Crystal structure of the 270 kDa homotetrameric lignin-degrading enzyme pyranose 2-oxidase

Journal of Molecular Biology

Volumn 341, Issue 3, 2004, Pages 781-796

  Martin Hallberg, B ^a   Leitner, Christian ^b   Haltrich, Dietmar ^b   Divne, Christina ^a  

^a ALBANOVA UNIVERSITY CENTER   (Sweden)

^b UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

Author keywords

ChOx, cholesterol oxidase; crystal structure; FAD, flavin adenine dinucleotide; GMC oxidoreductase; GMC, glucose methanol choline; GOx, glucose 1 oxidase; lignin degradation; P2Ox, pyranose 2 oxidase; pyranose 2 oxidase; regioselective sugar biotransformation

Indexed keywords

ACETIC ACID; CARBON; CARBOXYLIC ACID; CHOLINE; FUNGAL ENZYME; GLUCOSE; HYDROGEN PEROXIDE; LIGNIN; METHANOL; MONOSACCHARIDE; NITROGEN; PEROXIDASE; PYRANOSE 2 OXIDASE; SOLVENT; SUGAR; TETRAMER; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; CYTOPLASM; ENZYME ACTIVE SITE; ENZYME DEGRADATION; ENZYME SPECIFICITY; ENZYME SUBSTRATE; FUNGUS HYPHAE; MOLECULAR WEIGHT; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN INTERACTION; PROTEIN STRUCTURE;

FUNGI; TRAMETES; TRAMETES OCHRACEA;

EID: 4344582358     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.06.033     Document Type: Article

References (62)

1. Kirk T.K., Cullen D. Enzymology and molecular genetics of wood degradation by white-rot fungi. Young R.A., Akhtar M. Environmentally Friendly Technologies for the Pulp and Paper Industry. 1998;273-307 Wiley, New York. chapt. 9
2. ten Have R., Teunissen P.J. Oxidative mechanisms involved in lignin degradation by white-rot fungi. Chem. Rev. 101:2001;3397-3413
3. 2 during wood degradation by Phanerochaete chrysosporium, Trametes versicolor, and Oudemansiella mucida. Appl. Environ. Microbiol. 60:1994;2524-2532
4. Volc J., Denisova N.P., Nerud F., Musílek V. Glucose-2-oxidase activity in mycelial cultures of basidiomycetes. Folia Microbiol. 30:1985;141-147
5. Leitner C., Haltrich D., Nidetzky B., Prillinger H., Kulbe K.D. Production of a novel pyranose 2-oxidase by basidiomycete Trametes multicolor. Appl. Biochem. Biotechnol. 70-72:1998;237-248
6. Machida Y., Nakanishi T. Purification and properties of pyranose oxidase from Coriolus versicolor. Agric. Biol. Chem. 48:1984;2463-2470
7. Volc J., Eriksson K.-E. Pyranose 2-oxidase from Phanerochaete chrysosporium. Methods Enzymol. 161:1988;316-322
8. Danneel H.-J., Rössner E., Zeeck A., Giffhorn F. Purification and characterization of a pyranose oxidase from the basidiomycete Peniophora gigantea and chemical analyses of its reaction products. Eur. J. Biochem. 214:1993;795-802
9. Schäfer A., Bieg S., Huwig A., Kohring G.-W., Giffhorn F. Purification by immunoaffinity chromatography, characterization, and structural analysis of a thermostable pyranose oxidase from the white-rot fungus Phlebiopsis gigantea. Appl. Environ. Microbiol. 62:1996;2586-2592
10. Artolozaga M.J., Kubátová E., Volc J., Kalisz H.M. Pyranose 2-oxidase from Phanerochaete chrysosporium - further biochemical characterisation. Appl. Microbiol. Biotechnol. 47:1997;508-514
11. Leitner C., Volc J., Haltrich D. Purification and characterization of pyranose oxidase from the white rot fungus Trametes multicolor. Appl. Environ. Microbiol. 67:2001;3636-3644
12. Albrecht M., Lengauer T. Pyranose oxidase identified as a member of the GMC oxidoreductase family. Bioinformatics. 19:2003;1216-1220
13. Hallberg B.M., Leitner C., Haltrich D., Divne C. Crystallization and preliminary X-ray diffraction analysis of pyranose 2-oxidase from the white-rot fungus Trametes multicolor. Acta Crystallog. sect. D. 60:2004;197-199
14. Cavener D.R. GMC oxidoreductases. A newly defined family of homologous proteins with diverse catalytic activities. J. Mol. Biol. 223:1992;811-814
15. Giffhorn F. Fungal pyranose oxidases: occurrence, properties and biotechnical applications in carbohydrate chemistry. Appl. Microbiol. Biotechnol. 54:2000;727-740
16. Volc J., Sedmera P., Havlícek V., Prikrylová V., Daniel G. Conversion of D-glucose to D-erythro-hexos-2,3-diulose (2,3-diketo-D-glucose) by enzyme preparations from the basidiomycete Oudemansiella mucida. Carbohydr. Res. 278:1995;59-70
17. Freimund S., Huwig A., Giffhorn F., Köpper S. Rare keto-aldoses from enzymatic oxidation: substrates and oxidation products of pyranose 2-oxidase. Chem. Eur. J. 4:1998;2442-2455
18. Giffhorn F., Köpper S., Huwig A., Freimund S. Rare sugars and and sugar-based synthons by chemo-enzymatic synthesis. Enzyme Microb. Technol. 27:2000;734-742
19. Halada P., Leitner C., Sedmera P., Haltrich D., Volc J. Identification of the covalent flavin adenine dinucleotide-binding region in pyranose 2-oxidase from Trametes multicolor. Anal. Biochem. 314:2003;235-242
20. Perrakis A., Morris R., Lamzin V.S. Automated protein model building combined with iterative structure refinement. Nature Struct. Biol. 6:1999;458-463
21. Laskowski R.A., MacArthur M.W., Moss D.S., Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26:1993;283-291
22. Kleywegt G.J., Jones T.A. Phi/psichology: Ramachandran revisited. Structure. 4:1996;1395-1400
23. Vecerek B., Maresova H., Kocanova M., Kyslik P. Molecular cloning and expression of the pyranose 2-oxidase cDNA from Trametes ochracea MB49 in Escherichia coli. Appl. Microbiol. Biotechnol. 64:2003;525-530
24. Nishimura I., Okada K., Koyama Y. Cloning and expression of pyranose oxidase cDNA from Coriolus versicolor in Escherichia coli. J. Biotechnol. 52:1996;11-20
25. Wierenga R.K., DeJong R.J., Kalk K.H., Hol W.G.J. Crystal structure of p-hydroxybenzoate hydroxylase. J. Mol. Biol. 131:1979;55-73
26. Mattevi A. The PHBH fold: not only in flavoenzymes. Biophys. Chem. 70:1998;217-222
27. Hallberg B.M., Henriksson G., Pettersson G., Divne C. Crystal structure of the flavoprotein domain of the extracellular flavocytochrome cellobiose dehydrogenase. J. Mol. Biol. 315:2002;421-434
28. Rossmann, M. G., Liljas, A., Brändén, C. I. & Banaszak, L. J. (1975). Evolutionary and structural relationships among dehydrogenases. In The Enzymes (Boyer, P. D., ed.), vol. 11, pp. 61-102, Academic Press, New York.
29. Wierenga R.K., Drenth J., Schulz G.E. Comparison of the three-dimensional protein and nucleotide structure of the FAD-binding domain of p-hydroxybenzoate hydroxylase with the FAD- as well as NADPH-binding domains of glutathione reductase. J. Mol. Biol. 167:1983;725-739
30. Wierenga R.K., Terpstra P., Hol W.G.J. Prediction of the occurrence of the ADP-binding beta alpha beta-fold in proteins, using an amino acid sequence fingerprint. J. Mol. Biol. 187:1986;101-107
31. Raices M., Paifer E., Cremata J., Montesino R., Ståhlberg J., Divne C., et al. Cloning and characterization of a cDNA encoding a cellobiose dehydrogenase from the white rot fungus Phanerochaete chrysosporium. FEBS Letters. 369:1995;233-238
32. 2-producing enzyme pyranose oxidase in Phanerochaete chrysosporium grown under liquid culture conditions. Appl. Environ. Micobiol. 58:1992;3667-3676
33. Lee B., Richards F.M. The interpretation of protein structures: estimation of static accessibility. J. Mol. Biol. 55:1971;379-400
34. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography & NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D. 54:1998;905-921
35. Guillén F., Martínez M.J., Munoz C., Martínez A.T. Quinone redox cycling in the ligninolytic fungus Pleurotus eryngii leading to extracellular production of superoxide anion radical. Arch. Biochem. Biophys. 339:1997;190-199
36. Volc J., Kubátová E., Wood D.A., Daniel G. Pyranose 2-dehydrogenase, a novel sugar oxidoreductase from the basidiomaycete Agaricus bisporus. Arch. Microbiol. 167:1997;119-125
37. Mewies M., McIntire W.S., Scrutton N.S. Covalent attachment of flavin adenine dinucleotide (FAD) and flavin mononucleotide (FMN) to enzymes: the current state of affairs. Protein Sci. 7:1998;7-20
38. Vrielink A., Lloyd L.F., Blow D.M. Crystal structure of cholesterol oxidase from Brevibacterium sterolicum refined at 1.8 Å resolution. J. Mol. Biol. 219:1991;533-554
39. Hecht H.J., Kalisz H.M., Hendle J., Schmid R.D., Schomburg D. Crystal structure of glucose oxidase from Aspergillus niger refined at 2.3 Å resolution. J. Mol. Biol. 229:1993;153-172
40. Li J., Vrielink A., Brick P., Blow D.M. Crystal structure of cholecterol oxidase complexed with a steroid substrate: implications for flavin adenine dinucleotide dependent alcohol oxidases. Biochemistry. 32:1993;11507-11515
41. Hallberg B.M., Henriksson G., Pettersson G., Vasella A., Divne C. Mechanism of the reductive half reaction in cellobiose dehydrogenase. J. Biol. Chem. 278:2003;7160-7166
42. Kass I.J., Sampson N.S. Evaluation of the role of His447 in the reaction catalyzed by cholesterol oxidase. Biochemistry. 37:1998;17990-18000
43. Yamashita M., Toyama M., Ono H., Fujii I., Hirayama N., Murooka Y. Separation of the two reactions, oxidation and isomerization, catalyzed by Streptomyces cholesterol oxidase. Protein Eng. 11:1998;1075-1081
44. Yue Q.K., Kass I.J., Sampson N.S., Vrielink A. Crystal structure determination of cholesterol oxidase from Streptomyces and structural characterization of key active site mutants. Biochemistry. 38:1999;4277-4286
45. Witt S., Wohlfahrt G., Schomburg D., Hecht H.-J., Kalisz H.M. Conserved arginine-516 of Penicillium amagasakiense glucose oxidase is essential for the efficient binding of β-D-glucose. Biochem. J. 347:2000;553-559
46. Rotsaert F.A.J., Renganathan V., Gold M.H. Role of the flavin domain residues, His689 and Asn732, in the catalytic mechanism of cellobiose dehydrogenase from Phanerochaete chrysosporium. Biochemistry. 42:2003;4049-40556
47. Lario P.I., Sampson N., Vrielink A. Sub-atomic resolution crystal structure of cholesterol oxidase: what atomic resolution crystallography reveals about enzyme mechanism and the role of the FAD cofactor in redox activity. J. Mol. Biol. 326:2003;1635-1650
48. Yin Y., Sampson N.S., Vrielink A., Lario P.I. The presence of a hydrogen bond between asparagine 485 and the pi system of FAD modulates the redox potential in the reaction catalyzed by cholesterol oxidase. Biochemistry. 40:2001;13779-13787
49. Treitz G., Maria G., Giffhorn F., Heinzle E. Kinetic model discrimination via step-by-step experimental and computational procedure in the enzymatic oxidation of D-glucose. J. Biotechnol. 85:2001;271-287
50. Wohlfahrt G., Witt S., Hendle J., Schomburg D., Kalisz H.M., Hecht H.-J. 1.8 and 1.9 Å resolution structures of the Penicillium amagasakiense and Aspergillus niger glucose oxidases as a basis for modelling substrate complexes. Acta Crystallog. sect. D. 55:1999;969-977
51. Dreveny I., Gruber K., Glieder A., Thompson A., Kratky C. The hydroxynitrile lyase from almond: a lyase that looks like an oxidoreductase. Structure. 9:2001;803-815
52. Schulz G.E., Schirmer R.H., Sachsenheimer W., Pai E.F. The structure of the flavoenzyme glutathione reductase. Nature. 273:1978;120-124
53. Matthews B.W. Solvent content of protein crystals. J. Mol. Biol. 33:1968;491-497
54. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:1997;307-326
55. Kabsch W. Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallog. 26:1993;795-800
56. Schneider T.R., Sheldrick G.M. Substructure solution with SHELXD. Acta Crystallog. sect. D. 58:2002;1772-1779
57. Terwilliger T.C., Berendzen J. Automated structure solution for MIR and MAD. Acta Crystallog. sect. D. 55:1999;849-861
58. Terwilliger T.C. Automated structure solution, density modification and model building. Acta Crystallog. sect. D. 58:2002;1937-1940
59. Cowtan K. 'dm' an automated procedure for phase improvement by density modification. Joint CCP4 ESF-EACBM Newsletter Protein Crystallog. 31:1994;34-38
60. Murshudov G.N., Vagin A.A., Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallog. sect. D. 53:1997;240-255
61. Jones T.A., Zou J.-Y., Cowan S.W., Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A. 47:1991;110-119
62. Kleywegt G.J., Jones T.A. Detection, delineation, measurement and display of cavities in macromolecular structures. Acta Crystallog. sect. D. 50:1994;178-185