Probiotic supplementation attenuates age‐related sarcopenia via the gut–muscle axis in SAMP8 mice

Abstract Background Age‐related muscle dysfunctions are common disorders resulting in poor quality of life in the elderly. Probiotic supplementation is a potential strategy for preventing age‐related sarcopenia as evidence suggests that probiotics can enhance muscle function via the gut–muscle axis....

Full description

Bibliographic Details
Main Authors: Li‐Han Chen, Shy‐Shin Chang, Hsin‐Yi Chang, Chieh‐Hsi Wu, Chun‐Hsu Pan, Chun‐Chao Chang, Ching‐Hung Chan, Hui‐Yu Huang
Format: Article
Language:English
Published: Wiley 2022-02-01
Series:Journal of Cachexia, Sarcopenia and Muscle
Subjects:
Online Access:https://doi.org/10.1002/jcsm.12849
_version_ 1797826778598735872
author Li‐Han Chen
Shy‐Shin Chang
Hsin‐Yi Chang
Chieh‐Hsi Wu
Chun‐Hsu Pan
Chun‐Chao Chang
Ching‐Hung Chan
Hui‐Yu Huang
author_facet Li‐Han Chen
Shy‐Shin Chang
Hsin‐Yi Chang
Chieh‐Hsi Wu
Chun‐Hsu Pan
Chun‐Chao Chang
Ching‐Hung Chan
Hui‐Yu Huang
author_sort Li‐Han Chen
collection DOAJ
description Abstract Background Age‐related muscle dysfunctions are common disorders resulting in poor quality of life in the elderly. Probiotic supplementation is a potential strategy for preventing age‐related sarcopenia as evidence suggests that probiotics can enhance muscle function via the gut–muscle axis. However, the effects and mechanisms of probiotics in age‐related sarcopenia are currently unknown. In this study, we examined the effects of Lactobacillus casei Shirota (LcS), a probiotic previously reported to improve muscle function in young adult mice. Methods We administered LcS (1 × 108 or 1 × 109 CFU/mouse/day) by oral gavage to senescence‐accelerated mouse prone‐8 mice for 12 weeks (16‐ to 28‐week‐old). Sixteen‐week‐old and 28‐week‐old SMAP8 mice were included as non‐aged and aged controls, respectively. Muscle condition was evaluated using dual‐energy X‐ray absorptiometry for muscle mass, holding impulse and grip strength tests for muscle strength, and oxygen consumption rate, gene expressions of mitochondrial biogenesis, and mitochondrial number assays for mitochondria function. Inflammatory cytokines were determined using enzyme‐linked immunosorbent assay. Gas chromatography–mass spectrometry was utilized to measure the short‐chain fatty acid levels. The gut microbiota was analysed based on the data of 16S rRNA gene sequencing of mouse stool. Results The LcS supplementation reduced age‐related declines in muscle mass (>94.6%, P < 0.04), strength (>66% in holding impulse and >96.3% in grip strength, P < 0.05), and mitochondrial function (P < 0.05). The concentration of short‐chain fatty acids (acetic, isobutyric, butyric, penic, and hexanoic acid) was recovered by LcS (>65.9% in the mice given high dose of LcS, P < 0.05) in the aged mice, and LcS attenuated age‐related increases in inflammation (P < 0.05) and reactive oxygen species (>89.4%, P < 0.001). The high dose of LcS supplementation was also associated with distinct microbiota composition as indicated by the separation of groups in the beta‐diversity analysis (P = 0.027). LcS supplementation altered predicted bacterial functions based on the gut microbiota. Apoptosis (P = 0.026), p53 signalling (P = 0.017), and non‐homologous end‐joining (P = 0.031) were significantly reduced, whereas DNA repair and recombination proteins (P = 0.043), RNA polymerase (P = 0.008), and aminoacyl‐tRNA biosynthesis (P = 0.003) were increased. Finally, the genera enriched by high‐dose LcS [linear discriminant analysis (LDA) score > 2.0] were positively correlated with healthy muscle and physiological condition (P < 0.05), while the genera enriched in aged control mice (LDA score > 2.0) were negatively associated with healthy muscle and physiological condition (P < 0.05). Conclusions Lactobacillus casei Shirota represents an active modulator that regulates the onset and progression of age‐related muscle impairment potentially via the gut–muscle axis.
first_indexed 2024-04-09T12:37:40Z
format Article
id doaj.art-81c733f691ee440c852f2abd075cd6e2
institution Directory Open Access Journal
issn 2190-5991
2190-6009
language English
last_indexed 2024-04-09T12:37:40Z
publishDate 2022-02-01
publisher Wiley
record_format Article
series Journal of Cachexia, Sarcopenia and Muscle
spelling doaj.art-81c733f691ee440c852f2abd075cd6e22023-05-15T09:27:15ZengWileyJournal of Cachexia, Sarcopenia and Muscle2190-59912190-60092022-02-0113151553110.1002/jcsm.12849Probiotic supplementation attenuates age‐related sarcopenia via the gut–muscle axis in SAMP8 miceLi‐Han Chen0Shy‐Shin Chang1Hsin‐Yi Chang2Chieh‐Hsi Wu3Chun‐Hsu Pan4Chun‐Chao Chang5Ching‐Hung Chan6Hui‐Yu Huang7Institute of Fisheries Science National Taiwan University Taipei TaiwanDepartment of Family Medicine, School of Medicine, College of Medicine Taipei Medical University Taipei TaiwanGraduate Institute of Metabolism and Obesity Sciences, College of Nutrition Taipei Medical University Taipei TaiwanSchool of Pharmacy Taipei Medical University Taipei TaiwanSchool of Pharmacy Taipei Medical University Taipei TaiwanDivision of Gastroenterology and Hepatology, Department of Internal Medicine Taipei Medical University Hospital Taipei TaiwanDepartment of Chemical Engineering and Biotechnology Tatung University Taipei TaiwanGraduate Institute of Metabolism and Obesity Sciences, College of Nutrition Taipei Medical University Taipei TaiwanAbstract Background Age‐related muscle dysfunctions are common disorders resulting in poor quality of life in the elderly. Probiotic supplementation is a potential strategy for preventing age‐related sarcopenia as evidence suggests that probiotics can enhance muscle function via the gut–muscle axis. However, the effects and mechanisms of probiotics in age‐related sarcopenia are currently unknown. In this study, we examined the effects of Lactobacillus casei Shirota (LcS), a probiotic previously reported to improve muscle function in young adult mice. Methods We administered LcS (1 × 108 or 1 × 109 CFU/mouse/day) by oral gavage to senescence‐accelerated mouse prone‐8 mice for 12 weeks (16‐ to 28‐week‐old). Sixteen‐week‐old and 28‐week‐old SMAP8 mice were included as non‐aged and aged controls, respectively. Muscle condition was evaluated using dual‐energy X‐ray absorptiometry for muscle mass, holding impulse and grip strength tests for muscle strength, and oxygen consumption rate, gene expressions of mitochondrial biogenesis, and mitochondrial number assays for mitochondria function. Inflammatory cytokines were determined using enzyme‐linked immunosorbent assay. Gas chromatography–mass spectrometry was utilized to measure the short‐chain fatty acid levels. The gut microbiota was analysed based on the data of 16S rRNA gene sequencing of mouse stool. Results The LcS supplementation reduced age‐related declines in muscle mass (>94.6%, P < 0.04), strength (>66% in holding impulse and >96.3% in grip strength, P < 0.05), and mitochondrial function (P < 0.05). The concentration of short‐chain fatty acids (acetic, isobutyric, butyric, penic, and hexanoic acid) was recovered by LcS (>65.9% in the mice given high dose of LcS, P < 0.05) in the aged mice, and LcS attenuated age‐related increases in inflammation (P < 0.05) and reactive oxygen species (>89.4%, P < 0.001). The high dose of LcS supplementation was also associated with distinct microbiota composition as indicated by the separation of groups in the beta‐diversity analysis (P = 0.027). LcS supplementation altered predicted bacterial functions based on the gut microbiota. Apoptosis (P = 0.026), p53 signalling (P = 0.017), and non‐homologous end‐joining (P = 0.031) were significantly reduced, whereas DNA repair and recombination proteins (P = 0.043), RNA polymerase (P = 0.008), and aminoacyl‐tRNA biosynthesis (P = 0.003) were increased. Finally, the genera enriched by high‐dose LcS [linear discriminant analysis (LDA) score > 2.0] were positively correlated with healthy muscle and physiological condition (P < 0.05), while the genera enriched in aged control mice (LDA score > 2.0) were negatively associated with healthy muscle and physiological condition (P < 0.05). Conclusions Lactobacillus casei Shirota represents an active modulator that regulates the onset and progression of age‐related muscle impairment potentially via the gut–muscle axis.https://doi.org/10.1002/jcsm.12849ProbioticsGut–muscle axisAge‐related sarcopeniaGut microbiotaShort‐chain fatty acid
spellingShingle Li‐Han Chen
Shy‐Shin Chang
Hsin‐Yi Chang
Chieh‐Hsi Wu
Chun‐Hsu Pan
Chun‐Chao Chang
Ching‐Hung Chan
Hui‐Yu Huang
Probiotic supplementation attenuates age‐related sarcopenia via the gut–muscle axis in SAMP8 mice
Journal of Cachexia, Sarcopenia and Muscle
Probiotics
Gut–muscle axis
Age‐related sarcopenia
Gut microbiota
Short‐chain fatty acid
title Probiotic supplementation attenuates age‐related sarcopenia via the gut–muscle axis in SAMP8 mice
title_full Probiotic supplementation attenuates age‐related sarcopenia via the gut–muscle axis in SAMP8 mice
title_fullStr Probiotic supplementation attenuates age‐related sarcopenia via the gut–muscle axis in SAMP8 mice
title_full_unstemmed Probiotic supplementation attenuates age‐related sarcopenia via the gut–muscle axis in SAMP8 mice
title_short Probiotic supplementation attenuates age‐related sarcopenia via the gut–muscle axis in SAMP8 mice
title_sort probiotic supplementation attenuates age related sarcopenia via the gut muscle axis in samp8 mice
topic Probiotics
Gut–muscle axis
Age‐related sarcopenia
Gut microbiota
Short‐chain fatty acid
url https://doi.org/10.1002/jcsm.12849
work_keys_str_mv AT lihanchen probioticsupplementationattenuatesagerelatedsarcopeniaviathegutmuscleaxisinsamp8mice
AT shyshinchang probioticsupplementationattenuatesagerelatedsarcopeniaviathegutmuscleaxisinsamp8mice
AT hsinyichang probioticsupplementationattenuatesagerelatedsarcopeniaviathegutmuscleaxisinsamp8mice
AT chiehhsiwu probioticsupplementationattenuatesagerelatedsarcopeniaviathegutmuscleaxisinsamp8mice
AT chunhsupan probioticsupplementationattenuatesagerelatedsarcopeniaviathegutmuscleaxisinsamp8mice
AT chunchaochang probioticsupplementationattenuatesagerelatedsarcopeniaviathegutmuscleaxisinsamp8mice
AT chinghungchan probioticsupplementationattenuatesagerelatedsarcopeniaviathegutmuscleaxisinsamp8mice
AT huiyuhuang probioticsupplementationattenuatesagerelatedsarcopeniaviathegutmuscleaxisinsamp8mice