Histone Deacetylase 5 Epigenetically Controls Behavioral Adaptations to Chronic Emotional Stimuli

Neuron

Volumn 56, Issue 3, 2007, Pages 517-529

  Renthal, William ^a   Maze, Ian ^a   Krishnan, Vaishnav ^a   Covington III, Herbert E ^a   Xiao, Guanghua ^b   Kumar, Arvind ^a   Russo, Scott J ^a   Graham, Ami ^a   Tsankova, Nadia ^a   Kippin, Tod E ^c   Kerstetter, Kerry A ^c   Neve, Rachael L ^d   Haggarty, Stephen J ^e   McKinsey, Timothy A ^f   Bassel Duby, Rhonda ^b   Olson, Eric N ^b   Nestler, Eric J ^a  

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

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

^c UNIVERSITY OF CALIFORNIA   (United States)

^d MCLEAN HOSPITAL   (United States)

^e HARVARD UNIVERSITY   (United States)

^f Myogen Inc   (United States)

Author keywords

DNA; MOLNEURO; SYSNEURO

Indexed keywords

COCAINE; HISTONE DEACETYLASE 5;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BEHAVIOR GENETICS; CHROMATIN STRUCTURE; CHRONIC STRESS; CONTROLLED STUDY; EMOTION; GENE CONTROL; GENE EXPRESSION; GENE TARGETING; GENETIC REGULATION; GENETIC TRANSCRIPTION; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN FUNCTION; STIMULUS RESPONSE;

ACETYLATION; ADAPTATION, PHYSIOLOGICAL; ANIMALS; CHROMATIN; CHRONIC DISEASE; COCAINE; COCAINE-RELATED DISORDERS; DISEASE MODELS, ANIMAL; DOPAMINE UPTAKE INHIBITORS; EMOTIONS; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HISTONE DEACETYLASES; HISTONES; MICE; MICE, INBRED C57BL; NUCLEUS ACCUMBENS; REWARD; STRESS, PSYCHOLOGICAL;

EID: 35648934049     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2007.09.032     Document Type: Article

References (57)

1. Ahmed S.H., and Koob G.F. Cocaine- but not food-seeking behavior is reinstated by stress after extinction. Psychopharmacology (Berl.) 132 (1997) 289-295
2. Almeida M., Han L., Bellido T., Manolagas S.C., and Kousteni S. Wnt proteins prevent apoptosis of both uncommitted osteoblast progenitors and differentiated osteoblasts by beta-catenin-dependent and -independent signaling cascades involving Src/ERK and phosphatidylinositol 3-kinase/AKT. J. Biol. Chem. 280 (2005) 41342-41351
3. Ang E., Chen J., Zagouras P., Magna H., Holland J., Schaeffer E., and Nestler E.J. Induction of nuclear factor-kappaB in nucleus accumbens by chronic cocaine administration. J. Neurochem. 79 (2001) 221-224
4. Bannister A.J., Zegerman P., Partridge J.F., Miska E.A., Thomas J.O., Allshire R.C., and Kouzarides T. Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain. Nature 410 (2001) 120-124
5. Barrot M., Olivier J., Perrotti L., DiLeone R., Berton O., Eisch A., Impey S., Storm D., Neve R., Yin J., et al. CREB activity in the nucleus accumbens shell controls gating of behavioral responses to emotional stimuli. Proc. Natl. Acad. Sci. USA 99 (2002) 11435-11440
6. Berton O., McClung C., Dileone R., Krishnan V., Renthal W., Russo S., Graham D., Tsankova N., Bolanos C., Rios M., et al. Essential role of BDNF in the mesolimbic dopamine pathway in social defeat stress. Science 311 (2006) 864-868
7. Bird A. Perceptions of epigenetics. Nature 447 (2007) 396-398
8. Breslow, R., Marks, P., Rifkind, R., and Jursic, B. (1993). Novel potent inducers of terminal differentiation and methods thereof. April15, WO93/07148.
9. Carlezon Jr. W.A., Thome J., Olson V.G., Lane-Ladd S.B., Brodkin E.S., Hiroi N., Duman R.S., Neve R.L., and Nestler E.J. Regulation of cocaine reward by CREB. Science 282 (1998) 2272-2275
10. Carlezon W., Duman R., and Nestler E. The many faces of CREB. Trends Neurosci. 28 (2005) 436-445
11. Chang S., McKinsey T., Zhang C., Richardson J., Hill J., and Olson E. Histone deacetylases 5 and 9 govern responsiveness of the heart to a subset of stress signals and play redundant roles in heart development. Mol. Cell. Biol. 24 (2004) 8467-8476
12. Chawla S., Vanhoutte P., Arnold F., Huang C., and Bading H. Neuronal activity-dependent nucleocytoplasmic shuttling of HDAC4 and HDAC5. J. Neurochem. 85 (2003) 151-159
13. Czubryt M., McAnally J., Fishman G., and Olson E. Regulation of peroxisome proliferator-activated receptor gamma coactivator 1 alpha (PGC-1 alpha) and mitochondrial function by MEF2 and HDAC5. Proc. Natl. Acad. Sci. USA 100 (2003) 1711-1716
14. Dong Y., Green T., Saal D., Marie H., Neve R., Nestler E.J., and Malenka R.C. CREB modulates excitability of nucleus accumbens neurons. Nat. Neurosci. 9 (2006) 475-477
15. Eisch A., Bolanos C., de Wit J., Simonak R., Pudiak C., Barrot M., Verhaagen J., and Nestler E. Brain-derived neurotrophic factor in the ventral midbrain-nucleus accumbens pathway: a role in depression. Biol. Psychiatry 54 (2003) 994-1005
16. Erb S., Shaham Y., and Stewart J. Stress reinstates cocaine-seeking behavior after prolonged extinction and a drug-free period. Psychopharmacology (Berl.) 128 (1996) 408-412
17. Finnin M.S., Donigian J.R., Cohen A., Richon V.M., Rifkind R.A., Marks P.A., Breslow R., and Pavletich N.P. Structures of a histone deacetylase homologue bound to the TSA and SAHA inhibitors. Nature 401 (1999) 188-193
18. Green T.A., Alibhai I.N., Hommel J.D., DiLeone R.J., Kumar A., Theobald D.E., Neve R.L., and Nestler E.J. Induction of ICER expression in nucleus accumbens by stress or amphetamine increases behavioral responses to emotional stimuli. J. Neurosci. 26 (2006) 8235-8242
19. Harrison B., Kim M., van Rooij E., Plato C., Papst P., Vega R., McAnally J., Richardson J., Bassel-Duby R., Olson E., and McKinsey T. Regulation of cardiac stress signaling by protein kinase d1. Mol. Cell. Biol. 26 (2006) 3875-3888
20. Hyman S., Malenka R., and Nestler E. Neural mechanisms of addiction: the role of reward-related learning and memory. Annu. Rev. Neurosci. 29 (2006) 565-598
21. Kalivas P.W., and Miller J.S. Substance P modulation of dopamine in the nucleus accumbens. Neurosci. Lett. 48 (1984) 55-59
22. Kelz M., Chen J., Carlezon W.J., Whisler K., Gilden L., Beckmann A., Steffen C., Zhang Y., Marotti L., Self D.W., et al. Expression of the transcription factor deltaFosB in the brain controls sensitivity to cocaine. Nature 401 (1999) 272-276
23. Kombian S.B., Ananthalakshmi K.V., Parvathy S.S., and Matowe W.C. Substance P depresses excitatory synaptic transmission in the nucleus accumbens through dopaminergic and purinergic mechanisms. J. Neurophysiol. 89 (2003) 728-737
24. Koob G., and Kreek M.J. Stress, dysregulation of drug reward pathways, and the transition to drug dependence. Am. J. Psychiatry 164 (2007) 1149-1159
25. Kouzarides T. Chromatin modifications and their function. Cell 128 (2007) 693-705
26. Kuiperij H.B., de Rooij J., Rehmann H., van Triest M., Wittinghofer A., Bos J.L., and Zwartkruis F.J. Characterisation of PDZ-GEFs, a family of guanine nucleotide exchange factors specific for Rap1 and Rap2. Biochim. Biophys. Acta 1593 (2003) 141-149
27. Kumar A., Choi K., Renthal W., Tsankova N., Theobald D., Truong H., Russo S., Laplant Q., Sasaki T., Whistler K.N., et al. Chromatin remodeling is a key mechanism underlying cocaine-induced plasticity in striatum. Neuron 48 (2005) 303-314
28. Kurdistani S., and Grunstein M. Histone acetylation and deacetylation in yeast. Nat. Rev. Mol. Cell Biol. 4 (2003) 276-284
29. Lachner M., O'Carroll D., Rea S., Mechtler K., and Jenuwein T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature 410 (2001) 116-120
30. Lee J.H., Cho K.S., Lee J., Kim D., Lee S.B., Yoo J., Cha G.H., and Chung J. Drosophila PDZ-GEF, a guanine nucleotide exchange factor for Rap1 GTPase, reveals a novel upstream regulatory mechanism in the mitogen-activated protein kinase signaling pathway. Mol. Cell. Biol. 22 (2002) 7658-7666
31. Levine A., Guan Z., Barco A., Xu S., Kandel E., and Schwartz J. CREB-binding protein controls response to cocaine by acetylating histones at the fosB promoter in the mouse striatum. Proc. Natl. Acad. Sci. USA 102 (2005) 19186-19191
32. Linseman D., Bartley C., Le S., Laessig T., Bouchard R., Meintzer M., Li M., and Heidenreich K. Inactivation of the myocyte enhancer factor-2 repressor histone deacetylase-5 by endogenous Ca(2+) //calmodulin-dependent kinase II promotes depolarization-mediated cerebellar granule neuron survival. J. Biol. Chem. 278 (2003) 41472-41481
33. Lu J., McKinsey T., Nicol R., and Olson E. Signal-dependent activation of the MEF2 transcription factor by dissociation from histone deacetylases. Proc. Natl. Acad. Sci. USA 97 (2000) 4070-4075
34. Lu L., Koya E., Zhai H., Hope B.T., and Shaham Y. Role of ERK in cocaine addiction. Trends Neurosci. 29 (2006) 695-703
35. Mattson B., Bossert J., Simmons D., Nozaki N., Nagarkar D., Kreuter J., and Hope B. Cocaine-induced CREB phosphorylation in nucleus accumbens of cocaine-sensitized rats is enabled by enhanced activation of extracellular signal-related kinase, but not protein kinase A. J. Neurochem. 95 (2005) 1481-1494
36. McClung C., Ulery P., Perrotti L., Zachariou V., Berton O., and Nestler E. DeltaFosB: a molecular switch for long-term adaptation in the brain. Brain Res. Mol. Brain Res. 132 (2004) 146-154
37. McKinsey T., Zhang C., Lu J., and Olson E. Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation. Nature 408 (2000) 106-111
38. McKinsey T., Zhang C., and Olson E. Activation of the myocyte enhancer factor-2 transcription factor by calcium/calmodulin-dependent protein kinase-stimulated binding of 14-3-3 to histone deacetylase 5. Proc. Natl. Acad. Sci. USA 97 (2000) 14400-14405
39. McLaughlin J.P., Li S., Valdez J., Chavkin T.A., and Chavkin C. Social defeat stress-induced behavioral responses are mediated by the endogenous kappa opioid system. Neuropsychopharmacology 31 (2006) 1241-1248
40. Mermelstein, P. (2007). Dopaminergic regulation of NFAT-dependent gene expression in striatum. In Keystone Symposium, Neurobiology of Addiction (Santa Fe, NM).
41. Murtra P., Sheasby A.M., Hunt S.P., and De Felipe C. Rewarding effects of opiates are absent in mice lacking the receptor for substance P. Nature 405 (2000) 180-183
42. Nazarian A., Russo S.J., Festa E.D., Kraish M., and Quinones-Jenab V. The role of D1 and D2 receptors in the cocaine conditioned place preference of male and female rats. Brain Res. Bull. 63 (2004) 295-299
43. Nestler E., and Carlezon W. The mesolimbic dopamine reward circuit in depression. Biol. Psychiatry 59 (2006) 1151-1159
44. Nestler E.J., Barrot M., DiLeone R.J., Eisch A.J., Gold S.J., and Monteggia L.M. Neurobiology of depression. Neuron 34 (2002) 13-25
45. Newton S.S., Thome J., Wallace T., Shirayama Y., Dow A., Schlesinger L., Duman C.H., Sakai N., Chen J.S., Neve R., et al. Inhibition of CREB or dynorphin in the nucleus accumbens produces an antidepressant-like effect. J. Neurosci. 22 (2002) 10883-10890
46. Perrotti L.I., Hadeishi Y., Ulery P.G., Barrot M., Monteggia L., Duman R.S., and Nestler E.J. Induction of deltaFosB in reward-related brain structures after chronic stress. J. Neurosci. 24 (2004) 10594-10602
47. Placenza F.M., Vaccarino F.J., Fletcher P.J., and Erb S. Activation of central neurokinin-1 receptors induces reinstatement of cocaine-seeking behavior. Neurosci. Lett. 390 (2005) 42-47
48. Pliakas A.M., Carlson R.R., Neve R.L., Konradi C., Nestler E.J., and Carlezon Jr. W.A. Altered responsiveness to cocaine and increased immobility in the forced swim test associated with elevated CREB expression in the nucleus accumbens. J. Neurosci. 21 (2001) 7397-7403
49. Pulvirenti L., Maldonado-Lopez R., and Koob G.F. NMDA receptors in the nucleus accumbens modulate intravenous cocaine but not heroin self-administration in the rat. Brain Res. 594 (1992) 327-330
50. Ruiz-Velasco V., Ikeda S.R., and Puhl H.L. Cloning, tissue distribution, and functional expression of the human G protein beta 4-subunit. Physiol. Genomics 8 (2002) 41-50
51. Russo S.J., Bolanos C., Theobald D., DeCarolis N., Renthal W., Kumar A., Winstanley C., Renthal N., Wiley M., Self D.W., et al. IRS2-Akt pathway in midbrain dopamine neurons regulates behavioral and cellular responses to opiates. Nat. Neurosci. 10 (2007) 93-99
52. Shirayama Y., Chen A.C., Nakagawa S., Russell D.S., and Duman R.S. Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. J. Neurosci. 22 (2002) 3251-3261
53. Toda S., Shen H.W., Peters J., Cagle S., and Kalivas P.W. Cocaine increases actin cycling: effects in the reinstatement model of drug seeking. J. Neurosci. 26 (2006) 1579-1587
54. Tsankova N., Berton O., Renthal W., Kumar A., Neve R., and Nestler E. Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat. Neurosci. 9 (2006) 519-525
55. Tsankova N., Renthal W., Kumar A., and Nestler E.J. Epigenetic regulation in psychiatric disorders. Nat. Rev. Neurosci. 8 (2007) 355-367
56. Vega R.B., Matsuda K., Oh J., Barbosa A.C., Yang X., Meadows E., McAnally J., Pomajzl C., Shelton J.M., Richardson J.A., et al. Histone deacetylase 4 controls chondrocyte hypertrophy during skeletogenesis. Cell 119 (2004) 555-566
57. Zhang C., McKinsey T., Chang S., Antos C., Hill J., and Olson E. Class II histone deacetylases act as signal-responsive repressors of cardiac hypertrophy. Cell 110 (2002) 479-488