Epigenetic mechanisms of drug addiction

Neuropharmacology

Volumn 76, Issue PART B, 2014, Pages 259-268

  Nestler, Eric J ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Cocaine; DNA methylation; Histone acetylation; Histone methylation; microRNA; Opiates

Indexed keywords

UNTRANSLATED RNA;

ACETYLATION; BRAIN REGION; CLINICAL RESEARCH; DIAGNOSTIC TEST; DISEASE MODEL; DNA METHYLATION; DRUG DEPENDENCE; DRUG EXPOSURE; EPIGENETICS; GENE EXPRESSION; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN; METHYLATION; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; REWARD; VALIDATION STUDY;

COCAINE; DNA METHYLATION; HISTONE ACETYLATION; HISTONE METHYLATION; MICRORNA; OPIATES;

ANIMALS; EPIGENESIS, GENETIC; HUMANS; SUBSTANCE-RELATED DISORDERS;

EID: 84887080253     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.04.004     Document Type: Review

References (85)

1. M. Adli, and B.E. Bernstein Whole-genome chromatin profiling from limited numbers of cells using nano-ChIP-seq Nat. Protoc. 6 2011 1656 1668
2. K. Anier, K. Malinovskaja, A. Aonurm-Helm, A. Zharkovsky, and A. Kalda DNA methylation regulates cocaine-induced behavioral sensitization in mice Neuropsychopharmacology 35 2010 2450 2461
3. J. Bertran-Gonzalez, C. Bosch, M. Maroteaux, M. Matamales, D. Hervé, E. Valjent, and J.A. Girault Opposing patterns of signaling activation in dopamine D1 and D2 receptor-expressing striatal neurons in response to cocaine and haloperidol J. Neurosci. 28 2008 5671 5685
4. B. Botia, R. Legastelois, S. Alaux-Cantin, and M. Naassila Expression of ethanol-induced behavioral sensitization is associated with alteration of chromatin remodeling in mice PLoS One 7 2012 e47527
5. K. Brami-Cherrier, E. Valjent, D. Hervé, J. Darragh, J.C. Corvol, C. Pages, S.J. Arthur, J.A. Girault, and J. Caboche Parsing molecular and behavioral effects of cocaine in mitogen- and stress-activated protein kinase-1-deficient mice J. Neurosci. 25 2005 11444 11454 (Pubitemid 43083716)
6. K. Brami-Cherrier, E. Roze, J.A. Girault, S. Betuing, and J. Caboche Role of the ERK/MSK1 signalling pathway in chromatin remodelling and brain responses to drugs of abuse J. Neurochem. 108 2009 1323 1335
7. V. Chandrasekar, and J.L. Dreyer microRNAs miR-124, let-7d and miR-181a regulate cocaine-induced plasticity Mol. Cell. Neurosci. 42 2009 350 362
8. V. Chandrasekar, and J.L. Dreyer Regulation of MiR-124, Let-7d, and MiR-181a in the accumbens affects the expression, extinction, and reinstatement of cocaine-induced conditioned place preference Neuropsychopharmacology 36 2011 1149 1164
9. H.E. Covington III, I. Maze, H.S. Sun, E.Y. Wu, D. Dietz, M.K. Lobo, S. Ghose, R. Neve, C.A. Tamminga, and E.J. Nestler A role for repressive histone methylation in cocaine-induced vulnerability to stress Neuron 71 2011 656 670
10. C. D'Addario, F.F. Caputi, T.J. Ekström, M. Di Benedetto, M. Maccarrone, P. Romualdi, and S. Candeletti Ethanol induces epigenetic modulation of prodynorphin and pronociceptin gene expression in the rat amygdala complex J. Mol. Neurosci. 49 2013 312 319
11. D. Damez-Werno, Q. LaPlant, D.M. Dietz, S.H. Sun, K.N. Scobie, I. Walker, J.W. Koo, E. Mouzon, S.J. Russo, and E.J. Nestler Drug experience epigenetically primes fosB gene inducibility in rat nucleus accumbens and caudate putamen J. Neurosci. 32 2012 10267 10272
12. D. Damez-Werno, K.N. Scobie, H. Sun, D.M. Dietz, C.M. Dias, F. Casadio, R.L. Neve, and E.J. Nestler Histone arginine methylation in the nucleus accumbens in response to chronic cocaine and stress Soc. Neurosci. Abs 2012 69.09
13. J.V. Deng, R.M. Rodriguiz, A.N. Hutchinson, I.H. Kim, W.C. Wetsel, and A.E. West MeCP2 in the nucleus accumbens contributes to neural and behavioral responses to psychostimulants Nat. Neurosci. 13 2010 1128 1136
14. J.A. DiNieri, X. Wang, H. Szutorisz, S.M. Spano, J. Kaur, P. Casaccia, D. Dow-Edwards, and Y.L. Hurd Maternal cannabis use alters ventral striatal dopamine D2 gene regulation in the offspring Biol. Psychiatry 70 2011 763 769
15. I. Dunham, A. Kundaje, S.F. Aldred, P.J. Collins, C.A. Davis, F. Doyle, C.B. Epstein, S. Frietze, J. Harrow, and R. Kaul An integrated encyclopedia of DNA elements in the human genome Nature 489 2012 57 74
16. J.E. Eipper-Mains, D.D. Kiraly, D. Palakodeti, R.E. Mains, B.A. Eipper, and B.R. Graveley microRNA-Seq reveals cocaine-regulated expression of striatal microRNAs RNA 17 2011 1529 1543
17. D. Ferguson, N.Y. Shao, J.W. Koo, J. Feng, V. Vialou, D.M. Dietz, I. Maze, X.C. Liu, P. Kennedy, W. Renthal, R. Neve, L. Shen, V. Sartorelli, and E.J. Nestler Next generation sequencing using ChIP-Seq highlights essential role for SIRT1 in emotional plasticity Soc. Neurosci. Abs 2012 778.09
18. D. Govorko, R.A. Bekdash, C. Zhang, and D.K. Sarkar Male germline transmits fetal alcohol adverse effect on hypothalamic proopiomelanocortin gene across generations Biol. Psychiatry 72 2012 378 388
19. E. Heller, H. Sun, H. Cates, S. Knight, F. Zhang, S. Zhang, and E.J. Nestler Bidirectional regulation of the fosB gene using synthetic zinc-finger transcription factors for the study of addiction and depression Soc. Neurosci. Abs 2012 69.07
20. N. Hiroi, and S. Agatsuma Genetic susceptibility to substance dependence Mol. Psychiatry 10 2005 336 344
21. J.A. Hollander, H.I. Im, A.L. Amelio, J. Kocerha, P. Bali, Q. Lu, D. Willoughby, C. Wahlestedt, M.D. Conkright, and P.J. Kenny Striatal microRNA controls cocaine intake through CREB signalling Nature 466 2010 197 202
22. C.K. Hwang, K.Y. Song, C.S. Kim, H.S. Choi, X.H. Guo, P.Y. Law, L.N. Wei, and H.H. Loh Epigenetic programming of mu-opioid receptor gene in mouse brain is regulated by MeCP2 and Brg1 chromatin remodelling factor J. Cell. Mol. Med. 13 9B 2009 3591 3615
23. C.K. Hwang, Y. Wagley, P.Y. Law, L.N. Wei, and H.H. Loh MicroRNAs in opioid pharmacology J. Neuroimmune Pharmacol. 7 2012 808 819
24. H.I. Im, J.A. Hollander, P. Bali, and P.J. Kenny MeCP2 controls BDNF expression and cocaine intake through homeostatic interactions with microRNA-212 Nat. Neurosci. 13 2010 1120 1127
25. R. Jaenisch, and A. Bird Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals Nat. Genet. 33 Suppl. 2003 245 254 (Pubitemid 36278835)
26. T. Jenuwein, and C.D. Allis Translating the histone code Science 293 2001 1074 1080 (Pubitemid 32758077)
27. Y. Jiang, A. Matevossian, H.S. Huang, J. Straubhaar, and S. Akbarian Isolation of neuronal chromatin from brain tissue BMC Neurosci. 9 2008 42
28. A. Kalda, L.T. Heidmets, H.Y. Shen, A. Zharkovsky, and J.F. Chen Histone deacetylase inhibitors modulates the induction and expression of amphetamine induced behavioral sensitization partially through an associated learning of the environment in mice Behav. Brain Res. 181 2007 76 84 (Pubitemid 46765005)
29. P.J. Kennedy, A.J. Robison, I. Maze, J. Feng, A. Badimon, R. Bassel-Duby, E.N. Olson, and E.J. Nestler HDAC1 inhibition blocks cocaine-induced plasticity through targeted changes in histone methylation Nat. Neurosci. 16 2013 434 440
30. W.Y. Kim, S. Kim, and J.H. Kim Chronic microinjection of valproic acid into the nucleus accumbens attenuates amphetamine-induced locomotor activity Neurosci. Lett. 432 2008 54 57
31. R.J. Klose, and A.P. Bird Genomic DNA methylation: the mark and its mediators Trends Biochem. Sci. 31 2006 89 97 (Pubitemid 43221841)
32. S. Kriaucionis, and N. Heintz The nuclear DNA base 5- hydroxymethylcytosine is present in Purkinje neurons and the brain Science 324 2009 929 930
33. A. Kumar, K.-H. Choi, W. Renthal, N.M. Tsankova, D.E.H. Theobald, H.-T. Truong, S.J. Russo, Q. LaPlant, T.S. Sasaki, K.N. Whistler, R.L. Neve, D.W. Self, and E.J. Nestler Chromatin remodeling is a key mechanism underlying cocaine-induced plasticity in striatum Neuron 48 2005 303 314 (Pubitemid 41476363)
34. Q. LaPlant, V. Vialou, H.E. Covington, D. Dumitriu, J. Feng, B. Warren, I. Maze, D.M. Dietz, E.L. Watts, S.D. Iñiquez, J.-W. Koo, E. Mouzon, W. Renthal, F. Hollis, H. Wang, M.A. Noonan, Y.H. Ren, A.J. Eisch, C.A. Bolaños, M. Kabbaj, G.H. Xiao, R.L. Neve, Y.L. Hurd, R.S. Oosting, G.P. Fan, J.H. Morrison, and E.J. Nestler Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens Nat. Neurosci. 13 2010 1137 1143
35. A.A. Levine, Z. Guan, A. Barco, S. Xu, E.R. Kandel, and J.H. Schwartz CREB-binding protein controls response to cocaine by acetylating histones at the fosB promoter in the mouse striatum Proc. Natl. Acad. Sci. U. S. A. 102 2005 19186 19191 (Pubitemid 43049587)
36. A. Levine, Y. Huang, B. Drisaldi, E.A. Griffin Jr., D.D. Pollak, S. Xu, D. Yin, C. Schaffran, D.B. Kandel, and E.R. Kandel Molecular mechanism for a gateway drug: epigenetic changes initiated by nicotine prime gene expression by cocaine Sci. Transl. Med. 3 2011 107 109
37. R.F. Luco, M. Allo, I.E. Schor, A.R. Kornblihtt, and T. Misteli Epigenetics in alternative pre-mRNA splicing Cell 144 2011 16 26
38. M. Malvaez, C. Sanchis-Segura, D. Vo, K.M. Lattal, and M.A. Wood Modulation of chromatin modification facilitates extinction of cocaine-induced conditioned place preference Biol. Psychiatry 67 2010 36 43
39. M. Malvaez, E. Mhillaj, D.P. Matheos, M. Palmery, and M.A. Wood CBP in the nucleus accumbens regulates cocaine-induced histone acetylation and is critical for cocaine-associated behaviors J. Neurosci. 31 2011 16941 16948
40. M. Malvaez, S.C. McQuown, G.A. Rogge, M. Astarabadi, V. Jacques, S. Carreiro, J.R. Rusche, and M.A. Wood HDAC3-selective inhibitor enhances extinction of cocaine-seeking behavior in a persistent manner Proc. Natl. Acad. Sci. U. S. A. 110 2013 2647 2652
41. I. Maze, and E.J. Nestler The epigenetic landscape of addiction Ann. N.Y. Acad. Sci. 1216 2011 99 113
42. I. Maze, H.E. Covington III, D.M. Dietz, Q. LaPlant, W. Renthal, S.J. Russo, M. Mechanic, E. Mouzon, R.L. Neve, S.J. Haggarty, Y.H. Ren, S.C. Sampath, Y.L. Hurd, P. Greengard, A. Tarakovsky, A. Schaefer, and E.J. Nestler Essential role of the histone methyltransferase G9a in cocaine-induced plasticity Science 327 2010 213 216
43. I. Maze, J. Feng, M.B. Wilkinson, H.S. Sun, L. Shen, and E.J. Nestler Cocaine dynamically regulates heterochromatin and repetitive element unsilencing in nucleus accumbens Proc. Natl. Acad. Sci. U. S. A. 108 2011 3035 3040
44. M.S. Mazei-Robison, J.W. Koo, A. Friedman, C.S. Lansink, A.J. Robison, M. Vinish, V. Krishnan, S. Kim, M.A. Siuta, M.A. Galli, K.D. Niswender, R. Appasani, M.C. Horvath, R.L. Neve, P.F. Worley, S.H. Snyder, Y.L. Hurd, J.F. Cheer, M.H. Han, S.J. Russo, and E.J. Nestler Role for mTOR signaling and neuronal activity in morphine-induced adaptations in ventral tegmental area dopamine neurons Neuron 72 2011 977 990
45. S.K. Michelhaugh, L. Lipovich, J. Blythe, H. Jia, G. Kapatos, and M.J. Bannon Mining Affymetrix microarray data for long non-coding RNAs: altered expression in the nucleus accumbens of heroin abusers J. Neurochem. 116 2011 459 466
46. L.D. Moore, T. Le, and G. Fan DNA methylation and its basic function Neuropsychopharmacology 38 2013 23 38
47. D.A. Nielsen, V. Yuferov, S. Hamon, C. Jackson, A. Ho, J. Ott, and M.J. Kreek Increased OPRM1 DNA methylation in lymphocytes of methadone-maintained former heroin addicts Neuropsychopharmacology 34 2009 867 873
48. D.A. Nielsen, W. Huang, S.C. Hamon, L. Maili, B.M. Witkin, R.G. Fox, K.A. Cunningham, and F.G. Moeller Forced abstinence from cocaine self-administration is associated with DNA methylation changes in myelin genes in the corpus callosum: a preliminary study Front. Psychiatry 3 2012 60
49. M. Pascual, B.R. Do Couto, S. Alfonso-Loeches, M.A. Aguilar, M. Rodriguez-Arias, and C. Guerri Changes in histone acetylation in the prefrontal cortex of ethanol-exposed adolescent rats are associated with ethanol-induced place conditioning Neuropharmacology 62 2012 2309 2319
50. A.Z. Pietrzykowski, R.M. Friesen, G.E. Martin, S.I. Puig, C.L. Nowak, P.M. Wynne, H.T. Siegelmann, and S.N. Treistman Posttranscriptional regulation of BK channel splice variant stability by miR-9 underlies neuroadaptation to alcohol Neuron 59 2008 274 287 (Pubitemid 352033687)
51. I. Ponomarev, S. Wang, L. Zhang, R.A. Harris, and R.D. Mayfield Gene coexpression networks in human brain identify epigenetic modifications in alcohol dependence J. Neurosci. 32 2012 1884 1897
52. M. Qiang, A. Denny, M. Lieu, S. Carreon, and J. Li Histone H3K9 modifications are a local chromatin event involved in ethanol-induced neuroadaptation of the NR2B gene Epigenetics 6 2011 1095 1104
53. W. Renthal, I. Maze, V. Krishnan, H.E. Covington, G.H. Xiao, A. Kumar, S.J. Russo, A. Graham, N. Tsankova, K.A. Kerstetter, T.E. Kippin, R.L. Neve, S.J. Haggarty, T.A. McKinsey, R. Bassel-Duby, E.N. Olson, and E.J. Nestler Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli Neuron 56 2007 517 529 (Pubitemid 350030878)
54. W. Renthal, T.L. Carle, I. Maze, H.E. Covington III, H.-T. Truong, I. Alibhai, A. Kumar, E.N. Olson, and E.J. Nestler ΔFosB mediates epigenetic desensitization of the c-fos gene after chronic amphetamine exposure J. Neurosci. 28 2008 7344 7349
55. W. Renthal, A. Kumar, G.H. Xiao, M. Wilkinson, H.E. Convington III, I. Maze, D. Sikder, A.J. Robison, Q. LaPlant, D.M. Dietz, S.J. Russo, V. Vialou, S. Chakravarty, T.J. Kodadek, A. Stack, M. Kabbaj, and E.J. Nestler Genome wide analysis of chromatin regulation by cocaine reveals a novel role for sirtuins Neuron 62 2009 335 348
56. J.L. Rinn, and H.Y. Chang Genome regulation by long noncoding RNAs Annu. Rev. Biochem. 81 2012 145 166
57. A.J. Robison, and E.J. Nestler Transcriptional and epigenetic mechanisms of addiction Nat. Rev. Neurosci. 12 2011 623 637
58. A.J. Robison, V. Vialou, M. Mazei-Robison, J. Feng, S. Kourrich, M. Collins, S.M. Wee, G. Koob, G. Turecki, R. Neve, M. Thomas, and E.J. Nestler Behavioral and structural responses to chronic cocaine require a feed-forward loop involving ΔFosB and CaMKII in the nucleus accumbens shell J. Neurosci. 33 2013 4295 4307
59. G.A. Rogge, and M.A. Wood The role of histone acetylation in cocaine-induced neural plasticity and behavior Neuropsychopharmacology 38 2013 94 110
60. P. Romieu, L. Host, S. Gobaille, G. Sandner, D. Aunis, and J. Zwiller Histone deacetylase inhibitors decrease cocaine but not sucrose self-administration in rats J. Neurosci. 28 2008 9342 9348
61. D. Ron, and R.O. Messing Signaling pathways mediating alcohol effects Curr. Top. Behav. Neurosci. 13 2013 87 126
62. R. Saba, P.H. Storchel, A. Aksoy-Aksel, F. Kepura, G. Lippi, T.D. Plant, and G.M. Schratt Dopamine-regulated microRNA MiR-181a controls GluA2 surface expression in hippocampal neurons Mol. Cell. Biol. 32 2012 619 632
63. G. Sadri-Vakili, V. Kumaresan, H.G. Schmidt, K.R. Famous, P. Chawla, F.M. Vassoler, R.P. Overland, E. Xia, C.E. Bass, T.F. Terwilliger, R.C. Pierce, and J.H.J. Cha Cocaine-induced chromatin remodeling increases brain-derived neurotrophic factor transcription in the rat medial prefrontal cortex, which alters the reinforcing efficacy of cocaine J. Neurosci. 30 2010 11735 11744
64. A.J. Sakharkar, H. Zhang, L. Tang, G. Shi, and S.C. Pandey Histone deacetylases (HDAC)-induced histone modifications in the amygdala: a role in rapid tolerance to the anxiolytic effects of ethanol Alcohol. Clin. Exp. Res. 36 2012 61 71
65. G.C. Sartor, G. St Laurent 3rd, and C. Wahlestedt The emerging role of non-coding RNAs in drug addiction Front. Genet. 3 2012 106
66. A. Schaefer, H.I. Im, M.T. Veno, C.D. Fowler, A. Min, A. Intrator, J. Kjems, P.J. Kenny, D. O'Carroll, and P. Greengard Argonaute 2 in dopamine 2 receptor-expressing neurons regulates cocaine addiction J. Exp. Med. 207 2010 1843 1851
67. H.D. Schmidt, G.R. Sangrey, S.B. Darnell, R.L. Schassburger, J.H. Cha, R.C. Pierce, and G. Sadri-Vakili Increased brain-derived neurotrophic factor (BDNF) expression in the ventral tegmental area during cocaine abstinence is associated with increased histone acetylation at BDNF exon I-containing promoters J. Neurochem. 120 2012 202 209
68. F.A. Schroeder, K.L. Penta, A. Matevossian, S.R. Jones, C. Konradi, A.R. Tapper, and S. Akbarian Drug-induced activation of dopamine D(1) receptor signaling and inhibition of class I/II histone deacetylase induce chromatin remodeling in reward circuitry and modulate cocaine-related behaviors Neuropsychopharmacology 33 2008 2981 2992
69. K.N. Scobie, D. Damez-Werno, H. Sun, R.L. Neve, P. Caiafa, and E.J. Nestler Role of poly(ADP-ribosyl)ation in drug-seeking behavior Soc. Neurosci. Abs 2012 69.12
70. H.Y. Shen, A. Kalda, L. Yu, J. Ferrara, J. Zhu, and J.F. Chen Additive effects of histone deacetylase inhibitors and amphetamine on histone H4 acetylation, cAMP responsive element binding protein phosphorylation and DeltaFosB expression in the striatum and locomotor sensitization in mice Neuroscience 157 2008 644 655
71. J. Sheng, Z. Lv, L. Wang, Y. Zhou, and B. Hui Histone H3 phosphoacetylation is critical for heroin-induced place preference Neuroreport 22 2011 575 580
72. B.G. Starkman, A.J. Sakharkar, and S.C. Pandey Epigenetics-beyond the genome in alcoholism Alcohol. Res. 34 2012 293 305
73. A. Stipanovich, E. Valjent, M. Matamales, A. Nishi, J.H. Ahn, M. Maroteaux, J. Bertran-Gonzalez, K. Brami-Cherrier, H. Enslen, A.G. Corbillé, O. Filhol, A.C. Nairn, P. Greengard, D. Hervé, and J.A. Girault A phosphatase cascade by which rewarding stimuli control nucleosomal response Nature 453 2008 879 884 (Pubitemid 351832565)
74. J. Sun, L. Wang, B. Jiang, B. Hui, Z. Lv, and L. Ma The effects of sodium butyrate, an inhibitor of histone deacetylase, on the cocaine- and sucrose-maintained self administration in rats Neurosci. Lett. 441 2008 72 76
75. H.S. Sun, I. Maze, D.M. Dietz, K.N. Scobie, P.J. Kennedy, D. Damez-Werno, R.L. Neve, V. Zachariou, L. Shen, and E.J. Nestler Morphine epigenetically regulates behavior through alterations in histone H3 lysine 9 dimethylation in the nucleus accumbens J. Neurosci. 32 2012 17454 17464
76. H.S. Sun, D. Damez-Werno, K. Scobie, C. Dias, J.W. Koo, P. Kennedy, D.M. Dietz, R. Neve, P. Varga-Weisz, and E.J. Nestler Role of chromatin remodelers in the mouse nucleus accumbens in preclinical models of depression and cocaine addiction Soc. Neurosci. Abs 2012 69.10
77. K.E. Szulwach, X. Li, Y. Li, C.X. Song, H. Wu, Q. Dai, H. Irier, A.K. Upadhyay, M. Gearing, A.I. Levey, A. Vasanthakumar, L.A. Godley, Q. Chang, X. Cheng, C. He, and P. Jin 5-hmC-mediated epigenetic dynamics during postnatal neurodevelopment and aging Nat. Neurosci. 14 2011 1607 1616
78. M. Tahiliani, K.P. Koh, Y. Shen, W.A. Pastor, H. Bandukwala, Y. Brudno, S. Agarwal, L.M. Iyer, D.R. Liu, L. Aravind, and A. Rao Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1 Science 324 2009 930 935
79. M. Taniguchi, M.B. Carreira, L.N. Smith, B.C. Zirlin, R.L. Neve, and C.W. Cowan Histone deacetylase 5 limits cocaine reward through cAMP-induced nuclear import Neuron 73 2012 108 120
80. H.C. Tomasiewicz, M.M. Jacobs, M.B. Wilkinson, S.P. Wilson, E.J. Nestler, and Y.L. Hurd Proenkephalin mediates the enduring effects of adolescent cannabis exposure associated with adult opiate vulnerability Biol. Psychiatry 72 2012 803 810
81. N. Tsankova, W. Renthal, A. Kumar, and E.J. Nestler Epigenetic regulation in psychiatric disorders Nat. Rev. Neurosci. 8 2007 355 367 (Pubitemid 46652469)
82. F.M. Vassoler, S.L. White, H.D. Schmidt, G. Sadri-Vakili, and R.C. Pierce Epigenetic inheritance of a cocaine-resistance phenotype Nat. Neurosci. 16 2013 42 47
83. L. Wang, Z. Lv, Z. Hu, J. Sheng, B. Hui, J. Sun, and L. Ma Chronic cocaine-induced H3 acetylation and transcriptional activation of CaMKIIalpha in the nucleus accumbens is critical for motivation for drug reinforcement Neuropsychopharmacology 35 2010 913 928
84. W.S. Wang, S. Kang, W.T. Liu, M. Li, Y. Liu, C. Yu, J. Chen, Z.Q. Chi, L. He, and J.G. Liu Extinction of aversive memories associated with morphine withdrawal requires ERK-mediated epigenetic regulation of brain-derived neurotrophic factor transcription in the rat ventromedial prefrontal cortex J. Neurosci. 32 2012 13763 13775
85. H. Wu, and Y. Zhang Mechanisms and functions of Tet protein-mediated 5-methylcytosine oxidation Genes Dev. 25 2011 2436 2452