Transcriptional and epigenetic mechanisms of addiction

Nature Reviews Neuroscience

Volumn 12, Issue 11, 2011, Pages 623-637

  Robison, Alfred J ^a   Nestler, Eric J ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANNABINOID; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYTOSKELETON PROTEIN; DOPAMINE; GLUTAMIC ACID; HISTONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; ION CHANNEL; MORPHINE; MYOCYTE ENHANCER FACTOR 2; OPIATE RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOSB; UNTRANSLATED RNA;

AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; CHROMATIN STRUCTURE; CHROMOSOME; CORPUS STRIATUM; DNA METHYLATION; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; DORSAL RAPHE NUCLEUS; DRUG DEPENDENCE; EPIGENETICS; GENE CONTROL; GENE EXPRESSION REGULATION; GENE REPRESSION; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; HIPPOCAMPUS; HISTONE MODIFICATION; HUMAN; INTERNEURON; INTRACELLULAR SIGNALING; LOCUS CERULEUS; MESENCEPHALON; NONHUMAN; NUCLEOSOME; NUCLEUS ACCUMBENS; ORBITAL CORTEX; PREFRONTAL CORTEX; PRIORITY JOURNAL; REVIEW; REWARD; SEX DIFFERENCE; THALAMUS; VENTRAL TEGMENTUM;

ANIMALS; BEHAVIOR, ADDICTIVE; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; HUMANS; SUBSTANCE-RELATED DISORDERS; TRANSCRIPTION, GENETIC;

EID: 80054827869     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn3111     Document Type: Review

References (151)

1. Kendler, K. S., Myers, J. & Prescott, C. A. Specificity of genetic and environmental risk factors for symptoms of cannabis, cocaine, alcohol, caffeine, and nicotine dependence. Arch. Gen. Psychiatry 64, 1313-1320 (2007). (Pubitemid 350074829)
2. Volkow, N., Rutter, J., Pollock, J. D., Shurtleff, D. & Baler, R. One SNP linked to two diseases - addiction and cancer: a double whammy? Nicotine addiction and lung cancer susceptibility. Mol. Psychiatry 13, 990-992 (2008).
3. Goldman, D., Oroszi, G. & Ducci, F. The genetics of addictions: uncovering the genes. Nature Rev. Genet. 6, 521-532 (2005). (Pubitemid 40910429)
4. Henikoff, S. & Matzke, M. A. Exploring and explaining epigenetic effects. Trends Genet. 13, 293-295 (1997).
5. Sutherland, J. E. & Costa, M. Epigenetics and the environment. Ann. NY Acad. Sci. 983, 151-160 (2003). (Pubitemid 36399328)
6. Fraga, M. F. et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc. Natl Acad. Sci. USA 102, 10604-10609 (2005). (Pubitemid 41061601)
7. Koob, G. F. & Le Moal, M. Neurobiology of Addiction. (Academic Press, London, 2005).
8. Kalivas, P. W. & Volkow, N. D. The neural basis of addiction: a pathology of motivation and choice. Am. J. Psychiatry 162, 1403-1413 (2005). (Pubitemid 41105554)
9. Hyman, S. E., Malenka, R. C. & Nestler, E. J. Neural mechanisms of addiction: the role of reward-related learning and memory. Annu. Rev. Neurosci. 29, 565-598 (2006). (Pubitemid 44476856)
10. Robinson, T. E. & Berridge, K. C. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res. Brain Res. Rev. 18, 247-291 (1993). (Pubitemid 23219500)
11. Nestler, E. J. Molecular basis of long-term plasticity underlying addiction. Nature Rev. Neurosci. 2, 119-128 (2001). (Pubitemid 33673366)
12. Andersen, S. L. & Teicher, M. H. Desperately driven and no brakes: developmental stress exposure and subsequent risk for substance abuse. Neurosci. Biobehav. Rev. 33, 516-524 (2009).
13. Malanga, C. J. & Kosofsky, B. E. Does drug abuse beget drug abuseκ Behavioral analysis of addiction liability in animal models of prenatal drug exposure. Brain Res. Dev. Brain Res. 147, 47-57 (2003). (Pubitemid 38114696)
14. Nestler, E. J. Review. Transcriptional mechanisms of addiction: role of DeltaFosB. Phil. Trans. R. Soc. Lond. B 363, 3245-3255 (2008).
15. Jorissen, H. J. et al. Dimerization and DNA-binding properties of the transcription factor DeltaFosB. Biochemistry 46, 8360-8372 (2007). (Pubitemid 47075973)
16. Hiroi, N. et al. FosB mutant mice: loss of chronic cocaine induction of Fos-related proteins and heightened sensitivity to cocaines psychomotor and rewarding effects. Proc. Natl Acad. Sci. USA 94, 10397-10402 (1997). (Pubitemid 27407053)
17. Perrotti, L. I. et al. Distinct patterns of DeltaFosB induction in brain by drugs of abuse. Synapse 62, 358-369 (2008). (Pubitemid 351451804)
18. Carle, T. L. et al. Proteasome-dependent and -independent mechanisms for FosB destabilization: identification of FosB degron domains and implications for DeltaFosB stability. Eur. J. Neurosci. 25, 3009-3019 (2007). (Pubitemid 46888818)
19. Ulery, P. G., Rudenko, G. & Nestler, E. J. Regulation of DeltaFosB stability by phosphorylation. J. Neurosci. 26, 5131-5142 (2006).
20. Ulery-Reynolds, P. G., Castillo, M. A., Vialou, V., Russo, S. J. & Nestler, E. J. Phosphorylation of DeltaFosB mediates its stability in vivo. Neuroscience 158, 369-372 (2009).
21. Kelz, M. B. et al. Expression of the transcription factor deltaFosB in the brain controls sensitivity to cocaine. Nature 401, 272-276 (1999).
22. Zachariou, V. et al. An essential role for DeltaFosB in the nucleus accumbens in morphine action. Nature Neurosci. 9, 205-211 (2006). (Pubitemid 43164543)
23. Colby, C. R., Whisler, K., Steffen, C., Nestler, E. J. & Self, D. W. Striatal cell type-specific overexpression of DeltaFosB enhances incentive for cocaine. J. Neurosci. 23, 2488-2493 (2003). (Pubitemid 36368938)
24. Winstanley, C. A. et al. DeltaFosB induction in orbitofrontal cortex mediates tolerance to cocaine-induced cognitive dysfunction. J. Neurosci. 27, 10497-10507 (2007). (Pubitemid 47502009)
25. Winstanley, C. A. et al. DeltaFosB induction in orbitofrontal cortex potentiates locomotor sensitization despite attenuating the cognitive dysfunction caused by cocaine. Pharmacol. Biochem. Behav. 93, 278-284 (2009).
26. Werme, M. et al. Delta FosB regulates wheel running. J. Neurosci. 22, 8133-8138 (2002). (Pubitemid 35379119)
27. Wallace, D. L. et al. The influence of DeltaFosB in the nucleus accumbens on natural reward-related behavior. J. Neurosci. 28, 10272-10277 (2008).
28. Teegarden, S. L., Nestler, E. J. & Bale, T. L. Delta FosB-mediated alterations in dopamine signaling are normalized by a palatable high-fat diet. Biol. Psychiatry 64, 941-950 (2008).
29. Hedges, V. L., Chakravarty, S., Nestler, E. J. & Meisel, R. L. Delta FosB overexpression in the nucleus accumbens enhances sexual reward in female Syrian hamsters. Genes Brain Behav. 8, 442-449 (2009).
30. Pitchers, K. K. et al. DeltaFosB in the nucleus accumbens is critical for reinforcing effects of sexual reward. Genes Brain Behav. 9, 831-840 (2010).
31. McClung, C. A. & Nestler, E. J. Regulation of gene expression and cocaine reward by CREB and DeltaFosB. Nature Neurosci.6, 1208-1215 (2003). (Pubitemid 37346042)
32. Renthal, W. et al. Genome-wide analysis of chromatin regulation by cocaine reveals a role for sirtuins. Neuron 62, 335-348 (2009).
33. Bibb, J. A. et al. Effects of chronic exposure to cocaine are regulated by the neuronal protein Cdk5. Nature 410, 376-380 (2001). (Pubitemid 32246055)
34. Russo, S. J. et al. The addicted synapse: mechanisms of synaptic and structural plasticity in nucleus accumbens. Trends Neurosci. 33, 267-276 (2010).
35. Robinson, T. E. & Kolb, B. Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology 47, 33-46 (2004). (Pubitemid 39298251)
36. Kalivas, P. W. The glutamate homeostasis hypothesis of addiction. Nature Rev. Neurosci.10, 561-572 (2009).
37. Maze, I. et al. Essential role of the histone methyltransferase G9a in cocaine-induced plasticity. Science 327, 213-216 (2010).
38. Vialou, V. et al. DeltaFosB in brain reward circuits mediates resilience to stress and antidepressant responses. Nature Neurosci. 13, 745-752 (2010).
39. Robison, A. J. et al. Chronic cocaine engages a feedback loop involving δFosB and CaMKII in the nucleus accumbens. Soc. Neurosci. Abstr. 909.23 (Washington DC, 12-16 Nov 2011).
40. Wolf, M. E. & Ferrario, C. R. AMPA receptor plasticity in the nucleus accumbens after repeated exposure to cocaine. Neurosci. Biobehav. Rev. 35, 185-211 (2010).
41. Carlezon, W. A. Jr, Duman, R. S. & Nestler, E. J. The many faces of CREB. Trends Neurosci. 28, 436-445 (2005). (Pubitemid 40982557)
42. Briand, L. A. & Blendy, J. A. Molecular and genetic substrates linking stress and addiction. Brain Res. 1314, 219-234 (2010).
43. Edwards, S., Graham, D. L., Bachtell, R. K. & Self, D. W. Region-specific tolerance to cocaine-regulated cAMP-dependent protein phosphorylation following chronic self-administration. Eur. J. Neurosci. 25, 2201-2213 (2007). (Pubitemid 46581745)
44. Carlezon, W. A. Jr. et al. Regulation of cocaine reward by CREB. Science 282, 2272-2275 (1998). (Pubitemid 29004079)
45. Barrot, M. et al. CREB activity in the nucleus accumbens shell controls gating of behavioral responses to emotional stimuli. Proc. Natl Acad. Sci. USA 99, 11435-11440 (2002). (Pubitemid 34920943)
46. Larson, E. B. et al. Over-expression of CREB in the nucleus accumbens shell increases cocaine reinforcement in self-administering rats. J. Neurosci. (in the press).
47. Pluzarev, O. & Pandey, S. C. Modulation of CREB expression and phosphorylation in the rat nucleus accumbens during nicotine exposure and withdrawal. J. Neurosci. Res. 77, 884-891 (2004). (Pubitemid 39187071)
48. Misra, K., Roy, A. & Pandey, S. C. Effects of voluntary ethanol intake on the expression of Ca2+/calmodulin-dependent protein kinase IV and on CREB expression and phosphorylation in the rat nucleus accumbens. Neuroreport 12, 4133-4137 (2001). (Pubitemid 33152466)
49. Li, J., Li, Y. H. & Yuan, X. R. Changes of phosphorylation of cAMP response element binding protein in rat nucleus accumbens after chronic ethanol intake: naloxone reversal. Acta Pharmacol. Sin. 24, 930-936 (2003).
50. Brunzell, D. H., Mineur, Y. S., Neve, R. L. & Picciotto, M. R. Nucleus accumbens CREB activity is necessary for nicotine conditioned place preference. Neuropsychopharmacology 34, 1993-2001 (2009).
51. Rubino, T. et al. Cellular mechanisms underlying the anxiolytic effect of low doses of peripheral Delta9-tetrahydrocannabinol in rats. Neuropsychopharmacology 32, 2036-2045 (2007). (Pubitemid 47258523)
52. Shiflett, M. W., Mauna, J. C., Chipman, A. M., Peet, E. & Thiels, E. Appetitive Pavlovian conditioned stimuli increase CREB phosphorylation in the nucleus accumbens. Neurobiol. Learn. Mem. 92, 451-454 (2009).
53. Green, T. A. et al. Induction of activating transcription factors (ATFs) ATF2, ATF3, and ATF4 in the nucleus accumbens and their regulation of emotional behavior. J. Neurosci. 28, 2025-2032 (2008). (Pubitemid 351317626)
54. Dong, Y. et al. CREB modulates excitability of nucleus accumbens neurons. Nature Neurosci. 9, 475-477 (2006).
55. Huang, Y. H. et al. CREB modulates the functional output of nucleus accumbens neurons: a critical role of N-methyl-D-aspartate glutamate receptor (NMDAR) receptors. J. Biol. Chem. 283, 2751-2760 (2008).
56. Meffert, M. K., Chang, J. M., Wiltgen, B. J., Fanselow, M. S. & Baltimore, D. NF-κB functions in synaptic signaling and behavior. Nature Neurosci. 6, 1072-1078 (2003). (Pubitemid 37186199)
57. Russo, S. J. et al. Nuclear factor κB signaling regulates neuronal morphology and cocaine reward. J. Neurosci. 29, 3529-3537 (2009).
58. Sullivan, P. F. et al. Candidate genes for nicotine dependence via linkage, epistasis, and bioinformatics. Am. J. Med. Genet. B Neuropsychiatr. Genet. 126B, 23-36 (2004). (Pubitemid 38420117)
59. Christoffel, D. J. et al. IκB kinase regulates social defeat stress-induced synaptic and behavioral plasticity. J. Neurosci. 31, 314-321 (2011).
60. Pulipparacharuvil, S. et al. Cocaine regulates MEF2 to control synaptic and behavioral plasticity. Neuron 59, 621-633 (2008).
61. Chen, L. et al. Chronic ethanol feeding impairs AMPK and MEF2 expression and is associated with GLUT4 decrease in rat myocardium. Exp. Mol. Med. 42, 205-215 (2010).
62. Ambroggi, F. et al. Stress and addiction: glucocorticoid receptor in dopaminoceptive neurons facilitates cocaine seeking. Nature Neurosci. 12, 247-249 (2009).
63. Barik, J. et al. Glucocorticoid receptors in dopaminoceptive neurons, key for cocaine, are dispensable for molecular and behavioral morphine responses. Biol. Psychiatry 68, 231-239 (2010).
64. Desrivieres, S. et al. Glucocorticoid receptor (NR3C1) gene polymorphisms and onset of alcohol abuse in adolescents. Addict. Biol. 16, 510-513 (2011).
65. McQuown, S. C. & Wood, M. A. Epigenetic regulation in substance use disorders. Curr. Psychiatry Rep. 12, 145-153 (2010).
66. Renthal, W. & Nestler, E. J. Epigenetic mechanisms in drug addiction. Trends Mol. Med. 14, 341-350 (2008).
67. Borrelli, E., Nestler, E. J., Allis, C. D. & Sassone-Corsi, P. Decoding the epigenetic language of neuronal plasticity. Neuron 60, 961-974 (2008).
68. Berger, S. L. The complex language of chromatin regulation during transcription. Nature 447, 407-412 (2007). (Pubitemid 46816746)
69. Jenuwein, T. & Allis, C. D. Translating the histone code. Science 293, 1074-1080 (2001). (Pubitemid 32758077)
70. Maze, I. & Nestler, E. J. The epigenetic landscape of addiction. Ann. NY Acad. Sci. 1216, 99-113 (2011).
71. Su, I. H. & Tarakhovsky, A. Lysine methylation and signaling memory. Curr. Opin. Immunol. 18, 152-157 (2006).
72. Rumbaugh, G. & Miller, C. A. Epigenetic changes in the brain: measuring global histone modifications. Methods Mol. Biol. 670, 263-274 (2011).
73. Kumar, A. et al. Chromatin remodeling is a key mechanism underlying cocaine-induced plasticity in striatum. Neuron 48, 303-314 (2005). (Pubitemid 41476363)
74. Schroeder, F. A. et al. Drug-induced activation of dopamine D1 receptor signaling and inhibition of class I/II histone deacetylase induce chromatin remodeling in reward circuitry and modulate cocaine-related behaviors. Neuropsychopharmacology 33, 2981-2992 (2008).
75. Bertran-Gonzalez, J. et al. Opposing patterns of signaling activation in dopamine D1 and D2 receptor-expressing striatal neurons in response to cocaine and haloperidol. J. Neurosci. 28, 5671-5685 (2008).
76. Pandey, S. C., Ugale, R., Zhang, H., Tang, L. & Prakash, A. Brain chromatin remodeling: a novel mechanism of alcoholism. J. Neurosci. 28, 3729-3737 (2008).
77. Wang, Y., Krishnan, H. R., Ghezzi, A., Yin, J. C. & Atkinson, N. S. Drug-induced epigenetic changes produce drug tolerance. PLoS Biol. 5, e265 (2007).
78. Khare, M., Taylor, A. H., Konje, J. C. & Bell, S. C. Delta9-tetrahydrocannabinol inhibits cytotrophoblast cell proliferation and modulates gene transcription. Mol. Hum. Reprod. 12, 321-333 (2006). (Pubitemid 43821795)
79. Parmentier-Batteur, S., Jin, K., Xie, L., Mao, X. O. & Greenberg, D. A. DNA microarray analysis of cannabinoid signaling in mouse brain in vivo. Mol. Pharmacol.62, 828-835 (2002).
80. Renthal, W. et al. Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron 56, 517-529 (2007). (Pubitemid 350030878)
81. Romieu, P. et al. Histone deacetylase inhibitors decrease cocaine but not sucrose self-administration in rats. J. Neurosci. 28, 9342-9348 (2008).
82. Kim, W. Y., Kim, S. & Kim, J. H. Chronic microinjection of valproic acid into the nucleus accumbens attenuates amphetamine-induced locomotor activity. Neurosci. Lett. 432, 54-57 (2008).
83. Levine, A. 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)
84. Finkel, T., Deng, C. X. & Mostoslavsky, R. Recent progress in the biology and physiology of sirtuins. Nature 460, 587-591 (2009).
85. Maze, I. et al. Cocaine dynamically regulates heterochromatin and repetitive element unsilencing in nucleus accumbens. Proc. Natl Acad. Sci. USA 108, 3035-3040 (2011).
86. Sun, H. et al. Cocaine and stress regulates ATPase-containing chromatin remodelers. Soc. Neurosci. Abstr. 909.14 ((Washington DC, 12-16 Nov 2011).
87. Damez-Werno, D. et al. Histone arginine methylation in the nucleus accumbens in response to chronic cocaine and social stress. Soc. Neurosci. Abstr. 909.16 (Washington DC, 12-16 Nov 2011).
88. Kennedy, P. J. et al. Differential histone H2A variant expression in the nucleus accumbens following repeated exposure to cocaine or morphine. Soc. Neurosci. Abstr. 909.15 (Washington DC, 12-16 Nov 2011).
89. Scobie, K., Damez-Werno, D., Sun, H., Kennedy, P. J. & Nestler, E. J. Role of poly(ADP-ribosyl)ation in drug-seeking behavior and resiliency to stress. Soc. Neurosci. Abstr. 909.18 (Washington DC, 12-16 Nov 2011).
90. Renthal, W. et al. Delta FosB mediates epigenetic desensitization of the c-fos gene after chronic amphetamine exposure. J. Neurosci. 28, 7344-7349 (2008).
91. Newell-Price, J., Clark, A. J. & King, P. DNA methylation and silencing of gene expression. Trends Endocrinol. Metab. 11, 142-148 (2000). (Pubitemid 30238547)
92. Kim, J. K., Samaranayake, M. & Pradhan, S. Epigenetic mechanisms in mammals. Cell. Mol. Life Sci. 66, 596-612 (2009).
93. Chahrour, M. & Zoghbi, H. Y. The story of Rett syndrome: from clinic to neurobiology. Neuron 56, 422-437 (2007). (Pubitemid 350026269)
94. Wang, Y. & Leung, F. C. An evaluation of new criteria for CpG islands in the human genome as gene markers. Bioinformatics 20, 1170-1177 (2004). (Pubitemid 38660354)
95. Guo, J. U., Su, Y., Zhong, C., Ming, G. L. & Song, H. Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 145, 423-434 (2011).
96. Williams, K. et al. TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature 473, 343-348 (2011).
97. Wu, H. et al. Dual functions of Tet1 in transcriptional regulation in mouse embryonic stem cells. Nature 473, 389-393 (2011).
98. Pastor, W. A. et al. Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells. Nature 473, 394-397 (2011).
99. Ficz, G. et al. Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature 473, 398-402 (2011).
100. Chahrour, M. & Zoghbi, H. Y. The story of Rett syndrome: from clinic to neurobiology. Neuron 56, 422-437 (2007). (Pubitemid 350026269)
101. Host, L., Dietrich, J. B., Carouge, D., Aunis, D. & Zwiller, J. Cocaine self-administration alters the expression of chromatin-remodelling proteins; modulation by histone deacetylase inhibition. J. Psychopharmacol. 25, 222-229 (2011).
102. Cassel, S. et al. Fluoxetine and cocaine induce the epigenetic factors MeCP2 and MBD1 in adult rat brain. Mol. Pharmacol. 70, 487-492 (2006). (Pubitemid 44092309)
103. Im, H. I., Hollander, J. A., Bali, P. & Kenny, P. J. MeCP2 controls BDNF expression and cocaine intake through homeostatic interactions with microRNA-212. Nature Neurosci. 13, 1120-1127 (2010).
104. Deng, J. V. et al. MeCP2 in the nucleus accumbens contributes to neural and behavioral responses to psychostimulants. Nature Neurosci. 13, 1128-1136 (2010).
105. Graham, D. L. et al. Dynamic BDNF activity in nucleus accumbens with cocaine use increases self-administration and relapse. Nature Neurosci. 10, 1029-1037 (2007). (Pubitemid 47185197)
106. LaPlant, Q. et al. Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens. Nature Neurosci. 13, 1137-1143 (2010).
107. Vassoler, F. M., White, S. L., Ortinski, P. I., Sadri-Vakili, G. & Pierce, R. C. Paternal transmission of a cocaine resistance phenotype in male offspring. Soc. Neurosci. Abstr. 219.2 (Washington DC, 12-16 Nov 2011).
108. Taft, R. J., Pang, K. C., Mercer, T. R., Dinger, M. & Mattick, J. S. Non-coding RNAs: regulators of disease. J. Pathol. 220, 126-139 (2010).
109. Li, M. D. & van der Vaart, A. D. MicroRNAs in addiction: adaptations middlemen? Mol. Psychiatry 24 May 2011 (doi: 10.1038/mp.2011.58).
110. Hollander, J. A. et al. Striatal microRNA controls cocaine intake through CREB signalling. Nature 466, 197-202 (2010).
111. Chandrasekar, V. & Dreyer, J. L. microRNAs miR-124, let-7d and miR-181a regulate cocaine-induced plasticity. Mol. Cell. Neurosci. 42, 350-362 (2009).
112. Chandrasekar, V. & Dreyer, J. L. 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, 1149-1164 (2011).
113. Rajasethupathy P. et al. Characterization of small RNAs in Aplysia reveals a role for miR-124 in constraining synaptic plasticity through CREB. Neuron 63, 803-817 (2009).
114. Schaefer, A. et al. Argonaute 2 in dopamine 2 receptor-expressing neurons regulates cocaine addiction. J. Exp. Med. 207, 1843-1851 (2010).
115. Zheng, H. et al. mu-Opioid receptor agonists differentially regulate the expression of miR-190 and NeuroD. Mol. Pharmacol. 77, 102-109 (2010).
116. He, Y., Yang, C., Kirkmire, C. M. & Wang, Z. J. Regulation of opioid tolerance by let-7 family microRNA targeting the mu opioid receptor. J. Neurosci. 30, 10251-10258 (2010).
117. Sanchez-Simon, F. M., Zhang, X. X., Loh, H. H., Law, P. Y. & Rodriguez, R. E. Morphine regulates dopaminergic neuron differentiation via miR-133b. Mol. Pharmacol. 78, 935-942 (2010).
118. Pietrzykowski, A. Z. et al. Posttranscriptional regulation of BK channel splice variant stability by miR-9 underlies neuroadaptation to alcohol. Neuron 59, 274-287 (2008). (Pubitemid 352033687)
119. Pietrzykowski, A. Z. The role of microRNAs in drug addiction: a big lesson from tiny molecules. Int. Rev. Neurobiol. 91, 1-24 (2010).
120. Eipper-Mains, J. E. et al. MicroRNA-Seq reveals cocaine-regulated expression of striatal microRNAs. RNA 17, 1529-1543 (2011).
121. Pelloux, Y., Everitt, B. J. & Dickinson, A. Compulsive drug seeking by rats under punishment: effects of drug taking history. Psychopharmacology 194, 127-137 (2007). (Pubitemid 47282729)
122. Pickens, C. L. et al. Neurobiology of the incubation of drug craving. Trends Neurosci. 34, 411-420 (2011).
123. OConnor, E. C., Chapman, K., Butler, P. & Mead, A. N. The predictive validity of the rat self-administration model for abuse liability. Neurosci. Biobehav. Rev. 35, 912-938 (2011).
124. Laganiere, J. et al. An engineered zinc finger protein activator of the endogenous glial cell line-derived neurotrophic factor gene provides functional neuroprotection in a rat model of Parkinsons disease. J. Neurosci. 30, 16469-16474 (2010).
125. Zhang, F. et al. Efficient construction of sequence-specific TAL effectors for modulating mammalian transcription. Nature Biotech. 29, 149-153 (2011).
126. Cheung, I. et al. Developmental regulation and individual differences of neuronal H3K4me3 epigenomes in the prefrontal cortex. Proc. Natl Acad. Sci. USA 107, 8824-8829 (2010).
127. Philibert, R. A. et al. The effect of smoking on MAOA promoter methylation in DNA prepared from lymphoblasts and whole blood. Am. J. Med. Genet. B Neuropsychiatr. Genet. 153B, 619-628, (2010).
128. Launay, J. M. et al. Smoking induces long-lasting effects through a monoamine-oxidase epigenetic regulation. PLoS ONE 4, e7959 (2009).
129. Philibert, R. A., Gunter, T. D., Beach, S. R., Brody, G. H. & 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)
130. Lobo, M. K. et al. Cell type-specific loss of BDNF signaling mimics optogenetic control of cocaine reward. Science 330, 385-390 (2010).
131. Witten, I. B. et al. Cholinergic interneurons control local circuit activity and cocaine conditioning. Science 330, 1677-1681 (2010).
132. Self, D. W. in The Dopamine Receptors 2nd edn (ed. Neve, K. A.) 479-524 (Humana Press, New York, 2010).
133. Nye, H. E., Hope, B. T., Kelz, M. B., Iadarola, M. & Nestler, E. J. Pharmacological studies of the regulation of chronic FOS-related antigen induction by cocaine in the striatum and nucleus accumbens. J. Pharmacol. Exp. Ther. 275, 1671-1680 (1995). (Pubitemid 26129960)
134. Lee, K. W. et al. Cocaine-induced dendritic spine formation in D1 and D2 dopamine receptor-containing medium spiny neurons in nucleus accumbens. Proc. Natl Acad. Sci. USA 103, 3399-3404 (2006).
135. Maze, I. et al. G9a regulates cocaine-induced behavioral and transcriptional plasticity in a cell-type specific manner Soc. Neurosci. Abstr. 574.7 (California, 13-17 Nov 2010).
136. Singla, S., Kreitzer, A. C. & Malenka, R. C. Mechanisms for synapse specificity during striatal long-term depression. J. Neurosci. 27, 5260-5264 (2007). (Pubitemid 46741769)
137. Li, Y., Acerbo, M. J. & Robinson, T. E. The induction of behavioural sensitization is associated with cocaine-induced structural plasticity in the core (but not shell) of the nucleus accumbens. Eur. J. Neurosci. 20, 1647-1654 (2004). (Pubitemid 39274048)
138. Russo, S. J., Mazei-Robison, M. S., Ables, J. L. & Nestler, E. J. Neurotrophic factors and structural plasticity in addiction. Neuropharmacology 56, 73-82 (2009).
139. Nestler, E. J. & Aghajanian, G. K. Molecular and cellular basis of addiction. Science 278, 58-63 (1997). (Pubitemid 27446271)
140. Van Bockstaele, E. J., Reyes, B. A. & Valentino, R. J. The locus coeruleus: a key nucleus where stress and opioids intersect to mediate vulnerability to opiate abuse. Brain Res. 1314, 162-174(2010).
141. Han, M. H. et al. Role of cAMP response element-binding protein in the rat locus ceruleus: regulation of neuronal activity and opiate withdrawal behaviors. J. Neurosci. 26, 4624-4629 (2006).
142. Cao, J. L. et al. Essential role of the cAMP-cAMP response-element binding protein pathway in opiate-induced homeostatic adaptations of locus coeruleus neurons. Proc. Natl Acad. Sci. USA 107, 17011-17016 (2010).
143. Fattore, L., Altea, S. & Fratta, W. Sex differences in drug addiction: a review of animal and human studies. Womens Health 4, 51-65 (2008).
144. Carroll, M. E. & Anker, J. J. Sex differences and ovarian hormones in animal models of drug dependence. Horm. Behav. 58, 44-56 (2010).
145. Lynch, W. J. & Carroll, M. E. Sex differences in the acquisition of intravenously self-administered cocaine and heroin in rats. Psychopharmacology 144, 77-82 (1999). (Pubitemid 29242673)
146. Roth, M. E. & Carroll, M. E. Sex differences in the escalation of intravenous cocaine intake following long- or short-access to cocaine self-administration. Pharmacol. Biochem. Behav. 78, 199-207 (2004). (Pubitemid 38829354)
147. Cailhol, S. & Mormede, P. Strain and sex differences in the locomotor response and behavioral sensitization to cocaine in hyperactive rats. Brain Res. 842, 200-205 (1999). (Pubitemid 29447867)
148. Robinson, T. E., Becker, J. B. & Presty, S. K. Long-term facilitation of amphetamine-induced rotational behavior and striatal dopamine release produced by a single exposure to amphetamine: sex differences. Brain Res. 253, 231-241 (1982). (Pubitemid 13212235)
149. Hernandez-Avila, C. A., Rounsaville, B. J. & Kranzler, H. R. Opioid-, cannabis- and alcohol-dependent women show more rapid progression to substance abuse treatment. Drug Alcohol Depend. 74, 265-272 (2004). (Pubitemid 38759781)
150. Munro, C. A. et al. Sex differences in striatal dopamine release in healthy adults. Biol. Psychiatry 59, 966-974 (2006).
151. Hodes, G. E., Christoffel, D. J., Golden, S. A., Ahn, H. F. & Russo, S. J. Sex differences in epigenetic regulation of stress-related disorders. Soc. Neurosci. Abstr. 219.01 (Washington DC, 12-16 Nov 2011).