Histone acetylation and CREB binding protein are required for neuronal resistance against ischemic injury

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Yildirim, Ferah ^a,c   Ji, Shengbo ^a   Kronenberg, Golo ^a   Barco, Angel ^b   Olivares, Roman ^b   Benito, Eva ^b   Dirnagl, Ulrich ^a   Gertz, Karen ^a   Endres, Matthias ^a   Harms, Christoph ^a   Meisel, Andreas ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b CSIC   (Spain)

^c Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; GELSOLIN; GLUCOSE; HISTONE; HISTONE ACETYLTRANSFERASE; OXYGEN; CURCUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CELL SPECIFICITY; CELL STRESS; CONTROLLED STUDY; DISEASE PREDISPOSITION; DISEASE RESISTANCE; EMBRYO; ENZYME ACTIVITY; ENZYME INHIBITION; GELSOLIN GENE; HETEROZYGOTE; HISTONE ACETYLATION; IN VITRO STUDY; IN VIVO STUDY; ISCHEMIC PRECONDITIONING; KNOCKOUT MOUSE; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MOUSE; NERVE CELL LESION; NEUROPROTECTION; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN TRANSPORT; RAT; RNA INTERFERENCE; ACETYLATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BRAIN CORTEX; CYTOLOGY; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE SILENCING; GENETIC PREDISPOSITION; GENETICS; METABOLISM; NERVE CELL; PATHOLOGY;

ACETYLATION; ANIMALS; BRAIN ISCHEMIA; CEREBRAL CORTEX; CREB-BINDING PROTEIN; CURCUMIN; DISEASE MODELS, ANIMAL; GELSOLIN; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GENETIC PREDISPOSITION TO DISEASE; HISTONES; MALE; MICE; MICE, KNOCKOUT; NEURONS; PROMOTER REGIONS, GENETIC;

EID: 84899684448     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095465     Document Type: Article

References (42)

1. Saha RN, Pahan K (2006) HATs and HDACs in neurodegeneration: a tale of disconcerted acetylation homeostasis. Cell Death Differ 13: 539-550.
2. Faraco G, Pancani T, Formentini L, Mascagni P, Fossati G, 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. (Pubitemid 44771903)
3. Kontopoulos E, Parvin JD, Feany MB (2006) Alpha-synuclein acts in the nucleus to inhibit histone acetylation and promote neurotoxicity. Hum Mol Genet 15: 3012-3023. (Pubitemid 44530705)
4. Sadri-Vakili G, Cha JH (2006) Mechanisms of disease: Histone modifications in Huntington's disease. Nat Clin Pract Neurol 2: 330-338. (Pubitemid 43811543)
5. Hockly E, Richon VM, Woodman B, Smith DL, Zhou X, 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 U S A 100: 2041-2046. (Pubitemid 36254570)
6. 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. (Pubitemid 41403313)
7. Meisel A, Harms C, Yildirim F, Bosel J, Kronenberg G, et al. (2006) Inhibition of histone deacetylation protects wild-type but not gelsolin-deficient neurons from oxygen/glucose deprivation. J Neurochem 98: 1019-1031. (Pubitemid 44127779)
8. 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. (Pubitemid 38802657)
9. Sinn DI, Kim SJ, Chu K, Jung KH, Lee ST, et al. (2007) Valproic acidmediated neuroprotection in intracerebral hemorrhage via histone deacetylase inhibition and transcriptional activation. Neurobiol Dis 26: 464-472. (Pubitemid 46578295)
10. Steffan JS, Bodai L, Pallos J, Poelman M, McCampbell A, et al. (2001) Histone deacetylase inhibitors arrest polyglutamine-dependent neurodegeneration in Drosophila. Nature 413: 739-743. (Pubitemid 33009952)
11. Yildirim F, Gertz K, Kronenberg G, Harms C, Fink KB, et al. (2008) Inhibition of histone deacetylation protects wildtype but not gelsolin-deficient mice from ischemic brain injury. Exp Neurol 210: 531-542.
12. Alarcon JM, Malleret G, Touzani K, Vronskaya S, Ishii S, et al. (2004) Chromatin acetylation, memory, and LTP are impaired in CBP+/- mice: a model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron 42: 947-959. (Pubitemid 38798233)
13. Chen G, Zou X, Watanabe H, van Deursen JM, Shen J (2010) CREB binding protein is required for both short-term and long-term memory formation. J Neurosci 30: 13066-13077.
14. Valor LM, Pulopulos MM, Jimenez-Minchan M, Olivares R, Lutz B, et al. (2011) Ablation of CBP in forebrain principal neurons causes modest memory and transcriptional defects and a dramatic reduction of histone acetylation but does not affect cell viability. J Neurosci 31: 1652-1663.
15. Petrij F, Giles RH, Dauwerse HG, Saris JJ, Hennekam RC, et al. (1995) Rubinstein-Taybi syndrome caused by mutations in the transcriptional coactivator CBP. Nature 376: 348-351.
16. Marambaud P, Wen PH, Dutt A, Shioi J, Takashima A, et al. (2003) A CBP binding transcriptional repressor produced by the PS1/epsilon-cleavage of Ncadherin is inhibited by PS1 FAD mutations. Cell 114: 635-645. (Pubitemid 37159259)
17. Nucifora FC, Jr., Sasaki M, Peters MF, Huang H, Cooper JK, et al. (2001) Interference by huntingtin and atrophin-1 with cbp-mediated transcription leading to cellular toxicity. Science 291: 2423-2428. (Pubitemid 32231807)
18. Rouaux C, Loeffler JP, Boutillier AL (2004) Targeting CREB-binding protein (CBP) loss of function as a therapeutic strategy in neurological disorders. Biochem Pharmacol 68: 1157-1164. (Pubitemid 39094281)
19. Taylor JP, Taye AA, Campbell C, Kazemi-Esfarjani P, Fischbeck KH, et al. (2003) Aberrant histone acetylation, altered transcription, and retinal degeneration in a Drosophila model of polyglutamine disease are rescued by CREB-binding protein. Genes Dev 17: 1463-1468. (Pubitemid 36734703)
20. Mergenthaler P, Dirnagl U (2011) Protective conditioning of the brain: expressway or roadblock? J Physiol 589: 4147-4155.
21. Tanaka Y, Naruse I, Maekawa T, Masuya H, Shiroishi T, et al. (1997) Abnormal skeletal patterning in embryos lacking a single Cbp allele: a partial similarity with Rubinstein-Taybi syndrome. Proc Natl Acad Sci U S A 94:10215-10220
22. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 8: e1000412.
23. Harms C, Bosel J, Lautenschlager M, Harms U, Braun JS, et al. (2004) Neuronal gelsolin prevents apoptosis by enhancing actin depolymerization. Mol Cell Neurosci 25: 69-82. (Pubitemid 38220865)
24. Datwyler AL, Lattig-Tunnemann G, Yang W, Paschen W, Lee SL, et al. (2011) SUMO2/3 conjugation is an endogenous neuroprotective mechanism. J Cereb Blood Flow Metab 31: 2152-2159.
25. Hauck L, Harms C, An J, Rohne J, Gertz K, et al. (2008) Protein kinase CK2 links extracellular growth factor signaling with the control of p27(Kip1) stability in the heart. Nat Med 14: 315-324. (Pubitemid 351347917)
26. Ruscher K, Freyer D, Karsch M, Isaev N, Megow D, et al. (2002) Erythropoietin is a paracrine mediator of ischemic tolerance in the brain: evidence from an in vitro model. J Neurosci 22: 10291-10301. (Pubitemid 35416867)
27. Endres M, Fink K, Zhu J, Stagliano NE, Bondada V, et al. (1999) Neuroprotective effects of gelsolin during murine stroke. J Clin Invest 103: 347-354. (Pubitemid 29069984)
28. Endres M, Meisel A, Biniszkiewicz D, Namura S, Prass K, et al. (2000) DNA methyltransferase contributes to delayed ischemic brain injury. J Neurosci 20: 3175-3181. (Pubitemid 30263134)
29. Huang Z, Huang PL, Panahian N, Dalkara T, Fishman MC, et al. (1994) Effects of cerebral ischemia in mice deficient in neuronal nitric oxide synthase. Science 265: 1883-1885. (Pubitemid 24324247)
30. Balasubramanyam K, Varier RA, Altaf M, Swaminathan V, Siddappa NB, et al. (2004) Curcumin, a novel p300/CREB-binding protein-specific inhibitor of acetyltransferase, represses the acetylation of histone/nonhistone proteins and histone acetyltransferase-dependent chromatin transcription. J Biol Chem 279: 51163-51171. (Pubitemid 40017859)
31. Cong SY, Pepers BA, Evert BO, Rubinsztein DC, Roos RA, et al. (2005) Mutant huntingtin represses CBP, but not p300, by binding and protein degradation. Mol Cell Neurosci 30: 12-23. (Pubitemid 41133336)
32. Jiang H, Poirier MA, Liang Y, Pei Z, Weiskittel CE, et al. (2006) Depletion of CBP is directly linked with cellular toxicity caused by mutant huntingtin. Neurobiol Dis 23: 543-551. (Pubitemid 44234090)
33. Takahashi J, Fujigasaki H, Zander C, El Hachimi KH, Stevanin G, et al. (2002) Two populations of neuronal intranuclear inclusions in SCA7 differ in size and promyelocytic leukaemia protein content. Brain 125: 1534-1543. (Pubitemid 34755168)
34. McCampbell A, Taylor JP, Taye AA, Robitschek J, Li M, et al. (2000) CREB-binding protein sequestration by expanded polyglutamine. Hum Mol Genet 9: 2197-2202.
35. Rouaux C, Jokic N, Mbebi C, Boutillier S, Loeffler JP, et al. (2003) Critical loss of CBP/p300 histone acetylase activity by caspase-6 during neurodegeneration. EMBO J 22: 6537-6549. (Pubitemid 38009601)
36. Barrett RM, Malvaez M, Kramar E, Matheos DP, Arrizon A, et al. (2011) Hippocampal focal knockout of CBP affects specific histone modifications, longterm potentiation, and long-term memory. Neuropsychopharmacology 36: 1545-1556.
37. Belayev L, Ginsberg MD, Alonso OF, Singer JT, Zhao W, et al. (1996) Bilateral ischemic tolerance of rat hippocampus induced by prior unilateral transient focal ischemia: relationship to c-fos mRNA expression. Neuroreport 8: 55-59. (Pubitemid 126785531)
38. Digicaylioglu M, Lipton SA (2001) Erythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-kappaB signalling cascades. Nature 412: 641-647. (Pubitemid 32772276)
39. Hara T, Hamada J, Yano S, Morioka M, Kai Y, et al. (2003) CREB is required for acquisition of ischemic tolerance in gerbil hippocampal CA1 region. J Neurochem 86: 805-814. (Pubitemid 36988793)
40. Stenzel-Poore MP, Stevens SL, King JS, Simon RP (2007) Preconditioning reprograms the response to ischemic injury and primes the emergence of unique endogenous neuroprotective phenotypes: a speculative synthesis. Stroke 38: 680-685. (Pubitemid 46184241)
41. Stenzel-Poore MP, Stevens SL, Xiong Z, Lessov NS, Harrington CA, et al. (2003) Effect of ischaemic preconditioning on genomic response to cerebral ischaemia: similarity to neuroprotective strategies in hibernation and hypoxiatolerant states. Lancet 362: 1028-1037. (Pubitemid 37186880)
42. Meller R, Minami M, Cameron JA, Impey S, Chen D, et al. (2005) CREB-mediated Bcl-2 protein expression after ischemic preconditioning. J Cereb Blood Flow Metab 25: 234-246. (Pubitemid 40171205)