Valproic acid-mediated neuroprotection in intracerebral hemorrhage via histone deacetylase inhibition and transcriptional activation

Neurobiology of Disease

Volumn 26, Issue 2, 2007, Pages 464-472

  Sinn, Dong In ^a,b   Kim, Se Jeong ^a   Chu, Kon ^a,b,c   Jung, Keun Hwa ^a,b,d   Lee, Soon Tae ^a,b,c   Song, Eun Cheol ^a,b   Kim, Jeong Min ^a,b   Park, Dong Kyu ^a   Kun Lee, Sang ^a,b,c   Kim, Manho ^a,b   Roh, Jae Kyu ^a,b  

^a Stem Cell Research Center   (South Korea)

^b Seoul National University   (South Korea)

^c Seoul National University Hospital   (South Korea)

^d Korea Centers for Disease Control and Prevention   (South Korea)

Author keywords

Apoptosis; ERK; Heat shock protein; Histone deacetylase; Inflammation; Intracerebral hemorrhage; Valproic acid

Indexed keywords

CASPASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; FAS ANTIGEN; GELATINASE B; HEAT SHOCK PROTEIN 70; HISTONE DEACETYLASE; HISTONE H3; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; PHOSPHATE BUFFERED SALINE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN KINASE B; PROTEINASE; VALPROIC ACID;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BRAIN HEMATOMA; BRAIN HEMORRHAGE; CELL INFILTRATION; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; ENCEPHALITIS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION REGULATION; MALE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSLATION INITIATION;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; CELL DEATH; CEREBRAL HEMORRHAGE; CHEMOTAXIS, LEUKOCYTE; DISEASE MODELS, ANIMAL; ENCEPHALITIS; ENZYME INHIBITORS; HISTONE DEACETYLASES; MALE; NERVE DEGENERATION; NEUROPROTECTIVE AGENTS; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANS-ACTIVATION (GENETICS); TREATMENT OUTCOME; VALPROIC ACID;

EID: 34147199586     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2007.02.006     Document Type: Article

References (46)

1. Bijur G.N., and Jope R.S. Opposing actions of phosphatidylinositol 3-kinase and glycogen synthase kinase-3beta in the regulation of HSF-1 activity. J. Neurochem. 75 (2000) 2401-2408
2. Bolden J.E., Peart M.J., and Johnstone W. Anticancer activities of histone deacetylase inhibitors. Nat. Rev., Drug Discov. 5 (2006) 769-784
3. Broderick J.P., Brott T.G., Duldner J.E., Tomsick T., and Huster G. Volume of intracerebral hemorrhage: a powerful and easy-to-use predictor of 30-day mortality. Stroke 24 (1993) 987-993
4. Brott T., Broderick J., Kothari R., Barsan W., Tomsick T., Sauerbeck L., Spilker J., Duldner J., and Khoury J. Early hemorrhage growth in patients with intracerebral hemorrhage. Stroke 28 (1997) 1-5
5. Brunet A., Datta S.R., and Greenberg M.E. Transcription-dependent and independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr. Opin. Neurobiol. 11 (2001) 297-305
6. Camelo S., Iglesias A.H., Hwang D., Due B., Ryu H., Smith K., Gray S.G., Imitola J., Duran G., Assaf B., Langley B., Khoury S.J., Stephanopoulos G., De Girolami U., Ratan R.R., Ferrante R.J., and Dangond F. Transcriptional therapy with the histone deacetylase inhibitor trichostatin A ameliorates experimental autoimmune encephalomyelitis. J. Neuroimmunol. 164 (2005) 10-21
7. Choudhri T.F., Hoh B.L., Solomon R.A., Connolly Jr. E.S., and Pinsky D.J. Use of a spectrophotometric assay to objectively quantify intracerebral hemorrhage in mice. Stroke 28 (1997) 2296-2302
8. Chu K., Jeong S.W., Jung K.H., Han S.Y., Lee S.T., Kim M., and Roh J.K. Celecoxib induces functional recovery after intracerebral hemorrhage with reduction of brain edema and perihematomal cell death. J. Cereb. Blood Flow Metab. 24 (2004) 926-933
9. De Sarno P., Li X., and Jope R.S. Regulation of Akt and glycogen synthase kinase-3 beta phosphorylation by sodium valproate and lithium. Neuropharmacology 43 (2002) 1158-1164
10. Einat H., Yuan P., Gould T.D., Li J., Du J., Zhang L., Manji H.K., and Chen G. The role of the extracellular signal-regulated kinase signaling pathway in mood modulation. J. Neurosci. 23 (2003) 7311-7316
11. Faraco G., Pancani T., Formentini L., Mascagni P., Fossati G., Leoni F., Moroni F., and Chiarugi A. Pharmacological inhibition of histone deacetylases by suberoylanilide hydroxamic acid specifically alters gene expression and reduces ischemic injury in the mouse brain. Mol. Pharmacol. 70 (2006) 1876-1884
12. Fukumoto T., Morinobu S., Okamoto Y., Kagaya A., and Yamawaki S. Chronic lithium treatment increases the expression of brain-derived neutrophic factor in the rat brain. Psychopharmacology (Berlin) 158 (2001) 100-106
13. Gavrieli Y., Sherman Y., and Ben-Sasson S.A. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119 (1992) 493-501
14. Gong C., Hoff J.T., and Keep R.F. Acute inflammatory reaction following experimental intracerebral hemorrhage in rat. Brain Res. 871 (2000) 57-65
15. Gong Y., Hua Y., Keep R.F., Hoff J.T., and Xi G. Intracerebral hemorrhage: effects of aging on brain edema and neurological deficits. Stroke 35 (2004) 2571-2575
16. Hao Y., Creson T., Zhang L., Li P., Du F., Yuan P., Gould T.D., Manji H.K., and Chen G. Mood stabilizer valproate promotes ERK pathway-dependent cortical neuronal growth and neurogenesis. J. Neurosci. 24 (2004) 6590-6599
17. Hashimoto R., Hough C., Nakazawa T., Yamamoto T., and Chuang D.M. Lithium protection against glutamate excitotoxicity in rat cerebral cortical neurons: involvement of NMDA receptor inhibition possibly by decreasing NR2B tyrosine phosphorylation. J. Neurochem. 80 (2002) 589-597
18. Hassel B., Iversen E.G., Gjerstad L., and Tauboll E. Up-regulation of hippocampal glutamate transport during chronic treatment with sodium valproate. J. Neurochem. 77 (2001) 1285-1292
19. Heneka M.T., Gavrilyuk V., Landreth G.E., O'Banion M.K., Weinberg G., and Feinstein D.L. Noradrenergic depletion increases inflammatory responses in brain: effects on IκB and HSP70 expression. J. Neurochem. 85 (2003) 387-398
20. Hsieh J., and Gage FH. Chromatin remodeling in neural development and plasticity. Curr. Opin. Cell Biol. 17 (2005) 664-671
21. Hsieh J., Nakashima K., Kuwabara T., Mejia E., and Gage F.H. Histone deacetylase mediated neuronal differentiation of multipotent adult neural progenitor cells. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 16659-16664
22. Hua Y., Schallert T., Keep R.F., Wu J., Hoff J.T., and Xi G. Behavioral tests after intracerebral hemorrhage in the rat. Stroke 33 (2002) 2478-2484
23. Jeong M.R., Hashimoto R., Senatorov V.V., Fujimaki K., Ren M., Lee M.S., and Chuang D.M. 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 (2003) 74-78
24. Jung K.H., Chu K., Jeong S.W., Han S.Y., Lee S.T., Kim J.Y., Kim M., and Roh J.K. HMG-CoA reductase inhibitor, atorvastatin, promotes sensorimotor recovery, suppressing acute inflammatory reaction after experimental intracerebral hemorrhage. Stroke 35 (2004) 1744-1749
25. Lee S.R., and Lo E.H. Interactions between p38 mitogen-activated protein kinase and caspase-3 in cerebral endothelial cell death after hypoxia-reoxygenation. Stroke 34 (2003) 2704-2709
26. Lee S.T., Chu K., Jung K.H., Kim J., Kim E.H., Kim S.J., Sinn D.I., Ko S.Y., Kim M., and Roh J.K. Memantine reduces hematoma expansion in experimental intracerebral hemorrhage, resulting in functional improvement. J. Cereb. Blood Flow Metab. 26 (2006) 536-544
27. Lee S.T., Chu K., Sinn D.I., Jung K.H., Kim E.H., Kim S.J., Kim J.M., Ko S.Y., Kim M., and Roh J.K. Erythropoietin reduces perihematomal inflammation and cell death with eNOS and STAT3 activations in experimental intracerebral hemorrhage. J. Neurochem. 96 (2006) 1728-1739
28. Luo H.R., Hattori H., Hossain M.A., Hester L., Huang Y., Lee-Kwon W., Donowitz M., Nagata E., and Snyder S.H. Akt as a mediator of cell death. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 11712-11717
29. Mayer S.A., Brun N.C., Begtrup K., Broderick J., Davis S., Diringer M.N., Skolnicj B.E., and Seiner T. Recombinant activated factor VIIa for acute intracerebral hemorrhage. N. Engl. J. Med. 352 (2005) 777-785
30. Mayne M., Fortheringham J., Yan H.F., Power C., Del Bigio M.R., Peeling J., and Geiger J.D. Adenosine A2A receptor activation reduces proinflammatory events and decreases cell death following intracerebral hemorrhage. Ann. Neurol. 49 (2001) 727-735
31. Morland C., Boldingh K.A., Iversen E.G., and Hassel B. Valproate is neuroprotective against malonate toxicity in rat striatum: an association with augmentation of high-affinity glutamate uptake. J. Cereb. Blood Flow Metab. 24 (2004) 1226-1234
32. Pan T., Li X., Xie W., Jankovic J., and Le W. Valproic acid-mediated Hsp70 induction and anti-apoptotic neuroprotection in SH-SY5Y cells. FEBS Lett. 579 (2005) 6716-6720
33. Pandey P., Saleh A., Nakazawa A., Kumar S., Srinivasula S.M., Kumar V., Weichselbaum R., Nalin C., Alnemri E.S., Kufe D., and Kharbanda S. Negative regulation of cytochrome c-mediated oligomerization of Apaf-1 and activation of procaspase-9 by heat shock protein 90. EMBO J. 19 (2000) 4310-4322
34. Park H.K., Chu K., Lee S.T., Jung K.H., Kim E.H., Lee K.B., Song Y.M., Jeong S.W., Kim M., and Roh J.K. Granulocyte colony-stimulating factor induces sensorimotor recovery in intracerebral hemorrhage. Brain Res. 1041 (2005) 125-131
35. Perez M., Rojo A.I., Wandosell F., Diaz-Nido J., and Avilia J. Prion peptide induces neuronal cell death through a pathway involving glycogen synthase kinase 3. Biochem. J. 372 (2003) 129-136
36. Qureshi A.I., Ali Z., Suri M.F., Shuaib A., Baker G., Todd K., Guterman L.R., and Hopkins L.N. Extracellular glutamate and other amino acids in experimental intracerebral hemorrhage: an in vivo microdialysis study. Crit. Care Med. 31 (2003) 1482-1489
37. Reckling J.C. Neuroprotective effects of anticonvulsants in rat hippocampal slice cultures exposed to oxygen/glucose deprivation. Neurosci. Lett. 335 (2003) 167-170
38. Ren M., Leng Y., Jeong M., Leeds P.R., and 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. 89 (2004) 1358-1367
39. Richon V.M., Sandhoff T.W., Rifkind R.A., and Marks P.A. Histone deacetylase inhibitor selectively induces p21WAF1 expression and gene-associated histone acetylation. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 10014-10019
40. Rogawski M.A., and Loscher W. The neurobiology of antiepileptic drugs. Nat. Rev., Neurosci. 5 (2004) 553-564
41. Rosenberg G.A. Matrix metalloproteinases in brain injury. J. Neurotrauma. 12 (1995) 833-842
42. Rosenberg G.A., Mun-Bryce S., Wesley M., and Kornfeld M. Collagenase-induced intracerebral hemorrhage in rats. Stroke 21 (1990) 801-807
43. Schwartz M. Macrophages and microglia in central nervous system injury: are they helpful or harmful?. J. Cereb. Blood Flow Metab. 23 (2003) 385-394
44. Wu G., Xi G., and Huang F. Spontaneous intracerebral hemorrhage in humans: hematoma enlargement, clot lysis, and brain edema. Acta Neurochir., Suppl. 96 (2006) 78-80
45. Yenari M.A., Liu J., Zheng Z., Vexler Z.S., Lee J.E., and Giffard R.G. Antiapoptotic and anti-inflammatory mechanisms of heat-shock protein protection. Ann. N. Y. Acad. Sci. 1053 (2005) 74-83
46. Zhao Y., Sun H., Lu J., Li X., Chen X., Tao D., Huang W., and Huang B. Lifespan extension and elevated hsp gene expression in Drosophila caused by histone deacetylase inhibitors. J. Exp. Biol. 208 (2005) 697-705