Structural and biochemical analysis of mammalian methionine sulfoxide reductase B2

Proteins: Structure, Function and Bioinformatics

Volumn 79, Issue 11, 2011, Pages 3123-3131

  Aachmann, Finn L ^a   Kwak, Geun Hee ^b   del Conte, Rebecca ^c   Kim, Hwa Young ^b   Gladyshev, Vadim N ^d   Dikiy, Alexander ^a  

^a NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^b Yeungnam University College of Medicine   (South Korea)

^c UNIVERSITY OF FLORENCE   (Italy)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Catalytic mechanism; NMR spectroscopy; Oxidoreductases; Protein structure

Indexed keywords

METHIONINE SULFOXIDE REDUCTASE B2; OXIDOREDUCTASE; UNCLASSIFIED DRUG; ZINC;

ALPHA HELIX; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIUM; BINDING SITE; ELECTROPHYSIOLOGY; ENZYME KINETICS; MAMMAL; MOLECULAR CLONING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE;

ANIMALS; BINDING SITES; CATALYSIS; CATALYTIC DOMAIN; HYDROGEN-ION CONCENTRATION; METHIONINE SULFOXIDE REDUCTASES; MICE; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PROTEIN STRUCTURE, SECONDARY;

BACTERIA (MICROORGANISMS); MAMMALIA; MUS MUSCULUS;

EID: 80054001981     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.23141     Document Type: Article

References (49)

1. Kim HY, Gladyshev VN. Methionine sulfoxide reductases: selenoprotein forms and roles in antioxidant protein repair in mammals. Biochem J 2007; 407: 321-329.
2. Lee BC, Dikiy A, Kim HY, Gladyshev VN. Functions and evolution of selenoprotein methionine sulfoxide reductases. Biochim Biophys Acta 2009; 1790: 1471-1477.
3. Levine MS, Li Z, Cepeda C, Cromwell HC, Altemus KL. Neuromodulatory actions of dopamine on synaptically-evoked neostriatal responses in slices. Synapse 1996; 24: 65-78.
4. Luo S, Levine RL. Methionine in proteins defends against oxidative stress. FASEB J 2009; 23: 464-472.
5. Erickson JR, Joiner ML, Guan X, Kutschke W, Yang J, Oddis CV, Bartlett RK, Lowe JS, O'Donnell SE, Aykin-Burns N, Zimmerman MC, Zimmerman K, Ham AJ, Weiss RM, Spitz DR, Shea MA, Colbran RJ, Mohler PJ, Anderson ME. A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell 2008; 133: 462-474.
6. Koc A, Gasch AP, Rutherford JC, Kim HY, Gladyshev VN. Methionine sulfoxide reductase regulation of yeast lifespan reveals reactive oxygen species-dependent and -independent components of aging. Proc Natl Acad Sci USA 2004; 101: 7999-8004.
7. Ruan H, Tang XD, Chen ML, Joiner ML, Sun G, Brot N, Weissbach H, Heinemann SH, Iverson L, Wu CF, Hoshi T. High-quality life extension by the enzyme peptide methionine sulfoxide reductase. Proc Natl Acad Sci USA 2002; 99: 2748-2753.
8. Minniti AN, Cataldo R, Trigo C, Vasquez L, Mujica P, Leighton F, Inestrosa NC, Aldunate R. Methionine sulfoxide reductase A expression is regulated by the DAF-16/FOXO pathway in Caenorhabditis elegans. Aging Cell 2009; 8: 690-705.
9. Gabbita SP, Aksenov MY, Lovell MA, Markesbery WR. Decrease in peptide methionine sulfoxide reductase in Alzheimer's disease brain. J Neurochem 1999; 73: 1660-1666.
10. Liu F, Hindupur J, Nguyen JL, Ruf KJ, Zhu J, Schieler JL, Bonham CC, Wood KV, Davisson VJ, Rochet JC. Methionine sulfoxide reductase A protects dopaminergic cells from Parkinson's disease-related insults. Free Radic Biol Med 2008; 45: 242-255.
11. Oien DB, Osterhaus GL, Latif SA, Pinkston JW, Fulks J, Johnson M, Fowler SC, Moskovitz J. MsrA knockout mouse exhibits abnormal behavior and brain dopamine levels. Free Radic Biol Med 2008; 45: 193-200.
12. Kaya A, Uzunhasan I, Baskurt M, Ozkan A, Ataoglu E, Okcun B, Yigit Z. Oxidative status and lipid profile in metabolic syndrome: gender differences. Metab Syndr Relat Disord 2010; 8: 53-58.
13. Cao G, Lee KP, van der Wijst J, de Graaf M, van der Kemp A, Bindels RJ, Hoenderop JG. Methionine sulfoxide reductase B1 (MsrB1) recovers TRPM6 channel activity during oxidative stress. J Biol Chem 2010; 285: 26081-26087.
14. Kim HY, Gladyshev VN. Different catalytic mechanisms in mammalian selenocysteine- and cysteine-containing methionine-R-sulfoxide reductases. PLoS Biol 2005; 3: e375.
15. Kim HY, Kim JR. Thioredoxin as a reducing agent for mammalian methionine sulfoxide reductases B lacking resolving cysteine. Biochem Biophys Res Commun 2008; 371: 490-494.
16. Lee TH, Kim HY. An anaerobic bacterial MsrB model reveals catalytic mechanisms, advantages, and disadvantages provided by selenocysteine and cysteine in reduction of methionine-R-sulfoxide. Arch Biochem Biophys 2008; 478: 175-180.
17. Lowther WT, Weissbach H, Etienne F, Brot N, Matthews BW. The mirrored methionine sulfoxide reductases of Neisseria gonorrhoeae pilB. Nat Struct Biol 2002; 9: 348-352.
18. Boschi-Muller S, Azza S, Sanglier-Cianferani S, Talfournier F, Van Dorsselear A, Branlant G. A sulfenic acid enzyme intermediate is involved in the catalytic mechanism of peptide methionine sulfoxide reductase from Escherichia coli. J Biol Chem 2000; 275: 35908-35913.
19. Boschi-Muller S, Gand A, Branlant G. The methionine sulfoxide reductases: catalysis and substrate specificities. Arch Biochem Biophys 2008; 474: 266-273.
20. Tarrago L, Laugier E, Zaffagnini M, Marchand CH, Le Marechal P, Lemaire SD, Rey P. Plant thioredoxin CDSP32 regenerates 1-cys methionine sulfoxide reductase B activity through the direct reduction of sulfenic acid. J Biol Chem 2010; 285: 14964-14972.
21. Kim HY, Gladyshev VN. Methionine sulfoxide reduction in mammals: characterization of methionine-R-sulfoxide reductases. Mol Biol Cell 2004; 15: 1055-1064.
22. Kim HY, Gladyshev VN. Characterization of mouse endoplasmic reticulum methionine-R-sulfoxide reductase. Biochem Biophys Res Commun 2004; 320: 1277-1283.
23. Aachmann FL, Sal LS, Kim HY, Marino SM, Gladyshev VN, Dikiy A. Insights into function, catalytic mechanism, and fold evolution of selenoprotein methionine sulfoxide reductase B1 through structural analysis. J Biol Chem 2010; 285: 33315-33323.
24. Breivik AS, Aachmann FL, Sal LS, Kim HY, Del Conte R, Gladyshev VN, Dikiy A. 1H, 15N and 13C NMR assignments of mouse methionine sulfoxide reductase B2. Biomol NMR Assign 2008; 2: 199-201.
25. Keller RLJ. Optimizing the process of nuclear magnetic resonance spectrum analysis and computer aided resonance assignment. Zürich: CANTINA Verlag; 2004.
26. Farrow NA, Muhandiram R, Singer AU, Pascal SM, Kay CM, Gish G, Shoelson SE, Pawson T, Forman-Kay JD, Kay LE. Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry 1994; 33: 5984-6003.
27. Kay LE, Torchia DA, Bax A. Backbone dynamics of proteins as studied by 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry 1989; 28: 8972-8979.
28. Güntert P, Braun W, Wüthrich K. Efficient computation of three-dimensional protein structures in solution from nuclear magnetic resonance data using the program DIANA and the supporting programs CALIBA, HABAS and GLOMSA. J Mol Biol 1991; 217: 517-530.
29. Cornilescu G, Delaglio F, Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J Biomol NMR 1999; 13: 289-302.
30. Güntert P, Wüthrich K. Improved efficiency of protein structure calculations from NMR data using the program DIANA with redundant dihedral angle constraints. J Biomol NMR 1991; 1: 447-456.
31. Case DA, Cheatham TE, 3rd, Darden T, Gohlke H, Luo R, Merz KM, Jr, Onufriev A, Simmerling C, Wang B, Woods RJ. The Amber biomolecular simulation programs. J Comput Chem 2005; 26: 1668-1688.
32. Kumar RA, Koc A, Cerny RL, Gladyshev VN. Reaction mechanism, evolutionary analysis, and role of zinc in Drosophila methionine-R-sulfoxide reductase. J Biol Chem 2002; 277: 37527-37535.
33. Kwak GH, Kim MJ, Kim HY. Cysteine-125 is the catalytic residue of Saccharomyces cerevisiae free methionine-R-sulfoxide reductase. Biochem Biophys Res Commun 2010; 395: 412-415.
34. Colonna-Cesari F, Perahia D, Karplus M, Eklund H, Braden CI, Tapia O. Interdomain motion in liver alcohol dehydrogenase. Structural and energetic analysis of the hinge bending mode. J Biol Chem 1986; 261: 15273-15280.
35. Mechulam Y, Schmitt E, Maveyraud L, Zelwer C, Nureki O, Yokoyama S, Konno M, Blanquet S. Crystal structure of Escherichia coli methionyl-tRNA synthetase highlights species-specific features. J Mol Biol 1999; 294: 1287-1297.
36. Chantalat L, Leroy D, Filhol O, Nueda A, Benitez MJ, Chambaz EM, Cochet C, Dideberg O. Crystal structure of the human protein kinase CK2 regulatory subunit reveals its zinc finger-mediated dimerization. EMBO J 1999; 18: 2930-2940.
37. Li H, Robertson AD, Jensen JH. Very fast empirical prediction and rationalization of protein pK(a) values. Proteins 2005; 61: 704-721.
38. Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci USA 2001; 98: 10037-10041.
39. DeLano WL. The PyMOL molecular graphics system. Palo Alto, CA, USA: DeLano Scientific LLC; 2008.
40. Kryukov GV, Kumar RA, Koc A, Sun Z, Gladyshev VN. Selenoprotein R is a zinc-containing stereo-specific methionine sulfoxide reductase. Proc Natl Acad Sci USA 2002; 99: 4245-4250.
41. Boschi-Muller S, Olry A, Antoine M, Branlant G. The enzymology and biochemistry of methionine sulfoxide reductases. Biochim Biophys Acta 2005; 1703: 231-238.
42. Gruez A, Libiad M, Boschi-Muller S, Branlant G. Structural and biochemical characterization of free methionine-R-sulfoxide reductase from Neisseria meningitidis. J Biol Chem 2010; 285: 25033-25043.
43. Kornhaber GJ, Snyder D, Moseley HN, Montelione GT. Identification of zinc-ligated cysteine residues based on 13Calpha and 13Cbeta chemical shift data. J Biomol NMR 2006; 34: 259-269.
44. Kauffmann B, Aubry A, Favier F. The three-dimensional structures of peptide methionine sulfoxide reductases: current knowledge and open questions. Biochim Biophys Acta 2005; 1703: 249-260.
45. Kim HY, Gladyshev VN. Role of structural and functional elements of mouse methionine-S-sulfoxide reductase in its subcellular distribution. Biochemistry 2005; 44: 8059-8067.
46. Ranaivoson FM, Neiers F, Kauffmann B, Boschi-Muller S, Branlant G, Favier F. Methionine sulfoxide reductase B displays a high level of flexibility. J Mol Biol 2009; 394: 83-93.
47. Neiers F, Sonkaria S, Olry A, Boschi-Muller S, Branlant G. Characterization of the amino acids from Neisseria meningitidis methionine sulfoxide reductase B involved in the chemical catalysis and substrate specificity of the reductase step. J Biol Chem 2007; 282: 32397-32405.
48. Creighton TE. Proteins-structure and molecular properties. New York: W.H. Freeman and Company; 1996.
49. Kim YK, Shin YJ, Lee WH, Kim HY, Hwang KY. Structural and kinetic analysis of an MsrA-MsrB fusion protein from Streptococcus pneumoniae. Mol Microbiol 2009; 72: 699-709.