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Discrete role for maternal stress and gut microbes in shaping maternal and offspring immunity

Psychosocial stress is prevalent during pregnancy, and is associated with immune dysfunction, both for the mother and the child. The gut microbiome has been implicated as a potential mechanism by which stress during pregnancy can impact both maternal and offspring immune function; however, the compl...

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Autores principales: Chen, Helen J., Bischoff, Allison, Galley, Jeffrey D., Peck, Lauren, Bailey, Michael T., Gur, Tamar L.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Elsevier 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9755033/
https://www.ncbi.nlm.nih.gov/pubmed/36532381
http://dx.doi.org/10.1016/j.ynstr.2022.100480
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author Chen, Helen J.
Bischoff, Allison
Galley, Jeffrey D.
Peck, Lauren
Bailey, Michael T.
Gur, Tamar L.
author_facet Chen, Helen J.
Bischoff, Allison
Galley, Jeffrey D.
Peck, Lauren
Bailey, Michael T.
Gur, Tamar L.
author_sort Chen, Helen J.
collection PubMed
description Psychosocial stress is prevalent during pregnancy, and is associated with immune dysfunction, both for the mother and the child. The gut microbiome has been implicated as a potential mechanism by which stress during pregnancy can impact both maternal and offspring immune function; however, the complex interplay between the gut microbiome and the immune system is not well-understood. Here, we leverage a model of antimicrobial-mediated gut microbiome reduction, in combination with a well-established model of maternal restraint stress, to investigate the independent effects of and interaction between maternal stress and the gut microbiome in shaping maternal and offspring immunity. First, we confirmed that the antimicrobial treatment reduced maternal gut bacterial load and altered fecal alpha and beta diversity, with a reduction in commensal microbes and an increase in the relative abundance of rare taxa. Prenatal stress also disrupted the gut microbiome, according to measures of both alpha and beta diversity. Furthermore, prenatal stress and antimicrobials independently induced systemic and gastrointestinal immune suppression in the dam with a concomitant increase in circulating corticosterone. While stress increased neutrophils in the maternal circulation, lymphoid cells and monocytes were not impacted by either stress or antimicrobial treatment. Although the fetal immune compartment was largely spared, stress increased circulating neutrophils and CD8 T cells, and antibiotics increased neutrophils and reduced T cells in the adult offspring. Altogether, these data indicate similar, but discrete, roles for maternal stress and gut microbes in influencing maternal and offspring immune function.
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spelling pubmed-97550332022-12-17 Discrete role for maternal stress and gut microbes in shaping maternal and offspring immunity Chen, Helen J. Bischoff, Allison Galley, Jeffrey D. Peck, Lauren Bailey, Michael T. Gur, Tamar L. Neurobiol Stress Original Research Article Psychosocial stress is prevalent during pregnancy, and is associated with immune dysfunction, both for the mother and the child. The gut microbiome has been implicated as a potential mechanism by which stress during pregnancy can impact both maternal and offspring immune function; however, the complex interplay between the gut microbiome and the immune system is not well-understood. Here, we leverage a model of antimicrobial-mediated gut microbiome reduction, in combination with a well-established model of maternal restraint stress, to investigate the independent effects of and interaction between maternal stress and the gut microbiome in shaping maternal and offspring immunity. First, we confirmed that the antimicrobial treatment reduced maternal gut bacterial load and altered fecal alpha and beta diversity, with a reduction in commensal microbes and an increase in the relative abundance of rare taxa. Prenatal stress also disrupted the gut microbiome, according to measures of both alpha and beta diversity. Furthermore, prenatal stress and antimicrobials independently induced systemic and gastrointestinal immune suppression in the dam with a concomitant increase in circulating corticosterone. While stress increased neutrophils in the maternal circulation, lymphoid cells and monocytes were not impacted by either stress or antimicrobial treatment. Although the fetal immune compartment was largely spared, stress increased circulating neutrophils and CD8 T cells, and antibiotics increased neutrophils and reduced T cells in the adult offspring. Altogether, these data indicate similar, but discrete, roles for maternal stress and gut microbes in influencing maternal and offspring immune function. Elsevier 2022-09-28 /pmc/articles/PMC9755033/ /pubmed/36532381 http://dx.doi.org/10.1016/j.ynstr.2022.100480 Text en © 2022 The Authors https://creativecommons.org/licenses/by-nc-nd/4.0/This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
spellingShingle Original Research Article
Chen, Helen J.
Bischoff, Allison
Galley, Jeffrey D.
Peck, Lauren
Bailey, Michael T.
Gur, Tamar L.
Discrete role for maternal stress and gut microbes in shaping maternal and offspring immunity
title Discrete role for maternal stress and gut microbes in shaping maternal and offspring immunity
title_full Discrete role for maternal stress and gut microbes in shaping maternal and offspring immunity
title_fullStr Discrete role for maternal stress and gut microbes in shaping maternal and offspring immunity
title_full_unstemmed Discrete role for maternal stress and gut microbes in shaping maternal and offspring immunity
title_short Discrete role for maternal stress and gut microbes in shaping maternal and offspring immunity
title_sort discrete role for maternal stress and gut microbes in shaping maternal and offspring immunity
topic Original Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9755033/
https://www.ncbi.nlm.nih.gov/pubmed/36532381
http://dx.doi.org/10.1016/j.ynstr.2022.100480
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