Potential role of adolescent alcohol exposure-induced amygdaloid histone modifications in anxiety and alcohol intake during adulthood

Pandey, Subhash C.; Sakharkar, Amul J.; Tang, Lei; Zhang, Huaibo

doi:10.1016/j.nbd.2015.03.019

Cited by 191Histone Deacetylase Inhibitors ResearchNeurotransmitter Receptor Influence on BehaviorNeuroscience and Neuropharmacology Research

Potential role of adolescent alcohol exposure-induced amygdaloid histone modifications in anxiety and alcohol intake during adulthood

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Pandey, Subhash C., Sakharkar, Amul J., Tang, Lei, Zhang, Huaibo·2015·Neurobiology of Disease

DOI 10.1016/j.nbd.2015.03.019PMC PMC4581895

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Abstract

Binge drinking is common during adolescence and can lead to the development of psychiatric disorders, including alcoholism in adulthood. Here, the role and persistent effects of histone modifications during adolescent intermittent ethanol (AIE) exposure in the development of anxiety and alcoholism in adulthood were investigated. Rats received intermittent ethanol exposure during post-natal days 28-41, and anxiety-like behaviors were measured after 1 and 24 h of the last AIE. The effects of AIE on anxiety-like and alcohol-drinking behaviors in adulthood were measured with or without treatment with the histone deacetylase (HDAC) inhibitor, trichostatin A (TSA). Amygdaloid brain regions were collected to measure HDAC activity, global and gene-specific histone H3 acetylation, expression of brain-derived neurotrophic factor (BDNF) and activity-regulated cytoskeleton-associated (Arc) protein and dendritic spine density (DSD). Adolescent rats displayed anxiety-like behaviors after 24 h, but not 1 h, of last AIE with a concomitant increase in nuclear and cytosolic amygdaloid HDAC activity and HDAC2 and HDAC4 levels leading to deficits in histone (H3-K9) acetylation in the central (CeA) and medial (MeA), but not in basolateral nucleus of amygdala (BLA). Interestingly, some of AIE-induced epigenetic changes such as, increased nuclear HDAC activity, HDAC2 expression, and decreased global histone acetylation persisted in adulthood. In addition, AIE decreased BDNF exons I and IV and Arc promoter specific histone H3 acetylation that was associated with decreased BDNF, Arc expression and DSD in the CeA and MeA during adulthood. AIE also induced anxiety-like behaviors and enhanced ethanol intake in adulthood, which was attenuated by TSA treatment via normalization of deficits in histone H3 acetylation of BDNF and Arc genes. These novel results indicate that AIE induces long-lasting effects on histone modifications and deficits in synaptic events in the amygdala, which are associated with anxiety-like and alcohol drinking behaviors in adulthood.

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Alcohol use during adolescence might lead to epigenetic modifications that alter amygdalar gene expression and dendritic density, increasing susceptibility to anxiety-like behaviours and alcohol ingestion in adulthood.
“alcohol use during adolescence might lead to epigenetic modifications that alter amygdalar gene expression and dendritic density, increasing susceptibility to anxiety-like behaviours and alcohol ingestion in adulthood.140”
From Neurobiology of addiction: a neurocircuitry analysis (2016) · cites this paper as [140]
Adolescent alcohol exposure can lead to long-lasting histone modifications that alter synaptic function in the amygdala and likely contribute to anxiety-like behavior.
“For example, AAE can lead to long-lasting histone modifications that alter synaptic function in the amygdala and likely contributes anxiety-like behavior [50].”
From Consequences of adolescent drug use (2023) · cites this paper as [50]

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Adolescent alcohol exposure alters lysine demethylase 1 (LSD1) expression and histone methylation in the amygdala during adulthood
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Altered amygdala DNA methylation mechanisms after adolescent alcohol exposure contribute to adult anxiety and alcohol drinking
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Negative Affect and Excessive Alcohol Intake Incubate during Protracted Withdrawal from Binge-Drinking in Adolescent, But Not Adult, Mice
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The Transitional Age Brain
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Adolescent Binge Alcohol Enhances Early Alzheimer’s Disease Pathology in Adulthood Through Proinflammatory Neuroimmune Activation
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Intermittent Ethanol during Adolescence Leads to Lasting Behavioral Changes in Adulthood and Alters Gene Expression and Histone Methylation in the PFC
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Apoptosis-triggered decline in hippocampal microglia mediates adolescent intermittent alcohol exposure-induced depression-like behaviors in mice
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The histone deacetylase inhibitor suberoylanilide hydroxamic acid (SAHA) alleviates depression-like behavior and normalizes epigenetic changes in the hippocampus during ethanol withdrawal
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Driving the downward spiral: alcohol-induced dysregulation of extended amygdala circuits and negative affect
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“A uthor M anuscript A uthor M anuscript A uthor M anuscript A uthor M anuscript of HDAC2 and HDAC4, which parallels increased anxiety-like behaviors 24h after bingeethanol exposure (Pandey et al., 2015).”
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Epigenetic and gene expression changes in the adolescent brain: What have we learned from animal models?
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Sustained alterations in neuroimmune gene expression after daily, but not intermittent, alcohol exposure
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CRF 1 Receptor‐Dependent Increases in Irritability‐Like Behavior During Abstinence from Chronic Intermittent Ethanol Vapor Exposure
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Donepezil Reverses Dendritic Spine Morphology Adaptations and <i>Fmr1</i> Epigenetic Modifications in Hippocampus of Adult Rats After Adolescent Alcohol Exposure
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Repeated cycles of binge-like ethanol exposure induce immediate and delayed neurobehavioral changes and hippocampal dysfunction in adolescent female rats
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Gene Expression Changes in Glutamate and GABA-A Receptors, Neuropeptides, Ion Channels, and Cholesterol Synthesis in the Periaqueductal Gray Following Binge-Like Alcohol Drinking by Adolescent Alcohol-Preferring (P) Rats
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Adolescent intermittent ethanol reduces serotonin expression in the adult raphe nucleus and upregulates innate immune expression that is prevented by exercise
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Long-term ethanol self-administration induces ΔFosB in male and female adolescent, but not in adult, Wistar rats
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Postnatal Ethanol Exposure Activates HDAC-Mediated Histone Deacetylation, Impairs Synaptic Plasticity Gene Expression and Behavior in Mice
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Repeated mild traumatic brain injury causes persistent changes in histone deacetylase function in hippocampus: Implications in learning and memory deficits in rats
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Absence of compulsive drinking phenotype in adult male rats exposed to ethanol in a binge-like pattern during adolescence
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Adolescent binge alcohol exposure increases risk assessment behaviors in male Wistar rats after exposure to an acute psychological stressor in adulthood
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Adolescent alcohol exposure epigenetically regulates CREB signaling in the adult amygdala
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Epigenetic modification in alcohol use disorder and alcoholic cardiomyopathy: From pathophysiology to therapeutic opportunities
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Biological intersection of sex, age, and environment in the corticotropin releasing factor (CRF) system and alcohol
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Chronic intermittent ethanol during adolescence and adulthood alters dendritic spines in the primary motor and visual cortex in rats
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P.6.b.009 Alcohol intoxications during adolescence predict later vulnerability to alcohol self-administration in rats
Naassïla, M., Warnault, V., Kervern, M., Pierrefiche, O., Vilpoux, C., & Alaux‐Cantin, S. (2010) · European Neuropsychopharmacology · doi:10.1016/s0924-977x(10)70883-x
S31 * EPIGENETIC MECHANISMS OF ALCOHOLISM: FROM PRENATAL STAGE TO ADULTHOOD
Pandey, S. C., Naassïla, M., O'Brien, E. S., Warnault, V., Legastelois, R., Botia, B., Vilpoux, C., Alaux‐Cantin, S., Pierrefiche, O., Coley, R. L., et al. (2013) · Alcohol and Alcoholism · doi:10.1093/alcalc/agt109
Self-citation
A role for histone acetylation mechanisms in adolescent alcohol exposure-induced deficits in hippocampal brain-derived neurotrophic factor expression and neurogenesis markers in adulthood
Sakharkar, A. J., Vetreno, R. P., Zhang, H., Kokare, D. M., Crews, F. T., & Pandey, S. C. (2016) · Brain Structure and Function · doi:10.1007/s00429-016-1196-y · Cited by 122 · see citing works
Self-citation
Adolescent alcohol exposure alters lysine demethylase 1 (LSD1) expression and histone methylation in the amygdala during adulthood
Kyzar, E. J., Zhang, H., Sakharkar, A. J., & Pandey, S. C. (2016) · Addiction Biology · doi:10.1111/adb.12404 · Cited by 85 · see citing works
Self-citation
Altered amygdala DNA methylation mechanisms after adolescent alcohol exposure contribute to adult anxiety and alcohol drinking
Sakharkar, A. J., Kyzar, E. J., Gavin, D. P., Zhang, H., Chen, Y., Krishnan, H. R., Grayson, D. R., & Pandey, S. C. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.107679 · Cited by 75 · see citing works
Self-citation

Authors: Pandey, S. C., Sakharkar, A. J., Tang, L., & Zhang, H.
Affiliations: University of Illinois Chicago (US)
Corresponding author: Pandey, Subhash C.
ORCID: Pandey, Subhash C.
Sakharkar, Amul J.
Tang, Lei
Venue: Neurobiology of Disease
Publisher: Elsevier BV
Published: 2015-10
Volume: 82
Pages: 607-619
ISSN: 0969-9961 (ISSN-L)
DOI: 10.1016/j.nbd.2015.03.019
PMC: PMC4581895
OpenAlex: W1997141979
Cited by: 191
References: 68
Citations by year: 2026: 5 · 2025: 12 · 2024: 16 · 2023: 17 · 2022: 18 · 2021: 24 · 2020: 18 · 2019: 25 · 2018: 15 · 2017: 16 · 2016: 19 · 2015: 6
FWCI: 8.10
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: Neurobiology of Disease (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: National Institute on Alcohol Abuse and Alcoholism (AA-019971)
AA-010005
AA-013341
Department of Veterans Affairs (I01BX000143)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Histone Deacetylase Inhibitors Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: adolescent intermittent ethanol exposure, binge drinking, histone modifications, histone H3 acetylation, histone deacetylase, trichostatin A, amygdala, anxiety-like behavior, alcoholism, alcohol consumption, brain-derived neurotrophic factor, Arc protein, dendritic spine density, central amygdala, medial amygdala, epigenetic modifications, synaptic plasticity
MeSH terms: Underage Drinking, Acetylation, Ethanol, Alcoholism, Animals, Anxiety Disorders, Brain, Central Nervous System Depressants, Cytoskeletal Proteins, Disease Models, Animal, Histones, Hydroxamic Acids, Male, Nerve Tissue Proteins, Gene Expression, Rats, Sprague-Dawley, Brain-Derived Neurotrophic Factor, Histone Deacetylase 2, Histone Deacetylase Inhibitors, Binge Drinking

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Potential role of adolescent alcohol exposure-induced amygdaloid histone modifications in anxiety and alcohol intake during adulthood

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