Importance of the gating segment in the substrate-recognition loop of pyranose 2-oxidase

FEBS Journal

Volumn 277, Issue 13, 2010, Pages 2892-2909

  Spadiut, Oliver ^a   Tan, Tien Chye ^a,b   Pisanelli, Ines ^c   Haltrich, Dietmar ^c   Divne, Christina ^a,b  

^a ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

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

Author keywords

Active site loop; Alanine scanning mutagenesis; Crystal structure; Pyranose 2 oxidase; Site saturation mutagenesis

Indexed keywords

1,4 BENZOQUINONE; ENZYME; ENZYME VARIANT; FERROCENE; FLUORODEOXYGLUCOSE; HYDROQUINONE; MELIBIOSE; OXYGEN; PYRANOSE 2 OXIDASE; QUINONE DERIVATIVE; SUGAR; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARTICLE; CRYSTAL STRUCTURE; DELETION MUTANT; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME SPECIFICITY; MUTAGENESIS; OXIDATION; PRIORITY JOURNAL; PROTEIN FOLDING; SEQUENTIAL ANALYSIS; STRUCTURE ANALYSIS; TRAMETES;

CARBOHYDRATE DEHYDROGENASES; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; KETOSES; KINETICS; LIGNIN; MODELS, MOLECULAR; MOLECULAR STRUCTURE; SUBSTRATE SPECIFICITY; TRAMETES;

FUNGI; TRAMETES OCHRACEA;

EID: 77953606976     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2010.07705.x     Document Type: Article

References (51)

1. Janssen FW Ruelius HW (1968) Carbohydrate oxidase, novel enzyme from Polyporus obtusus. II. Specificity and characterization of reaction products. Biochim Biophys Acta 167, 501-510.
2. Volc J, Denisova NP, Nerud F Musílek V (1985) Glucose-2-oxidase activity in mycelial cultures of basidiomycetes. Folia Microbiol 30, 141-147.
3. 2 during wood degradation by Phanerochaete chrysosporium, Trametes versicolor, and Oudemansiella mucida. Appl Environ Microbiol 60, 2524-2532.
4. Leitner C, Haltrich D, Nidetzky B, Prillinger H Kulbe KD (1998) Production of a novel pyranose 2-oxidase by basidiomycete Trametes multicolor. Appl Biochem Biotechnol 70-72, 237-248.
5. Hallberg BM, Leitner C, Haltrich D Divne C (2004) Crystal structure of the 270 kDa homotetrameric lignin-degrading enzyme pyranose 2-oxidase. J Mol Biol 341, 781-796.
6. Ander P Marzullo L (1997) Sugar oxidoreductases and veratryl alcohol oxidase as related to lignin degradation. J Biotechnol 53, 115-131.
7. Volc J, Kubátová E, Daniel G Prikrylová V (1996) Only C-2 specific glucose oxidase activity is expressed in ligninolytic cultures of the white rot fungus Phanerochaete chrysosporium. Arch Microbiol 165, 421-424.
8. Leitner C, Volc J Haltrich D (2001) Purification and characterization of pyranose oxidase from the white rot fungus Trametes multicolor. Appl Environ Microbiol 67, 3636-3644.
9. Baute R, Baute MA Deffieux G (1987) Proposed pathway to the pyrones cortalcerone and microthecin in fungi. Phytochemistry 26, 1395-1397.
10. Gabriel J, Volc J, Kubátová E, Palkova Z Pospisek M (1994) A convenient laboratory procedure for the preparation of cortalcerone, a fungal antibiotic beta-pyrone. Carbohydr Res 252, 297-301.
11. Freimund S, Huwig A, Giffhorn F Köpper S (1998) Rare keto-aldoses from enzymatic oxidation: substrates and oxidation products of pyranose oxidase. Chem Eur J 4, 2442-2455.
12. Prongjit M, Sucharitakul J, Wongnate T, Haltrich D Chaiyen P (2009) Kinetic mechanism of pyranose 2-oxidase from Trametes multicolor. Biochemistry 48, 4170-4180.
13. Ghisla S Massey V (1989) Mechanisms of flavoprotein-catalyzed reactions. Eur J Biochem 181, 1 17.
14. Artolozaga MJ, Kubátová E, Volc J Kalisz HM (1997) Pyranose 2-oxidase from Phanerochaete chrysosporium - further biochemical characterisation. Appl Microbiol Biotechnol 47, 508-514.
15. Menon V, Hsieh C-T Fitzpatrick PE (1995) Substituted alcohols as mechanistic probes of alcohol oxidase. Bioorg Chem 23, 42-53.
16. Fitzpatrick PF (2001) Substrate dehydrogenation by flavoproteins. Acc Chem Res 34, 299-307.
17. Hallberg BM, Henriksson G, Pettersson G Divne C (2002) Crystal structure of the flavoprotein domain of the extracellular flavocytochrome cellobiose dehydrogenase. J Mol Biol 315, 421-434.
18. Hallberg BM, Henriksson G, Pettersson G, Vasella A Divne C (2003) Mechanism of the reductive half-reaction in cellobiose dehydrogenase. J Biol Chem 278, 7160-7166.
19. Kujawa M, Ebner H, Leitner C, Hallberg BM, Prongjit M, Sucharitakul J, Ludwig R, Rudsander U, Peterbauer C, Chaiyen P et al. (2006) Structural basis for substrate binding and regioselective oxidation of monosaccharides at C-3 by pyranose 2-oxidase. J Biol Chem 281, 35104-35115.
20. Spadiut O, Leitner C, Tan TC, Ludwig R, Divne C Haltrich D (2008) Mutations of Thr169 affect substrate specificity of pyranose 2-oxidase from Trametes multicolor. Biocatal Biotransformation 26, 120-127.
21. Pitsawong W, Sucharitakul J, Prongjit M, Tan TC, Spadiut O, Haltrich D, Divne C Chaiyen P (2010) A conserved active-site threonine is important for both sugar and flavin oxidations of pyranose 2-oxidase. J Biol Chem 285, 9697-9705.
22. Haltrich D, Leitner C, Neuhauser W, Nidetzky B, Kulbe KD Volc J (1998) A convenient enzymatic procedure for the production of aldose-free d-tagatose. Ann NY Acad Sci 864, 295-299.
23. Spadiut O, Nguyen TT Haltrich D (2010) Thermostable variants of pyranose 2-oxidase showing altered substrate selectivity for glucose and galactose. J Agric Food Chem 58, 3465-3471.
24. Morley KL Kazlauskas RJ (2005) Improving enzyme properties: when are closer mutations better? Trends Biotechnol 23, 231-237.
25. Lovell SC, Davis IW, Arendall WB, de Bakker PI, Word JM, Prisant MG, Richardson JS Richardson DC (2003) Structure validation by Cα geometry: φ, ψ and Cβ deviation. Proteins 50, 437-450.
26. Spadiut O, Leitner C, Salaheddin C, Varga B, Vertessy B, Tan TC, Divne C Haltrich D (2009) Improving thermostability and catalytic activity of pyranose 2-oxidase from Trametes multicolor by rational and semi-rational design. FEBS J 276, 776-792.
27. Spadiut O, Radakovits K, Pisanelli I, Salaheddin C, Yamabhai M, Tan TC, Divne C Haltrich D (2009) A thermostable triple mutant of pyranose 2-oxidase from Trametes multicolor with improved properties for biotechnological applications. Biotechnol J 4, 525-534.
28. Rozovsky S McDermott AE (2001) The time scale of the catalytic loop motion in triosephosphate isomerase. J Mol Biol 310, 259-270.
29. Gutteridge A Thornton J (2004) Conformational change in substrate binding, catalysis and product release: an open and shut case? FEBS Lett 567, 67-73.
30. Boehr DD, McElheny D, Dyson HJ Wright PE (2006) The dynamic energy landscape of dihydrofolate reductase catalysis. Science 313, 1638-1642.
31. Fetrow JS, Horner SR, Oehrl W, Schaak DL, Boose TL Burton RE (1997) Analysis of the structure and stability of omega loop A replacements in yeast iso-1-cytochrome c. Protein Sci 6, 197-210.
32. Roitel O, Ivinova O, Muronetz V, Nagradova N Branlant G (2002) Thermal unfolding used as a probe to characterize the intra- and intersubunit stabilizing interactions in phosphorylating d-glyceraldehyde-3-phosphate dehydrogenase from Bacillus stearothermophilus. Biochemistry 41, 7556-7564.
33. Wang L, Rivera EV, Benavides-Garcia MG Nall BT (2005) Loop entropy and cytochrome c stability. J Mol Biol 353, 719-729.
34. Sucharitakul J, Prongjit M, Haltrich D Chaiyen P (2008) Detection of a C4a-hydroperoxyflavin intermediate in the reaction of a flavoprotein oxidase. Biochemistry 47, 8485-8490.
35. Sampson NS, Kass IJ Ghoshroy KB (1998) Assessment of the role of an omega loop of cholesterol oxidase: a truncated loop mutant has altered substrate specificity. Biochemistry 37, 5770-5778.
36. Zhou HX McCammon JA (2009) The gates of ion channels and enzymes. Trends Biochem Sci 35, 179-185.
37. Malmström BG (1982) Enzymology of oxygen. Annu Rev Biochem 51, 21-59.
38. Ho SN, Hunt HD, Horton RM, Pullen JK Pease LR (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51-59.
39. Li S Wilkinson MF (1997) Site-directed mutagenesis: a two-step method using PCR and DpnI. BioTechniques 4, 588-590.
40. Danneel HJ, Ullrich M Giffhorn F (1992) Goal-oriented screening method for carbohydrate oxidases produced by filamentous fungi. Enzyme Microb Technol 14, 898-903.
41. Polizzi KM, Bommarius AS, Broering JM Chaparro-Riggers JF (2007) Stability of biocatalysts. Curr Opin Chem Biol 11, 220-225.
42. ®-adapted flavin ad hoc detection system for protein folding and ligand binding. FEBS J 276, 2833-2840.
43. Kabsch W (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J Appl Crystallogr 26, 795-800.
44. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC Read RJ (2007) Phaser crystallographic software. J Appl Crystallogr 40, 658-674.
45. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr D Biol Crystallogr 50, 760-763.
46. Murshudov GN, Vagin AA Dodson EJ (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr D Biol Crystallogr 53, 240-255.
47. Painter J Merritt EA (2006) Optimal description of a protein structure in terms of multiple groups undergoing TLS motion. Acta Crystallogr D Biol Crystallogr 62, 439-450.
48. Jones TA, Zou JY, Cowan SW Kjeldgaard M (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr A 47, 110-119.
49. Emsley P Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60, 2126-2132.
50. DeLano WL (2002) The PyMOL Molecular Graphics System. DeLano Scientific
51. Kleywegt GJ Jones TA (1994) Detection, delineation, measurement and display of cavities in macromolecular structures. Acta Crystallogr D Biol Crystallogr 50, 178-185.