Histone deacetylases govern cellular mechanisms underlying behavioral and synaptic plasticity in the developing and adult brain

Behavioural Pharmacology

Volumn 21, Issue 5-6, 2010, Pages 409-419

  Morris, Michael J ^a   Karra, Aroon S ^a   Monteggia, Lisa M ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

chromatin; epigenetic; histone deacetylases; learning and memory; synaptic plasticity

Indexed keywords

DNA METHYLTRANSFERASE; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE 4; HISTONE DEACETYLASE 5; HISTONE DEACETYLASE 7; HISTONE DEACETYLASE 8;

ACETYLATION; ADDICTION; ADENOSINE DIPHOSPHATE RIBOSYLATION; ADULT; AFFECT; BRAIN DEVELOPMENT; ENVIRONMENTAL FACTOR; HUMAN; LEARNING; MEMORY; METHYLATION; NERVE CELL; NERVE CELL PLASTICITY; NUCLEOSOME; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REVIEW; STIMULUS RESPONSE; SUMOYLATION; SYNAPSE; UBIQUITINATION;

ADULT; ANIMALS; BEHAVIOR; BEHAVIOR, ANIMAL; BRAIN; CENTRAL NERVOUS SYSTEM; GENE EXPRESSION REGULATION; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HUMANS; LEARNING; MEMORY; MICE; MICE, KNOCKOUT;

EID: 77955980364     PISSN: 09558810     EISSN: None     Source Type: Journal    
DOI: 10.1097/FBP.0b013e32833c20c0     Document Type: Review

References (98)

1. Adachi M, Barrot M, Autry AE, Theobald D, Monteggia LM (2008). Selective loss of brain-derived neurotrophic factor in the dentate gyrus attenuates antidepressant efficacy. Biol Psychiatry 63:642-649.
2. Akhtar MW, Raingo J, Nelson ED, Montgomery RL, Olson EN, Kavalali ET, Monteggia LM (2009). Histone deacetylases 1 and 2 form a developmental switch that controls excitatory synapse maturation and function. J Neurosci 29:8288-8297.
3. 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.
4. Albani D, Polito L, Forloni G (2009). Sirtuins as novel targets for Alzheimer's disease and other neurodegenerative disorders: experimental and genetic evidence. J Alzheimers Dis 19:11-26.
5. Allis C, Jenuwein T, Reinberg D (2007). Epigenetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
6. Bai S, Ghoshal K, Datta J, Majumder S, Yoon SO, Jacob ST (2005). DNA methyltransferase 3b regulates nerve growth factor-induced differentiation of PC12 cells by recruiting histone deacetylase 2. Mol Cell Biol 25:751-766.
7. 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.
8. Bliss TV, Collingridge GL (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361:31-39.
9. Bolger TA, Yao TP (2005). Intracellular trafficking of histone deacetylase 4 regulates neuronal cell death. J Neurosci 25:9544-9553.
10. Bramham CR, Messaoudi E (2005). BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis. Prog Neurobiol 76:99-125.
11. Brami-Cherrier K, Valjent E, Herve D, Darragh J, Corvol JC, Pages C, et al. (2005). Parsing molecular and behavioral effects of cocaine in mitogen-and stress-activated protein kinase-1-deficient mice. J Neurosci 25:11444-11454.
12. Bredy TW, Barad M (2008). The histone deacetylase inhibitor valproic acid enhances acquisition, extinction, and reconsolidation of conditioned fear. Learn Mem 15:39-45.
13. Bredy TW, Wu H, Crego C, Zellhoefer J, Sun YE, Barad M (2007). Histone modifications around individual BDNF gene promoters in prefrontal cortex are associated with extinction of conditioned fear. Learn Mem 14: 268-276.
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. Brunmeir R, Lagger S, Seiser C (2009). Histone deacetylase HDAC1/HDAC2-controlled embryonic development and cell differentiation. Int J Dev Biol 53:275-289.
16. Cai R, Kwon P, Yan-Neale Y, Sambuccetti L, Fischer D, Cohen D (2001). Mammalian histone deacetylase 1 protein is posttranslationally modified by phosphorylation. Biochem Biophys Res Commun 283:445-453.
17. Chahrour M, Zoghbi HY (2007). The story of Rett syndrome: from clinic to neurobiology. Neuron 56:422-437.
18. Chawla S, Vanhoutte P, Arnold FJ, Huang CL, Bading H (2003). Neuronal activity-dependent nucleocytoplasmic shuttling of HDAC4 and HDAC5. J Neurochem 85:151-159.
19. Chuang DM, Leng Y, Marinova Z, Kim HJ, Chiu CT (2009). Multiple roles of HDAC inhibition in neurodegenerative conditions. Trends Neurosci 32: 591-601.
20. Colon-Cesario WI, Martinez-Montemayor MM, Morales S, Felix J, Cruz J, Adorno M, et al. (2006). Knockdown of Nurr1 in the rat hippocampus: implications to spatial discrimination learning and memory. Learn Mem 13:734-744.
21. Covington HE III, Maze I, LaPlant QC, Vialou VF, Ohnishi YN, Berton O, et al. (2009). Antidepressant actions of histone deacetylase inhibitors. J Neurosci 29:11451-11460.
22. Dannenberg JH, David G, Zhong S, van der Torre J, Wong WH, Depinho RA (2005). mSin3A corepressor regulates diverse transcriptional networks governing normal and neoplastic growth and survival. Genes Dev 19: 1581-1595.
23. Dion MF, Altschuler SJ, Wu LF, Rando OJ (2005). Genomic characterization reveals a simple histone H4 acetylation code. Proc Natl Acad Sci\USA 102:5501-5506.
24. Durst KL, Hiebert SW (2004). Role of RUNX family members in transcriptional repression and gene silencing. Oncogene 23:4220-4224.
25. Duvic M, Vu J (2007). Vorinostat: a new oral histone deacetylase inhibitor approved for cutaneous T-cell lymphoma. Expert Opin Investig Drugs 16:1111-1120.
26. Espada J, Ballestar E, Fraga MF, Villar-Garea A, Juarranz A, Stockert JC, et al. (2004). Human DNA methyltransferase 1 is required for maintenance of the histone H3 modification pattern. J Biol Chem 279:37175-37184.
27. Fass DM, Butler JE, Goodman RH (2003). Deacetylase activity is required for cAMP activation of a subset of CREB target genes. J Biol Chem 278:43014-43019.
28. Feng J, Fouse S, Fan G (2007). Epigenetic regulation of neural gene expression and neuronal function. Pediatr Res 61:58R-63R.
29. Finkel T, Deng CX, Mostoslavsky R (2009). Recent progress in the biology and physiology of sirtuins. Nature 460:587-591.
30. 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.
31. Fischle W, Dequiedt F, Hendzel MJ, Guenther MG, Lazar MA, Voelter W, Verdin E (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.
32. Fuks F, Burgers WA, Brehm A, Hughes-Davies L, Kouzarides T (2000). DNA methyltransferase Dnmt1 associates with histone deacetylase activity. Nat Genet 24:88-91.
33. Fuks F, Burgers WA, Godin N, Kasai M, Kouzarides T (2001). Dnmt3a binds deacetylases and is recruited by a sequence-specific repressor to silence transcription. EMBO J 20:2536-2544.
34. Glaser KB, Staver MJ, Waring JF, Stender J, Ulrich RG, Davidsen SK (2003). Gene expression profiling of multiple histone deacetylase (HDAC) inhibitors: defining a common gene set produced by HDAC inhibition in T24 and MDA carcinoma cell lines. Mol Cancer Ther 2:151-163.
35. Glozak MA, Sengupta N, Zhang X, Seto E (2005). Acetylation and deacetylation of non-histone proteins. Gene 363:15-23.
36. Gottlieb G (1997). Synthesizing nature nurture: prenatal roots of instinctive behavior. Mahwah, NJ: Lawrence Erlbaum Associates
37. Gottlieb G (2007). Probabilistic epigenesis. Dev Sci 10:1-11.
38. Griffith JS, Mahler HR (1969). DNA ticketing theory of memory. Nature 223:580-582.
39. 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.
40. Haberland M, Montgomery RL, Olson EN (2009). The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat Rev Genet 10:32-42.
41. Haigis MC, Sinclair DA (2010). Mammalian sirtuins: biological insights and disease relevance. Annu Rev Pathol 5:253-295.
42. Hildmann C, Riester D, Schwienhorst A (2007). Histone deacetylases-an important class of cellular regulators with a variety of functions. Appl Microbiol Biotechnol 75:487-497.
43. Hobara T, Uchida S, Otsuki K, Matsubara T, Funato H, Matsuo K, et al. (2010). Altered gene expression of histone deacetylases in mood disorder patients. J Psychiatr Res 44:263-270.
44. Hubbert C, Guardiola A, Shao R, Kawaguchi Y, Ito A, Nixon A, et al. (2002). HDAC6 is a microtubule-associated deacetylase. Nature 417:455-458.
45. Jones PL, Veenstra GJ, Wade PA, Vermaak D, Kass SU, Landsberger N, et al. (1998). Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription. Nat Genet 19:187-191.
46. Kato H, Tamamizu-Kato S, Shibasaki F (2004). Histone deacetylase 7 associates with hypoxia-inducible factor 1alpha and increases transcriptional activity. J Biol Chem 279:41966-41974.
47. Keeley MB, Wood MA, Isiegas C, Stein J, Hellman K, Hannenhalli S, Abel T (2006). Differential transcriptional response to nonassociative and associative components of classical fear conditioning in the amygdala and hippocampus. Learn Mem 13:135-142.
48. Kendler KS, Karkowski LM, Prescott CA (1999). Causal relationship between stressful life events and the onset of major depression. Am J Psychiatry 156:837-841.
49. Kilgore M, Miller CA, Fass DM, Hennig KM, Haggarty SJ, Sweatt JD, Rumbaugh G (2010). Inhibitors of class 1 histone deacetylases reverse contextual memory deficits in a mouse model of Alzheimer's disease. Neuropsycho- pharmacology 35:870-880.
50. Kim SJ, Linden DJ (2007). Ubiquitous plasticity and memory storage. Neuron 56:582-592.
51. Korzus E, Rosenfeld MG, Mayford M (2004). CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 42:961-972.
52. Krishnan V, Nestler EJ (2008). The molecular neurobiology of depression. Nature 455:894-902.
53. Kristensen LS, Nielsen HM, Hansen LL (2009). Epigenetics and cancer treatment. Eur J Pharmacol 625:131-142.
54. 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.
55. Lagger G, O'Carroll D, Rembold M, Khier H, Tischler J, Weitzer G, et al. (2002). Essential function of histone deacetylase 1 in proliferation control and CDK inhibitor repression. EMBO J 21:2672-2681.
56. Lattal KM, Barrett RM, Wood MA (2007). Systemic or intrahippocampal delivery of histone deacetylase inhibitors facilitates fear extinction. Behav Neurosci 121:1125-1131.
57. Levenson JM, Sweatt JD (2006). Epigenetic mechanisms: a common theme in vertebrate and invertebrate memory formation. Cell Mol Life Sci 63:1009-1016.
58. Levenson JM, O'Riordan KJ, Brown KD, Trinh MA, Molfese DL, Sweatt JD (2004). Regulation of histone acetylation during memory formation in the hippocampus. J Biol Chem 279:40545-40559.
59. 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.
60. MacDonald JL, Roskams AJ (2008). Histone deacetylases 1 and 2 are expressed at distinct stages of neuro-glial development. Dev Dyn 237:2256-2267.
61. 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.
62. Maren S, Quirk GJ (2004). Neuronal signalling of fear memory. Nat Rev Neurosci 5:844-852.
63. Minucci S, Pelicci PG (2006). Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat Rev Cancer 6:38-51.
64. Monteggia LM, Kavalali ET (2009). Rett syndrome and the impact of MeCP2 associated transcriptional mechanisms on neurotransmission. Biol Psychiatry 65:204-210.
65. Montgomery RL, Davis CA, Potthoff MJ, Haberland M, Fielitz J, Qi X, et al. (2007). Histone deacetylases 1 and 2 redundantly regulate cardiac morphogenesis, growth, and contractility. Genes Dev 21:1790-1802.
66. Montgomery RL, Hsieh J, Barbosa AC, Richardson JA, Olson EN (2009). Histone deacetylases 1 and 2 control the progression of neural precursors to neurons during brain development. Proc Natl Acad Sci\USA 106:7876-7881.
67. Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, Bird A (1998). Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 393:386-389.
68. Ng HH, Feng Q, Wang H, Erdjument-Bromage H, Tempst P, Zhang Y, Struhl K (2002). Lysine methylation within the globular domain of histone H3 by Dot1 is important for telomeric silencing and Sir protein association. Genes Dev 16:1518-1527.
69. Nott A, Watson PM, Robinson JD, Crepaldi L, Riccio A (2008). S-Nitrosylation of histone deacetylase 2 induces chromatin remodelling in neurons. Nature 455:411-415.
70. Nusinzon I, Horvath CM (2005). Histone deacetylases as transcriptional activators? Role reversal in inducible gene regulation. Sci STKE 2005:re11.
71. Nuutinen T, Suuronen T, Kauppinen A, Salminen A (2010). Valproic acid stimulates clusterin expression in human astrocytes: implications for Alzheimer's disease. Neurosci Lett 475:64-68.
72. Pandey SC, Ugale R, Zhang H, Tang L, Prakash A (2008). Brain chromatin remodeling: a novel mechanism of alcoholism. J Neurosci 28:3729-3737.
73. Peart MJ, Smyth GK, van Laar RK, Bowtell DD, Richon VM, Marks PA, et al. (2005). Identification and functional significance of genes regulated by structurally different histone deacetylase inhibitors. Proc Natl Acad Sci\USA 102:3697-3702.
74. Pflum MK, Tong JK, Lane WS, Schreiber SL (2001). Histone deacetylase 1 phosphorylation promotes enzymatic activity and complex formation. J Biol Chem 276:47733-47741.
75. Renthal W, Maze I, Krishnan V, Covington HE III, Xiao G, Kumar A, et al. (2007). Histone deacetylase 5 epigenetically controls behavioral adaptations to chronic emotional stimuli. Neuron 56:517-529.
76. Ricobaraza A, Cuadrado-Tejedor M, Perez-Mediavilla A, Frechilla D, Del Rio J, Garcia-Osta A (2009). Phenylbutyrate ameliorates cognitive deficit and reduces tau pathology in an Alzheimer's disease mouse model. Neuropsychopharmacology 34:1721-1732.
77. Rojas P, Joodmardi E, Hong Y, Perlmann T, Ogren SO (2007). Adult mice with reduced Nurr1 expression: an animal model for schizophrenia. Mol Psychiatry 12:756-766.
78. 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.
79. Schoenherr CJ, Anderson DJ (1995). The neuron-restrictive silencer factor (NRSF): a coordinate repressor of multiple neuron-specific genes. Science 267:1360-1363.
80. Schroeder FA, Lin CL, Crusio WE, Akbarian S (2007). Antidepressant-like effects of the histone deacetylase inhibitor, sodium butyrate, in the mouse. Biol Psychiatry 62:55-64.
81. Semba J, Kuroda Y, Takahashi R (1989). Potential antidepressant properties of subchronic GABA transaminase inhibitors in the forced swimming test in mice. Neuropsychobiology 21:152-156.
82. Smillie DA, Llinas AJ, Ryan JT, Kemp GD, Sommerville J (2004). Nuclear import and activity of histone deacetylase in Xenopus oocytes is regulated by phosphorylation. J Cell Sci 117:1857-1866.
83. 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.
84. Strahl BD, Allis CD (2000). The language of covalent histone modifications. Nature 403:41-45.
85. Tsankova NM, Kumar A, Nestler EJ (2004). Histone modifications at gene promoter regions in rat hippocampus after acute and chronic electroconvulsive seizures. J Neurosci 24:5603-5610.
86. Tsankova NM, Berton O, Renthal W, Kumar A, Neve RL, Nestler EJ (2006). Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat Neurosci 9:519-525.
87. Tsankova N, Renthal W, Kumar A, Nestler EJ (2007). Epigenetic regulation in psychiatric disorders. Nat Rev Neurosci 8:355-367.
88. 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.
89. von Hertzen LS, Giese KP (2005). Memory reconsolidation engages only a subset of immediate-early genes induced during consolidation. J Neurosci 25:1935-1942.
90. Wallace DL, Vialou V, Rios L, Carle-Florence TL, Chakravarty S, Kumar A, et al. (2008). The influence of DeltaFosB in the nucleus accumbens on natural reward-related behavior. J Neurosci 28:10272-10277.
91. Wang Z, Zang C, Cui K, Schones DE, Barski A, Peng W, Zhao K (2009). Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 138:1019-1031.
92. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR, et al. (2004). Epigenetic programming by maternal behavior. Nat Neurosci 7:847-854.
93. Weaver IC, Champagne FA, Brown SE, Dymov S, Sharma S, Meaney MJ, Szyf M (2005). Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. J Neurosci 25:11045-11054.
94. Weaver IC, Meaney MJ, Szyf M (2006). Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proc Natl Acad Sci\USA 103:3480-3485.
95. Werme M, Messer C, Olson L, Gilden L, Thoren P, Nestler EJ, Brene S (2002). Delta FosB regulates wheel running. J Neurosci 22:8133-8138.
96. Wood MA, Hawk JD, Abel T (2006). Combinatorial chromatin modifications and memory storage: a code for memory? Learn Mem 13:241-244.
97. Yeh SH, Lin CH, Gean PW (2004). Acetylation of nuclear factor-kappaB in rat amygdala improves long-term but not short-term retention of fear memory. Mol Pharmacol 65:1286-1292.
98. Zhang Y, Li N, Caron C, Matthias G, Hess D, Khochbin S, Matthias P (2003). HDAC-6 interacts with and deacetylates tubulin and microtubules in vivo. EMBO J 22:1168-1179.