The role of histone acetylation in cocaine-induced neural plasticity and behavior

Neuropsychopharmacology

Volumn 38, Issue 1, 2013, Pages 94-110

  Rogge, George A ^a   Wood, Marcelo A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

acetylation; CBP; cocaine; epigenetics; HAT; HDAC

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; COCAINE; DOPAMINE; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE 4; HISTONE DEACETYLASE 5; HISTONE H3; HISTONE H4; SIRTUIN 1; SIRTUIN 2;

BEHAVIOR CHANGE; BEHAVIOR CONTROL; COMPLEX FORMATION; DOPAMINERGIC NERVE CELL; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION REGULATION; HISTONE ACETYLATION; HUMAN; IN VIVO STUDY; NERVE CELL PLASTICITY; NONHUMAN; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN LOCALIZATION; REVIEW; TRANSCRIPTION REGULATION; VENTRAL TEGMENTUM;

ACETYLATION; ANIMALS; COCAINE; DRUG-SEEKING BEHAVIOR; EPIGENESIS, GENETIC; HISTONES; HUMANS; NEURONAL PLASTICITY; SIGNAL TRANSDUCTION;

EID: 84869087521     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2012.154     Document Type: Review

References (92)

1. Ahn JH, McAvoy T, Rakhilin SV, Nishi A, Greengard P, Nairn AC (2007). Protein kinase A activates protein phosphatase 2A by phosphorylation of the B56delta subunit. Proc Natl Acad Sci USA 104: 2979-2984.
2. Alberini CM (2009). Transcription factors in long-term memory and synaptic plasticity. Physiol Rev 89: 121-145.
3. Alenghat T, Meyers K, Mullican SE, Leitner K, Adeniji-Adele A, Avila J et al (2008). Nuclear receptor corepressor and histone deacetylase 3 govern circadian metabolic physiology. Nature 456: 997-1000.
4. Barrett RM, Wood MA (2008). Beyond transcription factors: the role of chromatin modifying enzymes in regulating transcription required for memory. Learn Mem 15: 460-467.
5. Barrett RM, Malvaez M, Kramar E, Matheos DP, Arrizon A, Cabrera SM et al (2011). Hippocampal focal knockout of CBP affects specific histone modifications, longterm potentiation, and long-term memory. Neuropsychopharmacology 36: 1545-1556.
6. Berglind WJ, Whitfield TW Jr., LaLumiere RT, Kalivas PW, McGinty JF (2009). A single intra-PFC infusion of BDNF prevents cocaine-induced alterations in extracellular glutamate within the nucleus accumbens. J Neurosci 29: 3715-3719.
7. Berglind WJ, See RE, Fuchs RA, Ghee SM, Whitfield TW Jr., Miller SW et al (2007). A BDNF infusion into the medial prefrontal cortex suppresses cocaine seeking in rats. Eur J Neurosci 26: 757-766.
8. Bibb JA, Chen J, Taylor JR, Svenningsson P, Nishi A, Snyder GL et al (2001). Effects of chronic exposure to cocaine are regulated by the neuronal protein Cdk5. Nature 410: 376-380.
9. Carlezon WA Jr., Duman RS, Nestler EJ (2005). The many faces of CREB. Trends Neurosci 28: 436-445.
10. Carlezon WA Jr., Thome J, Olson VG, Lane-Ladd SB, Brodkin ES, Hiroi N et al (1998). Regulation of cocaine reward by CREB. Science 282: 2272-2275.
11. Chandrasekar V, Dreyer JL (2010). The Brain-Specific Neural Zinc Finger Transcription Factor 2b (NZF-2b/7ZFMyt1) Suppresses Cocaine Self-Administration in Rats. Front Behav Neurosci 4: 14.
12. Chandrasekar V, Dreyer JL (2010b). The brain-specific Neural Zinc Finger transcription factor 2b (NZF-2b/7ZFMyt1) causes suppression of cocaineinduced locomotor activity. Neurobiol Dis 37: 86-98.
13. Chawla S, Vanhoutte P, Arnold FJ, Huang CL, Bading H (2003). Neuronal activitydependent nucleocytoplasmic shuttling of HDAC4 and HDAC5. J Neurochem 85: 151-159.
14. Chrivia JC, Kwok RP, Lamb N, Hagiwara M, Montminy MR, Goodman RH (1993). Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 365: 855-859.
15. Daunais JB, Roberts DC, McGinty JF (1993). Cocaine self-administration increases preprodynorphin, but not c-fos, mRNA in rat striatum. Neuroreport 4: 543-546.
16. Dietrich JB, Takemori H, Grosch-Dirrig S, Bertorello A, Zwiller J (2012). Cocaine induces the expression of MEF2C transcription factor in rat striatum through activation of SIK1 and phosphorylation of the histone deacetylase HDAC5. Synapse 66: 61-70.
17. Edmondson DG, Davie JK, Zhou J, Mirnikjoo B, Tatchell K, Dent SY (2002). Sitespecific loss of acetylation upon phosphorylation of histone H3. J Biol Chem 277: 29496-29502.
18. Ehrman RN, Robbins SJ, Childress AR, O'Brien CP (1992). Conditioned responses to cocaine-related stimuli in cocaine abuse patients. Psychopharmacology (Berl) 107: 523-529.
19. Everitt BJ, Robbins TW (2005). Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 8: 1481-1489.
20. Everitt BJ, Belin D, Economidou D, Pelloux Y, Dalley JW, Robbins TW (2008). Review. Neural mechanisms underlying the vulnerability to develop compulsive drug-seeking habits and addiction. Philos Trans R Soc Lond B Biol Sci 363: 3125-3135.
21. Finkel T, Deng CX, Mostoslavsky R (2009). Recent progress in the biology and physiology of sirtuins. Nature 460: 587-591.
22. Fischer A, Sananbenesi F, Wang X, Dobbin M, Tsai LH (2007). Recovery of learning and memory is associated with chromatin remodelling. Nature 447: 178-182.
23. Fischle W, Dequiedt F, Hendzel MJ, Guenther MG, Lazar MA, Voelter W et al (2002). Enzymatic activity associated with class II HDACs is dependent on a multiprotein complex containing HDAC3 and SMRT/N-CoR. Mol Cell 9: 45-57.
24. Freeman WM, Patel KM, Brucklacher RM, Lull ME, Erwin M, Morgan D et al (2008). Persistent alterations in mesolimbic gene expression with abstinence from cocaine self-administration. Neuropsychopharmacology 33: 1807-1817.
25. Grimm JW, Lu L, Hayashi T, Hope BT, Su TP, Shaham Y (2003). 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.
26. Grozinger CM, Schreiber SL (2000). Regulation of histone deacetylase 4 and 5 and transcriptional activity by 14-3-3-dependent cellular localization. Proc Natl Acad Sci USA 97: 7835-7840.
27. Guan JS, Haggarty SJ, Giacometti E, Dannenberg JH, Joseph N, Gao J et al (2009) HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 459: 55-60.
28. Guenther MG, Barak O, Lazar MA (2001) The SMRT and N-CoR corepressors are activating cofactors for histone deacetylase 3. Mol Cell Biol 21: 6091-6101.
29. Hall FS, Sora I, Drgonova J, Li XF, Goeb M, Uhl GR (2004). Molecular mechanisms underlying the rewarding effects of cocaine. Ann NY Acad Sci 1025: 47-56.
30. Harting K, Knoll B (2009). SIRT2-mediated protein deacetylation: An emerging key regulator in brain physiology and pathology. Eur J Cell Biol 89: 262-269.
31. Hope B, Kosofsky B, Hyman SE, Nestler EJ (1992). 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.
32. Host L, Dietrich JB, Carouge D, Aunis D, Zwiller J (2012). Cocaine selfadministration alters the expression of chromatin-remodelling proteins; modulation by histone deacetylase inhibition. J Psychopharmacol 25: 222-229.
33. Hui B, Wang W, Li J (2010). Biphasic modulation of cocaine-induced conditioned place preference through inhibition of histone acetyltransferase and histone deacetylase. Saudi Med J 31: 389-393.
34. Hyman SE (2005). Addiction: a disease of learning and memory. Am J Psychiatry 162: 1414-1422.
35. Hyman SE, Malenka RC (2001). Addiction and the brain: the neurobiology of compulsion and its persistence. Nat Rev Neurosci 2: 695-703.
36. Hyman SE, Malenka RC, Nestler EJ (2006). Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 29: 565-598.
37. Kang-Decker N, Tong C, Boussouar F, Baker DJ, Xu W, Leontovich AA et al (2004). Loss of CBP causes T cell lymphomagenesis in synergy with p27Kip1 insufficiency. Cancer Cell 5: 177-189.
38. Karagianni P, Wong J (2007). HDAC3: taking the SMRT-N-CoRrect road to repression. Oncogene 26: 5439-5449.
39. Kilgore M, Miller CA, Fass DM, Hennig KM, Haggarty SJ, Sweatt JD et al (2010). Inhibitors of class 1 histone deacetylases reverse contextual memory deficits in a mouse model of Alzheimer's disease. Neuropsychopharmacology 35: 870-880.
40. Kilts CD, Schweitzer JB, Quinn CK, Gross RE, Faber TL, Muhammad F et al (2001). Neural activity related to drug craving in cocaine addiction. Arch Gen Psychiatry 58: 334-341.
41. Koob GF, Le Moal M (2005). Plasticity of reward neurocircuitry and the 0dark side' of drug addiction. Nat Neurosci 8: 1442-1444.
42. Koob GF, Volkow ND (2010). Neurocircuitry of addiction. Neuropsychopharmacology 35: 217-238.
43. Korutla L, Wang PJ, Mackler SA (2005). The POZ/BTB protein NAC1 interacts with two different histone deacetylases in neuronal-like cultures. J Neurochem 94: 786-793.
44. Korzus E, Rosenfield MG, Mayford M (2004). CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 42: 961-972.
45. Kouzarides T (2007). Chromatin modifications and their function. Cell 128: 693-705.
46. Kuhar MJ, Ritz MC, Sharkey J (1988). Cocaine receptors on dopamine transporters mediate cocaine-reinforced behavior. NIDA Res Monogr 88: 14-22.
47. Kumar A, Choi KH, Renthal W, Tsankova NM, Theobald DE, Truong HT et al (2005). Chromatin remodeling is a key mechanism underlying cocaine-induced plasticity in striatum. Neuron 48: 303-314.
48. Laherty CD, Yang WM, Sun JM, Davie JR, Seto E, Eisenman RN (1997). Histone deacetylases associated with the mSin3 corepressor mediate mad transcriptional repression. Cell 89: 349-356.
49. Lahm A, Paolini C, Pallaoro M, Nardi MC, Jones P, Neddermann P et al (2007). Unraveling the hidden catalytic activity of vertebrate class IIa histone deacetylases. Proc Natl Acad Sci USA 104: 17335-17340.
50. LaPlant Q, Nestler EJ (2011). CRACKing the histone code: cocaine0s effects on chromatin structure and function. Horm Behav 59: 321-330.
51. Lattal KM, Barrett RM, Wood MA (2007). Systemic or intrahippocampal delivery of histone deacetylase inhibitors facilitates fear extinction. Behav Neurosci 121: 1125-1131.
52. Levine AA, Guan Z, Barco A, Xu S, Kandel ER, Schwartz JH (2005). 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.
53. Liu QR, Lu L, Zhu XG, Gong JP, Shaham Y, Uhl GR (2006). Rodent BDNF genes, novel promoters, novel splice variants, and regulation by cocaine. Brain Res 1067: 1-12.
54. Malvaez M, Barrett RM, Wood MA, Sanchis-Segura C (2009). Epigenetic mechanisms underlying extinction of memory and drug-seeking behavior. Mamm Genome 20: 612-623.
55. Malvaez M, Sanchis-Segura C, Vo D, Lattal KM, Wood MA (2010). Modulation of chromatin modification facilitates extinction of cocaine-induced conditioned place preference. Biol Psychiatry 67: 36-43.
56. Malvaez M, Mhillaj E, Matheos DP, Palmery M, Wood MA (2011). CBP in the nucleus accumbens regulates cocaine-induced histone acetylation and is critical for cocaine-associated behaviors. J Neurosci 31: 16941-16948.
57. Maze I, Covington HE 3rd, Dietz DM, LaPlant Q, Renthal W, Russo SJ et al (2010). Essential role of the histone methyltransferase G9a in cocaine-induced plasticity. Science 327: 213-216.
58. Maze I, Nestler EJ (2011). The epigenetic landscape of addiction. Ann NY Acad Sci 1216: 99-113.
59. McClung CA, Nestler EJ (2003). Regulation of gene expression and cocaine reward by CREB and DeltaFosB. Nat Neurosci 6: 1208-1215.
60. McClung CA, Nestler EJ (2008). Neuroplasticity mediated by altered gene expression. Neuropsychopharmacology 33: 3-17.
61. McGinty JF, Whitfield TW Jr., Berglind WJ (2010). Brain-derived neurotrophic factor and cocaine addiction. Brain Res 1314: 183-193.
62. McQuown SC, Wood MA (2010). Epigenetic regulation in substance use disorders. Curr Psychiatry Rep 12: 145-153.
63. McQuown SC, Wood MA (2011b). HDAC3 and the molecular brake pad hypothesis. Neurobiol Learn Mem 96: 27-34.
64. McQuown SC, Barrett RM, Matheos DP, Post RJ, Rogge GA, Alenghat T et al (2011). HDAC3 is a critical negative regulator of long-term memory formation. J Neurosci 31: 764-774.
65. Nestler EJ (2001). Molecular basis of long-term plasticity underlying addiction. Nat Rev Neurosci 2: 119-128.
66. Nestler EJ (2002). Common molecular and cellular substrates of addiction and memory. Neurobiol Learn Mem 78: 637-647.
67. Nestler EJ (2004). Historical review: Molecular and cellular mechanisms of opiate and cocaine addiction. Trends Pharmacol Sci 25: 210-218.
68. Nestler EJ (2004b) Molecular mechanisms of drug addiction. Neuropharmacology 47(Suppl 1): 24-32.
69. O'Brien CP, Childress AR, Ehrman R, Robbins SJ (1998) Conditioning factors in drug abuse: can they explain compulsion? J Psychopharmacol 12: 15-22.
70. Pulipparacharuvil S, Renthal W, Hale CF, Taniguchi M, Xiao G, Kumar A et al (2008). Cocaine regulates MEF2 to control synaptic and behavioral plasticity. Neuron 59: 621-633.
71. Renthal W, Carle TL, Maze I, Covington HE 3rd, Truong HT, Alibhai I et al (2008). Delta FosB mediates epigenetic desensitization of the c-fos gene after chronic amphetamine exposure. J Neurosci 28: 7344-7349.
72. Renthal W, Maze I, Krishnan V, Covington HE 3rd, Xiao G, Kumar A et al (2007). Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron 56: 517-529.
73. Renthal W, Nestler EJ (2009a). Histone acetylation in drug addiction. Semin Cell Dev Biol 20: 387-394.
74. Renthal W, Kumar A, Xiao G, Wilkinson M, Covington HE 3rd, Maze I et al (2009). Genome-wide analysis of chromatin regulation by cocaine reveals a role for sirtuins. Neuron 62: 335-348.
75. Ritz MC, Lamb RJ, Goldberg SR, Kuhar MJ (1987). Cocaine receptors on dopamine transporters are related to self-administration of cocaine. Science 237: 1219-1223.
76. Ritz MC, Lamb RJ, Goldberg SR, Kuhar MJ (1988). Cocaine self-administration appears to be mediated by dopamine uptake inhibition. Prog Neuropsychopharmacol Biol Psychiatry 12: 233-239.
77. Robison AJ, Nestler EJ (2011). Transcriptional and epigenetic mechanisms of addiction. Nat Rev Neurosci 12: 623-637.
78. Romm E, Nielsen JA, Kim JG, Hudson LD (2005). Myt1 family recruits histone deacetylase to regulate neural transcription. J Neurochem 93: 1444-1453.
79. Roozendaal B, Hernandez A, Cabrera SM, Hagewoud R, Malvaez M, Stefanko DP et al (2010). Membrane-associated glucocorticoid activity is necessary for modulation of long-term memory via chromatin modification. J Neurosci 30: 5037-5046.
80. Sadri-Vakili G, Kumaresan V, Schmidt HD, Famous KR, Chawla P, Vassoler FM et al (2010). 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: 11735-11744.
81. Schmidt HD, Sangrey GR, Darnell SB, Schassburger RL, Cha JH, Pierce RC et al (2012). 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: 202-209.
82. Stafford JM, Raybuck JD, Ryabinin AE, Lattal KM (2012). Increasing Histone Acetylation in the Hippocampus-Infralimbic Network Enhances Fear Extinction. Biol Psychiatry 72: 25-33.
83. Strahl BO, Allis CD (2000). The language of covalent histone modifications. Nature 403: 41-45.
84. Tanaka Y, Naruse I, Maekawa T, Masuya H, Shiroishi T, Ishii S (1997). Abnormal skeletal patterning in embryos lacking a single Cbp allele: a partial similarity with Rubinstein-Taybi syndrome. Proc Natl Acad Sci USA 94: 10215-10220.
85. Taniguchi M, Carreira MB, Smith LN, Zirlin BC, Neve RL, Cowan CW (2012). Histone deacetylase 5 limits cocaine reward through cAMP-induced nuclear import. Neuron 73: 108-120.
86. Turner BM (2002). Cellular memory and the histone code. Cell 111: 285-291.
87. Vecsey CG, Hawk JD, Lattal KM, Stein JM, Fabian SA, Attner MA et al (2007). Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB:CBP-dependent transcriptional activation. J Neurosci 27: 6128-6140.
88. Verdin E, Dequiedt F, Kasler HG (2003). Class II histone deacetylases: versatile regulators. Trends Genet 19: 286-293.
89. Wang L, Lv Z, Hu Z, Sheng J, Hui B, Sun J et al (2010). 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.
90. West AE, Chen WG, Dalva MB, Dolmetsch RE, Kornhauser JM, Shaywitz AJ et al (2001). Calcium regulation of neuronal gene expression. Proc Natl Acad Sci USA 98: 11024-11031.
91. White FJ, Kalivas PW (1998). Neuroadaptations involved in amphetamine and cocaine addiction. Drug Alcohol Depend 51: 141-153.
92. Yuferov V, Kroslak T, Laforge KS, Zhou Y, Ho A, Kreek MJ (2003). Differential gene expression in the rat caudate putamen after 'binge0 cocaine administration: advantage of triplicate microarray analysis. Synapse 48: 157-169.