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The gut microbiota metabolite indole increases emotional responses and adrenal medulla activity in chronically stressed male mice

dc.rights.licenseopenen_US
dc.contributor.authorMIR, Hayatte-Dounia
dc.contributor.authorMILMAN, Alexandre
dc.contributor.authorMONNOYE, Magali
dc.contributor.authorDOUARD, Veronique
dc.contributor.authorPHILIPPE, Catherine
hal.structure.identifierNutrition et Neurobiologie intégrée [NutriNeuro]
dc.contributor.authorAUBERT, Agnes
hal.structure.identifierNutrition et Neurobiologie intégrée [NutriNeuro]
dc.contributor.authorCASTANON, Nathalie
hal.structure.identifierNutrition et Neurobiologie intégrée [NutriNeuro]
dc.contributor.authorVANCASSEL, Sylvie
dc.contributor.authorGUERINEAU, Nathalie C.
dc.contributor.authorNAUDON, Laurent
dc.contributor.authorRABOT, Sylvie
dc.date.accessioned2021-09-21T07:23:12Z
dc.date.available2021-09-21T07:23:12Z
dc.date.issued2020-06-05
dc.identifier.issn0306-4530en_US
dc.identifier.urihttps://oskar-bordeaux.fr/handle/20.500.12278/112263
dc.description.abstractEnBackground and aims: The gut microbiota produces metabolites that are an integral part of the metabolome and, as such, of the host physiology. Changes in gut microbiota metabolism could therefore contribute to pathophysiological processes. We showed previously that a chronic and moderate overproduction of indole from tryptophan in male individuals of the highly stress-sensitive F344 rat strain induced anxiety-like and helplessness behaviors. The aim of the present study was to extend the scope of these findings by investigating whether emotional behaviors of male mice that are moderately stress-sensitive but chronically exposed to environmental stressors would also be affected by indole.Methods: We colonized germ-free male C3H/HeN mice with a wild-type indole-producing Escherichia coli strain, or with the non-indole producing mutant. Gnotobiotic mice were subjected to an unpredictable chronic mild stress procedure, then to a set of tests aimed at assessing anxiety-like (novelty and elevated plus maze tests) and depression-like behaviors (coat state, splash, nesting, tail suspension and sucrose tests). Results of the individual tests were aggregated into a common z-score to estimate the overall emotional response to chronic mild stress and chronic indole production. We also carried out biochemical and molecular analyses in gut mucosa, plasma, brain hippocampus and striatum, and adrenal glands, to examine biological correlates that are usually associated with stress, anxiety and depression.Results: Chronic mild stress caused coat state degradation and anhedonia in both indole-producing and non-indole producing mice, but it did not influence behaviors in the other tests. Chronic indole production did not influence mice behavior when tests were considered individually, but it increased the overall emotionality z-score, specifically in mice under chronic mild stress. Interestingly, in the same mice, indole induced a dramatic increase of the expression of the adrenomedullary Pnmt gene, which is involved in catecholamine biosynthesis. By contrast, systemic tryptophan bioavailability, brain serotonin and dopamine levels and turnover, as well as expression of gut and brain genes involved in cytokine production and tryptophan metabolism along the serotonin and kynurenine pathways, remained similar in all mice.Conclusions: Chronic indole production by the gut microbiota increased the vulnerability of male mice to the adverse effects of chronic mild stress on emotional behaviors. It also targeted catecholamine biosynthetic pathway of the adrenal medulla, which plays a pivotal role in body's physiological adaptation to stressful events. Future studies will aim to investigate the action mechanisms responsible for these effects.
dc.language.isoENen_US
dc.subject.enAdrenal medulla
dc.subject.enAnxiety
dc.subject.enCatecholamines
dc.subject.enChromaffin cells
dc.subject.enDepression
dc.subject.enGnotobiotic
dc.subject.enTryptophan
dc.title.enThe gut microbiota metabolite indole increases emotional responses and adrenal medulla activity in chronically stressed male mice
dc.typeArticle de revueen_US
dc.identifier.doi10.1016/j.psyneuen.2020.104750en_US
dc.subject.halSciences du Vivant [q-bio]/Neurosciences [q-bio.NC]en_US
dc.identifier.pubmed32569990en_US
bordeaux.journalPsychoneuroendocrinologyen_US
bordeaux.page1-10en_US
bordeaux.volume119en_US
bordeaux.hal.laboratoriesNutriNeurO (Laboratoire de Nutrition et Neurobiologie Intégrée) - UMR 1286en_US
bordeaux.institutionUniversité de Bordeauxen_US
bordeaux.institutionINRAEen_US
bordeaux.teamPsychoneuroimmunologie et Nutrition: Approches expérimentales et cliniquesen_US
bordeaux.peerReviewedouien_US
bordeaux.inpressnonen_US
bordeaux.identifier.funderIDFondation de Franceen_US
bordeaux.identifier.funderIDInstitut National de la Recherche Agronomiqueen_US
hal.exportfalse
dc.rights.ccPas de Licence CCen_US
bordeaux.COinSctx_ver=Z39.88-2004&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.jtitle=Psychoneuroendocrinology&rft.date=2020-06-05&rft.volume=119&rft.spage=1-10&rft.epage=1-10&rft.eissn=0306-4530&rft.issn=0306-4530&rft.au=MIR,%20Hayatte-Dounia&MILMAN,%20Alexandre&MONNOYE,%20Magali&DOUARD,%20Veronique&PHILIPPE,%20Catherine&rft.genre=article


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