Hydride Transfer Made Easy in the Reaction of Alcohol Oxidation Catalyzed by Flavin-dependent Oxidases

Biochemistry

Volumn 47, Issue 52, 2008, Pages 13745-13753

  Gadda, Giovanni ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE RESIDUES; ALCOHOL DEHYDROGENASE; ALCOHOL OXIDATION; ALKOXIDES; ARTHROBACTER GLOBIFORMIS; ATOMIC LEVELS; CHOLINE OXIDASE; COFACTORS; ELECTRON ACCEPTOR; ENZYME-SUBSTRATE COMPLEXES; FLAVIN-DEPENDENT; GLYCINE BETAINE; HYDRIDE TRANSFERS; HYDROGEN BONDING INTERACTIONS; MECHANISTIC STUDIES; ORGANIC COFACTORS; OXIDATION OF ALCOHOLS; OXIDOREDUCTASES; QUANTUM MECHANICAL; SUBSTRATE ACTIVATION; WILD TYPES;

ALDEHYDES; CATALYSTS; COMPLEXATION; HYDROGEN BONDS; MOLECULAR OXYGEN; OXIDATION; QUANTUM THEORY; REACTION INTERMEDIATES; SUBSTRATES; ZINC;

ENZYMES;

ALCOHOL DEHYDROGENASE; CARBON; CHOLINE OXIDASE; HYDRIDE; HYDROXYL GROUP; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; OXIDE; OXIDOREDUCTASE; PROTON; QUERCETIN; UNCLASSIFIED DRUG; ZINC; ALCOHOL DERIVATIVE; HYDROGEN; RIBOFLAVIN DERIVATIVE;

ALCOHOL OXIDATION; ARTHROBACTER GLOBIFORMIS; ARTICLE; ATOM; CATALYSIS; CHELATION; CHEMICAL REACTION; ENZYME ACTIVATION; ENZYME MECHANISM; ENZYME METABOLISM; ENZYME STABILITY; ENZYME SUBSTRATE COMPLEX; ION TRANSPORT; NONHUMAN; PRIORITY JOURNAL; QUANTUM CHEMISTRY; ARTHROBACTER; CHEMISTRY; ENZYMOLOGY; METABOLISM; OXIDATION REDUCTION REACTION; REVIEW;

ARTHROBACTER GLOBIFORMIS;

ALCOHOL OXIDOREDUCTASES; ALCOHOLS; ARTHROBACTER; CATALYSIS; FLAVINS; HYDROGEN; NADP; OXIDATION-REDUCTION;

EID: 58849100936     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi801994c     Document Type: Article

References (79)

1. 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.
2. Gadda, G., and McAllister-Wilkins, E. E. (2003) Cloning, expression, and purification of choline dehydrogenase from the moderate halophile Halomonas elongata. Appl. Environ. Microbiol. 69, 2126-2132.
3. Menon, V., Hsieh, C. T., and Fitzpatrick, P. F. (1995) Substituted alcohols as mechanistic probes of alcohol oxidase. Bioorg. Chem. 23, 42-53.
4. Kohen, A., Jonsson, T., and Klinman, J. P. (1997) Effects of protein glycosylation on catalysis: changes in hydrogen tunneling and enthalpy of activation in the glucose oxidase reaction. Biochemistry 36, 2603-2611.
5. Chen, L., Lyubimov, A. Y., Brammer, L., Vrielink, A., and Sampson, N. S. (2008) The binding and release of oxygen and hydrogen peroxide are directed by a hydrophobic tunnel in cholesterol oxidase. Biochemistry 47, 5368-5377.
6. Sucharitakul, J., Prongjit, M., Haltrich, D., and Chaiyen, P. (2008) Detection of a C4a-hydrope:roxyflavin intermediate in the reaction of a flavoprotein oxidase. Biochemistry 47, 8485-8490.
7. Sygmund, C., Kittl, R., Vole, J., Halada, P., Kubatova, E., Haltrich, D., and Peterbauer, C. K. (2008) Characterization of pyranose dehydrogenase from Agaricus meleagris and its application in the C-2 specific conversion of D-galactose. J. Biotechnol. 133, 334-342.
8. Leferink, N. C., Heuts, D. P., Fraaije, M. W., and van Berkel, W. J. (2008) The growing VAO flavoprotein family. Arch. Biochem. Biophys. 474, 292-301.
9. Forneris, F., Heuts, D. P., Delvecchio, M., Rovida, S., Fraaije, M. W., and Mattevi, A. (2008) Structural analysis of the catalytic mechanism and stereoselectivity in Streptomyces coelicolor alditol oxidase. Biochemistry 47, 978-985.
10. Murray, M. S., Holmes, R. P., and Lowther, W. T. (2008) Active site and loop 4 movements within human glycolate oxidase: implications for substrate specificity and drug design. Biochemistry 47, 2439-2449.
11. Furuichi, M., Suzuki, N., Dhakshnamoorhty, B., Minagawa, H., Yamagishi, R., Watanabe, Y., Goto, Y., Kaneko, H., Yoshida, Y., Yagi, H., Waga, I., Kumar, P. K., and Mizuno, H. (2008) X-ray structures of Aerococcus viridans lactate oxidase and its complex with D-lactate at pH 4.5 show an a-hydroxyacid oxidation mechanism. J. Mol. Biol. 378, 436-446.
12. Tsai, C. L., Gokulan, K., Sobrado, P., Sacchettini, J. C., and Fitzpatrick, P. F. (2007) Mechanistic and structural studies of H373Q flavocytochroine b2: effects of mutating the active site base. Biochemistry 46, 7844-7851.
13. Massey, V. (2000) The chemical and biological versatility of riboflavin. Biochem. Soc. Trans. 28, 283-296.
14. Fitzpatrick, P. F. (2001) Substrate dehydrogenation by flavoproteins. Acc. Chem. Res. 34, 299-307.
15. Fitzpatrick, P. F. (2004) Carbanion versus hydride transfer mechanisms in flavoprotein-catalyzed dehydrogenations. Bioorg. Chem. 32, 125-139.
16. Ghanem, M., Fan, F., Francis, K., and Gadda, G. (2003) Spectroscopic and kinetic properties of recombinant choline oxidase from Arthrobacter globiformis. Biochemistry 42, 15179-15188.
17. Fan, F., Ghanem, M., and Gadda, G. (2004) Cloning, sequence analysis, and purification of choline oxidase from Arthrobacter globiformis: a bacterial enzyme involved in osmotic stress tolerance. Arch. Biochem. Biophys. 421, 149-158.
18. Ghanem, M., and Gadda, G. (2006) Effects of reversing the protein positive charge in the proximity of the flavin N(1) locus of choline oxidase. Biochemistry 45, 3437-3447.
19. Hoang, J. V., and Gadda, G. (2007) Trapping choline oxidase in a nonfunctional conformation by freezing at low pH. Proteins 66, 611-620.
20. 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.
21. Ghanem, M., and Gadda, G. (2005) On the catalytic role of the conserved active site residue His466 of choline oxidase. Biochemistry 44, 893-904.
22. Finnegan, S., and Gadda, G. (2008) Substitution of an active site valine uncovers a kinetically slow equilibrium between competent and incompetent forms of choline oxidase. Biochemistry 47, 13850-13861.
23. Gadda, G. (2003) pH and deuterium kinetic isotope effects studies on the oxidation of choline to betaine-aldehyde catalyzed by choline oxidase. Biochim. Biophys. Acta 1650, 4-9.
24. Gadda, G. (2003) Kinetic mechanism of choline oxidase from Arthrobacter globiformis. Biochim. Biophys. Acta 1646, 112-118.
25. Gadda, C., Powell, N. L., and Menon, P. (2004) The trimethylammonium headgroup of choline is a major determinant for substrate binding and specificity in choline oxidase. Arch. Biochem. Biophys. 430, 264-273.
26. Fan, F., and Gadda, G. (2005) Oxygen- and temperature-dependent kinetic isotope effects in choline oxidase: correlating reversible hydride transfer with environmentally enhanced tunneling. J. Am. Chem. Soc. 127, 17954-17961.
27. Fan, F., and Gadda, G. (2005) On the catalytic mechanism of choline oxidase. J. Am. Chem. Soc. 127, 2067-2074.
28. Fan, F., Germann, M. W., and Gadda, G. (2006) Mechanistic studies of choline oxidase with betaine aldehyde and its isosteric analogue 3,3-dimethylbutyraldehyde. Biochemistry 45, 1979-1986.
29. Gadda, C., Fan, F., and Hoang, J. V. (2006) On the contribution of the positively charged headgroup of choline to substrate binding and catalysis in the reaction catalyzed by choline oxidase. Arch. Biochem. Biophys. 451, 182-187.
30. Fan, F., and Gadda, G. (2007) An internal equilibrium preorganizes the enzyme-substrate complex for hydride tunneling in choline oxidase. Biochemistry 46, 6402-6408.
31. Ikuta, S., Imamura, S., Misaki, H., and Horiuti, Y. (1977) Purification and characterization of choline oxidase from Arthrobacter globiformis. J. Biochem. 82, 1741-1749.
32. Yue, Q. K., Kass, I. J., Sampson, N. S., and Vrielink, A. (1999) Crystal structure determination of cholesterol oxidase from Streptomyces and structural characterization of key active site mutants. Biochemistry 38, 4211-4286.
33. Li, J., Vrielink, A., Brick, P., and Blow, D. M. (1993) Crystal structure of cholesterol oxidase complexed with a steroid substrate: implications for flavin adenine dinucleotide dependent alcohol oxidases. Biochemistry 32, 11507-11515.
34. Bannwarth, M., Bastian, S., Heckmann-Pohl, D., Giffhorn, F., and Schulz, G. E. (2004) Crystal structure of pyranose 2-oxidase from the white-rot fungus Peniophora sp. Biochemistry 43, 11683-11690.
35. 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.
36. Kujawa, M., Ebner, H., Leitner, C., Hallberg, B. M., Prongjit, M., Sucharitakul, J., Ludwig, R., Rudsander, U., Peterbauer, C., Chaiyen, P., Haltrich, D., and Divne, C. (2006) Structural basis for substrate binding and regioselective oxidation of monosaccharides at C3 by pyranose 2-oxidase. J. Biol. Chem. 281, 35104-35115.
37. Wohlfahrt, C., Witt, S., Hendle, J., Schomburg, D., Kalisz, H. M., and Hecht, H. J. (1999) 1.8 and 1.9 A resolution structures of the Penicillium amagasakiense and Aspergillus niger glucose oxidases as a basis for modelling substrate complexes. Acta Crystallogr., Sect. D 55, 969-911.
38. Kiess, M., Hecht, H. J., and Kalisz, H. M. (1998) Glucose oxidase from Penicillium amagasakiense. Primary structure and comparison with other glucose-methanol-choline (GMC) oxidoreductases. Eur. J. Biochem. 252, 90-99.
39. 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 A resolution. J. Mol. Biol. 229, 153-172.
40. Hecht, H. J., Schomburg, D., Kalisz, H., and Schmid, R. D. (1993) The 3D structure of glucose oxidase from Aspergillus niger. Implications for the use of GOD as a biosensor enzyme. Biosens. Bioelectron. 8, 197-203.
41. 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.
42. Ghisla, S., and Massey, V. (1986) New flavins for old: artificial flavins as active site probes of flavoproteins. Biochem. J. 239, 1-12.
43. Mincey, T., Tayrien, C., Mildvan, A. S., and Abeles, R. H. (1980) Presence of a flavin semiquinone in methanol oxidase. Proc. Natl. Acad. Sci. U.S.A. 77, 7099-7101.
44. Sobrado, P., Daubner, S. C., and Fitzpatrick, P. F. (2001) Probing the relative timing of hydrogen abstraction steps in the flavocytochrome b2 reaction with primary and solvent deuterium isotope effects and mutant enzymes. Biochemistry 40, 994-1001.
45. Bright, H. J., and Gibson, Q. H. (1967) The oxidation of 1-deuterated glucose by glucose oxidase. J. Biol. Chem. 242, 994-1003.
46. Kass, I. J., and Sampson, N. S. (1998) The importance of Glu361 position in the reaction catalyzed by cholesterol oxidase. Bioorg. Med. Chem. Lett. 8, 2663-2668.
47. 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.
48. 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.
49. Bannwarth, M., Heckmann-Pohl, D., Bastian, S., Giffhorn, F., and Schulz, G. E. (2006) Reaction geometry and thermostable variant of pyranose 2-oxidase from the white-rot fungus Peniophora sp. Biochemistry 45, 6587-6595.
50. Rotsaert, F. A., 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.
51. Muh, U., Williams, C. H., Jr., and Massey, V. (1994) Lactate monooxygenase. II. Site-directed mutagenesis of the postulated active site base histidine 290. J. Biol. Chem. 269, 7989-7993.
52. a of the activesite histidine in flavocytochrome b2 (yeast L-lactate dehydrogenase). Protein Sci. 7, 1531-1537.
53. Gaume, B., Sharp, R. E., Manson, F. D., Chapman, S. K., Reid, G. A., and Lederer, F. (1995) Mutation to glutamine of histidine 373, the catalytic base of flavocytochrome b2 (L-lactate dehydrogenase). Biochimie 77, 621-630.
54. Lehoux, I. E., and Mitra, B. (1999) (S)-Mandelate dehydrogenase from Pseudomonas putida: mutations of the catalytic base histidine274 and chemical rescue of activity. Biochemistry 38, 9948-9955.
55. Sobrado, P., and Fitzpatrick, P. F. (2003) Solvent and primary deuterium isotope effects show that lactate CH and OH bond cleavages are concerted in Y254F flavocytochrome b2, consistent with a hydride transfer mechanism. Biochemistry 42, 15208-15214.
56. Seymour, S. L., and Klinman, J. P. (2002) Comparison of rates and kinetic isotope effects using PEG-modified variants and glycoforms of glucose oxidase: the relationship of modification of the protein envelope to C-H activation and tunneling. Biochemistry 41, 8747-8758.
57. El-Kabbani, O., Darmanin, C., and Chung, R. P. (2004) Sorbitol dehydrogenase: structure, function and ligand design. Curr. Med. Chem. 11, 465-476.
58. Plapp, B. V., Eklund, H., Jones, T. A., and Branden, C. I. (1983) Three-dimensional structure of isonicotinimidylated liver alcohol dehydrogenase. J. Biol. Chem. 258, 5537-5547.
59. Adolph, H. W., Zwart, P., Meijers, R., Hubatsch, I., Kiefer, M., Lamzin, V., and Cedergren-Zeppezauer, E. (2000) Structural basis for substrate specificity differences of horse liver alcohol dehydrogenase isozymes. Biochemistry 39, 12885-12897.
60. Cho, H., Ramaswamy, S., and Plapp, B. V. (1997) Flexibility of liver alcohol dehydrogenase in stereoselective binding of 3-butylthiolane 1-oxides. Biochemistry 36, 382-389.
61. Zheng, Y. J., Xia, Z., Chen, Z., Mathews, F. S., and Bruice, T. C. (2001) Catalytic mechanism of quinoprotein methanol dehydrogenase: A theoretical and x-ray crystallographic investigation. Proc. Natl. Acad. Sci. U.S.A. 98, 432-434.
62. Xia, Z. X., He, Y. N., Dai, W. W., White, S. A., Boyd, G. D., and Mathews, F. S. (1999) Detailed active site configuration of a new crystal form of methanol dehydrogenase from Methylophilus W3A1 at 1.9 Å resolution. Biochemistry 38, 1214-1220.
63. Xia, Z. X., Dai, W. W., He, Y. N., White, S. A., Mathews, F. S., and Davidson, V. L. (2003) X-ray structure of methanol dehydrogenase from Paracoccus denitrificans and molecular modeling of its interactions with cytochrome c-551i. J. Biol. Inorg. Chem. 8, 843-854.
64. Oubrie, A., Rozeboom, H. J., Kalk, K. H., Huizinga, E. C., and Dijkstra, B. W. (2002) Crystal structure of quinohemoprotein alcohol dehydrogenase from Comamonas testosteroni: structural basis for substrate oxidation and electron transfer. J. Biol. Chem. 277, 3727-3732.
65. Oubrie, A., and Dijkstra, B. W. (2000) Structural requirements of pyrroloquinoline quinone dependent enzymatic reactions. Protein Sci. 9, 1265-1273.
66. Vignaud, C., Pietrancosta, N., Williams, E. L., Rumsby, C., and Lederer, F. (2007) Purification and characterization of recombinant human liver glycolate oxidase. Arch. Biochem. Biophys. 465, 410-416.
67. Mowat, C. G., Wehenkel, A., Green, A. J., Walkinshaw, M. D., Reid, G. A., and Chapman, S. K. (2004) Altered substrate specificity in flavocytochrome b2: structural insights into the mechanism of L-lactate dehydrogenation. Biochemistry 43, 9519-9526.
68. Gondry, M., Dubois, J., Terrier, M., and Lederer, F. (2001) The catalytic role of tyrosine 254 in flavocytochrome b2 (L-lactate dehydrogenase from baker's yeast). Comparison between the Y254F and Y254L mutant proteins. Eur. J. Biochem. 268, 4918-4927.
69. Yorita, K., Misaki, H., Palfey, B. A., and Massey, V. (2000) On the interpretation of quantitative structure-function activity relationship data for lactate oxidase. Proc. Natl. Acad. Sci. U.S.A. 97, 2480-2485.
70. Billeter, S. R., Webb, S. P., Agarwal, P. K., Iordanov, T., and Hammes-Schiffer, S. (2001) Hydride transfer in liver alcohol dehydrogenase: quantum dynamics, kinetic isotope effects, and role of enzyme motion. J. Am. Chem. Soc. 123, 11262-11272.
71. LeBrun, L. A., Park, D. H., Ramaswamy, S., and Plapp, B. V. (2004) Participation of histidine-51 in catalysis by horse liver alcohol dehydrogenase. Biochemistry 43, 3014-3026.
72. + complex controls formation of the ternary complexes. Biochemistry 44, 12797-12808.
73. Klinman, J. P. (1976) Isotope effects and structure-reactivity correlations in the yeast alcohol dehydrogenase reaction. A study of the enzyme-catalyzed oxidation of aromatic alcohols. Biochemistry 15, 2018-2026.
74. Kohen, A., Cannio, R., Bartolucci, S., and Klinman, J. P. (1999) Enzyme dynamics and hydrogen tunnelling in a thermophilic alcohol dehydrogenase. Nature 399, 496-499.
75. Liang, Z. X., Tsigos, I., Lee, T., Bouriotis, V., Resing, K. A., Ahn, N. G., and Klinman, J. P. (2004) Evidence for increased local flexibility in psychrophilic alcohol dehydrogenase relative to its thermophilic homologue. Biochemistry 43, 14676-14683.
76. Reddy, S. Y., and Bruice, T. C. (2004) Mechanism of glucose oxidation by quinoprotein soluble glucose dehydrogenase: insights from molecular dynamics studies. J. Am. Chem. Soc. 126, 2431-2438.
77. Anthony, C., and Williams, P. (2003) The structure and mechanism of methanol dehydrogenase. Biochim. Biophys. Acta 1647, 18-23.
78. Jongejan, A., Jongejan, J. A., and Hagen, W. R. (2001) Direct hydride transfer in the reaction mechanism of quinoprotein alcohol dehydrogenases: a quantum mechanical investigation. J. Comput. Chem. 22, 1732-1749.
79. Olsthoorn, A. J., and Duine, J. A. (1998) On the mechanism and specificity of soluble, quinoprotein glucose dehydrogenase in the oxidation of aldose sugars. Biochemistry 37, 13854-13861.