A ditryptophan cross-link is responsible for the covalent dimerization of human superoxide dismutase 1 during its bicarbonate-dependent peroxidase activity

Free Radical Biology and Medicine

Volumn 49, Issue 6, 2010, Pages 1046-1053

  Medinas, Danilo B ^a   Gozzo, Fabio C ^b   Santos, Luiz F A ^b   Iglesias, Amadeu H ^b   Augusto, Ohara ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF CAMPINAS   (Brazil)

Author keywords

Carbonate radical; Ditryptophan; Free radicals; Neurodegenerative diseases; Peroxidase activity; Protein cross link; Superoxide dismutase 1

Indexed keywords

BICARBONATE; COPPER ZINC SUPEROXIDE DISMUTASE; DIMER; DITRYPTOPHAN; PEROXIDASE; TETRAMER; TRYPSIN; TRYPTOPHAN; UNCLASSIFIED DRUG; WATER;

ARTICLE; COVALENT BOND; CROSS LINKING; DIMERIZATION; ENZYME ACTIVITY; ENZYME MECHANISM; HUMAN; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN MODIFICATION; TANDEM MASS SPECTROMETRY; ULTRAVIOLET RADIATION; ULTRAVIOLET SPECTROSCOPY;

EID: 77955515375     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2010.06.018     Document Type: Article

References (54)

1. Davies M.J., Dean R.T. Radical-Mediated Protein Oxidation: from Chemistry to Medicine 1997, Oxford Univ. Press, Oxford/New York.
2. Rhee S.G., Chae H.Z., Kim K. Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic. Biol. Med. 2005, 38:1543-1552.
3. Winterbourn C.C., Hampton M.B. Thiol chemistry and specificity in redox signaling. Free Radic. Biol. Med. 2008, 45:549-561.
4. Berlett B.S., Stadtman E.R. Protein oxidation in aging, disease, and oxidative stress. J. Biol. Chem. 1997, 272:20313-20316.
5. Davies M.J., Fu S., Wang H., Dean R.T. Stable markers of oxidant damage to proteins and their application in the study of human disease. Free Radic. Biol. Med. 1999, 27:1151-1163.
6. Stadtman E.R. Protein oxidation in aging and age-related diseases. Ann. NY Acad. Sci. 2001, 928:22-38.
7. Dalle-Donne I., Rossi R., Colombo R., Giustarini D., Milzani A. Biomarkers of oxidative damage in human disease. Clin. Chem. 2006, 52:601-623.
8. Alvarez B., Radi R. Peroxynitrite reactivity with amino acids and proteins. Amino Acids 2003, 25:295-311.
9. Yamakura F., Ikeda K. Modification of tryptophan and tryptophan residues in proteins by reactive nitrogen species. Nitric Oxide 2006, 14:152-161.
10. Vaz S.M., Prado F.M., Di Mascio P., Augusto O. Oxidation and nitration of ribonuclease and lysozyme by peroxynitrite and myeloperoxidase. Arch. Biochem. Biophys. 2009, 484:127-133.
11. Rebrin I., Bregere C., Gallaher T.K., Sohal R.S. Detection and characterization of peroxynitrite-induced modifications of tyrosine, tryptophan, and methionine residues by tandem mass spectrometry. Methods Enzymol. 2008, 441:283-294.
12. Shringarpure R., Davies K.J. Protein turnover by the proteasome in aging and disease. Free Radic. Biol. Med. 2002, 32:1084-1089.
13. Grune T., Jung T., Merker K., Davies K.J. Decreased proteolysis caused by protein aggregates, inclusion bodies, plaques, lipofuscin, ceroid, and 'aggresomes' during oxidative stress, aging, and disease. Int. J. Biochem. Cell Biol. 2004, 36:2519-2530.
14. Sayre L.M., Perry G., Smith M.A. Oxidative stress and neurotoxicity. Chem. Res. Toxicol. 2008, 21:172-188.
15. Fu X., Kao J.L., Bergt C., Kassim S.Y., Huq N.P., d'Avignon A., Parks W.C., Mecham R.P., Heinecke J.W. Oxidative cross-linking of tryptophan to glycine restrains matrix metalloproteinase activity: specific structural motifs control protein oxidation. J. Biol. Chem. 2004, 279:6209-6212.
16. Zhao H., Sun C., Stewart R.J., Waite J.H. Cement proteins of the tube-building polychaete Phragmatopoma californica. J. Biol. Chem. 2005, 280:42938-42944.
17. Shen H.-R., Spikes J.D., Kopeceková P., Kopecek J. Photodynamic crosslinking of proteins. I. Models studies using histidine- and lysine-containing N-(2-hydroxypropyl)methacrylamide copolymers. J. Photochem. Photobiol. B Biol. 1996, 34:206-210.
18. Shen H.-R., Spikes J.D., Smith C.J., Kopecek J. Photodynamic cross-link of proteins. IV. Nature of the His-His bond(s) formed in the rose bengal-photosensitized cross-linking of N-benzoyl-L-histidine. J. Photochem. Photobiol. A Chem. 2000, 130:1-6.
19. Zhang H., Andrekopoulos C., Joseph J., Chandran K., Karoui H., Crow J.P., Kalyanaraman B. Bicarbonate-dependent peroxidase activity of human Cu,Zn-superoxide dismutase induces covalent aggregation of protein: intermediacy of tryptophan-derived oxidation products. J. Biol. Chem. 2003, 278:24078-24089.
20. Zhang H., Andrekopoulos C., Joseph J., Crow J.P., Kalyanaraman B. The carbonate radical anion-induced covalent aggregation of human copper, zinc superoxide dismutase, and α-synuclein: intermediacy of tryptophan- and tyrosine-derived oxidation products. Free Radic. Biol. Med. 2004, 36:1355-1365.
21. Zhang H., Joseph J., Crow J.P., Kalyanaraman B. Mass spectral evidence for carbonate-anion-radical-induced posttranslational modification of tryptophan to kynurenine in human Cu,Zn superoxide dismutase. Free Radic. Biol. Med. 2004, 37:2018-2026.
22. Ehrenshaft M., Silva S.O., Perdivara I., Bilski P., Sik R.H., Chignell C.F., Tomer K.B., Mason R.P. Immunological detection of N-formylkynurenine in oxidized proteins. Free Radic. Biol. Med. 2009, 46:1260-1266.
23. Medinas D.B., Toledo J.C., Cerchiaro G., do-Amaral A.T., de-Rezende L., Malvezzi A., Augusto O. Peroxymonocarbonate and carbonate radical displace the hydroxyl-like oxidant in the Sod1 peroxidase activity under physiological conditions. Chem. Res. Toxicol. 2009, 22:639-648.
24. Aquilina J.A., Carver J.A., Truscott R.J. Polypeptide modification and cross-linking by oxidized 3-hydroxykynurenine. Biochemistry 2000, 39:16176-16184.
25. Vazquez S., Aquilina J.A., Jamie J.F., Sheil M.M., Truscott R.J. Novel protein modification by kynurenine in human lenses. J. Biol. Chem. 2002, 277:4867-4873.
26. Johnston J.A., Dalton M.J., Gurney M.E., Kopito R.R. Formation of high molecular weight complexes of mutant Cu, Zn-superoxide dismutase in a mouse model for familial amyotrophic lateral sclerosis. Proc. Natl Acad. Sci. USA 2000, 97:12571-12576.
27. Obata Y., Niikura T., Kanekura K., Hashimoto Y., Kawasumi M., Kita Y., Aiso S., Matsuoka M., Nishimoto I. Expression of N19S-SOD1, an SOD1 mutant found in sporadic amyotrophic lateral sclerosis patients, induces low-grade motoneuronal toxicity. J. Neurosci. Res. 2005, 81:720-729.
28. Choi J., Rees H.D., Weintraub S.T., Levey A.I., Chin L.S., Li L. Oxidative modifications and aggregation of Cu,Zn-superoxide dismutase associated with Alzheimer and Parkinson diseases. J. Biol. Chem. 2005, 280:11648-11655.
29. Taylor D.M., Gibbs B.F., Kabashi E., Minotti S., Durham H.D., Agar J.N. Tryptophan 32 potentiates aggregation and cytotoxicity of a copper/zinc superoxide dismutase mutant associated with familial amyotrophic lateral sclerosis. J. Biol. Chem. 2007, 282:16329-16335.
30. Shaw B.F., Valentine J.S. How do ALS-associated mutations in superoxide dismutase 1 promote aggregation of the protein?. Trends Biochem. Sci. 2007, 32:78-85.
31. Gruzman A., Wood W.L., Alpert E., Prasad M.D., Miller R.G., Rothstein J.D., Bowser R., Hamilton R., Wood T.D., Cleveland D.W., Lingappa V.R., Liu J. Common molecular signature in SOD1 for both sporadic and familial amyotrophic lateral sclerosis. Proc. Natl Acad. Sci. USA 2007, 104:12524-12529.
32. Tang X., Munske G.R., Siems W.F., Bruce J.E. Mass spectrometry identifiable cross-linking strategy for studying protein-protein interactions. Anal. Chem. 2005, 77:311-318.
33. Huyett J.E., Doan P.E., Gurbiel R., Houseman A.L.P., Sivaraja M., Goodin D.B., Hoffman B.M. Compound ES of cytochrome-c peroxidase contains a Trp pi-cation radical: characterization by continuous wave and pulsed Q-band external nuclear double resonance spectroscopy. J. Am. Chem. Soc. 1995, 117:9033-9041.
34. Walden S.E., Wheeler R.A. Distinguishing features of indolyl radical and radical cation: implications for tryptophan radical studies. J. Phys. Chem. 1996, 100:1530-1535.
35. Connor H.D., Sturgeon B.E., Mottley C., Sipe H.J., Mason R.P. L-tryptophan radical cation electron spin resonance studies: connecting solution-derived hyperfine coupling constants with protein spectral interpretations. J. Am. Chem. Soc. 2008, 130:6381-6387.
36. Domingues M.R.M., Domingues P., Reis A., Fonseca C., Amado F.M., Ferrer-Correia A.J. Identification of oxidation products and free radicals of tryptophan by mass spectrometry. J. Am. Soc. Mass Spectrom. 2003, 14:406-416.
37. Augusto O., Bonini M.G., Amanso A.M., Linares E., Santos C.C., de Menezes S.L. Nitrogen dioxide and carbonate radical anion: two emerging radicals in biology. Free Radic. Biol. Med. 2002, 32:841-859.
38. Yamakura F., Matsumoto T., Fujimura T., Taka H., Murayama K., Imai T., Uchida K. Modification of a single tryptophan residue in human Cu,Zn-superoxide dismutase by peroxynitrite in the presence of bicarbonate. Biochim. Biophys. Acta 2001, 1548:38-46.
39. Yamakura F., Matsumoto T., Ikeda K., Taka H., Fujimura T., Murayama K., Watanabe E., Tamaki M., Imai T., Takamori K. Nitrated and oxidized products of a single tryptophan residue in human Cu, Zn-superoxide dismutase treated with either peroxynitrite-carbon dioxide or myeloperoxidase-hydrogen peroxide-nitrite. J. Biochem. 2005, 138:57-69.
40. Bonini M.G., Radi R., Ferrer-Sueta G., Ferreira A.M., Augusto O. Direct EPR detection of the carbonate radical anion produced from peroxynitrite and carbon dioxide. J. Biol. Chem. 1999, 274:10802-10806.
41. Bonini M.G., Miyamoto S., Di Mascio P., Augusto O. Production of the carbonate radical anion during xanthine oxidase turnover in the presence of bicarbonate. J. Biol. Chem. 2004, 279:51836-51843.
42. Ramirez D.C., Mejiba S.E., Mason R.P. Copper-catalyzed protein oxidation and its modulation by carbon dioxide: enhancement of protein radicals in cells. J. Biol. Chem. 2005, 280:27402-27411.
43. Arai H., Berlett B.S., Chock P.B., Stadtman E.R. Effect of bicarbonate on iron-mediated oxidation of low-density lipoprotein. Proc. Natl Acad. Sci. USA 2005, 102:10472-10477.
44. Stadtman E.R., Arai H., Berlett B.S. Protein oxidation by the cytochrome P450 mixed-function oxidation system. Biochem. Biophys. Res. Commun. 2005, 338:432-436.
45. 2 in cobalt-catalyzed peroxidations. Arch. Biochem. Biophys. 2005, 439:99-104.
46. Alvarez M.N., Peluffo G., Folkes L., Wardman P., Radi R. Reaction of the carbonate radical with the spin trap 5, 5-dimethyl-1-pyrroline-N-oxide in chemical and cellular systems: pulse radiolysis, electron paramagnetic resonance, and kinetic-competition studies. Free Radic. Biol. Med. 2007, 43:1523-1533.
47. Ferrer-Sueta G., Radi R. Chemical biology of peroxynitrite: kinetics, diffusion, and radicals. ACS Chem. Biol. 2009, 4:161-177.
48. Lushchak O.V., Bayliak M.M., Korobova O.V., Levine R.L., Lushchak V.I. Buffer modulation of menadione-induced oxidative stress in Saccharomyces cerevisiae. Redox Rep. 2009, 14:214-220.
49. Barbosa L.F., Cerqueira F.M., Macedo A.F., Garcia C.C., Angeli J.P., Schumacher R.I., Sogayar M.C., Augusto O., Carrì M.T., Di Mascio P., Medeiros M.H. Increased SOD1 association with chromatin, DNA damage, p53 activation, and apoptosis in a cellular model of SOD1-linked ALS. Biochim. Biophys. Acta 2010, 1802:462-471.
50. Medinas D.B., Cerchiaro G., Trindade D.F., Augusto O. The carbonate radical and related oxidants derived from bicarbonate buffer. IUBMB Life 2007, 59:255-262.
51. Xie Y., Cohen J.B. Contributions of torpedo nicotinic acetylcholine receptor gamma Trp-55 and delta Trp-57 to agonist and competitive antagonist function. J. Biol. Chem. 2001, 276:2417-2426.
52. Ramakrishnan B., Boeggeman E., Qasba P.K. β-1, 4-Galactosyltransferase and lactose synthase: molecular mechanical devices. Biochem. Biophys. Res. Commun. 2002, 291:1113-1118.
53. Huntley J.J., Fast W., Benkovic S.J., Wright P.E., Dyson H.J. Role of a solvent-exposed tryptophan in the recognition and binding of antibiotic substrates for a metallo-beta-lactamase. Protein Sci. 2003, 12:1368-1375.
54. Madabushi S., Gross A.K., Philippi A., Meng E.C., Wensel T.G., Lichtarge O. Evolutionary trace of G protein-coupled receptors reveals clusters of residues that determine global and class-specific functions. J. Biol. Chem. 2004, 279:8126-8132.