Valproic acid reduces brain damage induced by transient focal cerebral ischemia in rats: Potential roles of histone deacetylase inhibition and heat shock protein induction

Journal of Neurochemistry

Volumn 89, Issue 6, 2004, Pages 1358-1367

  Ren, Ming ^a   Leng, Yan ^a   Jeong, MiRa ^a   Leeds, Peter R ^a   Chuang, De Maw ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

Acetylated histone 3; Cerebral ischemia; Heat shock protein 70; Neuroprotection; Rat; Valproic acid

Indexed keywords

CASPASE 3; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; HISTONE DEACETYLASE; HISTONE H3; VALPROIC ACID;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN INFARCTION SIZE; BRAIN INJURY; BRAIN ISCHEMIA; CONTROLLED STUDY; CORPUS STRIATUM; ENZYME ACTIVATION; ENZYME INHIBITION; IN VITRO STUDY; MIDDLE CEREBRAL ARTERY OCCLUSION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; RAT; TRANSIENT ISCHEMIC ATTACK;

ACETYLATION; ANIMALS; BEHAVIOR, ANIMAL; CASPASE 3; CASPASES; CEREBRAL CORTEX; CEREBRAL INFARCTION; DISEASE MODELS, ANIMAL; GABA AGENTS; HEAT-SHOCK PROTEINS; HISTONE DEACETYLASES; HISTONES; HSP70 HEAT-SHOCK PROTEINS; ISCHEMIC ATTACK, TRANSIENT; MALE; NEOSTRIATUM; NEUROLOGIC EXAMINATION; NEUROPROTECTIVE AGENTS; RATS; RATS, SPRAGUE-DAWLEY; UP-REGULATION; VALPROIC ACID;

ANIMALIA;

EID: 3042651448     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02406.x     Document Type: Article

References (45)

1. Benchoua A., Guegan C., Couriaud C., Hosseini H., Sampaio N., Morin D. and Onteniente B. (2001) Specific caspase pathways are activated in the two stages of cerebral infarction. J. Neurosci. 21, 7127-7134.
2. Berger S. L. (1999) Gene activation by histone and factor acetyltransferases. Curr. Opin. Cell. Biol. 11, 336-341.
3. Bijur G. N. and Jope R. S. (2000) Opposing actions of phosphatidylinositol 3-kinase and glycogen synthase kinase-3beta in the regulation of HSF-1 activity. J. Neurochem. 75, 2401-2408.
4. Bown C. D., Wang J. F. and Young L. T. (2000) Increased expression of endoplasmic reticulum stress proteins following chronic valproate treatment of rat C6 glioma cells. Neuropharmacology 39, 2162-2169.
5. Broderick J. P. and Hacke W. (2002) Treatment of acute ischemic stroke Part II: Neuroprotection and medical management. Circulation 106, 1736-1740.
6. Calabresi P., Cupini L. M., Centonze D., Pisani F. and Bernardi G. (2003) Antiepileptic drugs as a possible neuroprotective strategy in brain ischemia. Ann. Neurol. 53, 693-702.
7. Chang K. T. and Min K. T. (2002) Regulation of lifespan by histone deacetylase. Aging Res. Rev. 1, 313-326.
8. Chen G., Zeng W. Z., Yuan P. X., Huang L. D., Jiang Y. M., Zhao Z. H. and Manji H. K. (1999) The mood-stabilizing agents lithium and valproate robustly increase the levels of the neuroprotective protein bcl-2 in the CNS. J. Neurochem. 72, 879-882.
9. Chen T., Sun H., Lu J., Zhao Y., Tao D., Li X. and Huang B. (2002) Histone acetylation is involved in hsp70 gene transcription regulation in Drosophila melanogaster. Arch. Biochem. Biophys. 408, 171-176.
10. De Sarno P., Li X. and Jope R. S. (2002) Regulation of Akt and glycogen synthase kinase-3 beta phosphorylation by sodium valproate and lithium. Neuropharmacology. 43, 1158-1164.
11. Fredduzzi S., Mariucci G., Tantucci M. and Ambrosini M. V. (2001) Generalized induction of 72-kDa heat-shock protein after transient focal ischemia in rat brain. Exp. Brain Res. 136, 19-24.
12. Fukumoto T., Morinobu S., Okamoto Y., Kagaya A. and Yamawaki S. (2001) Chronic lithium treatment increases the expression of brain-derived neurotrophic factor in the rat brain. Psychopharmacology 158, 100-106.
13. Gabai V. L., Meriin A. B., Yaglom J. A., Wei J. Y., Mosser D. D. and Sherman M. Y. (2000) Suppression of stress kinase JNK is involved in HSP72-mediated protection of myogenic cells from transient energy deprivation. Hsp72 alleviates the stress-induced inhibition of JNK dephosphorylation. J. Biol. Chem. 275, 38088-38094.
14. Giffard R. G. and Yenari M. A. (2004) Many mechanisms for hsp70 protection from cerebral ischemia. J. Neurosurg. Anesthesiol 16, 53-61.
15. Göttlicher M., Minucci S., Zhu P. et al. (2001) Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J. 20, 6969-6978.
16. Hashimoto R., Hough C., Nakazawa T., Yamamoto T. and Chuang D.-M. (2002) Lithium protection against glutamate excitotoxicity in rat cerebral cortical neurons: involvement of NMDA receptor inhibition possibly by decreasing NR2B tyrosine phosphorylation. J. Neurochem. 80, 589-597.
17. Hassel B., Iversen E. G., Gjerstad L. and Tauboll E. (2001) Up-regulation of hippocampal glutamate transport during chronic treatment with sodium valproate. J. Neurochem. 77, 1285-1292.
18. Hendrick J. P. and Hartl F. U. (1993) Molecular chaperone functions of heat-shock proteins. Annu. Rev. Biochem. 62, 349-384.
19. Heneka M. T., Gavrilyuk V., Landreth G. E., O'Banion M. K., Weinberg G. and Feinstein D. L. (2003) Noradrenergic depletion increases inflammatory responses in brain: effects on IκB and HSP70 expression. J. Neurochem. 85, 387-398.
20. Hoehn B., Ringer T. M., Xu L., Giffard R. G., Sapolsky R. M., Steinberg G. K. and Yenari M. A. (2001) Overexpression of HSP72 after induction of experimental stroke protects neurons from ischemic damage. J. Cereb. Blood Flow Metab. 21, 1303-1309.
21. Jaattela M., Wissing D., Kokholm K., Kallunki T. and Egeblad M. (1998) Hsp70 exerts its anti-apoptotic function downstream of caspase-3-like proteases. EMBO J. 17, 6124-6134.
22. Jeong M. R., Hashimoto R., Senatorov V. V., Fujimaki K., Ren M., Lee M. S. and Chuang D.-M. (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.
23. Johannessen C. U. (2000) Mechanisms of action of valproate: a commentatory. Neurochem. Int. 37, 103-110.
24. Kanai H., Sawa A. and Chuang D.-M. (2002) Possible involvement of histone deacetylase inhibition in the neuroprotective and neurotoxic effects of valproate in cultured cerebellar granule cells. 32nd Annual Meeting. Society for Neuroscience. Abstract no. 701.2.
25. Kinouchi H., Sharp F. R., Hill M. P., Koistinaho J., Sagar S. M. and Chan P. H. (1993) Induction of 70-kDa heat shock protein and hsp70 mRNA following transient focal cerebral ischemia in the rat. J. Cereb. Blood Flow Metab. 13, 105-115.
26. Leker R. R. and Neufeld M. Y. (2003) Anti-epileptic drugs as possible neuroprotectants in cerebral ischemia. Brain Res. Brain Res. Rev. 42, 187-203.
27. Li Y., Chopp M., Chen J., Wang L., Gautam S. C., Xu Y. X. and Zhang Z. (2000) Intrastriatal transplantation of bone marrow nonhematopoietic cells improves functional recovery after stroke in adult mice. J. Cereb. Blood Flow Metab. 20, 1311-1319.
28. Lin T. N., He Y. Y., Wu G., Khan M. and Hsu C. Y. (1993) Effect of brain edema on infarct volume in a focal cerebral ischemia model in rats. Stroke 24, 117-121.
29. Manabat C., Han B. H., Wendland M., Derugin N., Fox C. K., Choi J., Holtzman D. M., Ferriero D. M. and Vexler Z. S. (2003) Reperfusion differentially induces caspase-3 activation in ischemic core and penumbra after stroke in immature brain. Stroke 34, 207-213.
30. 2+ deregulation, and cytoskeletal pathology. Neurobiol. Aging 16, 187-198.
31. +. Eur. J. Biochem. 266, 886-891.
32. National Institute of Neurological Disorders and Stroke rt-PA Stroke Study Group. (1995) Tissue plasminogen activator for acute ischemic stroke. N. Engl. J. Med. 333, 1581-1587.
33. Nonaka S. and Chuang D.-M. (1998) Neuroprotective effects of chronic VPA on focal cerebral ischemia in rats. Neuroreport 229, 2081-2084.
34. Pandey P., Saleh A., Nakazawa A. et al. (2000) Negative regulation of cytochrome c-mediated oligomerization of Apaf-1 I and activation of procaspase-9 by heat shock protein 90. EMBO J. 19, 4310-4322.
35. Park H. S., Lee J. S., Huh S. H., Seo J. S. and Choi E. J. (2001) Hsp72 functions as a natural inhibitory protein of c-Jun N-terminal kinase. EMBO J. 20, 446-456.
36. Phiel C. J., Zhang F., Huang E. Y., Guenther M. G., Lazar M. A. and Klein P. S. (2001) Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J. Biol. Chem. 276, 36734-36741.
37. Post R. M., Speer A. M., Obvocea G. V. and Leverich G. S. (2002) Acute and prophylatic effects of anticonvulsants in bipolar depression. Clin. Neurosci. Res. 2, 228-251.
38. Rajdev S., Hara K., Kokubo Y., Mestril R., Dillmann W., Weinstein P. R. and Sharp F. R. (2000) Mice overexpressing rat heat shock protein 70 are protected against cerebral infarction. Ann. Neurol. 47, 782-791.
39. Ravagnan L., Gurbuxani S., Susin S. A. et al. (2001) Heat-shock protein 70 antagonizes apoptosis-inducing factor. Nat. Cell. Biol. 3, 839-843.
40. Ren M., Senatorov V. V., Chen R. W. and Chuang D.-M. (2003) Post-insult treatment with lithium reduces brain damage and facilitates neurological recovery in a rat ischemia/reperfusion model. Proc. Natl Acad. Sci. USA 100, 6210-6215.
41. Ryu H., Lee J., Olofsson B. A., Mwidau A., Deodeoglu A., Escudero M., Flemington E., Azizkhan-Clifford J., Ferrante R. J. and Ratan R. R. (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.
42. Tunnicliff G. (1999) Actions of sodium valproate on the central nervous system. J. Physiol. Pharmacol. 50, 347-365.
43. Wang J. F., Azzam J. E. and Young L. T. (2003) Valproate inhibits oxidative damage to lipid and protein in primary cultured rat cerebrocortical cells. Neuroscience 116, 485-489.
44. Xu J., Culman J., Blume A., Brecht S. and Gohlke P. (2003) Chronic treatment with a low dose of lithium protects the brain against ischemic injury by reducing apoptotic death. Stroke 34, 1287-1292.
45. Yenari M. A., Fink S. L., Sun G. H., Chang L. K., Patel M. K., Kunis D. M., Onley D., Ho D. Y., Sapolsky R. M. and Steinberg G. K. (1998) Gene therapy with Hsp72 is neuroprotective in rat models of stroke and epilepsy. Ann. Neurol. 44, 584-591.