Class IIa histone deacetylases affect neuronal remodeling and functional outcome after stroke

Neurochemistry International

Volumn 96, Issue , 2016, Pages 24-31

  Kassis, Haifa ^a,c   Shehadah, Amjad ^a,d   Li, Chao ^a   Zhang, Yi ^a   Cui, Yisheng ^a   Roberts, Cynthia ^a   Sadry, Neema ^a   Liu, Xianshuang ^a   Chopp, Michael ^a,b   Zhang, Zheng Gang ^a  

^a HENRY FORD HOSPITAL   (United States)

^b OAKLAND UNIVERSITY   (United States)

^c UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^d NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

Epigenetics; Neuronal repair; Stroke

Indexed keywords

3 [4 [3 (3 FLUOROPHENYL) 3 OXO 1 PROPENYL] 1 METHYL 1H PYRROL 2 YL]ACRYLOHYDROXAMIC ACID; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; HISTONE DEACETYLASE; HISTONE DEACETYLASE 2A; MICROTUBULE ASSOCIATED PROTEIN 2; MYELIN BASIC PROTEIN; PROTEIN C FOS; UNCLASSIFIED DRUG; VORINOSTAT; HDAC2 PROTEIN, RAT; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE INHIBITOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AXON; BRAIN CELL; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INHIBITION; HEAVY CHAIN; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; IN VIVO STUDY; LASER CAPTURE MICRODISSECTION; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; MYELINATION; NEUROFILAMENT HEAVY CHAIN; NEUROLOGIC DISEASE; NEURONAL REMODELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; QUANTITATIVE ANALYSIS; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CEREBROVASCULAR ACCIDENT; CONVALESCENCE; DRUG EFFECTS; ENZYMOLOGY; METABOLISM; NERVE CELL; NERVE CELL PLASTICITY; PATHOLOGY; PHYSIOLOGY; RANDOMIZATION; WISTAR RAT;

ANIMALS; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE INHIBITORS; MALE; NEURONAL PLASTICITY; NEURONS; RANDOM ALLOCATION; RATS; RATS, WISTAR; RECOVERY OF FUNCTION; STROKE;

EID: 84964921033     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2016.04.006     Document Type: Article

References (47)

1. T.M. Barth, M.L. Grant, and T. Schallert Effects of MK-801 on recovery from sensorimotor cortex lesions Stroke 21 1990 III153 157
2. L.I. Benowitz, and S.T. Carmichael Promoting axonal rewiring to improve outcome after stroke Neurobiol. Dis. 37 2010 259 266
3. S.T. Carmichael, L. Wei, C.M. Rovainen, and T.A. Woolsey New patterns of intracortical projections after focal cortical stroke Neurobiol. Dis. 8 2001 910 922
4. H. Chen, M. Chopp, Z.G. Zhang, and J.H. Garcia The effect of hypothermia on transient middle cerebral artery occlusion in the rat J. Cereb. Blood Flow. Metab. 12 1992 621 628
5. D.M. Chuang, Y. Leng, Z. Marinova, H.J. Kim, and C.T. Chiu Multiple roles of HDAC inhibition in neurodegenerative conditions Trends Neurosci. 32 2009 591 601
6. J. Dai, K.K. Bercury, W. Jin, and W.B. Macklin Olig1 acetylation and nuclear export mediate oligodendrocyte development J. Neurosci. 35 2015 15875 15893
7. N. Dancause, S. Barbay, S.B. Frost, E.J. Plautz, D. Chen, E.V. Zoubina, A.M. Stowe, and R.J. Nudo Extensive cortical rewiring after brain injury J. Neurosci. 25 2005 10167 10179
8. M.J. Darcy, K. Calvin, K. Cavnar, and C.C. Ouimet Regional and subcellular distribution of HDAC4 in mouse brain J. Comp. Neurol. 518 2010 722 740
9. A.J. de Ruijter, A.H. van Gennip, H.N. Caron, S. Kemp, and A.B. van Kuilenburg Histone deacetylases (HDACs): characterization of the classical HDAC family Biochem. J. 370 2003 737 749
10. G. Faraco, T. Pancani, L. Formentini, P. Mascagni, G. Fossati, F. Leoni, F. Moroni, and A. Chiarugi 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
11. G. Gardian, L. Yang, C. Cleren, N.Y. Calingasan, P. Klivenyi, and M.F. Beal Neuroprotective effects of phenylbutyrate against MPTP neurotoxicity Neuromolecular Med. 5 2004 235 241
12. J.M. Gensert, and J.E. Goldman Endogenous progenitors remyelinate demyelinated axons in the adult CNS Neuron 19 1997 197 203
13. C.L. Gibson, and S.P. Murphy Benefits of histone deacetylase inhibitors for acute brain injury: a systematic review of animal studies J. Neurochem. 115 2010 806 813
14. G.J. Hankey, K. Jamrozik, R.J. Broadhurst, S. Forbes, and C.S. Anderson Long-term disability after first-ever stroke and related prognostic factors in the perth community stroke study, 1989-1990 Stroke 33 2002 1034 1040
15. S.S. Hannila, and M.T. Filbin The role of cyclic AMP signaling in promoting axonal regeneration after spinal cord injury Exp. Neurol. 209 2008 321 332
16. K. Huber, G. Doyon, J. Plaks, E. Fyne, J.W. Mellors, and N. Sluis-Cremer Inhibitors of histone deacetylases: correlation between isoform specificity and reactivation of HIV type 1 (HIV-1) from latently infected cells J. Biol. Chem. 286 2011 22211 22218
17. H. Kassis, M. Chopp, X.S. Liu, A. Shehadah, C. Roberts, and Z.G. Zhang Histone deacetylase expression in white matter oligodendrocytes after stroke Neurochem. Int. 77 2014 17 23
18. H. Kassis, A. Shehadah, M. Chopp, C. Roberts, and Z.G. Zhang Stroke induces nuclear shuttling of histone deacetylase 4 Stroke 46 2015 1909 1915
19. M. Kilgore, C.A. Miller, D.M. Fass, K.M. Hennig, S.J. Haggarty, J.D. Sweatt, and G. Rumbaugh Inhibitors of class 1 histone deacetylases reverse contextual memory deficits in a mouse model of Alzheimer's disease Neuropsychopharmacology 35 2010 870 880
20. H.J. Kim, P. Leeds, and D.M. Chuang The HDAC inhibitor, sodium butyrate, stimulates neurogenesis in the ischemic brain J. Neurochem. 110 2009 1226 1240
21. H.J. Kim, M. Rowe, M. Ren, J.S. Hong, P.S. Chen, and D.M. Chuang Histone deacetylase inhibitors exhibit anti-inflammatory and neuroprotective effects in a rat permanent ischemic model of stroke: multiple mechanisms of action J. Pharmacol. Exp. Ther. 321 2007 892 901
22. K. Kitagawa CREB and cAMP response element-mediated gene expression in the ischemic brain FEBS J. 274 2007 3210 3217
23. T. Kristian, and B.K. Siesjo Calcium in ischemic cell death Stroke 29 1998 705 718
24. B. Langley, C. Brochier, and M.A. Rivieccio Targeting histone deacetylases as a multifaceted approach to treat the diverse outcomes of stroke Stroke 40 2009 2899 2905
25. B.E. Lauffer, R. Mintzer, R. Fong, S. Mukund, C. Tam, I. Zilberleyb, B. Flicke, A. Ritscher, G. Fedorowicz, R. Vallero, D.F. Ortwine, J. Gunzner, Z. Modrusan, L. Neumann, C.M. Koth, P.J. Lupardus, J.S. Kaminker, C.E. Heise, and P. Steiner Histone deacetylase (HDAC) inhibitor kinetic rate constants correlate with cellular histone acetylation but not transcription and cell viability J. Biol. Chem. 288 2013 26926 26943
26. Y. Li, J. Chen, X.G. Chen, L. Wang, S.C. Gautam, Y.X. Xu, M. Katakowski, L.J. Zhang, M. Lu, N. Janakiraman, and M. Chopp Human marrow stromal cell therapy for stroke in rat: neurotrophins and functional recovery Neurology 59 2002 514 523
27. X.S. Liu, M. Chopp, R.L. Zhang, A. Hozeska-Solgot, S.C. Gregg, B. Buller, M. Lu, and Z.G. Zhang Angiopoietin 2 mediates the differentiation and migration of neural progenitor cells in the subventricular zone after stroke J. Biol. Chem. 284 2009 22680 22689
28. Z. Liu, R.L. Zhang, Y. Li, Y. Cui, and M. Chopp Remodeling of the corticospinal innervation and spontaneous behavioral recovery after ischemic stroke in adult mice Stroke 40 2009 2546 2551
29. K.J. Livak, and T.D. Schmittgen Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method Methods 25 2001 402 408
30. A. Mai, S. Massa, R. Pezzi, S. Simeoni, D. Rotili, A. Nebbioso, A. Scognamiglio, L. Altucci, P. Loidl, and G. Brosch Class II (IIa)-selective histone deacetylase inhibitors. 1. Synthesis and biological evaluation of novel (aryloxopropenyl)pyrrolyl hydroxyamides J. Med. Chem. 48 2005 3344 3353
31. I. Mannaerts, N. Eysackers, O.O. Onyema, K. Van Beneden, S. Valente, A. Mai, M. Odenthal, and L.A. van Grunsven Class II HDAC inhibition hampers hepatic stellate cell activation by induction of microRNA-29 PLoS One 8 2013 e55786
32. J.I. Morgan, and T. Curran Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun Annu. Rev. Neurosci. 14 1991 421 451
33. D. Mozaffarian, E.J. Benjamin, A.S. Go, D.K. Arnett, M.J. Blaha, M. Cushman, S. de Ferranti, J.P. Despres, H.J. Fullerton, V.J. Howard, M.D. Huffman, S.E. Judd, B.M. Kissela, D.T. Lackland, J.H. Lichtman, L.D. Lisabeth, S. Liu, R.H. Mackey, D.B. Matchar, D.K. McGuire, E.R. Mohler 3rd, C.S. Moy, P. Muntner, M.E. Mussolino, K. Nasir, R.W. Neumar, G. Nichol, L. Palaniappan, D.K. Pandey, M.J. Reeves, C.J. Rodriguez, P.D. Sorlie, J. Stein, A. Towfighi, T.N. Turan, S.S. Virani, J.Z. Willey, D. Woo, R.W. Yeh, M.B. Turner American Heart Association Statistics, C., Stroke Statistics, S Heart disease and stroke statistics-2015 update: a report from the American Heart Association Circulation 131 2015 e29 322
34. S.P. Murphy, R.J. Lee, M.E. McClean, H.E. Pemberton, T. Uo, R.S. Morrison, C. Bastian, and S. Baltan MS-275, a class I histone deacetylase inhibitor, protects the p53-deficient mouse against ischemic injury J. Neurochem. 129 2014 509 515
35. A. Nebbioso, C. Dell'Aversana, A. Bugge, R. Sarno, S. Valente, D. Rotili, F. Manzo, D. Teti, S. Mandrup, P. Ciana, A. Maggi, A. Mai, H. Gronemeyer, and L. Altucci HDACs class II-selective inhibition alters nuclear receptor-dependent differentiation J. Mol. Endocrinol. 45 2010 219 228
36. A. Nebbioso, F. Manzo, M. Miceli, M. Conte, L. Manente, A. Baldi, A. De Luca, D. Rotili, S. Valente, A. Mai, A. Usiello, H. Gronemeyer, and L. Altucci Selective class II HDAC inhibitors impair myogenesis by modulating the stability and activity of HDAC-MEF2 complexes EMBO Rep. 10 2009 776 782
37. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates sixth ed. 2007 Academic Press/Elsevier Amsterdam; Boston
38. X. Qi, T. Hosoi, Y. Okuma, M. Kaneko, and Y. Nomura Sodium 4-phenylbutyrate protects against cerebral ischemic injury Mol. Pharmacol. 66 2004 899 908
39. M. Ren, Y. Leng, M. Jeong, P.R. Leeds, and D.M. Chuang 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
40. H. Ryu, K. Smith, S.I. Camelo, I. Carreras, J. Lee, A.H. Iglesias, F. Dangond, K.A. Cormier, M.E. Cudkowicz, R.H. Brown Jr., and R.J. Ferrante Sodium phenylbutyrate prolongs survival and regulates expression of anti-apoptotic genes in transgenic amyotrophic lateral sclerosis mice J. Neurochem. 93 2005 1087 1098
41. J.S. Steffan, L. Bodai, J. Pallos, M. Poelman, A. McCampbell, B.L. Apostol, A. Kazantsev, E. Schmidt, Y.Z. Zhu, M. Greenwald, R. Kurokawa, D.E. Housman, G.R. Jackson, J.L. Marsh, and L.M. Thompson Histone deacetylase inhibitors arrest polyglutamine-dependent neurodegeneration in Drosophila Nature 413 2001 739 743
42. S. Sugiura, K. Kitagawa, E. Omura-Matsuoka, T. Sasaki, S. Tanaka, Y. Yagita, K. Matsushita, D.R. Storm, and M. Hori CRE-mediated gene transcription in the peri-infarct area after focal cerebral ischemia in mice J. Neurosci. Res. 75 2004 401 407
43. R.A. Swanson, M.T. Morton, G. Tsao-Wu, R.A. Savalos, C. Davidson, and F.R. Sharp A semiautomated method for measuring brain infarct volume J. Cereb. Blood Flow. Metab. 10 1990 290 293
44. K. Tanaka, E. Nagata, S. Suzuki, T. Dembo, S. Nogawa, and Y. Fukuuchi Immunohistochemical analysis of cyclic AMP response element binding protein phosphorylation in focal cerebral ischemia in rats Brain Res. 818 1999 520 526
45. J. Zhang, Y. Li, Z.G. Zhang, M. Lu, J. Borneman, B. Buller, S. Savant-Bhonsale, S.B. Elias, and M. Chopp Bone marrow stromal cells increase oligodendrogenesis after stroke J. Cereb. Blood Flow. Metab. 29 2009 1166 1174
46. R.L. Zhang, M. Chopp, Z.G. Zhang, Q. Jiang, and J.R. Ewing A rat model of focal embolic cerebral ischemia Brain Res. 766 1997 83 92
47. Z.G. Zhang, and M. Chopp Neurorestorative therapies for stroke: underlying mechanisms and translation to the clinic Lancet Neurol. 8 2009 491 500