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

被引:11
作者
Chen, Helen J. [1 ,2 ,3 ,4 ]
Bischoff, Allison [1 ]
Galley, Jeffrey D. [1 ,2 ]
Peck, Lauren [1 ,5 ]
Bailey, Michael T. [1 ,6 ,7 ]
Gur, Tamar L. [1 ,2 ,3 ,4 ,8 ,9 ,10 ]
机构
[1] Ohio State Univ, Wexner Med Ctr, Inst Behav Med Res, Columbus, OH USA
[2] Ohio State Univ, Wexner Med Ctr, Dept Psychiat & Behav Hlth, Columbus, OH USA
[3] Ohio State Univ, Wexner Med Ctr, Dept Neurosci, Columbus, OH USA
[4] Ohio State Univ, Med Scientist Training Program, Columbus, OH USA
[5] Ohio State Univ, Coll Med, Columbus, OH USA
[6] Nationwide Childrens Hosp, Res Inst, Ctr Microbial Pathogenesis, Columbus, OH USA
[7] Ohio State Univ, Coll Dent, Biosci Div, Columbus, OH USA
[8] Ohio State Univ, Wexner Med Ctr, Dept Pediat, Columbus, OH USA
[9] Ohio State Univ, Wexner Med Ctr, Dept Obstet & Gynecol, Columbus, OH USA
[10] 120A Inst Behav Med Res Bldg,460 Med Ctr Dr, Columbus, OH 43210 USA
关键词
Prenatal stress; Microbiome; Antibiotics; Antifungals; Antimicrobials; Immune; PRENATAL STRESS; INTESTINAL MICROBIOTA; CORTICOSTERONE; PREGNANCY; ANTIBIOTICS; EXPOSURE; RISK; COLONIZATION; BEHAVIOR; CONSEQUENCES;
D O I
10.1016/j.ynstr.2022.100480
中图分类号
Q189 [神经科学];
学科分类号
071006 ;
摘要
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.
引用
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页数:14
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共 89 条
[1]   Toll-like receptors and their role in the trophoblast [J].
Abrahams, VM ;
Mor, G .
PLACENTA, 2005, 26 (07) :540-547
[2]   The intestinal microbiota are necessary for stressor-induced enhancement of splenic macrophage microbicidal activity [J].
Allen, Rebecca G. ;
Lafuse, William P. ;
Galley, Jeffrey D. ;
Ali, Mohamed M. ;
Ahmer, Brian M. M. ;
Bailey, Michael T. .
BRAIN BEHAVIOR AND IMMUNITY, 2012, 26 (03) :371-382
[3]   Unique maternal immune and functional microbial profiles during prenatal stress [J].
Antonson, Adrienne M. ;
Evans, Morgan, V ;
Galley, Jeffrey D. ;
Chen, Helen J. ;
Rajasekera, Therese A. ;
Lammers, Sydney M. ;
Hale, Vanessa L. ;
Bailey, Michael T. ;
Gur, Tamar L. .
SCIENTIFIC REPORTS, 2020, 10 (01)
[4]   Exposure to a social stressor alters the structure of the intestinal microbiota: Implications for stressor-induced immunomodulation [J].
Bailey, Michael T. ;
Dowd, Scot E. ;
Galley, Jeffrey D. ;
Hufnagle, Amy R. ;
Allen, Rebecca G. ;
Lyte, Mark .
BRAIN BEHAVIOR AND IMMUNITY, 2011, 25 (03) :397-407
[5]   Prenatal stress alters bacterial colonization of the gut in infant monkeys [J].
Bailey, MT ;
Lubach, GR ;
Coe, CL .
JOURNAL OF PEDIATRIC GASTROENTEROLOGY AND NUTRITION, 2004, 38 (04) :414-421
[6]   Early Life Programming and Neurodevelopmental Disorders [J].
Bale, Tracy L. ;
Baram, Tallie Z. ;
Brown, Alan S. ;
Goldstein, Jill M. ;
Insel, Thomas R. ;
McCarthy, Margaret M. ;
Nemeroff, Charles B. ;
Reyes, Teresa M. ;
Simerly, Richard B. ;
Susser, Ezra S. ;
Nestler, Eric J. .
BIOLOGICAL PSYCHIATRY, 2010, 68 (04) :314-319
[7]   Maternal corticosterone in the mouse alters oxidative stress markers, antioxidant function and mitochondrial content in placentas of female fetuses [J].
Bartho, Lucy A. ;
Holland, Olivia J. ;
Moritz, Karen M. ;
Perkins, Anthony V. ;
Cuffe, James S. M. .
JOURNAL OF PHYSIOLOGY-LONDON, 2019, 597 (12) :3053-3067
[8]   Intestinal Fungal Dysbiosis Is Associated With Visceral Hypersensitivity in Patients With Irritable Bowel Syndrome and Rats [J].
Botschuijver, Sara ;
Roeselers, Guus ;
Levin, Evgeni ;
Jonkers, Daisy M. ;
Welting, Olaf ;
Heinsbroek, Sigrid E. M. ;
de Weerd, Heleen H. ;
Boekhout, Teun ;
Fornai, Matteo ;
Masclee, Ad A. ;
Schuren, Frank H. J. ;
de Jonge, Wouter J. ;
Seppen, Jurgen ;
Van den Wijngaard, Rene M. .
GASTROENTEROLOGY, 2017, 153 (04) :1026-1039
[9]   Stressor-specific alterations in corticosterone and immune responses in mice [J].
Bowers, Stephanie L. ;
Bilbo, Staci D. ;
Dhabhar, Firdaus S. ;
Nelson, Randy J. .
BRAIN BEHAVIOR AND IMMUNITY, 2008, 22 (01) :105-113
[10]  
Callahan BJ, 2016, NAT METHODS, V13, P581, DOI [10.1038/NMETH.3869, 10.1038/nmeth.3869]