Mechanisms of epigenetic memory and addiction

EMBO Journal

Volumn 33, Issue 10, 2014, Pages 1091-1103

  Tuesta, Luis M ^a,b,c,d   Zhang, Yi ^a,b,c,d  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d HARVARD STEM CELL INSTITUTE   (United States)

Author keywords

Addiction; DNA methylation; Epigenetics; Histone modifications; Learning memory

Indexed keywords

DNA; HISTONE; MICRORNA;

BRAIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA METHYLATION; DRUG DEPENDENCE; EPIGENETICS; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN; INHERITANCE; LEARNING; LONG TERM POTENTIATION; MEMORY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REINFORCEMENT; REVIEW; REWARD; ADDICTION; GENETIC EPIGENESIS; GENETICS; METABOLISM; PHYSIOLOGY;

DNA METHYLATION; EPIGENESIS, GENETIC; HISTONES; HUMANS; LEARNING; MEMORY; SUBSTANCE-RELATED DISORDERS;

EID: 84900873681     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1002/embj.201488106     Document Type: Review

References (157)

1. Alarcon JM, Malleret G, Touzani K, Vronskaya S, Ishii S, Kandel ER, Barco A, (2004) Chromatin acetylation, memory, and LTP are impaired in CBP+/-mice: a model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron 42: 947-959
2. Amir RE, Van den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY, (1999) Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat Genet 23: 185-188
3. Anier K, Malinovskaja K, Aonurm-Helm A, Zharkovsky A, Kalda A, (2010) DNA methylation regulates cocaine-induced behavioral sensitization in mice. Neuropsychopharmacology 35: 2450-2461
4. Anthony JC, Warner LA, Kessler RC, (1994) Comparative epidemiology of dependence on tobacco, alcohol, controlled substances, and inhalants: basic findings from the National Comorbidity Survey. Exp Clin Psychopharmacol 2: 244-268
5. Bahari-Javan S, Maddalena A, Kerimoglu C, Wittnam J, Held T, Bahr M, Burkhardt S, Delalle I, Kugler S, Fischer A, Sananbenesi F, (2012) HDAC1 regulates fear extinction in mice. J Neurosci 32: 5062-5073
6. Bali P, Kenny PJ, (2013) MicroRNAs and drug addiction. Frontiers in genetics 4: 43
7. Bannister AJ, Kouzarides T, (2011) Regulation of chromatin by histone modifications. Cell Res 21: 381-395
8. Benson LJ, Gu Y, Yakovleva T, Tong K, Barrows C, Strack CL, Cook RG, Mizzen CA, Annunziato AT, (2006) Modifications of H3 and H4 during chromatin replication, nucleosome assembly, and histone exchange. J Biol Chem 281: 9287-9296
9. Bestor TH, (1992) Activation of mammalian DNA methyltransferase by cleavage of a Zn binding regulatory domain. EMBO J 11: 2611-2617
10. Bird AP, (1986) CpG-rich islands and the function of DNA methylation. Nature 321: 209-213
11. Bliss TV, Collingridge GL, (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31-39
12. Bocklisch C, Pascoli V, Wong JC, House DR, Yvon C, de Roo M, Tan KR, Luscher C, (2013) Cocaine disinhibits dopamine neurons by potentiation of GABA transmission in the ventral tegmental area. Science 341: 1521-1525
13. Borrelli E, Nestler EJ, Allis CD, Sassone-Corsi P, (2008) Decoding the epigenetic language of neuronal plasticity. Neuron 60: 961-974
14. Broide RS, Redwine JM, Aftahi N, Young W, Bloom FE, Winrow CJ, (2007) Distribution of histone deacetylases 1-11 in the rat brain. J Mol Neurosci 31: 47-58
15. Brooks PJ, Marietta C, Goldman D, (1996) DNA mismatch repair and DNA methylation in adult brain neurons. J Neurosci 16: 939-945
16. Brueckner B, Garcia Boy R, Siedlecki P, Musch T, Kliem HC, Zielenkiewicz P, Suhai S, Wiessler M, Lyko F, (2005) Epigenetic reactivation of tumor suppressor genes by a novel small-molecule inhibitor of human DNA methyltransferases. Cancer Res 65: 6305-6311
17. Campos EI, Reinberg D, (2009) Histones: annotating chromatin. Annu Rev Genet 43: 559-599
18. Chandrasekar V, Dreyer JL, (2009) microRNAs miR-124, let-7d and miR-181a regulate cocaine-induced plasticity. Mol Cell Neurosci 42: 350-362
19. Chandrasekar V, Dreyer JL, (2011) 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
20. Chen BT, Bowers MS, Martin M, Hopf FW, Guillory AM, Carelli RM, Chou JK, Bonci A, (2008) Cocaine but not natural reward self-administration nor passive cocaine infusion produces persistent LTP in the VTA. Neuron 59: 288-297
21. Chestier A, Yaniv M, (1979) Rapid turnover of acetyl groups in the four core histones of simian virus 40 minichromosomes. Proc Natl Acad Sci USA 76: 46-50
22. Colquitt BM, Allen WE, Barnea G, Lomvardas S, (2013) Alteration of genic 5-hydroxymethylcytosine patterning in olfactory neurons correlates with changes in gene expression and cell identity. Proc Natl Acad Sci USA 110: 14682-14687
23. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, Hsu PD, Wu X, Jiang W, Marraffini LA, Zhang F, (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339: 819-823
24. Coutellier L, Beraki S, Ardestani PM, Saw NL, Shamloo M, (2012) Npas4: a neuronal transcription factor with a key role in social and cognitive functions relevant to developmental disorders. PLoS ONE 7: e46604
25. Day JJ, Sweatt JD, (2011) Cognitive neuroepigenetics: a role for epigenetic mechanisms in learning and memory. Neurobiol Learn Mem 96: 2-12
26. Day JJ, Childs D, Guzman-Karlsson MC, Kibe M, Moulden J, Song E, Tahir A, Sweatt JD, (2014) DNA methylation regulates associative reward learning. Nat Neurosci 16: 1445-1452
27. Deng JV, Rodriguiz RM, Hutchinson AN, Kim IH, Wetsel WC, West AE, (2010) MeCP2 in the nucleus accumbens contributes to neural and behavioral responses to psychostimulants. Nat Neurosci 13: 1128-1136
28. Dias BG, Ressler KJ, (2014) Parental olfactory experience influences behavior and neural structure in subsequent generations. Nat Neurosci 17: 89-96
29. Emsley JG, Mitchell BD, Kempermann G, Macklis JD, (2005) Adult neurogenesis and repair of the adult CNS with neural progenitors, precursors, and stem cells. Prog Neurobiol 75: 321-341
30. Endres M, Meisel A, Biniszkiewicz D, Namura S, Prass K, Ruscher K, Lipski A, Jaenisch R, Moskowitz MA, Dirnagl U, (2000) DNA methyltrans-ferase contributes to delayed ischemic brain injury. J Neurosci 20: 3175-3181
31. Endres M, Fan G, Meisel A, Dirnagl U, Jaenisch R, (2001) Effects of cerebral ischemia in mice lacking DNA methyltransferase 1 in post-mitotic neurons. NeuroReport 12: 3763-3766
32. English CM, Maluf NK, Tripet B, Churchill ME, Tyler JK, (2005) ASF1 binds to a heterodimer of histones H3 and H4: a two-step mechanism for the assembly of the H3-H4 heterotetramer on DNA. Biochemistry 44: 13673-13682
33. English CM, Adkins MW, Carson JJ, Churchill ME, Tyler JK, (2006) Structural basis for the histone chaperone activity of Asf1. Cell 127: 495-508
34. Esteve PO, Chin HG, Smallwood A, Feehery GR, Gangisetty O, Karpf AR, Carey MF, Pradhan S, (2006) Direct interaction between DNMT1 and G9a coordinates DNA and histone methylation during replication. Genes Dev 20: 3089-3103
35. Everitt BJ, Dickinson A, Robbins TW, (2001) The neuropsychological basis of addictive behaviour. Brain Res Brain Res Rev 36: 129-138
36. Fan G, Beard C, Chen RZ, Csankovszki G, Sun Y, Siniaia M, Biniszkiewicz D, Bates B, Lee PP, Kuhn R, Trumpp A, Poon C, Wilson CB, Jaenisch R, (2001) DNA hypomethylation perturbs the function and survival of CNS neurons in postnatal animals. J Neurosci 21: 788-797
37. Fedorova E, Zink D, (2008) Nuclear architecture and gene regulation. Biochim Biophys Acta 1783: 2174-2184
38. Feng J, Nestler EJ, (2013) Epigenetic mechanisms of drug addiction. Curr Opin Neurobiol 23: 521-528
39. Feng J, Chang H, Li E, Fan G, (2005) Dynamic expression of de novo DNA methyltransferases Dnmt3a and Dnmt3b in the central nervous system. J Neurosci Res 79: 734-746
40. Feng J, Zhou Y, Campbell SL, Le T, Li E, Sweatt JD, Silva AJ, Fan G, (2010) Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons. Nat Neurosci 13: 423-430
41. 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
42. Fowler CD, Kenny PJ, (2011) Intravenous nicotine self-administration and cue-induced reinstatement in mice: effects of nicotine dose, rate of drug infusion and prior instrumental training. Neuropharmacology 61: 687-698
43. Goll MG, Bestor TH, (2005) Eukaryotic cytosine methyltransferases. Annu Rev Biochem 74: 481-514
44. Guan JS, Haggarty SJ, Giacometti E, Dannenberg JH, Joseph N, Gao J, Nieland TJ, Zhou Y, Wang X, Mazitschek R, Bradner JE, DePinho RA, Jaenisch R, Tsai LH, (2009) HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 459: 55-60
45. Guo JU, Ma DK, Mo H, Ball MP, Jang MH, Bonaguidi MA, Balazer JA, Eaves HL, Xie B, Ford E, Zhang K, Ming GL, Gao Y, Song H, (2011a) Neuronal activity modifies the DNA methylation landscape in the adult brain. Nat Neurosci 14: 1345-1351
46. Guo JU, Su Y, Zhong C, Ming GL, Song H, (2011b) Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 145: 423-434
47. He J, Ye J, Cai Y, Riquelme C, Liu JO, Liu X, Han A, Chen L, (2011a) Structure of p300 bound to MEF2 on DNA reveals a mechanism of enhanceosome assembly. Nucleic Acids Res 39: 4464-4474
48. He YF, Li BZ, Li Z, Liu P, Wang Y, Tang Q, Ding J, Jia Y, Chen Z, Li L, Sun Y, Li X, Dai Q, Song CX, Zhang K, He C, Xu GL, (2011b) Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333: 1303-1307
49. Hermann A, Goyal R, Jeltsch A, (2004) The Dnmt1 DNA-(cytosine-C5)- methyltransferase methylates DNA processively with high preference for hemimethylated target sites. J Biol Chem 279: 48350-48359
50. Hollander JA, Im HI, Amelio AL, Kocerha J, Bali P, Lu Q, Willoughby D, Wahlestedt C, Conkright MD, Kenny PJ, (2010) Striatal microRNA controls cocaine intake through CREB signalling. Nature 466: 197-202
51. Holliday R, Pugh JE, (1975) DNA modification mechanisms and gene activity during development. Science 187: 226-232
52. Huang C, Xu M, Zhu B, (2013) Epigenetic inheritance mediated by histone lysine methylation: maintaining transcriptional states without the precise restoration of marks? Philos Trans R Soc Lond B Biol Sci 368: 20110332
53. 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
54. Im HI, Hollander JA, Bali P, Kenny PJ, (2010) MeCP2 controls BDNF expression and cocaine intake through homeostatic interactions with microRNA-212. Nat Neurosci 13: 1120-1127
55. Inano K, Suetake I, Ueda T, Miyake Y, Nakamura M, Okada M, Tajima S, (2000) Maintenance-type DNA methyltransferase is highly expressed in post-mitotic neurons and localized in the cytoplasmic compartment. J Biochem 128: 315-321
56. Ito S, D'Alessio AC, Taranova OV, Hong K, Sowers LC, Zhang Y, (2010) Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 466: 1129-1133
57. Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, He C, Zhang Y, (2011) Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333: 1300-1303
58. Jackson V, Shires A, Chalkley R, Granner DK, (1975) Studies on highly metabolically active acetylation and phosphorylation of histones. J Biol Chem 250: 4856-4863
59. Jaenisch R, Bird A, (2003) Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33 (Suppl): 245-254
60. Jin SG, Wu X, Li AX, Pfeifer GP, (2011) Genomic mapping of 5-hydroxymethyl-cytosine in the human brain. Nucleic Acids Res 39: 5015-5024
61. Johnson PM, Kenny PJ, (2010) Dopamine D2 receptors in addiction-like reward dysfunction and compulsive eating in obese rats. Nat Neurosci 13: 635-641
62. Kaas GA, Zhong C, Eason DE, Ross DL, Vachhani RV, Ming GL, King JR, Song H, Sweatt JD, (2013) TET1 controls CNS 5-methylcytosine hydroxylation, active DNA demethylation, gene transcription, and memory formation. Neuron 79: 1086-1093
63. Kalivas PW, Duffy P, DuMars LA, Skinner C, (1988) Behavioral and neurochemical effects of acute and daily cocaine administration in rats. J Pharmacol Exp Ther 245: 485-492
64. Kelley AE, (2004) Memory and addiction: shared neural circuitry and molecular mechanisms. Neuron 44: 161-179
65. Kennedy PJ, Feng J, Robison AJ, Maze I, Badimon A, Mouzon E, Chaudhury D, Damez-Werno DM, Haggarty SJ, Han MH, Bassel-Duby R, Olson EN, Nestler EJ, (2013) Class I HDAC inhibition blocks cocaine-induced plasticity by targeted changes in histone methylation. Nat Neurosci 16: 434-440
66. Khare T, Pai S, Koncevicius K, Pal M, Kriukiene E, Liutkeviciute Z, Irimia M, Jia P, Ptak C, Xia M, Tice R, Tochigi M, Morera S, Nazarians A, Belsham D, Wong AH, Blencowe BJ, Wang SC, Kapranov P, Kustra R, et al, (2012) 5-hmC in the brain is abundant in synaptic genes and shows differences at the exon-intron boundary. Nat Struct Mol Biol 19: 1037-1043
67. Kim JJ, Jung MW, (2006) Neural circuits and mechanisms involved in Pavlovian fear conditioning: a critical review. Neurosci Biobehav Rev 30: 188-202
68. Kim MS, Akhtar MW, Adachi M, Mahgoub M, Bassel-Duby R, Kavalali ET, Olson EN, Monteggia LM, (2012) An essential role for histone deacetylase 4 in synaptic plasticity and memory formation. J Neurosci 32: 10879-10886
69. Klose RJ, Bird AP, (2006) Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci 31: 89-97
70. Klose RJ, Kallin EM, Zhang Y, (2006) JmjC-domain-containing proteins and histone demethylation. Nat Rev Genet 7: 715-727
71. Kohli RM, Zhang Y, (2013) TET enzymes, TDG and the dynamics of DNA demethylation. Nature 502: 472-479
72. Koob GF, Le Moal M, (2001) Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology 24: 97-129
73. Kornberg RD, Lorch Y, (1999) Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 98: 285-294
74. Kouzarides T, (2007) Chromatin modifications and their function. Cell 128: 693-705
75. Kriaucionis S, Heintz N, (2009) The nuclear DNA base 5- hydroxymethylcytosine is present in Purkinje neurons and the brain. Science 324: 929-930
76. Kumar A, Choi KH, Renthal W, Tsankova NM, Theobald DE, Truong HT, Russo SJ, Laplant Q, Sasaki TS, Whistler KN, Neve RL, Self DW, Nestler EJ, (2005) Chromatin remodeling is a key mechanism underlying cocaine-induced plasticity in striatum. Neuron 48: 303-314
77. LaPlant Q, Vialou V, Covington HE 3rd, Dumitriu D, Feng J, Warren BL, Maze I, Dietz DM, Watts EL, Iniguez SD, Koo JW, Mouzon E, Renthal W, Hollis F, Wang H, Noonan MA, Ren Y, Eisch AJ, Bolanos CA, Kabbaj M, et al, (2010) Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens. Nat Neurosci 13: 1137-1143
78. Le AD, Li Z, Funk D, Shram M, Li TK, Shaham Y, (2006) Increased vulnerability to nicotine self-administration and relapse in alcohol-naive offspring of rats selectively bred for high alcohol intake. J Neurosci 26: 1872-1879
79. Leffak IM, Grainger R, Weintraub H, (1977) Conservative assembly and segregation of nucleosomal histones. Cell 12: 837-845
80. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, Chen L, Chen L, Chen TM, Chin MC, Chong J, Crook BE, Czaplinska A, Dang CN, Datta S, Dee NR, et al, (2007) Genome-wide atlas of gene expression in the adult mouse brain. Nature 445: 168-176
81. Leonhardt H, Page AW, Weier HU, Bestor TH, (1992) A targeting sequence directs DNA methyltransferase to sites of DNA replication in mammalian nuclei. Cell 71: 865-873
82. Levenson JM, Roth TL, Lubin FD, Miller CA, Huang IC, Desai P, Malone LM, Sweatt JD, (2006) Evidence that DNA (cytosine-5) methyltransferase regulates synaptic plasticity in the hippocampus. J Biol Chem 281: 15763-15773
83. 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
84. Lin Y, Bloodgood BL, Hauser JL, Lapan AD, Koon AC, Kim TK, Hu LS, Malik AN, Greenberg ME, (2008) Activity-dependent regulation of inhibitory synapse development by Npas4. Nature 455: 1198-1204
85. Lisman JE, Grace AA, (2005) The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron 46: 703-713
86. Luscher C, Malenka RC, (2012) NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD). Cold Spring Harb Perspect Biol 4: pii: a005710
87. Ma DK, Jang MH, Guo JU, Kitabatake Y, Chang ML, Pow-Anpongkul N, Flavell RA, Lu B, Ming GL, Song H, (2009) Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323: 1074-1077
88. Malvaez M, McQuown SC, Rogge GA, Astarabadi M, Jacques V, Carreiro S, Rusche JR, Wood MA, (2013) HDAC3-selective inhibitor enhances extinction of cocaine-seeking behavior in a persistent manner. Proc Natl Acad Sci USA 110: 2647-2652
89. Margueron R, Trojer P, Reinberg D, (2005) The key to development: interpreting the histone code? Curr Opin Genet Dev 15: 163-176
90. Margueron R, Justin N, Ohno K, Sharpe ML, Son J, Drury WJ 3rd, Voigt P, Martin SR, Taylor WR, De Marco V, Pirrotta V, Reinberg D, Gamblin SJ, (2009) Role of the polycomb protein EED in the propagation of repressive histone marks. Nature 461: 762-767
91. Martin C, Zhang Y, (2005) The diverse functions of histone lysine methylation. Nat Rev Mol Cell Biol 6: 838-849
92. Martin C, Zhang Y, (2007) Mechanisms of epigenetic inheritance. Curr Opin Cell Biol 19: 266-272
93. Maze I, Covington HE 3rd, Dietz DM, LaPlant Q, Renthal W, Russo SJ, Mechanic M, Mouzon E, Neve RL, Haggarty SJ, Ren Y, Sampath SC, Hurd YL, Greengard P, Tarakhovsky A, Schaefer A, Nestler EJ, (2010) Essential role of the histone methyltransferase G9a in cocaine-induced plasticity. Science 327: 213-216
94. Metzger E, Wissmann M, Yin N, Muller JM, Schneider R, Peters AH, Gunther T, Buettner R, Schule R, (2005) LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 437: 436-439
95. Miller CA, Sweatt JD, (2007) Covalent modification of DNA regulates memory formation. Neuron 53: 857-869
96. Miller CA, Gavin CF, White JA, Parrish RR, Honasoge A, Yancey CR, Rivera IM, Rubio MD, Rumbaugh G, Sweatt JD, (2010) Cortical DNA methylation maintains remote memory. Nat Neurosci 13: 664-666
97. Milutinovic S, Zhuang Q, Szyf M, (2002) Proliferating cell nuclear antigen associates with histone deacetylase activity, integrating DNA replication and chromatin modification. J Biol Chem 277: 20974-20978
98. Moore LD, Le T, Fan G, (2013) DNA methylation and its basic function. Neuropsychopharmacology 38: 23-38
99. Nabel CS, Jia H, Ye Y, Shen L, Goldschmidt HL, Stivers JT, Zhang Y, Kohli RM, (2012) AID/APOBEC deaminases disfavor modified cytosines implicated in DNA demethylation. Nat Chem Biol 8: 751-758
100. Nisell M, Nomikos GG, Svensson TH, (1994) Systemic nicotine-induced dopamine release in the rat nucleus accumbens is regulated by nicotinic receptors in the ventral tegmental area. Synapse 16: 36-44
101. Oliveira AM, Hemstedt TJ, Bading H, (2012) Rescue of aging-associated decline in Dnmt3a2 expression restores cognitive abilities. Nat Neurosci 15: 1111-1113
102. Ooi SK, Bestor TH, (2008) The colorful history of active DNA demethylation. Cell 133: 1145-1148
103. Palamarchouk V, Smagin G, Goeders NE, (2009) Self-administered and passive cocaine infusions produce different effects on corticosterone concentrations in the medial prefrontal cortex (MPC) of rats. Pharmacol Biochem Behav 94: 163-168
104. Pesavento JJ, Yang H, Kelleher NL, Mizzen CA, (2008) Certain and progressive methylation of histone H4 at lysine 20 during the cell cycle. Mol Cell Biol 28: 468-486
105. Picciotto MR, Zoli M, Rimondini R, Lena C, Marubio LM, Pich EM, Fuxe K, Changeux JP, (1998) Acetylcholine receptors containing the beta2 subunit are involved in the reinforcing properties of nicotine. Nature 391: 173-177
106. Ramamoorthi K, Fropf R, Belfort GM, Fitzmaurice HL, McKinney RM, Neve RL, Otto T, Lin Y, (2011) Npas4 regulates a transcriptional program in CA3 required for contextual memory formation. Science 334: 1669-1675
107. Ran FA, Hsu PD, Lin CY, Gootenberg JS, Konermann S, Trevino AE, Scott DA, Inoue A, Matoba S, Zhang Y, Zhang F, (2013a) Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154: 1380-1389
108. Ran FA, Hsu PD, Wright J, Agarwala V, Scott DA, Zhang F, (2013b) Genome engineering using the CRISPR-Cas9 system. Nat Protoc 8: 2281-2308
109. Renthal W, Carle TL, Maze I, Covington HE 3rd, Truong HT, Alibhai I, Kumar A, Montgomery RL, Olson EN, Nestler EJ, (2008) Delta FosB mediates epigenetic desensitization of the c-fos gene after chronic amphetamine exposure. J Neurosci 28: 7344-7349
110. Renthal W, Kumar A, Xiao G, Wilkinson M, Covington HE 3rd, Maze I, Sikder D, Robison AJ, LaPlant Q, Dietz DM, Russo SJ, Vialou V, Chakravarty S, Kodadek TJ, Stack A, Kabbaj M, Nestler EJ, (2009) Genome-wide analysis of chromatin regulation by cocaine reveals a role for sirtuins. Neuron 62: 335-348
111. Robison AJ, Nestler EJ, (2011) Transcriptional and epigenetic mechanisms of addiction. Nat Rev Neurosci 12: 623-637
112. Rogan MT, Staubli UV, LeDoux JE, (1997) Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390: 604-607
113. Rudenko A, Dawlaty MM, Seo J, Cheng AW, Meng J, Le T, Faull KF, Jaenisch R, Tsai LH, (2013) Tet1 is critical for neuronal activity-regulated gene expression and memory extinction. Neuron 79: 1109-1122
114. Russo SJ, Nestler EJ, (2013) The brain reward circuitry in mood disorders. Nat Rev Neurosci 14: 609-625
115. Sadri-Vakili G, Kumaresan V, Schmidt HD, Famous KR, Chawla P, Vassoler FM, Overland RP, Xia E, Bass CE, Terwilliger EF, Pierce RC, Cha JH, (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
116. Sando R 3rd, Gounko N, Pieraut S, Liao L, Yates J 3rd, Maximov A, (2012) HDAC4 governs a transcriptional program essential for synaptic plasticity and memory. Cell 151: 821-834
117. Saper CB, Chou TC, Elmquist JK, (2002) The need to feed: homeostatic and hedonic control of eating. Neuron 36: 199-211
118. Scatton B, Simon H, Le Moal M, Bischoff S, (1980) Origin of dopamin-ergic innervation of the rat hippocampal formation. Neurosci Lett 18: 125-131
119. Schroeder FA, Penta KL, Matevossian A, Jones SR, Konradi C, Tapper AR, Akbarian S, (2008) 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: 2981-2992
120. Shen HY, Kalda A, Yu L, Ferrara J, Zhu J, Chen JF, (2008) 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: 644-655
121. Shen L, Wu H, Diep D, Yamaguchi S, D'Alessio AC, Fung HL, Zhang K, Zhang Y, (2013) Genome-wide analysis reveals TET-and TDG-dependent 5-methylcytosine oxidation dynamics. Cell 153: 692-706
122. Smith ZD, Meissner A, (2013) DNA methylation: roles in mammalian development. Nat Rev Genet 14: 204-220
123. Stefanko DP, Barrett RM, Ly AR, Reolon GK, Wood MA, (2009) Modulation of long-term memory for object recognition via HDAC inhibition. Proc Natl Acad Sci USA 106: 9447-9452
124. Sun H, Maze I, Dietz DM, Scobie KN, Kennedy PJ, Damez-Werno D, Neve RL, Zachariou V, Shen L, Nestler EJ, (2012) Morphine epigenomically regulates behavior through alterations in histone H3 lysine 9 dimethylation in the nucleus accumbens. J Neurosci 32: 17454-17464
125. Sutcliffe JS, Nelson DL, Zhang F, Pieretti M, Caskey CT, Saxe D, Warren ST, (1992) DNA methylation represses FMR-1 transcription in fragile X syndrome. Hum Mol Genet 1: 397-400
126. Swank MW, Sweatt JD, (2001) Increased histone acetyltransferase and lysine acetyltransferase activity and biphasic activation of the ERK/RSK cascade in insular cortex during novel taste learning. J Neurosci 21: 3383-3391
127. Sweet SM, Li M, Thomas PM, Durbin KR, Kelleher NL, (2010) Kinetics of re-establishing H3K79 methylation marks in global human chromatin. J Biol Chem 285: 32778-32786
128. Szulwach KE, Li X, Li Y, Song CX, Wu H, Dai Q, Irier H, Upadhyay AK, Gearing M, Levey AI, Vasanthakumar A, Godley LA, Chang Q, Cheng X, He C, Jin P, (2011) 5-hmC-mediated epigenetic dynamics during postnatal neurodevelopment and aging. Nat Neurosci 14: 1607-1616
129. Szyf M, (2009) Epigenetics, DNA methylation, and chromatin modifying drugs. Annu Rev Pharmacol Toxicol 49: 243-263
130. Tagami H, Ray-Gallet D, Almouzni G, Nakatani Y, (2004) Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116: 51-61
131. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, Rao A, (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324: 930-935
132. Thomas MJ, Kalivas PW, Shaham Y, (2008) Neuroplasticity in the mesolimbic dopamine system and cocaine addiction. Br J Pharmacol 154: 327-342
133. Toni N, Buchs PA, Nikonenko I, Bron CR, Muller D, (1999) LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 402: 421-425
134. Torregrossa MM, Corlett PR, Taylor JR, (2011) Aberrant learning and memory in addiction. Neurobiol Learn Mem 96: 609-623
135. Tsukada Y, Fang J, Erdjument-Bromage H, Warren ME, Borchers CH, Tempst P, Zhang Y, (2006) Histone demethylation by a family of JmjC domain-containing proteins. Nature 439: 811-816
136. Tuesta LM, Fowler CD, Kenny PJ, (2011) Recent advances in understanding nicotinic receptor signaling mechanisms that regulate drug self-administration behavior. Biochem Pharmacol 82: 984-995
137. Van Esch H, Bauters M, Ignatius J, Jansen M, Raynaud M, Hollanders K, Lugtenberg D, Bienvenu T, Jensen LR, Gecz J, Moraine C, Marynen P, Fryns JP, Froyen G, (2005) Duplication of the MECP2 region is a frequent cause of severe mental retardation and progressive neurological symptoms in males. Am J Hum Genet 77: 442-453
138. Vassoler FM, White SL, Schmidt HD, Sadri-Vakili G, Pierce RC, (2013) Epigenetic inheritance of a cocaine-resistance phenotype. Nat Neurosci 16: 42-47
139. Veldic M, Caruncho HJ, Liu WS, Davis J, Satta R, Grayson DR, Guidotti A, Costa E, (2004) DNA-methyltransferase 1 mRNA is selectively overexpressed in telencephalic GABAergic interneurons of schizophrenia brains. Proc Natl Acad Sci USA 101: 348-353
140. Volkel P, Angrand PO, (2007) The control of histone lysine methylation in epigenetic regulation. Biochimie 89: 1-20
141. Volkow ND, Fowler JS, Wang GJ, Hitzemann R, Logan J, Schlyer DJ, Dewey SL, Wolf AP, (1993) Decreased dopamine D2 receptor availability is associated with reduced frontal metabolism in cocaine abusers. Synapse 14: 169-177
142. Volkow ND, Wang GJ, Telang F, Fowler JS, Thanos PK, Logan J, Alexoff D, Ding YS, Wong C, Ma Y, Pradhan K, (2008) Low dopamine striatal D2 receptors are associated with prefrontal metabolism in obese subjects: possible contributing factors. NeuroImage 42: 1537-1543
143. Weintraub H, Worcel A, Alberts B, (1976) A model for chromatin based upon two symmetrically paired half-nucleosomes. Cell 9: 409-417
144. Wood MA, Attner MA, Oliveira AM, Brindle PK, Abel T, (2006a) A transcription factor-binding domain of the coactivator CBP is essential for long-term memory and the expression of specific target genes. Learn Mem 13: 609-617
145. Wood MA, Hawk JD, Abel T, (2006b) Combinatorial chromatin modifications and memory storage: a code for memory? Learn Mem 13: 241-244
146. Wu H, Zhang Y, (2011) Mechanisms and functions of Tet protein-mediated 5-methylcytosine oxidation. Genes Dev 25: 2436-2452
147. Xu M, Long C, Chen X, Huang C, Chen S, Zhu B, (2010) Partitioning of histone H3-H4 tetramers during DNA replication-dependent chromatin assembly. Science 328: 94-98
148. Xu M, Wang W, Chen S, Zhu B, (2012) A model for mitotic inheritance of histone lysine methylation. EMBO Rep 13: 60-67
149. Yamane K, Toumazou C, Tsukada Y, Erdjument-Bromage H, Tempst P, Wong J, Zhang Y, (2006) JHDM2A, a JmjC-containing H3K9 demethylase, facilitates transcription activation by androgen receptor. Cell 125: 483-495
150. Yu M, Hon GC, Szulwach KE, Song CX, Zhang L, Kim A, Li X, Dai Q, Shen Y, Park B, Min JH, Jin P, Ren B, He C, (2012) Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome. Cell 149: 1368-1380
151. Zee BM, Levin RS, Xu B, LeRoy G, Wingreen NS, Garcia BA, (2010) In vivo residue-specific histone methylation dynamics. J Biol Chem 285: 3341-3350
152. van Zessen R, Phillips JL, Budygin EA, Stuber GD, (2012) Activation of VTA GABA neurons disrupts reward consumption. Neuron 73: 1184-1194
153. Zhang Y, (2003) Transcriptional regulation by histone ubiquitination and deubiquitination. Genes Dev 17: 2733-2740
154. Zhang L, Lu X, Lu J, Liang H, Dai Q, Xu GL, Luo C, Jiang H, He C, (2012) Thymine DNA glycosylase specifically recognizes 5-carboxylcytosine-modified DNA. Nat Chem Biol 8: 328-330
155. Zhang RR, Cui QY, Murai K, Lim YC, Smith ZD, Jin S, Ye P, Rosa L, Lee YK, Wu HP, Liu W, Xu ZM, Yang L, Ding YQ, Tang F, Meissner A, Ding C, Shi Y, Xu GL, (2013) Tet1 regulates adult hippocampal neurogenesis and cognition. Cell Stem Cell 13: 237-245
156. Zheng H, Berthoud HR, (2007) Eating for pleasure or calories. Curr Opin Pharmacol 7: 607-612
157. Zhu B, Reinberg D, (2011) Epigenetic inheritance: uncontested? Cell Res 21: 435-441