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Social Stress Affects Colonic Inflammation, the Gut Microbiome, and Short-chain Fatty Acid Levels and Receptors.

ABSTRACT: OBJECTIVES:Gastrointestinal disorders, such as inflammatory bowel diseases (IBDs) and functional gastrointestinal disorders (FGIDs), involve disrupted homeostatic interactions between the microbiota and the host. Both disorders are worsened during stress, and in laboratory mice, stress exposure has been shown to change the composition of the gut microbiome. Stress-induced changes to the microbiome exacerbate intestinal inflammation and alter intestinal motility in mice. It is, however, not yet known whether microbiota-derived short-chain fatty acids (butyrate, propionate, and acetate) and their receptors contribute to this effect. METHODS:Mice were exposed to a social disruption stress, or left undisturbed as a control. After the first stress exposure, mice were orally challenged with Citrobacter rodentium or with vehicle. The levels of short-chain fatty acids (SCFAs) were measured using gas chromatography-mass spectrometry. SCFA receptors were measured via real-time polymerase chain reaction. Microbial community composition was assessed using 16S rRNA gene sequencing. RESULTS:Stress exposure reduced colonic SCFA levels. Stress exposure and C rodentium, however, significantly increased SCFA levels and changed the expression of SCFA receptors. The levels of SCFAs did not correlate with the severity of colonic inflammation, but the colonic expression of the SCFA receptor GPR41 was positively associated with inflammatory cytokines and colonic histopathology scores. The relative abundances of several taxa of colonic bacteria were significantly changed by stress exposure, including SCFA producers. CONCLUSIONS:Social stress can have a significant effect on infection-induced colonic inflammation, and stress-induced changes in microbial-produced metabolites and their receptors may be involved.

SUBMITTER: Maltz RM

PROVIDER: S-EPMC6428608 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Social Stress Affects Colonic Inflammation, the Gut Microbiome, and Short-chain Fatty Acid Levels and Receptors.

Maltz Ross M RM Keirsey Jeremy J Kim Sandra C SC Mackos Amy R AR Gharaibeh Raad Z RZ Moore Cathy C CC Xu Jinyu J Somogyi Arpad A Bailey Michael T MT

Journal of pediatric gastroenterology and nutrition 20190401 4

<h4>Objectives</h4>Gastrointestinal disorders, such as inflammatory bowel diseases (IBDs) and functional gastrointestinal disorders (FGIDs), involve disrupted homeostatic interactions between the microbiota and the host. Both disorders are worsened during stress, and in laboratory mice, stress exposure has been shown to change the composition of the gut microbiome. Stress-induced changes to the microbiome exacerbate intestinal inflammation and alter intestinal motility in mice. It is, however, n ...[more]

PMID: 30540706

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Project description:ObjectiveTo determine the longer-term effects of metformin treatment and behavioral weight loss on gut microbiota and short-chain fatty acids (SCFAs).Research design and methodsWe conducted a 3-parallel-arm, randomized trial. We enrolled overweight/obese adults who had been treated for solid tumors but had no ongoing cancer treatment and randomized them (n = 121) to either 1) metformin (up to 2,000 mg), 2) coach-directed behavioral weight loss, or 3) self-directed care (control) for 12 months. We collected stool and serum at baseline (n = 114), 6 months (n = 109), and 12 months (n = 105). From stool, we extracted microbial DNA and conducted amplicon and metagenomic sequencing. We measured SCFAs and other biochemical parameters from fasting serum.ResultsOf the 121 participants, 79% were female and 46% were Black, and the mean age was 60 years. Only metformin treatment significantly altered microbiota composition. Compared with control, metformin treatment increased amplicon sequence variants for Escherichia (confirmed as Escherichia coli by metagenomic sequencing) and Ruminococcus torques and decreased Intestinibacter bartlettii at both 6 and 12 months and decreased the genus Roseburia, including R. faecis and R. intestinalis, at 12 months. Effects were similar in comparison of the metformin group with the behavioral weight loss group. Metformin versus control also increased butyrate, acetate, and valerate at 6 months (but not at 12 months). Behavioral weight loss versus control did not significantly alter microbiota composition but did increase acetate at 6 months (but not at 12 months). Increases in acetate were associated with decreases in fasting insulin. Additional whole genome metagenomic sequencing of a subset of the metformin group showed that metformin altered 62 metagenomic functional pathways, including an acetate producing pathway and three pathways in glucose metabolism.ConclusionsMetformin, but not behavioral weight loss, impacted gut microbiota composition at 6 months and 12 months. Both metformin and behavioral weight loss altered circulating SCFAs at 6 months, including increasing acetate, which correlated with lower fasting insulin. Future research is needed to elucidate whether the gut microboime mediates or modifies metformin's health effects.

Project description:BACKGROUND:While some of the variance observed in adiposity and weight change within populations can be accounted for by traditional risk factors, a new factor, the gut microbiota, has recently been associated with obesity. However, the causal mechanisms through which the gut microbiota and its metabolites, short chain fatty acids (SCFAs) influence obesity are unknown, as are the individual obesogenic effects of the individual SCFAs (butyrate, acetate and propionate). This study, METS-Microbiome, proposes to examine the influence of novel risk factors, the gut microbiota and SCFAs, on obesity, adiposity and weight change in an international established cohort spanning the epidemiologic transition. METHODS:The parent study; Modeling the Epidemiologic Transition Study (METS) is a well-established and ongoing prospective cohort study designed to assess the association between body composition, physical activity, and relative weight, weight gain and cardiometabolic disease risk in five diverse population-based samples in 2500 people of African descent. The cohort has been prospectively followed since 2009. Annual measures of obesity risk factors, including body composition, objectively measured physical activity and dietary intake, components which vary across the spectrum of social and economic development. In our new study; METS-Microbiome, in addition to continuing yearly measures of obesity risk, we will also measure gut microbiota and stool SCFAs in all contactable participants, and follow participants for a further 3 years, thus providing one of the largest gut microbiota population-based studies to date. DISCUSSION:This new study capitalizes upon an existing, extensively well described cohort of adults of African-origin, with significant variability as a result of the widespread geographic distributions, and therefore variation in the environmental covariate exposures. The METS-Microbiome study will substantially advance the understanding of the role gut microbiota and SCFAs play in the development of obesity and provide novel obesity therapeutic targets targeting SCFAs producing features of the gut microbiota. TRIAL REGISTRATION:Registered NCT03378765 Date first posted: December 20, 2017.

Dataset Information

Social Stress Affects Colonic Inflammation, the Gut Microbiome, and Short-chain Fatty Acid Levels and Receptors.

Publications

Social Stress Affects Colonic Inflammation, the Gut Microbiome, and Short-chain Fatty Acid Levels and Receptors.

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