Hydroxamic acid-based histone deacetylase (HDAC) inhibitors can mediate neuroprotection independent of HDAC inhibition

Journal of Neuroscience

Volumn 34, Issue 43, 2014, Pages 14328-14337

  Sleiman, Sama F ^a,c   Olson, David E ^b   Bourassa, Megan W ^c,d   Karuppagounder, Saravanan S ^c,d   Zhang, Yan Ling ^b   Gale, Jennifer ^b   Wagner, Florence F ^b   Basso, Manuela ^e   Coppola, Giovanni ^f   Pinto, John T ^g   Holson, Edward B ^b   Ratan, Rajiv R ^a,b  

^a BURKE MEDICAL RESEARCH INSTITUTE   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c LEBANESE AMERICAN UNIVERSITY   (Lebanon)

^d BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^e UNIVERSITY OF TRENTO   (Italy)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g NEW YORK MEDICAL COLLEGE   (United States)

Author keywords

HDAC inhibitors; HDAC8; Hydroxamic acids; Neuroprotection; Oxidative stress; PCI 34051

Indexed keywords

APICIDIN; BRD 8461; BRD 9715; GLUTATHIONE; HISTONE DEACETYLASE; HISTONE DEACETYLASE 8; HISTONE DEACETYLASE INHIBITOR; PCI 34051; TRICHOSTATIN A; UNCLASSIFIED DRUG; VORINOSTAT; NEUROPROTECTIVE AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CELL; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; EPIGENETICS; GENE EXPRESSION; GENOTYPE; IMMUNOBLOTTING; IMMUNOPRECIPITATION; MOUSE; MTT ASSAY; MUS MUSCULUS; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PROTON NUCLEAR MAGNETIC RESONANCE; STRUCTURE ACTIVITY RELATION; WESTERN BLOTTING; ANIMAL; BRAIN CORTEX; CELL CULTURE; DRUG EFFECTS; FEMALE; NERVE CELL; PATHOLOGY; PREGNANCY; TRANSGENIC MOUSE;

ANIMALS; CELLS, CULTURED; CEREBRAL CORTEX; FEMALE; HISTONE DEACETYLASE INHIBITORS; MICE; MICE, TRANSGENIC; NEURONS; NEUROPROTECTIVE AGENTS; PREGNANCY;

EID: 84908065243     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1010-14.2014     Document Type: Article

References (41)

1. Aminova LR, Siddiq A, Ratan RR (2008) Antioxidants, HIF prolyl hydroxylase inhibitors or short interfering RNAs to BNIP3 or PUMA, can prevent prodeath effects of the transcriptional activator, HIF-1alpha, in a mouse hippocampal neuronal line. Antiox Redox Signal 10:1989–1998. CrossRef Medline
2. Balasubramanian S, Ramos J, Luo W, Sirisawad M, Verner E, Buggy JJ (2008) A novel histone deacetylase 8 (HDAC8)-specific inhibitor PCI-34051 induces apoptosis in T-cell lymphomas. Leukemia 22:1026–1034. CrossRef Medline
3. Bardai FH, D’Mello SR (2011) Selective toxicity by HDAC3 in neurons: regulation by Akt and GSK3beta. J Neurosci 31:1746–1751. CrossRef Medline
4. Bardai FH, Price V, Zaayman M, Wang L, D’Mello SR (2012) Histone deacetylase-1 (HDAC1) is a molecular switch between neuronal survival and death. J Biol Chem 287:35444–35453. CrossRef Medline
5. Bardai FH, Verma P, Smith C, Rawat V, Wang L, D’Mello SR (2013) Disassociation of histone deacetylase-3 from normal huntingtin underlies mutant huntingtin neurotoxicity. J Neurosci 33:11833–11838. CrossRef Medline
6. Bradner JE, West N, Grachan ML, Greenberg EF, Haggarty SJ, Warnow T, Mazitschek R (2010) Chemical phylogenetics of histone deacetylases. Nat Chem Biol 6:238–243. CrossRef Medline
7. Brochier C, Dennis G, Rivieccio MA, McLaughlin K, Coppola G, Ratan RR, Langley B (2013) Specific acetylation of p53 by HDAC inhibition prevents DNA damage-induced apoptosis in neurons. J Neurosci 33:8621–8632. CrossRef Medline
8. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV, Mann M (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325:834–840. CrossRef Medline
9. Dailey LA, Imming P (1999) 12-Lipoxygenase: classification, possible therapeutic benefits from inhibition, and inhibitors. Curr Med Chem 6:389–398. CrossRef Medline
10. Deardorff MA, Bando M, Nakato R, Watrin E, Itoh T, Minamino M, Saitoh K, Komata M, Katou Y, Clark D, Cole KE, De Baere E, Decroos C, Di Donato N, Ernst S, Francey LJ, Gyftodimou Y, Hirashima K, Hullings M, Ishikawa Y, et al. (2012) HDAC8 mutations in Cornelia de Lange syndrome affect the cohesin acetylation cycle. Nature 489:313–317. CrossRef Medline
11. Dixon SJ, Lemberg KM, Lamprecht MR, Skouta R, Zaitsev EM, Gleason CE, Patel DN, Bauer AJ, Cantley AM, Yang WS, Morrison B, Stockwell BR (2012) Ferroptosis: an iron-dependent form of nonapoptotic cell death. Cell 149:1060–1072. CrossRef Medline
12. Ferrante RJ, Kubilus JK, Lee J, Ryu H, Beesen A, Zucker B, Smith K, Kowall NW, Ratan RR, Luthi-Carter R, Hersch SM (2003) Histone deacetylase inhibition by sodium butyrate chemotherapy ameliorates the neurodegenerative phenotype in Huntington’s disease mice. J Neurosci 23:9418–9427. Medline
13. Fischer A, Sananbenesi F, Wang X, Dobbin M, Tsai LH (2007) Recovery of learning and memory is associated with chromatin remodelling. Nature 447:178–182. CrossRef Medline
14. Gaub P, Tedeschi A, Puttagunta R, Nguyen T, Schmandke A, Di Giovanni S (2010) HDAC inhibition promotes neuronal outgrowth and counteracts growth cone collapse through CBP/p300 and P/CAF-dependent p53 acetylation. Cell Death Differ 17:1392–1408. CrossRef Medline
15. Gräff J, Rei D, Guan JS, Wang WY, Seo J, Hennig KM, Nieland TJ, Fass DM, Kao PF, Kahn M, Su SC, Samiei A, Joseph N, Haggarty SJ, Delalle I, Tsai LH (2012) An epigenetic blockade of cognitive functions in the neurodegenerating brain. Nature 483:222–226. CrossRef Medline
16. Guan JS, Haggarty SJ, Giacometti E, Dannenberg JH, Joseph N, Gao J, Nieland TJ, Zhou Y, Wang X, Mazitschek R, Bradner JE, DePinho RA, Jaenisch R, Tsai LH (2009) HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 459:55–60. CrossRef Medline
17. Gui CY, Ngo L, Xu WS, Richon VM, Marks PA (2004) Histone deacetylase (HDAC) inhibitor activation of p21WAF1 involves changes in promoterassociated proteins, including HDAC1. Proc Natl Acad Sci U S A 101: 1241–1246. CrossRef Medline
18. Haberland M, Mokalled MH, Montgomery RL, Olson EN (2009) Epigenetic control of skull morphogenesis by histone deacetylase 8. Genes Dev 23:1625–1630. CrossRef Medline
19. Hanson JE, Deng L, Hackos DH, Lo SC, Lauffer BE, Steiner P, Zhou Q (2013) Histone deacetylase 2 cell autonomously suppresses excitatory and enhances inhibitory synaptic function in CA1 pyramidal neurons. J Neurosci 33:5924–5929. CrossRef Medline
20. Hayashi S, McMahon AP (2002) Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol 244:305–318. CrossRef Medline
21. Kazantsev AG, Thompson LM (2008) Therapeutic application of histone deacetylase inhibitors for central nervous system disorders. Nat Rev Drug Discov 7:854–868. CrossRef Medline
22. Kim C, Choi H, Jung ES, Lee W, Oh S, Jeon NL, Mook-Jung I (2012) HDAC6 inhibitor blocks amyloid beta-induced impairment of mitochondrial transport in hippocampal neurons. PLoS One 7:e42983. CrossRef Medline
23. Kouzarides T (2000) Acetylation: a regulatory modification to rival phosphorylation? EMBO J 19:1176–1179. CrossRef Medline
24. Lange PS, Chavez JC, Pinto JT, Coppola G, Sun CW, Townes TM, Geschwind DH, Ratan RR (2008) ATF4 is an oxidative stress-inducible, prodeath transcription factor in neurons in vitro and in vivo. J Exp Med 205:1227–1242. CrossRef Medline
25. Langley B, D’Annibale MA, Suh K, Ayoub I, Tolhurst A, Bastan B, Yang L, Ko B, Fisher M, Cho S, Beal MF, Ratan RR (2008) Pulse inhibition of histone deacetylases induces complete resistance to oxidative death in cortical neurons without toxicity and reveals a role for cytoplasmic p21(waf1/ cip1) in cell cycle-independent neuroprotection. J Neurosci 28:163–176. CrossRef Medline
26. Li Y, Maher P, Schubert D (1997) A role for 12-lipoxygenase in nerve cell death caused by glutathione depletion. Neuron 19:453–463. CrossRef Medline
27. Morris MJ, Mahgoub M, Na ES, Pranav H, Monteggia LM (2013) Loss of histone deacetylase 2 improves working memory and accelerates extinction learning. J Neurosci 33:6401–6411. CrossRef Medline
28. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63. CrossRef Medline
29. Oehme I, Deubzer HE, Wegener D, Pickert D, Linke JP, Hero B, Kopp- Schneider A, Westermann F, Ulrich SM, von Deimling A, Fischer M, Witt O (2009) Histone deacetylase 8 in neuroblastoma tumorigenesis. Clin Cancer Res 15:91–99. CrossRef Medline
30. Olson DE, et al. (2014) An unbiased approach to identify endogenous substrates of “histone” deacetylase 8. ACS Chem Biol. Advance online publication. Retrieved Aug. 11, 2014. doi: 10.1021/cb500492r. CrossRef Medline
31. Ratan RR, Murphy TH, Baraban JM (1994a) Macromolecular synthesis inhibitors prevent oxidative stress-induced apoptosis in embryonic cortical neurons by shunting cysteine from protein synthesis to glutathione. J Neurosci 14:4385–4392. Medline
32. Ratan RR, Murphy TH, Baraban JM (1994b) Oxidative stress induces apoptosis in embryonic cortical neurons. J Neurochem 62:376–379. CrossRef Medline
33. Rivieccio MA, Brochier C, Willis DE, Walker BA, D’Annibale MA, McLaughlin K, Siddiq A, Kozikowski AP, Jaffrey SR, Twiss JL, Ratan RR, Langley B (2009) HDAC6 is a target for protection and regeneration following injury in the nervous system. Proc Natl Acad Sci U S A 106:19599–19604. CrossRef Medline
34. Ryu H, Lee J, Olofsson BA, Mwidau A, Dedeoglu A, Escudero M, Flemington E, Azizkhan-Clifford J, Ferrante RJ, Ratan RR (2003) Histone deacetylase inhibitors prevent oxidative neuronal death independent of expanded polyglutamine repeats via an Sp1-dependent pathway. Proc Natl Acad Sci U S A 100:4281–4286. CrossRef Medline
35. Siddiq A, Aminova LR, Troy CM, Suh K, Messer Z, Semenza GL, Ratan RR (2009) Selective inhibition of hypoxia-inducible factor (HIF) prolylhydroxylase 1 mediates neuroprotection against normoxic oxidative death via HIF- and CREB-independent pathways. J Neurosci 29:8828–8838. CrossRef Medline
36. Sleiman SF, Basso M, Mahishi L, Kozikowski AP, Donohoe ME, Langley B, Ratan RR (2009) Putting the ‘HAT’ back on survival signalling: the promises and challenges of HDAC inhibition in the treatment of neurological conditions. Exp Opin Invest Drugs 18:573–584. CrossRef Medline
37. Sleiman SF, Berlin J, Basso M, Karuppagounder SS, Rohr J, Ratan RR (2011) Histone deacetylase inhibitors and mithramycin A impact a similar neuroprotective pathway at a crossroad between cancer and neurodegeneration. Pharmaceuticals 4:1183–1195. CrossRef Medline
38. Smith MA, Harris PL, Sayre LM, Perry G (1997) Iron accumulation in Alzheimer disease is a source of redox-generated free radicals. Proc Natl Acad Sci U S A 94:9866–9868. CrossRef Medline
39. Stavniichuk R, Shevalye H, Hirooka H, Nadler JL, Obrosova IG (2012) Interplay of sorbitol pathway of glucose metabolism, 12/15-lipoxygenase, and mitogen-activated protein kinases in the pathogenesis of diabetic peripheral neuropathy. Biochem Pharmacol 83:932–940. CrossRef Medline
40. Sudo H, Baas PW (2010) Acetylation of microtubules influences their sensitivity to severing by katanin in neurons and fibroblasts. J Neurosci 30: 7215–7226. CrossRef Medline
41. Weinreb O, Amit T, Mandel S, Kupershmidt L, Youdim MB (2010) Neuroprotective multifunctional iron chelators: from redox-sensitive process to novel therapeutic opportunities. Antiox Redox Signal 13:919–949. CrossRef Medline