Epigenetics of drug abuse: Predisposition or response

Pharmacogenomics

Volumn 13, Issue 10, 2012, Pages 1149-1160

  Nielsen, David A ^a   Utrankar, Amol ^b   Reyes, Jennifer A ^b   Simons, Daniel D ^b   Kosten, Thomas R ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b RICE UNIVERSITY   (United States)

Author keywords

alcohol; azacitidine; cocaine; Depakote; dependence; epigenetic; gene; histone; methylation; opioid; SAHA; sodium butyrate; suberoylanilide hydroxamic acid; trichostatin A; valproic acid

Indexed keywords

ALCOHOL; COCAINE; DNA; METHYL CPG BINDING PROTEIN 2; OPIATE;

ALCOHOLISM; CHROMATIN ASSEMBLY AND DISASSEMBLY; COCAINE DEPENDENCE; DNA METHYLATION; DNA MODIFICATION; DRUG ABUSE; DRUG DEPENDENCE; DRUG EXPOSURE; DRUG WITHDRAWAL; EPIGENETICS; GENE EXPRESSION; GENE MUTATION; GENETIC PREDISPOSITION; GENOME IMPRINTING; HUMAN; NERVE CELL PLASTICITY; NONHUMAN; OPIATE ADDICTION; PATHOPHYSIOLOGY; PROTEIN PHOSPHORYLATION; REVIEW;

BEHAVIOR, ADDICTIVE; CHROMATIN ASSEMBLY AND DISASSEMBLY; COCAINE; DNA METHYLATION; EPIGENESIS, GENETIC; GENETIC PREDISPOSITION TO DISEASE; HEROIN; HUMANS; RECEPTORS, OPIOID, MU; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; SUBSTANCE-RELATED DISORDERS;

EID: 84865343936     PISSN: 14622416     EISSN: 17448042     Source Type: Journal    
DOI: 10.2217/pgs.12.94     Document Type: Review

References (88)

1. Kreek MJ, Bart G, Lilly C, LaForge KS, Nielsen DA. Pharmacogenetics and human molecular genetics of opiate and cocaine addictions and their treatments. Pharmacol. Rev. 57, 1-26 (2005). (Pubitemid 40283968)
2. Koob G, Kreek MJ. Stress, dysregulation of drug reward pathways, and the transition to drug dependence. Am. J. Psychiatry 164, 1149-1159 (2007). (Pubitemid 47292402)
3. Kreek MJ, Nielsen DA, Butelman ER, LaForge KS. Genetic influences on impulsivity, risk taking, stress responsivity and vulnerability to drug abuse and addiction. Nat. Neurosci. 8, 1450-1457 (2005). (Pubitemid 41573655)
4. Kendler KS, Prescott CA, Myers J, Neale MC. The structure of genetic and environmental risk factors for common psychiatric and substance use disorders in men and women. Arch. Gen. Psychiatry 60, 929-937 (2003). (Pubitemid 37122313)
5. Kendler KS, Schmitt E, Aggen SH, Prescott CA. Genetic and environmental influences on alcohol, caffeine, cannabis, and nicotine use from early adolescence to middle adulthood. Arch. Gen. Psychiatry 65, 674-682 (2008). (Pubitemid 351787238)
6. Tsuang MT, Lyons MJ, Meyer JM et al. Co-occurrence of abuse of different drugs in men: the role of drug-specific and shared vulnerabilities. Arch. Gen. Psychiatry 55, 967-972 (1998). (Pubitemid 28506837)
7. Han D, Gu H. Comparison of the monoamine transporters from human and mouse in their sensitivities to psychostimulant drugs. BMC Pharmacol. 6, 6 (2006).
8. Lesch KP, Bengel D, Heils A et al. Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science 274, 1527-1531 (1996). (Pubitemid 26403928)
9. Brody GH, Beach SR, Philibert RA, Chen YF, Murry VM. Prevention effects moderate the association of 5-HTTLPR and youth risk behavior initiation: gene x environment hypotheses tested via a randomized prevention design. Child Dev. 80, 645-661 (2009).
10. Maze I, Nestler EJ. The epigenetic landscape of addiction. Ann. NY Acad. Sci. 1216, 99-113 (2011).
11. Suzuki MM, Bird A. DNA methylation landscapes: provocative insights from epigenomics. Nat. Rev. Genet. 9, 465-476 (2008). (Pubitemid 351693975)
12. Heller G, Schmidt WM, Ziegler B et al. Genome-wide transcriptional response to 5-aza-2́-deoxycytidine and trichostatin A in multiple myeloma cells. Cancer Res. 68, 44-54 (2008). (Pubitemid 351380104)
13. Robertson KD, Wolffe AP. DNA methylation in health and disease. Nat. Rev. Genet. 1, 11-19 (2000).
14. Zardo G, Fazi F, Travaglini L, Nervi C. Dynamic and reversibility of heterochromatic gene silencing in human disease. Cell Res. 15, 679-690 (2005). (Pubitemid 41673852)
15. Nan X, Meehan RR, Bird A. Dissection of the methyl-CpG binding domain from the chromosomal protein MeCP2. Nucleic Acids Res. 21, 4886-4892 (1993). (Pubitemid 23330162)
16. Deng JV, Rodriguiz RM, Hutchinson AN et al. MeCP2 in the nucleus accumbens contributes to neural and behavioral responses to psychostimulants. Nat. Neurosci. 13, 1128-1136 (2010).
17. Im HI, Hollander JA, Bali P, Kenny PJ. MeCP2 controls BDNF expression and cocaine intake through homeostatic interactions with microRNA-212. Nat. Neurosci. 13(9), 1120-1127 (2010).
18. Veeneman MM, Broekhoven MH, Damsteegt R, Vanderschuren LJ. Distinct contributions of dopamine in the dorsolateral striatum and nucleus accumbens shell to the reinforcing properties of cocaine. Neuropsychopharmacology 37, 487-498 (2012).
19. Day JJ, Sweatt JD. DNA methylation and memory formation. Nat. Neurosci. 13, 1319-1323 (2010).
20. Miller CA, Sweatt JD. Covalent modification of DNA regulates memory formation. Neuron 53, 857-869 (2007). (Pubitemid 46367557)
21. Heijmans BT, Tobi EW, Stein AD et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc. Natl Acad. Sci. USA 105, 17046-17049 (2008).
22. Kornberg RD, Lorch Y. Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98, 285-294 (1999). (Pubitemid 29380564)
23. McQuown SC, Wood MA. Epigenetic regulation in substance use disorders. Curr. Psychiatry Rep. 12, 145-153 (2010).
24. Jenuwein T, Allis CD. Translating the histone code. Science 293, 1074-1080 (2001). (Pubitemid 32758077)
25. Ito T. Role of histone modification in chromatin dynamics. J. Biochem. 141, 609-614 (2007). (Pubitemid 47014007)
26. Barski A, Cuddapah S, Cui K et al. High-resolution profiling of histone methylations in the human genome. Cell 129, 823-837 (2007). (Pubitemid 46802390)
27. Kouzarides T. Chromatin modifications and their function. Cell 128, 693-705 (2007). (Pubitemid 46273577)
28. Nan X, Ng HH, Johnson CA et al. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393, 386-389 (1998). (Pubitemid 28269714)
29. Hu JL, Zhou BO, Zhang RR et al. The N-terminus of histone H3 is required for de novo DNA methylation in chromatin. Proc. Natl Acad. Sci. USA 106, 22187-22192 (2009).
30. Guan Z, Giustetto M, Lomvardas S et al. Integration of long-term-memory-related synaptic plasticity involves bidirectional regulation of gene expression and chromatin structure. Cell 111, 483-493 (2002). (Pubitemid 35363296)
31. Korzus E, Rosenfeld MG, Mayford M. CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 42, 961-972 (2004). (Pubitemid 38798234)
32. Lee JL, Di Ciano P, Thomas KL, Everitt BJ. Disrupting reconsolidation of drug memories reduces cocaine-seeking behavior. Neuron 47, 795-801 (2005). (Pubitemid 41266947)
33. Everitt BJ, Robbins TW. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat. Neurosci. 8, 1481-1489 (2005). (Pubitemid 41573659)
34. Di Ciano P, Everitt BJ. Conditioned reinforcing properties of stimuli paired with self-administered cocaine, heroin or sucrose: implications for the persistence of addictive behaviour. Neuropharmacology 47(Suppl. 1), 202-213 (2004). (Pubitemid 39298265)
35. Turner BM. Cellular memory and the histone code. Cell 111, 285-291 (2002). (Pubitemid 35341385)
36. Yuferov V, Nielsen D, Butelman E, Kreek MJ. Microarray studies of psychostimulant-induced changes in gene expression. Addict. Biol. 10, 101-118 (2005).
37. Ammon-Treiber S, Hollt V. Morphine-induced changes of gene expression in the brain. Addict. Biol. 10, 81-89 (2005).
38. Paulsen M, Ferguson-Smith AC. DNA methylation in genomic imprinting, development, and disease. J. Pathol. 195, 97-110 (2001).
39. Singh P, Han L, Rivas GE et al. Allele-specific H3K79 di-versus trimethylation distinguishes opposite parental alleles at imprinted regions. Mol. Cell. Biol. 30, 2693-2707 (2010).
40. McClung CA, Nestler EJ. Regulation of gene expression and cocaine reward by CREB and DeltaFosB. Nat. Neurosci. 6, 1208-1215 (2003). (Pubitemid 37346042)
41. Graybiel AM, Moratalla R, Robertson HA. Amphetamine and cocaine induce drug-specific activation of the c-fos gene in striosome-matrix compartments and limbic subdivisions of the striatum. Proc. Natl Acad. Sci. USA 87, 6912-6916 (1990).
42. Hope B, Kosofsky B, Hyman SE, Nestler EJ. Regulation of immediate early gene expression and AP-1 binding in the rat nucleus accumbens by chronic cocaine. Proc. Natl Acad. Sci. USA 89, 5764-5768 (1992).
43. Anier K, Malinovskaja K, Aonurm-Helm A, Zharkovsky A, Kalda A. DNA methylation regulates cocaine-induced behavioral sensitization in mice. Neuropsychopharmacology 35, 2450-2461 (2010).
44. Kumar A, Choi KH, Renthal W et al. Chromatin remodeling is a key mechanism underlying cocaine-induced plasticity in striatum. Neuron 48, 303-314 (2005). (Pubitemid 41476363)
45. Levine AA, Guan Z, Barco A et al. CREB-binding protein controls response to cocaine by acetylating histones at the fosB promoter in the mouse striatum. Proc. Natl Acad. Sci. USA 102, 19186-19191 (2005). (Pubitemid 43049587)
46. Renthal W, Carle TL, Maze I et al. Delta FosB mediates epigenetic desensitization of the c-fos gene after chronic amphetamine exposure. J. Neurosci. 28, 7344-7349 (2008).
47. McClung CA, Ulery PG, Perrotti LI et al. DeltaFosB: a molecular switch for long-term adaptation in the brain. Brain Res. Mol. Brain Res. 132, 146-154 (2004). (Pubitemid 39586757)
48. Renthal W, Maze I, Krishnan V et al. Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron 56, 517-529 (2007). (Pubitemid 350030878)
49. Wang L, Lv Z, Hu Z et al. Chronic cocaine-induced H3 acetylation and transcriptional activation of CaMKIIalpha in the nucleus accumbens is critical for motivation for drug reinforcement. Neuropsychopharmacology 35, 913-928 (2010).
50. Mao LM, Horton E, Guo ML et al. Cocaine increases phosphorylation of MeCP2 in the rat striatum in vivo: a differential role of NMDA receptors. Neurochem. Int. 59, 610-617 (2011).
51. Zhou Z, Hong EJ, Cohen S et al. Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron 52, 255-269 (2006). (Pubitemid 44548348)
52. Levine A, Huang Y, Drisaldi B et al. Molecular mechanism for a gateway drug: epigenetic changes initiated by nicotine prime gene expression by cocaine. Sci. Transl. Med. 3, 107ra109 (2011).
53. Bibb JA, Chen J, Taylor JR et al. Effects of chronic exposure to cocaine are regulated by the neuronal protein Cdk5. Nature 410, 376-380 (2001). (Pubitemid 32246055)
54. Benavides DR, Quinn JJ, Zhong P et al. Cdk5 modulates cocaine reward, motivation, and striatal neuron excitability. J. Neurosci. 27, 12967-12976 (2007). (Pubitemid 350159589)
55. Graham DL, Edwards S, Bachtell RK et al. Dynamic BDNF activity in nucleus accumbens with cocaine use increases self-administration and relapse. Nat. Neurosci. 10, 1029-1037 (2007). (Pubitemid 47185197)
56. Filip M, Faron-Gorecka A, Kusmider M et al. Alterations in BDNF and trkB mRNAs following acute or sensitizing cocaine treatments and withdrawal. Brain Res. 1071, 218-225 (2006). (Pubitemid 43255491)
57. Grimm JW, Lu L, Hayashi T et al. Time-dependent increases in brain-derived neurotrophic factor protein levels within the mesolimbic dopamine system after withdrawal from cocaine: implications for incubation of cocaine craving. J. Neurosci. 23, 742-747 (2003). (Pubitemid 36206164)
58. Hollander JA, Im HI, Amelio AL et al. Striatal microRNA controls cocaine intake through CREB signalling. Nature 466, 197-202 (2010).
59. Novikova SI, He F, Bai J et al. Maternal cocaine administration in mice alters DNA methylation and gene expression in hippocampal neurons of neonatal and prepubertal offspring. PLoS ONE 3, e1919 (2008).
60. He F, Lidow IA, Lidow MS. Consequences of paternal cocaine exposure in mice. Neurotoxicol. Teratol. 28, 198-209 (2006).
61. Hwang CK, Song KY, Kim CS et al. Evidence of endogenous mu opioid receptor regulation by epigenetic control of the promoters. Mol. Cell. Biol. 27, 4720-4736 (2007).
62. Andria ML, Simon EJ. Localization of promoter elements in the human mu-opioid receptor gene and regulation by DNA methylation. Brain Res. Mol. Brain Res. 70, 54-65 (1999). (Pubitemid 29278607)
63. Hwang CK, Kim CS, Kim do K et al. Up-regulation of the mu-opioid receptor gene is mediated through chromatin remodeling and transcriptional factors in differentiated neuronal cells. Mol. Pharmacol. 78, 58-68 (2010).
64. Hwang CK, Song KY, Kim CS et al. Epigenetic programming of mu-opioid receptor gene in mouse brain is regulated by MeCP2 and Brg1 chromatin remodelling factor. J. Cell Mol. Med. 13, 3591-3615 (2009).
65. Sanchis-Segura C, Lopez-Atalaya JP, Barco A. Selective boosting of transcriptional and behavioral responses to drugs of abuse by histone deacetylase inhibition. Neuropsychopharmacology 34, 2642-2654 (2009).
66. Nielsen DA, Yuferov V, Hamon S et al. Increased OPRM1 DNA methylation in lymphocytes of methadone-maintained former heroin addicts. Neuropsychopharmacology 34, 867-873 (2009).
67. Nielsen DA, Hamon S, Yuferov V et al. Ethnic diversity of DNA methylation in the OPRM1 promoter region in lymphocytes of heroin addicts. Hum. Genet. 127, 639-649 (2010).
68. Chorbov VM, Todorov AA, Lynskey MT, Cicero TJ. Elevated levels of DNA methylation at the OPRM1 promoter in blood and sperm from male opioid addicts. J. Opioid Manag. 7, 258-264 (2011).
69. Toskulkao T, Pornchai R, Akkarapatumwong V, Vatanatunyakum S, Govitrapong P. Alteration of lymphocyte opioid receptors in methadone maintenance subjects. Neurochem. Int. 56, 285-290 (2010).
70. Byrnes JJ, Babb JA, Scanlan VF, Byrnes EM. Adolescent opioid exposure in female rats: transgenerational effects on morphine analgesia and anxiety-like behavior in adult offspring. Behav. Brain Res. 218, 200-205 (2011).
71. Marutha Ravindran CR, Ticku MK. Role of CpG islands in the up-regulation of NMDA receptor NR2B gene expression following chronic ethanol treatment of cultured cortical neurons of mice. Neurochem. Int. 46, 313-327 (2005). (Pubitemid 40221845)
72. Qiang M, Denny A, Lieu M, Carreon S, Li J. Histone H3K9 modifications are a local chromatin event involved in ethanol-induced neuroadaptation of the NR2B gene. Epigenetics 6(9), 1095-1104 (2011).
73. Pandey SC, Ugale R, Zhang H, Tang L, Prakash A. Brain chromatin remodeling: a novel mechanism of alcoholism. J. Neurosci. 28, 3729-3737 (2008).
74. Park PH, Miller R, Shukla SD. Acetylation of histone H3 at lysine 9 by ethanol in rat hepatocytes. Biochem. Biophys. Res. Commun. 306, 501-504 (2003). (Pubitemid 36683102)
75. Bardag-Gorce F, French BA, Joyce M et al. Histone acetyltransferase p300 modulates gene expression in an epigenetic manner at high blood alcohol levels. Exp. Mol. Pathol. 82, 197-202 (2007). (Pubitemid 46483380)
76. D'Addario C, Johansson S, Candeletti S et al. Ethanol and acetaldehyde exposure induces specific epigenetic modifications in the prodynorphin gene promoter in a human neuroblastoma cell line. FASEB J. 25, 1069-1075 (2011).
77. Taqi MM, Bazov I, Watanabe H et al. Prodynorphin CpG-SNPs associated with alcohol dependence: elevated methylation in the brain of human alcoholics. Addict. Biol. 16, 499-509 (2011).
78. Xuei X, Dick D, Flury-Wetherill L et al. Association of the kappa-opioid system with alcohol dependence. Mol. Psychiatry 11, 1016-1024 (2006). (Pubitemid 44631644)
79. Bonsch D, Lenz B, Fiszer R et al. Lowered DNA methyltransferase (DNMT-3b) mRNA expression is associated with genomic DNA hypermethylation in patients with chronic alcoholism. J. Neural Transm. 113, 1299-1304 (2006). (Pubitemid 44291023)
80. Bleich S, Lenz B, Ziegenbein M et al. Epigenetic DNA hypermethylation of the HERP gene promoter induces down-regulation of its mRNA expression in patients with alcohol dependence. Alcohol Clin. Exp. Res. 30, 587-591 (2006).
81. Bonsch D, Lenz B, Reulbach U, Kornhuber J, Bleich S. Homocysteine associated genomic DNA hypermethylation in patients with chronic alcoholism. J. Neural Transm. 111, 1611-1616 (2004). (Pubitemid 40064478)
82. Bonsch D, Lenz B, Kornhuber J, Bleich S. DNA hypermethylation of the alpha synuclein promoter in patients with alcoholism. Neuroreport 16, 167-170 (2005). (Pubitemid 40250393)
83. Hillemacher T, Frieling H, Luber K et al. Epigenetic regulation and gene expression of vasopressin and atrial natriuretic peptide in alcohol withdrawal. Psychoneuroendocrinology 34, 555-560 (2009).
84. Philibert RA, Gunter TD, Beach SR, Brody GH, Madan A. MAOA methylation is associated with nicotine and alcohol dependence in women. Am. J. Med. Genet. B Neuropsychiatr. Genet. 147B, 565-570 (2008). (Pubitemid 351961658)
85. Heberlein A, Muschler M, Frieling H et al. Epigenetic down regulation of nerve growth factor during alcohol withdrawal. Addict. Biol. doi:10.1111/j.1369-1600.2010.00307.x. (2011) (Epub ahead of print).
86. Ouko LA, Shantikumar K, Knezovich J et al. Effect of alcohol consumption on CpG methylation in the differentially methylated regions of H19 and IG-DMR in male gametes: implications for fetal alcohol spectrum disorders. Alcohol Clin. Exp. Res. 33, 1615-1627 (2009).
87. Issa JP, Kantarjian H. Azacitidine. Nat. Rev. Drug. Discov. Suppl, S6-S7 (2005). (Pubitemid 40674335)
88. Phiel CJ, Zhang F, Huang EY et al. Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J. Biol. Chem. 276, 36734-36741 (2001).