Structure-function relationship in an archaebacterial methionine sulphoxide reductase B

Molecular Microbiology

Volumn 79, Issue 2, 2011, Pages 342-358

  Carella, Michela ^a   Becher, Juliane ^a   Ohlenschläger, Oliver ^a   Ramachandran, Ramadurai ^a   Gührs, Karl Heinz ^a   Wellenreuther, Gerd ^b   Meyer Klaucke, Wolfram ^b   Heinemann, Stefan H ^c   Görlach, Matthias ^a  

^a FRITZ LIPMANN INSTITUTE   (Germany)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACID; CYSTEINE; GENOMIC DNA; METHIONINE SULFOXIDE; METHIONINE SULFOXIDE REDUCTASE B; PROTEIN MTH711; SULPHENIC ACID; UNCLASSIFIED DRUG;

AEROBIC BACTERIUM; ARTICLE; CATALYSIS; CONTROLLED STUDY; DISULFIDE BOND; ENZYME ACTIVITY; ENZYME METABOLISM; ENZYME STRUCTURE; MESOPHILIC BACTERIUM; METHANOTHERMOBACTER THERMAUTOTROPHICUS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OPEN READING FRAME; PRIORITY JOURNAL; SEQUENCE ALIGNMENT; SPECIES COMPARISON; STRUCTURE ACTIVITY RELATION;

AMINO ACID SEQUENCE; ARCHAEAL PROTEINS; CATALYTIC DOMAIN; METHANOBACTERIACEAE; METHIONINE; METHIONINE SULFOXIDE REDUCTASES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OXIDATION-REDUCTION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ALIGNMENT;

ARCHAEA; METHANOTHERMOBACTER THERMAUTOTROPHICUS;

EID: 78651089206     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07447.x     Document Type: Article

References (80)

1. Amegbey, G.Y., Monzavi, H., Habibi-Nazhad, B., Bhattacharyya, S., and Wishart, D.S. (2003) Structural and functional characterization of a thioredoxin-like protein (Mt0807) from Methanobacterium thermoautotrophicum. Biochemistry 42: 8001-8010.
2. Auld, D.S. (2001) Zinc coordination sphere in biochemical zinc sites. Biometals 14: 271-313.
3. Balch, W.E., and Wolfe, R.S. (1979) Specificity and biological distribution of coenzyme M (2-mercaptoethanesulfonic acid). J Bacteriol 137: 256-263.
4. Bartels, C., Billeter, T.H., Güntert, P., and Wüthrich, K. (1995) The program xeasy for computer-supported NMR spectral analysis of biological macromolecules. J Biomol NMR 5: 1-10.
5. Bartlett, R.K., Bieber Urbauer, R.J., Anbanandam, A., Smallwood, H.S., Urbauer, J.L., and Squier, T.C. (2003) Oxidation of Met144 and Met145 in calmodulin blocks calmodulin dependent activation of the plasma membrane Ca-ATPase. Biochemistry 42: 3231-3238.
6. Beckman, K.B., and Ames, B.N. (1998) The free radical theory of aging matures. Physiol Rev 78: 547-581.
7. Berlett, B.S., and Stadtman, E.R. (1997) Protein oxidation in aging, disease, and oxidative stress. J Biol Chem 272: 20313-20316.
8. Bhattacharyya, S., Habibi-Nazhad, B., Amegbey, G., Slupsky, C.M., Yee, A., Arrowsmith, C., and Wishart, D.S. (2002) Identification of a novel archaebacterial thioredoxin: determination of function through structure. Biochemistry 41: 4760-4770.
9. Bigelow, D.J., and Squier, T.C. (2005) Redox modulation of cellular signaling and metabolism through reversible oxidation of methionine sensors in calcium regulatory proteins. Biochim Biophys Acta 1703: 121-134.
10. Binsted, N., Strange, R.W., and Hasnain, S.S. (1992) Constrained and restrained refinement in EXAFS data analysis with curved wave theory. Biochemistry 31: 12117-12125.
11. Boschi-Muller, S., Azza, S., Sanglier-Cianferani, S., Talfournier, F., Van Dorsselear, A., and Branlant, G. (2000) A sulfenic acid enzyme intermediate is involved in the catalytic mechanism of peptide methionine sulfoxide reductase from Escherichia coli. J Biol Chem 275: 35908-35913.
12. Boschi-Muller, S., Olry, A., Antoine, M., and Branlant, G. (2005) The enzymology and biochemistry of methionine sulfoxide reductases. Biochim Biophys Acta 1703: 231-238.
13. Boschi-Muller, S., Gand, A., and Branlant, G. (2008) The methionine sulfoxide reductases: catalysis and substrate specificities. Arch Biochem Biophys 474: 266-273.
14. Carella, M., Ohlenschlager, O., Ramachandran, R., and Gorlach, M. (2010) 1H, 13C and 15N resonance assignment of a zinc-binding methionine sulfoxide reductase type-B from the thermophilic archeabacterium Methanothermobacter thermoautotrophicus. Biomol NMR Assign 4: 93-95.
15. Claiborne, A., Miller, H., Parsonage, D., and Ross, R.P. (1993) Protein-sulfenic acid stabilization and function in enzyme catalysis and gene regulation. FASEB J 7: 1483-1490.
16. Cornell, W.D., Cieplak, P., Bayly, C.I., Gould, I.R., Merz, K.M., Ferguson, D.M., et al. (1995) A second generation force field for the simulation of proteins, nucleic acids and organic molecules. J Am Chem Soc 117: 5179-5197.
17. Coudevylle, N., Antoine, M., Bouguet-Bonnet, S., Mutzenhardt, P., Boschi-Muller, S., Branlant, G., and Cung, M.T. (2007) Solution structure and backbone dynamics of the reduced form and an oxidized form of E. coli methionine sulfoxide reductase A (MsrA): structural insight of the MsrA catalytic cycle. J Mol Biol 366: 193-206.
18. D'Autreaux, B., and Toledano, M.B. (2007) ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 8: 813-824.
19. Delaglio, F., Grzesiek, S., Vuister, G.W., Zhu, G., Pfeifer, J., and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J Biomol NMR 6: 277-293.
20. Delaye, L., Becerra, A., Orgel, L., and Lazcano, A. (2007) Molecular evolution of peptide methionine sulfoxide reductases (MsrA and MsrB): on the early development of a mechanism that protects against oxidative damage. J Mol Evol 64: 15-32.
21. Erickson, J.R., Joiner, M.L., Guan, X., Kutschke, W., Yang, J., Oddis, C.V., et al. (2008) A dynamic pathway for calcium-independent activation of CaMKII by methionine oxidation. Cell 133: 462-474.
22. Fahey, R.C. (2001) Novel thiols of prokaryotes. Annu Rev Microbiol 55: 333-356.
23. Finkel, T. (2003) Oxidant signals and oxidative stress. Curr Opin Cell Biol 15: 247-254.
24. Fukushima, E., Shinka, Y., Fukui, T., Atomi, H., and Imanaka, T. (2007) Methionine sulfoxide reductase from the hyperthermophilic archaeon Thermococcus kodakaraensis, an enzyme designed to function at suboptimal growth temperatures. J Bacteriol 189: 7134-7144.
25. Fushman, D., Cahill, S., and Cowburn, D. (1997) The main-chain dynamics of the dynamin pleckstrin homology (PH) domain in solution: analysis of 15N relaxation with monomer/dimer equilibration. J Mol Biol 266: 173-194.
26. Giorgio, M., Trinei, M., Migliaccio, E., and Pelicci, P.G. (2007) Hydrogen peroxide: a metabolic by-product or a common mediator of ageing signals? Nat Rev Mol Cell Biol 8: 722-728.
27. Glaser, C.B., Morser, J., Clarke, J.H., Blasko, E., McLean, K., Kuhn, I., et al. (1992) Oxidation of a specific methionine in thrombomodulin by activated neutrophil products blocks cofactor activity. A potential rapid mechanism for modulation of coagulation. J Clin Invest 90: 2565-2573.
28. Glaser, C.B., Yamin, G., Uversky, V.N., and Fink, A.L. (2005) Methionine oxidation, alpha-synuclein and Parkinson's disease. Biochim Biophys Acta 1703: 157-169.
29. Guntert, P. (1998) Structure calculation of biological macromolecules from NMR data. Q Rev Biophys 31: 145-237.
30. Hall, J.B., and Fushman, D. (2003) Characterization of the overall and local dynamics of a protein with intermediate rotational anisotropy: differentiating between conformational exchange and anisotropic diffusion in the B3 domain of protein G. J Biomol NMR 27: 261-275.
31. Halliwell, B., and Gutteridge, J.M.C. (1999) Free Radicals in Biology and Medicine, 4th edn. Oxford: Oxford University Press.
32. Hansel, A., Jung, S., Hoshi, T., and Heinemann, S.H. (2003) A second human methionine sulfoxide reductase (hMSRB2) reducing methionine-R-sulfoxide displays a tissue expression pattern distinct from hMSRB1. Redox Rep 8: 384-388.
33. Hansel, A., Heinemann, S.H., and Hoshi, T. (2005) Heterogeneity and function of mammalian MSRs: enzymes for repair, protection and regulation. Biochim Biophys Acta 1703: 239-247.
34. Herrmann, T., Guntert, P., and Wuthrich, K. (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J Mol Biol 319: 209-227.
35. Hoshi, T., and Heinemann, S. (2001) Regulation of cell function by methionine oxidation and reduction. J Physiol 531: 1-11.
36. Jacob, C., Giles, G.I., Giles, N.M., and Sies, H. (2003) Sulfur and selenium: the role of oxidation state in protein structure and function. Angew Chem Int Ed Engl 42: 4742-4758.
37. Johnson, D., and Travis, J. (1979) The oxidative inactivation of human alpha-1-proteinase inhibitor. Further evidence for methionine at the reactive center. J Biol Chem 254: 4022-4026.
38. Jung, S., Hansel, A., Kasperczyk, H., Hoshi, T., and Heinemann, S.H. (2002) Activity, tissue distribution and site-directed mutagenesis of a human peptide methionine sulfoxide reductase of type B: hCBS1. FEBS Lett 527: 91-94.
39. Keller, R. (2004) The Computer Aided Resonance Assignment Tutorial. Goldau: Cantina Verlag.
40. Kettenhofen, N.J., and Wood, M.J. (2010) Formation, reactivity, and detection of protein sulfenic acids. Chem Res Toxicol doi: 10.1021/tx100237w.
41. Kim, K.S., Fuchs, J.A., and Woodward, C.K. (1993) Hydrogen exchange identifies native-state motional domains important in protein folding. Biochemistry 32: 9600-9608.
42. Kim, H.Y., and Gladyshev, V.N. (2004) Methionine sulfoxide reduction in mammals: characterization of methionine-R-sulfoxide reductases. Mol Biol Cell 15: 1055-1064.
43. Koradi, R., Billeter, M., and Wuthrich, K. (1996) molmol: a program for display and analysis of macromolecular structures. J Mol Graph 14: 51-55, 29-32.
44. Korbas, M., Fulla Marsa, D., and Meyer-Klaucke, W. (2006) kemp: a program script for automated biological x-ray absorption spectroscopy data reduction. Rev Sci Instrum 77: 063105. (063105 pages).
45. Kornhaber, G.J., Snyder, D., Moseley, H.N., and Montelione, G.T. (2006) Identification of zinc-ligated cysteine residues based on 13Calpha and 13Cbeta chemical shift data. J Biomol NMR 34: 259-269.
46. Kumar, R.A., Koc, A., Cerny, R.L., and Gladyshev, V.N. (2002) Reaction mechanism, evolutionary analysis, and role of zinc in Drosophila methionine-R-sulfoxide reductase. J Biol Chem 277: 37527-37535.
47. Laskowski, R.A., Rullmannn, J.A., MacArthur, M.W., Kaptein, R., and Thornton, J.M. (1996) aqua and procheck-nmr: programs for checking the quality of protein structures solved by NMR. J Biomol NMR 8: 477-486.
48. Levine, R.L., Mosoni, L., Berlett, B.S., and Stadtman, E.R. (1996) Methionine residues as endogenous antioxidants in proteins. Proc Natl Acad Sci USA 93: 15036-15040.
49. Lipari, G., and Szabo, A. (1981) Nuclear magnetic resonance relaxation in nucleic acid fragments: models for internal motion. Biochemistry 20: 6250-6256.
50. Lowther, W.T., Weissbach, H., Etienne, F., Brot, N., and Matthews, B.W. (2002) The mirrored methionine sulfoxide reductases of Neisseria gonorrhoeae pilB. Nat Struct Biol 9: 348-352.
51. Luginbuhl, P., Guntert, P., Billeter, M., and Wuthrich, K. (1996) The new program opal for molecular dynamics simulations and energy refinements of biological macromolecules. J Biomol NMR 8: 136-146.
52. Moskovitz, J. (2005) Methionine sulfoxide reductases: ubiquitous enzymes involved in antioxidant defense, protein regulation, and prevention of aging-associated diseases. Biochim Biophys Acta 1703: 213-219.
53. Neiers, F., Kriznik, A., Boschi-Muller, S., and Branlant, G. (2004) Evidence for a new sub-class of methionine sulfoxide reductases B with an alternative thioredoxin recognition signature. J Biol Chem 279: 42462-42468.
54. Ohlenschlager, O., Seiboth, T., Zengerling, H., Briese, L., Marchanka, A., Ramachandran, R., et al. (2006) Solution structure of the partially folded high-risk human papilloma virus 45 oncoprotein E7. Oncogene 25: 5953-5959.
55. Olry, A., Boschi-Muller, S., Marraud, M., Sanglier-Cianferani, S., Dorsselear, A.V., and Branlant, G. (2002) Characterization of the methionine sulfoxide reductase activities of PILB, a probable virulence factor from Neisseria meningitidis. J Biol Chem 277: 12016-12022.
56. Olry, A., Boschi-Muller, S., Yu, H., Burnel, D., and Branlant, G. (2005) Insights into the role of the metal binding site in methionine-R-sulfoxide reductases B. Protein Sci 14: 2828-2837.
57. Petropoulos, I., and Friguet, B. (2006) Maintenance of proteins and aging: the role of oxidized protein repair. Free Radic Res 40: 1269-1276.
58. Poole, L.B., Karplus, P.A., and Claiborne, A. (2004) Protein sulfenic acids in redox signaling. Annu Rev Pharmacol Toxicol 44: 325-347.
59. Powell, M. (1977) Restart procedures for the conjugate gradient method. Math Prog 12: 241-254.
60. Ranaivoson, F.M., Antoine, M., Kauffmann, B., Boschi-Muller, S., Aubry, A., Branlant, G., and Favier, F. (2008) A structural analysis of the catalytic mechanism of methionine sulfoxide reductase A from Neisseria meningitidis. J Mol Biol 377: 268-280.
61. Ranaivoson, F.M., Neiers, F., Kauffmann, B., Boschi-Muller, S., Branlant, G., and Favier, F. (2009) Methionine sulfoxide reductase B displays a high level of flexibility. J Mol Biol 394: 83-93.
62. Sagher, D., Brunell, D., Hejtmancik, J.F., Kantorow, M., Brot, N., and Weissbach, H. (2006) Thionein can serve as a reducing agent for the methionine sulfoxide reductases. Proc Natl Acad Sci USA 103: 8656-8661.
63. Schoneich, C. (2005) Methionine oxidation by reactive oxygen species: reaction mechanisms and relevance to Alzheimer's disease. Biochim Biophys Acta 1703: 111-119.
64. Shchedrina, V.A., Vorbruggen, G., Lee, B.C., Kim, H.Y., Kabil, H., Harshman, L.G., and Gladyshev, V.N. (2009) Overexpression of methionine-R-sulfoxide reductases has no influence on fruit fly aging. Mech Ageing Dev 130: 429-443.
65. Smith, D.R., Doucette-Stamm, L.A., Deloughery, C., Lee, H., Dubois, J., Aldredge, T., et al. (1997) Complete genome sequence of Methanobacterium thermoautotrophicum deltaH: functional analysis and comparative genomics. J Bacteriol 179: 7135-7155.
66. Sohal, R.S. (2002) Oxidative stress hypothesis of aging. Free Radic Biol Med 33: 573-574.
67. Stadtman, E.R., and Berlett, B.S. (1997) Reactive oxygen-mediated protein oxidation in aging and disease. Chem Res Toxicol 10: 485-494.
68. Stadtman, E.R., Moskovitz, J., and Levine, R.L. (2003) Oxidation of methionine residues of proteins: biological consequences. Antioxid Redox Signal 5: 577-582.
69. Stadtman, E.R., Van Remmen, H., Richardson, A., Wehr, N.B., and Levine, R.L. (2005) Methionine oxidation and aging. Biochim Biophys Acta 1703: 135-140.
70. Tarrago, L., Laugier, E., Zaffagnini, M., Marchand, C., Le Marechal, P., Rouhier, N., et al. (2009) Regeneration mechanisms of Arabidopsis thaliana methionine sulfoxide reductases B by glutaredoxins and thioredoxins. J Biol Chem 284: 18963-18971.
71. Tarrago, L., Laugier, E., Zaffagnini, M., Marchand, C.H., Le Marechal, P., Lemaire, S.D., and Rey, P. (2010) Plant thioredoxin CDSP32 regenerates 1-cys methionine sulfoxide reductase B activity through the direct reduction of sulfenic acid. J Biol Chem 285: 14964-14972.
72. Thauer, R.K., Kaster, A.K., Seedorf, H., Buckel, W., and Hedderich, R. (2008) Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev Microbiol 6: 579-591.
73. Turell, L., Botti, H., Carballal, S., Ferrer-Sueta, G., Souza, J.M., Duran, R., et al. (2008) Reactivity of sulfenic acid in human serum albumin. Biochemistry 47: 358-367.
74. Viles, J.H., Donne, D., Kroon, G., Prusiner, S.B., Cohen, F.E., Dyson, H.J., and Wright, P.E. (2001) Local structural plasticity of the prion protein. Analysis of NMR relaxation dynamics. Biochemistry 40: 2743-2753.
75. Vogt, W. (1995) Oxidation of methionyl residues in proteins: tools, targets, and reversal. Free Radic Biol Med 18: 93-105.
76. Wassef, R., Haenold, R., Hansel, A., Brot, N., Heinemann, S.H., and Hoshi, T. (2007) Methionine sulfoxide reductase A and a dietary supplement S-methyl-l-cysteine prevent Parkinson's-like symptoms. J Neurosci 27: 12808-12816.
77. Weissbach, H., Etienne, F., Hoshi, T., Heinemann, S.H., Lowther, W.T., Matthews, B., et al. (2002) Peptide methionine sulfoxide reductase: structure, mechanism of action, and biological function. Arch Biochem Biophys 397: 172-178.
78. Wellenreuther, G., and Meyer-Klaucke, W. (2007) Towards a black-box for biological EXAFS data analysis - I. Identification of zinc finger proteins. In: X-RAY ABSORPTION FINE STRUCTURE - XAFS13: 13th International Conference. pp. 322-324.
79. Williamson, R.A., Carr, M.D., Frenkiel, T.A., Feeney, J., and Freedman, R.B. (1997) Mapping the binding site for matrix metalloproteinase on the N-terminal domain of the tissue inhibitor of metalloproteinases-2 by NMR chemical shift perturbation. Biochemistry 36: 13882-13889.
80. Wong, Y.Q., Binger, K.J., Howlett, G.J., and Griffin, M.D. (2010) Methionine oxidation induces amyloid fibril formation by full-length apolipoprotein A-I. Proc Natl Acad Sci USA 107: 1977-1982.