Cited by 193Maternal Mental Health During Pregnancy and PostpartumBirth, Development, and HealthMicroRNA in disease regulation

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Maternal Stress Induces Epigenetic Signatures of Psychiatric and Neurological Diseases in the Offspring

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Zucchi, Fabiola C. R., Yao, Youli, Ward, Isaac D., Ilnytskyy, Yaroslav, Olson, David M., Benzies, Karen, Kovalchuk, Igor, Kovalchuk, Olga, Metz, Gerlinde A. S.·2013·PLoS ONE

DOI 10.1371/journal.pone.0056967PMC PMC3579944

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Abstract

The gestational state is a period of particular vulnerability to diseases that affect maternal and fetal health. Stress during gestation may represent a powerful influence on maternal mental health and offspring brain plasticity and development. Here we show that the fetal transcriptome, through microRNA (miRNA) regulation, responds to prenatal stress in association with epigenetic signatures of psychiatric and neurological diseases. Pregnant Long-Evans rats were assigned to stress from gestational days 12 to 18 while others served as handled controls. Gestational stress in the dam disrupted parturient maternal behaviour and was accompanied by characteristic brain miRNA profiles in the mother and her offspring, and altered transcriptomic brain profiles in the offspring. In the offspring brains, prenatal stress upregulated miR-103, which is involved in brain pathologies, and downregulated its potential gene target Ptplb. Prenatal stress downregulated miR-145, a marker of multiple sclerosis in humans. Prenatal stress also upregulated miR-323 and miR-98, which may alter inflammatory responses in the brain. Furthermore, prenatal stress upregulated miR-219, which targets the gene Dazap1. Both miR-219 and Dazap1 are putative markers of schizophrenia and bipolar affective disorder in humans. Offspring transcriptomic changes included genes related to development, axonal guidance and neuropathology. These findings indicate that prenatal stress modifies epigenetic signatures linked to disease during critical periods of fetal brain development. These observations provide a new mechanistic association between environmental and genetic risk factors in psychiatric and neurological disease.

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Authors: Zucchi, F. C. R., Yao, Y., Ward, I. D., Ilnytskyy, Y., Olson, D. M., Benzies, K., Kovalchuk, I., Kovalchuk, O., & Metz, G. A. S.
Affiliations: University of Lethbridge (CA)
University of Alberta (CA)
University of Calgary (CA)
Corresponding author: Metz, Gerlinde A. S.
ORCID: Yao, Youli
Olson, David M.
Benzies, Karen
Kovalchuk, Igor
Kovalchuk, Olga
Metz, Gerlinde A. S.
Venue: PLoS ONE
Publisher: Public Library of Science (PLoS)
Published: 2013-02-22
Volume: 8
Issue: 2
Pages: e56967
ISSN: 1932-6203 (ISSN-L)
DOI: 10.1371/journal.pone.0056967
PMC: PMC3579944
OpenAlex: W2016612502
Cited by: 193
References: 100
Citations by year: 2026: 6 · 2025: 5 · 2024: 6 · 2023: 12 · 2022: 13 · 2021: 12 · 2020: 19 · 2019: 13 · 2018: 18 · 2017: 20 · 2016: 18 · 2015: 21 · 2014: 24 · 2013: 6
FWCI: 23.46
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS ONE (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, other-oa)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: Alberta Innovates (200700595)
Canadian Institutes of Health Research
Topics: Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
Keywords: prenatal stress, maternal stress, epigenetic signatures, microRNA, offspring neurodevelopment, miR-103, miR-145, miR-219, miR-98, DAZAP1, schizophrenia, bipolar disorder, multiple sclerosis, neuroinflammation, Long-Evans rats, environmental risk factors
MeSH terms: Animals, Base Sequence, Mental Disorders, Brain, Female, Nervous System Diseases, Pregnancy, Pregnancy Complications, Stress, Psychological, DNA Primers, Reverse Transcriptase Polymerase Chain Reaction, Rats, Long-Evans, MicroRNAs, Epigenesis, Genetic, Transcriptome, Real-Time Polymerase Chain Reaction

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Maternal Stress Induces Epigenetic Signatures of Psychiatric and Neurological Diseases in the Offspring

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