Regulation of hippocampal H3 histone methylation by acute and chronic stress
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The hippocampal formation is a brain region noted for its plasticity in response to stressful events and adrenal steroid hormones. Recent work has shown that chromatin remodeling in various brain regions, including the hippocampus, is associated with the effects of stress in a variety of models. We chose to examine the effects of stress, stress duration, corticosterone administration, and fluoxetine treatment on the levels of hippocampal histone H3 methylation at lysines 4, 9, and 27, marks associated, respectively, with active transcription, heterochromatin formation, and transcriptional repression. We found that acute stress increased the levels of H3K9 tri-methylation (H3K9me3) in the dentate gyrus (DG) and CA1, while it reduced levels of H3K9 mono-methylation (H3K9me1) and H3K27 tri-methylation (H3K27me3) in the same regions, and had no effect on levels of H3K4 tri-methylation (H3K4me3). Seven days of restraint stress reduced levels of H3K4me3 in the CA1 and H3K27me3 in the DG and CA1, while increasing basal levels of H3K9me3. Chronic restraint stress (CRS) for 21 days mildly increased levels of H3K4me3 and reduced H3K9me3 levels in the DG. Treatment with fluoxetine during CRS reversed the decrease in DG H3K9me3, but had no effect on the other marks. These results show a complex, surprisingly rapid, and regionally specific pattern of chromatin remodeling within hippocampus produced by stress and anti-depressant treatment that may open an avenue of understanding the interplay of stress and hippocampal gene expression, and reveal the outlines of a potential chromatin stress response that may be diminished or degraded by chronic stress.
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Reduced levels of H3K9me3 were detected in rats subjected to chronic restraint stress, a finding that was reversed on administration of the antidepressant fluoxetine.
“Reduced levels of H3K9me3 was detected, a finding that was reversed on administration of the antidepressant fluoxetine, though neither gene expression changes nor anxiety phenotype were measured (Hunter et al., 2009).”
From The Epigenetics of Anxiety Pathophysiology: A DNA Methylation and Histone Modification Focused Review (2023) · cites this paper as Hunter et al., 2009
In rodents, chronic stress affects the total levels of acetylated histones in certain limbic regions.
“In rodents, chronic stress affects the total levels of acetylated histones in certain limbic regions.”
From Epigenetic mechanisms of major depression: Targeting neuronal plasticity (2018) · cites this paper as [67]
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Caradonna, S. G., Paul, M. R., & Marrocco, J. (2022) · Neurobiology of Stress · doi:10.1016/j.ynstr.2022.100475 · Cited by 13 · see citing works
Cognition and mood-related behaviors in L3mbtl1 null mutant mice
Shen, E. Y., Jiang, Y., Mao, W., Futai, K., Hock, H., & Akbarian, S. (2015) · PLoS ONE · doi:10.1371/journal.pone.0121252 · Cited by 4 · see citing works
- Authors
- Hunter, R. G., McCarthy, K. J., Milne, T. A., Pfaff, D. W., & McEwen, B. S.
- Affiliations
- Rockefeller University (US)
- Laboratory of Neuroendocrinology,
- Laboratory of Neurobiology and Behavior, and
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2009-12-08
- Volume
- 106
- Issue
- 49
- Pages
- 20912-20917
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC2791599
- OpenAlex
- W1972943884
- Cited by
- 290
- References
- 60
- Citations by year
- 2026: 7 · 2025: 7 · 2024: 11 · 2023: 6 · 2022: 18 · 2021: 23 · 2020: 12 · 2019: 17 · 2018: 21 · 2017: 23 · 2016: 29 · 2015: 20 · 2014: 27 · 2013: 18 · 2012: 19
- FWCI
- 6.48
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Barnard College
- National Institutes of Health (MH41256)
- National Institute of Mental Health (MH-41256, MH-15125, R37MH041256, T32MH015125, R01MH041256)
- 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 › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- hippocampus, histone H3 methylation, acute stress, chronic restraint stress, H3K4me3, H3K9me3, H3K27me3, chromatin remodeling, fluoxetine, corticosterone, dentate gyrus, CA1, antidepressant treatment, stress response, transcriptional repression, heterochromatin
- MeSH terms
- Acute Disease, Animals, Chronic Disease, Fluoxetine, Hippocampus, Histones, Lysine, Male, Methylation, Restraint, Physical, Stress, Psychological, Rats, Sprague-Dawley, Dentate Gyrus, Rats
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