Gut bacteria are critical for optimal muscle function: A potential link with glucose homeostasis

Journal article


Nay, Kevin, Jollet, Maxence, Goustard, Benedicte, Baati, Narjes, Vernus, Barbara, Pontones, Maria, Lefeuvre-Orfila, Luz, Bendavid, Claude, Rué, Olivier, Mariadassou, Mahendra, Bonnieu, Anne, Ollendorff, Vincent, Lepage, Patricia, Derbré, Frédéric and Koechlin-Ramonatxo, Christelle. (2019) Gut bacteria are critical for optimal muscle function: A potential link with glucose homeostasis. American Journal of Physiology - Endocrinology and Metabolism. 317(1), pp. 158 - 171. https://doi.org/10.1152/ajpendo.00521.2018
AuthorsNay, Kevin, Jollet, Maxence, Goustard, Benedicte, Baati, Narjes, Vernus, Barbara, Pontones, Maria, Lefeuvre-Orfila, Luz, Bendavid, Claude, Rué, Olivier, Mariadassou, Mahendra, Bonnieu, Anne, Ollendorff, Vincent, Lepage, Patricia, Derbré, Frédéric and Koechlin-Ramonatxo, Christelle
Abstract

Gut microbiota is involved in the development of several chronic diseases, including diabetes, obesity, and cancer, through its interactions with the host organs. It has been suggested that the cross talk between gut microbiota and skeletal muscle plays a role in different pathological conditions, such as intestinal chronic inflammation and cachexia. However, it remains unclear whether gut microbiota directly influences skeletal muscle function. In this work, we studied the impact of gut microbiota modulation on mice skeletal muscle function and investigated the underlying mechanisms. We determined the consequences of gut microbiota depletion after treatment with a mixture of a broad spectrum of antibiotics for 21 days and after 10 days of natural reseeding. We found that, in gut microbiota-depleted mice, running endurance was decreased, as well as the extensor digitorum longus muscle fatigue index in an ex vivo contractile test. Importantly, the muscle endurance capacity was efficiently normalized by natural reseeding. These endurance changes were not related to variation in muscle mass, fiber typology, or mitochondrial function. However, several pertinent glucose metabolism markers, such as ileum gene expression of short fatty acid chain and glucose transporters G protein-coupled receptor 41 and sodium-glucose cotransporter 1 and muscle glycogen level, paralleled the muscle endurance changes observed after treatment with antibiotics for 21 days and reseeding. Because glycogen is a key energetic substrate for prolonged exercise, modulating its muscle availability via gut microbiota represents one potent mechanism that can contribute to the gut microbiota-skeletal muscle axis. Taken together, our results strongly support the hypothesis that gut bacteria are required for host optimal skeletal muscle function.

Keywordscontractile properties; dysbiosis; maximal aerobic velocity; mitochondrial biogenesis; muscle fatigue
Year2019
JournalAmerican Journal of Physiology - Endocrinology and Metabolism
Journal citation317 (1), pp. 158 - 171
PublisherAmerican Physiological Society
ISSN0193-1849
Digital Object Identifier (DOI)https://doi.org/10.1152/ajpendo.00521.2018
Scopus EID2-s2.0-85069296618
Page range158 - 171
Research GroupMary MacKillop Institute for Health Research
Publisher's version
File Access Level
Controlled
Place of publicationUnited States of America
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