Inhibition of tubulin polymerization by hypochlorous acid and chloramines

Free Radical Biology and Medicine

Volumn 50, Issue 8, 2011, Pages 1000-1008

  Landino, Lisa M ^a   Hagedorn, Tara D ^a   Kim, Shannon B ^a   Hogan, Katherine M ^a  

^a The College of William and Mary   (United States)

Author keywords

Chloramine; Cysteine oxidation; Free radicals; Hypochlorous acid; Methionine oxidation; Nitroxyl; Peroxynitrite; Tubulin

Indexed keywords

5 IODOACETAMIDOFLUORESCEIN; 5,5' DITHIOBIS(2 NITROBENZOIC ACID); ANGELI SALT; CHLORAMINE DERIVATIVE; CYSTEINE; CYTOSKELETON PROTEIN; DISULFIDE; FLUORESCEIN DERIVATIVE; HYPOCHLOROUS ACID; METHIONINE; NITRIC OXIDE DONOR; PEROXYNITRITE; SODIUM CHLORIDE; THIOL; TUBULIN; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; MICROTUBULE ASSEMBLY; NITRATION; NONHUMAN; OXIDATION KINETICS; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN POLYMERIZATION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; BRAIN; CHLORAMINES; HYPOCHLOROUS ACID; METHIONINE; OXIDATION-REDUCTION; SWINE; TUBULIN;

EID: 79952447228     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2011.01.018     Document Type: Article

References (45)

1. I. Sponne, A. Fifre, B. Drouet, C. Klein, V. Koziel, M. Pincon-Raymond, J.-L. Olivier, J. Chambaz, and T. Pillot Apoptotic neuronal cell death induced by the non-fibrillar amyloid beta peptide proceeds through an early reactive oxygen species-dependent cytoskeletal perturbation J. Biol. Chem. 278 2003 3437 3445 (Pubitemid 36801260)
2. M. Paula-Barbosa, M.A. Tavares, and A. Cadete-Leite A quantitative study of frontal cortex dendritic microtubules in patients with Alzheimers disease Brain Res. 417 1987 139 142 (Pubitemid 18012265)
3. P.F. Good, P. Werner, A. Hsu, C.W. Olanow, and D.P. Perl Evidence for neuronal oxidative damage in Alzheimers disease Am. J. Pathol. 149 1996 21 28 (Pubitemid 26230974)
4. L. Lyras, N.J. Cairns, A. Jenner, P. Jenner, and B. Halliwell An assessment of oxidative damage to proteins, lipids and DNA in brain from patients with Alzheimers disease J. Neurochem. 68 1997 2061 2069 (Pubitemid 27176143)
5. D.A. Butterfield, M. Perluigi, and R. Sultana Oxidative stress in Alzheimers disease brain: new insights from redox proteomics Eur. J. Pharmacol. 545 2006 39 50 (Pubitemid 44215876)
6. A.D. Cash, G. Aliev, S.L. Seidlak, A. Nunomura, H. Fujioka, X. Zhu, M. Tabaton, A.B. Johnson, M. Paula-Barbosa, J. Avila, P.K. Jones, R.J. Castellani, M.A. Smith, and G. Perry Microtubule reduction in Alzheimers disease and aging is independent of tau filament formation Am. J. Pathol. 162 2003 1623 1627 (Pubitemid 36512845)
7. R.C. Cumming, N.L. Andon, P.A. Haynes, M. Park, W.H. Fischer, and D. Schubert Protein disulfide bond formation in the cytoplasm during oxidative stress J. Biol. Chem. 279 2004 21749 21758 (Pubitemid 38679361)
8. R. Pamplona, E. Dalfo, V. Ayala, M.J. Bellmunt, J. Prat, I. Ferrer, and M. Portero-Otin Proteins in human brain cortex are modified by oxidation, glycoxidation, and lipoxidation J. Biol. Chem. 280 2005 21522 21530
9. J.P. Brennan, R. Wait, S. Begum, J.R. Bell, M.J. Dunn, and P. Eaton Detection and mapping of widespread intermolecular protein disulfide formation during cardiac oxidative stress using proteomics with diagonal electrophoresis J. Biol. Chem. 279 2004 41352 41360 (Pubitemid 39313574)
10. M. Sparaco, L.M. Gaeta, G. Tozzi, E. Bertini, A. Pastore, A. Simonati, F.M. Santorelli, and F. Piemonte Protein glutathionylation in human central nervous system: potential role in redox regulation of neuronal defense against free radicals J. Neurosci. Res. 83 2006 256 263 (Pubitemid 43184389)
11. C. Lind, R. Gerdes, Y. Hamnell, Shuppe-Koistinen, H. Brockenhuus von Lowenhielm, A. Holmgren, and I.A. Cotgreave Identification of S-glutathionylated cellular proteins during oxidative stress and constitutive metabolism by affinity purification and proteomic analysis Arch. Biochem. Biophys. 406 2002 229 240 (Pubitemid 35216349)
12. S.R. Jaffrey, H. Erdjument-Bromage, C.D. Ferris, P. Tempst, and S.H. Snyder Protein S-nitrosylation: a physiological signal for neuronal nitric oxide Nat. Cell Biol. 3 2001 193 197 (Pubitemid 32118373)
13. E. Nogales, S.G. Wolf, and K.H. Downing Structure of the αβ-tubulin dimer by electron crystallography Nature 391 1998 199 203 (Pubitemid 28092482)
14. R.F. Luduena, and M.C. Roach Tubulin sulfhydryl groups as probes and targets for antimitotic and antimicrotubule agents Pharmacol. Ther. 49 1991 133 152
15. J.B. Olmsted Tubulin pools in differentiating neuroblastoma cells J. Cell Biol. 89 1981 418 423 (Pubitemid 11035950)
16. P.J. Anderson The structure and amount of tubulin in cells and tissues J. Biol. Chem. 254 1979 2168 2171 (Pubitemid 9160034)
17. L.M. Landino, J.S. Iwig, K.L. Kennett, and K.L. Moynihan Repair of peroxynitrite damage to tubulin by the thioredoxin reductase system Free Radic. Biol. Med. 36 2004 497 506 (Pubitemid 38224520)
18. L.M. Landino, R. Hasan, A. McGaw, S. Cooley, A.W. Smith, K. Masselam, and G. Kim Peroxynitrite oxidation of tubulin sulfhydryls inhibits microtubule polymerization Arch. Biochem. Biophys. 398 2002 213 220 (Pubitemid 34848588)
19. L.M. Landino, K.L. Moynihan, J.V. Todd, and K.L. Kennett Modulation of the redox state of tubulin by the glutathione/glutaredoxin reductase system Biochem. Biophys. Res. Commun. 314 2004 555 560 (Pubitemid 38084754)
20. P.S. Green, A.J. Mendez, J.S. Jacob, J.R. Crowley, W. Growdon, B.T. Hyman, and J.W. Heinecke Neuronal expression of myeloperoxidase is increased in Alzheimers disease J. Neurochem. 90 2004 724 733 (Pubitemid 38989404)
21. R.A. Maki, V.A. Tyurin, R.C. Lyon, R.L. Hamilton, S.T. DeKosky, V.E. Kagan, and W.F. Reynolds Aberrant expression of myeloperoxidase in astrocytes promotes phospholipid oxidation and memory deficits in a mouse model of Alzheimer disease J. Biol. Chem. 284 2009 3158 3169
22. A.V. Peskin, and C.C. Winterbourn Taurine chloramine is more selective than hypochlorous acid at targeting critical cysteines and inactivating creatine kinase and glyceraldehyde-3-phosphate dehydrogenase Free Radic. Biol. Med. 40 2006 45 53 (Pubitemid 41759402)
23. A.V. Peskin, and C.C. Winterbourn Kinetics of the reactions of hypochlorous acid and amino acid chloramines with thiols, methionine and ascorbate Free Radic. Biol. Med. 30 2001 572 579 (Pubitemid 32162964)
24. L.M. Landino, M.T. Koumas, C.E. Mason, and J.A. Alston Modification of tubulin cysteines by nitric oxide and nitroxyl donors alters tubulin polymerization activity Chem. Res. Toxicol. 20 2007 1693 1700 (Pubitemid 350275615)
25. C.C. Winterbourn, and S.O. Brennan Characterization of the oxidation products of the reaction between reduced glutathione and hypochlorous acid Biochem. J. 326 1997 87 92 (Pubitemid 27386921)
26. T. Miron, A. Rabinkov, D. Mirelman, L. Weiner, and M. Wilchek A spectrophotometric assay for allicin and alliinase (alliin lyase) activity: reaction of 2-nitro-thiobenzoate with thiosulfinates Anal. Biochem. 265 1998 317 325 (Pubitemid 29002078)
27. L.M. Landino, C.B. Mall, J.J. Nicklay, S.K. Dutcher, and K.L. Moynihan Oxidation of 5-thio-2-nitrobenzoic acid by the biologically relevant oxidants peroxynitrite anion, hydrogen peroxide and hypochlorous acid Nitric Oxide 18 2008 11 18 (Pubitemid 350299199)
28. E.L. Thomas, M.B. Grisham, and M.M. Jefferson Preparation and characterization of chloramines Meth. Enzymol. 132 1986 569 585 (Pubitemid 17233604)
29. J.S. Beckman, J. Chen, H. Ischiropoulos, and J.P. Crow Oxidative chemistry of peroxynitrite Meth. Enzymol. 233 1994 229 240 (Pubitemid 24177546)
30. R.C. Williams, and J.C. Lee Preparation of tubulin from brain Meth. Enzymol. 85 1982 376 385
31. P.W. Riddles, R.L. Blakeley, and B. Zerner Reassessment of Ellmans reagent Meth. Enzymol. 91 1983 49 60
32. N.R. Stanley, D.I. Pattison, and C.L. Hawkins Ability of hypochlorous acid and N-chloramines to chlorinate DNA and its constituents Chem. Res. Toxicol. 23 2010 1293 1302
33. C.L. Hawkins, and M.J. Davies Hypochlorite-induced damage to nucleosides: formation of chloramines and nitrogen-centered radicals Chem. Res. Toxicol. 14 2001 1071 1081 (Pubitemid 32800163)
34. F.R.N. Gurd Carboxymethylation Meth. Enzymol. 11 1967 532 541
35. P.J. Britto, L. Knipling, and J. Wolff The local electrostatic environment determines cysteine reactivity of tubulin J. Biol. Chem. 277 2002 29018 29027
36. P.J. Britto, L. Knipling, P. McPhie, and J. Wolff Thiol-disulphide interchange in tubulin: kinetics and the effect on polymerization Biochem. J. 389 2005 549 558 (Pubitemid 41021158)
37. R. Radi, J.S. Beckman, K.M. Bush, and B.A. Freeman Peroxynitrite oxidation of sulfhydryls J. Biol. Chem. 266 1991 4244 4250
38. A.L.P. Chapman, C.C. Winterbourn, S.O. Brennan, T.W. Jordan, and A.J. Kettle Characterization of non-covalent oligomers of proteins treated with hypochlorous acid Biochem. J. 375 2003 33 40 (Pubitemid 37255379)
39. J. Lowe, H. Li, K.H. Downing, and E. Nogales Refined structure of αβ-tubulin at 3.5 A resolution J. Mol. Biol. 313 2001 1045 1057 (Pubitemid 33081900)
40. L.M. Landino, T.E. Skreslet, and J.A. Alston Cysteine oxidation of tau and microtubule-associated protein-2 by peroxynitrite: modulation of microtubule assembly kinetics by the thioredoxin reductase system J. Biol. Chem. 279 2004 35101 35105 (Pubitemid 39318146)
41. L.M. Landino Protein thiol modification by peroxynitrite anion and nitric oxide donors Meth. Enzymol. 440 2008 95 109
42. I. Dalle-Donne, R. Rossi, D. Giustarini, N. Gagliano, P. Di Simplicio, R. Colombo, and A. Milzani Methionine oxidation as the major cause of the functional impairment of oxidized actin Free Radic. Biol. Med. 32 2002 927 937 (Pubitemid 34439264)
43. K.M. Miranda, N. Paolocci, T. Katori, D.D. Thomas, E. Ford, M.D. Bartberger, M.G. Espey, D.A. Kass, J.M. Fukuto, and D.A. Wink A biochemical rationale for the discrete behavior of nitroxyl and nitric oxide in the cardiovascular system Proc. Natl Acad. Sci. USA 100 2003 9197 9201
44. R.F. Luduena Multiple forms of tubulin: different gene products and covalent modifications Int. Rev. Cytol. 178 1998 207 275 (Pubitemid 128717548)
45. P.G. McKean, S. Vaughan, and K. Gull The extended tubulin superfamily J. Cell Sci. 114 2001 2723 2733 (Pubitemid 32785452)