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Brain Behav Immun. 2017 Aug;64:50-58. doi: 10.1016/j.bbi.2016.12.021. Epub 2016 Dec 24.

Prenatal stress affects placental cytokines and neurotrophins, commensal microbes, and anxiety-like behavior in adult female offspring.

Author information

1
Department of Psychiatry & Behavioral Health, Wexner Medical Center at The Ohio State University, United States; Department of Neuroscience, Wexner Medical Center at The Ohio State University, United States; Department of Obstetrics & Gynecology, Wexner Medical Center at The Ohio State University, United States; Institute for Behavioral Medicine Research, Wexner Medical Center at The Ohio State University, United States. Electronic address: tamar.gur@osumc.edu.
2
Department of Psychiatry & Behavioral Health, Wexner Medical Center at The Ohio State University, United States.
3
Department of Psychiatry & Behavioral Health, Wexner Medical Center at The Ohio State University, United States; Institute for Behavioral Medicine Research, Wexner Medical Center at The Ohio State University, United States.
4
Department of Psychiatry & Behavioral Health, Wexner Medical Center at The Ohio State University, United States; Institute for Behavioral Medicine Research, Wexner Medical Center at The Ohio State University, United States; Center for Microbial Pathogenesis, The Research Institute, Nationwide Children's Hospital, The Ohio State University, United States.
5
Center for Microbial Pathogenesis, The Research Institute, Nationwide Children's Hospital, The Ohio State University, United States; Biosciences Division, College of Dentistry, The Ohio State University, United States; Department of Pediatrics, Wexner Medical Center at The Ohio State University, United States.
6
Research and Testing Laboratory and Medical Biofilm Research Institute, Lubbock, TX 79407, United States.
7
Institute for Behavioral Medicine Research, Wexner Medical Center at The Ohio State University, United States; Center for Microbial Pathogenesis, The Research Institute, Nationwide Children's Hospital, The Ohio State University, United States; Biosciences Division, College of Dentistry, The Ohio State University, United States; Department of Pediatrics, Wexner Medical Center at The Ohio State University, United States.

Abstract

Recent studies demonstrate that exposure to stress changes the composition of the intestinal microbiota, which is associated with development of stress-induced changes to social behavior, anxiety, and depression. Stress during pregnancy has also been related to the emergence of these disorders; whether commensal microbes are part of a maternal intrauterine environment during prenatal stress is not known. Here, we demonstrate that microbiome changes are manifested in the mother, and also found in female offspring in adulthood, with a correlation between stressed mothers and female offspring. Alterations in the microbiome have been shown to alter immune responses, thus we examined cytokines in utero. IL-1β was increased in placenta and fetal brain from offspring exposed to the prenatal stressor. Because IL-1β has been shown to prevent induction of brain derived neurotrophic factor (BDNF), we examined BDNF and found a reduction in female placenta and adult amygdala, suggesting in utero impact on neurodevelopment extending into adulthood. Furthermore, gastrointestinal microbial communities were different in adult females born from stressed vs. non-stressed pregnancies. Adult female offspring also demonstrated increased anxiety-like behavior and alterations in cognition, suggesting a critical window where stress is able to influence the microbiome and the intrauterine environment in a deleterious manner with lasting behavioral consequences. The microbiome may be a key link between the intrauterine environment and adult behavioral changes.

KEYWORDS:

Anxiety-like behavior; Gut–brain axis; Microbiota; Placenta; Prenatal stress

PMID:
28027927
DOI:
10.1016/j.bbi.2016.12.021
[Indexed for MEDLINE]

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