Chronic Stress Induces Sex-Specific Alterations in Methylation and Expression of Corticotropin-Releasing Factor Gene in the Rat

Sterrenburg, Linda; Gaszner, Balázs; Boerrigter, Jeroen; Santbergen, Lennart; Bramini, Mattia; Elliott, Evan; Chen, Alon; Peeters, Bernard W. M. M.; Roubos, Eric W.; Kozicz, Tamás

doi:10.1371/journal.pone.0028128

Cited by 149Stress Responses and CortisolEpigenetics and DNA MethylationNeurotransmitter Receptor Influence on Behavior

Chronic Stress Induces Sex-Specific Alterations in Methylation and Expression of Corticotropin-Releasing Factor Gene in the Rat

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Sterrenburg, Linda, Gaszner, Balázs, Boerrigter, Jeroen, Santbergen, Lennart, Bramini, Mattia, Elliott, Evan, Chen, Alon, Peeters, Bernard W. M. M. +2 more·2011·PLoS ONE

DOI 10.1371/journal.pone.0028128PMC PMC3223222

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Abstract

BACKGROUND: Although the higher prevalence of depression in women than in men is well known, the neuronal basis of this sex difference is largely elusive. METHODS: Male and female rats were exposed to chronic variable mild stress (CVMS) after which immediate early gene products, corticotropin-releasing factor (CRF) mRNA and peptide, various epigenetic-associated enzymes and DNA methylation of the Crf gene were determined in the hypothalamic paraventricular nucleus (PVN), oval (BSTov) and fusiform (BSTfu) parts of the bed nucleus of the stria terminalis, and central amygdala (CeA). RESULTS: CVMS induced site-specific changes in Crf gene methylation in all brain centers studied in female rats and in the male BST and CeA, whereas the histone acetyltransferase, CREB-binding protein was increased in the female BST and the histone-deacetylase-5 decreased in the male CeA. These changes were accompanied by an increased amount of c-Fos in the PVN, BSTfu and CeA in males, and of FosB in the PVN of both sexes and in the male BSTov and BSTfu. In the PVN, CVMS increased CRF mRNA in males and CRF peptide decreased in females. CONCLUSIONS: The data confirm our hypothesis that chronic stress affects gene expression and CRF transcriptional, translational and secretory activities in the PVN, BSTov, BSTfu and CeA, in a brain center-specific and sex-specific manner. Brain region-specific and sex-specific changes in epigenetic activity and neuronal activation may play, too, an important role in the sex specificity of the stress response and the susceptibility to depression.

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Rats exposed to variable mild stress manifested decreased HDAC5 in the central amygdala.
“Rats exposed to variable mild stress manifested decreased HDAC5 in the central amygdala (CeA).150”
From Epigenetic regulation in major depression and other stress-related disorders: molecular mechanisms, clinical relevance and therapeutic potential (2023) · cites this paper as [150]
The Discussion (Limbic centers) reports decreased HDAC5 mRNA in the central amygdala after chronic variable mild stress, but specifies that the finding was in male rats. Table 1 (Results, Epigenetic factors) confirms a significant decrease in males and identifies the measurement as mRNA, not HDAC5 protein. The citing sentence omits both qualifications. (LLM, conf=0.88)
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Increased DNA methylation levels of Gdnf and Crh in rodent models of chronic stress have been observed, with effects appearing both gender- and brain region-dependent.
“Increased DNA methylation levels of Gdnf (Glial cell-derived neurotrophic factor) and Crh in rodent models of chronic stress have been observed, although the effects appear to be both gender and brain region-dependent [42,43].”
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 [42]

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Chronic stress induces sex-specific alterations in methylation and expression of corticotropin-releasing factor gene in the rat. PLoS One 6: e28128. doi: 10.1371/journal.pone.0028128 PMID: 22132228
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Authors: Sterrenburg, L., Gaszner, B., Boerrigter, J., Santbergen, L., Bramini, M., Elliott, E., Chen, A., Peeters, B. W. M. M., Roubos, E. W., & Kozicz, T.
Affiliations: Radboud University Nijmegen (NL)
University of Pecs (HU)
Bar-Ilan University (IL)
Weizmann Institute of Science (IL)
Corresponding author: Kozicz, Tamás
ORCID: Gaszner, Balázs
Bramini, Mattia
Elliott, Evan
Chen, Alon
Kozicz, Tamás
Venue: PLoS ONE
Publisher: Public Library of Science (PLoS)
Published: 2011-11-23
Volume: 6
Issue: 11
Pages: e28128
ISSN: 1932-6203 (ISSN-L)
DOI: 10.1371/journal.pone.0028128
PMC: PMC3223222
OpenAlex: W2159916106
Cited by: 149
References: 80
Citations by year: 2026: 4 · 2025: 3 · 2024: 1 · 2023: 8 · 2022: 11 · 2021: 12 · 2020: 17 · 2019: 10 · 2018: 10 · 2017: 9 · 2016: 16 · 2015: 9 · 2014: 15 · 2013: 13 · 2012: 10
FWCI: 4.90
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)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Institutional Repository of the University of Granada (University of Granada) (submittedVersion, cc-by-nc-nd)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Figshare (submittedVersion, cc-by)
Radboud Repository (Radboud University) (submittedVersion)
Radboud Repository (Radboud University) (submittedVersion, other-oa)
Funders: Nederlandse Organisatie voor Wetenschappelijk Onderzoek (864.05.008)
Magyar Tudományos Akadémia
Topics: Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords: corticotropin-releasing factor, DNA methylation, sex differences, depression, hypothalamic paraventricular nucleus, bed nucleus of the stria terminalis, central amygdala, CREB-binding protein, HDAC5, c-fos, FosB, immediate early genes, epigenetic regulation, stress response
MeSH terms: Animals, Body Weight, Chronic Disease, Corticosterone, Corticotropin-Releasing Hormone, Female, Gene Expression Regulation, Immunohistochemistry, Male, Models, Biological, Paraventricular Hypothalamic Nucleus, Septal Nuclei, Sex Characteristics, Stress, Psychological, Rats, Wistar, In Situ Hybridization, DNA Methylation, Epigenesis, Genetic, Rats

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Chronic Stress Induces Sex-Specific Alterations in Methylation and Expression of Corticotropin-Releasing Factor Gene in the Rat

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