Epigenetic regulation of RAC1 induces synaptic remodeling in stress disorders and depression
Open accessAbstract
Depression induces structural and functional synaptic plasticity in brain reward circuits, although the mechanisms promoting these changes and their relevance to behavioral outcomes are unknown. Transcriptional profiling of the nucleus accumbens (NAc) for Rho GTPase-related genes, which are known regulators of synaptic structure, revealed a sustained reduction in RAS-related C3 botulinum toxin substrate 1 (Rac1) expression after chronic social defeat stress. This was associated with a repressive chromatin state surrounding the proximal promoter of Rac1. Inhibition of class 1 histone deacetylases (HDACs) with MS-275 rescued both the decrease in Rac1 transcription after social defeat stress and depression-related behavior, such as social avoidance. We found a similar repressive chromatin state surrounding the RAC1 promoter in the NAc of subjects with depression, which corresponded with reduced RAC1 transcription. Viral-mediated reduction of Rac1 expression or inhibition of Rac1 activity in the NAc increases social defeat-induced social avoidance and anhedonia in mice. Chronic social defeat stress induces the formation of stubby excitatory spines through a Rac1-dependent mechanism involving the redistribution of synaptic cofilin, an actin-severing protein downstream of Rac1. Overexpression of constitutively active Rac1 in the NAc of mice after chronic social defeat stress reverses depression-related behaviors and prunes stubby spines. Taken together, our data identify epigenetic regulation of RAC1 in the NAc as a disease mechanism in depression and reveal a functional role for Rac1 in rodents in regulating stress-related behaviors.
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Activation of H3K27me3 in the NAc of mice exposed to social defeat stress inhibits expression of Rac1.
“The activation of H3K27me3 in the NAc of mice exposed to social defeat stress inhibits the expression of RAS-related C3 botulinum toxin substrate 1 (Rac1), a Rho GTPase–related gene known for synaptic structure regulation.158”
From Epigenetic regulation in major depression and other stress-related disorders: molecular mechanisms, clinical relevance and therapeutic potential (2023) · cites this paper as [158]
The Results section on stress-induced epigenetic regulation reports enhanced H3K27me3 methylation upstream of the Rac1 promoter in susceptible mice after social defeat; the transcriptional-regulation Results report reduced NAc Rac1 expression in those mice. The paper does not establish that H3K27me3 itself inhibits Rac1 expression, and the finding does not extend to all defeated mice. (LLM, conf=0.85)
Experimental — accuracy not yet measuredChronic antidepressant treatment can reverse CSDS-induced depression-like behaviors, including social avoidance.
“Chronic antidepressant treatment can reverse CSDS-induced depression-like behaviors, including social avoidance25, 32.”
From Social stress induces neurovascular pathology promoting depression (2017) · cites this paper as [32]
The Results section on stress-induced Rac1 regulation reports that 35 days of imipramine treatment partially reversed social avoidance in mice after chronic social defeat. It does not establish reversal of other depression-like behaviors by that treatment, and the claim omits the qualification that the observed reversal was partial. Page numbers are unavailable in our copy. (LLM, conf=0.87)
Experimental — accuracy not yet measuredExpression of Rac1 was low in NAc postmortem tissues in MDD and was associated with lower histone H3 pan acetylation and more histone H3K27 trimethylation.
“Expression of Rac1, involved in synaptic structure regulation, was low in NAc postmortem tissues in MDD and associated with lower histone H3 pan acetylation and more histone H3K27 trimethylation.158”
From Epigenetic regulation in major depression and other stress-related disorders: molecular mechanisms, clinical relevance and therapeutic potential (2023) · cites this paper as [158]
The subthreshold micro-defeat protocol is insufficient to induce depression-like behaviors without pro-depressive manipulations and can be used to identify pro-susceptibility factors.
“Without the introduction of pro-depressive manipulations, this protocol is insufficient to induce depression-like behaviors and thus can be used to identify pro-susceptibility factors32.”
From Social stress induces neurovascular pathology promoting depression (2017) · cites this paper as [32]
Sample size for CSDS mouse cohorts was calculated based on previous studies of CSDS and depression-like behaviors.
“Sample size for CSDS mouse cohorts was calculated based on previous studies of CSDS and depression-like behaviors11, 32”
From Social stress induces neurovascular pathology promoting depression (2017) · cites this paper as [32]
Cohorts were matched as closely as possible for gender, age, race, pH, postmortem interval and RNA integrity number.
“Cohorts were matched as closely as possible for gender, age, race, pH, postmortem interval and RNA integrity number32.”
From Social stress induces neurovascular pathology promoting depression (2017) · cites this paper as [32]
The Results section on MDD subjects describes two postmortem cohorts and refers to supplemental demographic tables, but the passages in our copy do not say the cohorts were matched on the listed characteristics. Searches for matching, postmortem interval, RNA integrity number, and the other specified characteristics did not locate that assertion. (LLM, conf=0.72)
Experimental — accuracy not yet measuredRac1 controls stubby spine formation in mice through an epigenetic mechanism.
“Rac1 expression, which is significantly decreased in human depressed patients, has been shown to mediate changes in stubby spine formation in mice via an epigenetic mechanism (86).”
From Emerging Role for Nucleus Accumbens Medium Spiny Neuron Subtypes in Depression (2017) · cites this paper as [86]
Rac1 expression is markedly lower in people with depression.
“Rac1 expression, which is significantly decreased in human depressed patients, has been shown to mediate changes in stubby spine formation in mice via an epigenetic mechanism (86).”
From Emerging Role for Nucleus Accumbens Medium Spiny Neuron Subtypes in Depression (2017) · cites this paper as [86]
Intra-NAc HDAC inhibition reverses social avoidance induced by CSDS, likely caused by increased Rac1 expression.
“Intra-NAc HDAC inhibition reverses social avoidance induced by CSDS, likely caused by increased Rac1 expression [141].”
From The molecular and cellular mechanisms of depression: a focus on reward circuitry (2019) · cites this paper as [141]
Rac1 is a GTPase downregulated by CSDS.
“Permissive acetylation on the Rac1 promotor, a GTPase downregulated by CSDS, is significantly reduced in susceptible mice, and susceptible mice have enhanced methylation directly upstream of the promotor [141].”
From The molecular and cellular mechanisms of depression: a focus on reward circuitry (2019) · cites this paper as [141]
Susceptible mice have enhanced methylation directly upstream of the Rac1 promoter.
“Permissive acetylation on the Rac1 promotor, a GTPase downregulated by CSDS, is significantly reduced in susceptible mice, and susceptible mice have enhanced methylation directly upstream of the promotor [141].”
From The molecular and cellular mechanisms of depression: a focus on reward circuitry (2019) · cites this paper as [141]
Permissive acetylation on the Rac1 promoter is significantly reduced in susceptible mice.
“Permissive acetylation on the Rac1 promotor, a GTPase downregulated by CSDS, is significantly reduced in susceptible mice, and susceptible mice have enhanced methylation directly upstream of the promotor [141].”
From The molecular and cellular mechanisms of depression: a focus on reward circuitry (2019) · cites this paper as [141]
The mechanism underlying structural plasticity of MSNs in CSDS is altered expression and activity of Rho GTPases.
“The mechanism underlying structural plasticity of MSNs in CSDS is altered expression and activity of Rho GTPases [88, 89, 138, 141].”
From The molecular and cellular mechanisms of depression: a focus on reward circuitry (2019) · cites this paper as [141]
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Inhibition of Rac1 Activity in the Hippocampus Impairs the Forgetting of Contextual Fear Memory
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Wei, J., Xiong, Z., Lee, J. B., Cheng, J., Duffney, L. J., Matas, E., & Yan, Z. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.3056-15.2016 · Cited by 56 · see citing works
Bath, K. G., Russo, S. J., Pleil, K. E., Wohleb, E. S., Duman, R. S., & Radley, J. J. (2017) · Neurobiology of Stress · doi:10.1016/j.ynstr.2017.05.001 · Cited by 55 · see citing works
Self-citationNutrition, Epigenetics, and Major Depressive Disorder: Understanding the Connection
Ortega, M. A., Fraile‐Μartinez, O., Montero, C. G., Álvarez-Mon, M. Á., Lahera, G., Monserrat, J., Llavero-Valero, M., Mora, F., Rodríguez–Jiménez, R., Fernández-Rojo, S., et al. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.867150 · Cited by 57 · see citing works
Losses and gains: chronic pain and altered brain morphology
Borsook, D., Erpelding, N., & Becerra, L. R. (2013) · Expert Review of Neurotherapeutics · doi:10.1586/14737175.2013.846218 · Cited by 56 · see citing works
Repurposing Vorinostat for the Treatment of Disorders Affecting Brain
Athira, K. V., Sadanandan, P., & Chakravarty, S. (2021) · NeuroMolecular Medicine · doi:10.1007/s12017-021-08660-4 · Cited by 52 · see citing works
- Authors
- Golden, S. A., Christoffel, D. J., Heshmati, M., Hodes, G. E., Magida, J., Davis, K., Cahill, M. E., Dias, C., Ribeiro, E., Ables, J. L., Kennedy, P. J., Robison, A. J., Gonzalez-Maeso, J., Neve, R. L., Turecki, G., Ghose, S., Tamminga, C. A., & Russo, S. J.
- Affiliations
- Icahn School of Medicine at Mount Sinai (US)
- Rockefeller University (US)
- McGovern Institute for Brain Research (US)
- Douglas Mental Health University Institute (CA)
- The University of Texas Southwestern Medical Center (US)
- Corresponding author
- Russo, Scott J
- ORCID
- Venue
- Nature Medicine
- Published
- 2013-02-17
- Volume
- 19
- Issue
- 3
- Pages
- 337-344
- ISSN
- 1078-8956 (ISSN-L)
- 1546-170X
- PMC
- PMC3594624
- OpenAlex
- W2052390712
- Cited by
- 322
- References
- 64
- Citations by year
- 2026: 10 · 2025: 7 · 2024: 38 · 2023: 19 · 2022: 20 · 2021: 27 · 2020: 24 · 2019: 24 · 2018: 28 · 2017: 25 · 2016: 36 · 2015: 33 · 2014: 17 · 2013: 14
- FWCI
- 24.47
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Medicine (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (P50 MH66172, R01MH090264, P50MH096890, P50MH066172, R01MH084894, T32MH087004)
- National Institute of General Medical Sciences (T32GM062754)
- Topics
- Health Sciences › Medicine › Pharmacology › Treatment of Major Depression
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- Rac1, epigenetic regulation, chronic social defeat stress, depression, nucleus accumbens, synaptic plasticity, histone deacetylase, entinostat, chromatin reprogramming, social avoidance, anhedonia, Rho GTPases, stress disorders
- MeSH terms
- Animals, Antidepressive Agents, Tricyclic, Behavior, Animal, Major Depressive Disorder, Histones, Humans, Imipramine, Male, Mice, Inbred C57BL, Molecular Sequence Data, Nucleus Accumbens, Promoter Regions, Genetic, Social Behavior, Stress, Psychological, Transcription, Genetic, rac1 GTP-Binding Protein, Gene Expression Profiling, Stress Disorders, Traumatic, Epigenesis, Genetic, Dendritic Spines, Actin Depolymerizing Factors, Mice
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