Hydroxamate-based histone deacetylase inhibitors can protect neurons from oxidative stress via a histone deacetylase-independent catalase-like mechanism

Chemistry and Biology

Volumn 22, Issue 4, 2015, Pages 439-445

  Olson, David E ^a   Sleiman, Sama F ^b   Bourassa, Megan W ^c,d   Wagner, Florence F ^a   Gale, Jennifer P ^a   Zhang, Yan Ling ^a   Ratan, Rajiv R ^c,d   Holson, Edward B ^a  

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

^b LEBANESE AMERICAN UNIVERSITY   (Lebanon)

^c BURKE MEDICAL RESEARCH INSTITUTE   (United States)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; COORDINATION COMPOUND; FENTON'S REAGENT; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; HYDROGEN PEROXIDE; HYDROXAMIC ACID; IRON; NEUROPROTECTIVE AGENT; PROTEIN BINDING; REACTIVE OXYGEN METABOLITE;

ANIMAL; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; METABOLISM; MOUSE; NERVE CELL; OXIDATIVE STRESS;

ANIMALS; CATALASE; COORDINATION COMPLEXES; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HYDROGEN PEROXIDE; HYDROXAMIC ACIDS; IRON; MICE; NEURONS; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; PROTEIN BINDING; REACTIVE OXYGEN SPECIES;

EID: 84928386009     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chembiol.2015.03.014     Document Type: Article

References (33)

1. K. Baker, C.B. Marcus, K. Huffman, H. Kruk, B. Malfroy, and S.R. Doctrow Synthetic combined superoxide dismutase/catalase mimetics are protective as a delayed treatment in a rat stroke model: a key role for reactive oxygen species in ischemic brain injury J. Pharmacol. Exp. Ther. 284 1998 215 221
2. A. Balasubramanian, J. Ramos, W. Luo, M. Sirisawad, E. Verner, and J.J. Buggy A novel histone deacetylase 8 (HDAC8)-specific inhibitor PCI-34051 induces apoptosis in T-cell lymphomas Leukemia 22 2008 1026 1034
3. K.V. Butler, J. Kalin, C. Brochier, G. Vistoli, B. Langley, and A.P. Kozikowski Rational design and simple chemistry yield a superior, neuroprotective HDAC6 inhibitor, tubastatin A J. Am. Chem. Soc. 132 2010 10842 10846
4. Z.I. Cabantchik, H. Glickstein, P. Milgram, and W. Breuer A fluorescence assay for assessing chelation of intracellular iron in a membrane model system and in mammalian cells Anal. Biochem. 233 1996 221 227
5. A. Fiedler, T. Reinert, M. Morawski, G. Brückner, T. Arendt, and T. Butz Intracellular iron concentration of neurons with and without perineuronal nets Nucl. Instrum. Methods Phys. Res. B 260 2007 153 158
6. B. Fleiss, M.K.L. Nilsson, K. Blomgren, and C. Mallard Neuroprotection by the histone deacetylase inhibitor trichostatin A in a model of lipopolysaccharide-sensitised neonatal hypoxic-ischaemic brain injury J. Neuroinflamm. 9 2012 1 15
7. D.C. Fung, and D.T. Petrishko Capillary tube catalase test Appl. Microbiol. 26 1973 631 632
8. I.V. Gregoretti, Y.-M. Lee, and H.V. Goodson Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis J. Mol. Biol. 338 2004 17 31
9. C. Hubbert, A. Guardiola, R. Shao, Y. Kawaguchi, A. Ito, A. Nixon, M. Yoshida, X.F. Wang, and T.P. Yao HDAC6 is a microtubule-associated deacetylase Nature 417 2002 455 458
10. P.A. Hyslop, Z. Zhang, D.V. Pearson, and L.A. Phebus Measurement of striatal H2O2 by microdialysis following global forebrain ischemia and reperfusion in the rat: correlation with the cytotoxic potential of H2O2 in vitro Brain Res. 671 1995 181 186
11. S.K. Jonas, and P.A. Riley The effect of ligands on the uptake of iron by cells in culture Cell Biochem. Funct. 9 1991 245 253
12. 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
13. R. Kohen, and A. Nyska Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification Toxicol. Pathol. 30 2002 620 650
14. J. Lu, J.M. Frerich, L.C. Turtzo, S. Li, J. Chiang, C. Yang, X. Wang, C. Zhang, C. Wu, and Z. Sun Histone deacetylase inhibitors are neuroprotective and preserve NGF-mediated cell survival following traumatic brain injury Proc. Natl. Acad. Sci. USA 110 2013 10747 10752
15. S. Melov, J. Ravenscroft, S. Malik, M.S. Gill, D.W. Walker, P.E. Clayton, D.C. Wallace, B. Malfroy, S.R. Doctrow, and G.J. Lithgow Extension of life-span with superoxide dismutase/catalase mimetics Science 289 2000 1567 1569
16. T.H. Murphy, R.L. Schnaar, and J.T. Coyle Immature cortical neurons are uniquely sensitive to glutamate toxicity by inhibition of cystine uptake FASEB J. 4 1990 1624 1633
17. D.E. Olson, F.F. Wagner, T. Kaya, J.P. Gale, N. Aidoud, E.L. Davoine, F. Lazzaro, M. Wëiwer, Y.-L. Zhang, and E.B. Holson Discovery of the first histone deacetylase 6/8 dual inhibitors J. Med. Chem. 56 2013 4816 4820
18. D.E. Olson, N.D. Udeshi, N.A. Wolfson, C.A. Pitcairn, E.D. Sullivan, J. Jaffe, T. Svinkina, T. Natoli, X. Liu, and J. Paulk An unbiased approach to identify endogenous substrates of "histone" deacetylase 8 ACS Chem. Biol. 9 2014 2210 2216
19. H. Pan, J. Cao, and W. Xu Selective histone deacetylase inhibitors Anticancer Agents Med. Chem. 12 2012 247 270
20. G. Piperno, M. LeDizet, and X.-J. Chang Microtubules containing acetylated alpha-tubulin in mammalian cells in culture J. Cell Biol. 104 1987 289 302
21. J. Prousek Fenton chemistry in biology and medicine Pure Appl. Chem. 79 2007 2325 2338
22. R.R. Ratan, and J.M. Baraban Apoptotic death in an in vitro model of neuronal oxidative stress Clin. Exp. Pharmacol. Physiol. 22 1995 309 310
23. R.R. Ratan, T.H. Murphy, and J.M. Baraban Oxidative stress induces apoptosis in embryonic cortical neurons J. Neurochem. 62 1994 376 379
24. U. Rauen, T. Li, R. Sustmann, and H. De Groot Protection against iron- and hydrogen peroxide-dependent cell injuries by a novel synthetic iron catalase mimic and its precursor, the iron-free ligand Free Radic. Biol. Med. 37 2004 1369 1383
25. H. Ryu, J. Lee, B.A. Olofsson, A. Mwidau, A. Dedeoglu, M. Escudero, E. Flemington, J. Azizkhan-Clifford, R.J. Ferrante, and R.R. Ratan Histone deacetylase inhibitors prevent oxidative neuronal death independent of expanded polyglutamine repeats via an Sp1-dependent pathway Proc. Natl. Acad. Sci. USA 100 2003 4281 4286
26. S. Schweizer, A. Meisel, and S. Märschenz Epigenetic mechanisms in cerebral ischemia J. Cerebr. Blood F. Met. 33 2013 1335 1346
27. N.A. Shein, N. Grigoriadis, A.G. Alexandrovich, C. Simeonidou, A. Lourbopoulos, E. Polyzoidou, V. Trembovler, P. Mascagni, C.A. Dinarello, and E. Shohami Histone deacetylase inhibitor ITF2357 is neuroprotective, improves functional recovery, and induces glial apoptosis following experimental traumatic brain injury FASEB J. 23 2009 4266 4275
28. S.F. Sleiman, D.E. Olson, M.W. Bourassa, S.S. Karuppagounder, Y.-L. Zhang, J. Gale, F.F. Wagner, M. Basso, G. Coppola, and J.T. Pinto Hydroxamic acid-based histone deacetylase (HDAC) inhibitors can mediate neuroprotection independent of HDAC inhibition J. Neurosci. 34 2014 14328 14337
29. S. Spange, T. Wagner, T. Heinzel, and O.H. Krämer Acetylation of non-histone proteins modulates cellular signalling at multiple levels Int. J. Biochem. Cell Biol. 41 2009 185 198
30. R. Sustmann, H.G. Korth, D. Kobus, J. Baute, K.H. Seiffert, E. Verheggen, E. Bill, M. Kirsch, and H. de Groot Fe(III) complexes of 1,4,8,11-tetraaza[14]annulenes as catalase mimetics Inorg. Chem. 46 2007 11416 11430
31. C. Thomas, M.M. Mackey, A.A. Diaz, and D.P. Cox Hydroxyl radical is produced via the Fenton reaction in submitochondrial particles under oxidative stress: implications for diseases associated with iron accumulation Redox Rep. 14 2009 102 108
32. B. Uttara, A.V. Singh, P. Zamboni, and R.T. Mahajan Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options Curr. Neuropharmacol. 7 2009 65 74
33. F.F. Wagner, D.E. Olson, J.P. Gale, T. Kaya, M. Wëiwer, N. Aidoud, M. Thomas, E.L. Davoine, B.C. Lemercier, Y.-L. Zhang, and E.B. Holson Potent and selective inhibition of histone deacetylase 6 (HDAC6) does not require a surface-binding motif J. Med. Chem. 56 2013 1772 1776