Exercise-acclimated microbiota improves skeletal muscle metabolism via circulating bile acid deconjugation

被引:16
作者
Aoi, Wataru [1 ]
Inoue, Ryo [1 ,2 ]
Mizushima, Katsura [2 ,3 ]
Honda, Akira [3 ,4 ]
Bjornholm, Marie [4 ,5 ]
Takagi, Tomohisa [6 ,7 ]
Naito, Yuji [3 ]
机构
[1] Kyoto Prefectural Univ, Grad Sch Life & Environm Sci, Div Appl Life Sci, Kyoto 6068522, Japan
[2] Setsunan Univ, Fac Agr, Dept Appl Biol Sci, Lab Anim Sci, Osaka 5730101, Japan
[3] Kyoto Prefectural Univ Med, Grad Sch Med Sci, Dept Human Immunol & Nutr Sci, Kyoto 6028566, Japan
[4] Tokyo Med Univ, Ibaraki Med Ctr, Gastroenterol, Ibaraki 3000395, Japan
[5] Karolinska Inst, Dept Mol Med & Surg, S-17176 Stockholm, Sweden
[6] Kyoto Prefectural Univ Med, Grad Sch Med Sci, Mol Gastroenterol & Hepatol, Kyoto 6028566, Japan
[7] Kyoto Prefectural Univ Med, Grad Sch Med Sci, Dept Med Innovat & Translat Med Sci, Kyoto 6028566, Japan
基金
日本学术振兴会;
关键词
Habitual exercise; diet -induced metabolic; skeletal muscle; Altered microbiota; PROTEIN-KINASE-C; GUT MICROBIOTA; MITOCHONDRIAL BIOGENESIS; SEDENTARY BEHAVIOR; PHYSICAL-ACTIVITY; ADIPOSE-TISSUE; AMP-KINASE; DIET; ACTIVATION; HEALTH;
D O I
10.1016/j.isci.2023.106251
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
Habitual exercise alters the intestinal microbiota composition, which may mediate its systemic benefits. We examined whether transplanting fecal microbiota from trained mice improved skeletal muscle metabolism in high-fat diet (HFD)-fed mice. Fecal samples from sedentary and exercise-trained mice were gavage-fed to germ-free mice. After receiving fecal samples from trained donor mice for 1 week, recipient mice had elevated levels of AMP-activated protein kinase (AMPK) and insulin growth factor-1 in skeletal muscle. In plasma, bile acid (BA) deconjugation was found to be promoted in recipients transplanted with feces from trained donor mice; free-form BAs also induced more AMPK signaling and glucose uptake than tauro-conjugated BAs. The transplantation of exercise-acclimated fecal microbiota improved glucose tolerance after 8 weeks of HFD administration. Intestinal microbiota may mediate exercise-induced metabolic improvements in mice by modifying circulating BAs. Our findings provide insights into the prevention and treatment of metabolic diseases.
引用
收藏
页数:20
相关论文
共 69 条
[1]   Gut microbiota-derived metabolites as central regulators in metabolic disorders [J].
Agus, Allison ;
Clement, Karine ;
Sokol, Harry .
GUT, 2021, 70 (06) :1174-1182
[2]  
Allen JM, 2018, MED SCI SPORT EXER, V50, P747, DOI [10.1249/MSS.0000000000001495, 10.1249/mss.0000000000001495]
[3]   Dietary whey hydrolysate with exercise alters the plasma protein profile: A comprehensive protein analysis [J].
Aoi, Wataru ;
Takanami, Yoshikazu ;
Kawai, Yukari ;
Morifuji, Masashi ;
Koga, Jinichiro ;
Kanegae, Minoru ;
Mihara, Kenichi ;
Yanohara, Taishi ;
Mukai, Jun ;
Naito, Yuji ;
Yoshikawa, Toshikazu .
NUTRITION, 2011, 27 (06) :687-692
[4]   The microRNA miR-696 regulates PGC-1α in mouse skeletal muscle in response to physical activity [J].
Aoi, Wataru ;
Naito, Yuji ;
Mizushima, Katsura ;
Takanami, Yoshikazu ;
Kawai, Yukari ;
Ichikawa, Hiroshi ;
Yoshikawa, Toshikazu .
AMERICAN JOURNAL OF PHYSIOLOGY-ENDOCRINOLOGY AND METABOLISM, 2010, 298 (04) :E799-E806
[5]   The 5′-AMP-activated protein kinase γ3 isoform has a key role in carbohydrate and lipid metabolism in glycolytic skeletal muscle [J].
Barnes, BR ;
Marklund, S ;
Steiler, TL ;
Walter, M ;
Hjälm, G ;
Amarger, V ;
Mahlapuu, M ;
Leng, Y ;
Johansson, C ;
Galuska, D ;
Lindgren, K ;
Åbrink, M ;
Stapleton, D ;
Zierath, JR ;
Andersson, L .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2004, 279 (37) :38441-38447
[6]   Effect of AMPK activation on muscle glucose metabolism in conscious rats [J].
Bergeron, R ;
Russell, RR ;
Young, LH ;
Ren, JM ;
Marcucci, M ;
Lee, A ;
Shulman, GI .
AMERICAN JOURNAL OF PHYSIOLOGY-ENDOCRINOLOGY AND METABOLISM, 1999, 276 (05) :E938-E944
[7]   Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 [J].
Bolyen, Evan ;
Rideout, Jai Ram ;
Dillon, Matthew R. ;
Bokulich, NicholasA. ;
Abnet, Christian C. ;
Al-Ghalith, Gabriel A. ;
Alexander, Harriet ;
Alm, Eric J. ;
Arumugam, Manimozhiyan ;
Asnicar, Francesco ;
Bai, Yang ;
Bisanz, Jordan E. ;
Bittinger, Kyle ;
Brejnrod, Asker ;
Brislawn, Colin J. ;
Brown, C. Titus ;
Callahan, Benjamin J. ;
Caraballo-Rodriguez, Andres Mauricio ;
Chase, John ;
Cope, Emily K. ;
Da Silva, Ricardo ;
Diener, Christian ;
Dorrestein, Pieter C. ;
Douglas, Gavin M. ;
Durall, Daniel M. ;
Duvallet, Claire ;
Edwardson, Christian F. ;
Ernst, Madeleine ;
Estaki, Mehrbod ;
Fouquier, Jennifer ;
Gauglitz, Julia M. ;
Gibbons, Sean M. ;
Gibson, Deanna L. ;
Gonzalez, Antonio ;
Gorlick, Kestrel ;
Guo, Jiarong ;
Hillmann, Benjamin ;
Holmes, Susan ;
Holste, Hannes ;
Huttenhower, Curtis ;
Huttley, Gavin A. ;
Janssen, Stefan ;
Jarmusch, Alan K. ;
Jiang, Lingjing ;
Kaehler, Benjamin D. ;
Bin Kang, Kyo ;
Keefe, Christopher R. ;
Keim, Paul ;
Kelley, Scott T. ;
Knights, Dan .
NATURE BIOTECHNOLOGY, 2019, 37 (08) :852-857
[8]   Voluntary exercise improves insulin sensitivity and adipose tissue inflammation in diet-induced obese mice [J].
Bradley, Richard L. ;
Jeon, Justin Y. ;
Liu, Fen-Fen ;
Maratos-Flier, Eleftheria .
AMERICAN JOURNAL OF PHYSIOLOGY-ENDOCRINOLOGY AND METABOLISM, 2008, 295 (03) :E586-E594
[9]   Exercise is a Novel Promoter of Intestinal Health and Microbial Diversity [J].
Campbell, Sara C. ;
Wisniewski, Paul J., II .
EXERCISE AND SPORT SCIENCES REVIEWS, 2017, 45 (01) :41-47
[10]   Gut Microbiota and Predicted Metabolic Pathways in a Sample of Mexican Women Affected by Obesity and Obesity Plus Metabolic Syndrome [J].
Chavez-Carbajal, Alejandra ;
Nirmalkar, Khemlal ;
Perez-Lizaur, Ana ;
Hernandez-Quiroz, Fernando ;
Ramirez-del-Alto, Silvia ;
Garcia-Mena, Jaime ;
Hernandez-Guerrero, Cesar .
INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES, 2019, 20 (02)