Histone deacetylase (Hdac) inhibitors - Emerging roles in neuronal memory, learning, synaptic plasticity and neural regeneration

Current Neuropharmacology

Volumn 14, Issue 1, 2016, Pages 55-71

  Ganai, Shabir Ahmad ^a   Ramadoss, Mahalakshmi ^a   Mahadevan, Vijayalakshmi ^a  

^a SASTRA UNIVERSITY   (India)

Author keywords

Chromatin; Histone deacetylase inhibitor; Histone deacetylases; Histones; Immune response; Ischemia; Osteogenic differentiation; Regeneration

Indexed keywords

ALANINE AMINOTRANSFERASE; AMYLOID BETA PROTEIN; ASPARTATE AMINOTRANSFERASE; COLLAGEN TYPE 1; COLLAPSIN RESPONSE MEDIATOR PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; EPIGALLOCATECHIN GALLATE; HEAT SHOCK PROTEIN 70; HEME OXYGENASE 1; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE; HISTONE DEACETYLASE 2; HISTONE DEACETYLASE 3; HISTONE DEACETYLASE 6; HISTONE DEACETYLASE INHIBITOR; HISTONE H3; HISTONE H4; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE P38; OLIGODENDROCYTE MYELIN GLYCOPROTEIN; TRICHOSTATIN A; VASCULOTROPIN; VORINOSTAT;

ACETYLATION; AMNESIA; AMYOTROPHIC LATERAL SCLEROSIS; APOPTOSIS; ARTICLE; AUTISM; CLINICAL TRIAL (TOPIC); COLONY FORMING CELL; DEACETYLATION; DNA MICROARRAY; EPIGENETICS; GENE EXPRESSION; HUMAN; HUNTINGTON CHOREA; LEARNING; MEMORY; MOTOR COORDINATION; MOTOR FUNCTION TEST; MUSCULAR DYSTROPHY; NERVE CELL PLASTICITY; NERVE DEGENERATION; NERVE REGENERATION; NONHUMAN; OXIDATIVE STRESS; SPINAL MUSCULAR ATROPHY; ANIMAL; DRUG EFFECTS; METABOLISM; NEURODEGENERATIVE DISEASES; PHYSIOLOGY;

ANIMALS; HISTONE DEACETYLASE INHIBITORS; HUMANS; LEARNING; MEMORY; NERVE REGENERATION; NEURODEGENERATIVE DISEASES; NEURONAL PLASTICITY;

EID: 84958547952     PISSN: 1570159X     EISSN: 18756190     Source Type: Journal    
DOI: 10.2174/1570159x13666151021111609     Document Type: Article

References (145)

1. [1] Barton, M.C.; Crowe, A.J. Chromatin alteration, transcription and replication: What's the opening line to the story? Oncogene, 2001, 20, 3094-9. http://dx.doi.org/10.1038/sj.onc.1204334
2. [2] Dillon, N. Gene regulation and large-scale chromatin organization in the nucleus. Chromosome Res., 2006, 14(1), 117-26. http://dx.doi.org/10.1007/s10577-006-1027-8
3. [3] Saha, A.; Wittmeyer, J.; Cairns, B.R. Chromatin remodelling: the industrial revolution of DNA around histones. Nat. Rev. Mol. Cell Biol., 2006, 7, 437-47. http://dx.doi.org/10.1038/nrm1945
4. [4] Luger, K.; Mader, A.W.; Richmond, R.K.; Sargent, D.F.; Richmond, T.J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature, 1997, 389, 251-60. http://dx.doi.org/ 10.1038/38444
5. [5] Kouzarides, T. Chromatin modifications and their function. Cell, 2007, 128, 693-705. http://dx.doi.org/10.1016/j.cell.2007.02.005
6. [6] Althaus, F.R.; Naegeli, H.; Realini, C.; Mathis, G.; Loetscher, P.; Mattenberger, M. The poly-ADPribosylation system of higher eukaryotes: a protein shuttle mechanism in chromatin? Acta Biol. Hung., 1990, 41, 9-18.
7. [7] Grunstein, M. Histone acetylation in chromatin structure and transcription. Nature, 1997, 389, 349-52. http://dx.doi.org/10.1038/ 38664
8. [8] Nowak, S.J.; Corces, V.G. Phosphorylation of histone H3: a balancing act between chromosome condensation and transcriptional activation. Trends Genet., 2004, 20(4), 214-20. http://dx.doi.org/10.1016/j.tig.2004.02.007
9. [9] Weake, V.M.; Workman, J.L. Histone ubiquitination: triggering gene activity. Mol. Cell, 2008, 29, 653-63. http://dx.doi.org/10. 1016/ j.molcel.2008.02.014
10. [10] Zhang, Y.; Reinberg, D. Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Gene Dev., 2001, 15, 2343-60. http://dx.doi. org/10.1101/gad.927301
11. [11] Jenuwein, T.; Allis, C.D. Translating the histone code. Science, 2001, 293, 1074-80. http://dx.doi.org/10.1126/science.1063127
12. [12] Strahl, B.D.; Allis, C.D. The language of covalent histone modifications. Nature, 2000, 403(6765), 41-45. http://dx.doi.org/ 10.1038/47412
13. [13] Kuo, M.H.; Allis, C.D. Roles of histone acetyltransferases and deacetylases in gene regulation. BioEssays, 1998, 20, 615-26. http://dx.doi.org/10.1002/(SICI)1521- 1878(199808)20:8<615::AID-BIES4>3.0.CO;2-H
14. [14] Butler, K.V.; Kozikowski, A.P. Chemical origins of isoform selectivity in histone deacetylase inhibitors. Curr. Pharm. Des., 2008, 14, 505-28. http://dx.doi.org/10.2174/138161208783885353
15. [15] Illi, B.; Russo, D.C.; Colussi, C.; Rosati, J.; Pallaoro, M.; Spallotta, F.; Rotili, D.; Valente, S.; Ragone, G.; Martelli, F.; Biglioli, P.; Steinkuhler, C.; Gallinari, P.; Mai, A.; Capogrossi, M.C.; Gaetano, C. Nitric Oxide modulates chromatin folding in human endothelial cells via protein phosphatase 2A activation and class II histone deacetylases nuclear shuttling. Circ. Res., 2008, 102(1), 51-8. http://dx.doi.org/10.1161/CIRCRESAHA.107.157305
16. [16] de Ruijter, A.J.; van Gennip, A.H.; Caron, H.N.; Kemp, S.; van Kuilenburg, A.B. Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem. J., 2003, 370, 737-49. http://dx.doi.org/10.1042/bj20021321
17. [17] Munshi, A.; Kurland, J.F.; Nishikawa, T.; Tanaka, T.; Hobbs, M.L.; Tucker, S.L.; Ismail, S.; Stevens, C.; Meyn, R.E. Histone deacetylase inhibitors radiosensitize human melanoma cells by suppressing DNA repair activity. Clin. Cancer Res., 2005, 11(13), 4912-22. http://dx.doi.org/10.1158/1078-0432.CCR-04-2088
18. [18] Ren, M.; Leng, Y.; Jeong, M.; Leeds, P.R.; 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(6), 1358-67. http://dx.doi.org/10.1111/j.1471-4159.2004.02406.x
19. [19] Qi, X.; Hosoi, T.; Okuma, Y.; Kaneko, M.; Nomura, Y. Sodium 4- phenylbutyrate protects against cerebral ischemic injury. Mol. Pharmacol., 2004, 66(4), 899-908. http://dx.doi.org/10.1124/ mol.104.001339
20. [20] Wu, S.Y.; Tang, S.E.; Ko, F.C.; Wu, G.C.; Huang, K.L.; Chu, S.J. VPA attenuates acute lung injury induced by ischemia-reperfusion in rats. Anesthesiology, 2015, 122(6), 1327-1337. http://dx.doi.org/ 10.1097/ALN.0000000000000618
21. [21] Zhao, T.C.; Cheng, G.; Zhang, L.X.; Tseng, Y.T.; Padbury, J.F. Inhibition of histone deacetylases triggers pharmacologic preconditioning effects against myocardial ischemic injury. Cardiovasc. Res., 2007, 76(3), 473-481. http://dx.doi.org/10.1016/ j.cardiores.2007.08.010
22. [22] Granger, A.; Abdullah, I.; Huebner, F.; Stout, A.; Wang, T.; Huebner, T.; Epstein, J.A.; Gruber, P.J. Histone deacetylase inhibition reduces myocardial ischemia-reperfusion injury in mice. FASEB J., 2008, 22, 3549-3560. http://dx.doi.org/10.1096/fj.08- 108548
23. [23] Wang, D.; Fang, C.; Zong, N.C.; Liem, D.A.; Cadeiras, M.; Scruggs, S.B.; Yu, H.; Kim, A.K.; Yang, P.; Deng, M.; Lu, H.; Ping, P. Regulation of Acetylation Restores Proteolytic Function of Diseased Myocardium in Mouse and Human. Mol. Cell Proteom., 2013, 12(12), 3793-802. http://dx.doi.org/10.1074/mcp.M113. 028332
24. [24] Xie, M.; Kong, Y.; Tan, W.; May, H.; Battiprolu, P.K.; Pedrozo, Z.; Wang, Z.V.; Morales, C.; Luo, X.; Cho, G.; Jiang, N.; Jessen, M.E.; Warner, J.J.; Lavandero, S.; Gillette, T.G.; Turer, A.T.; Hill, J.A. Histone Deacetylase Inhibition Blunts Ischemia/Reperfusion Injury by Inducing Cardiomyocyte Autophagy. Circulation, 2014, 129, 1139-1151. http://dx.doi.org/10.1161/CIRCULATIONAHA.113.002416
25. [25] Ma, X.H.; Gao, Q.; Jia, Z.; Zhang, Z.W. Neuroprotective Capabilities of TSA against Cerebral ischemia/ reperfusion injury via PI3K/ Akt signaling pathway in rats. Int. J. Neurosci., 2015, 125(2), 140-6. http://dx.doi.org/10.3109/00207454.2014.912217
26. [26] Palii, C.G.; Vulesevic, B.; Fraineau, S.; Pranckeviciene, E.; Griffith, A.J.; Chu, A.; Faralli, H.; Li, Y.; McNeill, B.; Sun, J.; Perkins, T.J.; Dilworth, F.J.; Perez-Iratxeta, C.; Suuronen, E.J.; Allan, D.S.; Brand, M. Trichostatin A Enhances Vascular Repair by Injected Human Endothelial Progenitors through Increasing the Expression of TAL1-Dependent Genes. Cell Stem Cell, 2014, 14(5), 644-657. http://dx.doi.org/10.1016/j.stem.2014.03.003
27. [27] Sun, J.; Wu, Q.; Sun, H.; Qiao, Y. Inhibition of Histone Deacetylase by Butyrate Protects Rat Liver from Ischemic Reperfusion Injury. Int. J. Mol. Sci., 2014, 15(11), 21069-21079. http://dx.doi.org/10.3390/ijms151121069
28. [28] Kim, H.J.; Chuang, D.M. HDAC inhibitors mitigate ischemiainduced oligodendrocyte damage: potential roles of oligodendrogenesis, VEGF, and anti-inflammation. Am. J. Transl. Res., 2014, 6(3), 206-23.
29. [29] Aune, S.E.; Herr, D.J.; Mani, S.K.; Menick, D.R. Selective inhibition of class I but not class IIb histone deacetylases exerts cardiac protection from ischemia reperfusion. J. Mol. Cell. Cardiol., 2014, 72, 138-45. http://dx.doi.org/10.1016/j.yjmcc. 2014.03.005
30. [30] Kaur, H.; Kumar, A.; Jaggi, A.S.; Singh, N. Pharmacologic investigations on the role of Sirt-1 in neuroprotective mechanism of postconditioning in mice. J. Surg. Res., 2015, 197(1), 191-200. http://dx.doi.org/10.1016/j.jss.2015.03.010
31. [31] Faraco, G.; Pancani, T.; Formentini, L.; Mascagni, P.; Fossati, G.; Leoni, F.; Moroni, F.; 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., 2006, 70(6), 1876-84. http://dx.doi.org/10.1124/mol.106.027912
32. [32] Yildirim, F.; Gertz, K.; Kronenberg, G.; Harms, C.; Fink, K.B.; Meisel, A.; Endres, M. Inhibition of histone deacetylation protects wildtype but not gelsolin-deficient mice from ischemic brain injury. Exp. Neurol., 2008, 210, 531-42. http://dx.doi.org/10. 1016/j.expneurol.2007.11.031
33. [33] Murphy, S.P.; Lee, R.J.; McClean, M.E.; Pemberton, H.E.; Uo, T.; Morrison, R.S.; Bastian, C.; Baltan, S. MS-275, a -class I histone deacetylase inhibitor, protects the p53-deficient mouse against ischemic injury. J. Neurochem., 2014, 129(3), 509-15. http://dx.doi. org/10.1111/jnc.12498
34. [34] Dregan, A.; Charlton, J.; Wolfe, C.D.; Gulliford, M.C.; Markus, H.S. Is Sodium Valproate, an HDAC inhibitor, associated with reduced risk of stroke and myocardial infarction? A nested casecontrol study. Pharmacoepidemiol. Drug Saf., 2014, 23(7), 759-767. http://dx.doi.org/10.1002/pds.3651
35. [35] Nural-Guvener, H.; Zakharova, L.; Feehery, L.; Sljukic, S.; Gaballa, M. Anti-fibrotic effects of class I HDAC inhibitor, mocetinostat is associated with IL-6/stat3 signaling in ischemic heart failure. Int. J. Mol. Sci., 2015, 16(5), 11482-1499. http://dx.doi.org/10.3390/ijms160511482
36. [36] Formisano, L.; Guida, N.; Valsecchi, V.; Cantile, M.; Cuomo, O.; Vinciguerra, A.; Laudati, G.; Pignataro, G.; Sirabella, R.; Di Renzo, G.; Annunziato, L. Sp3/ REST/ HDAC1/ HDAC2 Complex Represses and Sp1/ HIF-1/ p300 Complex Activates ncx1 Gene Transcription, in Brain Ischemia and in Ischemic Brain Preconditioning, by Epigenetic Mechanism. J. Neurosci., 2015, 35(19), 7332-7348. http://dx.doi.org/10.1523/JNEUROSCI.2174- 14.2015
37. [37] Hasan, M.R.; Kim, J.H.; Kim, Y.J.; Kwon, K.J.; Shin, C.Y.; Kim, H.Y.; Han, S.H.; Choi, D.H.; Lee, J. Effect of HDAC Inhibitors on Neuroprotection and Neurite Outgrowth in Primary Rat Cortical Neurons Following Ischemic Insult. Neurochem. Res., 2013, 38(9), 1921-34. http://dx.doi.org/10.1007/s11064-013-1098-9
38. [38] Broide, R.S.; Redwine, J.M.; Aftahi, N.; Young, W.; Bloom, F.E.; Winrow, C.J. Distribution of histone deacetylases 1-11 in the rat brain. J. Mol. Neurosci., 2007, 31, 47-58. http://dx.doi.org/10.1007/ BF02686117
39. [39] Guan, J.; Haggarty, S.J.; Giacometti, E.; Dannenberg, J.H.; Joseph, N.; Gao, J.; Nieland, T.J.F.; Zhou, Y.; Wang, X.; Mazitschek, R.; Bradner, J.E.; DePinho, R.A.; Jaenisch, R.; Tsai, L.H. HDAC2 negatively regulates memory formation and synaptic plasticity, Nature, 2009, 459(7243), 55-60. http://dx.doi.org/10.1038/ nature07925
40. [40] MacDonald, J.L.; Roskams, A.J. Histone deacetylases 1 and 2 are expressed at distinct stages of neuro-glial development. Dev. Dynam., 2008, 237, 2256-67. http://dx.doi.org/10.1002/dvdy.21626
41. [41] Montgomery, R.L.; Hsieh, J.; Barbosa, A.C.; Richardson, J.A.; Olson, EN. Histone deacetylases 1 and 2 control the progression of neural precursors to neurons during brain development. Proc. Natl. Acad. Sci. U.S.A., 2009, 106(19), 7876-81. http://dx.doi.org/10. 1073/pnas.0902750106
42. [42] Wood, M.A.; Hawk, J.D.; Abel, T. Combinatorial chromatin modifications and memory storage: a code for memory? Learn Mem., 2006, 13, 241-4. http://dx.doi.org/10.1101/lm.278206
43. [43] Korzus, E.; Rosenfeld, M.G.; Mayford, M. CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron, 2004, 42, 961-72. http://dx.doi.org/ 10.1016/j.neuron.2004.06.002
44. [44] Stefanko, D.P.; Barrett, R.M.; Ly, A.R.; Reolon, G.K.; Wood, M.A. Modulation of long-term memory for object recognition via HDAC inhibition. Proc. Natl. Acad. Sci. U.S.A., 2009, 106(23), 9447-52. http://dx.doi.org/10.1073/pnas.0903964106
45. [45] Haettig, J.; Stefanko, D.P.; Multani, M.L.; Figueroa, D.X.; McQuown, S.C.; Wood, M.A. HDAC inhibition modulates hippocampus-dependent long-term memory for object location in a CBP-dependent manner. Learn Memory, 2011, 18, 71-9. http://dx.doi.org/10.1101/lm.1986911
46. [46] Fass, D.M.; Reis, S.A.; Ghosh, B.; Hennig, K.M.; Joseph, N.F.; Zhao, W.N.; Nieland, T.J.; Guan, J.S.; Kuhnle, C.E.; Tang, W.; Barker, D.D.; Mazitschek, R.; Schreiber, S.L.; Tsai, L.H.; Haggarty, S.J. Crebinostat: a novel cognitive enhancer that inhibits histone deacetylase activity and modulates chromatinmediated neuroplasticity. Neuropharmacology, 2013, 64, 81-96. http://dx.doi.org/10.1016/j.neuropharm.2012.06.043
47. [47] Lopez-Atalaya, J.P.; Ito, S.; Valor, L.M.; Benito, E.; Barco, A.; Genomic targets, and histone acetylation and gene expression profiling of neural HDAC inhibition. Nuclei Acids Res., 2013, 41(17), 8072-8074. http://dx.doi.org/10.1093/nar/gkt590
48. [48] Dompierre, J.P.; Godin, J.D.; Charrin, B.C.; Cordelieres, F.P.; King, S.J.; Humbert, S.; Saudou, F. Histone deacetylase 6 inhibition compensates for the transport deficit in Huntington's disease by increasing tubulin acetylation. J. Neurosci., 2007, 27, 3571-83. http://dx.doi.org/10.1523/JNEUROSCI.0037-07.2007
49. [49] Haggarty, S.J.; Koeller, K.M.; Wong, J.C.; Grozinger, C.M.; Schreiber, S.L. Domain-selective smallmolecule inhibitor of histone deacetylase 6 (HDAC6)-mediated tubulin deacetylation. Proc. Natl. Acad. Sci. U.S.A., 2003, 100, 4389-94. http://dx.doi. org/10.1073/pnas.0430973100
50. [50] Chen, S.; Owens, G.C.; Makarenkova, H.; Edelman, D.B. HDAC6 regulates mitochondrial transport in hippocampal neurons. PloS One, 2010, 5(5), e10848. http://dx.doi.org/10.1371/journal.pone. 0010848
51. [51] Bieszczad, K.M.; Bechay, K.; Rusche, J.R.; Jacques, V.; Kudugunti, S.; Miao, W.; Weinberger, N.M.; McGaugh, J.L.; Wood, M.A. Histone Deacetylase Inhibition via RGFP966 Releases the Brakes on Sensory Cortical Plasticity and the Specificity of Memory Formation. J. Neurosci., 2015, 35(38), 13124-13132. http://dx.doi.org/10.1523/JNEUROSCI.0914-15.2015
52. [52] Roozendaal, B.; Hernandez, A.; Cabrera, S.M.; Hagewoud, R.; Malvaez, M.; Stefanko, D.P.; Haettig, J.; Wood, M.A.. Membraneassociated glucocorticoid activity is necessary for modulation of long-term memory via chromatin modification. J. Neurosci., 2010, 30(14), 5037-46. http://dx.doi.org/10.1523/JNEUROSCI.5717- 09.2010
53. [53] Covington, H.E. 3rd; Maze, I.; LaPlant, Q.C.; Vialou, V.F.; Ohnishi, Y.N.; Berton, O.; Fass, D.M.; Renthal, W.; Rush, A.J. 3rd; Wu, E.Y.; Ghose, S.; Krishnan, V.; Russo, S.J.; Tamminga, C.; Haggarty, S.J.; Nestler, E.J. Antidepressant actions of histone deacetylase inhibitors. Eur. J. Neurosci., 2009, 29, 11451-60. http://dx.doi.org/10.1523/JNEUROSCI.1758-09.2009
54. [54] Sung, Y.M.; Lee, T.; Yoon, H.; DiBattista, A.M.; Song, J.M.; Sohn, Y.; Moffat, E.I.; Turner, R.S.; Jung, M.; Kim, J.; Hoe, H.S. Mercaptoacetamidebased class II HDAC inhibitor lowers Abeta levels and improves learning and memory in a mouse model of Alzheimer's disease. Exp. Neurol., 2013, 239, 192-201. http://dx.doi.org/10.1016/j.expneurol.2012.10.005
55. [55] Kilgore, M.; Miller, C.A.; Fass, D.M.; Hennig, K.M.; Haggarty, S.J.; Sweatt, J.D.; Rumbaugh, G. Inhibitors of class 1 histone deacetylases reverse contextual memory deficits in a mouse model of alzheimer's disease. Neuropsychopharmacology, 2010, 35(4), 870-880. http://dx.doi.org/10.1038/npp.2009.197
56. [56] Dagnas, M.; Micheau, J.; Decorte, L.; Beracochea, D.; Mons, N. Post-training, intra- hippocampal HDAC inhibition differentially impacts neural circuits underlying spatial memory in adult and aged mice. Hippocampus, 2015, 25(7), 827-37. http://dx.doi.org/ 10.1002/hipo.22406
57. [57] Graff, J.; Joseph, N.F.; Horn, M.E.; Samiei, A.; Meng, J.; Seo, J.; Rei, D.; Bero, A.W.; Phan, T.X.; Wagner, F.; Holson, E.; Xu, J.; Sun, J.; Neve, R.L.; Mach, R.H.; Haggarty, S.J.; Tsai, L.H. Epigenetic priming of memory updating during reconsolidation to attenuate remote fear memories. Cell, 2014, 156, 261-76. http://dx.doi.org/10.1016/j.cell.2013.12.020
58. [58] Toropova, K.A.; Anokhin, K.V.; Tiunova, A.A. Inhibition of histone deacetylases in the chick brain modulates expression of c- Fos and ZENK transcription factors and facilitates establishment of long-term memory. Zh Vyssh. Nerv. Deiat. Im. I P Pavlova., 2014, 64(5), 551-61.
59. [59] Sewal, A.S.; Patzke, H.; Perez, E.J.; Park, P.; Lehrmann, E.; Zhang, Y.; Becker, K.G.; Fletcher, B.R.; Long, J.M.; Rapp, P.R. Experience Modulates the Effects of Histone Deacetylase Inhibitors on Gene and Protein Expression in the Hippocampus: Impaired Plasticity in Aging. J. Eurosci., 2015, 35(33), 11729-42. http://dx.doi.org/10.1523/jneurosci.4339-14.2015
60. [60] Steckert, A.V.; Comim, C.M.; Igna, D.M.; Dominguini, D.; Mendonça, B.P.; Ornell, F.; Colpo, G.D.; Gubert, C.; Kapczinski, F.; Barichello, T.; Quevedo, J.; Dal-Pizzol, F. Effects of sodium butyrate on aversive memory in rats submitted to sepsis. Neurosci. Lett., 2015, 595, 134-8. http://dx.doi.org/10.1016/j.neulet.2015. 04.019
61. [61] Chang, X.; Rong, C.; Chen, Y.; Yang, C.; Hu, Q.; Mo, Y.; Zhang, C.; Gu, X.; Zhang, L.; He, W.; Cheng, S.; Hou, X.; Su, R.; Liu, S.; Dun, W.; Wang, Q.; Fang, S. (-)- Epigallocatechin-3-gallate attenuates cognitive deterioration in Alzheimer's disease model mice by upregulating neprilysin expression. Exp. Cell Res., 2015, 334 (1), 136-145. http://dx.doi.org/10.1016/j.yexcr.2015.04.004
62. [62] Wagner, F.F.; Zhang, Y.L.; Fass, D.M.; Joseph, N.; Gale, J.P.; Weiwer, M.; McCarren, P.; Fisher, S.L.; Kaya, T.; Zhao, W.N.; Reis, S.A.; Hennig, K.M.; Thomas, M.; Lemercier, B.C.; Lewis, M.C.; Guan, J.S.; Moyer, M.P.; Scolnick, E.; Haggarty, S.J.; Tsai, L.H.; Holson, E.B. Kinetically Selective Inhibitors of Histone Deacetylase 2 (HDAC2) as Cognition Enhancers. Chem. Sci., 2015, 6(1), 804-15. http://dx.doi.org/10.1039/C4SC02130D
63. [63] Rumbaugh, G.; Sillivan, S.E.; Ozkan, E.D.; Rojas, C.S.; Hubbs, C.R.; Aceti, M.; Kilgore, M.; Kudugunti, S.; Puthanveettil, S.V.; Sweatt, J.D.; Rusche, J.; Miller, C.A. Pharmacological Selectivity within Class I Histone Deacetylases Predicts Effects on Synaptic Function and Memory Rescue. Neuropsychopharmacology, 2015, 40(10), 2307-16. http://dx.doi.org/10.1038/npp.2015.93
64. [64] Bowers, M.E.; Xia, B.; Carreiro, S.; Ressler, K.J. The Class I HDAC inhibitor RGFP963 enhances consolidation of cued fear extinction. Learn. Mem., 2015, 22, 225-231. http://dx.doi.org/ 10.1101/lm.036699.114
65. [65] Barichello, T.; Generoso, J.S.; Simões, L.R.; Faller, C.J.; Ceretta, R.A.; Petronilho, F.; Lopes-Borges, J.; Valvassori, S.S.; Quevedo, J. Sodium Butyrate Prevents Memory Impairment by Reestablishing BDNF and GDNF Expression in Experimental Pneumococcal Meningitis. Mol. Neurobiol., 2015, 52(1), 734-40. http://dx.doi.org/10.1007/s12035-014-8914-3
66. [66] Yoo, D.Y.; Kim, D.W.; Kim, M.J.; Choi, J.H.; Jung, H.Y.; Nam, S.M.; Kim, J.W.; Yoon, Y.S.; Choi, S.Y.; Hwang, I.K. Sodium butyrate, a histone deacetylase Inhibitor, ameliorates SIRT2- induced memory impairment, reduction of cell proliferation, and neuroblast differentiation in the dentate gyrus. Neurol. Res., 2014, 37(1), 69-76. http://dx.doi.org/10.1179/1743132814Y.0000000416
67. [67] Castellano, J.F.; Fletcher, B.R.; Patzke, H.; Long, J.M.; Sewal, A.; Kim, D.H.; Kelley-Bell, B.; Rapp, P.R. Reassessing the effects of histone deacetylase inhibitors on hippocampal memory and cognitive aging. Hippocampus, 2014, 24(8), 1006-16. http://dx. doi.org/10.1002/hipo.22286
68. [68] Selenica, M.L.; Benner, L.; Housley, S.B.; Manchec, B.; Lee, D.C.; Nash, K.R.; Kalin, J.; Bergman, J.A.; Kozikowski, A.; Gordon, M.N.; Morgan, D. Histone deacetylase 6 inhibition improves memory and reduces total tau levels in a mouse model of tau deposition. Alzheimers Res. Ther., 2014, 6(1), 12. http://dx.doi.org/ 10.1186/alzrt241
69. [69] Morris, M.J.; Mahgoub, M.; Na, E.S.; Pranav, H.; Monteggia, L.M. Loss of histone deacetylase 2 improves working memory and accelerates extinction learning. J. Neurosci., 2013, 33(15), 6401-6411. http://dx.doi.org/10.1523/JNEUROSCI.1001-12.2013
70. [70] Bouton, M.E.; Westbrook, R.F.; Corcoran, K.A.; Maren, S. Contextual and Temporal Modulation of Extinction: Behavioral and Biological Mechanisms. Biol. Psychiatry, 2006, 60, 352-60. http://dx.doi.org/10.1016/j.biopsych.2005.12.015
71. [72] Lattal, K.M.; Bernardi, R.E. Cellular learning theory: theoretical comment on Cole and McNally. Behav. Neurosci., 2007, 121(5), 1140-3. http://dx.doi.org/10.1037/0735-7044.121.5.1140
72. [73] Wang, Y.; Lai, J.; Cui, H.; Zhu, Y.; Zhao, B.; Wang, W.; Wei, S. Inhibition of Histone Deacetylase in the Basolateral Amygdala Facilitates Morphine Context-Associated Memory Formation in Rats. J. Mol. Neurosci., 2014, 55(1), 269-78. http://dx.doi.org/ 10.1007/s12031-014-0317-4
73. [74] Blank, M.; Dornelles, A.S.; Werenicz, A.; Velho, L.A.; Pinto, D.F.; Fedi, A.C.; Schröder, N.; Roesler, R. Basolateral amygdala activity is required for enhancement of memory consolidation produced by histone deacetylase inhibition in the hippocampus. Neurobiol. Learn. Mem., 2014, 111, 1-8. http://dx.doi.org/10.1016/j.nlm.2014. 02.009
74. [75] Itzhak, Y.; Liddie, S.; Anderson, K.L. Sodium butyrateinduced histone acetylation strengthens the expression of cocaineassociated contextual memory. Neurobiol. Learn. Mem., 2013, 102, 34-42. http://dx.doi.org/10.1016/j.nlm.2013.03.007
75. [76] Zhong, T.; Qing, Q.J.; Yang, Y.; Zou, W.Y.; Ye, Z.; Yan, J.Q.; Guo, Q.L. Repression of contexual fear memory induced by isoflurane is accompanied by reduction in histone acetylation and rescued by sodium butyrate. Br. J. Anaesth., 2014, 113(4), 634-43. http://dx.doi.org/10.1093/bja/aeu184
76. [77] Malvaez, M.; McQuown, S.C.; Rogge, G.A.; Astarabadi, M.; Jacques, V.; Carreiro, S.; Rusche, J.R.; Wood, M.A. HDAC3- selective inhibitor enhances extinction of cocaine-seeking behavior in a persistent manner. Proc. Natl. Acad. Sci. U.S.A., 2013, 110(7), 2647-52. http://dx.doi.org/10.1073/pnas.1213364110
77. [78] Whittle, N.; Schmuckermair, C.; Cinar, G.O.; Hauschild, M.; Ferraguti, F.; Holmes, A.; Singewald, N. Deep brain stimulation, histone deacetylase inhibitors and glutamatergic drugs rescue resistance to fear extinction in a genetic mouse model. Neuropharmacology, 2013, 64, 414-23. http://dx.doi.org/10.1016/ j.neuropharm.2012.06.001
78. [79] Fujita, Y.; Morinobu, S.; Takei, S.; Fuchikami, M.; Matsumoto, T.; Yamamoto, S.; Yamawaki, S. Vorinostat, a histone deacetylase inhibitor, facilitates fear extinction and enhances expression of the hippocampal NR2B-containing NMDA receptor gene. J. Psychiatr. Res., 2012, 46(5), 635-43. http://dx.doi.org/10.1016/j.jpsychires. 2012.01.026
79. [80] Yu, C.W.; Chang, P.T.; Hsin, L.W.; Chern, J.W. Quinazolin-4-one derivatives as selective histone deacetylase-6 inhibitors for the treatment of Alzheimer's disease. J. Med. Chem., 2013, 56(17), 6775-91. http://dx.doi.org/10.1021/jm400564j
80. [81] Ferrante, R.J.; Kubilus, J.K.; Lee, J.; Ryu, H.; Beesen, A.; Zucker, B.; Smith, K.; Kowall, N.W.; Ratan, R.R.; Luthi-Carter, R.; Hersch, S.M. Histone deacetylase inhibition by NaB chemotherapy ameliorates the neurodegenerative phenotype in Huntington's disease mice. J. Neurosci., 2003, 23(28), 9418-27.
81. [82] Gardian, G.; Browne, S.E.; Choi, D.K.; Klivenyi, P.; Gregorio, J.; Kubilus, J.K.; Ryu, H.; Langley, B.; Ratan, R.R.; Ferrante, R.J.; Beal, M.F. Neuroprotective effects of phenylbutyrate in the N171-82Q transgenic mouse model of Huntington's disease. J. Biol. Chem., 2005, 280(1), 556-63. http://dx.doi.org/10.1074/jbc. M410210200
82. [83] Hockly, E.; Richon, V.M.; Woodman, B.; Smith, D.L.; Zhou, X.; Rosa, E.; Sathasivam, K.; Ghazi-Noori, S.; Mahal, A.; Lowden, P.A.; Steffan, J.S.; Marsh, J.L.; Thompson, L.M.; Lewis, C.M.; Marks, P.A.; Bates, G.P. 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., 2003, 100(4), 2041-6. http://dx.doi.org/10.1073/pnas. 0437870100
83. [84] Chang, J.G.; Hsieh-Li, H.M.; Jong, Y.J.; Wang, N.M.; Tsai, C.H.; Li, H. Treatment of spinal muscular atrophy by NaB. Proc. Natl. Acad. Sci., 2001, 98, 9808-13. http://dx.doi.org/10.1073/pnas. 171105098
84. [85] Corcoran, J.P.; So, P.L.; Maden, M. Disruption of the retinoid signaling pathway causes a deposition of amyloid beta in the adult rat brain. Eur. J. Neurosci., 2004, 20, 896-902. http://dx.doi.org/10. 1111/j.1460-9568.2004.03563.x
85. [86] Petri, S.; Kiaei, M.; Kipiani, K.; Chen, J.; Calingasan, N.Y.; Crow, J.P.; Beal, M.F. Additive neuroprotective effects of a histone deacetylase inhibitor and a catalytic antioxidant in a transgenic mouse model of amyotrophic lateral sclerosis. Neurobiol. Dis., 2006, 22(1), 40-9. http://dx.doi.org/10.1016/j.nbd.2005.09.013
86. [87] Ryu, H.; Lee, J.; Olofsson, B.A.; Mwidau, A.; Dedeoglu, A.; Escudero, M.; Flemington, E.; Azizkhan-Clifford, J.; Ferrante, R.J.; Ratan, R.R. Histone deacetylase inhibitors prevent oxidative neuronal death independent of expanded polyglutamine repeats via an Sp1-dependent pathway. Proc. Natl. Acad. Sci. U.S.A., 2003, 100(7), 4281-6. http://dx.doi.org/10.1073/pnas.0737363100
87. [88] Sussmuth, S.D.; Haider, S.; Landwehrmeyer, G.B.; Farmer, R.; Frost, C.; Tripepi, G.; Andersen, C.A.; Di Bacco, M.; Lamanna, C.; Diodato, E.; Massai, L.; Diamanti, D.; Mori, E.; Magnoni, L.; Dreyhaupt, J.; Schiefele, K.; Craufurd, D.; Saft, C.; Rudzinska, M.; Ryglewicz, D.; Orth, M.; Brzozy, S.; Baran, A.; Pollio, G.; Andre, R.; Tabrizi, S.J.; Darpo, B.; Westerberg, G.; PADDINGTON Consortium. An exploratory double blind, randomised clinical trial with selisistat,a SirT1 inhibitor, in patients with Huntington’s disease. Br. J. Clin. Pharmacol., 2015, 79(3), 465-76. http://dx.doi. org/10.1111/bcp.12512
88. [89] Mercuri, E.; Bertini, E.; Messina, S.; Solari, A.; D’Amico, A.; Angelozzi, C.; Battini, R.; Berardinelli, A.; Boffi, P.; Bruno, C.; Cini, C.; Colitto, F.; Kinali, M.; Minetti, C.; Mongini, T.; Morandi, L.; Neri, G.; Orcesi, S.; Pane, M.; Pelliccioni, M.; Pini, A.; Tiziano, F.D.; Villanova, M.; Vita, G.; Brahe C. Randomized, double-blind, placebo-controlled trial of phenylbutyrate in spinalmuscular atrophy. Neurology, 2007, 68(1), 51-5. http://dx.doi.org/10.1212/ 01.wnl.0000249142.82285.d6
89. [90] Hogarth, P.; Lovrecic, L.; Krainc, D. Sodium phenylbutyrate in Huntington’s disease: a dose-finding study. Mov. Disord., 2007, 22(13), 1962-4. http://dx.doi.org/10.1002/mds.21632
90. [91] Cudkowicz, M.E.; Andres, P.L.; Macdonald, S.A.; Bedlack, R.S.; Choudry, R.; Brown, R.H. Jr.; Zhang, H.; Schoenfeld, D.A.; Shefner, J.; Matson, S.; Matson, W.R.; Ferrante, R.J.; Northeast ALS and National VA ALS Research Consortiums. Phase 2 study of sodium phenylbutyrate in ALS. Amyotroph. Lateral Scler., 2009, 10(2), 99-106. http://dx.doi.org/10.1080/ 17482960802320487
91. [92] Steffan, J.S.; Bodai, L.; Pallos, J.; Poelman, M.; McCampbell, A.; Apostol, B.L.; Kazantsev, A.; Schmidt, E.; Zhu, Y.Z.; Greenwald, M.; Kurokawa, R.; Housman, D.E.; Jackson, G.R.; Marsh, J.L.; Thompson, L.M. Histone deacetylase inhibitors arrest polyglutamine-dependent neurodegeneration in Drosophila. Nature, 2001, 413(6857), 739-43. http://dx.doi.org/10.1038/35099568
92. [93] Saft, C.; Lauter, T.; Kraus, P.H.; Przuntek, H.; Andrich, J.E. Dosedependent improvement of myoclonic hyperkinesia due to Valproic acid in eight Huntington's Disease patients: a case series. BMC Neurol., 2006, 6, 11. http://dx.doi.org/10.1186/1471-2377-6-11
93. [94] Ferrante, R.J.; Kubilus, J.K.; Lee, J.; Ryu, H.; Beesen, A.; Zucker, B.; Smith, K.; Kowall, N.W.; Ratan, R.R.; Luthi-Carter, R.; Hersch, S.M. Histone deacetylase inhibition by sodium butyrate chemotherapy ameliorates the neurodegenerative phenotype in Huntington's disease mice. J. Neurosci., 2003, 23(28), 9418-27.
94. [95] Mielcarek, M.; Landles, C.; Weiss, A.; Bradaia, A.; Seredenina, T.; Inuabasi, L.; Osborne, G.; Wadel, K.; Touller, C.; Butler, R.; Robertson, J.; Franklin, S. A.; Smith, D. L.; Park, L.; Marks, P. A.; Wanker, E. E.; Olson, E. N.; Luthi-Carter, R.; van der Putten, H.; Beaumont, V.; Bates, G. P. HDAC4 reduction: a novel therapeutic strategy to target cytoplasmic huntingtin and ameliorate neurodegeneration, PLoS Biol., 2013, 11, e1001717. http://dx.doi.org/ 10.1371/journal.pbio.1001717
95. [96] Jia, H.; Morris, C.D.; Williams, R.M.; Loring, J.F.; Thomas, E.A. HDAC inhibition imparts beneficial transgenerational effects in Huntington's disease mice via altered DNA and histone methylation. Proc. Natl. Acad. Sci. U.S.A., 2015, 112(1), 56-64. http://dx.doi.org/10.1073/pnas.1415195112
96. [97] Gardian, G.; Browne, S.E.; Choi, D.K.; Klivenyi, P.; Gregorio, J.; Kubilus, J.K.; Ryu, H.; Langley, B.; Ratan, R.R.; Ferrante, R.J.; Beal, M.F. Neuroprotective effects of phenylbutyrate in the N171-82Q transgenic mouse model of Huntington's disease. J. Biol. Chem., 2005, 280(1), 556-63. http://dx.doi.org/10.1074/jbc. M410210200
97. [98] Smith, M.R.; Syed, A.; Lukacsovich, T.; Purcell, J.; Barbaro, B.A.; Worthge, S.A.; Wei, S.R.; Pollio, G.; Magnoni, L.; Scali, C.; Massai, L.; Franceschini, D.; Camarri, M.; Gianfriddo, M.; Diodato, E.; Thomas, R.; Gokce, O.; Tabrizi, S.J.; Caricasole, A.; Landwehrmeyer, B.; Menalled, L.; Murphy, C.; Ramboz, S.; Luthi- Carter, R.; Westerberg, G.; Marsh, J.L. A potent and selective Sirtuin 1 inhibitor alleviates pathology in multiple animal and cell models of Huntington’s disease. Hum. Mol. Gen., 2014, 23(11), 2995-3007. http://dx.doi.org/10.1093/hmg/ddu010
98. [99] Sugai, F.; Yamamoto, Y.; Miyaguchi, K.; Zhou, Z.; Sumi, H.; Hamasaki, T.; Goto, M.; Sakoda, S. Benefit of valproic acid in suppressing disease progression of ALS model mice. Eur. J. Neurosci., 2004, 20(11), 3179-3183. http://dx.doi.org/10.1111/ j.1460-9568.2004.03765.x
99. [100] Ryu, H.; Smith, K.; Camelo, S.I.; Carreras, I.; Lee, J.; Iglesias, A.H.; Dangond, F.; Cormier, K.A.; Cudkowicz, M.E.; Brown, R.H. Jr; Ferrante, R.J. Sodium phenylbutyrate prolongs survival and regulates expression of anti-apoptotic genes in transgenic amyotrophic lateral sclerosis mice. J. Neurochem., 2005, 93(5), 1087-1098. http://dx.doi.org/10.1111/j.1471-4159.2005.03077.x
100. [101] Andreassi, C.; Angelozzi, C.; Tiziano, F.D.; Vitali, T.; De Vincenzi, E.; Boninsegna, A.; Villanova, M.; Bertini, E.; Pini, A.; Neri, G.; Brahe, C. Phenylbutyrate increases SMN expression in vitro: relevance for treatment of spinal muscular atrophy. Eur. J. Hum. Genet., 2004, 12(1), 59-65. http://dx.doi.org/10.1038/sj.ejhg. 5201102
101. [102] Sumner, C.J.; Huynh, T.N.; Markowitz, J.A.; Perhac, J.S.; Hill, B.; Coovert, D.D.; Schussler, K.; Chen, X.; Jarecki, J.; Burghes, A.H.; Taylor, J.P.; Fischbeck, K.H. Valproic acid increases SMN levels in spinal muscular atrophy patient cells. Ann. Neurol., 2003, 54(5), 647-54. http://dx.doi.org/10.1002/ana.10743
102. [103] Riessland, M.; Brichta, L.; Hahnen, E.; Wirth, B. The benzamide M344, a novel histone deacetylase inhibitor, significantly increases SMN2 RNA/protein levels in spinal muscular atrophy cells. Hum. Genet., 2006, 120(1), 101-10. http://dx.doi.org/10.1007/s00439- 006-0186-1
103. [104] Chang, J.G.; Hsieh-Li, H.M.; Jong, Y.J.; Wang, N.M.; Tsai, C.H.; Li, H. Treatment of spinal muscular atrophy by sodium butyrate. Proc. Natl. Acad. Sci. U.S.A., 2001, 98(17), 9808-9813. http://dx.doi.org/10.1073/pnas.171105098
104. [105] Hahnen, E.; Eyüpoglu, I.Y.; Brichta, L.; Haastert, K.; Tränkle, C.; Siebzehnrübl, F.A.; Riessland, M.; Hölker, I.; Claus, P.; Romstöck, J.; Buslei, R.; Wirth, B.; Blümcke, I. In vitro and ex vivo evaluation of second-generation histone deacetylase inhibitors for the treatment of spinal muscular atrophy. J. Neurochem., 2006, 98(1), 193-202. http://dx.doi.org/10.1111/j.1471-4159.2006.03868.x
105. [106] Brahe, C.; Vitali, T.; Tiziano, F.D.; Angelozzi, C.; Pinto, A.M.; Borgo, F.; Moscato, U.; Bertini, E.; Mercuri, E.; Neri, G. Phenylbutyrate increases SMN gene expression in spinal muscular atrophy patients. Eur. J. Hum. Genet., 2005, 13(2), 256-9. http://dx.doi.org/10.1038/sj.ejhg.5201320
106. [107] Brichta, L.; Holker, I.; Haug, K.; Klockgether, T.; Wirth, B. In vivo activation of SMN in spinal muscular atrophy carriers and patients treated with Valproate. Ann. Neurol., 2006, 59(6), 970-5. http://dx.doi.org/10.1002/ana.20836
107. [108] Avila, A.M.; Burnett, B.G.; Taye, A.A.; Gabanella, F.; Knight, M.A.; Hartenstein, P.; Cizman, Z.; Di Prospero, N.A.; Pellizzoni, L.; Fischbeck, K.H.; Sumner, C.J. Trichostatin A increases SMN expression and survival in a mouse model of spinal muscular atrophy. J. Clin. Invest., 2007, 117(3), 659-671. http://dx.doi.org/ 10.1172/JCI29562
108. [109] Weihl, C.C.; Connolly, A.M.; Pestronk, A. Valproate may improve strength and function in patients with type III/IV spinal muscle atrophy. Neurology, 2006, 67(3), 500-1. http://dx.doi.org/10. 1212/01.wnl.0000231139.26253.d0
109. [110] Rak, K.; Lechner, B.D.; Schneider, C.; Drexl, H.; Sendtner, M.; Jablonka, S. Valproic acid blocks excitability in SMA type I mouse motor neurons. Neurobiol. Dis., 2009, 36(3), 477-87. http://dx.doi.org/10.1016/j.nbd.2009.08.014
110. [111] Kwon, D.Y.; Motley, W.W.; Fischbeck, K.H.; Burnett, B.G. Increasing expression and decreasing degradation of SMN ameliorate the spinal muscular atrophy phenotype in mice. Hum. Mol. Genet., 2011, 20(18), 3667-3677. http://dx.doi.org/10.1093/ hmg/ddr288
111. [112] Riessland, M.; Ackermann, B.; Förster, A.; Jakubik, M.; Hauke, J.; Garbes, L.; Fritzsche, I.; Mende, Y.; Blumcke, I.; Hahnen, E.; Wirth, B. SAHA ameliorates the SMA phenotype in two mouse models for spinal muscular atrophy. Hum. Mol. Genet., 2010, 19(8), 1492-506. http://dx.doi.org/10.1093/hmg/ddq023
112. [113] Wadman, R.I.; Bosboom, W.M.; van der Pol, W.L.; van den Berg, L.H.; Wokke, J.H.; Iannaccone, S.T.; Vrancken, A.F. Drug treatment for spinal muscular atrophy types II and III. Cochrane Database Syst. Rev., 2012, 4, CD006282. http://dx.doi.org/10. 1002/14651858.cd006282.pub4
113. [114] Consalvi, S.; Saccone, V.; Giordani, L.; Minetti, G.; Mozzetta, C.; Puri, P.L. Histone deacetylase inhibitors in the treatment of muscular dystrophies: epigenetic drugs for genetic diseases. Mol. Med., 2011, 17, 457-65. http://dx.doi.org/10.2119/molmed. 2011.00049
114. [115] Anderson, M.F.; Sims, N.R. The effects of focal ischemia and reperfusion on the glutathione content of mitochondria from rat brain sub regions. J. Neurochem., 2002, 81, 541-9. http://dx.doi. org/10.1046/j.1471-4159.2002.00836.x
115. [116] Young, W. Secondary injury mechanisms in acute spinal cord injury. Emerg. Med. J., 1993, 11(1), 13-22.
116. [117] Rivieccio, M.A.; Brochier, C.; Willis, D.E.; Walker, B.A.; D'Annibale, M.A.; McLaughlin, K.; Siddiq, A.; Kozikowski, A.P.; Jaffrey, S.R.; Twiss, J.L; Ratan, R.R.; Langley, B. HDAC6 is a target for protection and regeneration following injury in the nervous system. Proc. Natl. Acad. Sci. U.S.A., 2009, 106(46), 19599-604. http://dx.doi.org/10.1073/pnas.0907935106
117. [118] Colussi, C.; Mozzetta, C.; Gurtner, A.; Illi, B.; Rosati, J.; Straino, S.; Ragone, G.; Pescatori, M.; Zaccagnini, G.; Antonini, A.; Minetti, G.; Martelli, F.; Piaggio, G.; Gallinari, P.; Steinkuhler, C.; Clementi, E.; Dell'Aversana, C.; Altucci, L.; Mai, A.; Capogrossi, M.C.; Puri, P.L.; Gaetano, C. HDAC2 blockade by Nitric Oxide and histone deacetylase inhibitors reveals a common target in Duchenne muscular dystrophy treatment. Proc. Natl. Acad. Sci. U.S.A., 2008, 105(49), 19183-7. http://dx.doi.org/10.1073/pnas. 0805514105
118. [119] Yao, X.; Zhang, J.R.; Huang, H.R.; Dai, L.C.; Liu, Q.J.; Zhang, M. Histone deacetylase inhibitor promotes differentiation of embryonic stem cells into neural cells in adherent monoculture. Chin. Med. J. (Engl), 2010, 123(6), 734-8.
119. [120] Morita, K.; Gotohda, T.; Arimochi, H.; Lee, M.S.; Her, S. Histone deacetylase inhibitors promote neurosteroid-mediated cell differentiation and enhance serotonin-stimulated brain-derived neurotrophic factor gene expression in rat C6 glioma cells. J. Neurosci. Res., 2009, 89(11), 2608-14. http://dx.doi.org/10.1002/ jnr.22072
120. [121] Shen, S.; Sandoval, J.; Swiss, V.A.; Li, J.; Dupree, J.; Franklin, R.J.; Casaccia-Bonnefil, P. Age-dependent epigenetic control of differentiation inhibitors is critical for remyelination efficiency. Nat. Neurosci., 2008, 11(9), 1024-1034. http://dx.doi.org/10.1038/ nn.2172
121. [122] Gaub, P.; Tedeschi, A.; Puttagunta, R.; Nguyen, T.; Schmandke, A.; Di Giovanni, S. HDAC inhibition promotes neuronal outgrowth and counteracts growth cone collapse through CBP/p300 and P/CAF-dependent p53 acetylation. Cell Death Differ., 2010, 17, 1392-1408. http://dx.doi.org/10.1038/cdd.2009.216
122. [123] Finelli, M.J.; Wong, J.K.; Zou, H. Epigenetic Regulation of Sensory Axon Regeneration after Spinal Cord Injury. J. Neurosci., 2013, 33(50), 19664-19676. http://dx.doi.org/10.1523/JNEUROSCI. 0589-13.2013
123. [124] Liu, C.M.; Wang, R.Y.; Saijilafu; Jiao, Z.X.; Zhang, B.Y.; Zhou, F.Q. MicroRNA-138 and SIRT1 form a mutual negative feedback loop to regulate mammalian axon regeneration. Genes Dev., 2013, 27(13),1473-83. http://dx.doi.org/10.1101/gad.209619.112
124. [125] Lv, L.; Han, X.; Sun, Y.; Wang, X.; Dong, Q. Valproic acid improves locomotion in vivo after SCI and axonal growth of neurons in vitro. Exp. Neurol., 2012, 233(2), 783-90. http://dx.doi.org/10.1016/j.expneurol.2011.11.042
125. [126] Ng, F.; Tang, B.L. Protein deacetylases and axonal regeneration. Neural Regen. Res., 2015, 10, 870-1. http://dx.doi.org/10.4103/ 1673-5374.158333
126. [127] Hashioka, S.; Klegeris, A.; McGeer, P.L. The histone deacetylase inhibitor suberoylanilide hydroxamic acid attenuates human astrocyte neurotoxicity induced by interferon-γ. J. Neuroinflam., 2012, 9, 113. http://dx.doi.org/10.1186/1742-2094-9-113
127. [128] Fukui, T.; Asakura, K.; Hikichi, C.; Ishikawa, T.; Murai, R.; Hirota, S.; Murate, K.; Kizawa, M.; Ueda, A.; Ito, S.; Mutoh, T. Histone deacetylase inhibitor attenuates neurotoxicity of clioquinol in PC12 cells. Toxicology, 2015, 331, 112-8. http://dx.doi.org/10. 1016/j.tox.2015.01.013
128. [129] Durham, B. Novel histone deacetylase (HDAC) inhibitors with improved selectivity for HDAC2 and 3 protect against neural cell death. Biosci. Horizons, 2012, 5, hzs003.
129. [130] Seo, J.; Jo, S.A.; Hwang, S.; Byun, C.J.; Lee, H.J.; Cho, D.H.; Kim, D.; Koh, Y.H.; Jo, I. Trichostatin A epigenetically increases calpastatin expression and inhibits calpain activity and calciuminduced SH-SY5Y neuronal cell toxicity. FEBS J., 2013, 280(24), 6691-701. http://dx.doi.org/10.1111/febs.12572
130. [131] Formisano, L.; Guida, N.; Laudati, G.; Mascolo, L.; Di Renzo, G.; Canzoniero, L.M. MS-275 inhibits aroclor 1254-induced SH-SY5Y neuronal cell toxicity by preventing the formation of the HDAC3/REST complex on the synapsin-1 promoter. J. Pharmacol. Exp. Ther., 2015, 352(2), 236-43. http://dx.doi.org/10.1124/ jpet.114.219345
131. [132] Kim, J.Y.; Shen, S.; Dietz, K.; He, Y.; Howell, O.; Reynolds, R.; Casaccia, P. HDAC1 nuclear export induced by pathological conditions is essential for the onset of axonal damage. Nat. Neurosci., 2010, 13(2),180-9. http://dx.doi.org/10.1038/nn.2471
132. [133] Sun, Q.; Yao, Y.; Liu, C.; Li H, Yao H, Xue X, Liu J, Tu Z, Jiang S. Design, synthesis, and biological evaluation of novel histone deacetylase 1 inhibitors through click chemistry. Bioorg. Med. Chem. Lett., 2013, 23(11), 3295-9. http://dx.doi.org/10.1016/j.bmcl. 2013.03.102
133. [134] Bieliauskas, A.V.; Pflum, M.K. Isoform-selective histone deacetylase inhibitors. Chem. Soc. Rev., 2008, 37, 1402-13. http://dx.doi.org/10.1039/b703830p
134. [135] Kalyaanamoorthy, S.; Chen, Y.P.P. Energy based pharmacophore mapping of HDAC inhibitorsagainst class i HDAC enzymes. Biochim. Biophys., 2013, 1834, 317-28.
135. [136] Ganai, S.A.; Shanmugam, K.; Mahadevan, V. Energy-optimised pharmacophore approach to identify potential hotspots during inhibition of Class II HDAC isoforms. J. Biomol. Struct. Dyn., 2015, 33(2), 374-87. http://dx.doi.org/10.1080/07391102.2013. 879073
136. [137] Tsankova, N.M.; Berton, O.; Renthal, W.; Kumar, A.; Neve, R.L.; Nestler, E.J. Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat. Neurosci., 2006, 9(4), 519-525. http://dx.doi.org/10.1038/nn1659
137. [138] Fujiki, R.; Sato, A.; Fujitani, M.; Yamashita, T. A proapoptotic effect of VPA on progenitors of embryonic stem cell-derived glutamatergic neurons. Cell Death Dis., 2013, 4, e677-10. http://dx.doi.org/10.1038/cddis.2013.205
138. [139] Bardai, F.H.; Price, V.; Zaayman, M.; Wang, L.; D'Mello, S.R. Histone deacetylase-1 (HDAC1) is a molecular switch between neuronal survival and death. J. Biol. Chem., 2012, 287(42), 35444-53. http://dx.doi.org/10.1074/jbc.M112.394544
139. [140] Bardai, F.H.; D'Mello, S.R. Selective toxicity by HDAC3 in neurons: regulation by Akt and GSK3beta. J. Neurosci., 2011, 31(5), 1746-51. http://dx.doi.org/10.1523/JNEUROSCI.5704-10.2011
140. [141] Pfister, J. A.; Ma, C.; Morrison, B.E.; D’Mello, S.R. Opposing effects of sirtuins on neuronal survival: SIRT1-mediated neuroprotection is independent of its deacetylase activity. PLoS ONE, 2008, 3, e4090. http://dx.doi.org/10.1371/journal.pone.0004090
141. [142] Shah, M.H.; Binkley, P.; Chan, K.; Xiao, J.; Arbogast, D.; Collamore, M.; Farra, Y.; Young, D.; Grever, M. Cardiotoxicity of histone deacetylase inhibitor depsipeptide in patients with metastatic neuroendocrine tumors. Clin. Cancer Res., 2006, 12(13), 3997-4003. http://dx.doi.org/10.1158/1078-0432.CCR-05-2689
142. [143] Molife, R.; Fong, P.; Scurr, M.; Judson, I.; Kaye, S.; de Bono, J. HDAC inhibitors and cardiac safety. Clin. Cancer Res., 2007, 13(3), 1068-9. http://dx.doi.org/10.1158/1078-0432.CCR-06-1715
143. [144] Bastian, L.; Hof, J.; Pfau, M.; Fichtner, I.; Eckert, C.; Henze, G.; Prada, J.; von Stackelberg, A.; Seeger, K.; Shalapour, S. Synergistic activity of bortezomib and HDACi in preclinical models of B-cell precursor acute lymphoblastic leukemia via modulation of p53, PI3K/AKT, and NF-kappaB. Clin. Cancer Res., 2013, 19, 1445-57. http://dx.doi.org/10.1158/1078-0432.CCR-12- 1511
144. [145] Dowdy, S.C.; Jiang, S.; Zhou, X.C.; Hou, X.; Jin, F.; Podratz, K.C.; Jiang, S.W. Histone deacetylase inhibitors and paclitaxel cause synergistic effects on apoptosis and microtubule stabilization in papillary serous endometrial cancer cells. Mol. Cancer Ther., 2006, 5, 2767-76. http://dx.doi.org/10.1158/1535-7163.MCT-06-0209
145. [146] Eriksson, I.; Joosten, M.; Roberg, K.; Ollinger, K. The histone deacetylase inhibitor Trichostatin A reduces lysosomal pH and enhances cisplatin-induced apoptosis. Exp. Cell Res., 2013, 319(1), 12-20. http://dx.doi.org/10.1016/j.yexcr.2012.10.004