Epigenetic mechanisms within the cingulate cortex regulate innate anxiety-like behavior
Open accessAbstract
BACKGROUND: Pathological anxiety originates from a complex interplay of genetic predisposition and environmental factors, acting via epigenetic mechanisms. Epigenetic processes that can counteract detrimental genetic risk towards innate high anxiety are not well characterized. METHODS: We used female mouse lines of selectively bred high (HAB)- vs low (LAB)-innate anxiety-related behavior and performed select environmental and pharmacological manipulations to alter anxiety levels as well as brain-specific manipulations and immunohistochemistry to investigate neuronal mechanisms associated with alterations in anxiety-related behavior. RESULTS: Inborn hyperanxiety of high anxiety-like phenotypes was effectively reduced by environmental enrichment exposure. c-Fos mapping revealed that hyperanxiety in high anxiety-like phenotypes was associated with blunted challenge-induced neuronal activation in the cingulate-cortex, which was normalized by environmental enrichment. Relating this finding with epigenetic modifications, we found that high anxiety-like phenotypes (compared with low-innate anxiety phenotypes) showed reduced acetylation in the hypoactivated cingulate-cortex neurons following a mild emotional challenge, which again was normalized by environmental enrichment. Paralleling the findings using environmental enrichment, systemic administration of histone-deacetylase-inhibitor MS-275 elicited an anxiolytic-like effect, which was correlated with increased acetylated-histone-3 levels within cingulate-cortex. Finally, as a proof-of-principle, local MS-275 injection into cingulate-cortex rescued enhanced innate anxiety and increased acetylated-histone-3 within the cingulate-cortex, suggesting this epigenetic mark as a biomarker for treatment success. CONCLUSIONS: Taken together, the present findings provide the first causal evidence that the attenuation of high innate anxiety-like behavior via environmental/pharmacological manipulations is epigenetically mediated via acetylation changes within the cingulate-cortex. Finally, histone-3 specific histone-deacetylase-inhibitor could be of therapeutic importance in anxiety disorders.
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Histone-deacetylase inhibitors may be useful in anxiety disorders by promoting relevant gene expression and targeting some common comorbidities of anxiety disorders.
“histone-deacetylase inhibitors may be useful in anxiety disorders, by promoting relevant gene expression (Sah et al., 2019;Tran, Schulkin, Ligon, & Greenwood-Van Meerveld, 2015;Whittle & Singewald, 2014) and targeting also some common comorbidities of anxiety disorders (Moloney, Stilling, Dinan, & Cryan, 2015).”
From Novel pharmacological targets in drug development for the treatment of anxiety and anxiety-related disorders (2019) · cites this paper as Sah et al., 2019
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- Authors
- Sah, A., Sotnikov, S., Kharitonova, M., Schmuckermair, C., Diepold, R. P., Landgraf, R., Whittle, N., & Singewald, N.
- Affiliations
- Universität Innsbruck (AT)
- Max Planck Institute of Psychiatry (DE)
- Corresponding author
- Singewald, Nicolas
- Venue
- International Journal of Neuropsychopharmacology
- Publisher
- Oxford University Press (OUP)
- Published
- 2019-01-21
- Volume
- 22
- Issue
- 4
- Pages
- 317-328
- ISSN
- 1461-1457 (ISSN-L)
- 1469-5111
- PMC
- PMC6441131
- OpenAlex
- W2913564378
- Cited by
- 24
- References
- 77
- Citations by year
- 2026: 2 · 2025: 3 · 2024: 2 · 2023: 5 · 2022: 3 · 2021: 3 · 2020: 5 · 2019: 1
- FWCI
- 1.73
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- The International Journal of Neuropsychopharmacology (publishedVersion, cc-by-nc)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- Austrian Science Fund (SFB F4410, W1206-B18)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Keywords
- cingulate cortex, epigenetic regulation, histone acetylation, histone deacetylase inhibition, entinostat, environmental enrichment, anxiety-like behavior, c-Fos neuronal activation, histone H3 acetylation, anxiety disorders, anxiolytic effects
- MeSH terms
- Proof of Concept Study, Animals, Anxiety, Behavior, Animal, Benzamides, Environment, Female, Gyrus Cinguli, Histones, Instinct, Male, Mice, Inbred Strains, Pyridines, Anti-Anxiety Agents, Epigenesis, Genetic, Mice, Histone Deacetylase Inhibitors
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