Prenatal stress decreases Bdnf expression and increases methylation of Bdnf exon IV in rats

Boersma, Gretha J; Lee, Richard S; Cordner, Zachary A; Ewald, Erin R; Purcell, Ryan H; Moghadam, Alexander A; Tamashiro, Kellie L

doi:10.4161/epi.27558

Cited by 175Epigenetics and DNA MethylationMaternal Mental Health During Pregnancy and PostpartumBirth, Development, and Health

Prenatal stress decreases Bdnf expression and increases methylation of Bdnf exon IV in rats

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Boersma, Gretha J, Lee, Richard S, Cordner, Zachary A, Ewald, Erin R, Purcell, Ryan H, Moghadam, Alexander A, Tamashiro, Kellie L·2014·Epigenetics

DOI 10.4161/epi.27558PMC PMC4053462

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Abstract

There is ample evidence that exposure to stress during gestation increases the risk of the offspring to develop mood disorders. Brain-derived neurotrophic factor (Bdnf) plays a critical role during neuronal development and is therefore a prime candidate to modulate neuronal signaling in adult offspring of rat dams that were stressed during gestation. In the current study, we tested the hypothesis that alterations in Bdnf expression in prenatally stressed (PNS) offspring are mediated by changes in DNA methylation in exons IV and VI of the Bdnf gene. We observed decreased Bdnf expression in the amygdala and hippocampus of prenatally stressed rats both at weaning and in adulthood. This decrease in Bdnf expression was accompanied by increased DNA methylation in Bdnf exon IV in the amygdala and hippocampus, suggesting that PNS-induced reduction in Bdnf expression may, at least in part, be mediated by increased DNA methylation of Bdnf exon IV. Expression of DNA methyltransferases (Dnmt) 1 and 3a was increased in PNS rats in the amygdala and hippocampus. Our data suggest that PNS induces decreases in Bdnf expression that may at least in part be mediated by increased DNA methylation of Bdnf exon IV.

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Prenatally stressed rats had increased brain-derived neurotrophic factor (Bdnf) promoter methylation and correspondingly decreased expression in the amygdala and hippocampus, observed at weaning and persisting into adulthood.
“For example, prenatally stressed rats were shown to have increased brain-derived neurotrophic factor (Bdnf) promoter methylation and correspondingly decreased expression in the amygdala and hippocampus [38]. This was observed in early life (at weaning) and persisted into adulthood.”
From Biological Embedding of Early-Life Adversity and a Scoping Review of the Evidence for Intergenerational Epigenetic Transmission of Stress and Trauma in Humans (2023) · cites this paper as [38]
The expression results report decreased Bdnf expression in the amygdala and hippocampus at both weaning (PND21) and adulthood (PND80). The exon IV promoter methylation results report an overall increase in both regions at PND21, but at PND80 the overall increase persisted only in the amygdala; the hippocampus had increases at specific CpG sites, not in overall methylation. Thus the claim overstates what persisted in both regions. (LLM, conf=0.89)
Experimental — accuracy not yet measured
Early-life trauma in rodent models can influence DNA methylation of various candidate genes in brain regions important in stress signaling.
“Numerous subsequent studies using rodent models have shown that early-life trauma (e.g., chronic and unpredictable maternal behavior, separation, fear conditioning), can influence DNA methylation of various candidate genes in brain regions important in stress signaling.”
From Biological Embedding of Early-Life Adversity and a Scoping Review of the Evidence for Intergenerational Epigenetic Transmission of Stress and Trauma in Humans (2023) · cites this paper as [38]
The Results section (DNA methylation of Bdnf exon IV promoter at PND21; page unavailable) reports increased Bdnf methylation in the amygdala of rats exposed to prenatal maternal stress, with increases at specific sites in the hippocampus. This supports the general point that early stress can affect methylation in relevant brain regions, but this study examines one candidate gene and prenatal stress, not the range of genes or postnatal experiences listed in the citing sentence. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Enduring behavioral responses to stress and epigenetic alterations in adult offspring have been demonstrated to be mediated by changes in gametes, in utero effects, variations in early postnatal care, and/or other early life experiences influenced by parental exposure.
“Enduring behavioral responses to stress and epigenetic alterations in adult offspring have been demonstrated to be mediated by changes in gametes (10)(11)(12)(13), in utero effects (14), variations in early postnatal care (15,16), and/or other early life experiences (17) that are influenced by parental exposure (18).”
From Holocaust Exposure Induced Intergenerational Effects on FKBP5 Methylation (2016) · cites this paper as [14]

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“For example, prenatally stressed rats were shown to have increased brainderived neurotrophic factor (Bdnf ) promoter methylation and correspondingly decreased expression in the amygdala and hippocampus [38].”
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An example of DNA methylation as a means to quantify stress in wildlife using killer whales
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Sex-Specific Effects of Prenatal Stress on Bdnf Expression in Response to an Acute Challenge in Rats: a Role for Gadd45β
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The psychopathology of prenatal stress: The role of epigenetic regulation of brain-derived neurotrophic factor (BDNF) promoter
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Gestational stress induces depressive-like and anxiety-like phenotypes through epigenetic regulation of BDNF expression in offspring hippocampus
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Authors: Boersma, G. J., Lee, R. S., Cordner, Z. A., Ewald, E. R., Purcell, R. H., Moghadam, A. A., & Tamashiro, K. L.
Affiliations: Johns Hopkins University (US)
Corresponding author: Boersma, Gretha J
ORCID: Boersma, Gretha J
Lee, Richard S
Cordner, Zachary A
Purcell, Ryan H
Moghadam, Alexander A
Tamashiro, Kellie L
Venue: Epigenetics
Publisher: Informa UK Limited
Published: 2013-12-23
Volume: 9
Issue: 3
Pages: 437-447
ISSN: 1559-2294 (ISSN-L)
1559-2308
DOI: 10.4161/epi.27558
PMC: PMC4053462
OpenAlex: W1994352959
Cited by: 172
References: 52
Citations by year: 2026: 11 · 2025: 3 · 2024: 8 · 2023: 11 · 2022: 11 · 2021: 18 · 2020: 12 · 2019: 14 · 2018: 16 · 2017: 23 · 2016: 22 · 2015: 14 · 2014: 8 · 2012: 1
FWCI: 6.56
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Epigenetics (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Alliance for Research on Schizophrenia and Depression
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (825.10.032)
National Institutes of Health (825.10.032, HD055030)
National Institute of General Medical Sciences (T32GM008605)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (HD-055030, R00HD055030, K99HD055030)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
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
Keywords: prenatal stress, brain-derived neurotrophic factor, DNA methylation, DNA methyltransferases, amygdala, hippocampus, epigenetic regulation, gene expression
MeSH terms: DNA (Cytosine-5-)-Methyltransferase 1, DNA Methyltransferase 3A, Amygdala, Animals, DNA (Cytosine-5-)-Methyltransferases, Exons, Female, Hippocampus, Male, Pregnancy, Prenatal Exposure Delayed Effects, Promoter Regions, Genetic, Stress, Psychological, Rats, Sprague-Dawley, Prefrontal Cortex, DNA Methylation, Brain-Derived Neurotrophic Factor, Rats

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Prenatal stress decreases Bdnf expression and increases methylation of Bdnf exon IV in rats

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