Molecular mechanisms of synaptic remodeling in alcoholism

Neuroscience Letters

Volumn 601, Issue , 2014, Pages 11-19

  Kyzar, Evan J ^a   Pandey, Subhash C ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Alcoholism; Amygdala; Dendritic spines; Epigenetics; Histone acetylation; Histone deacetylases; Synaptic plasticity

Indexed keywords

ALCOHOL; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE INHIBITOR; KAPPA OPIATE RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ALCOHOL ABUSE; ALCOHOLISM; COGNITION; DENDRITIC SPINE; EPIGENETICS; HUMAN; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SYNAPSE; GENETIC EPIGENESIS; MALE; METABOLISM; PATHOLOGY; PHYSIOLOGY;

ALCOHOLISM; COGNITION; DENDRITIC SPINES; EPIGENESIS, GENETIC; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE INHIBITORS; HUMANS; MALE; NEURONAL PLASTICITY; RECEPTORS, OPIOID, KAPPA; SYNAPSES;

EID: 84952628389     PISSN: 03043940     EISSN: 18727972     Source Type: Journal    
DOI: 10.1016/j.neulet.2015.01.051     Document Type: Review

References (144)

1. Spanagel R. Alcoholism: a systems approach from molecular physiology to addictive behavior. Physiol. Rev. 2009, 89:649-705.
2. Pandey S.C. Anxiety and alcohol abuse disorders: a common role for CREB and its target the neuropeptide Y gene. Trends Pharmacol. Sci. 2003, 24:456-460.
3. Moonat S., Pandey S.C. Stress, epigenetics, and alcoholism. Alcohol Res. 2012, 34:495-505.
4. Koob G.F., Volkow N.D. Neurocircuitry of addiction. Neuropsychopharmacology 2010, 35:217-238.
5. Koob G.F. Addiction is a reward deficit and stress surfeit disorder. Front. Psychiatry 2013, 4:72.
6. Koob G.F., Moal M.Le Plasticity of reward neurocircuitry and the 'dark side' of drug addiction. Nat. Neurosci. 2005, 8:1442-1444.
7. Koob G.F. Alcoholism: allostasis and beyond. Alcohol. Clin. Exp. Res. 2003, 27:232-243.
8. Alheid G.F. Extended amygdala and basal forebrain. Ann. N.Y. Acad. Sci. 2003, 985:185-205.
9. Kauer J.A., Malenka R.C. Synaptic plasticity and addiction. Nat. Rev. Neurosci. 2007, 8:844-858.
10. Spiga S., Mulas G., Piras F., Diana M. The addicted spine. Front. Neuroanat. 2014, 8:110.
11. Maze I., Nestler E.J. The epigenetic landscape of addiction. Ann. N.Y. Acad. Sci. 2011, 1216:99-113.
12. Dong Y., Nestler E.J. The neural rejuvenation hypothesis of cocaine addiction. Trends Pharmacol. Sci. 2014, 35:374-383.
13. Abbott L.F., Nelson S.B. Synaptic plasticity: taming the beast. Nat. Neurosci. 2000, 3(Suppl):1178-1183.
14. Bliss T.V., Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361:31-39.
15. Yoon B.-J., Smith G.B., Heynen A.J., Neve R.L., Bear M.F. Essential role for a long-term depression mechanism in ocular dominance plasticity. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:9860-9865.
16. Creed M.C., Lüscher C. Drug-evoked synaptic plasticity: beyond metaplasticity. Curr. Opin. Neurobiol. 2013, 23:553-558.
17. Lüscher C., Malenka R.C. Drug-evoked synaptic plasticity in addiction: from molecular changes to circuit remodeling. Neuron 2011, 69:650-663.
18. McCool B.A. Ethanol modulation of synaptic plasticity. Neuropharmacology 2011, 61:1097-1108.
19. Engert F., Bonhoeffer T. Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 1999, 399:66-70.
20. Steward O., Wallace C.S., Lyford G.L., Worley P.F. Synaptic activation causes the mRNA for the lEG Arc to localize selectively near activated postsynaptic sites on dendrites. Neuron 1998, 21:741-751.
21. Steward O., Worley P.F. Selective targeting of newly synthesized Arc mRNA to active synapses requires NMDA receptor activation. Neuron 2001, 30:227-240.
22. Yoshimura A., Fujii R., Watanabe Y., Okabe S., Fukui K., Takumi T. Myosin-Va facilitates the accumulation of mRNA/protein complex in dendritic spines. Curr. Biol. 2006, 16:2345-2351.
23. Chowdhury S., Shepherd J.D., Okuno H., Lyford G., Petralia R.S., Plath N., et al. Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron 2006, 52:445-459.
24. Pandey S.C., Zhang H., Ugale R., Prakash A., Xu T., Misra K. Effector immediate-early gene arc in the amygdala plays a critical role in alcoholism. J. Neurosci. 2008, 28:2589-2600.
25. You C., Zhang H., Sakharkar A.J., Teppen T., Pandey S.C. Reversal of deficits in dendritic spines, BDNF and Arc expression in the amygdala during alcohol dependence by HDAC inhibitor treatment. Int. J. Neuropsychopharmacol. 2014, 17:313-322.
26. Zhou F.C., Anthony B., Dunn K.W., Lindquist W.B., Xu Z.C., Deng P. Chronic alcohol drinking alters neuronal dendritic spines in the brain reward center nucleus accumbens. Brain Res. 2007, 1134:148-161.
27. Riley J.N., Walker D.W. Morphological alterations in hippocampus after long-term alcohol consumption in mice. Science 1978, 201:646-648.
28. Ferrer I., Fabregues I., Rairiz J., Galofre E. Decreased numbers of dendritic spines on cortical pyramidal neurons in human chronic alcoholism. Neurosci. Lett. 1986, 69:115-119.
29. Bramham C.R., Worley P.F., Moore M.J., Guzowski J.F. The immediate early gene arc/arg3.1: regulation, mechanisms, and function. J. Neurosci. 2008, 28:11760-11767.
30. Moonat S., Sakharkar A.J., Zhang H., Pandey S.C. The role of amygdaloid brain-derived neurotrophic factor, activity-regulated cytoskeleton-associated protein and dendritic spines in anxiety and alcoholism. Addict. Biol. 2011, 16:238-250.
31. Malenka R.C., Nicoll R.A. NMDA-receptor-dependent synaptic plasticity: multiple forms and mechanisms. Trends Neurosci. 1993, 16:521-527.
32. Tsien J.Z., Huerta P.T., Tonegawa S. The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 1996, 87:1327-1338.
33. Lau C.G., Zukin R.S. NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders. Nat. Rev. Neurosci. 2007, 8:413-426.
34. Lovinger D.M., White G., Weight F.F. Ethanol inhibits NMDA-activated ion current in hippocampal neurons. Science 1989, 243:1721-1724.
35. Roberto M., Schweitzer P., Madamba S.G., Stouffer D.G., Parsons L.H., Siggins G.R. Acute and chronic ethanol alter glutamatergic transmission in rat central amygdala: an in vitro and in vivo analysis. J. Neurosci. 2004, 24:1594-1603.
36. Roberto M., Bajo M., Crawford E., Madamba S.G., Siggins G.R. Chronic ethanol exposure and protracted abstinence alter NMDA receptors in central amygdala. Neuropsychopharmacology 2006, 31:988-996.
37. Carpenter-Hyland E.P., Woodward J.J., Chandler L.J. Chronic ethanol induces synaptic but not extrasynaptic targeting of NMDA receptors. J. Neurosci. 2004, 24:7859-7868.
38. Zhu W., Bie B., Pan Z.Z. Involvement of non-NMDA glutamate receptors in central amygdala in synaptic actions of ethanol and ethanol-induced reward behavior. J. Neurosci. 2007, 27:289-298.
39. Läck A.K., Diaz M.R., Chappell A., DuBois D.W., McCool B.A. Chronic ethanol and withdrawal differentially modulate pre- and post-synaptic function at glutamatergic synapses in rat basolateral amygdala. J. Neurophysiol. 2007, 98:3185-3196.
40. Spiga S., Talani G., Mulas G., Licheri V., Fois G.R., Muggironi G., et al. Hampered long-term depression and thin spine loss in the nucleus accumbens of ethanol-dependent rats. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:3745-3754.
41. Gambrill A.C., Barria A. NMDA receptor subunit composition controls synaptogenesis and synapse stabilization. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:5855-5860.
42. Tovar K.R., Westbrook G.L. The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J. Neurosci. 1999, 19:4180-4188.
43. Williams K., Russell S.L., Shen Y.M., Molinoff P.B. Developmental switch in the expression of NMDA receptors occurs in vivo and in vitro. Neuron 1993, 10:267-278.
44. Sheng M., Cummings J., Roldan L.A., Jan Y.N., Jan L.Y. Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 1994, 368:144-147.
45. Barria A., Malinow R. Subunit-specific NMDA receptor trafficking to synapses. Neuron 2002, 35:345-353.
46. Barria A., Malinow R. NMDA receptor subunit composition controls synaptic plasticity by regulating binding to CaMKII. Neuron 2005, 48:289-301.
47. Halt A.R., Dallapiazza R.F., Zhou Y., Stein I.S., Qian H., Juntti S., et al. CaMKII binding to GluN2B is critical during memory consolidation. EMBO J. 2012, 31:1203-1216.
48. Suvarna N., Borgland S.L., Wang J., Phamluong K., Auberson Y.P., Bonci A., et al. Ethanol alters trafficking and functional N-methyl-d-aspartate receptor NR2 subunit ratio via H-Ras. J. Biol. Chem. 2005, 280:31450-31459.
49. Kroener S., Mulholland P.J., New N.N., Gass J.T., Becker H.C., Chandler L.J. Chronic alcohol exposure alters behavioral and synaptic plasticity of the rodent prefrontal cortex. PLoS One 2012, 7:e37541.
50. Kim A., Zamora-Martinez E.R., Edwards S., Mandyam C.D. Structural reorganization of pyramidal neurons in the medial prefrontal cortex of alcohol dependent rats is associated with altered glial plasticity. Brain Struct. Funct. 2014, (Mar). (Epub ahead of print).
51. Gass J.T., Chandler L.J. The Plasticity of Extinction: contribution of the prefrontal cortex in treating addiction through inhibitory learning. Front. Psychiatry 2013, 4:46.
52. Carpenter-Hyland E.P., Chandler L.J. Homeostatic plasticity during alcohol exposure promotes enlargement of dendritic spines. Eur. J. Neurosci. 2006, 24:3496-3506.
53. Huang Y.H., Lin Y., Mu P., Lee B.R., Brown T.E., Wayman G., et al. In vivo cocaine experience generates silent synapses. Neuron 2009, 63:40-47.
54. Gipson C.D., Reissner K.J., Kupchik Y.M., Smith A.C.W., Stankeviciute N., Hensley-Simon M.E., et al. Reinstatement of nicotine seeking is mediated by glutamatergic plasticity. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:9124-9129.
55. Shen H., Moussawi K., Zhou W., Toda S., Kalivas P.W. Heroin relapse requires long-term potentiation-like plasticity mediated by NMDA2b-containing receptors. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:19407-19412.
56. Crair M.C., Malenka R.C. A critical period for long-term potentiation at thalamocortical synapses. Nature 1995, 375:325-328.
57. Carmignoto G., Vicini S. Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science 1992, 258:1007-1011.
58. Murrell A., Rakyan V.K., Beck S. From genome to epigenome. Hum. Mol. Genet. 2005, 14:R3-R10.
59. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705.
60. Suzuki M.M., Bird A. DNA methylation landscapes: provocative insights from epigenomics. Nat. Rev. Genet. 2008, 9:465-476.
61. Starkman B.G., Sakharkar A.J., Pandey S.C. Epigenetics-beyond the genome in alcoholism. Alcohol Res. 2012, 34:293-305.
62. Borrelli E., Nestler E.J., Allis C.D., Sassone-Corsi P. Decoding the epigenetic language of neuronal plasticity. Neuron 2008, 60:961-974.
63. Allis C.D., Berger S.L., Cote J., Dent S., Jenuwien T., Kouzarides T., et al. New nomenclature for chromatin-modifying enzymes. Cell 2007, 131:633-636.
64. Strahl B.D., Allis C.D. The language of covalent histone modifications. Nature 2000, 403:41-45.
65. Abraham W.C. Metaplasticity: tuning synapses and networks for plasticity. Nat. Rev. Neurosci. 2008, 9:387.
66. Tsankova N., Renthal W., Kumar A., Nestler E.J. Epigenetic regulation in psychiatric disorders. Nat. Rev. Neurosci. 2007, 8:355-367.
67. Klose R.J., Bird A.P. Genomic DNA methylation: the mark and its mediators. Trends Biochem. Sci. 2006, 31:89-97.
68. Gardiner-Garden M., Frommer M. CpG islands in vertebrate genomes. J. Mol. Biol. 1987, 196:261-282.
69. Boyes J., Bird A. DNA methylation inhibits transcription indirectly via a methyl-CpG binding protein. Cell 1991, 64:1123-1134.
70. Nan X., Meehan R.R., Bird A. Dissection of the methyl-CpG binding domain from the chromosomal protein MeCP2. Nucleic Acids Res. 1993, 21:4886-4892.
71. Feng J., Zhou Y., Campbell S.L., Le T., Li E., Sweatt J.D., et al. Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons. Nat. Neurosci. 2010, 13:423-430.
72. Chen W.G., Chang Q., Lin Y., Meissner A., West A.E., Griffith E.C., et al. Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2. Science 2003, 302:885-889.
73. Gavin D.P., Chase K.A., Sharma R.P. Active DNA demethylation in post-mitotic neurons: a reason for optimism. Neuropharmacology 2013, 75:233-245.
74. Goll M.G., Bestor T.H. Eukaryotic cytosine methyltransferases. Annu. Rev. Biochem. 2005, 74:481-514.
75. Meehan R.R., Lewis J.D., McKay S., Kleiner E.L., Bird A.P. Identification of a mammalian protein that binds specifically to DNA containing methylated CpGs. Cell 1989, 58:499-507.
76. Chahrour M., Jung S.Y., Shaw C., Zhou X., Wong S.T.C., Qin J., et al. MeCP2 a key contributor to neurological disease, activates and represses transcription. Science 2008, 320:1224-1229.
77. Martinowich K., Hattori D., Wu H., Fouse S., He F., Hu Y., et al. DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science 2003, 302:890-893.
78. Zhou Z., Hong E.J., Cohen S., ning Zhao W., yi H., Ho H., Schmidt L., et al. Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation. Neuron 2006, 52:255-269.
79. Tahiliani M., Koh K.P., Shen Y., Pastor W.A., Bandukwala H., Brudno Y., et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009, 324:930-935.
80. 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 2011, 145:423-434.
81. Mellén M., Ayata P., Dewell S., Kriaucionis S., Heintz N. MeCP2 binds to 5hmC enriched within active genes and accessible chromatin in the nervous system. Cell 2012, 151:1417-1430.
82. Barreto G., Schäfer A., Marhold J., Stach D., Swaminathan S.K., Handa V., et al. Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 2007, 445:671-675.
83. Ma D.K., Jang M.-H., Guo J.U., Kitabatake Y., Chang M.-L., Pow-Anpongkul N., et al. Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 2009, 323:1074-1077.
84. Kaas G., Zhong C., Eason D., Ross D., Vachhani R., li Ming G., et al. TET1 controls CNS 5-methylcytosine hydroxylation, active DNA demethylation, gene transcription, and memory formation. Neuron 2013, 79:1086-1093.
85. Rudenko A., Dawlaty M., Seo J., Cheng A., Meng J., Le T., et al. Tet1 is critical for neuronal activity-regulated gene expression and memory extinction. Neuron 2013, 79:1109-1122.
86. Sultan F.A., Wang J., Tront J., Liebermann D.A., Sweatt J.D. Genetic deletion of gadd45b a regulator of active DNA demethylation, enhances long-term memory and synaptic plasticity. J. Neurosci. 2012, 32:17059-17066.
87. Wee S., Koob G.F. The role of the dynorphin-kappa opioid system in the reinforcing effects of drugs of abuse. Psychopharmacology (Berl.) 2010, 210:121-135.
88. Koob G.F., Le Moal M. Addiction and the brain antireward system. Annu. Rev. Psychol. 2008, 59:29-53.
89. Tejeda H.A., Shippenberg T.S., Henriksson R. The dynorphin/κ-opioid receptor system and its role in psychiatric disorders. Cell. Mol. Life Sci. 2012, 69:857-896.
90. Cole R.L., Konradi C., Douglass J., Hyman S.E. Neuronal adaptation to amphetamine and dopamine: molecular mechanisms of prodynorphin gene regulation in rat striatum. Neuron 1995, 14:813-823.
91. Knoll A.T., Carlezon W.A. Dynorphin, stress, and depression. Brain Res. 2010, 1314:56-73.
92. Nestler E.J. Historical review: molecular and cellular mechanisms of opiate and cocaine addiction. Trends Pharmacol. Sci. 2004, 25:210-218.
93. D'Addario C., Caputi F.F., Ekström T.J., Di Benedetto M., Maccarrone M., Romualdi P., et al. Ethanol induces epigenetic modulation of prodynorphin and pronociceptin gene expression in the rat amygdala complex. J. Mol. Neurosci. 2013, 49:312-319.
94. Walker B.M., Zorrilla E.P., Koob G.F. Systemic κ-opioid receptor antagonism by nor-binaltorphimine reduces dependence-induced excessive alcohol self-administration in rats. Addict. Biol. 2011, 16:116-119.
95. Taqi M.M., Bazov I., Watanabe H., Sheedy D., Harper C., Alkass K., et al. Prodynorphin CpG-SNPs associated with alcohol dependence: elevated methylation in the brain of human alcoholics. Addict. Biol. 2011, 16:499-509.
96. Valdez G.R., Platt D.M., Rowlett J.K., Rüedi-Bettschen D., Spealman R.D. Kappa agonist-induced reinstatement of cocaine seeking in squirrel monkeys: a role for opioid and stress-related mechanisms. J. Pharmacol. Exp. Ther. 2007, 323:525-533.
97. Rainnie D.G., Bergeron R., Sajdyk T.J., Patil M., Gehlert D.R., Shekhar A. Corticotrophin releasing factor-induced synaptic plasticity in the amygdala translates stress into emotional disorders. J. Neurosci. 2004, 24:3471-3479.
98. Schierloh A., Deussing J., Wurst W., Zieglgänsberger W., Rammes G. Corticotropin-releasing factor (CRF) receptor type 1-dependent modulation of synaptic plasticity. Neurosci. Lett. 2007, 416:82-86.
99. Baldwin H.A., Rassnick S., Rivier J., Koob G.F., Britton K.T. CRF antagonist reverses the anxiogenic response to ethanol withdrawal in the rat. Psychopharmacology (Berl.) 1991, 103:227-232.
100. Rassnick S., Heinrichs S.C., Britton K.T., Koob G.F. Microinjection of a corticotropin-releasing factor antagonist into the central nucleus of the amygdala reverses anxiogenic-like effects of ethanol withdrawal. Brain Res. 1993, 605:25-32.
101. Valdez G.R., Zorrilla E.P., Roberts A.J., Koob G.F. Antagonism of corticotropin-releasing factor attenuates the enhanced responsiveness to stress observed during protracted ethanol abstinence. Alcohol 2003, 29:55-60.
102. Pandey S.C., Ugale R., Zhang H., Tang L., Prakash A. Brain chromatin remodeling: a novel mechanism of alcoholism. J. Neurosci. 2008, 28:3729-3737.
103. Moonat S., Sakharkar A.J., Zhang H., Tang L., Pandey S.C. Aberrant histone deacetylase2-mediated histone modifications and synaptic plasticity in the amygdala predisposes to anxiety and alcoholism. Biol. Psychiatry 2013, 73:763-773.
104. Gonzalez G.A., Montminy M.R. Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 1989, 59:675-680.
105. Chrivia J.C., Kwok R.P., Lamb N., Hagiwara M., Montminy M.R., Goodman R.H. Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 1993, 365:855-859.
106. Murphy D.D., Segal M. Morphological plasticity of dendritic spines in central neurons is mediated by activation of cAMP response element binding protein. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:1482-1487.
107. Lonze B.E., Riccio A., Cohen S., Ginty D.D. Apoptosis, axonal growth defects, and degeneration of peripheral neurons in mice lacking CREB. Neuron 2002, 34:371-385.
108. Aguado F., Díaz-Ruiz C., Parlato R., Martínez A., Carmona M.A., Bleckmann S., et al. The CREB/CREM transcription factors negatively regulate early synaptogenesis and spontaneous network activity. J. Neurosci. 2009, 29:328-333.
109. Ogryzko V.V., Schiltz R.L., Russanova V., Howard B.H., Nakatani Y. The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell 1996, 87:953-959.
110. 2+ influx regulates BDNF transcription by a CREB family transcription factor-dependent mechanism. Neuron 1998, 20:709-726.
111. Poo M.M. Neurotrophins as synaptic modulators. Nat. Rev. Neurosci. 2001, 2:24-32.
112. Sakharkar A.J., Zhang H., Tang L., Baxstrom K., Shi G., Moonat S., et al. Effects of histone deacetylase inhibitors on amygdaloid histone acetylation and neuropeptide Y expression: a role in anxiety-like and alcohol-drinking behaviours. Int. J. Neuropsychopharmacol. 2014, 17:1207-1220.
113. Sakharkar A.J., Zhang H., Tang L., Shi G., Pandey S.C. Histone deacetylases (HDAC)-induced histone modifications in the amygdala: a role in rapid tolerance to the anxiolytic effects of ethanol. Alcohol. Clin. Exp. Res. 2012, 36:61-71.
114. Legastelois R., Botia B., Naassila M. Blockade of ethanol-induced behavioral sensitization by sodium butyrate: descriptive analysis of gene regulations in the striatum. Alcohol. Clin. Exp. Res. 2013, 37:1143-1153.
115. Guan J.-S., Haggarty S.J., Giacometti E., Dannenberg J.-H., Joseph N., Gao J., et al. HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 2009, 459:55-60.
116. Gräff J., Joseph N.F., Horn M.E., Samiei A., Meng J., Seo J., et al. Epigenetic priming of memory updating during reconsolidation to attenuate remote fear memories. Cell 2014, 156:261-276.
117. Gräff J., Rei D., Guan J.-S., Wang W.-Y., Seo J., Hennig K.M., et al. An epigenetic blockade of cognitive functions in the neurodegenerating brain. Nature 2012, 483:222-226.
118. Gräff J., Tsai L.-H. Histone acetylation: molecular mnemonics on the chromatin. Nat. Rev. Neurosci. 2013, 14:97-111.
119. Mastroeni D., Grover A., Delvaux E., Whiteside C., Coleman P.D., Rogers J. Epigenetic changes in Alzheimer's disease: decrements in DNA methylation. Neurobiol. Aging 2010, 31:2025-2037.
120. Brunmeir R., Lagger S., Seiser C. Histone deacetylase HDAC1/HDAC2-controlled embryonic development and cell differentiation. Int. J. Dev. Biol. 2009, 53:275-289.
121. Minucci S., Pelicci P.G. Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat. Rev. Cancer 2006, 6:38-51.
122. Wagner J.M., Hackanson B., Lübbert M., Jung M. Histone deacetylase (HDAC) inhibitors in recent clinical trials for cancer therapy. Clin. Epigenetics 2010, 1:117-136.
123. Gryder B.E., Sodji Q.H., Oyelere A.K. Targeted cancer therapy: giving histone deacetylase inhibitors all they need to succeed. Future Med. Chem. 2012, 4:505-524.
124. Kim H.-J., Bae S.-C. Histone deacetylase inhibitors: molecular mechanisms of action and clinical trials as anti-cancer drugs. Am. J. Transl. Res. 2011, 3:166-179.
125. Tan J., Cang S., Ma Y., Petrillo R.L., Liu D. Novel histone deacetylase inhibitors in clinical trials as anti-cancer agents. J. Hematol. Oncol. 2010, 3:5.
126. Kim H.S., Kim E.M., Kim N.J., Chang K.A., Choi Y., Ahn K.W., et al. Inhibition of histone deacetylation enhances the neurotoxicity induced by the C-terminal fragments of amyloid precursor protein. J. Neurosci. Res. 2004, 75:117-124.
127. Salminen A., Tapiola T., Korhonen P., Suuronen T. Neuronal apoptosis induced by histone deacetylase inhibitors. Mol. Brain Res. 1998, 61:203-206.
128. Khan O., La Thangue N.B. HDAC inhibitors in cancer biology: emerging mechanisms and clinical applications. Immunol. Cell Biol. 2012, 90:85-94.
129. Fischer A., Sananbenesi F., Wang X., Dobbin M., Tsai L.-H. Recovery of learning and memory is associated with chromatin remodelling. Nature 2007, 447:178-182.
130. Ricobaraza A., Cuadrado-Tejedor M., Pérez-Mediavilla A., Frechilla D., Del Río J., García-Osta A. Phenylbutyrate ameliorates cognitive deficit and reduces tau pathology in an Alzheimer's disease mouse model. Neuropsychopharmacology 2009, 34:1721-1732.
131. Francis Y.I., Fà M., Ashraf H., Zhang H., Staniszewski A., Latchman D.S., et al. Dysregulation of histone acetylation in the APP/PS1 mouse model of Alzheimer's disease. J. Alzheimers Dis. 2009, 18:131-139.
132. Walker M.P., Laferla F.M., Oddo S.S., Brewer G.J. Reversible epigenetic histone modifications and Bdnf expression in neurons with aging and from a mouse model of Alzheimer's disease. Age (Omaha) 2013, 35:519-531.
133. Peleg S., Sananbenesi F., Zovoilis A., Burkhardt S., Bahari-Javan S., Agis-Balboa R.C., et al. Altered histone acetylation is associated with age-dependent memory impairment in mice. Science 2010, 328:753-756.
134. Thomas E.A., Coppola G., Desplats P.A., Tang B., Soragni E., Burnett R., et al. The HDAC inhibitor 4b ameliorates the disease phenotype and transcriptional abnormalities in Huntington's disease transgenic mice. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:15564-15569.
135. Ferrante R.J., Kubilus J.K., Lee J., Ryu H., Beesen A., Zucker B., et al. Histone deacetylase inhibition by sodium butyrate chemotherapy ameliorates the neurodegenerative phenotype in Huntington's disease mice. J. Neurosci. 2003, 23:9418-9427.
136. Sadri-Vakili G., Bouzou B., Benn C.L., Kim M.O., Chawla P., Overland R.P., et al. Histones associated with downregulated genes are hypo-acetylated in Huntington's disease models. Hum. Mol. Genet. 2007, 16:1293-1306.
137. Rouaux C., Jokic N., Mbebi C., Boutillier S., Loeffler J.P., Boutillier A.L. Critical loss of CBP/p300 histone acetylase activity by caspase-6 during neurodegeneration. EMBO J. 2003, 22:6537-6549.
138. Rouaux C., Panteleeva I., René F., Gonzalez de Aguilar J.-L., Echaniz-Laguna A., Dupuis L., et al. Sodium valproate exerts neuroprotective effects in vivo through CREB-binding protein-dependent mechanisms but does not improve survival in an amyotrophic lateral sclerosis mouse model. J. Neurosci. 2007, 27:5535-5545.
139. Petrij F., Giles R.H., Dauwerse H.G., Saris J.J., Hennekam R.C., Masuno M., et al. Rubinstein-Taybi syndrome caused by mutations in the transcriptional co-activator CBP. Nature 1995, 376:348-351.
140. Korzus E., Rosenfeld M.G., Mayford M. CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 2004, 42:961-972.
141. Alarcón J.M., Malleret G., Touzani K., Vronskaya S., Ishii S., Kandel E.R., et al. Chromatin acetylation, memory, and LTP are impaired in CBP+/- mice: a model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron 2004, 42:947-959.
142. Covington H.E., Maze I., LaPlant Q.C., Vialou V.F., Ohnishi Y.N., Berton O., et al. Antidepressant actions of histone deacetylase inhibitors. J. Neurosci. 2009, 29:11451-11460.
143. Kurita M., Holloway T., García-Bea A., Kozlenkov A., Friedman A.K., Moreno J.L., et al. HDAC2 regulates atypical antipsychotic responses through the modulation of mGlu2 promoter activity. Nat. Neurosci. 2012, 15:1245-1254.
144. Malvaez M., Sanchis-Segura C., Vo D., Lattal K.M., Wood M.A. Modulation of chromatin modification facilitates extinction of cocaine-induced conditioned place preference. Biol. Psychiatry 2010, 67:36-43.