(A) Number of newly started clinical trials for diseases other than COVID-19; (B) Percentage change of newly started clinical trials for diseases other than COVID-19
Relationship between total cases of COVID-19 and percentage change of the number of newly started clinical trials for diseases other than COVID-19 in regions with more than 30 studies
The size of the bubbles reflected the number of studies
The number of clinical trials for diseases other than COVID-19 that were started during the fourth quarter of 2020 showed signs of recovery
but this was due to the increase in the number started in the United States
the number of clinical trials started for diseases other than COVID-19 was still less than that in during the same month of the previous year in regions other than the United States
the total number of clinical trials (COVID-19 and non-COVID-19) recovered rapidly and has exceeded the number in the same month of the previous year since June 2020
(A) Number of clinical trials for diseases other than COVID-19 with results; (B) Percentage change of clinical trials for diseases other than COVID-19 with results
Relationship between total cases of COVID-19 and percentage change of the number of clinical trials with results in regions with more than 30 studies
A similar tendency was observed in the number of completed clinical trials with results in 2020. The mean number of completed clinical trials with results for diseases other than COVID-19 in 2020 was 373 (SD, 38). The mean percentage change for each month between 2019 and 2020 was −7.9% (SD, 12.5%). The decrease from May to July 2020 was notable compared with the same period during the previous year (Supplementary Table 2, Supplementary Figure 7)
The total numbers of completed clinical trials with results in 2020 decreased compared with the number in 2019 in Africa
this decrease in current clinical trials will affect new treatments for at least several years to come
It is important to note that this study showed regional trends in addition to global trends of clinical trials conducted during the COVID-19 pandemic. Interestingly, there was a negative correlation between the number of COVID-19 cases and clinical trial activity. Demographic effects have been reported (19, 20)
and it is clear that the number of COVID-19 cases varies by region
where the number of COVID-19 cases per 1 million population was <100 at the end of April 2020
the percentage decrease in the numbers of newly started clinical trials and reported results was modest compared with the decrease seen in Europe and the United States
where the number of COVID-19 cases per 1 million population was more than 2000
Given that international clinical trials are now frequently performed
if a region is unable to participate in a pivotal international clinical trial due to the COVID-19 epidemic
this will cause a delay in new drug development in that region
This could exacerbate the existing global inequalities
It is suggested that the control of COVID-19 by each country/region is also important for the development of future treatments in that country/region
It is unlikely that COVID-19 will disappear in the near future
and therefore some medical resources will continue to be dedicated to COVID-19 even in the post-COVID era
It is necessary to consider budget and staffing levels
with a view to developing new treatments for diseases other than COVID-19
To evaluate the impact of the COVID-19 pandemic on overall clinical development
we examined the number of newly started clinical trials
all indicators showed a marked drop in quarters 2 and 3 of 2020 compared with the same period during the previous year
indicating the magnitude of the impact of the first wave of COVID-19 on clinical development
The decrease in the number of clinical trials started might reflect the increase in workload of medical staff and/or the financial situation of sponsors
The decrease in the number of completed studies might reflect the effect of delayed patient recruitment and/or required visits
and the decrease in the number of submitted applications might reflect the termination of studies before they are competed and/or the increased workload of the applicant company and/or the regulatory authority
Many experts are involved from the initiation of clinical trials to the submission of new drug applications
thus it can be seen that the COVID-19 pandemic affected various stages of clinical development
because information about an approved drug and its approval date is made publicly available
it will be possible to evaluate the number of new approvals in another year or so
During the first wave of the COVID-19 pandemic, there was a significant decline in clinical trial activity and subsequent new drug applications. This decline will affect the development of new treatments in the future, and it is necessary to recognize this situation and continue to make efforts to perform clinical trials for diseases other than COVID-19, as well as for COVID-19. Utilizing the COVID-19 prediction (30)
it will be possible to reduce the impact by allocating resources so that activities for non-COVID clinical trials will not decrease before the rapid increase of COVID-19 infections in the future
It takes a lot of time and effort to launch and complete a clinical trial and to establish a new treatment
therefore a long-term perspective is required
Even in a situation in which the COVID-19 pandemic is not yet under control
it is important to implement concrete strategies that minimize the impact on new or ongoing clinical trials
based on our analysis of the first wave of the COVID-19 pandemic
The original contributions presented in the study are included in the article/Supplementary Material
further inquiries can be directed to the corresponding author/s
performed the analysis and interpreted the data
All authors reviewed and approved the final draft
This work was partly supported by JSPS KAKENHI Grant No
YA reports grants and personal fees from Chugai Pharmaceutical Co.
grants and personal fees from Daiichi Sankyo Company
The remaining author declares 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/fmed.2021.812370/full#supplementary-material
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Citation: Nishiwaki S and Ando Y (2021) COVID-19 Pandemic and Trends in Clinical Trials: A Multi-Region and Global Perspective
Received: 10 November 2021; Accepted: 08 December 2021; Published: 24 December 2021
Copyright © 2021 Nishiwaki and Ando. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY)
distribution or reproduction in other forums is permitted
provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited
in accordance with accepted academic practice
distribution or reproduction is permitted which does not comply with these terms
*Correspondence: Satoshi Nishiwaki, bi0zMTA0QHRmNy5zby1uZXQubmUuanA=
Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations
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to meet some of the talented teenagers in two of the pre-college division's four orchestras; here on this 2,162nd edition of the McGraw Family's Young Artist Showcase
I didn't misspeak earlier there are indeed four orchestras in MSM pre- college division
nearly 300 youngsters spend their Saturdays taking private lessons and then rehearsing within one of those symphonic ensembles
Our own musical adventures as always are presented with high community pride by the Harold W
One of the very impressive elements of these pre-college orchestral programs that MSM
but 20th-century works that would pose significant challenges (I suspect) for a professional orchestra
Nathan Hetherington guiding his pre-college Philharmonic youngsters through the rhythmic tangles of David Diamond's Symphony Number One
Bob Sherman No applause because the rest of David Diamond's first symphony
yet to come in this May 11th concert by the 16 and 17 year old players in the Manhattan school's Pre-College Philharmonic conducted by Nathan Hetherington
Nell Flanders led the even younger members of the Pre-College Symphony
and it's similarly a daunting work that they (as I suspect most of us) had never even heard of before: William Grant Still's Afro-American symphony
This historically significant work: -it was the first symphony by an African-American composer to be played by a major American orchestra (I think it was back in 1930 or 31)
Bob Sherman It's in four movements each bearing lines from a poem by Paul Laurence Dunbar
We don't have time for the complete symphony
It's mighty tiresome lying around on this sorrow-laden earthly ground and oftentimes I think it would be a sweet thing just to die and go long home"
Bob Sherman Paul Laurence Dunbar's poetic thoughts for the finale of William Grant Still symphony are upbeat and exultant
"Be proud my race in mind and soul/thy name is written on glory scroll/in characters of fire/high amid the clouds of Fame's Bright Sky/the banner emblazoned folds now fly/and truth shall lift them higher."
Bob Sherman Part of the slow movement and the finale of William Grant Still's Afro-American Symphony..
Nell Flanders leading the 14 and 15 year old players in the Manhattan School's Pre-College Division Symphony
We'll rejoin the older kids in the Pre-College Philharmonic and meet the two winners of its' own Concerto Competition after we call a short intermission
here on the McGraw Family's Young Artists Showcase
Bob Sherman I'm Bob Sherman and as promised we return to the Manhattan School of Music Graduation day this past May 11th when all four of the Pre-College orchestras were in performing action
The most advance of the ensembles: the Pre-College Philharmonic
and the two top winners were featured that evening
Abigail Nishiwaki; then a graduating senior at Scarsdale High School
studying at MSM with Elizabeth Faidley; now a freshman at Princeton
where she plans to divide her attention between music and public policy..
Abigail also served as concertmaster of the Pre-College Philharmonic and her concerto choice was the first movement of the Sibelius
Bob Sherman Quite a compelling performance: first moment from the D minor Concerto of John Sibelius
played last May by the winner of the Manhattan School's Pre-College Philharmonic Concerto Competition
The Pianist laureate of the concerto competition was 16 year-old Esteban Castro
quite a number of awards and prizes have been for his jazz performances
he's also composed more than 40 pieces and looks with a special pride on a big band commission from the Jazz at Lincoln Center Orchestra
Esteban Castro did stay within the classical world to collect the Manhattan School prize though
and here is his exciting performance of Prokofiev's Piano Concerto Number one
again with music director Nathan Hetherington conducting
Bob Sherman Resounding and well-deserved applause for that sterling account of Prokofiev's Piano Concerto Number one
played just a couple of months ago by 16 year-old Esteban Castro with Nathan Hetherington at the helm of the other teenagers in the Manhattan School's Pre-College Philharmonic
director of the Pre-College division for making these performances available to us
And that does end our showcase adventures for tonight
meaning that it's time for our weekly greeting from the fellow whose personal enthusiasm and financial generosity have combined to let the Young Artist Showcase move about halfway through it's 42nd consecutive year on WQXR
There's nothing more satisfying than seeing some of the wonderful young musicians we introduce on young artist showcase
go on to become part of our musical mainstream
And it happens all the time on this program
It shows we're not only on the right track
but leading the way towards a great American future in the arts
Last month Astral Artists announced the 2019 winners of it's national auditions
but next week we'll be eavesdropping on recitals by some of the 2018 laureates; an occasion to which you are most cordially invited
Our Young Artists Showcase far in-away the longest ongoing series in WQXR's history is supported as a community service by Terry McGraw and the family foundation named for his dad
McGraw Jr. Max Fine as my stalwart producing partner with thanks due as well
to you: members of our faithful listening panel
Young Artists Showcase is a WQXR weekly radio show that since 1978 has sought out and displayed the talents of young emerging artists
WQXR’s Young Artists Showcase is supported by The Harold W
HYOGO: A long-awaited Arabic pita bread bakery ‘The Babylon Bakery’ opened it’s doors on Friday in Nishiwaki
“Many Middle Eastern and Mediterranean Muslims live in the neighboring cities of Kobe
Osaka as well as lots of other parts of Japan,” the bakery owner
Iraqi-born Haithem Humadi told Arab News Japan
“I hope they will be able to experience pita bread
which is just like the one in their hometown,” he said
The project was established after seven years of planning with great care taken to produce an authentic taste
He imported the Syrian-designed pita bread manufacturing machine from Turkey
he is going to produce 300 kilograms a day
but the machine has so much capacity of 5 tonnes of bread per day
the foreign technicians who are capable of maintaining these machines cannot come to Japan at present due to COVID restrictions
“The Babylon Bakery” will mainly deal with businesses such as halal shops and restaurants throughout Japan
although individuals will be able to buy online
Humadi commented: “We posted on Facebook and Twitter only last week and received more than 200 responses in five days from Tokyo
Hiroshima and other regions not only the people from overseas residing in Japan
Japanese version
Japanese version
Japanese version
Copyright THE MAINICHI NEWSPAPERS. All rights reserved.
Michiko Nishiwaki’s career spans bodybuilding, martial arts, and action cinema. Born on November 21, 1957, in Japan, she has challenged norms and inspired change in multiple fields. With her action movies, she was a key figure in the martial arts boom era of filmmaking.
In the early 1980s, Michiko Nishiwaki became Japan’s first female bodybuilding champion. She held the title for three years. Her success came without using performance-enhancing drugs.
At a time when muscular women faced criticism, Nishiwaki showed that strength and femininity could coexist. Her achievements led to a fitness boom in Japan. She opened three gyms and appeared frequently on television.
Nishiwaki is trained in several martial arts. She holds a black belt in Gōjū-ryū karate and has studied Shotokan karate, wushu, and taekwondo. These skills became central to her film career.
View this post on Instagram A post shared by LowKick MMA (@lowkickmma)
Nishiwaki debuted in the 1985 film My Lucky Stars with Jackie Chan and Sammo Hung. She often played villains and tough female characters in action films. Her roles helped popularize the “girls with guns” subgenre
such as In the Line of Duty III and Avenging Quartet
highlighted her martial arts and stunt abilities
She became a key figure in Hong Kong action cinema during the 1980s and 1990s
She worked as a stuntwoman for stars like Lucy Liu in Charlie’s Angels and Kelly Hu in The Scorpion King
Her stunts appeared in films like Kill Bill: Vol
Nishiwaki broke barriers for women in fitness
She inspired more women to pursue strength training and martial arts
Her work brought Hong Kong action styles to global audiences
Timothy Wheaton is a combat sports writer who covers MMA
He has been an avid follower of these sports since 2005
Tim also works with a host of other media sites such as Calf Kick Sports
Tim is the authority on kickboxing and an MMA journalist who has covered K-1
in Persona 3 Reload with all dialogue options
Here is the Strength Social Link Guide for Yuko Nishiwaki in Persona 3 Reload
This includes the answers for Social Link events with Yuko Nishiwaki
Yuko is located in the 2F Classroom Hallway in Gekkoukan High School and is available on Wednesdays and Saturdays as long as it is a school day
not be available the week leading up to exams
To begin the Strength Social Link for Yuko
you must first start the Chariot Social Link
you will get the option to greet Yuko and invite her to walk home with you
This will then start the Strength Social Link
having a Persona of the Strength Arcana in your stock will increase each interaction by one point and will speed up the progress of the Social Link
The protagonist will receive the Kid's Letter from Yuko Nishiwaki when the Strength Social Link reaches Rank 10
This decision to enter a romantic relationship with Yuko Nishiwaki happens when leveling up the Social Link to Rank 9
Here are all of the dialogue options and answers for Yuko Nishiwaki in Persona 3 Reload
Dialogue options in bold are the best options
a friendly reminder to have a Persona of the Strength Arcana when you spend time with Yuko
Choosing “I'm honored” or “I don't mind” may be Romance flags for Yuko
Choosing “Wanna make that true?” may be a Romance Flag for Yuko
Only digital versions are available for Xbox
Jesseyriche Cortez wrote about video games for ClutchPoints
Jesseyriche also reviews games and plays the critically acclaimed MMORPG Final Fantasy XIV that has a free trial up to level 70 and includes the entirety of A Realm Reborn
and Stormblood with no restrictions on playtime
Here is our Strength Social Link guide for Yuko Nishiwaki in Persona 3 Portable
The guide may contain spoilers, so do be careful. It is also important to note that this guide is for Persona 3 Portable, which originally came out in 2010, as well as in 2023 with the port. The Social Link Guide for Strength in Persona 3 Reload is a different guide altogether
You can find Yuko during the day outside Classroom 2-F in Gekkoukan on Wednesdays and Saturdays
the Protagonist does not get additional skills during battle
If you choose to play as the male protagonist, you can start the Social Link as early as April 28. To start it, the player must ask to walk her home during Ranks 2 and 3 of the Chariot Social Link
You can also romance Yuko as the male protagonist
The affection points below assume that you have a Persona of the Strength arcana with you
If you choose to play as the female protagonist, you will not have Yuko as your Strength Social Link. Instead, Koromaru will be your Strength Social Link
That's all for our guide on Persona 3 Portable's Strength Social Link, Yuko Nishiwaki. Persona 3 Portable is available on PC. For more gaming news from us, you can check out our gaming news articles
Yuko Nishiwaki is the team manager of the Track Team you signed up for
You’ll have to jump through some slight hoops to unlock her Social Link
This guide will be completely spoiler-free
If you’re in the middle of Yuko’s social link
this guide will only list the answers and avoid spoilers altogether
Each Social Link allows you to interact with characters outside of S.E.E.S.
allowing you to experience a fun or emotional side story in the meantime
you’ll encounter some prompts where you’ll have to respond to a question with a specific answer
Some of these answers will reward you with points that allow you to proceed through a Social Link faster
We’ll list out the best answers for you to pick for each rank so you can run through each Social Link efficiently
Important Note: You can obtain even more points by having a Persona with a matching Arcana in your party
if you have a Strength Persona in your arsenal
you’ll be able to go through Yuko’s Social Link even faster
Yuko’s Social Link is easy to unlock but requires you to unlock the Chariot Social Link first
you’ll meet Yuko and have the option to ask her to walk home with you
but as you progress through the Chariot Social Link
she will eventually agree to walk home with you
no choices you make will impact the course of your Social Link
as you will automatically reach the final rank no matter which choice you make
Writer and journalist covering the gaming industry for The Nerd Stash