Impact of Hydrogen Peroxide on the Activity, Structure, and Conformational Stability of the Oxidized Protein Repair Enzyme Methionine Sulfoxide Reductase A

Journal of Molecular Biology

Volumn 393, Issue 1, 2009, Pages 58-66

  Le, Hai Tuong ^a   Chaffotte, Alain F ^b   Demey Thomas, Emmanuelle ^b   Vinh, Jöelle ^b   Friguet, Bertrand ^a,c   Mary, Jean ^a,b  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b CNRS   (France)

^c SORBONNE UNIVERSITÉ   (France)

Author keywords

20S proteasome; conformational stability; MsrA; protein degradation; protein oxidation

Indexed keywords

CYSTEINE; HYDROGEN PEROXIDE; METHIONINE SULFOXIDE REDUCTASE A; PROTEASOME;

ANIMAL TISSUE; ARTICLE; CIRCULAR DICHROISM; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME CONFORMATION; ENZYME DEGRADATION; ENZYME INACTIVATION; ENZYME METABOLISM; ENZYME MODIFICATION; ENZYME STABILITY; ENZYME STRUCTURE; LIVER PARENCHYMA; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT;

EID: 70349402567     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.07.072     Document Type: Article

References (35)

1. Sun H., Gao J., Ferrington D.A., Biesiada H., Williams T.D., and Squier T.C. Repair of oxidized calmodulin by methionine sulfoxide reductase restores ability to activate the plasma membrane Ca-ATPase. Biochemistry 38 (1999) 105-112
2. van Montfort R.L., Congreve M., Tisi D., Carr R., and Jhoti H. Oxidation state of the active-site cysteine in protein tyrosine phosphatase 1B. Nature 423 (2003) 773-777
3. Mary J., Vougier S., Picot C.R., Perichon M., Petropoulos I., and Friguet B. Enzymatic reactions involved in the repair of oxidized proteins. Exp. Gerontol. 39 (2004) 1117-1123
4. Kim H.Y., and Gladyshev V.N. Methionine sulfoxide reductases: selenoprotein forms and roles in antioxidant protein repair in mammals. Biochem. J. 407 (2007) 321-329
5. Levine R.L., Mosoni L., Berlett B.S., and Stadtman E.R. Methionine residues as endogenous antioxidants in proteins. Proc. Natl. Acad. Sci. USA 93 (1996) 15036-15040
6. 2-mediated oxidative stress. Free Radic. Biol. Med. 39 (2005) 1332-1341
7. Cabreiro F., Picot C.R., Perchon M., Friguet B., and Petropoulos I. Overexpression of methionine sulfoxide reductase A and B2 protects MOLT-4 cells against zinc-induced oxidative stress. Antioxid. Redox Signal. 11 (2009) 215-225
8. Abrams W.R., Weinbaum G., Weissbach L., and Brot N. Enzymatic reduction of oxidized alpha-1-proteinase inhibitor restores biological activity. Proc. Natl. Acad. Sci. USA 78 (1981) 7483-7486
9. Vougier S., Mary J., Dautin N., Vinh J., Friguet B., and Ladant D. Essential role of methionine residues in calmodulin binding to Bordetella pertussis adenylate cyclase, as probed by selective oxidation and repair by the peptide methionine sulfoxide reductases. J. Biol. Chem. 279 (2004) 30210-30218
10. Lowther W.T., Weissbach H., Etienne F., Brot N., and Matthews B.W. The mirrored methionine sulfoxide reductases of Neisseria gonorrhoeae pilB. Nat. Struct. Biol. 9 (2002) 348-352
11. Boschi-Muller S., Assa S., Sanglier-Cianferani S., Talfournier F., Van Dorsselear A., and Branlant G. A sulfenic acid enzyme intermediate is involved in the catalytic mechanism of peptide methionine sulfoxide reductase from Escherichia coli. J. Biol. Chem. 275 (2000) 35908-35913
12. Orly A., Boschi-Muller S., Marraud M., Sanglier-Cianferani S., Van Dorsselear A., and Branlant G. Characterization of the methionine sulfoxide reductase activities of PILB, a probable virulence factor from Neisseria meningitides. J. Biol. Chem. 277 (2002) 12016-12022
13. Vougier S., Mary J., and Friguet B. Subcellular localization of methionine sulphoxide reductase A (MsrA): evidence for mitochondrial and cytosolic isoforms in rat liver cells. Biochem. J. 373 (2003) 531-537
14. Grune T., Merker K., Sandig G., and Davies K.J. Selective degradation of oxidatively modified protein substrates by the proteasome. Biochem. Biophys. Res. Commun. 305 (2003) 709-718
15. Friguet B., Szweda L.I., and Stadtman E.R. Susceptibility of glucose-6-phosphate dehydrogenase modified by 4-hydroxy-2-nonenal and metal-catalyzed oxidation to proteolysis by the multicatalytic protease. Arch. Biochem. Biophys. 311 (1994) 168-173
16. Pacifici R.E., Kono Y., and Davies K.J. Hydrophobicity as the signal for selective degradation of hydroxyl radical-modified hemoglobin by the multicatalytic proteinase complex, proteasome. J. Biol. Chem. 268 (1993) 15405-15411
17. Guilivi C., Pacifici R.E., Kono Y., and Davies K.J. Exposure of hydrophobic moieties promotes the selective degradation of hydrogen peroxide-modified hemoglobin by the multicatalytic proteinase complex, proteasome. Arch. Biochem. Biophys. 311 (1994) 329-341
18. Chao C.C., Ma Y.S., and Stadtman E.R. Modification of protein surface hydrophobicity and methionine oxidation by oxidative systems. Proc. Natl. Acad. Sci. USA 94 (1997) 2969-2974
19. Lasch P., Petras T., Ullrich O., Backmann J., Naumann D., and Grune T. Hydrogen peroxide-induced structural alterations of RNase A. J. Biol. Chem. 276 (2001) 9492-9502
20. Lowther W.T., Brot N., Weissbach H., and Matthews B.W. Structure and mechanism of peptide methionine sulfoxide reductase, an "anti-oxidation" enzyme. Biochemistry 39 (2000) 13307-13312
21. Tête-Favier F., Cobessi D., Boschi-Muller S., Azza S., Branlant G., and Aubry A. Crystal structure of the Escherichia coli peptide methionine sulphoxide reductase at 1.9 Ǻ resolution. Structure 8 (2000) 1167-1178
22. Haenold R., Wassef R., Brot N., Neugebauer S., Leipold E., Heinemann S.H., and Hoshi T. Protection of vascular smooth muscle cells by over-expressed methionine sulphoxide reductase A: role of intracellular localization and substrate availability. Free Radic. Res. 42 (2008) 978-988
23. Stadtman E.R. Protein oxidation and aging. Science 257 (1992) 1220-1224
24. Petropoulos I., and Friguet B. Maintenance of proteins and aging: the role of oxidized protein repair. Free Radic. Res. 40 (2006) 1269-1276
25. 2) in the epidermis of patients with vitiligo. J. Invest. Dermatol. 128 (2007) 808-815
26. 2-mediated oxidative stress affects human hair color by blunting methionine sulfoxide repair. FASEB J. 23 (2009) 2065-2075
27. Picot C.R., Perichon M., Lundberg K.C., Friguet B., Szweda L.I., and Petropoulos I. Alterations in mitochondrial and cytosolic methionine sulfoxide reductase activity during cardiac ischemia and reperfusion. Exp. Gerontol. 41 (2006) 663-667
28. Picot C.R., Moreau M., Juan M., Noblesse E., Nizard C., Petropoulos I., and Friguet B. Impairment of methionine sulfoxide reductase during UV irradiation and photoaging. Exp. Gerontol. 42 (2007) 859-863
29. Antoine M., Gand A., Boschi-Muller S., and Branlant G. Characterization of the amino acids from Neisseria meningitidis MsrA involved in the chemical catalysis of the methionine sulfoxide reduction step. J. Biol. Chem. 281 (2006) 39062-39070
30. Petropoulos I., Mary J., Perichon M., and Friguet B. Rat peptide methionine sulphoxide reductase: cloning of the cDNA, and down-regulation of gene expression and enzyme activity during aging. Biochem. J. 355 (2001) 819-825
31. Gasteiger E., Gattiker A., Hoogland C., Ivanyi I., Appel R.D., and Bairoch A. ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res. 31 (2003) 3784-3788
32. Brot N., Werth J., Koster D., and Weissbach H. Reduction of N-acetyl methionine sulfoxide: a simple assay for peptide methionine sulfoxide reductase. Anal. Biochem. 122 (1982) 291-294
33. Conconi M., Szweda L.I., Levine R.L., Stadtman E.R., and Friguet B. Age-related decline of rat liver multicatalytic proteinase activity and protection from oxidative inactivation by heat-shock protein 90. Arch. Biochem. Biophys. 331 (1996) 232-240
34. Farout L., Mary J., Vinh J., Szweda L.I., and Friguet B. Inactivation of the proteasome by 4-hydroxy-2-nonenal is site specific and dependant on 20S proteasome subtypes. Arch. Biochem. Biophys. 453 (2006) 135-142
35. Friguet B., Szweda L.I., and Stadtman E.R. Susceptibility of glucose-6-phosphate dehydrogenase modified by 4-hydroxy-2-nonenal and metal-catalyzed oxidation to proteolysis by the multicatalytic protease. Arch. Biochem. Biophys. 311 (1994) 168-173