The role of Cys108 in Trigonopsis variabilis d-amino acid oxidase examined through chemical oxidation studies and point mutations C108S and C108D

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1804, Issue 7, 2010, Pages 1483-1491

  Mueller, Mario ^a   Kratzer, Regina ^a   Schiller, Margaretha ^a   Slavica, Anita ^b   Rechberger, Gerald ^c   Kollroser, Manfred ^d   Nidetzky, Bernd ^a,b  

^a GRAZ UNIVERSITY OF TECHNOLOGY   (Austria)

^b RESEARCH CENTRE APPLIED BIOCATALYSIS   (Austria)

^c UNIVERSITY OF GRAZ   (Austria)

^d MEDICAL UNIVERSITY OF GRAZ   (Austria)

Author keywords

Cysteine sulfinic and sulfonic acid; d amino acid oxidase; Denaturation pathway; Mass spectrometric characterization of chemical oxidation; Oxidative inactivation; Site directed mutagenesis

Indexed keywords

ASPARTIC ACID; CYSTEIC ACID; CYSTEINE; DEXTRO AMINO ACID OXIDASE; SERINE;

AMINO ACID SUBSTITUTION; ARTICLE; BIOCHEMISTRY; CHEMICAL REACTION KINETICS; COLORIMETRY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME BINDING; ENZYME MODIFICATION; NUCLEOTIDE SEQUENCE; OXIDATION; POINT MUTATION; PRIORITY JOURNAL; TANDEM MASS SPECTROMETRY; THERMOSTABILITY; TRIGONOPSIS VARIABILIS; YEAST;

AMINO ACID OXIDOREDUCTASES; ASCOMYCOTA; BENZOATES; COLORIMETRY; CYSTEINE; KINETICS; MASS SPECTROMETRY; MUTAGENESIS, SITE-DIRECTED; OXYGEN; PEPTIDES; POINT MUTATION; PROTEIN CONFORMATION; QUATERNARY AMMONIUM COMPOUNDS; TEMPERATURE; TRYPSIN;

TRIGONOPSIS VARIABILIS;

EID: 77952321234     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2010.02.009     Document Type: Article

References (53)

1. Davies M.J. The oxidative environment and protein damage. Biochim. Biophys. Acta 1703 (2005) 93-109
2. 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
3. Nyström T. Aging in bacteria. Curr. Opin. Microbiol. 5 (2002) 596-601
4. Stadtman E.R., Arai H., and Berlett B.S. Protein oxidation by the cytochrome P450 mixed-function oxidation system. Biochem. Biophys. Res. Commun. 338 (2005) 432-436
5. Le Moan N., Clement G., Le Maout S., Tacnet F., and Toledano M.B. The Saccharomyces cerevisiae proteome of oxidized protein thiols: contrasted functions for the thioredoxin and glutathione pathways. J. Biol. Chem. 281 (2006) 10420-10430
6. Perez V.I., Buffenstein R., Masamsetti V., Leonard S., Salmon A.B., Mele J., Andziak B., Yang T., Edrey Y., Friguet B., Ward W., Richardson A., and Chaudhuri A. Protein stability and resistance to oxidative stress are determinants of longevity in the longest-living rodent, the naked mole-rat. Proc. Natl. Acad. Sci. U. S. A. 106 (2009) 3059-3064
7. Cross J.V., and Templeton D.J. Thiol oxidation of cell signaling proteins: controlling an apoptotic equilibrium. J. Cell. Biochem. 93 (2004) 104-111
8. 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
9. Poole L.B., and Nelson K.J. Discovering mechanisms of signaling-mediated cysteine oxidation. Curr. Opin. Chem. Biol. 12 (2008) 18-24
10. Konz J.O., King J., and Cooney C.L. Effects of oxygen on recombinant protein expression. Biotechnol. Prog. 14 (1998) 393-409
11. Houde D., Kauppinen P., Mhatre R., and Lyubarskaya Y. Determination of protein oxidation by mass spectrometry and method transfer to quality control. J. Chromatogr. A 1123 (2006) 189-198
12. Orru S., Amoresano A., Siciliano R., Napoleoni R., Finocchiaro O., Datola A., De Luca E., Sirna A., and Pucci P. Structural analysis of modified forms of recombinant IFN-beta produced under stress-simulating conditions. Biol. Chem. 381 (2000) 7-17
13. Stauffer C.E., and Etson D. The effect on subtilisin activity of oxidizing a methionine residue. J. Biol. Chem. 244 (1969) 5333-5338
14. Van Berkel W.J., and Müller F. The elucidation of the microheterogeneity of highly purified p-hydroxybenzoate hydroxylase from Pseudomonas fluorescens by various biochemical techniques. Eur. J. Biochem. 167 (1987) 35-46
15. van der Bolt F.J., Drijfhout M.C., Eppink M.H., Hagen W.R., and van Berkel W.J. Selective cysteine→serine replacements in p-hydroxybenzoate hydroxylase from Pseudomonas fluorescens allow the unambiguous assignment of Cys211 as the site of modification by spin-labeled p-chloromercuribenzoate. Protein Eng. 7 (1994) 801-804
16. Grey C.E., Rundbäck F., and Adlercreutz P. Improved operational stability of chloroperoxidase through use of antioxidants. J. Biotechnol. 135 (2008) 196-201
17. Garcia-Saez I., Docquier J.D., Rossolini G.M., and Dideberg O. The three-dimensional structure of VIM-2, a Zn-β-lactamase from Pseudomonas aeruginosa in its reduced and oxidised form. J. Mol. Biol. 375 (2008) 604-611
18. Fujiwara N., Nakano M., Kato S., Yoshihara D., Ookawara T., Eguchi H., Taniguchi N., and Suzuki K. Oxidative modification to cysteine sulfonic acid of Cys111 in human copper-zinc superoxide dismutase. J. Biol. Chem. 282 (2007) 35933-35944
19. Kemble D.J., and Sun G. Direct and specific inactivation of protein tyrosine kinases in the Src and FGFR families by reversible cysteine oxidation. Proc. Natl. Acad. Sci. U. S. A. 106 (2009) 5070-5075
20. Men L., and Wang Y. The oxidation of yeast alcohol dehydrogenase-1 by hydrogen peroxide in vitro. J. Proteome Res. 6 (2007) 216-225
21. Dib I., Slavica A., Riethorst W., and Nidetzky B. Thermal inactivation of d-amino acid oxidase from Trigonopsis variabilis occurs via three parallel paths of irreversible denaturation. Biotechnol. Bioeng. 94 (2006) 645-654
22. Slavica A., Dib I., and Nidetzky B. Single-site oxidation, cysteine 108 to cysteine sulfinic acid, in d-amino acid oxidase from Trigonopsis variabilis and its structural and functional consequences. Appl. Environ. Microbiol. 71 (2005) 8061-8068
23. Sanchez R., Riddle M., Woo J., and Momand J. Prediction of reversibly oxidized protein cysteine thiols using protein structure properties. Protein Sci. 17 (2008) 473-481
24. Claiborne A., Mallett T.C., Yeh J.I., Luba J., and Parsonage D. Structural, redox, and mechanistic parameters for cysteine-sulfenic acid function in catalysis and regulation. Adv. Protein Chem. 58 (2001) 215-276
25. Jacob C., Lancaster J.R., and Giles G.I. Reactive sulphur species in oxidative signal transduction. Biochem. Soc. Trans. 32 (2004) 1015-1017
26. Kinumi T., Shimomae Y., Arakawa R., Tatsu Y., Shigeri Y., Yumoto N., and Niki E. Effective detection of peptides containing cysteine sulfonic acid using matrix-assisted laser desorption/ionization and laser desorption/ionization on porous silicon mass spectrometry. J. Mass Spectrom. 41 (2006) 103-112
27. 2. Arch. Biochem. Biophys. 450 (2006) 9-19
28. Seth D., and Rudolph J. Redox regulation of MAP kinase phosphatase 3. Biochemistry 45 (2006) 8476-8487
29. Rua J., Soler J., Busto F., and de Arriaga D. Specific and reversible inactivation of Phycomyces blakesleeanus isocitrate lyase by ascorbate-iron: role of two redox-active cysteines. Fungal Genet. Biol. 35 (2002) 223-234
30. Schräder T., and Andreesen J.R. Studies on the inactivation of the flavoprotein d-amino acid oxidase from Trigonopsis variabilis. Appl. Microbiol. Biotechnol. 45 (1996) 458-464
31. +-ATPase caused by Fe- and Cu-containing Fenton reagents. Folia Microbiol. (Praha) 48 (2003) 589-596
32. Fu X., Kassim S.Y., Parks W.C., and Heinecke J.W. Hypochlorous acid oxygenates the cysteine switch domain of pro-matrilysin (MMP-7). A mechanism for matrix metalloproteinase activation and atherosclerotic plaque rupture by myeloperoxidase. J. Biol. Chem. 276 (2001) 41279-41287
33. Fu X., Mueller D.M., and Heinecke J.W. Generation of intramolecular and intermolecular sulfenamides, sulfinamides, and sulfonamides by hypochlorous acid: a potential pathway for oxidative cross-linking of low-density lipoprotein by myeloperoxidase. Biochemistry 41 (2002) 1293-1301
34. Pullar J.M., Vissers M.C., and Winterbourn C.C. Glutathione oxidation by hypochlorous acid in endothelial cells produces glutathione sulfonamide as a major product but not glutathione disulfide. J. Biol. Chem. 276 (2001) 22120-22125
35. Winterbourn C.C., and Brennan S.O. Characterization of the oxidation products of the reaction between reduced glutathione and hypochlorous acid. Biochem. J. 326 (1997) 87-92
36. Giles N.M., Giles G.I., and Jacob C. Multiple roles of cysteine in biocatalysis. Biochem. Biophys. Res. Commun. 300 (2003) 1-4
37. Fürlinger M., Haltrich D., Kulbe K.D., and Nidetzky B. A multistep process is responsible for product-induced inactivation of glucose-fructose oxidoreductase from Zymomonas mobilis. Eur. J. Biochem. 251 (1998) 955-963
38. Kimmel J.L., and Tipton P.A. Inactivation of GDP-mannose dehydrogenase from Pseudomonas aeruginosa by penicillic acid identifies a critical active site loop. Arch. Biochem. Biophys. 441 (2005) 132-140
39. Tishkov V.I., and Popov V.O. Protein engineering of formate dehydrogenase. Biomol. Eng. 23 (2006) 89-110
40. Vintem A.P., Price N.T., Silverman R.B., and Ramsay R.R. Mutation of surface cysteine 374 to alanine in monoamine oxidase A alters substrate turnover and inactivation by cyclopropylamines. Bioorg. Med. Chem. 13 (2005) 3487-3495
41. Yamamoto H., Mitsuhashi K., Kimoto N., Kobayashi Y., and Esaki N. Robust NADH-regenerator: improved alpha-haloketone-resistant formate dehydrogenase. Appl. Microbiol. Biotechnol. 67 (2005) 33-39
42. Dib I., Stanzer D., and Nidetzky B. Trigonopsis variabilis d-amino acid oxidase: control of protein quality and opportunities for biocatalysis through production in Escherichia coli. Appl. Environ. Microbiol. 73 (2007) 331-333
43. Riethorst W., and Reichert A. An industrial view on enzymes for the cleavage of cephalosporin C. Chimia 53 (1999) 600-607
44. Pollegioni L., Butò S., Tischer W., Ghisla S., and Pilone M.S. Characterization of d-amino acid oxidase from Trigonopsis variabilis. Biochem. Mol. Biol. Int. 31 (1993) 709-717
45. Fitzpatrick P.F. Oxidation of amines by flavoproteins. Arch. Biochem. Biophys. 493 (2010) 13-25
46. Pollegioni L., Molla G., Sacchi S., Rosini E., Verga R., and Pilone M.S. Properties and applications of microbial d-amino acid oxidases: current state and perspectives. Appl. Microbiol. Biotechnol. 78 (2008) 1-16
47. Schräder T., and Andreesen J.R. Evidence for the functional importance of Cys298 in d-amino acid oxidase from Trigonopsis variabilis. Eur. J. Biochem. 218 (1993) 735-744
48. Wang W., and Malcolm B.A. Two-stage PCR protocol allowing introduction of multiple mutations, deletions and insertions using QuikChange Site-Directed Mutagenesis. Biotechniques 26 (1999) 680-682
49. Trampitsch C., Slavica A., Riethorst W., and Nidetzky B. Reaction of Trigonopsis variabilis d-amino acid oxidase with 2,6-dichloroindophenol: kinetic characterization and development of an oxygen-independent assay of the enzyme activity. J. Mol. Catal. B Enzym. 32 (2005) 271-278
50. Habeeb A.F.S.A. Reaction of protein sulfhydryl groups with Ellman's reagent. Methods Enzymol. 25 (1972) 457-464
51. Morris J.C. The acid ionization constant of HOCl from 5 to 35°. J. Phys. Chem. 70 (1966) 3798-3805
52. Birner-Gruenberger R., Susani-Etzerodt H., Waldhuber M., Riesenhuber G., Schmidinger H., Rechberger G., Kollroser M., Strauss J.G., Lass A., Zimmermann R., Haemmerle G., Zechner R., and Hermetter A. The lipolytic proteome of mouse adipose tissue. Mol. Cell. Proteomics 4 (2005) 1710-1717
53. Nagy P., and Ashby M.T. Reactive sulfur species: kinetics and mechanisms of the oxidation of cysteine by hypohalous acid to give cysteine sulfenic acid. J. Am. Chem. Soc. 129 (2007) 14082-14091