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 Radical Biology and Medicine

Volumn 36, Issue 11, 2004, Pages 1355-1365

  Zhang, Hao ^a   Andrekopoulos, Christopher ^a   Joseph, Joy ^a   Crow, John ^b   Kalyanaraman, B ^a  

^a FREE RADICAL RESEARCH CENTER   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

3,5 dibromo 4 nitrosobenzenesulfonic acid; 5,5 dimethyl 1 pyrroline N oxide; ALS; amyotrophic lateral sclerosis; bovine copper, zinc superoxide dismutase; bSOD1; Co complex; DBNBS; DMPO; ESR; pentammine carbonato complex of Co(III)

Indexed keywords

ALPHA SYNUCLEIN; ANION; BICARBONATE; CARBONIC ACID; COPPER; KYNURENINE; OXIDIZING AGENT; PEROXIDASE; RADICAL; SUPEROXIDE DISMUTASE; TRYPTOPHAN; TYROSINE;

CHEMICAL REACTION; COVALENT BOND; CROSS LINKING; CYTOTOXICITY; DIFFUSION; ELECTRON SPIN RESONANCE; ENZYME ACTIVITY; OXIDATION; PRIORITY JOURNAL; REVIEW; SPIN TRAPPING; SYNTHESIS;

ALPHA-SYNUCLEIN; CARBONATES; FREE RADICALS; HUMANS; MONOPHENOL MONOOXYGENASE; NERVE TISSUE PROTEINS; OXIDATION-REDUCTION; SUPEROXIDE DISMUTASE; SYNUCLEINS; TRYPTOPHAN;

BOVINAE;

EID: 2342626577     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2004.02.038     Document Type: Review

References (66)

1. Price D.L., Cleveland D.W., Koliatsos V.E. Motor neuron disease and animal models. Neurobiol. Dis. 1:1994;3-11
2. Rosen D.R., Siddique T., Patterson D., Figlewicz D.A., Sapp P., Hentati A., Donaldson D., Goto J., O'Regan J.P., Deng H.X., Rahmani Z., Krizus A., McKenna-Yasek D., Cayabyab A., Gaston S., Berger M., Ranzi R.E., Halperin J.J., Herzfeldt B., Van den Bergh R., Hung W.Y., Bird T., Deng G., Mulder D.W., Smyth C., Laing N.G., Soriano E., Pericak-Vance M.A., Haines J., Rouleau G.A., Gusella J.S., Horvitz H.R., Brown R.H. Jr. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature. 362:1993;59-62
3. Bruijn L.I., Cleveland D.W. Mechanisms of selective motor neuron death in ALS: insights from transgenic mouse models of motor neuron disease. Neuropathol. Appl. Neurobiol. 22:1996;373-387
4. Brown R.H. Jr. Amyotrophic lateral sclerosis: recent insights from genetics and transgenic mice. Cell. 80:1995;687-692
5. Deng H.X., Hentati A., Tainer J.A., Iqbal Z., Cayabyab A., Hung W.Y., Getzoff E.D., Ping H., Herzfeldt B., Roos R.P., Warner C., Deng G., Soriano E., Smyth C., Parge H.E., Ahmed A., Roses A.D., Hallewell R.A., Pericak-Vance M.A., Siddique T. Amyotrophic lateral sclerosis and structural defects in Cu, Zn superoxide dismutase. Science. 261:1993;1047-1051
6. Siddique T. ALS: molecular clues to the jigsaw puzzle of neuronal degeneration. Cold Spring Harbor Symp. Quan. Biol. 61:1996;699-708
7. Smith R.G., Appel S.H. Molecular approaches to amyotrophic lateral sclerosis. Annu. Rev. Med. 46:1995;133-145
8. Rowland L.P. Amyotrophic lateral sclerosis: human challenge for neuroscience. Proc. Natl. Acad. Sci. USA. 92:1995;1251-1253
9. Siddique T., Figlewicz D.A., Pericak-Vance M.A., Haines J.L., Rouleau G., Jeffers A.J., Sapp P., Hung W.Y., Bebout J., McKenna-Yasek D., Deng G., Horvitz H.R., Gusella J.F., Brown R.H. Jr., Roses A.D., et al. Linkage of a gene causing familial amyotrophic lateral sclerosis to chromosome 21 and evidence of genetic locus heterogeneity. N. Engl. J. Med. 324:1991;1381-1384
10. Wong P.C., Pardo C.A., Borchelt D.R., Lee M.K., Copeland N.G., Jenkins N.A., Sisodia S.S., Cleveland D.W., Price D.L. An adverse property of a familial ALS-linked Sod1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron. 14:1995;1105-1116
11. Brown R.H. Jr. Superoxide dismutase and familial amyotrophic sclerosis: new insights into mechanisms and treatments. Ann. Neurol. 39:1996;145-146
12. Rosen D.R., Bowling A.C., Patterson D., Usdin T.B., Sapp P., Mezey E., Mekenna-Yasek D., O'Regan J., Rahmani Z., Ferrante R.J., et al. A frequent Ala 4 to Val superoxide dismutase is associated with a rapidly progressive familial amyotrophic lateral sclerosis. Hum. Mol. Genet. 51:1994;61-69
13. Beckman J.S., Carson M., Smith C.D., Koppenol W.H. ALS, SOD and peroxynitrite. Nature. 364:1993;584
14. Lyons T.J., Liu H., Goto J.J., Nersissian A., Roe J.A., Graden J.A., Cafe C., Ellerby L.M., Bredesen D.E., Gralla E.B., Valentine J.S. Mutations in copper-zinc superoxide dismutase that cause amyotrophic lateral sclerosis alter the zinc binding site and the redox behavior of the protein. Proc. Natl. Acad. Sci. USA. 93:1996;12240-12244
15. Borchelt D.R., Lel M.K., Slunt H.S., Guarnieri M., Xu Z.-S., Wong P.C., Brown R.H. Jr., Price D.L., Sisodia S.S., Cleveland D.W. Superoxide dismutase 1 with mutations linked to familial amyotrophic lateral sclerosis possesses significant activity. Proc. Natl. Acad. Sci. USA. 91:1994;8292-8296
16. Ripps M.E., Huntley G.W., Hof P.R., Morrison J.H., Gordon J.W. Transgenic mice expressing an altered murine superoxide dismutase gene provide an animal model of amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. USA. 92:1995;689-693
17. Rabizadeh S., Gralla E.B., Borchelt D.R., Gwinn R., Valentine J.S., Sisodia S., Wong P., Lee M., Hahn H., Bredesen D.E. Mutations associated with amyotrophic lateral sclerosis convert superoxide dismutase from an antiapoptotic gene to a proapoptotic gene: studies in yeast and neural cells. Proc. Natl. Acad. Sci. USA. 92:1995;3024-3028
18. Wiedau-Pazos M., Goto J.J., Rabizadeh S., Gralla E.B., Roe J.A., Lee M.K., Valentine J.S., Bredesen D.E. Altered reactivity of superoxide dismutase in familial amyotrophic lateral sclerosis. Science. 271:1996;515-518
19. m for hydrogen peroxide. Proc. Natl. Acad. Sci. USA. 93:1996;5709-5714
20. Volterra A., Trotti D., Tromba C., Floridi S., Racagni G. Glutamate uptake inhibition by oxygen free radicals in rat cortical astrocytes. J. Neurosci. 14:1994;2924-2932
21. Bredesen D.E., Wiedau-Pazos M., Goto J.J., Rabizadeh S., Roe J.A., Gralla E.B., Ellerby L.M., Valentine J.S. Cell death mechanisms in ALS. Neurology. 47(Suppl. 2):1996;S36-S39
22. Simonian N.A., Coyle J.T. Oxidative stress in neurodegenerative diseases. Annu. Rev. Pharmacol. Toxicol. 36:1996;83-106
23. Gurney M.E., Cutting F.B., Zhai P., Doble A., Taylor C.P., Andrus P.K., Hall E.D. Benefit of vitamin E, riluzole, and gabapentin in a transgenic model of familial amyotrophic lateral sclerosis. Ann. Neurol. 39:1996;147-157
24. Hall E.D., Oostveen J.A., Andrus P.K., Anderson D.K., Thomas C.E. Immunocytochemical method for investigating in vivo neuronal oxygen radical-induced lipid peroxidation. J. Neurosci. Methods. 76:1997;115-122
25. Bowling A.C., Schulz J.B., Brown R.H., Beal M.F. Superoxide dismutase activity, oxidative damage, and mitochondrial energy metabolism in familial and sporadic amyotrophic lateral sclerosis. J. Neurochem. 61:1993;2322-2325
26. Bruijn L.I., Beal M.F., Becher M.W., Schulz J.B., Wong P.C., Price D.L., Cleveland D.W. Elevated free nitrotyrosine levels, but not protein-bound nitrotyrosine or hydroxyl radicals, throughout amyotrophic lateral sclerosis (ALS)-like disease implicate tyrosine nitration as an aberrant in vivo property of one familial ALS-linked superoxide dismutase 1 mutant. Proc. Natl. Acad. Sci. USA. 94:1997;7606-7611
27. Ferrante R.J., Shinobu L.A., Schultz J.B., Matthews R.T., Thomas C.E., Kowall N.W., Gurney M.E., Beal M.F. Increased 3-nitrotyrosine and oxidative damage in mice with a human Cu, Zn superoxide dismutase mutation. Ann. Neurol. 42:1997;326-334
28. Taylor J.P., Hardy J., Fischbeck K.H. Toxic proteins in neurodegenerative disease. Science. 296:2002;1991-1995
29. Shibata N., Hirano A., Kobayashi M., Siddique T., Deng H.X., Hung W.Y., Kato T., Asayama K. Intense superoxide dismutase-1 immunoreactivity in intracytoplasmic hyaline inclusions of familial amyotrophic lateral sclerosis with posterior column involvement. J. Neuropathol. Exp. Neurol. 55:1996;481-490
30. Bruijn L.I., Becher M.W., Lee M.K., Anderson K.L., Jenkins N.A., Copeland N.G., Sisodia S.S., Rothstein J.D., Borchelt D.R., Price D.L., Cleveland D.W. ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron. 18:1997;327-338
31. Watanabe M., Dykes-Hoberg M., Culotta V.C., Price D.L., Wong P.C., Rothstein J.D. Histological evidence of protein aggregation in mutant SOD1 transgenic mice and in amyotrophic lateral sclerosis neural tissues. Neurobiol. Dis. 8:2001;933-941
32. Julien J.P. Amyotrophic lateral sclerosis. unfolding the toxicity of the misfolded. Cell. 104:2001;581-591
33. Cleveland D.W., Liu J. Oxidation versus aggregation: how do SOD1 mutants cause ALS? Nat. Med. 6:2000;1320-1321
34. Urushitani M., Kurisu J., Tsukita K., Takahashi R. Proteasomal inhibition by misfolded mutant superoxide dismutase 1 induces selective motor neuron death in familial amyotrophic lateral sclerosis. J. Neurochem. 83:2002;1030-1042
35. Vleminckx V.Van, Damme P., Goffin K., Delye H., Van Den Bosch L., Robberecht W. Upregulation of HSP27 in a transgenic model of ALS. J. Neuropathol. Exp. Neurol. 61:2002;968-974
36. Okado-Matsumoto A., Fridovich I. Amyotrophic lateral sclerosis: a proposed mechanism. Proc. Natl. Acad. Sci. USA. 99:2002;9010-9014
37. 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. 97:2000;12571-12576
38. Valentine J.S. Do oxidatively modified proteins cause ALS? Free Radic. Biol. Med. 33:2002;1314-1320
39. Hodgson E.K., Fridovich I. The mechanism of the activity-dependent luminescence of xanthine oxidase. Arch. Biochem. Biophys. 172:1976;202-205
40. Liochev S.I., Fridovich I. On the role of bicarbonate in peroxidations catalyzed by Cu, Zn superoxide dismutase. Free Radic. Biol. Med. 27:1999;1444-1447
41. Goss S.P.A., Singh R.J., Kalyanaraman B. Bicarbonate enhances the peroxidase activity of Cu, Zn-superoxide dismutase: role of carbonate anion radical. J. Biol. Chem. 274:1999;28233-28239
42. Zhang H., Joseph J., Gurney M., Becker D., Kalyanaraman B. Bicarbonate enhances peroxidase activity of Cu, Zn-superoxide dismutase: role of carbonate anion radical and scavenging of carbonate anion radical by metalloporphyrin antioxidant enzyme mimetics. J. Biol. Chem. 277:2002;1013-1020
43. Parge H.E., Hallewell R.A., Tainer J.A. Atomic structures of wild-type and thermostable mutant recombinant human Cu, Zn superoxide dismutase. Proc. Natl. Acad. Sci. USA. 89:1992;6109-6113
44. Hodgson E.K., Fridovich I. The interaction of bovine erythrocyte superoxide dismutase with hydrogen peroxide: inactivation of the enzyme. Biochemistry. 14:1975;5294-5298
45. Hodgson E.K., Fridovich I. The interaction of bovine erythrocyte superoxide dismutase with hydrogen peroxide: chemiluminescence and peroxidation. Biochemistry. 14:1975;5299-5303
46. Said Ahmed M., Hung W.Y., Zu J.S., Hockberger P., Siddique T. Increased reactive oxygen species in familial amyotrophic lateral sclerosis with mutations in SOD1. J. Neurol. Sci. 176:2000;88-94
47. Ciriolo M.R., De Martino A., Lafavia E., Rossi L., Carri M.T., Rotilio G. Cu, Zn-superoxide dismutase-dependent apoptosis induced by nitric oxide in neuronal cells. J. Biol. Chem. 275:2000;5065-5072
48. 2. J. Biol. Chem. 277:2002;34674-34678
49. 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. 274:1999;10802-10806
50. Zhang H., Andrekopoulos C., Joseph J., Chandran K., Karoui H., Crow J.P., Kalyanaraman B. Bicarbonate dependent peroxidase activity of human copper, zinc superoxide dismutase induces covalent aggregation of protein: intermediacy of tryptophan-derived oxidation products. J. Biol. Chem. 278:2003;24078-24089
51. Stachel S.J., Habeeb R.L., Van Vranken D.A. Formation of constrained, fluorescent peptides via tryptophan dimerization and oxidation. J. Am. Chem. Soc. 118:1996;1225-1226
52. Aquilina J.A., Carver J.A., Truscott R.J. Polypeptide modification and crosslinking by oxidized 3-hydroxykynurenine. Biochemistry. 39:2000;16176-16184
53. Aquilina J.A., Carver J.A., Truscott R.J. Elucidation of a novel polypeptide cross-link involving 3-hydroxykynurenine. Biochemistry. 38:1999;11455-11464
54. Gunther M.R., Kelman D.J., Corbett J.T., Mason R.P. Self-peroxidation of metmyoglobin results in formation of an oxygen-reactive tryptophan-centered radical. J. Biol. Chem. 270:1995;16075-16081
55. Giasson B.I., Duda J.E., Murray I.V., Chen Q., Souza J.M., Hurtig H.I., Ischiropoulos H., Trojanowski J.Q., Lee V.M. Oxidative damage linked to neurodegeneration by selective alpha-synuclein nitration in synucleinopathy lesions. Science. 290:2000;985-989
56. Souza J.M., Giasson B.I., Chen Q., Lee V.M., Ischiropoulos H. Dityrosine crosslinking promotes formation of stable alpha-synuclein polymers: implication of nitrative and oxidative stress in the pathogenesis of neurodegenerative synucleinopathies. J. Biol. Chem. 275:2000;18344-19349
57. Kruger R., Muller T., Riess O. Involvement of alpha-synuclein in Parkinson's disease and other neurodegenerative disorders. J. Neural. Transm. 107:2000;31-40
58. Kim K.S., Choi S.Y., Kwon H.Y., Won M.H., Kang T.C., Kang J.H. Aggregation of alpha-synuclein induced by the Cu, Zn-superoxide dismutase and hydrogen peroxide system. Free Radic. Biol. Med. 32:2002;544-550
59. Kang J.H., Kim K.S. Enhanced oligomerization of the alpha-synuclein mutant by the Cu, Zn-superoxide dismutase and hydrogen peroxide system. Mol. Cells. 15:2003;87-93
60. Andrekopoulos C., Zhang H., Joseph J., Kalivendi S., Kalyanaraman B. Bicarbonate enhances α-synuclein oligomerization and nitration: intermediacy of carbonate radical anion and nitrogen dioxide radical. Biochem. J. 378:2004;435-447
61. Zhang H., Joseph J., Felix C., Kalyanaraman B. Bicarbonate enhances the hydroxylation, nitration, and peroxidation reactions catalyzed by copper, zinc superoxide dismutase: intermediacy of carbonate anion radical. J. Biol. Chem. 275:2000;14038-14045
62. Liu R., Li B., Flanagan S.W., Oberley L.W., Gozal D., Qiu M. Increased mitochondrial antioxidative activity or decreased oxygen free radical propagation prevent mutant SOD1-mediated motor neuron cell death and increase amyotrophic lateral sclerosis-like transgenic mouse survival. J. Neurochem. 80:2002;488-500
63. Liochev S.I., Fridovich I. Mutant Cu, Zn superoxide dismutases and familial amyotrophic lateral sclerosis: evaluation of oxidative hypotheses. Free Radic. Biol. Med. 34:2003;1383-1389
64. Shipp E.L., Cantini F., Bertini I., Valentine J.S., Banci L. Dynamic properties of the G93A mutant of copper-zinc superoxide dismutase as detected by NMR spectroscopy: implications for the pathology of familial amyotrophic lateral sclerosis. Biochemistry. 42:2003;1890-1899
65. Winterbourn C.C., Peskin A.V., Parsons-Mair H.N. Thiol oxidase activity of copper, zinc superoxide dismutase. J. Biol. Chem. 277:2002;1906-1911
66. 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. 1548:2001;38-46