Impact of prenatal maternal cytokine exposure on sex differences in brain circuitry regulating stress in offspring 45 years later
Open accessAbstract
Stress is associated with numerous chronic diseases, beginning in fetal development with in utero exposures (prenatal stress) impacting offspring's risk for disorders later in life. In previous studies, we demonstrated adverse maternal in utero immune activity on sex differences in offspring neurodevelopment at age seven and adult risk for major depression and psychoses. Here, we hypothesized that in utero exposure to maternal proinflammatory cytokines has sex-dependent effects on specific brain circuitry regulating stress and immune function in the offspring that are retained across the lifespan. Using a unique prenatal cohort, we tested this hypothesis in 80 adult offspring, equally divided by sex, followed from in utero development to midlife. Functional MRI results showed that exposure to proinflammatory cytokines in utero was significantly associated with sex differences in brain activity and connectivity during response to negative stressful stimuli 45 y later. Lower maternal TNF-α levels were significantly associated with higher hypothalamic activity in both sexes and higher functional connectivity between hypothalamus and anterior cingulate only in men. Higher prenatal levels of IL-6 were significantly associated with higher hippocampal activity in women alone. When examined in relation to the anti-inflammatory effects of IL-10, the ratio TNF-α:IL-10 was associated with sex-dependent effects on hippocampal activity and functional connectivity with the hypothalamus. Collectively, results suggested that adverse levels of maternal in utero proinflammatory cytokines and the balance of pro- to anti-inflammatory cytokines impact brain development of offspring in a sexually dimorphic manner that persists across the lifespan.
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“analysis of fetal human brain reveals high levels of gene expression consistent with increased baseline immune reactivity in PTSD (46, 47), which may be transmitted to offspring in a sex-specific manner through varying levels of maternal proinflammatory cytokines over the course of pregnancy (84).”
Background
- Authors
- Goldstein, J. M., Cohen, J. E., Mareckova, K., Holsen, L., Whitfield-Gabrieli, S., Gilman, S. E., Buka, S. L., & Hornig, M.
- Affiliations
- Harvard University (US)
- Central European Institute of Technology, Masaryk University, 601 77 Brno, Czech Republic;
- Brigham and Women's Hospital (US)
- Northeastern University Interdisciplinary Science and Engineering Complex, Northeastern University, Boston, MA 02120;
- Johns Hopkins University (US)
- Brown University (US)
- Columbia University (US)
- Corresponding author
- Goldstein, Jill M.
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2021-04-05
- Volume
- 118
- Issue
- 15
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC8054010
- OpenAlex
- W3147428953
- Cited by
- 70
- References
- 75
- Citations by year
- 2026: 11 · 2025: 11 · 2024: 18 · 2023: 12 · 2022: 13 · 2021: 5
- FWCI
- 7.68
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- HHS | NIH | National Institute of Mental Health (NIMH R03 MH105585, NIMH R01 MH56956 Phase III)
- HHS | NIH | Office of Research on Women's Health (ORWH-NIMH P50 MH082679, ORWH-NIMH U54 MH118919)
- Harvard Catalyst (NIH #UL1 RR025758)
- European Social Fund and Czech Republic Government (CZ.1.07/2.3.00/30.0009)
- Topics
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
- Keywords
- prenatal immune exposure, maternal cytokines, inflammatory cytokines, sex differences, stress response, hypothalamus, hippocampus, anterior cingulate cortex, functional connectivity, TNF-α, interleukin-6, IL-10, brain development, midlife, chronic stress, depression risk
- MeSH terms
- Adult, Female, Humans, Hypothalamus, Magnetic Resonance Imaging, Male, Pregnancy, Prenatal Exposure Delayed Effects, Sex Factors, Stress, Psychological, Cytokines, Connectome
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