Crystallographic, spectroscopic, and computational analysis of a flavin C4a-oxygen adduct in choline oxidase

Biochemistry

Volumn 48, Issue 4, 2009, Pages 720-728

  Orville, Allen M ^a   Lountos, George T ^b,c   Finnegan, Steffan ^d   Gadda, Giovanni ^d   Prabhakar, Rajeev ^e  

^a BROOKHAVEN NATIONAL LABORATORY   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d GEORGIA STATE UNIVERSITY   (United States)

^e Department of Biology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITES; CHOLINE OXIDASE; COMPUTATIONAL ANALYSIS; CRYOGENIC TEMPERATURES; DENSITY FUNCTIONAL THEORY CALCULATIONS; FLAVOENZYME; IN-SITU; MICROSPECTROPHOTOMETRY; OH ADDUCTS; RAPID TRANSIENTS; REACTION MECHANISMS; SPECTROSCOPIC METHODS; STABILIZATION ENERGIES; X-RAY BEAMS; X-RAY CRYSTAL STRUCTURES;

DENSITY FUNCTIONAL THEORY; ELECTRONIC STRUCTURE; HYDROGEN; HYDROGEN BONDS; OXYGEN; REACTION KINETICS; SPECTROSCOPIC ANALYSIS;

CRYSTAL STRUCTURE;

CHOLINE OXIDASE; FLAVINE ADENINE NUCLEOTIDE; FLAVOPROTEIN; OXYGEN; PROTON; QUERCETIN; ALCOHOL DEHYDROGENASE; BACTERIAL PROTEIN; ISOALLOXAZINE; RIBOFLAVIN DERIVATIVE;

ARTICLE; COVALENT BOND; CRYSTAL STRUCTURE; DENSITY FUNCTIONAL THEORY; ENZYME ACTIVE SITE; ENZYME MECHANISM; HYDROGEN BOND; KINETICS; MATHEMATICAL ANALYSIS; MICROSPECTROPHOTOMETRY; PRIORITY JOURNAL; TEMPERATURE; X RAY; X RAY CRYSTALLOGRAPHY; ARTHROBACTER; BINDING SITE; BIOLOGY; CHEMISTRY; COMPARATIVE STUDY; ENZYMOLOGY; METABOLISM; METHODOLOGY; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE; SPECTROMETRY;

ALCOHOL OXIDOREDUCTASES; ARTHROBACTER; BACTERIAL PROTEINS; BINDING SITES; COMPUTATIONAL BIOLOGY; CRYSTALLOGRAPHY, X-RAY; FLAVIN-ADENINE DINUCLEOTIDE; FLAVINS; FLAVOPROTEINS; OXYGEN; PROTEIN STRUCTURE, SECONDARY; SPECTROMETRY, X-RAY EMISSION;

EID: 60749096264     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801918u     Document Type: Article

References (44)

1. Massey, V. (2000) The chemical and biological versatility of riboflavin. Biochem. Soc. Trans. 28, 283-296.
2. Mattevi, A. (2006) To be or not to be an oxidase: Challenging the oxygen reactivity of flavoenzymes. Trends Biochem. Sci. 31, 276-283.
3. Entsch, B., Ballou, D. P., and Massey, V. (1976) Flavin-oxygen derivatives involved in hydroxylation by p-hydroxybenzoate hydroxylase. J. Biol. Chem. 251, 2550-2563.
4. Sucharitakul, J., Chaiyen, P., Entsch, B., and Ballou, D. P. (2006) Kinetic mechanisms of the oxygenase from a two-component enzyme, p-hydroxyphenylacetate 3-hydroxylase from Acinetobacter baumannii. J. Biol. Chem. 281, 17044-17053.
5. Abu-Soud, H., Clark, A., Francisco, W., Baldwin, T., and Raushel, F. (1993) Kinetic destabilization of the hydroperoxy flavin intermediate by site-directed modification of the reactive thiol in bacterial luciferase. J. Biol. Chem. 268, 7699-7706.
6. Jones, K. C., and Ballou, D. P. (1986) Reactions of the 4ahydroperoxide of liver microsomal flavin-containing monooxygenase with nucleophilic and electrophilic substrates. J. Biol. Chem. 261, 2553-2559.
7. 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.
8. Mallett, T. C., and Claiborne, A. (1998) Oxygen reactivity of an NADH oxidase C42S mutant: Evidence for a C(4a)-peroxyflavin intermediate and a rate-limiting conformational change. Biochemistry 37, 8790-8802.
9. Massey, V. (1994) Activation of molecular oxygen by flavins and flavoproteins. J. Biol. Chem. 269, 22459-22462.
10. Prabhakar, R., Siegbahn, P. E. M., Minaev, B. F., and Agren, H. (2002) Activation of triplet dioxygen by glucose oxidase: Spinorbit coupling in the superoxide ion. J. Phys. Chem. B 106, 3742-3750.
11. Fan, F., and Gadda, G. (2005) On the catalytic mechanism of choline oxidase. J. Am. Chem. Soc. 127, 2067-2074.
12. 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.
13. 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.
14. 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.
15. Gadda, G., 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.
16. 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 oxidases as a basis for modelling substrate complexes. Acta Crystallogr. D55, 969-977.
17. Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., Montgomery, J. A., Jr., Vreven, T., Kudin, K. N., Burant, J. C., Millam, J. M., Iyengar, S. S., Tomasi, J., Barone, V., Mennucci, B., Cossi, M., Scalmani, G., Rega, N., Petersson, G. A., Nakatsuji, H., Hada, M., Ehara, M., Toyota, K., Fukuda, R., Hasegawa, J., Ishida, M., Nakajima, T., Honda, Y., Kitao, O., Nakai, H., Klene, M., Li, X., Knox, J. E., Hratchian, H. P., Cross, J. B., Bakken, V., Adamo, C., Jaramillo, J., Gomperts, R., Stratmann, R. E., Yazyev, O., Austin, A. J., Cammi, R., Pomelli, C. Ochterski, J. W., Ayala, P. Y., Morokuma, K., Voth, G. A., Salvador, P., Dannenberg, J. J., Zakrzewski, V. G., Dapprich, S., Daniels, A. D., Strain, M. C., Farkas, O., Malick, D. K., Rabuck, A. D., Raghavachari, K., Foresman, J. B., Ortiz, J. V., Cui, Q., Baboul, A. G., Clifford, S., Cioslowski, J., Stefanov, B. B., Liu, G., Liashenko, A., Piskorz, P., Komaromi, I., Martin, R. L., Fox, D. J., Keith, T., Al-Laham, M. A., Peng, C. Y., Nanayakkara, A., Challacombe, M., Gill, P. M. W., Johnson, B., Chen, W., Wong, M. W., Gonzalez, C., and Pople, J. A. (2004) Gaussian 03, revision C1, Gaussian, Inc., Wallingford, CT
18. Becke, A. D. (1988) Density-functional exchange-energy approximation with correct asymptotic behavior. Phys. Rev. A 38, 3098-3100.
19. Becke, A. D. (1993) Density-functional thermochemistry. III. The role of exact exchange. J. Chem. Phys. 98, 5648-5652.
20. Lee, C. T., Yang, W. T., and Parr, R. G. (1988) Development of the Colle-Salvetti correlation-energy formula into a functional of the electron-density. Phys. Rev. B 37, 785-789.
21. Cances, E., Mennucci, B., and Tomasi, J. (1997) A new integral equation formalism for the polarizable continuum model: Theoretical background and applications to isotropic and anisotropic dielectrics. J. Chem. Phys. 107, 3032-3041.
22. Prabhakar, R., Morokuma, K., and Musaev, D. G. (2005) A comparative study of various computational approaches in calculating the structure of pyridoxal 5'-phosphate (PLP)-dependent β-lyase protein. The importance of protein environment. J. Comput. Chem. 26, 443-446.
23. De la Mora-Rey, T., and Wilmot, C. M. (2007) Synergy within structural biology of single crystal optical spectroscopy and X-ray crystallography. Curr. Opin. Struct. Biol. 17, 580-586.
24. Siddiqui, M. S., and Stanley, R. J. (2005) A cryogenic optical waveguide spectrometer for the measurement of low-temperature absorption spectra of dilute biological samples. Anal. Biochem. 337, 121-129.
25. 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.
26. Dixon, D. A., Lindner, D. L., Branchaud, B., and Lipscomb, W. N. (1979) Conformations and electronic structures of oxidized and reduced isoalloxazine. Biochemistry 18, 5770-5775.
27. Ridder, L., Harvey, J. N., Rietjens, I. M. C. M., Vervoort, J., and Mulholland, A. J. (2003) Ab initio QM/MM modeling of the hydroxylation step in p-hydroxybenzoate hydroxylase. J. Phys. Chem. B 107, 2118-2126.
28. Ridder, L., Mulholland, A. J., Rietjens, I. M. C. M., and Vervoort, J. (2000) A quantum mechanical/molecular mechanical study of the hydroxylation of phenol and halogenated derivatives by phenol hydroxylase. J. Am. Chem. Soc. 122, 8728-8738.
29. Schlichting, I., Berendzen, J., Chu, K., Stock, A. M., Maves, S. A., Benson, D. E., Sweet, R. M., Ringe, D., Petsko, G. A., and Sligar, S. G. (2000) The catalytic pathway of cytochrome p450cam at atomic resolution. Science 287, 1615-1622.
30. Karlsson, A., Parales, J. V., Parales, R. E., Gibson, D. T., Eklund, H., and Ramaswamy, S. (2003) Crystal structure of naphthalene dioxygenase: Side-on binding of dioxygen to iron. Science 299, 1039-1042.
31. Katona, G., Carpentier, P., Niviere, V., Amara, P., Adam, V., Ohana, J., Tsanov, N., and Bourgeois, D. (2007) Raman-assisted crystallography reveals end-on peroxide intermediates in a nonheme iron enzyme. Science 316, 449-453.
32. 2+ dioxygenase superoxo, alkylperoxo, and bound product intermediates. Science 316, 453-457.
33. Wilmot, C. M., Hajdu, J., McPherson, M. J., Knowles, P. F., and Phillips, S. E. (1999) Visualization of dioxygen bound to copper during enzyme catalysis. Science 286, 1724-1728.
34. Iwata, M., Bruice, T. C., Carrell, H. L., and Glusker, J. P. (1980) Reactions of 4a-peroxides and 4a-pseudobases of N10- and N5-phenethylflavins. J. Am. Chem. Soc. 102, 5036-5044.
35. Xu, G., and Chance, M. R. (2007) Hydroxyl radical-mediated modification of proteins as probes for structural proteomics. Chem. Rev. 107, 3514-3543.
36. Gray, H. B., and Winkler, J. R. (1996) Electron transfer in proteins. Annu. Rev. Biochem. 65, 537-561.
37. 3O2 with dihydroflavins. 1. N3,5-Dimethyl-1,5- dihydrolumiflavin and 1,5-dihydroisoalloxazines. J. Am. Chem. Soc. 99, 7272-7286.
38. Bach, R. D., and Dmitrenko, O. (2003) Electronic Requirements for Oxygen Atom Transfer from Alkyl Hydroperoxides. Model Studies on Multisubstrate Flavin-Containing Monooxygenases. J. Phys. Chem. B 107, 12851-12861.
39. Srajer, V., Teng, T., Ursby, T., Pradervand, C., Ren, Z., Adachi, S., Schildkamp, W., Bourgeois, D., Wulff, M., and Moffat, K. (1996) Photolysis of the carbon monoxide complex of myoglobin: Nanosecond time-resolved crystallography. Science 274, 1726-1729.
40. Schotte, F., Lim, M., Jackson, T. A., Smirnov, A. V., Soman, J., Olson, J. S., Phillips, G. N., Jr., Wulff, M., and Anfinrud, P. A. (2003) Watching a protein as it functions with 150-ps time-resolved X-ray crystallography. Science 300, 1944-1947.
41. 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.
42. 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.
43. 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.
44. 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.