Valproic acid inhibits histone deacetylase activity and suppresses excitotoxicity-induced GAPDH nuclear accumulation and apoptotic death in neurons

Pharmacogenomics Journal

Volumn 4, Issue 5, 2004, Pages 336-344

  Kanai, H ^a,c   Sawa, A ^b   Chen, R W ^a   Leeds, P ^a   Chuang, D M ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

Author keywords

Cerrebellar granule cells; Excitotoxicity; GAPDH; Histone deacetylase; Neuroprotection; Valproate

Indexed keywords

4 METHYLGLUTAMIC ACID; BUTYRIC ACID; CASPASE INHIBITOR; DIZOCILPINE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; HISTONE DEACETYLASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; TRICHOSTATIN A; VALPROIC ACID;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CULTURE; CELL STRUCTURE; CELL VIABILITY; CHROMATIN; CONTROLLED STUDY; CYTOTOXICITY; DRUG MECHANISM; ENZYME ACTIVITY; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; NERVE CELL NECROSIS; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT; STATISTICAL ANALYSIS; STATISTICAL SIGNIFICANCE; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; CELL DEATH; CELL NUCLEUS; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; GLUTAMATES; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; HISTONE DEACETYLASES; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; VALPROIC ACID;

EID: 5044240976     PISSN: 1470269X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.tpj.6500269     Document Type: Article

References (42)

1. Johannessen CU. Mechanisms of action of valproate: a commentatory. Neurochem Int 2000; 37: 103-110.
2. Post RM, Speer AM, Obrocea GV, Leverich GS. Acute and prophylactic effects of anticonvulsants in bipolar depression. Clin Neurosci Res 2002; 2: 208-251.
3. Phiel CJ, Zhang F, Huang EY, Guenther MG, Lazar MA, Klein PS. Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J Biol Chem 2001; 276: 36734-36741.
4. Göttlicher M, Minucci S, Zhu P, Kramer OH, Schimpf A, Giavara S et al. Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J 2001; 20: 6969-6978.
5. Gray SG Ekstrom TJ. The human histone deacetylase family. Exp Cell Res 2001; 262: 75-83.
6. Han JW, Ahn SH, Park SH, Wang SY, Bae GU, Seo DW et al. Apicidin, a histone deacetylase inhibitor, inhibits proliferation of tumor cells via induction of p21WAF1/Cip1 and gelsolin. Cancer Res 2000; 60: 6068-6074.
7. Medina V, Edmonds B, Young GP, James R, Appleton S, Zalewski PD. Induction of caspase-3 protease activity and apoptosis by butyrate and trichostatin A (inhibitors of histone deacetylase): dependence on protein synthesis and synergy with a mitochondrial/cytochrome c-dependent pathway. Cancer Res 1997; 57: 3697-3707.
8. Kwon SH, Ahn SH, Kim YK, Bae GU, Yoon JW, Hong S et al. Apicidin, a histone deacetylase inhibitor, induces apoptosis and Fas/Fas ligand expression in human acute promyelocytic leukemia cells. J Biol Chem 2002; 277: 2073-2080.
9. Ryu H, Lee J, Olofsson BA, Mwidau A, Deodoglu A, Escudero M et al. Histone deacetylase inhibitors prevent oxidative neuronal death independent of expanded polyglutamine repeats via an Sp1-dependent pathway. Proc Natl Acad Sci USA 2003; 100: 4281-4286.
10. Kang HL, Benzer S, Min KT. Life extension in Drosophila by feeding a drug. Proc Natl Acad Sci USA 2002; 99: 838-843.
11. Loy R, Tariot PN. Neuroprotective properties of valproate - potential benefit for AD and tauopathies. J Mol Neurosci 2002; 19: 303-307.
12. Bown CD, Wang JF, Young L. Increased expression of endoplasmic reticulum stress proteins following chronic valproate treatment of rat C6 glioma cells. Neuropharmacology 2000; 39: 2162-2169.
13. Hall AC, Brennan A, Goold RG, Cleverley K, Lucas FR, Gordon-Weeks PR et al. Valproate regulates GSK-3-mediated axonal remodeling and synapsin I clustering in developing neurons. Mol Cell Neurosci 2002; 20: 257-270.
14. Vandenberg RJ, Mitrovic AD, Chebib M, Balcar VJ, Johnston GAR. Contrasting modes of action of methylglutamate derivatives on the excitatory amino acid transporters, EAAT1 and EAAT2. Mol Pharmacol 1997; 51: 809-815.
15. Donevan SD, Beg A, Gunther JM, Twyman RE. The methylglutamate, SYM 2081, is a potent and highly selective agonist at kainate receptors. J Pharmacol Exp Ther 1998; 285: 539-545.
16. Chen RW, Saunders PA, Wei H, Li Z, Seth P, Chuang D-M. Involvement of glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and p53 in neuronal apoptosis: evidence that GAPDH is upregulated by p53. J Neurosci 1999; 19: 9654-9662.
17. Wells J, Farnham PJ. Characterizing transcription factor binding sites using formaldehyde crosslinking and immunoprecipitation. Methods 2002; 26: 48-56.
18. Ishitani R, Chuang D-M. Glyceraldehyde-3-phosphate dehydrogenase antisense oligodeoxynucleotides protect against cytosine arabinonucleoside-induced apoptosis in cultured cerebellar neurons. Proc Natl Acad Sci USA 1996; 93: 9937-9941.
19. Saunders PA, Chalecka-Franaszek E, Chuang D-M. Subcellular distribution of glyceraldehyde-3-phosphate dehydrogenase in cerebellar granule cells undergoing cytosine arabinoside-induced apoptosis. J Neurochem 1997; 69: 1820-1828.
20. Sawa A, Khan AA, Hester LD, Snyder SH. Glyceraldehyde-3-phosphate dehydrogenase: nuclear translocation participates in neuronal and nonneuronal cell death. Proc Natl Acad Sci USA 1997; 94: 11669-11674.
21. Nonaka S, Hough C, Chuang D-M. Chronic lithium treatment robustly protects CNS neurons against excitotoxicity by inhibiting NMDA receptor-mediated calcium influx. Proc Natl Acad Sci USA 1998; 95: 2642-2647.
22. Berman FW, Lepage KT, Murray TF. Domoic acid neurotoxicity in cultured cerebellar granule neurons is controlled preferentially by the NMDA receptor Ca(2+) influx pathway. Brain Res 2002; 924: 20-29.
23. Ha BK, Vicini S, Rogers RC, Bresnahan JC, Buray RW, Beattie MS. Kainate-induced excitotoxicity is dependent upon extracellular potassium concentrations that regulate the activity of AMPA/KA type glutamate receptors. J Neurochem 2002; 83: 934-945.
24. Velasco I, Tapia R, Massieu L. Inhibition of glutamate uptake induces progressive accumulation of extracellular glutamate and neuronal damage in rat cortical cultures. J Neurosci Res 1998; 44: 551-561.
25. Chaudhry FA, Lehre KP, Campagne MV, Ottersen OP, Danbolt NC, Stormmathisen J. Glutamate transporters in glial plasma-membranes - highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 1995; 15: 711-720.
26. Mafra RA, Leao RM, Beirao PSL, Cruz JS. Electrophysiological evidence for glial-subtype glutamate transporter functional expression in rat cerebellar granule neurons. Braz J Med Biol Res 2003; 36: 951-957.
27. Saunders PA, Chen RW, Chuang D-M. Nuclear translocation of glyceraldehyde-3-phosphate dehydrogenase isoforms during neuronal apoptosis. J Neurochem 1999; 72: 925-932.
28. Carlile GW, Chalmers-Redman RME, Tatton NA, Pong A, Borden KE, Tatton WG. Reduced apoptosis after nerve growth factor and serum withdrawal: conversion of tetrameric glyceraldehyde-3-phosphate dehydrogenase to a dimer. Mol Pharmacol 2000; 57: 2-12.
29. Krynetski EY, Kryneskaia NF, Gallo AE, Murti KG, Evans WE. A novel protein complex distinct from mismatch repair binds thioguanylated DNA. Mol Pharmacol 2001; 59: 367-374.
30. Brown VM, Krynetski EY, Krynetskaia NF, Grieger D, Mukatira ST, Murti KG et al. A novel CRM1 -mediated nuclear export signal governs nuclear accumulation of glyceraldehyde-3-phosphate dehydrogenase following genotoxic stress. J Biol Chem 2004; 279: 5984-5992.
31. Zheng L, Roeder RG, Luo Y. S phase activation of the histone H2B promoter by OCA-S, a coactivator complex that contains GAPDH as a key component. Cell 2003; 114: 255-266.
32. Burke JR, Enghild JJ, Martin ME, Jou YS, Myers RM, Roses AD et al. Huntingtin and DRPLA proteins selectively interact with the enzyme GAPDH. Nat Med 1996; 2: 347-350.
33. Senatorov VV, Charles V, Reddy PH, Tagle DA, Chuang D-M. Overexpression and nuclear accumulation of glyceraldehyde-3-phosphate dehydrogenase in a transgenic mouse model of Huntington's disease. Mol Cell Neurosci 2003; 22: 285-297.
34. Steffan JS, Bodai L, Pallos J, Poelman M, McCampbell A, Apostol BL et al. Histone deacetylase inhibitors arrest polyglutamine-dependent neurodegeneration in Drosophila. Nature 2001; 413: 739-743.
35. Zhang CL, Mckinsey TA, Olson EN. Association of class II histone deacetylases with heterochromatin protein 1: potential role for histone methylation in control of muscle differentiation. Mol Cell Biol 2002; 22: 7302-7312.
36. Tremolizzo L, Carboni G, Ruzicka WB, Mitchell CP, Sugaya I, Tueting P et al. An epigenetic mouse model for molecular and behavioral neuropathologies related to schizophrenia vulnerability. Proc Natl Acad Sci USA 2002; 99: 17095-17100.
37. Yildirim E, Zhang Z, Uz T, Chen C-Q, Manev R, Manev H. Valproate administration to mice increases histone acetylation and 5-lipoxygenase content in the hippocampus. Neurosci Lett 2003; 345: 141-143.
38. Chen G, Zeng WZ, Yuan PX, Huang LD, Jiang YM, Zhao ZH et al. The mood-stabilizing agents lithium and valproate robustly increase the levels of the neuroprotective protein bcl-2 in the CNS. J Neurochem 1999; 72: 879-882.
39. Bown CD, Wang JF, Chen B, Young LT. Regulation of ER stress proteins by valproate: therapeutic implications. Bipolar Disord 2002; 4: 145-151.
40. Jeong MR, Hashimoto R, Senatorov VV, Fujimaki K, Ren M, Lee MS et al. Valproic acid, a mood stabilizer and anticonvulsant, protects rat cerebral cortical neurons from spontaneous cell death: a role of histone deacetylase inhibition. FEBS Lett 2003; 542: 74-78.
41. Ren M, Leng Y, Jeong MR, Leeds PR, Chuang D-M. 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 2004; 89: 1358-1367.
42. Fukumoto T, Morinobu S, Okamoto Y, Kagaya A, Yamawaki S. Chronic lithium treatment increases the expression of brain-derived neurotrophic factor in the rat brain. Psychopharmacology (Berl) 2001; 158: 100-106.