Peroxidative aggregation of α-synuclein requires tyrosines

Protein Science

Volumn 13, Issue 11, 2004, Pages 2852-2856

  Olteanu, Alina ^a   Pielak, Gary J ^a,b,c  

^a University of North Carolina at Chapel Hill   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

synuclein; Aggregation; Lewy bodies; Oxidative stress; Parkinson's disease; Tyrosine

Indexed keywords

ALPHA SYNUCLEIN; CYTOCHROME C; HYDROGEN PEROXIDE; TYROSINE DERIVATIVE;

ARTICLE; HUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; PEROXIDATION; PRIORITY JOURNAL; PROTEIN AGGREGATION;

ALPHA-SYNUCLEIN; CYTOCHROMES C; DIMERIZATION; HUMANS; HYDROGEN PEROXIDE; NERVE TISSUE PROTEINS; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES; SYNUCLEINS; TYROSINE;

EID: 7244253283     PISSN: 09618368     EISSN: None     Source Type: Journal    
DOI: 10.1110/ps.04947204     Document Type: Article

References (32)

1. Atwood, C.S., Perry, G., Zeng, H., Kato, Y., Jones, W.D., Ling, K.Q., Huang, X., Moir, R.D., Wang, D., Sayre, L.M., et al. 2004. Copper mediates dityrosine cross-linking of Alzheimer's amyloid-β. Biochemistry 43: 560-568.
2. Barr, D.P., Gunther, M.R., Deterding, L.J., Tomer, K.B., and Mason, R.P. 1996. ESR spin-trapping of a protein-derived tyrosyl radical from the reaction of cytochrome c with hydrogen peroxide. J. Biol. Chem. 271: 15498-15503.
3. Berlett, B.S. and Stadtman, E.R. 1997. Protein oxidation in aging, disease, and oxidative stress. J. Biol. Chem. 272: 20313-20316.
4. Boveris, A. and Chance, B. 1973. The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem. J. 134: 707-716.
5. Boveris, A., Oshino, N., and Chance, B. 1972. The cellular production of hydrogen peroxide. Biochem. J. 128: 617-630.
6. Chen, Y.R., Deterding, L.J., Sturgeon, B.E., Tomer, K.B., and Mason, R.P. 2002. Protein oxidation of cytochrome c by reactive halogen species enhances its peroxidase activity. J. Biol. Chem. 277: 29781-29791.
7. Davidson, W.S., Jonas, A., Clayton, D.F., and George, J.M. 1998. Stabilization of α-synuclein secondary structure upon binding to synthetic membranes. J. Biol. Chem. 273: 9443-9449.
8. Deterding, L.J., Barr, D.P., Mason, R.P., and Tomer, K.B. 1998. Characterization of cytochrome c free radical reactions with peptides by mass spectrometry. J. Biol. Chem. 273: 12863-12869.
9. Erman, J.E. and Vitello, L.B. 2002. Yeast cytochrome c peroxidase: Mechanistic studies via protein engineering. Biochim. Biophys. Acta. 1597: 193-220.
10. Giulivi, C. and Davies, K.J. 1993. Dityrosine and tyrosine oxidation products are endogenous markers for the selective proteolysis of oxidatively modified red blood cell hemoglobin by (the 19 S) proteasome. J. Biol. Chem. 268: 8752-8759.
11. Hashimoto, M., Takeda, A., Hsu, L.J., Takenouchi, T., and Masliah, E. 1999. Role of cytochrome c as a stimulator of α-synuclein aggregation in Lewy body disease. J. Biol. Chem. 274: 28849-28852.
12. Heinecke, J.W., Li, W., Daehnke 3rd, H.L., and Goldstein, J.A. 1993. Dityrosine, a specific marker of oxidation, is synthesized by the myeloperoxidase-hydrogen peroxide system of human neutrophils and macrophages. J. Biol. Chem. 268: 4069-4077.
13. Holdorff, B. 2002. Friedrich Heinrich Lewy (1885-1950) and his work. J. Hist. Neurosci. 11: 19-28.
14. Huggins, T.G., Wells-Knecht, M.C., Detorie, N.A., Baynes, J.W., and Thorpe, S.R. 1993. Formation of o-tyrosine and dityrosine in proteins during radiolytic and metal-catalyzed oxidation. J. Biol. Chem. 268: 12341-12347.
15. Kato, Y., Kitamoto, N., Kawai, Y., and Osawa, T. 2001. The hydrogen peroxide/copper ion system, but not other metal-catalyzed oxidation systems, produces protein-bound dityrosine. Free Radic. Biol. Med. 31: 624-632.
16. Kim, J. 1997. Evidence that the precursor protein of non-Aβ component of Alzheimer's disease amyloid (NACP) has an extended structure primarily composed of random-coil. Mol. Cell. 7: 78-83.
17. Lang, A.E. and Lozano, A.M. 1998. Parkinson's disease. Second of two parts. N. Engl J. Med. 339: 1130-1143.
18. Lashuel, H.A., Hartley, D., Petre, B.M., Walz, T., and Lansbury Jr., P.T. 2002. Amyloid pores from pathogenic mutations. Nature 418: 291.
19. Morar, A.S., Olteanu, A., Young, G.B., and Pielak, G.J. 2001. Solvent-induced collapse of α-synuclein and acid-denatured cytochrome c. Protein. Sci. 10: 2195-2199.
20. Nagano, S., Huang, X., Moir, R.D., Payton, S.M., Tanzi, R.E., and Bush, A.I. 2004. Peroxidase activity of cyclooxygenase-2 (COX-2) cross-links β-amyloid (Aβ) and generates Aβ-COX-2 hetero-oligomers that are increased in Alzheimer's disease. J. Biol. Chem. 279: 14673-14678.
21. Norris, E.H., Giasson, B.I., Ischiropoulos, H., and Lee, V.M. 2003. Effects of oxidative and nitrative challenges on α-synuclein fibrillogenesis involve distinct mechanisms of protein modifications. J. Biol. Chem. 278: 27230-27240.
22. Olteanu, A., Patel, C.N., Dedmon, M.M., Kennedy, S., Linhoff, M.W., Minder, C.M., Potts, P.R., Deshmukh, M., and Pielak, G.J. 2003. Stability and apoptotic activity of recombinant human cytochrome c. Biochem. Biophys. Res. Commun. 312: 733-740.
23. Pennathur, S., Jackson-Lewis, V., Przedborski, S., Heinecke, J.W., Polacino, P.S., Stallard, V., Klaniecki, J.E., Montefiori, D.C., Langlois, A.J., Richardson, B.A., et al. 1999. Mass spectrometric quantification of 3-nitrotyrosine, ortho-tyrosine, and o,o′-dityrosine in brain tissue of 1-methyl-4-phenyl-1,2,3, 6-tetrahydropyridine-treated mice, a model of oxidative stress in Parkinson's disease. J. Biol. Chem. 274: 34621-34628.
24. Polymerpoulos, M.H., Lavedan, C., Leroy, E., Ide, S.E., Dehejia, A., Dutra, A., Pike, B., Root, H., Rubenstein, J., Boyer, R., et al. 1997. Mutations in the α-synuclein gene identified in families with Parkinson's disease. Science 276: 2045-2047.
25. Qian, S.Y., Chen, Y.R., Deterding, L.J., Fann, Y.C., Chignell, C.F., Tomer, K.B., Mason, R.P., Barr, D.P., and Gunther, M.R. 2002. Identification of protein-derived tyrosyl radical in the reaction of cytochrome c and hydrogen peroxide; Characterization by ESR spin-trapping, HPLC and MS ESR spin-trapping of a protein-derived tyrosyl radical from the reaction of cytochrome c with hydrogen peroxide. Biochem. J. 363: 281-288.
26. Shigenaga, M.K., Hagen, T.M., and Ames, B.N. 1994. Oxidative damage and mitochondrial decay in aging. Proc. Natl. Acad. Sci. 91: 10771-10778.
27. Sies, H. 1991. Oxidative stress: From basic research to clinical application. Am. J. Med. 91: 31S-38S.
28. Souza, J.M., Giasson, B.I., Chen, Q., Lee, V.M., and Ischiropoulos, H. 2000. Dityrosine cross-linking promotes formation of stable α-synuclein polymers. Implication of nitrative and oxidative stress in the pathogenesis of neurodegenerative synucleinopathies. J. Biol. Chem. 275: 18344-18349.
29. Spillantini, M.G., Schmidt, M.L., Lee, V.M.-Y., Trojanowski, J.Q., Jakes, R., and Goedert, M. 1997. α Synuclein in Lewy bodies. Nature 388: 839-840.
30. Stadtman, E.R. 1993. Oxidation of free amino acids and amino acid residues in proteins by radiolysis and by metal-catalyzed reactions. Annu. Rev. Biochem. 62: 797-821.
31. Volles, M.J., and Lansbury Jr., P.T. 2002. Vesicle permeabilization by protofibrillar α-synuclein is sensitive to Parkinson's disease-linked mutations and occurs by a pore-like mechanism. Biochemistry 41: 4595-4602.
32. Weinreb, P.H., Zhen, W., Poon, A.W., Conway, K.A., and Lansbury Jr., P.T. 1996. NACP, a protein implicated in Alzheimer's disease and learning, is natively unfolded. Biochemistry 35: 13709-13715.