HDAC4 inhibits cell-cycle progression and protects neurons from cell death

Developmental Neurobiology

Volumn 68, Issue 8, 2008, Pages 1076-1092

  Majdzadeh, Nazanin ^a   Wang, Lulu ^a   Morrison, Brad E ^a   Bassel Duby, Rhonda ^b   Olson, Eric N ^b   D'Mello, Santosh R ^a  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

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

Author keywords

Apoptosis; Cell cycle; HDAC4; Histone deacetylase; Neuronal survival

Indexed keywords

BROXURIDINE; CYCLIN DEPENDENT KINASE 1; HISTONE DEACETYLASE 4; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RAF PROTEIN; STRESS ACTIVATED PROTEIN KINASE;

ARTICLE; CANCER CELL CULTURE; CELL CULTURE; CELL CYCLE PROGRESSION; CELL NUCLEUS; CEREBELLUM; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; GRANULE CELL; HUMAN; HUMAN CELL; NERVE CELL NECROSIS; NEUROBLASTOMA CELL; NEUROPROTECTION; NUCLEAR LOCALIZATION SIGNAL; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PURKINJE CELL;

ADENOVIRIDAE; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CDC2 PROTEIN KINASE; CELL CYCLE; CELL LINE; CELL LINE, TUMOR; CEREBELLAR CORTEX; GREEN FLUORESCENT PROTEINS; HISTONE DEACETYLASES; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; NEURONS; PLASMIDS; POTASSIUM; PURKINJE CELLS; RATS; REPRESSOR PROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 46149115160     PISSN: 00223034     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.20637     Document Type: Article

References (67)

1. Aulia S, Tang BL. 2006. Cdh1-APC/C, cyclin B-Cdc2, and Alzheimer's disease pathology. Biochem Biophys Res Commun 339:1-6.
2. Bates EA, Victor M, Jones AK, Shi Y, Hart AC. 2006. Differential contributions of Caenorhabditis elegans histone deacetylases to huntingtin polyglutamine toxicity. J Neurosci 26:2830-2838.
3. Becker EB, Bonni A. 2004. Cell cycle regulation of neuronal apoptosis in development and disease. Prog Neurobiol 72:1-25.
4. Bolger TA, Yao TP. 2005. Intracellular trafficking of histone deacetylase 4 regulates neuronal cell death. J Neurosci 25:9544-9553.
5. Boutillier AL, Trinh E, Loeffler JP. 2003. Selective E2F-dependent gene transcription is controlled by histone deacetylase activity during neuronal apoptosis. J Neurochem 84:814-828.
6. Butler R, Bates GP. 2006. Histone deacetylase inhibitors as therapeutics for polyglutamine disorders. Nat Rev Neurosci 7:784-796.
7. Butts BD, Linseman DA, Le SS, Laessig TA, Heidenreich KA. 2003. Insulin-like growth factor-I suppresses degradation of the pro-survival transcription factor myocyte enhancer factor 2D (MEF2D) during neuronal apoptosis. Horm Metab Res 35:763-770.
8. Cecconi F, Alvarez-Bolado G, Meyer BI, Roth KA, Gruss P. 1998. Apaf1 (CED-4 homolog) regulates programmed cell death in mammalian development. Cell 94:727-737.
9. Chang S, Bezprozvannaya S, Li S, Olson EN. 2005. An expression screen reveals modulators of class II histone deacetylase phosphorylation. Proc Natl Acad Sci USA 102:8120-8125.
10. Chang S, McKinsey TA, Zhang CL, Richardson JA, Hill JA, Olson EN. 2004. 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 24:8467-8476.
11. Chang S, Young BD, Li S, Qi X, Richardson JA, Olson EN. 2006. Histone deacetylase 7 maintains vascular integrity by repressing matrix metalloproteinase 10. Cell 126:321-334.
12. 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.
13. Chen PS, Peng GS, Li G, Yang S, Wu X, Wang CC, Wilson B, et al. 2006. Valproate protects dopaminergic neurons in midbrain neuron/glia cultures by stimulating the release of neurotrophic factors from astrocytes. Mol Psychiatry 11:1116-1125.
14. Chin PC, Majdzadeh N, D'Mello SR. 2005. Inhibition of GSK3beta is a common event in neuroprotection by different survival factors. Brain Res Mol Brain Res 137: 193-201.
15. Copani A, Uberti D, Sortino MA, Bruno V, Nicoletti F, Memo M. 2001. Activation of cell-cycle-associated proteins in neuronal death: A mandatory or dispensable path? Trends Neurosci 24:25-31.
16. D'Mello SR, Chin PC. 2005. Treating neurodegenerative conditions through the understanding of neuronal apoptosis. Curr Drug Targets CNS Neurol Disord 4:3-23.
17. D'Mello SR, Galli C, Ciotti T, Calissano P. 1993. Induction of apoptosis in cerebellar granule neurons by low potassium: Inhibition of death by insulin-like growth factor 1 and cAMP. Proc Natl Acad Sci USA 90:10989-10993.
18. de Ruijter AJ, van Gennip AH, Caron HN, Kemp S, van Kuilenburg AB. 2003. Histone deacetylases (HDACs): Characterization of the classical HDAC family. Biochem J 370:737-749.
19. Estus S, Zaks WJ, Freeman RS, Gruda M, Bravo R, Johnson EM Jr. 1994. Altered gene expression in neurons during programmed cell death: Identification of c-jun as necessary for neuronal apoptosis. J Cell Biol 127:1717-1727.
20. Faraco G, Pancani T, Formentini L, Mascagni P, Fossati G, Leoni F, Moroni F, et al. 2006. Pharmacological inhibition of histone deacetylases by suberoylanilide hydroxamic acid specifically alters gene expression and reduces ischemic injury in the mouse brain. Mol Pharmacol 70: 1876-1884.
21. Ferrante RJ, Kubilus JK, Lee J, Ryu H, Beesen A, Zucker B, Smith K, Kowall NW, Ratan RR, Luthi-Carter R, Hersch SM. 2003. Histone deacetylase inhibition by sodium butyrate chemotherapy ameliorates the neurodegenerative phenotype in Huntington's disease mice. J Neurosci 23:9418-9427.
22. Freeman RS, Estus S, Johnson EM Jr. 1994. Analysis of cell cycle-related gene expression in postmitotic neurons: Selective induction of Cyclin D1 during programmed cell death. Neuron 12:343-355.
23. Gardian G, Browne SE, Choi DK, Klivenyi P, Gregorio J, Kubilus JK, Ryu H, et al. 2005. Neuroprotective effects of phenylbutyrate in the N171-82Q transgenic mouse model of Huntington's disease. J Biol Chem 280:556-563.
24. Gardian G, Yang L, Cleren C, Calingasan NY, Klivenyi P, Beal MF. 2004. Neuroprotective effects of phenylbutyrate against MPTP neurotoxicity. Neuromolecular Med 5:235-241.
25. Greene LA, Biswas SC, Liu DX. 2004. Cell cycle molecules and vertebrate neuron death: E2F at the hub. Cell Death Differ 11:49-60.
26. Grozinger CM, Hassig CA, Schreiber SL. 1999. Three proteins define a class of human histone deacetylases related to yeast Hdalp. Proc Natl Acad Sci USA 96:4868-4873.
27. Hakem R, Hakem A, Duncan GS, Henderson JT, Woo M, Soengas MS, Elia A, et al. 1998. Differential requirement for caspase 9 in apoptotic pathways in vivo. Cell 94:339-352.
28. Ham J, Babij C, Whitfield J, Pfarr CM, Lallemand D, Yaniv M, Rubin LL. 1995. A c-Jun dominant negative mutant protects sympathetic neurons against programmed cell death. Neuron 14:927-939.
29. Hockly E, Richon VM, Woodman B, Smith DL, Zhou X, Rosa E, Sathasivam K, et al. 2003. Suberoylanilide hydroxamic acid, a histone deacetylase inhibitor, ameliorates motor deficits in a mouse model of Huntington's disease. Proc Natl Acad Sci USA 100:2041-2046.
30. Jeong MR, Hashimoto R, Senatorov VV, Fujimaki K, Ren M, Lee MS, Chuang DM. 2003. Valproic acid, a mood stabilizer and anticonvulsant, protects rat cerebral cortical neurons from spontaneous cell death: A role of histone deacetylase inhibition. FEBS Lett 542:74-78.
31. Kanai H, Sawa A, Chen RW, Leeds P, Chuang DM. 2004. Valproic acid inhibits histone deacetylase activity and suppresses excitotoxicity-induced GAPDH nuclear accumulation and apoptotic death in neurons. Pharmacogenomics J 4:336-344.
32. Kaytor MD, Orr HT. 2002. The GSK3 beta signaling cascade and neurodegenerative disease. Curr Opin Neurobiol 12:275-278.
33. Konishi Y, Bonni A. 2003. The E2F-Cdc2 cell-cycle pathway specifically mediates activity deprivation-induced apoptosis of postmitotic neurons. J Neurosci 23:1649-1658.
34. Konishi Y, Lehtinen M, Donovan N, Bonni A. 2002. Cdc2 phosphorylation of BAD links the cell cycle to the cell death machinery. Mol Cell 9:1005-1016.
35. Koulich E, Nguyen T, Johnson K, Giardina C, D'Mello S. 2001. NF-κB is involved in the survival of cerebellar granule neurons: Association of IκBβ [correction of Iκβ] phosphorylation with cell survival. J Neurochem 76:1188-1198.
36. Krantic S, Mechawar N, Reix S, Quirion R. 2005. Molecular basis of programmed cell death involved in neurodegeneration. Trends Neurosci 28:670-676.
37. Kuida K, Haydar TF, Kuan CY, Gu Y, Taya C, Karasuyama H, Su MS, et al. 1998. Reduced apoptosis and cytochrome c-mediated caspase activation in mice-lacking caspase 9. Cell 94:325-337.
38. Kuida K, Zheng TS, Na S, Kuan C, Yang D, Karasuyama H, Rakic P, et al. 1996. Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 384:368-372.
39. Lagger G, O'Carroll D, Rembold M, Khier H, Tischler J, Weitzer G, Schuettengruber B, Hauser C, Brunmeir R, Jenuwein T, Seiser C. 2002. Essential function of histone deacetylase 1 in proliferation control and CDK inhibitor repression. Embo J 21:2672-2681.
40. Langley B, Gensert JM, Beal MF, Ratan RR. 2005. Remodeling chromatin and stress resistance in the central nervous system: Histone deacetylase inhibitors as novel and broadly effective neuroprotective agents. Curr Drug Targets CNS Neurol Disord 4:41-50.
41. 2+ //calmodulin-dependent kinase II promotes depolarization-mediated cerebellar granule neuron survival. J Biol Chem 278:41472-41481.
42. Lu J, McKinsey TA, Nicol RL, Olson EN. 2000. Signal-dependent activation of the MEF2 transcription factor by dissociation from histone deacetylases. Proc Natl Acad Sci USA 97:4070-4075.
43. McKinsey TA, Zhang CL, Olson EN. 2000. 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 97:14400-14405.
44. Mitchell BD, Gibbons B, Allen LR, Stella J, D'Mello SR. 2001. Aberrant apoptosis in the neurological mutant flathead is associated with defective cytokinesis of neural progenitor cells. Brain Res Dev Brain Res 130:53-63.
45. Montgomery RL, Davis CA, Potthoff MJ, Haberland M, Fielitz J, Qi X, Hill JA, Richardson JA, Olson EN. 2007. Histone deacetylases 1 and 2 redundantly regulate cardiac morphogenesis, growth, and contractility. Genes Dev 21:1790-1802.
46. Morrison BE, Majdzadeh N, Zhang X, Lyles A, Bassel-Duby R, Olson EN, D'Mello SR. 2006. Neuroprotection by histone deacetylase-related protein. Mol Cell Biol 26:3550-3564.
47. Okamoto S, Krainc D, Sherman K, Lipton SA. 2000. Antiapoptotic role of the p38 mitogen-activated protein kinase-myocyte enhancer factor 2 transcription factor pathway during neuronal differentiation. Proc Natl Acad Sci USA 97:7561-7566.
48. Padmanabhan J, Park DS, Greene LA, Shelanski ML. 1999. Role of cell cycle regulatory proteins in cerebellar granule neuron apoptosis. J Neurosci 19:8747-8756.
49. Petri S, Kiaei M, Kipiani K, Chen J, Calingasan NY, Crow JP, Beal MF. 2006. Additive neuroprotective effects of a histone deacetylase inhibitor and a catalytic antioxidant in a transgenic mouse model of amyotrophic lateral sclerosis. Neurobiol Dis 22:40-49.
50. Potter GB, Beaudoin GM III, DeRenzo CL, Zarach JM, Chen SH, Thompson CC. 2001. The hairless gene mutated in congenital hair loss disorders encodes a novel nuclear receptor corepressor. Genes Dev 15:2687-2701.
51. Ren M, Leng Y, Jeong M, Leeds PR, Chuang DM. 2004. Valproic acid reduces brain damage induced by transient focal cerebral ischemia in rats: Potential roles of histone deacetylase inhibition and heat shock protein induction. J Neurochem 89:1358-1367.
52. Ryu H, Lee J, Olofsson BA, Mwidau A, Dedeoglu A, Escudero M, Flemington E, et al. 2003. Histone deacetylase inhibitors prevent oxidative neuronal death independent of expanded polyglutamine repeats via an Sp1-dependent pathway. Proc Natl Acad Sci USA 100: 4281-4286.
53. Sakai K, Suzuki K, Tanaka S, Koike T. 1999. Up-regulation of cyclin D1 occurs in apoptosis of immature but not mature cerebellar granule neurons in culture. J Neurosci Res 58:396-406.
54. Salminen A, Tapiola T, Korhonen P, Suuronen T. 1998. Neuronal apoptosis induced by histone deacetylase inhibitors. Brain Res Mol Brain Res 61:203-206.
55. Schenkel J. 2004. Activation of the c-Jun transcription factor following neurodegeneration in vivo. Neurosci Lett 361:36-39.
56. Steffan JS, Bodai L, Pallos J, Poelman M, McCampbell A, Apostol BL, Kazantsev A, et al. 2001. Histone deacetylase inhibitors arrest polyglutamine-dependent neurodegeneration in Drosophila. Nature 413:739-743.
57. Trivedi CM, Luo Y, Yin Z, Zhang M, Zhu W, Wang T, Floss T, Goettlicher M, Noppinger PR, Wurst W, Ferrari VA, Abrams CS, Gruber PJ, Epstein JA. 2007. Hdac2 regulates the cardiac hypertrophic response by modulating Gsk3 beta activity. Nat Med 13:324-331.
58. 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.
59. Vega RB, Matsuda K, Oh J, Barbosa AC, Yang X, Meadows E, McAnally J, et al. 2004. Histone deacetylase 4 controls chondrocyte hypertrophy during skeletogenesis. Cell 119:555-566.
60. Verdin E, Dequiedt F, Kasler HG. 2003. Class II histone deacetylases: Versatile regulators. Trends Genet 19:286-293.
61. Wang AH, Bertos NR, Vezmar M, Pelletier N, Crosato M, Heng HH, Th'ng J, et al. 1999. HDAC4, a human histone deacetylase related to yeast HDA1, is a transcriptional corepressor. Mol Cell Biol 19:7816-7827.
62. Watson A, Eilers A, Lallemand D, Kyriakis J, Rubin LL, Ham J. 1998. Phosphorylation of c-Jun is necessary for apoptosis induced by survival signal withdrawal in cerebellar granule neurons. J Neurosci 18:751-762.
63. Yalcin A, Koulich E, Mohamed S, Liu L, D'Mello SR. 2003. Apoptosis in cerebellar granule neurons is associated with reduced interaction between CREB-binding protein and NF-κB. J Neurochem 84:397-408.
64. Yang XJ, Gregoire S. 2005. Class II histone deacetylases: From sequence to function, regulation, and clinical implication. Mol Cell Biol 25:2873-2884.
65. Yoshida H, Kong YY, Yoshida R, Elia AJ, Hakem A, Hakem R, Penninger JM, et al. 1998. Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell 94:739-750.
66. Zhang CL, McKinsey TA, Olson EN. 2001. The transcriptional corepressor MITR is a signal-responsive inhibitor of myogenesis. Proc Natl Acad Sci USA 98:7354-7359.
67. Zhao LJ, Zhang S, Chinnadurai G. 2002. Sox9 transactivation and testicular expression of a novel human gene. KIAA0800 J Cell Biochem 86:277-289.