Prenatal stress affects placental cytokines and neurotrophins, commensal microbes, and anxiety-like behavior in adult female offspring
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.
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Female offspring displayed increased cognitive deficits and anxiety-like behavior following prenatal stress, which were associated with gut microbiota alterations in pregnant females and increased IL-1β and decreased BDNF levels in utero.
“Female offspring displayed increased cognitive deficits and anxiety-like behavior following prenatal stress, which were associated with GM alterations in the pregnant females and increased IL-1β and decreased BDNF levels in utero (381).”
From Signalling cognition: The gut microbiota and hypothalamic-pituitary-adrenal axis (2023) · cites this paper as [381]
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Self-citation
- Authors
- Gur, T. L., Shay, L., Palkar, A. V., Fisher, S., Varaljay, V. A., Dowd, S., & Bailey, M. T.
- Affiliations
- The Ohio State University Wexner Medical Center (US)
- Nationwide Children's Hospital (US)
- Corresponding author
- Gur, Tamar L.
- Venue
- Brain, Behavior, and Immunity
- Publisher
- Elsevier BV
- Published
- 2017-08
- Volume
- 64
- Pages
- 50-58
- ISSN
- 0889-1591 (ISSN-L)
- OpenAlex
- W2561533004
- Cited by
- 213
- References
- 68
- Citations by year
- 2026: 17 · 2025: 17 · 2024: 30 · 2023: 25 · 2022: 23 · 2021: 27 · 2020: 22 · 2019: 23 · 2018: 22 · 2017: 7
- FWCI
- 17.19
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- Brain Behavior and Immunity (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Alliance for Research on Schizophrenia and Depression
- March of Dimes Prematurity Research Center Ohio Collaborative
- Brain and Behavior Research Foundation
- Ohio State University
- Topics
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- prenatal stress, placenta, cytokines, IL-1β, brain-derived neurotrophic factor, neurotrophins, gut microbiota, commensal microorganisms, anxiety-like behavior, maternal stress, female offspring, amygdala, brain development, cognition, mother-to-child transmission
- MeSH terms
- Gastrointestinal Microbiome, Animals, Anxiety, Encephalitis, Female, Inflammation, Mice, Inbred C57BL, Nerve Growth Factors, Placenta, Pregnancy, Pregnancy Complications, Prenatal Exposure Delayed Effects, Stress, Psychological, Symbiosis, Cytokines, Inflammation Mediators, Brain-Derived Neurotrophic Factor, Interleukin-1beta
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