Early-life stress and ovarian hormones alter transcriptional regulation in the nucleus accumbens resulting in sex-specific responses to cocaine
Early-life stress and ovarian hormones contribute to increased female vulnerability to cocaine addiction. Here, we reveal molecular substrates in the reward area, the nucleus accumbens, through which these female-specific factors affect immediate and conditioning responses to cocaine. We find shared...
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| Published in | Cell reports (Cambridge) Vol. 42; no. 10; p. 113187 |
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| Main Authors | , , , , , , |
| Format | Journal Article |
| Language | English |
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United States
Elsevier Inc
31.10.2023
Elsevier |
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| Abstract | Early-life stress and ovarian hormones contribute to increased female vulnerability to cocaine addiction. Here, we reveal molecular substrates in the reward area, the nucleus accumbens, through which these female-specific factors affect immediate and conditioning responses to cocaine. We find shared involvement of X chromosome inactivation-related and estrogen signaling-related gene regulation in enhanced conditioning responses following early-life stress and during the low-estrogenic state in females. Low-estrogenic females respond to acute cocaine by opening neuronal chromatin enriched for the sites of ΔFosB, a transcription factor implicated in chronic cocaine response and addiction. Conversely, high-estrogenic females respond to cocaine by preferential chromatin closing, providing a mechanism for limiting cocaine-driven chromatin and synaptic plasticity. We find that physiological estrogen withdrawal, early-life stress, and absence of one X chromosome all nullify the protective effect of a high-estrogenic state on cocaine conditioning in females. Our findings offer a molecular framework to enable understanding of sex-specific neuronal mechanisms underlying cocaine use disorder.
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•Early-life stress more strongly alters gene expression and cocaine reward in females•Ovarian hormone status affects cocaine-induced chromatin and behavioral changes•Acute cocaine causes sex- and estrous cycle-dependent increased accessibility of ΔFosB sites•X chromosome inactivation mechanistically links female-specific risk factors and cocaine use
Rocks et al. reveal transcriptional mechanisms through which female-specific factors, early-life stress and ovarian hormones, induce sex-specific cocaine responses. Both factors alter X chromosome inactivation-related and estrogen signaling-related gene regulation in the nucleus accumbens. Cocaine acutely enhances ΔFosB-site accessibility, especially in low-estrogenic females, providing a “priming” mechanism for future exposures. |
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| AbstractList | Early-life stress and ovarian hormones contribute to increased female vulnerability to cocaine addiction. Here, we reveal molecular substrates in the reward area, the nucleus accumbens, through which these female-specific factors affect immediate and conditioning responses to cocaine. We find shared involvement of X chromosome inactivation-related and estrogen signaling-related gene regulation in enhanced conditioning responses following early-life stress and during the low-estrogenic state in females. Low-estrogenic females respond to acute cocaine by opening neuronal chromatin enriched for the sites of ΔFosB, a transcription factor implicated in chronic cocaine response and addiction. Conversely, high-estrogenic females respond to cocaine by preferential chromatin closing, providing a mechanism for limiting cocaine-driven chromatin and synaptic plasticity. We find that physiological estrogen withdrawal, early-life stress, and absence of one X chromosome all nullify the protective effect of a high-estrogenic state on cocaine conditioning in females. Our findings offer a molecular framework to enable understanding of sex-specific neuronal mechanisms underlying cocaine use disorder. Early-life stress and ovarian hormones contribute to increased female vulnerability to cocaine addiction. Here, we reveal molecular substrates in the reward area, the nucleus accumbens, through which these female-specific factors affect immediate and conditioning responses to cocaine. We find shared involvement of X chromosome inactivation-related and estrogen signaling-related gene regulation in enhanced conditioning responses following early-life stress and during the low-estrogenic state in females. Low-estrogenic females respond to acute cocaine by opening neuronal chromatin enriched for the sites of ΔFosB, a transcription factor implicated in chronic cocaine response and addiction. Conversely, high-estrogenic females respond to cocaine by preferential chromatin closing, providing a mechanism for limiting cocaine-driven chromatin and synaptic plasticity. We find that physiological estrogen withdrawal, early-life stress, and absence of one X chromosome all nullify the protective effect of a high-estrogenic state on cocaine conditioning in females. Our findings offer a molecular framework to enable understanding of sex-specific neuronal mechanisms underlying cocaine use disorder. [Display omitted] •Early-life stress more strongly alters gene expression and cocaine reward in females•Ovarian hormone status affects cocaine-induced chromatin and behavioral changes•Acute cocaine causes sex- and estrous cycle-dependent increased accessibility of ΔFosB sites•X chromosome inactivation mechanistically links female-specific risk factors and cocaine use Rocks et al. reveal transcriptional mechanisms through which female-specific factors, early-life stress and ovarian hormones, induce sex-specific cocaine responses. Both factors alter X chromosome inactivation-related and estrogen signaling-related gene regulation in the nucleus accumbens. Cocaine acutely enhances ΔFosB-site accessibility, especially in low-estrogenic females, providing a “priming” mechanism for future exposures. Early-life stress and ovarian hormones contribute to increased female vulnerability to cocaine addiction. Here, we reveal molecular substrates in the reward area, the nucleus accumbens, through which these female-specific factors affect immediate and conditioning responses to cocaine. We find shared involvement of X chromosome inactivation-related and estrogen signaling-related gene regulation in enhanced conditioning responses following early-life stress and during the low-estrogenic state in females. Low-estrogenic females respond to acute cocaine by opening neuronal chromatin enriched for the sites of ΔFosB, a transcription factor implicated in chronic cocaine response and addiction. Conversely, high-estrogenic females respond to cocaine by preferential chromatin closing, providing a mechanism for limiting cocaine-driven chromatin and synaptic plasticity. We find that physiological estrogen withdrawal, early-life stress, and absence of one X chromosome all nullify the protective effect of a high-estrogenic state on cocaine conditioning in females. Our findings offer a molecular framework to enable understanding of sex-specific neuronal mechanisms underlying cocaine use disorder.Early-life stress and ovarian hormones contribute to increased female vulnerability to cocaine addiction. Here, we reveal molecular substrates in the reward area, the nucleus accumbens, through which these female-specific factors affect immediate and conditioning responses to cocaine. We find shared involvement of X chromosome inactivation-related and estrogen signaling-related gene regulation in enhanced conditioning responses following early-life stress and during the low-estrogenic state in females. Low-estrogenic females respond to acute cocaine by opening neuronal chromatin enriched for the sites of ΔFosB, a transcription factor implicated in chronic cocaine response and addiction. Conversely, high-estrogenic females respond to cocaine by preferential chromatin closing, providing a mechanism for limiting cocaine-driven chromatin and synaptic plasticity. We find that physiological estrogen withdrawal, early-life stress, and absence of one X chromosome all nullify the protective effect of a high-estrogenic state on cocaine conditioning in females. Our findings offer a molecular framework to enable understanding of sex-specific neuronal mechanisms underlying cocaine use disorder. Early-life stress and ovarian hormones contribute to increased female vulnerability to cocaine addiction. Here, we reveal molecular substrates in the reward area, the nucleus accumbens, through which these female-specific factors affect immediate and conditioning responses to cocaine. We find shared involvement of X chromosome inactivation-related and estrogen signaling-related gene regulation in enhanced conditioning responses following early-life stress and during the low-estrogenic state in females. Low-estrogenic females respond to acute cocaine by opening neuronal chromatin enriched for the sites of ΔFosB, a transcription factor implicated in chronic cocaine response and addiction. Conversely, high-estrogenic females respond to cocaine by preferential chromatin closing, providing a mechanism for limiting cocaine-driven chromatin and synaptic plasticity. We find that physiological estrogen withdrawal, early-life stress, and absence of one X chromosome all nullify the protective effect of a high-estrogenic state on cocaine conditioning in females. Our findings offer a molecular framework to enable understanding of sex-specific neuronal mechanisms underlying cocaine use disorder. Rocks et al. reveal transcriptional mechanisms through which female-specific factors, early-life stress and ovarian hormones, induce sex-specific cocaine responses. Both factors alter X chromosome inactivation-related and estrogen signaling-related gene regulation in the nucleus accumbens. Cocaine acutely enhances ΔFosB-site accessibility, especially in low-estrogenic females, providing a ‘‘priming’’ mechanism for future exposures. |
| ArticleNumber | 113187 |
| Author | Kundakovic, Marija Bellia, Fabio Jaric, Ivana Rocks, Devin Cham, Heining Suzuki, Masako Greally, John M. |
| AuthorAffiliation | 2 Department of Psychology, Fordham University, Bronx, NY, USA 6 Lead contact 5 Present address: Animal Welfare Division, Vetsuisse Faculty, University of Bern, Bern, Switzerland 1 Department of Biological Sciences, Fordham University, Bronx, NY, USA 3 Center for Epigenomics, Department of Genetics, Albert Einstein College of Medicine, Bronx, NY, USA 4 Department of Nutrition, Texas A&M University, College Station, TX, USA |
| AuthorAffiliation_xml | – name: 2 Department of Psychology, Fordham University, Bronx, NY, USA – name: 4 Department of Nutrition, Texas A&M University, College Station, TX, USA – name: 6 Lead contact – name: 5 Present address: Animal Welfare Division, Vetsuisse Faculty, University of Bern, Bern, Switzerland – name: 3 Center for Epigenomics, Department of Genetics, Albert Einstein College of Medicine, Bronx, NY, USA – name: 1 Department of Biological Sciences, Fordham University, Bronx, NY, USA |
| Author_xml | – sequence: 1 givenname: Devin surname: Rocks fullname: Rocks, Devin organization: Department of Biological Sciences, Fordham University, Bronx, NY, USA – sequence: 2 givenname: Ivana surname: Jaric fullname: Jaric, Ivana organization: Department of Biological Sciences, Fordham University, Bronx, NY, USA – sequence: 3 givenname: Fabio surname: Bellia fullname: Bellia, Fabio organization: Department of Biological Sciences, Fordham University, Bronx, NY, USA – sequence: 4 givenname: Heining surname: Cham fullname: Cham, Heining organization: Department of Psychology, Fordham University, Bronx, NY, USA – sequence: 5 givenname: John M. surname: Greally fullname: Greally, John M. organization: Center for Epigenomics, Department of Genetics, Albert Einstein College of Medicine, Bronx, NY, USA – sequence: 6 givenname: Masako surname: Suzuki fullname: Suzuki, Masako organization: Center for Epigenomics, Department of Genetics, Albert Einstein College of Medicine, Bronx, NY, USA – sequence: 7 givenname: Marija orcidid: 0000-0002-6734-4217 surname: Kundakovic fullname: Kundakovic, Marija email: mkundakovic@fordham.edu organization: Department of Biological Sciences, Fordham University, Bronx, NY, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/37777968$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_1016_j_tins_2023_09_007 |
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| Issue | 10 |
| Keywords | reward ovarian hormones sex difference cocaine CP: Neuroscience nucleus accumbens chromatin epigenetic regulation early life stress gene expression neuroplasticity |
| Language | English |
| License | This is an open access article under the CC BY license. Copyright © 2023 The Author(s). Published by Elsevier Inc. All rights reserved. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS D.R., I.J., F.B., and M.K. performed experiments. D.R., H.C., and M.S. performed data analyses. D.R., H.C., M.S., and M.K. interpreted the data and constructed the figures. J.M.G. contributed computational resources. D.R. and M.K. wrote the article. M.K. conceived and directed the project. All authors commented on and approved the final version of the paper. |
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| SubjectTerms | Adverse Childhood Experiences Chromatin cocaine Cocaine - pharmacology CP: Neuroscience early life stress epigenetic regulation Estrogens - pharmacology Female gene expression Humans Male neuroplasticity Nucleus Accumbens ovarian hormones reward sex difference |
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| Title | Early-life stress and ovarian hormones alter transcriptional regulation in the nucleus accumbens resulting in sex-specific responses to cocaine |
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