Physical Activity Shapes the Intestinal Microbiome and Immunity of Healthy Mice but Has No Protective Effects against Colitis in MUC2<sup>−/−</sup> Mice

ABSTRACT The interactions among humans, their environment, and the trillions of microbes residing within the human intestinal tract form a tripartite relationship that is fundamental to the overall health of the host. Disruptions in the delicate balance between the intestinal microbiota and host imm...

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Autores principales:	Mehrbod Estaki, Douglas W. Morck, Sanjoy Ghosh, Candice Quin, Jason Pither, Jacqueline A. Barnett, Sandeep K. Gill, Deanna L. Gibson
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	IBD colitis exercise inflammatory bowel disease microbiome mucin Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d0eacc14e3124d89848915442d1074f4
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spelling	oai:doaj.org-article:d0eacc14e3124d89848915442d1074f42021-12-02T19:47:36ZPhysical Activity Shapes the Intestinal Microbiome and Immunity of Healthy Mice but Has No Protective Effects against Colitis in MUC2<sup>−/−</sup> Mice10.1128/mSystems.00515-202379-5077https://doaj.org/article/d0eacc14e3124d89848915442d1074f42020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00515-20https://doaj.org/toc/2379-5077ABSTRACT The interactions among humans, their environment, and the trillions of microbes residing within the human intestinal tract form a tripartite relationship that is fundamental to the overall health of the host. Disruptions in the delicate balance between the intestinal microbiota and host immunity are implicated in various chronic diseases, including inflammatory bowel disease (IBD). There is no known cure for IBD; therefore, novel therapeutics targeting prevention and symptom management are of great interest. Recently, physical activity in healthy mice was shown to be protective against chemically induced colitis; however, the benefits of physical activity during or following disease onset are not known. In this study, we examine whether voluntary wheel running is protective against primary disease symptoms in a mucin 2-deficient (Muc2−/−) lifelong model of murine colitis. We show that 6 weeks of wheel running in healthy C57BL/6 mice leads to distinct changes in fecal bacteriome, increased butyrate production, and modulation in colonic gene expression of various cytokines, suggesting an overall primed anti-inflammatory state. However, these physical activity-derived benefits are not present in Muc2−/− mice harboring a dysfunctional mucosal layer from birth, ultimately showing no improvements in clinical signs. We extrapolate from our findings that while physical activity in healthy individuals may be an important preventative measure against IBD, for those with a compromised intestinal mucosa, a commonality in IBD patients, these benefits are lost. IMPORTANCE Perturbation in the gut microbial ecosystem has been associated with various diseases, including inflammatory bowel disease. Habitual physical activity, through its ability to modulate the gut microbiome, has recently been shown to prophylactically protect against chemically induced models of murine colitis. Here, we (i) confirm previous reports that physical activity has limited but significant effects on the gut microbiome of mice and (ii) show that such changes are associated with anti-inflammatory states in the gut, such as increased production of beneficial short-chain fatty acids and lower levels of proinflammatory immune markers implicated in human colitis; however, we also show that (iii) these physical activity-derived benefits are completely lost in the absence of a healthy intestinal mucus layer, a hallmark phenotype of human colitis.Mehrbod EstakiDouglas W. MorckSanjoy GhoshCandice QuinJason PitherJacqueline A. BarnettSandeep K. GillDeanna L. GibsonAmerican Society for MicrobiologyarticleIBDcolitisexerciseinflammatory bowel diseasemicrobiomemucinMicrobiologyQR1-502ENmSystems, Vol 5, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	IBD colitis exercise inflammatory bowel disease microbiome mucin Microbiology QR1-502
spellingShingle	IBD colitis exercise inflammatory bowel disease microbiome mucin Microbiology QR1-502 Mehrbod Estaki Douglas W. Morck Sanjoy Ghosh Candice Quin Jason Pither Jacqueline A. Barnett Sandeep K. Gill Deanna L. Gibson Physical Activity Shapes the Intestinal Microbiome and Immunity of Healthy Mice but Has No Protective Effects against Colitis in MUC2<sup>−/−</sup> Mice
description	ABSTRACT The interactions among humans, their environment, and the trillions of microbes residing within the human intestinal tract form a tripartite relationship that is fundamental to the overall health of the host. Disruptions in the delicate balance between the intestinal microbiota and host immunity are implicated in various chronic diseases, including inflammatory bowel disease (IBD). There is no known cure for IBD; therefore, novel therapeutics targeting prevention and symptom management are of great interest. Recently, physical activity in healthy mice was shown to be protective against chemically induced colitis; however, the benefits of physical activity during or following disease onset are not known. In this study, we examine whether voluntary wheel running is protective against primary disease symptoms in a mucin 2-deficient (Muc2−/−) lifelong model of murine colitis. We show that 6 weeks of wheel running in healthy C57BL/6 mice leads to distinct changes in fecal bacteriome, increased butyrate production, and modulation in colonic gene expression of various cytokines, suggesting an overall primed anti-inflammatory state. However, these physical activity-derived benefits are not present in Muc2−/− mice harboring a dysfunctional mucosal layer from birth, ultimately showing no improvements in clinical signs. We extrapolate from our findings that while physical activity in healthy individuals may be an important preventative measure against IBD, for those with a compromised intestinal mucosa, a commonality in IBD patients, these benefits are lost. IMPORTANCE Perturbation in the gut microbial ecosystem has been associated with various diseases, including inflammatory bowel disease. Habitual physical activity, through its ability to modulate the gut microbiome, has recently been shown to prophylactically protect against chemically induced models of murine colitis. Here, we (i) confirm previous reports that physical activity has limited but significant effects on the gut microbiome of mice and (ii) show that such changes are associated with anti-inflammatory states in the gut, such as increased production of beneficial short-chain fatty acids and lower levels of proinflammatory immune markers implicated in human colitis; however, we also show that (iii) these physical activity-derived benefits are completely lost in the absence of a healthy intestinal mucus layer, a hallmark phenotype of human colitis.
format	article
author	Mehrbod Estaki Douglas W. Morck Sanjoy Ghosh Candice Quin Jason Pither Jacqueline A. Barnett Sandeep K. Gill Deanna L. Gibson
author_facet	Mehrbod Estaki Douglas W. Morck Sanjoy Ghosh Candice Quin Jason Pither Jacqueline A. Barnett Sandeep K. Gill Deanna L. Gibson
author_sort	Mehrbod Estaki
title	Physical Activity Shapes the Intestinal Microbiome and Immunity of Healthy Mice but Has No Protective Effects against Colitis in MUC2<sup>−/−</sup> Mice
title_short	Physical Activity Shapes the Intestinal Microbiome and Immunity of Healthy Mice but Has No Protective Effects against Colitis in MUC2<sup>−/−</sup> Mice
title_full	Physical Activity Shapes the Intestinal Microbiome and Immunity of Healthy Mice but Has No Protective Effects against Colitis in MUC2<sup>−/−</sup> Mice
title_fullStr	Physical Activity Shapes the Intestinal Microbiome and Immunity of Healthy Mice but Has No Protective Effects against Colitis in MUC2<sup>−/−</sup> Mice
title_full_unstemmed	Physical Activity Shapes the Intestinal Microbiome and Immunity of Healthy Mice but Has No Protective Effects against Colitis in MUC2<sup>−/−</sup> Mice
title_sort	physical activity shapes the intestinal microbiome and immunity of healthy mice but has no protective effects against colitis in muc2<sup>−/−</sup> mice
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/d0eacc14e3124d89848915442d1074f4
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Physical Activity Shapes the Intestinal Microbiome and Immunity of Healthy Mice but Has No Protective Effects against Colitis in MUC2<sup>−/−</sup> Mice

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