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COMMENTARY

Identification of stress-induced epigenetic methylation onto dopamine D2 gene and neurological and behavioral consequences

Kenneth Blum1,2,3,4,5,6,7,8,9* ,  Abdalla Bowirrat1 ,  David Baron2 ,  Igor Elman9,10 ,  Milan T. Makale11 ,  Jean Lud Cadet12 ,  Panayotis K. Thanos13 ,  Colin Hanna13 ,  Rania Ahmed13 ,  Marjorie C. Gondre-Lewis14 ,  Catherine A. Dennen15 ,  Eric R. Braverman6 ,  Diwanshu Soni2 ,  Paul Carney16 ,  Jag Khalsa17 ,  Edward J. Modestino18 ,  Debmalya Barh7,19 ,  Debasis Bagchi20 ,  Rajendra D. Badgaiyan21 ,  Thomas McLaughlin6 ,  Rene Cortese22 ,  Mauro Ceccanti23 ,  Kevin T. Murphy24 ,  Ashim Gupta25 ,  Miles T. Makale26 ,  Keerthy Sunder9,27 ,  Mark S. Gold28
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1 Department of Molecular Biology, Adelson School of Medicine, Ariel University, Ariel, Israel
2 Division of Addiction Research & Education, Center for Sports, Exercise & Mental Health, Western University of the Health Sciences, Pomona, CA, United States of America
3 Institute of Psychology, ELTE Eötvös Loránd University, Budapest, Hungary
4 Department of Psychiatry, University of Vermont, Burlington, VT 05405, United States of America
5 Department of Psychiatry, Wright University Boonshoft School of Medicine, Dayton, OH, United States of America
6 Division of Nutrigenomics, The Kenneth Blum Behavioral Neurogenetic Institute, Austin, TX United States of America
7 Centre for Genomics and Applied Gene Technology, Institute of Integrative Omics and Applied Biotechnology, Nonakuri, Purba Medinipur, West Bengal, India
8 Department of Nutrigenomic Research, Victory Nutrition International, Inc., Bonita Springs, FL, United States of America
9 Division of Personalized Neuromodulation Research, Sunder Foundation, Palm Springs, CA, United States of America
10 Cambridge Health Alliance, Harvard Medical School, Cambridge, MA, United States of America
11 Department of Radiation Medicine and Applied Sciences, UC San Diego, 3855 Health Sciences Drive, La Jolla, CA 92093-0819, United States of America
12 Molecular Neuropsychiatry Research Branch, National Institute on Drug Abuse, National Institutes of Health, Bethesda, MD., United States of America
13 Behavioral Neuropharmacology and Neuroimaging Laboratory on Addictions, Clinical Research Institute on Addictions, Department of Pharmacology and Toxicology, Jacobs School of Medicine and Biosciences, State University of New York at Buffalo, Buffalo, NY; Department of Psychology, State University of New York at Buffalo, Buffalo, NY., United States of America
14 Department of Anatomy, Howard University College of Medicine, and Developmental Neuropsychopharmacology Laboratory, Howard University College of Medicine, Washington D.C., United States of America
15 Department of Family Medicine, Jefferson Health Northeast, Philadelphia, PA, United States of America
16 Division Pediatric Neurology, University of Missouri, School of Medicine, Columbia, MO., United States of America
17 Department of Microbiology, Immunology and Tropical Medicine, George Washington University, School of Medicine and Health Sciences, Washington, DC, United States of America
18 Department of Psychology, Curry College, Milton, MA., United States of America
19 Departamento de Genética, Ecologia e Evolução, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil
20 Department of Pharmaceutical Sciences, Texas Southern University College of Pharmacy and Health Sciences, Houston, TX, United States of America
21 Department of Psychiatry, Case Western Reserve University School of Medicine, Cleveland OH., 44106, USA and Department of Psychiatry, Mt. Sinai School of Medicine, New York, NY, United States of America
22 Department of Child Health – Child Health Research Institute, & Department of Obstetrics, Gynecology and Women’s Health School of Medicine, University of Missouri, MO, United States of America
23 Alcohol Addiction Program, Latium Region Referral Center, Sapienza University of Rome, Roma, Italy
24 Division of Personalized Neuromodulation and Patient Care, PeakLogic, LLC, Del Mar, CA, United States of America
25 Future Biologics, Lawrenceville, Georgia, 30043, United States of America
26 Department of Psychology, UC San Diego, 3855 Health Sciences Drive, La Jolla, CA 92093-0819, United States of America
27 Department of Psychiatry, UC Riverside School of Medicine, Riverside, CA, United States of America
28 Department of Psychiatry, Washington University School of Medicine, St. Louis, MO, United States of America
GPD 2024, 3(1), 1966 https://doi.org/10.36922/gpd.1966
Submitted: 29 September 2023 | Accepted: 14 December 2023 | Published: 29 March 2024
© 2024 by the Author (s). This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution 4.0 International License ( https://creativecommons.org/licenses/by/4.0/ )
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Abstract

The D2 dopamine receptor (DRD2) gene has garnered substantial attention as one of the most extensively studied genes across various neuropsychiatric disorders. Since its initial association with severe alcoholism in 1990, particularly through the identification of the DRD2 Taq A1 allele, numerous international investigations have been conducted to elucidate its role in different conditions. As of February 22, 2024, there are 5485 articles focusing on the DRD2 gene listed in PUBMED. There have been 120 meta-analyses with mixed results. In our opinion, the primary cause of negative reports regarding the association of various DRD2 gene polymorphisms is the inadequate screening of controls, not adequately eliminating many hidden reward deficiency syndrome behaviors. Moreover, pleiotropic effects of DRD2 variants have been identified in neuropsychologic, neurophysiologic, stress response, social stress defeat, maternal deprivation, and gambling disorder, with epigenetic DNA methylation and histone post-translational negative methylation identified as discussed in this article. There are 70 articles listed in PUBMED for DNA methylation and 20 articles listed for histone methylation as of October 19, 2022. For this commentary, we did not denote DNA and/or histone methylation; instead, we provided a brief summary based on behavioral effects. Based on the fact that Blum and Noble characterized the DRD2 Taq A1 allele as a generalized reward gene and not necessarily specific alcoholism, it now behooves the field to find ways to either use effector moieties to edit the neuroepigenetic insults or possibly harness the idea of potentially removing negative mRNA-reduced expression by inducing “dopamine homeostasis.”

Keywords
Dopamine D2 receptor
Epigenetic modification
Neurological disorders
Stress
Funding
None.
Conflict of interest
Kenneth Blum holds patents, both domestic and foreign, related to pro-dopamine regulation complexes and genetic testing for addiction risk. Other authors declare no conflict of interest.
References
  1. Domi E, Domi A, Adermark L, Heilig M, Augier E. Neurobiology of alcohol seeking behavior. J Neurochem. 2021;157(5):1585-1614. doi: 10.1111/jnc.15343

 

  1. Haass-Koffler CL, Magill M, Cannella N, et al. Mifepristone as a pharmacological intervention for stress-induced alcohol craving: A human laboratory study. Addict Biol. 2023;28(7):e13288. doi: 10.1111/adb.13288

 

  1. Blum, K, Chen TJH, Meshkin B, et al. Manipulation of catechol-O-methyl-transferase (COMT) activity to influence the attenuation of substance seeking behavior, a subtype of Reward Deficiency Syndrome (RDS), is dependent upon gene polymorphisms: A hypothesis. Med Hypotheses. 2007;69(5):1054-1060. doi: 10.1016/j.mehy.2006.12.062

 

  1. Blum K, Trachtenberg MC, Elliott CE, et al. Enkephalinase inhibition and precursor amino acid loading improves inpatient treatment of alcohol and polydrug abusers: Double-blind placebo-controlled study of the nutritional adjunct SAAVE. Alcohol. 1988;5(6):481-493. doi: 10.1016/0741-8329(88)90087-0

 

  1. Blum K, Chen ALC, Chen TJH, et al. Activation instead of blocking mesolimbic dopaminergic reward circuitry is a preferred modality in the long term treatment of reward deficiency syndrome (RDS): A commentary. Theor Biol Med Model. 2008;5:24. doi: 10.1186/1742-4682-5-24

 

  1. Blum K, Giordano J, Morse S, et al. Understanding the hugh mind: Humans are still evolving genetically. Tne IIOAB. 2010;1:1-14.

 

  1. Drug Overdose Deaths; 2023. Available from: https://www. cdc.gov/drugoverdose/deaths/index.html [Last accessed on 2024 Jan 29].

 

  1. 2022 Overdose Epidemic Report. Available from: https:// end-overdose-epidemic.org/highlights/ama-reports/2022- report [Last accessed on 2024 Mar 07].

 

  1. Comings DE, Blum K. Reward deficiency syndrome: Genetic aspects of behavioral disorders. Prog Brain Res. 2000;126:325-341. doi: 10.1016/S0079-6123(00)26022-6

 

  1. Blum K, Chen AL, Oscar-Berman M, et al. Generational association studies of dopaminergic genes in reward deficiency syndrome (RDS) subjects: Selecting appropriate phenotypes for reward dependence behaviors. Int J Environ Res Public Health. 2011;8(12):4425-4459. doi: 10.3390/ijerph8124425

 

  1. Febo M, Blum K, Badgaiyan RD, et al. Dopamine homeostasis: Brain functional connectivity in reward deficiency syndrome. Front Biosci (Landmark Ed). 2017;22(4):669-691. doi: 10.2741/4509

 

  1. Gold MS, Blum K, Febo M, et al. Molecular role of dopamine in anhedonia linked to reward deficiency syndrome (RDS) and anti- reward systems. Front Biosci (Schol Ed). 2018;10(2):309-325. doi: 10.2741/s518

 

  1. Borsook D, Linnman C, Faria V, Strassman AM, Becerra L, Elman I. Reward deficiency and anti-reward in pain chronification. Neurosci Biobehav Rev. 2016;68:282-297. doi: 10.1016/j.neubiorev.2016.05.033

 

  1. Bowirrat A, Oscar-Berman M. Relationship between dopaminergic neurotransmission, alcoholism, and reward deficiency syndrome. Am J Med Genet B Neuropsychiatr Genet. 2005;132b(1):29-37. doi: 10.1002/ajmg.b.30080

 

  1. Filippi A, Mueller T, Driever W. Vglut2 and gad expression reveal distinct patterns of dual GABAergic versus glutamatergic cotransmitter phenotypes of dopaminergic and noradrenergic neurons in the zebrafish brain. J Comp Neurol. 2014;522(9):2019-2037. doi: 10.1002/cne.23524

 

  1. Valentino RJ, Koroshetz W, Volkow ND. Neurobiology of the opioid epidemic: Basic and translational perspectives. Biol Psychiatry. 2020;87(1):2-3. doi: 10.1016/j.biopsych.2019.09.003

 

  1. Browne CJ, Godino A, Salery M, Nestler EJ. Epigenetic mechanisms of opioid addiction. Biol Psychiatry. 2020;87(1):22-33. doi: 10.1016/j.biopsych.2019.06.027

 

  1. Rosell DR, Siever LJ. The neurobiology of aggression and violence. CNS Spectr. 2015;20(3):254-279. doi: 10.1017/S109285291500019X

 

  1. Mahna D, Puri S, Sharma S. DNA methylation signatures: Biomarkers of drug and alcohol abuse. Mutat Res Rev Mutat Res. 2018;777:19-28. doi: 10.1016/j.mrrev.2018.06.002

 

  1. D’Aquila PS, Elia D, Galistu A. Role of dopamine D1-like and D2-like receptors in the activation of ingestive behaviour in thirsty rats licking for water. Psychopharmacology (Berl). 2019;236(12):3497-3512. doi: 10.1007/s00213-019-05317-w

 

  1. Volkow ND, Morales M. The brain on drugs: From reward to addiction. Cell. 2015;162(4):712-725. doi: 10.1016/j.cell.2015.07.046

 

  1. Yamamoto K, Fontaine R, Pasqualini C, Vernier P. Classification of dopamine receptor genes in vertebrates: Nine subtypes in osteichthyes. Brain Behav Evol. 2015;86(3-4):164-175. doi: 10.1159/000441550

 

  1. Noble EP, Blum K, Ritchie T, Montgomery A, Sheridan PJ. Allelic association of the D2 dopamine receptor gene with receptor-binding characteristics in alcoholism. Arch Gen Psychiatry. 1991;48(7):648-654. doi: 10.1001/archpsyc.1991.01810310066012

 

  1. Volkow ND, Chang L, Wang GJ, et al. Low level of brain dopamine D2 receptors in methamphetamine abusers: Association with metabolism in the orbitofrontal cortex. Am J Psychiatry. 2001;158(12):2015-2021. doi: 10.1176/appi.ajp.158.12.2015

 

  1. Volkow ND, Wang GJ, Telang F, et al. Low dopamine striatal D2 receptors are associated with prefrontal metabolism in obese subjects: Possible contributing factors. Neuroimage. 2008;42(4):1537-1543. doi: 10.1016/j.neuroimage.2008.06.002

 

  1. Noble EP, Blum K, Khalsa ME, et al. Allelic association of the D2 dopamine receptor gene with cocaine dependence. Drug Alcohol Depend. 1993;33(3):271-285. doi: 10.1016/0376-8716(93)90113-5

 

  1. Deng XD, Jiang H, Ma Y, et al. Association between DRD2/ANKK1 TaqIA polymorphism and common illicit drug dependence: Evidence from a meta-analysis. Hum Immunol. 2015;76(1):42-51. doi: 10.1016/j.humimm.2014.12.005

 

  1. Vereczkei A, Barta C, Magi A, et al. FOXN3 and GDNF polymorphisms as common genetic factors of substance use and addictive behaviors. J Pers Med. 2022;12(5):690. doi: 10.3390/jpm12050690

 

  1. Dackis CA, Gold MS. Bromocriptine as treatment of cocaine abuse. Lancet. 1985;1(8438):1151-1152. doi: 10.1016/s0140-6736(85)92448-1

 

  1. Blum K, Cadet JL, Gold MS. Psychostimulant use disorder emphasizing methamphetamine and the opioid-dopamine connection: Digging out of a hypodopaminergic ditch. J Neurol Sci. 2021;420:117252. doi: 10.1016/j.jns.2020.117252

 

  1. Bogomolova EV, Rauschenbach IY, Adonyeva NV, Alekseev AA, Faddeeva NV, Gruntenko NE. Dopamine down-regulates activity of alkaline phosphatase in Drosophila: The role of D2-like receptors. J Insect Physiol. 2010;56(9):1155-1159. doi: 10.1016/j.jinsphys.2010.03.014

 

  1. Nestler EJ, Peña CJ, Kundakovic M, Mitchell A, Akbarian S. Epigenetic basis of mental illness. Neuroscientist. 2016;22(5):447-463. doi: 10.1177/1073858415608147

 

  1. Cadet JL, McCoy MT, Jayanthi S. Epigenetics and addiction. Clin Pharmacol Ther. 2016;99(5):502-511. doi: 10.1002/cpt.345

 

  1. Robison AJ, Nestler EJ. Transcriptional and epigenetic mechanisms of addiction. Nat Rev Neurosci. 2011;12(11):623-637. doi: 10.1038/nrn3111

 

  1. Hamilton PJ, Nestler EJ. Epigenetics and addiction. Curr Opin Neurobiol. 2019;59:128-136. doi: 10.1016/j.conb.2019.05.005

 

  1. Allis CD, Jenuwein T. The molecular hallmarks of epigenetic control. Nat Rev Genet. 2016;17(8):487-500. doi: 10.1038/nrg.2016.59

 

  1. Blum K, Gold MS, Cadet JL, et al. Dopaminylation in psychostimulant use disorder protects against psychostimulant seeking behavior by normalizing nucleus accumbens (NAc) dopamine expression. Curr Psychopharmacol. 2022;11(1):11-17. doi: 10.2174/2211556009666210108112737

 

  1. Bowman GD, Poirier MG. Post-translational modifications of histones that influence nucleosome dynamics. Chem Rev. 2015;115(6):2274-2295. doi: 10.1021/cr500350x

 

  1. Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res. 2011;21(3):381-395. doi: 10.1038/cr.2011.22

 

  1. Rogge GA, Wood MA. The role of histone acetylation in cocaine-induced neural plasticity and behavior. Neuropsychopharmacology. 2013;38(1):94-110. doi: 10.1038/npp.2012.154

 

  1. Egervari G, Ciccocioppo R, Jentsch JD, Hurd YL. Shaping vulnerability to addiction-the contribution of behavior, neural circuits and molecular mechanisms. Neurosci Biobehav Rev. 2018;85:117-125. doi: 10.1016/j.neubiorev.2017.05.019

 

  1. Kennedy PJ, Harvey E. Histone deacetylases as potential targets for cocaine addiction. CNS Neurol Disord Drug Targets. 2015;14(6):764-772. doi: 10.2174/1871527314666150529144804

 

  1. Archer T, Oscar-Berman M, Blum K, Gold M. Neurogenetics and epigenetics in impulsive behaviour: Impact on reward circuitry. J Genet Syndr Gene Ther. 2012;3(3):1000115. doi: 10.4172/2157-7412.1000115

 

  1. Archer T, Oscar-Berman M, Blum K. Epigenetics in developmental disorder: ADHD and endophenotypes. J Genet Syndr Gene Ther. 2011;2(104):1000104. doi: 10.4172/2157-7412.1000104

 

  1. Dennen CA, Blum K, Bowirrat A, et al. Neurogenetic and epigenetic aspects of cannabinoids. Epigenomes. 2022;6(3):27. doi: 10.3390/epigenomes6030027

 

  1. Blum K, Febo M, Smith DE, et al. Neurogenetic and epigenetic correlates of adolescent predisposition to and risk for addictive behaviors as a function of prefrontal cortex dysregulation. J Child Adolesc Psychopharmacol. 2015;25(4):286-292. doi: 10.1089/cap.2014.0146

 

  1. Blum K, Steinberg B, Gondre-Lewis MC, et al. A review of DNA risk alleles to determine epigenetic repair of mRNA expression to prove therapeutic effectiveness in Reward Deficiency Syndrome (RDS): Embracing “Precision Behavioral Management”. Psychol Res Behav Manag. 2021;14:2115-2134. doi: 10.2147/PRBM.S292958

 

  1. Archer T, Oscar-Berman M, Blum K, Gold M. Epigenetic modulation of mood disorders. J Genet Syndr Gene Ther. 2013;4(120):1000120. doi: 10.4172/2157-7412.1000120

 

  1. Blum K, Bowirrat A, Gondre Lewis MC, et al. Exploration of epigenetic state hyperdopaminergia (Surfeit) and genetic trait hypodopaminergia (Deficit) during adolescent brain development. Curr Psychopharmacol. 2021. doi: 10.2174/2211556010666210215155509

 

  1. Blum K, McLaughlin T, Modestino EJ, et al. Epigenetic repair of terrifying lucid dreams by enhanced brain reward functional connectivity and induction of dopaminergic homeostatic signaling. Curr Psychopharmacol. 2021. doi: 10.2174/2211556010666210215153513

 

  1. Edwards D, Roy AK 3rd, Boyett B, et al. Addiction by any other name is still addiction: Embracing molecular neurogenetic/epigenetic basis of reward deficiency. J Addict Sci. 2020;6(1):1-4.

 

  1. Blum K, Brodie MS, Pandey SC, et al. Researching mitigation of alcohol binge drinking in polydrug abuse: KCNK13 and RASGRF2 Gene(s) risk polymorphisms coupled with genetic addiction risk severity (GARS) guiding precision pro-dopamine regulation. J Pers Med. 2022;12(6):1009. doi: 10.3390/jpm12061009

 

  1. Zhang X, Yu H, Bai R, Ma C. Identification and characterization of biomarkers and their role in opioid addiction by integrated bioinformatics analysis. Front Neurosci. 2020;14:608349. doi: 10.3389/fnins.2020.608349

 

  1. Law PP, Holland ML. DNA methylation at the crossroads of gene and environment interactions. Essays Biochem. 2019;63(6):717-726. doi: 10.1042/EBC20190031

 

  1. Li CJ. DNA demethylation pathways: Recent insights. Genet Epigenet. 2013;5:43-49. doi: 10.4137/GEG.S12143

 

  1. Moore LD, Le T, Fan G. DNA methylation and its basic function. Neuropsychopharmacology. 2013;38(1):23-38. doi: 10.1038/npp.2012.112

 

  1. Jang HS, Shin WJ, Lee JE, Do JT. CpG and Non-CpG methylation in epigenetic gene regulation and brain function. Genes (Basel). 2017;8(6):148. doi: 10.3390/genes8060148

 

  1. Bogdanović O, Lister R. DNA methylation and the preservation of cell identity. Curr Opin Genet Dev. 2017;46:9-14. doi: 10.1016/j.gde.2017.06.007

 

  1. Sivalingam K, Samikkannu T. Neuroprotective effect of piracetam against cocaine-induced neuro epigenetic modification of DNA methylation in astrocytes. Brain Sci. 2020;10(9):611. doi: 10.3390/brainsci10090611

 

  1. Kulis M, Esteller M. DNA methylation and cancer. Adv Genet. 2010;70:27-56. doi: 10.1016/B978-0-12-380866-0.60002-2

 

  1. Dawson MA, Kouzarides T. Cancer epigenetics: From mechanism to therapy. Cell. 2012;150(1):12-27. doi: 10.1016/j.cell.2012.06.013

 

  1. Nishiyama A, Nakanishi M. Navigating the DNA methylation landscape of cancer. Trends Genet. 2021;37(11):1012-1027. doi: 10.1016/j.tig.2021.05.002

 

  1. Meng H, Cao Y, Qin J, et al. DNA methylation, its mediators and genome integrity. Int J Biol Sci. 2015;11(5):604-617. doi: 10.7150/ijbs.11218

 

  1. Cavalli G, Heard E. Advances in epigenetics link genetics to the environment and disease. Nature. 2019;571(7766):489-499. doi: 10.1038/s41586-019-1411-0

 

  1. Bajrami E, Spiroski M. Genomic imprinting. Open Access Maced J Med Sci. 2016;4(1):181-184. doi: 10.3889/oamjms.2016.028

 

  1. Cassidy SB, Schwartz S. Prader-Willi and Angelman syndromes. Disorders of genomic imprinting. Medicine (Baltimore). 1998;77(2):140-151. doi: 10.1097/00005792-199803000-00005

 

  1. Liu C, Jiao C, Wang K, Yuan N. DNA methylation and psychiatric disorders. Prog Mol Biol Transl Sci. 2018;157:175-232. doi: 10.1016/bs.pmbts.2018.01.006

 

  1. Zhang X, Fu R, Yu J, Wu X. DNA demethylation: Where genetics meets epigenetics. Curr Pharm Des. 2014;20(11):1625-1631. doi: 10.2174/13816128113199990546

 

  1. Bochtler M, Kolano A, Xu GL. DNA demethylation pathways: Additional players and regulators. Bioessays. 2017;39(1):1-13. doi: 10.1002/bies.201600178

 

  1. Kafer GR, Li X, Horii T, et al. 5-Hydroxymethylcytosine marks sites of DNA damage and promotes genome stability. Cell Rep. 2016;14(6):1283-1292. doi: 10.1016/j.celrep.2016.01.035

 

  1. Chen ZX, Riggs AD. DNA methylation and demethylation in mammals. J Biol Chem. 2011;286(21):18347-18353. doi: 10.1074/jbc.R110.205286.

 

  1. Wu X, Zhang Y. TET-mediated active DNA demethylation: Mechanism, function and beyond. Nat Rev Genet. 2017;18(9):517-534. doi: 10.1038/nrg.2017.33

 

  1. Ross SE, Bogdanovic O. TET enzymes, DNA demethylation and pluripotency. Biochem Soc Trans. 2019;47(3):875-885. doi: 10.1042/BST20180606

 

  1. An J, González-Avalos E, Chawla A, et al. Acute loss of TET function results in aggressive myeloid cancer in mice. Nat Commun. 2015;6:10071. doi: 10.1038/ncomms10071

 

  1. Dalton SR, Bellacosa A. DNA demethylation by TDG. Epigenomics. 2012;4(4):459-467. doi: 10.2217/epi.12.36

 

  1. Zentner GE, Henikoff S. Regulation of nucleosome dynamics by histone modifications. Nat Struct Mol Biol. 2013;20(3):259-266. doi: 10.1038/nsmb.2470

 

  1. Tessarz P, Kouzarides T. Histone core modifications regulating nucleosome structure and dynamics. Nat Rev Mol Cell Biol. 2014;15(11):703-708. doi: 10.1038/nrm3890

 

  1. Stillman B. Histone modifications: Insights into their influence on gene expression. Cell. 2018;175(1):6-9. doi: 10.1016/j.cell.2018.08.032

 

  1. Zhao Z, Shilatifard A. Epigenetic modifications of histones in cancer. Genome Biol. 2019;20(1):245. doi: 10.1186/s13059-019-1870-5

 

  1. Gräff J, Tsai LH. Histone acetylation: Molecular mnemonics on the chromatin. Nat Rev Neurosci. 2013;14(2):97-111. doi: 10.1038/nrn3427

 

  1. Hyland EM, Cosgrove MS, Molina H, et al. Insights into the role of histone H3 and histone H4 core modifiable residues in Saccharomyces cerevisiae. Mol Cell Biol. 2005;25(22):10060-10070. doi: 10.1128/MCB.25.22.10060-10070.2005

 

  1. Varela RB, Resende WR, Dal-Pont GC, et al. Role of epigenetic regulatory enzymes in animal models of mania induced by amphetamine and paradoxical sleep deprivation. Eur J Neurosci. 2021;53(2):649-662. doi: 10.1111/ejn.14922

 

  1. Kim S, Kaang BK. Epigenetic regulation and chromatin remodeling in learning and memory. Exp Mol Med. 2017;49(1):e281. doi: 10.1038/emm.2016.140

 

  1. Clapier CR, Cairns BR. The biology of chromatin remodeling complexes. Annu Rev Biochem. 2009;78:273-304. doi: 10.1146/annurev.biochem.77.062706.153223

 

  1. Han P, Hang CT, Yang J, Chang CP. Chromatin remodeling in cardiovascular development and physiology. Circ Res. 2011;108(3):378-396. doi: 10.1161/CIRCRESAHA.110.224287

 

  1. Beermann J, Piccoli MT, Viereck J, Thum T. Non-coding RNAs in development and disease: Background, mechanisms, and therapeutic approaches. Physiol Rev. 2016;96(4):1297-1325. doi: 10.1152/physrev.00041.2015

 

  1. Mattick JS, Makunin IV. Non-coding RNA. Hum Mol Genet. 2006;15(Spec No 1):R17-R29. doi: 10.1093/hmg/ddl046

 

  1. Blum K, Noble EP, Sheridan PJ, et al. Allelic association of human dopamine D2 receptor gene in alcoholism. JAMA. 1990;263(15):2055-2060.

 

  1. Thompson J, Thomas N, Singleton A, et al. D2 dopamine receptor gene (DRD2) Taq1 A polymorphism: Reduced dopamine D2 receptor binding in the human striatum associated with the A1 allele. Pharmacogenetics. 1997;7(6):479-484. doi: 10.1097/00008571-199712000-00006

 

  1. Savitz J, Hodgkinson CA, Martin-Soelch C, et al. DRD2/ANKK1 Taq1A polymorphism (rs1800497) has opposing effects on D2/3 receptor binding in healthy controls and patients with major depressive disorder. Int J Neuropsychopharmacol. 2013;16(9):2095-2101. doi: 10.1017/S146114571300045X

 

  1. Schellekens AF, Franke B, Ellenbroek B, et al. Reduced dopamine receptor sensitivity as an intermediate phenotype in alcohol dependence and the role of the COMT Val158Met and DRD2 Taq1A genotypes. Arch Gen Psychiatry. 2012;69(4):339-348. doi: 10.1001/archgenpsychiatry.2011.1335

 

  1. Benton D, Young HA. A meta-analysis of the relationship between brain dopamine receptors and obesity: A matter of changes in behavior rather than food addiction? Int J Obes (Lond). 2016;40(Suppl 1):S12-S21. doi: 10.1038/ijo.2016.9

 

  1. Eisenstein SA, Bogdan R, Love-Gregory L, et al. Prediction of striatal D2 receptor binding by DRD2/ANKK1 TaqIA allele status. Synapse. 2016;70(10):418-431. doi: 10.1002/syn.21916

 

  1. Shi S, Leites C, He D, et al. MicroRNA-9 and microRNA-326 regulate human dopamine D2 receptor expression, and the microRNA-mediated expression regulation is altered by a genetic variant. J Biol Chem. 2014;289(19):13434-1344. doi: 10.1074/jbc.M113.535203

 

  1. Völter C, Riedel M, Wöstmann N, et al. Sensorimotor gating and D2 receptor signalling: Evidence from a molecular genetic approach. Int J Neuropsychopharmacol. 2012;15(10):1427-1440. doi: 10.1017/S1461145711001787

 

  1. Sambataro F, Fazio L, Taurisano P, et al. DRD2 genotype-based variation of default mode network activity and of its relationship with striatal DAT binding. Schizophr Bull. 2013;39(1):206-216. doi: 10.1093/schbul/sbr128

 

  1. Frank MJ, Hutchison K. Genetic contributions to avoidance-based decisions: Striatal D2 receptor polymorphisms. Neuroscience. 2009;164(1):131-140. doi: 10.1016/j.neuroscience.2009.04.048

 

  1. Bertolino A, Fazio L, Di Giorgio A, et al. Genetically determined interaction between the dopamine transporter and the D2 receptor on prefronto-striatal activity and volume in humans. J Neurosci. 2009;29(4):1224-1234. doi: 10.1523/JNEUROSCI.4858-08.2009

 

  1. Bertolino A, Taurisano P, Pisciotta NM, et al. Genetically determined measures of striatal D2 signaling predict prefrontal activity during working memory performance. PLoS One. 2010;5(2):e9348. doi: 10.1371/journal.pone.0009348

 

  1. Moyer RA, Wang D, Papp AC, et al. Intronic polymorphisms affecting alternative splicing of human dopamine D2 receptor are associated with cocaine abuse. Neuropsychopharmacology. 2011;36(4):753-762. doi: 10.1038/npp.2010.208

 

  1. Vercammen A, Weickert CS, Skilleter AJ, Lenroot R, Schofield PR, Weickert TW. Common polymorphisms in dopamine-related genes combine to produce a ‘schizophrenia-like’ prefrontal hypoactivity. Transl Psychiatry. 2014;4(2):e356. doi: 10.1038/tp.2013.125

 

  1. Davis C, Levitan RD, Kaplan AS, et al. Reward sensitivity and the D2 dopamine receptor gene: A case-control study of binge eating disorder. Prog Neuropsychopharmacol Biol Psychiatry. 2008;32(3):620-628. doi: 10.1016/j.pnpbp.2007.09.024

 

  1. Kraschewski A, Reese J, Anghelescu I, et al. Association of the dopamine D2 receptor gene with alcohol dependence: Haplotypes and subgroups of alcoholics as key factors for understanding receptor function. Pharmacogenet Genomics. 2009;19(7):513-527.

 

  1. Bohnsack JP, Zhang H, Wandling GM, et al. Targeted epigenomic editing ameliorates adult anxiety and excessive drinking after adolescent alcohol exposure. Sci Adv. 2022;8(18):eabn2748. doi: 10.1126/sciadv.abn2748

 

  1. Oyaci Y, Aytac HM, Pasin O, Cetinay Aydin P, Pehlivan S. Detection of altered methylation of MB-COMT promotor and DRD2 gene in cannabinoid or synthetic cannabinoid use disorder regarding gene variants and clinical parameters. J Addict Dis. 2021;39(4):526-536.

 

  1. Gerra MC, Jayanthi S, Manfredini M, et al. Gene variants and educational attainment in cannabis use: Mediating role of DNA methylation. Transl Psychiatry. 2018;8(1):23. doi: 10.1038/s41398-017-0087-1

 

  1. DiNieri JA, Wang X, Szutorisz H, et al. Maternal cannabis use alters ventral striatal dopamine D2 gene regulation in the offspring. Biol Psychiatry. 2011;70(8):763-769. doi: 10.1016/j.biopsych.2011.06.027

 

  1. Dalterio S, Blum K, DeLallo L, Sweeney C, Briggs A, Bartke A. Perinatal exposure to delta 9-THC in mice: Altered enkephalin and norepinephrine sensitivity in vas deferens. Subst Alcohol Actions Misuse. 1980;1(5-6):467-471.

 

  1. Liu Q, Xu Y, Mao Y, et al. Genetic and epigenetic analysis revealing variants in the NCAM1-TTC12-ANKK1- DRD2 cluster associated significantly with nicotine dependence in Chinese Han smokers. Nicotine Tob Res. 2020;22(8):1301-1309. doi: 10.1093/ntr/ntz240

 

  1. Roussotte FF, Jahanshad N, Hibar DP, et al. Altered regional brain volumes in elderly carriers of a risk variant for drug abuse in the dopamine D2 receptor gene (DRD2). Brain Imaging Behav. 2015;9(2):213-222. doi: 10.1007/s11682-014-9298-8

 

  1. Pandey SC, Kyzar EJ, Zhang H. Epigenetic basis of the dark side of alcohol addiction. Neuropharmacology. 2017;122:74-84. doi: 10.1016/j.neuropharm.2017.02.002

 

  1. Bidwell LC, Karoly HC, Thayer RE, et al. DRD2 promoter methylation and measures of alcohol reward: Functional activation of reward circuits and clinical severity. Addict Biol. 2019;24(3):539-548. doi: 10.1111/adb.12614

 

  1. Morales M, Margolis EB. Ventral tegmental area: Cellular heterogeneity, connectivity and behaviour. Nat Rev Neurosci. 2017;18:73-85. doi: 10.1038/nrn.2016.165

 

  1. Hagerty SL, YorkWilliams SL, Bidwell LC, et al. DRD2 methylation is associated with executive control network connectivity and severity of alcohol problems among a sample of polysubstance users. Addict Biol. 2020;25(1):e12684. doi: 10.1111/adb.12684

 

  1. Klaus K, Vaht M, Pennington K, Harro J. Interactive effects of DRD2 rs6277 polymorphism, environment and sex on impulsivity in a population-representative study. Behav Brain Res. 2021;403:113131. doi: 10.1016/j.bbr.2021.113131

 

  1. Hill SY, Sharma VK. DRD2 methylation and regional grey matter volumes in young adult offspring from families at ultra-high risk for alcohol dependence. Psychiatry Res Neuroimaging. 2019;286:31-38. doi: 10.1016/j.pscychresns.2019.03.006

 

  1. Hillemacher T, Rhein M, Burkert A, et al. DNA-methylation of the dopamin receptor 2 gene is altered during alcohol withdrawal. Eur Neuropsychopharmacol. 2019;29(11):1250-1257. doi: 10.1016/j.euroneuro.2019.09.002

 

  1. Blum K, Baron D, Lott L, et al. In search of reward deficiency syndrome (RDS)-free controls: The “Holy Grail” in genetic addiction risk testing. Curr Psychopharmacol. 2020;9(1):7-21.

 

  1. Feltmann K, Borroto-Escuela DO, Rüegg J, et al. Effects of long-term alcohol drinking on the dopamine D2 receptor: Gene expression and heteroreceptor complexes in the striatum in rats. Alcohol Clin Exp Res. 2018;42(2):338-351. doi: 10.1111/acer.13568

 

  1. Blum K, Briggs AH, Elston SF, et al. Reduced leucine-enkephalin--like immunoreactive substance in hamster basal ganglia after long-term ethanol exposure. Science. 1982;216(4553):1425-1427. doi: 10.1126/science.7089531

 

  1. González B, Jayanthi S, Gomez N, et al. Repeated methamphetamine and modafinil induce differential cognitive effects and specific histone acetylation and DNA methylation profiles in the mouse medial prefrontal cortex. Prog Neuropsychopharmacol Biol Psychiatry. 2018;82:1-11. doi: 10.1016/j.pnpbp.2017.12.009

 

  1. Damez-Werno DM, Sun H, Scobie KN, et al. Histone arginine methylation in cocaine action in the nucleus accumbens. Proc Natl Acad Sci U S A. 2016;113(34):9623-9628. doi: 10.1073/pnas.1605045113

 

  1. Lepack AE, Werner CT, Stewart AF, et al. Dopaminylation of histone H3 in ventral tegmental area regulates cocaine seeking. Science. 2020;368(6487):197-201. doi: 10.1126/science.aaw8806

 

  1. Nohesara S, Ghadirivasfi M, Barati M, et al. Methamphetamine-induced psychosis is associated with DNA hypomethylation and increased expression of AKT1 and key dopaminergic genes. Am J Med Genet B Neuropsychiatr Genet. 2016;171(8):1180-1189. doi: 10.1002/ajmg.b.32506

 

  1. Zhang J, Fan Y, Zhou J, et al. Methylation quantitative trait locus rs5326 is associated with susceptibility and effective dosage of methadone maintenance treatment for heroin use disorder. Psychopharmacology (Berl). 2021;238(12):3511-3518. doi: 10.1007/s00213-021-05968-8

 

  1. Munn-Chernoff MA, Johnson EC, Chou YL, et al. Shared genetic risk between eating disorder-and substance-use-related phenotypes: Evidence from genome-wide association studies. Addict Biol. 2021;26(1):e12880. doi: 10.1111/adb.12880

 

  1. Braun CM, Chouinard MJ. Is anorexia nervosa a neuropsychological disease? Neuropsychol Rev. 1992;3(2):171-212. doi: 10.1007/BF01108842

 

  1. Rask-Andersen M, Olszewski PK, Levine AS, et al. Molecular mechanisms underlying anorexia nervosa: Focus on human gene association studies and systems controlling food intake. Brain Res Rev. 2010;62(2):147-164. doi: 10.1016/j.brainresrev.2009.10.007

 

  1. Wang GJ, Volkow ND, Logan J, et al. Brain dopamine and obesity. Lancet. 2001;357(9253):354-357. doi: 10.1016/s0140-6736(00)03643-6

 

  1. Frieling H, Römer KD, Scholz S, et al. Epigenetic dysregulation of dopaminergic genes in eating disorders. Int J Eat Disord. 2010;43(7):577-83. doi: 10.1002/eat.20745

 

  1. Groleau P, Joober R, Israel M, Zeramdini N, DeGuzman R, Steiger H. Methylation of the dopamine D2 receptor (DRD2) gene promoter in women with a bulimia-spectrum disorder: Associations with borderline personality disorder and exposure to childhood abuse. J Psychiatr Res. 2014;48(1):121-127. doi: 10.1016/j.jpsychires.2013.10.003

 

  1. Linnet J. The anticipatory dopamine response in addiction: A common neurobiological underpinning of gambling disorder and substance use disorder? Prog Neuropsychopharmacol Biol Psychiatry. 2020;98:109802. doi: 10.1016/j.pnpbp.2019.109802

 

  1. Guerra RF, Batista IR, Kim HS, et al. Neuroimaging of dopamine transporter density in the striatum of disordered gamblers. J Gambl Stud. 2023;39(1):119-136. doi: 10.1007/s10899-021-10100-8

 

  1. Hillemacher T, Frieling H, Buchholz V, et al. Alterations in DNA-methylation of the dopamine-receptor 2 gene are associated with abstinence and health care utilization in individuals with a lifetime history of pathologic gambling. Prog Neuropsychopharmacol Biol Psychiatry. 2015;63:30-34. doi: 10.1016/j.pnpbp.2015.05.013

 

  1. Staes, N, White CM, Guevara EE, et al. Chimpanzee Extraversion scores vary with epigenetic modification of dopamine receptor gene D2 (DRD2) and early rearing conditions. Epigenetics. 2022;17(12):1701-1714. doi: 10.1080/15592294.2022.2058224

 

  1. Juraś-Darowny M, Strzelecki D, Talarowska M. Borderline personality-from psychoanalysis to epigenetics. Biological basis of attachment. Psychiatr Pol. 2023:1-15. doi: 10.12740/PP/OnlineFirst/166492

 

  1. Coelho AA, Lima-Bastos S, Gobira PH, Lisboa SF. Endocannabinoid signaling and epigenetics modifications in the neurobiology of stress-related disorders. Neuronal Signal. 2023;7(2):NS20220034. doi: 10.1042/NS20220034

 

  1. Zoratto F, Romano E, Pascale E, et al. Down-regulation of serotonin and dopamine transporter genes in individual rats expressing a gambling-prone profile: A possible role for epigenetic mechanisms. Neuroscience. 2017;340:101-116. doi: 10.1016/j.neuroscience.2016.10.041

 

  1. Cattane N, Rossi R, Lanfredi M, Cattaneo A. Borderline personality disorder and childhood trauma: Exploring the affected biological systems and mechanisms. BMC Psychiatry. 2017;17(1):221. doi: 10.1186/s12888-017-1383-2

 

  1. McDonald S. Understanding the genetics and epigenetics of bulimia nervosa/bulimia spectrum disorder and comorbid borderline personality disorder (BN/BSD-BPD): A systematic review. Eat Weight Disord. 2019; 24(5):799-814. doi: 10.1007/s40519-019-00688-7

 

  1. Bassey RB, Gondré-Lewis MC. Combined early life stressors: Prenatal nicotine and maternal deprivation interact to influence affective and drug seeking behavioral phenotypes in rats. Behav Brain Res. 2019;359:814-822. doi: 10.1016/j.bbr.2018.07.022

 

  1. Gondré-Lewis MC, Warnock KT, Wang H, et al. Early life stress is a risk factor for excessive alcohol drinking and impulsivity in adults and is mediated via a CRF/GABA(A) mechanism. Stress. 2016;19(2):235-247. doi: 10.3109/10253890.2016.1160280

 

  1. Gondré-Lewis MC, Darius PJ, Wang H, Allard JS. Stereological analyses of reward system nuclei in maternally deprived/separated alcohol drinking rats. J Chem Neuroanat. 2016;76(Pt B):122-132. doi: 10.1016/j.jchemneu.2016.02.004

 

  1. Guo Z, Li S, Wu J, Zhu X, Zhang Y. Maternal deprivation increased vulnerability to depression in adult rats through DRD2 promoter methylation in the ventral tegmental area. Front Psychiatry. 2022;13:827667. doi: 10.3389/fpsyt.2022.827667

 

  1. Li T, Peng S, Ma X, Chen X, Zhang X. Maternal deprivation-caused behavioral abnormalities in adult rats relate to a non-methylation-regulated D2 receptor levels in the nucleus accumbens. Behav Brain Res. 2010;209(2):281-288. doi: 10.1016/j.bbr.2010.02.005

 

  1. Vialou V, Maze I, Renthal W, et al. Serum response factor promotes resilience to chronic social stress through the induction of DeltaFosB. J Neurosci. 2010;30(43):14585-14592. doi: 10.1523/JNEUROSCI.2496-10.2010

 

  1. Hamilton PJ, Burek DJ, Lombroso SI, et al. Cell-type-specific epigenetic editing at the fosb gene controls susceptibility to social defeat stress. Neuropsychopharmacology. 2018;43(2):272-284. doi: 10.1038/npp.2017.88

 

  1. Hall DB, Struhl K. The VP16 activation domain interacts with multiple transcriptional components as determined by protein-protein cross-linking in vivo. J Biol Chem. 2002;277(48):46043-46050. doi: 10.1074/jbc.M208911200

 

  1. Stege JT, Guan X, Ho T, Beachy RN, Barbas CF 3rd. Controlling gene expression in plants using synthetic zinc finger transcription factors. Plant J. 2002;32(6):1077-1086. doi: 10.1046/j.1365-313x.2002.01492.x

 

  1. Crocker J, Stern DL. TALE-mediated modulation of transcriptional enhancers in vivo. Nat Methods. 2013;10(8):762-767. doi: 10.1038/nmeth.2543

 

  1. Polstein LR, Perez-Pinera P, Kocak DD, et al. Genome-wide specificity of DNA binding, gene regulation, and chromatin remodeling by TALE- and CRISPR/ Cas9-based transcriptional activators. Genome Res. 2015;25(8):1158-1169. doi: 10.1101/gr.179044.114

 

  1. Black JB, Adler AF, Wang HG, et al. Targeted epigenetic remodeling of endogenous Loci by CRISPR/Cas9-based transcriptional activators directly converts fibroblasts to neuronal cells. Cell Stem Cell. 2016;19(3):406-414. doi: 10.1016/j.stem.2016.07.001

 

  1. Zhou H, Liu J, Zhou C, et al. In vivo simultaneous transcriptional activation of multiple genes in the brain using CRISPR-dCas9-activator transgenic mice. Nat Neurosci. 2018;21(3):440-446. doi: 10.1038/s41593-017-0060-6

 

  1. Liao HK, Hatanaka F, Araoka T, et al. In vivo target gene activation via CRISPR/Cas9-mediated trans-epigenetic modulation. Cell. 2017;171(7):1495-1507.e15. doi: 10.1016/j.cell.2017.10.025

 

  1. Kim SS, Chen YM, O’Leary E, Witzgall R, Vidal M, Bonventre JV. A novel member of the RING finger family, KRIP-1, associates with the KRAB-A transcriptional repressor domain of zinc finger proteins. Proc Natl Acad Sci U S A. 1996;93(26):15299-15304. doi: 10.1073/pnas.93.26.15299

 

  1. Groner AC, Meylan S, Ciuffi A, et al. KRAB-zinc finger proteins and KAP1 can mediate long-range transcriptional repression through heterochromatin spreading. PLoS Genet. 2010;6(3):e1000869. doi: 10.1371/journal.pgen.1000869

 

  1. Zheng Y, Shen W, Zhang J, et al. CRISPR interference-based specific and efficient gene inactivation in the brain. Nat Neurosci. 2018;21(3):447-454. doi: 10.1038/s41593-018-0077-5

 

  1. Vojta A, Dobrinić P, Tadić V, et al. Repurposing the CRISPR-Cas9 system for targeted DNA methylation. Nucleic Acids Res. 2016;44(12):5615-5628. doi: 10.1093/nar/gkw159

 

  1. Stepper P, Kungulovski G, Jurkowska RZ, et al. Efficient targeted DNA methylation with chimeric dCas9- Dnmt3a-Dnmt3L methyltransferase. Nucleic Acids Res. 2017;45(4):1703-1713. doi: 10.1093/nar/gkw1112

 

  1. Liu XS, Wu H, Ji X, et al. Editing DNA methylation in the mammalian genome. Cell. 2016;167(1):233-247.e17. doi: 10.1016/j.cell.2016.08.056

 

  1. Liu, XS, Wu H, Krzisch M, et al. Rescue of fragile X syndrome neurons by DNA methylation editing of the FMR1 gene. Cell. 2018;172(5):979-992.e6. doi: 10.1016/j.cell.2018.01.012

 

  1. Arredondo C, González M, Andrés ME, Gysling K. Opposite effects of acute and chronic amphetamine on Nurr1 and NF-κB p65 in the rat ventral tegmental area. Brain Res. 2016;1652:14-20. doi: 10.1016/j.brainres.2016.09.031

 

  1. Anderson EM, Sun H, Guzman D, et al. Knockdown of the histone di-methyltransferase G9a in nucleus accumbens shell decreases cocaine self-administration, stress-induced reinstatement, and anxiety. Neuropsychopharmacology. 2019;44(8):1370-1376. doi: 10.1038/s41386-018-0305-4

 

  1. Dulman RS, Auta J, Teppen T, Pandey SC. Acute ethanol produces ataxia and induces fmr1 expression via histone modifications in the rat cerebellum. Alcohol Clin Exp Res. 2019;43(6):1191-1198. doi: 10.1111/acer.14044

 

  1. Cong L, Zhou R, Kuo YC, Cunniff M, Zhang F. Comprehensive interrogation of natural TALE DNA-binding modules and transcriptional repressor domains. Nat Commun. 2012;3:968. doi: 10.1038/ncomms1962

 

  1. Konermann S, Brigham MD, Trevino AE, et al. Optical control of mammalian endogenous transcription and epigenetic states. Nature. 2013;500(7463):472-476. doi: 10.1038/nature12466

 

  1. Kearns NA, Pham H, Tabak B, et al. Functional annotation of native enhancers with a Cas9-histone demethylase fusion. Nat Methods. 2015;12(5):401-403. doi: 10.1038/nmeth.3325

 

  1. Cano-Rodriguez D, Gjaltema RA, Jilderda LJ, et al. Writing of H3K4Me3 overcomes epigenetic silencing in a sustained but context-dependent manner. Nat Commun. 2016;7:12284. doi: 10.1038/ncomms12284

 

  1. Lei Y, Zhang X, Su J, et al. Targeted DNA methylation in vivo using an engineered dCas9-MQ1 fusion protein. Nat Commun. 2017;8:16026. doi: 10.1038/ncomms16026

 

  1. Kwon DY, Zhao YT, Lamonica JM, Zhou Z. Locus-specific histone deacetylation using a synthetic CRISPR-Cas9- based HDAC. Nat Commun. 2017;8:15315. doi: 10.1038/ncomms15315

 

  1. Lorsch ZS, Hamilton PJ, Ramakrishnan A, et al. Stress resilience is promoted by a Zfp189-driven transcriptional network in prefrontal cortex. Nat Neurosci. 2019;22(9):1413-1423. doi: 10.1038/s41593-019-0462-8
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