Cell-Type-Specific Epigenetic Editing at the Fosb Gene Controls Susceptibility to Social Defeat Stress
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Chronic social defeat stress regulates the expression of Fosb in the nucleus accumbens (NAc) to promote the cell-type-specific accumulation of ΔFosB in the two medium spiny neuron (MSN) subtypes in this region. ΔFosB is selectively induced in D1-MSNs in the NAc of resilient mice, and in D2-MSNs of susceptible mice. However, little is known about the consequences of such selective induction, particularly in D2-MSNs. This study examined how cell-type-specific control of the endogenous Fosb gene in NAc regulates susceptibility to social defeat stress. Histone post-translational modifications (HPTMs) were targeted specifically to Fosb using engineered zinc-finger proteins (ZFPs). Fosb-ZFPs were fused to either the transcriptional repressor, G9a, which promotes histone methylation or the transcriptional activator, p65, which promotes histone acetylation. These ZFPs were expressed in D1- vs D2-MSNs using Cre-dependent viral expression in the NAc of mice transgenic for Cre recombinase in these MSN subtypes. We found that stress susceptibility is oppositely regulated by the specific cell type and HPTM targeted. We report that Fosb-targeted histone acetylation in D2-MSNs or histone methylation in D1-MSNs promotes a stress-susceptible, depressive-like phenotype, while histone methylation in D2-MSNs or histone acetylation in D1-MSNs increases resilience to social stress as quantified by social interaction behavior and sucrose preference. This work presents the first demonstration of cell- and gene-specific targeting of histone modifications, which model naturally occurring transcriptional phenomena that control social defeat stress behavior. This epigenetic-editing approach, which recapitulates physiological changes in gene expression, reveals clear differences in the social defeat phenotype induced by Fosb gene manipulation in MSN subtypes.
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Specific cell types and epigenetic changes affect stress susceptibility in an opposing manner.
“Specific cell types and epigenetic changes affect stress susceptibility in an opposing manner.196”
From Epigenetic regulation in major depression and other stress-related disorders: molecular mechanisms, clinical relevance and therapeutic potential (2023) · cites this paper as [196]
Fosb-targeted histone acetylation or methylation in D2-type versus D1-type medium spiny neurons controls stress susceptibility and resilience to social stress.
“Fosb-targeted histone acetylation or methylation in different types of medium spiny neurons (i.e., D2-type vs. D1-type) controls stress susceptibility and resilience to social stress.”
From Epigenetic regulation in major depression and other stress-related disorders: molecular mechanisms, clinical relevance and therapeutic potential (2023) · cites this paper as [196]
In mice, dopamine D2 receptor neuron-specific targeting of histone acetylation or methylation at the Fosb gene within the NAc led to a phenotype of stress susceptibility or resilience, respectively.
“A recent study in mice found that dopamine D2 receptor neuron-specific targeting of histone acetylation/methylation at the Fosb gene within the NAc led to a phenotype of stress susceptibility or resilience, respectively [158].”
From Cell-type-specific epigenetic effects of early life stress on the brain (2022) · cites this paper as [158]
Histone acetylation on the Fosb promotor drives resilience in D1-MSNs, but susceptibility in D2-MSNs.
“Histone acetylation on the Fosb promotor drives resilience in D1-MSNs, but susceptibility in D2-MSNs [124].”
From The molecular and cellular mechanisms of depression: a focus on reward circuitry (2019) · cites this paper as [124]
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Early Life Stress- and Drug-Induced Histone Modifications Within the Ventral Tegmental Area
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Self-citationStereotaxic Surgery and Viral Delivery of Zinc-Finger Epigenetic Editing Tools in Rodent Brain
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Self-citationEpigenetic editing of Cartpt promotes acquisition and extinction of cocaine memoryPreprint
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Self-citationCell- and Pathway-Specific Disruptions in the Accumbens of Fragile X Mouse
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Self-citationLaine, M. A. (2021) · Työväentutkimus Vuosikirja
- Authors
- Hamilton, P. J., Burek, D. J., Lombroso, S. I., Neve, R. L., Robison, A. J., Nestler, E. J., & Heller, E. A.
- Affiliations
- Icahn School of Medicine at Mount Sinai (US)
- University of Pennsylvania (US)
- McGovern Institute for Brain Research (US)
- Michigan State University (US)
- Corresponding author
- Heller, Elizabeth A
- ORCID
- Venue
- Neuropsychopharmacology
- Published
- 2017-05-02
- Volume
- 43
- Issue
- 2
- Pages
- 272-284
- ISSN
- 0893-133X (ISSN-L)
- 1740-634X
- PMC
- PMC5729576
- OpenAlex
- W2611897471
- Cited by
- 113
- References
- 52
- Citations by year
- 2026: 7 · 2025: 10 · 2024: 14 · 2023: 13 · 2022: 10 · 2021: 10 · 2020: 10 · 2019: 20 · 2018: 19
- FWCI
- 6.56
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Neuropsychopharmacology (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (P50MH096890, R01MH051399, R01MH111604)
- National Institute on Drug Abuse (DP1DA044250, R37DA007359, F32DA035518, P01DA008227, R01DA007359, R01DA040621)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Pharmacology › Treatment of Major Depression
- Keywords
- FosB, ΔFosB, social defeat stress, nucleus accumbens, medium spiny neurons, histone acetylation, histone methylation, epigenome editing, zinc finger proteins, G9a, NF-κB p65, stress resilience, depression-like behavior, sucrose preference, social interaction behavior
- MeSH terms
- Animals, Behavior, Animal, Depression, Disease Models, Animal, Disease Susceptibility, Dominance-Subordination, Male, Mice, Transgenic, Nucleus Accumbens, Phenotype, Stress, Psychological, Proto-Oncogene Proteins c-fos, Receptors, Dopamine D1, Receptors, Dopamine D2, Epigenesis, Genetic, Mice
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