Role of active site histidines in the two half-reactions of the aryl-alcohol oxidase catalytic cycle

Biochemistry

Volumn 51, Issue 33, 2012, Pages 6595-6608

  Hernández Ortega, Aitor ^a   Lucas, Fátima ^b   Ferreira, Patricia ^d   Medina, Milagros ^d   Guallar, Victor ^b,c   Martínez, Angel T ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b BARCELONA SUPERCOMPUTING CENTER   (Spain)

^c INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^d UNIVERSITY OF ZARAGOZA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; ARYL-ALCOHOL OXIDASE; CATALYTIC BASE; CATALYTIC CYCLES; COMPUTATIONAL SIMULATION; ELECTRON TRANSFER; FLAVOENZYMES; HALF-REACTIONS; HYDRIDE TRANSFERS; LIGNIN DEGRADATION; ORDERS OF MAGNITUDE; PROTON ABSTRACTION; QUANTUM MECHANICAL/MOLECULAR MECHANICAL; REDOX STATE; SOLVENT KINETIC ISOTOPE EFFECTS; STEREO-SELECTIVE;

AMINO ACIDS; DEGRADATION; DEUTERIUM; ELECTRON TRANSITIONS; MOLECULAR MODELING;

PROTON TRANSFER;

ARYL ALCOHOL OXIDASE; HISTIDINE DERIVATIVE; HYDROPEROXIDE; HYDROXYL GROUP; OXIDOREDUCTASE; OXYGEN; PROTON; QUERCETIN; SOLVENT; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CRYSTAL STRUCTURE; ELECTRON TRANSPORT; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME METABOLISM; KINETIC ISOTOPE EFFECT; KINETICS; MOLECULAR MECHANICS; MUTAGENESIS; OXIDATION REDUCTION STATE; PH; PRIORITY JOURNAL; PROTEIN TRANSPORT; QUANTUM MECHANICS; STEADY STATE; STEREOCHEMISTRY;

ALCOHOL OXIDOREDUCTASES; BENZYL ALCOHOLS; CATALYSIS; CATALYTIC DOMAIN; FLAVINS; HISTIDINE; HYDROGEN-ION CONCENTRATION; KINETICS; MUTATION; OXIDATION-REDUCTION; PLEUROTUS; QUANTUM THEORY;

EID: 84865428476     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300505z     Document Type: Article

References (61)

1. Ferreira, P., Medina, M., Guillén, F., Martínez, M. J., van Berkel, W. J. H., and Martínez, A. T. (2005) Spectral and catalytic properties of aryl-alcohol oxidase, a fungal flavoenzyme acting on polyunsaturated alcohols Biochem. J. 389, 731-738 (Pubitemid 41117333)
2. Ruiz-Dueñas, F. J. and Martínez, A. T. (2009) Microbial degradation of lignin: How a bulky recalcitrant polymer is efficiently recycled in nature and how we can take advantage of this Microbial Biotechnol. 2, 164-177
3. Martínez, A. T., Ruiz-Dueñas, F. J., Martínez, M. J., del Río, J. C., and Gutiérrez, A. (2009) Enzymatic delignification of plant cell wall: from nature to mill Curr. Opin. Biotechnol. 20, 348-357
4. Varela, E., Martínez, A. T., and Martínez, M. J. (1999) Molecular cloning of aryl-alcohol oxidase from Pleurotus eryngii, an enzyme involved in lignin degradation Biochem. J. 341, 113-117 (Pubitemid 29359054)
5. Varela, E., Martínez, M. J., and Martínez, A. T. (2000) Aryl-alcohol oxidase protein sequence: A comparison with glucose oxidase and other FAD oxidoreductases Biochim. Biophys. Acta 1481, 202-208 (Pubitemid 30658096)
6. Hecht, H. J., Kalisz, H. M., Hendle, J., Schmid, R. D., and Schomburg, D. (1993) Crystal structure of glucose oxidase from Aspergillus niger refined at 2.3 Å resolution J. Mol. Biol. 229, 153-172 (Pubitemid 23037920)
7. Hallberg, B. M., Leitner, C., Haltrich, D., and Divne, C. (2004) Crystal structure of the 270 kDa homotetrameric lignin- degrading enzyme pyranose 2-oxidase J. Mol. Biol. 341, 781-796 (Pubitemid 39118411)
8. Vrielink, A., Lloyd, L. F., and Blow, D. M. (1991) Crystal structure of cholesterol oxidase from Brevibacterium sterolicum refined at 1.8 Å resolution J. Mol. Biol. 219, 533-554
9. Quaye, O., Lountos, G. T., Fan, F., Orville, A. M., and Gadda, G. (2008) Role of Glu312 in binding and positioning of the substrate for the hydride transfer reaction in choline oxidase Biochemistry 47, 243-256
10. Hallberg, B. M., Henriksson, G., Pettersson, G., and Divne, C. (2002) Crystal structure of the flavoprotein domain of the extracellular flavocytochrome cellobiose dehydrogenase J. Mol. Biol. 315, 421-434 (Pubitemid 34729350)
11. Fernández, I. S., Ruiz-Dueñas, F. J., Santillana, E., Ferreira, P., Martínez, M. J., Martínez, A. T., and Romero, A. (2009) Novel structural features in the GMC family of oxidoreductases revealed by the crystal structure of fungal aryl-alcohol oxidase Acta Crystallogr. D. Biol. Crystallogr. 65, 1196-1205
12. Sakai, Y. and Tani, Y. (1992) Cloning and sequencing of the alcohol oxidase-encoding gene (AODI) from the formaldehyde-producing asporogeneus methylotrophic yeast, Candida boidinii S2 Gene 114, 67-73
13. Gadda, G. (2008) Hydride transfer made easy in the reaction of alcohol oxidation catalyzed by flavin-dependent oxidases Biochemistry 47, 13745-13753
14. Kass, I. J. and Sampson, N. S. (1998) Evaluation of the role of His447 in the reaction catalyzed by cholesterol oxidase Biochemistry 37, 17990-18000 (Pubitemid 29023955)
15. Witt, S., Wohlfahrt, G., Schomburg, D., Hecht, H. J., and Kalisz, H. M. (2000) Conserved arginine-516 of Penicillium amagasakiense glucose oxidase is essential for the efficient binding of β- d -glucose Biochem. J. 347, 553-559 (Pubitemid 30229404)
16. Yin, Y., Liu, P., Anderson, R. G., and Sampson, N. S. (2002) Construction of a catalytically inactive cholesterol oxidase mutant: investigation of the interplay between active site-residues glutamate 361 and histidine 447 Arch. Biochem. Biophys. 402, 235-242 (Pubitemid 34848641)
17. Rotsaert, F. A. J., Renganathan, V., and Gold, M. H. (2003) Role of the flavin domain residues, His689 and Asn732, in the catalytic mechanism of cellobiose dehydrogenase from Phanerochaete chrysosporium Biochemistry 42, 4049-4056 (Pubitemid 36418298)
18. Ghanem, M. and Gadda, G. (2005) On the catalytic role of the conserved active site residue His466 of choline oxidase Biochemistry 44, 893-904 (Pubitemid 40129649)
19. Rungsrisuriyachai, K. and Gadda, G. (2010) Role of asparagine 510 in the relative timing of substrate bond cleavages in the reaction catalyzed by choline oxidase Biochemistry 49, 2483-2490
20. Wongnate, T., Sucharitakul, J., and Chaiyen, P. (2011) Identification of a catalytic base for sugar oxidation in the pyranose-2 oxidation reaction ChemBioChem 12, 2577-2586
21. Hernández-Ortega, A., Borrelli, K., Ferreira, P., Medina, M., Martínez, A. T., and Guallar, V. (2011) Substrate diffusion and oxidation in GMC oxidoreductases: An experimental and computational study on fungal aryl-alcohol oxidase Biochem. J. 436, 341-350
22. Massey, V. (1994) Activation of molecular oxygen by flavins and flavoproteins J. Biol. Chem. 269, 22459-22462 (Pubitemid 24273342)
23. Mattevi, A. (2006) To be or not to be an oxidase: challenging the oxygen reactivity of flavoenzymes Trends Biochem. Sci. 31, 276-283 (Pubitemid 43674353)
24. Klinman, J. P. (2007) How do enzymes activate oxygen without inactivating themselves? Acc. Chem. Res. 40, 325-333
25. Gadda, G. (2012) Oxygen activation in flavoprotein oxidases: The importance of being positive Biochemistry 10.1021/bi300277d
26. Pennati, A. and Gadda, G. (2011) Stabilization of an Intermediate in the Oxidative Half-Reaction of Human Liver Glycolate Oxidase Biochemistry 50, 1-3
27. 2-producing enzyme Protein Express Purif. 45, 191-199 (Pubitemid 41773326)
28. Macheroux, P. (1999) UV-visible spectroscopy as a tool to study flavoproteins, in Flavoprotein Protocols (Chapman, S. and Reid, G. A., Eds.) pp 1-7, Humana Press, Totowa, USA.
29. Ferreira, P., Hernández-Ortega, A., Herguedas, B., Martínez, A. T., and Medina, M. (2009) Aryl-alcohol oxidase involved in lignin degradation: A mechanistic study based on steady and pre-steady state kinetics and primary and solvent isotope effects with two different alcohol substrates J. Biol. Chem. 284, 24840-24847
30. Hernández-Ortega, A., Ferreira, P., Merino, P., Medina, M., Guallar, V., and Martínez, A. T. (2012) Stereoselective hydride transfer by aryl-alcohol oxidase, a member of the GMC superfamily ChemBioChem 13, 427-435
31. Maestro 9.2 (2011) Schrödinger Inc., New York.
32. Borrelli, K. W., Vitalis, A., Alcantara, R., and Guallar, V. (2005) PELE: Protein energy landscape exploration. A novel Monte Carlo based technique J. Chem. Theory Comput. 1, 1304-1311
33. 2 reactivity in a fungal flavoenzyme: Involvement of aryl-alcohol oxidase Phe-501 contiguous to catalytic histidine J. Biol. Chem. 286, 41105-41114
34. Jaguar 7.8 (2011) Schrödinger Inc., New York.
35. Zhao, Y. and Truhlar, D. G. (2008) The M06 suite of density functionals for main group thermochemistry, thermochemical kinetics, noncovalent interactions, excited states, and transition elements: two new functionals and systematic testing of four M06-class functionals and 12 other functionals Theor. Chem. Acc. 120, 215-241
36. Jensen, F. (1999) Introduction to Computational Chemistry, John Wiley and Sons, Chichester, UK.
37. QSite 4.5 (2007) Schrödinger, Inc., Portland, OR.
38. Ferreira, P., Hernández-Ortega, A., Herguedas, B., Rencoret, J., Gutiérrez, A., Martínez, M. J., Jiménez-Barbero, J., Medina, M., and Martínez, A. T. (2010) Kinetic and chemical characterization of aldehyde oxidation by fungal aryl-alcohol oxidase Biochem. J. 425, 585-593
39. Abramovitz, A. S. and Massey, V. (1976) Interaction of phenols with old yellow enzyme-Physical evidence for charge-transfer complexes J. Biol. Chem. 251, 5327-5336
40. Nakanishi, Y., Ohashi, K., and Tsuge, H. (1984) Essential histidyl residues in glucose oxidase. Chemical modification of histidyl residues with diethylpyrocarbonate Agric. Biol. Chem. 48, 2951-2959
41. Wohlfahrt, G., Witt, S., Hendle, J., Schomburg, D., Kalisz, H. M., and Hecht, H.-J. (1999) 1.8 and 1.9 Å resolution structures of the Penicillium amagasakiense and Aspergillus niger glucose oxidase as a basis for modelling substrate complexes Acta Crystallogr. D. Biol. Crystallogr. 55, 969-977 (Pubitemid 29235594)
42. Gutiérrez, A., Caramelo, L., Prieto, A., Martínez, M. J., and Martínez, A. T. (1994) Anisaldehyde production and aryl-alcohol oxidase and dehydrogenase activities in ligninolytic fungi from the genus Pleurotus Appl. Environ. Microbiol. 60, 1783-1788 (Pubitemid 24165819)
43. 2 production by Pleurotus eryngii Appl. Environ. Microbiol. 60, 2811-2817 (Pubitemid 24242273)
44. Brinkley, D. W. and Roth, J. P. (2005) Determination of a large reorganization energy barrier for hydride abstraction by glucose oxidase J. Am. Chem. Soc. 127, 15720-15721 (Pubitemid 41643278)
45. Menon, V., Hsieh, C. T., and Fitzpatrick, P. F. (1995) Substituted alcohols as mechanistic probes of alcohol oxidase Bioorg. Chem. 23, 42-53
46. Meyer, M., Wohlfahrt, G., Knäblein, J., and Schomburg, D. (1998) Aspects of the mechanism of catalysis of glucose oxidase: A docking, molecular mechanics and quantum chemical study J. Comput.-Aided Mol. Des. 12, 425-440 (Pubitemid 128512815)
47. Lario, P. I., Sampson, N., and Vrielink, A. (2003) 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, 1635-1650 (Pubitemid 36269098)
48. Rungsrisuriyachai, K. and Gadda, G. (2008) On the role of histidine 351 in the reaction of alcohol oxidation catalyzed by choline oxidase Biochemistry 47, 6762-6769 (Pubitemid 351898931)
49. Piubelli, L., Pedotti, M., Molla, G., Feindler-Boeckh, S., Ghisla, S., Pilone, M. S., and Pollegioni, L. (2008) On the oxygen reactivity of flavoprotein oxidases-An oxygen access tunnel and gate in Brevibacterium sterolicum cholesterol oxidase J. Biol. Chem. 283, 24738-24747
50. Kommoju, P. R., Bruckner, R. C., Ferreira, P., Carrell, C. J., Mathews, F. S., and Jorns, M. S. (2009) Factors that affect oxygen activation and coupling of the two redox cycles in the aromatization reaction catalyzed by NikD, an unusual amino acid oxidase Biochemistry 48, 9542-9555
51. Sucharitakul, J., Prongjit, M., Haltrich, D., and Chaiyen, P. (2008) Detection of a C4a-hydroperoxyflavin intermediate in the reaction of a flavoprotein oxidase Biochemistry 47, 8485-8490
52. 2 with dihydroflavins. 1. N3,5-Dimethyl-1,5- dihydrolumiflavin and 1,5-dihydroisoalloxazines J. Am. Chem. Soc. 99, 7272-7286
53. Orville, A. M., Lountos, G. T., Finnegan, S., Gadda, G., and Prabhakar, R. (2009) Crystallographic, spectroscopic, and computational analysis of a flavin C4a-oxygen adduct in choline oxidase Biochemistry 48, 720-728
54. Sucharitakul, J., Wongnate, T., and Chaiyen, P. (2011) Hydrogen peroxide elimination from C4a-hydroperoxyflavin in a flavoprotein oxidase occurs through a single proton transfer from flavin N5 to a peroxide leaving group J. Biol. Chem. 286, 16900-16909
55. 2 by the flavoprotein glucose oxidase Proc. Natl. Acad. Sci. U.S.A. 100, 62-67 (Pubitemid 36078030)
56. Su, Q. and Klinman, J. P. (1999) Nature of oxygen activation in glucose oxidase from Aspergillus niger: the importance of electrostatic stabilization in superoxide formation Biochemistry 38, 8572-8581
57. 2 probed using chemically modified flavins bound to glucose oxidase J. Am. Chem. Soc. 126, 15120-15131 (Pubitemid 39561733)
58. Finnegan, S., Agniswamy, J., Weber, I. T., and Gadda, G. (2010) Role of valine 464 in the flavin oxidation reaction catalyzed by choline oxidase Biochemistry 49, 2952-2961
59. Zhao, G. H., Bruckner, R. C., and Jorns, M. S. (2008) Identification of the oxygen activation site in monomeric sarcosine oxidase: Role of Lys265 in catalysis Biochemistry 47, 9124-9135
60. McDonald, C. A., Fagan, R. L., Collard, F., Monnier, V. M., and Palfey, B. A. (2011) Oxygen reactivity in flavoenzymes: Context matters J. Am. Chem. Soc. 133, 16809-16811
61. Pozzi, M. H. and Fitzpatrick, P. F. (2010) A lysine conserved in the monoamine oxidase family is involved in oxidation of the reduced flavin in mouse polyamine oxidase Arch. Biochem. Biophys. 498, 83-88