Dopaminylation of histone H3 in ventral tegmental area regulates cocaine seeking

Vulnerability to relapse during periods of attempted abstinence from cocaine use is hypothesized to result from the rewiring of brain reward circuitries, particularly ventral tegmental area (VTA) dopamine neurons. How cocaine exposures act on midbrain dopamine neurons to precipitate addiction-releva...

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Vydáno v:	Science (American Association for the Advancement of Science) Ročník 368; číslo 6487; s. 197
Hlavní autoři:	Lepack, Ashley E, Werner, Craig T, Stewart, Andrew F, Fulton, Sasha L, Zhong, Ping, Farrelly, Lorna A, Smith, Alexander C W, Ramakrishnan, Aarthi, Lyu, Yang, Bastle, Ryan M, Martin, Jennifer A, Mitra, Swarup, O'Connor, Richard M, Wang, Zi-Jun, Molina, Henrik, Turecki, Gustavo, Shen, Li, Yan, Zhen, Calipari, Erin S, Dietz, David M, Kenny, Paul J, Maze, Ian
Médium:	Journal Article
Jazyk:	angličtina
Vydáno:	United States 10.04.2020
Témata:	Animals Cocaine - adverse effects Cocaine-Related Disorders - genetics Cocaine-Related Disorders - metabolism Cocaine-Related Disorders - psychology Dopamine - metabolism Dopaminergic Neurons - metabolism Drug-Seeking Behavior Gene Expression Regulation Glutamine - metabolism Histones - metabolism Humans Male Mice Mice, Inbred C57BL Neuronal Plasticity Nucleus Accumbens - metabolism Rats Rats, Sprague-Dawley Synaptic Transmission Ventral Tegmental Area - metabolism
ISSN:	1095-9203, 1095-9203
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Abstract	Vulnerability to relapse during periods of attempted abstinence from cocaine use is hypothesized to result from the rewiring of brain reward circuitries, particularly ventral tegmental area (VTA) dopamine neurons. How cocaine exposures act on midbrain dopamine neurons to precipitate addiction-relevant changes in gene expression is unclear. We found that histone H3 glutamine 5 dopaminylation (H3Q5dop) plays a critical role in cocaine-induced transcriptional plasticity in the midbrain. Rats undergoing withdrawal from cocaine showed an accumulation of H3Q5dop in the VTA. By reducing H3Q5dop in the VTA during withdrawal, we reversed cocaine-mediated gene expression changes, attenuated dopamine release in the nucleus accumbens, and reduced cocaine-seeking behavior. These findings establish a neurotransmission-independent role for nuclear dopamine in relapse-related transcriptional plasticity in the VTA.
AbstractList	Vulnerability to relapse during periods of attempted abstinence from cocaine use is hypothesized to result from the rewiring of brain reward circuitries, particularly ventral tegmental area (VTA) dopamine neurons. How cocaine exposures act on midbrain dopamine neurons to precipitate addiction-relevant changes in gene expression is unclear. We found that histone H3 glutamine 5 dopaminylation (H3Q5dop) plays a critical role in cocaine-induced transcriptional plasticity in the midbrain. Rats undergoing withdrawal from cocaine showed an accumulation of H3Q5dop in the VTA. By reducing H3Q5dop in the VTA during withdrawal, we reversed cocaine-mediated gene expression changes, attenuated dopamine release in the nucleus accumbens, and reduced cocaine-seeking behavior. These findings establish a neurotransmission-independent role for nuclear dopamine in relapse-related transcriptional plasticity in the VTA. Vulnerability to relapse during periods of attempted abstinence from cocaine use is hypothesized to result from the rewiring of brain reward circuitries, particularly ventral tegmental area (VTA) dopamine neurons. How cocaine exposures act on midbrain dopamine neurons to precipitate addiction-relevant changes in gene expression is unclear. We found that histone H3 glutamine 5 dopaminylation (H3Q5dop) plays a critical role in cocaine-induced transcriptional plasticity in the midbrain. Rats undergoing withdrawal from cocaine showed an accumulation of H3Q5dop in the VTA. By reducing H3Q5dop in the VTA during withdrawal, we reversed cocaine-mediated gene expression changes, attenuated dopamine release in the nucleus accumbens, and reduced cocaine-seeking behavior. These findings establish a neurotransmission-independent role for nuclear dopamine in relapse-related transcriptional plasticity in the VTA.Vulnerability to relapse during periods of attempted abstinence from cocaine use is hypothesized to result from the rewiring of brain reward circuitries, particularly ventral tegmental area (VTA) dopamine neurons. How cocaine exposures act on midbrain dopamine neurons to precipitate addiction-relevant changes in gene expression is unclear. We found that histone H3 glutamine 5 dopaminylation (H3Q5dop) plays a critical role in cocaine-induced transcriptional plasticity in the midbrain. Rats undergoing withdrawal from cocaine showed an accumulation of H3Q5dop in the VTA. By reducing H3Q5dop in the VTA during withdrawal, we reversed cocaine-mediated gene expression changes, attenuated dopamine release in the nucleus accumbens, and reduced cocaine-seeking behavior. These findings establish a neurotransmission-independent role for nuclear dopamine in relapse-related transcriptional plasticity in the VTA.
Author	Ramakrishnan, Aarthi Lepack, Ashley E Dietz, David M Smith, Alexander C W Lyu, Yang Zhong, Ping Mitra, Swarup Shen, Li Calipari, Erin S Farrelly, Lorna A Stewart, Andrew F Werner, Craig T Martin, Jennifer A Bastle, Ryan M Fulton, Sasha L Kenny, Paul J Molina, Henrik Wang, Zi-Jun Maze, Ian O'Connor, Richard M Turecki, Gustavo Yan, Zhen
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0000-0002-8891-344X surname: Zhong fullname: Zhong, Ping organization: Department of Physiology and Biophysics, Jacobs School of Medicine and Biomedical Sciences, State University of New York at Buffalo, Buffalo, NY 14203, USA – sequence: 6 givenname: Lorna A surname: Farrelly fullname: Farrelly, Lorna A organization: Department of Neuroscience, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – sequence: 7 givenname: Alexander C W orcidid: 0000-0001-7724-6234 surname: Smith fullname: Smith, Alexander C W organization: Department of Neuroscience, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – sequence: 8 givenname: Aarthi orcidid: 0000-0002-6329-6502 surname: Ramakrishnan fullname: Ramakrishnan, Aarthi organization: Department of Neuroscience, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – sequence: 9 givenname: Yang orcidid: 0000-0002-4442-9015 surname: Lyu fullname: Lyu, Yang organization: Department of Neuroscience, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – sequence: 10 givenname: Ryan M orcidid: 0000-0003-3184-0398 surname: Bastle fullname: Bastle, Ryan M organization: Department of Neuroscience, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – sequence: 11 givenname: Jennifer A orcidid: 0000-0002-6854-1319 surname: Martin fullname: Martin, Jennifer A organization: Department of Pharmacology and Toxicology, Program in Neuroscience, State University of New York at Buffalo, Buffalo, NY 14214, USA – sequence: 12 givenname: Swarup surname: Mitra fullname: Mitra, Swarup organization: Department of Pharmacology and Toxicology, Program in Neuroscience, State University of New York at Buffalo, Buffalo, NY 14214, USA – sequence: 13 givenname: Richard M surname: O'Connor fullname: O'Connor, Richard M organization: Department of Neuroscience, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – sequence: 14 givenname: Zi-Jun surname: Wang fullname: Wang, Zi-Jun organization: Department of Physiology and Biophysics, Jacobs School of Medicine and Biomedical Sciences, State University of New York at Buffalo, Buffalo, NY 14203, USA – sequence: 15 givenname: Henrik orcidid: 0000-0001-8950-4990 surname: Molina fullname: Molina, Henrik organization: Proteomics Resource Center, The Rockefeller University, New York, NY 10065, USA – sequence: 16 givenname: Gustavo surname: Turecki fullname: Turecki, Gustavo organization: Department of Psychiatry, McGill University, Montreal, QC H3A 1A1, Canada – sequence: 17 givenname: Li orcidid: 0000-0002-5190-2851 surname: Shen fullname: Shen, Li organization: Department of Neuroscience, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – sequence: 18 givenname: Zhen orcidid: 0000-0002-3519-9596 surname: Yan fullname: Yan, Zhen organization: Department of Physiology and Biophysics, Jacobs School of Medicine and Biomedical Sciences, State University of New York at Buffalo, Buffalo, NY 14203, USA – sequence: 19 givenname: Erin S orcidid: 0000-0003-4723-0623 surname: Calipari fullname: Calipari, Erin S organization: Department of Pharmacology, Center for Addiction Research, Vanderbilt University School of Medicine, Nashville, TN 37232, USA – sequence: 20 givenname: David M orcidid: 0000-0002-6927-9236 surname: Dietz fullname: Dietz, David M organization: Department of Pharmacology and Toxicology, Program in Neuroscience, State University of New York at Buffalo, Buffalo, NY 14214, USA – sequence: 21 givenname: Paul J surname: Kenny fullname: Kenny, Paul J organization: Department of Neuroscience, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA – sequence: 22 givenname: Ian orcidid: 0000-0003-1490-7781 surname: Maze fullname: Maze, Ian email: ian.maze@mssm.edu organization: Department of Pharmacological Sciences, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA
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Copyright	Copyright © 2020 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.
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Snippet	Vulnerability to relapse during periods of attempted abstinence from cocaine use is hypothesized to result from the rewiring of brain reward circuitries,...
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SubjectTerms	Animals Cocaine - adverse effects Cocaine-Related Disorders - genetics Cocaine-Related Disorders - metabolism Cocaine-Related Disorders - psychology Dopamine - metabolism Dopaminergic Neurons - metabolism Drug-Seeking Behavior Gene Expression Regulation Glutamine - metabolism Histones - metabolism Humans Male Mice Mice, Inbred C57BL Neuronal Plasticity Nucleus Accumbens - metabolism Rats Rats, Sprague-Dawley Synaptic Transmission Ventral Tegmental Area - metabolism
Title	Dopaminylation of histone H3 in ventral tegmental area regulates cocaine seeking
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