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Article: Ruminococcus gnavus plays a pathogenic role in diarrhea-predominant irritable bowel syndrome by increasing serotonin biosynthesis

TitleRuminococcus gnavus plays a pathogenic role in diarrhea-predominant irritable bowel syndrome by increasing serotonin biosynthesis
Authors
Zhai, LHuang, CNing, ZZhang, YZhuang, MYang, WWang, XWang, JZhang, LXiao, HZhao, LAsthana, PLam, YYChow, CFWHuang, JDYuan, SChan, KMYuan, CSLau, JYWong, HLXBian, ZX
Keywordsaromatic trace amines
colonic secretion
gastrointestinal motility
gut microbiota
irritable bowel syndrome
phenethylamine
serotonin
trace amine-associated receptor 1
tryptamine
Issue Date11-Jan-2023
PublisherCell Press
Citation
Cell Host & Microbe, 2023, v. 31, n. 1, p. 33-44 How to Cite?
DOI: http://dx.doi.org/10.1016/j.chom.2022.11.006
Abstract

Diarrhea-predominant irritable bowel syndrome (IBS-D), a globally prevalent functional gastrointestinal (GI) disorder, is associated with elevated serotonin that increases gut motility. While anecdotal evidence suggests that the gut microbiota contributes to serotonin biosynthesis, mechanistic insights are limited. We determined that the bacterium Ruminococcus gnavus plays a pathogenic role in IBS-D. Monocolonization of germ-free mice with R. gnavus induced IBS-D-like symptoms, including increased GI transit and colonic secretion, by stimulating the production of peripheral serotonin. R. gnavus-mediated catabolism of dietary phenylalanine and tryptophan generated phenethylamine and tryptamine that directly stimulated serotonin biosynthesis in intestinal enterochromaffin cells via a mechanism involving activation of trace amine-associated receptor 1 (TAAR1). This R. gnavus-driven increase in serotonin levels elevated GI transit and colonic secretion but was abrogated upon TAAR1 inhibition. Collectively, our study provides molecular and pathogenetic insights into how gut microbial metabolites derived from dietary essential amino acids affect serotonin-dependent control of gut motility.


Persistent Identifierhttp://hdl.handle.net/10722/329040
ISSN
1931-3128
2023 Impact Factor: 20.6
2023 SCImago Journal Rankings: 7.760
ISI Accession Number ID
WOS:001028843700001

 

DC FieldValueLanguage
dc.contributor.authorZhai, L-
dc.contributor.authorHuang, C-
dc.contributor.authorNing, Z-
dc.contributor.authorZhang, Y-
dc.contributor.authorZhuang, M-
dc.contributor.authorYang, W-
dc.contributor.authorWang, X-
dc.contributor.authorWang, J-
dc.contributor.authorZhang, L-
dc.contributor.authorXiao, H-
dc.contributor.authorZhao, L-
dc.contributor.authorAsthana, P-
dc.contributor.authorLam, YY-
dc.contributor.authorChow, CFW-
dc.contributor.authorHuang, JD-
dc.contributor.authorYuan, S-
dc.contributor.authorChan, KM-
dc.contributor.authorYuan, CS-
dc.contributor.authorLau, JY-
dc.contributor.authorWong, HLX-
dc.contributor.authorBian, ZX-
dc.date.accessioned2023-08-05T07:54:49Z-
dc.date.available2023-08-05T07:54:49Z-
dc.date.issued2023-01-11-
dc.identifier.citationCell Host & Microbe, 2023, v. 31, n. 1, p. 33-44-
dc.identifier.issn1931-3128-
dc.identifier.urihttp://hdl.handle.net/10722/329040-
dc.description.abstract<p>Diarrhea-predominant irritable bowel syndrome (IBS-D), a globally prevalent functional gastrointestinal (GI) disorder, is associated with elevated serotonin that increases gut motility. While anecdotal evidence suggests that the <a href="https://www.sciencedirect.com/topics/immunology-and-microbiology/intestine-flora" title="Learn more about gut microbiota from ScienceDirect's AI-generated Topic Pages">gut microbiota</a> contributes to serotonin biosynthesis, mechanistic insights are limited. We determined that the bacterium <a href="https://www.sciencedirect.com/topics/immunology-and-microbiology/ruminococcus" title="Learn more about Ruminococcus from ScienceDirect's AI-generated Topic Pages">Ruminococcus</a><em> gnavus</em> plays a pathogenic role in IBS-D. Monocolonization of germ-free mice with <em>R. gnavus</em> induced IBS-D-like symptoms, including increased <a href="https://www.sciencedirect.com/topics/immunology-and-microbiology/gastrointestinal-transit" title="Learn more about GI transit from ScienceDirect's AI-generated Topic Pages">GI transit</a> and <a href="https://www.sciencedirect.com/topics/immunology-and-microbiology/colonic-secretion" title="Learn more about colonic secretion from ScienceDirect's AI-generated Topic Pages">colonic secretion</a>, by stimulating the production of peripheral serotonin. <em>R. gnavus</em>-mediated catabolism of dietary phenylalanine and tryptophan generated phenethylamine and tryptamine that directly stimulated serotonin biosynthesis in intestinal <a href="https://www.sciencedirect.com/topics/immunology-and-microbiology/enterochromaffin-cell" title="Learn more about enterochromaffin cells from ScienceDirect's AI-generated Topic Pages">enterochromaffin cells</a> via a mechanism involving activation of trace amine-associated receptor 1 (TAAR1). This <em>R. gnavus-</em>driven increase in <a href="https://www.sciencedirect.com/topics/immunology-and-microbiology/serotonin-level" title="Learn more about serotonin levels from ScienceDirect's AI-generated Topic Pages">serotonin levels</a> elevated <a href="https://www.sciencedirect.com/topics/immunology-and-microbiology/gastrointestinal-transit" title="Learn more about GI transit from ScienceDirect's AI-generated Topic Pages">GI transit</a> and <a href="https://www.sciencedirect.com/topics/immunology-and-microbiology/colonic-secretion" title="Learn more about colonic secretion from ScienceDirect's AI-generated Topic Pages">colonic secretion</a> but was abrogated upon TAAR1 inhibition. Collectively, our study provides molecular and pathogenetic insights into how gut microbial metabolites derived from dietary essential amino acids affect serotonin-dependent control of gut motility.<br></p>-
dc.languageeng-
dc.publisherCell Press-
dc.relation.ispartofCell Host & Microbe-
dc.rightsThis work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.-
dc.subjectaromatic trace amines-
dc.subjectcolonic secretion-
dc.subjectgastrointestinal motility-
dc.subjectgut microbiota-
dc.subjectirritable bowel syndrome-
dc.subjectphenethylamine-
dc.subjectserotonin-
dc.subjecttrace amine-associated receptor 1-
dc.subjecttryptamine-
dc.titleRuminococcus gnavus plays a pathogenic role in diarrhea-predominant irritable bowel syndrome by increasing serotonin biosynthesis-
dc.typeArticle-
dc.identifier.doi10.1016/j.chom.2022.11.006-
dc.identifier.scopuseid_2-s2.0-85146006778-
dc.identifier.volume31-
dc.identifier.issue1-
dc.identifier.spage33-
dc.identifier.epage44-
dc.identifier.eissn1934-6069-
dc.identifier.isiWOS:001028843700001-
dc.identifier.issnl1931-3128-

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