Role of ser-257 in the sliding mechanism of NADP(H) in the reaction catalyzed by the aspergillus fumigatus flavin-dependent ornithine N 5-monooxygenase SidA

Journal of Biological Chemistry

Volumn 288, Issue 45, 2013, Pages 32440-32448

  Shirey, Carolyn ^a   Badieyan, Somayesadat ^a   Sobrado, Pablo ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASPERGILLUS FUMIGATUS; FLAVIN-DEPENDENT; KINETIC ISOTOPE EFFECTS; MOLECULAR DYNAMICS SIMULATIONS; REACTION CATALYZED; SITE DIRECTED MUTAGENESIS; SLIDING MECHANISM; STOPPED-FLOW KINETICS;

AMINO ACIDS; ASPERGILLUS; ISOTOPES; MOLECULAR DYNAMICS; STABILIZATION;

CATALYSIS;

C4A HYDROPEROXYFLAVIN; NICOTINAMIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; QUERCETIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SIDEROPHORE; SIDEROPHORE A; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CONTROLLED STUDY; MOLECULAR DYNAMICS; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REDUCTION; SITE DIRECTED MUTAGENESIS; STEADY STATE;

ASPERGILLUS; C4A-HYDROPEROXYFLAVIN; FLAVIN; FLAVIN-DEPENDENT MONOOXYGENASE; MOLECULAR DYNAMICS; MUTAGENESIS; N-HYDROXYLATING; NADP(H) ROLE; SIDA; SIDEROPHORES;

AMINO ACID SUBSTITUTION; ASPERGILLUS FUMIGATUS; CATALYSIS; FLAVINS; FUNGAL PROTEINS; MIXED FUNCTION OXYGENASES; MUTAGENESIS, SITE-DIRECTED; MUTATION, MISSENSE; NADP; SERINE;

EID: 84887486191     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.487181     Document Type: Article

References (37)

1. van Berkel, W. J., Kamerbeek, N. M., and Fraaije, M. W. (2006) Flavopro-tein monooxygenases, a diverse class of oxidative biocatalysts. J. Biotech-nol 124, 670-689
2. Massey, V. (1994) Activation of molecular oxygen by flavins and flavopro-teins. J. Biol Chem. 269, 22459-22462
3. Torres Pazmino, D. E., Winkler, M., Glieder, A., and Fraaije, M. W. (2010) Monooxygenases as biocatalysts: classification, mechanistic aspects and biotechnological applications. J. Biotechnol. 146, 9-24
4. Ziegler, D. M. (2002) An overview of the mechanism, substrate specificities, and structure of FMOs. DrugMetab. Rev. 34, 503-511
5. Chocklett, S. W., and Sobrado, P. (2010) Aspergillus fumigates SidA is a highly specific ornithine hydroxylase with bound flavin cofactor. Biochemistry 49, 6777-6783
6. Franceschini, S., Fedkenheuer, M., Vogelaar, N. J., Robinson, H. H., Sobrado, P., and Mattevi, A. (2012) Structural insight into the mechanism of oxygen activation and substrate selectivity of flavin-dependent AT-hy-droxylating monooxygenases. Biochemistry 51, 7043-7045
7. Eisendle, M., Oberegger, H., Zadra, I., and Haas, H. (2003) The sidero-phore system is essential for viability of Aspergillus nidulans: functional analysis of two genes encoding L-ornithine N5-monooxygenase (SidA) and a non-ribosomal peptide synthetase (SidC). Mol. Microbiol. 49, 359-375
8. Hissen, A. H., Wan, A. N., Warwas, M. L., Pinto, L. J., and Moore, M. M. (2005) The Aspergillus fumigatus siderophore biosynthetic gene sidA, encoding L-ornithine N5-oxygenase, is required for virulence. Infect. Immun. 73, 5493-5503
9. Chaiyen, P., Fraaije, M. W., and Mattevi, A. (2012) The enigmatic reaction of flavins with oxygen. Trends Biochem. Sci. 37, 373-380
10. Beaty, N. B., and Ballou, D. P. (1980) Transient kinetic study of liver microsomal FAD-containing monooxygenase. J. Biol. Chem. 255, 3817-3819
11. Beaty, N. B., and Ballou, D. P. (1981) The oxidative half-reaction of liver microsomal FAD-containing monooxygenase. J. Biol. Chem. 256, 4619-4625
12. Torres Pazmino, D. E., Baas, B. J., Janssen, D. B., and Fraaije, M. W. (2008) Kinetic mechanism of phenylacetone monooxygenase from Thermobifida fusca. Biochemistry 47, 4082-4093
13. Sheng, D., Ballou, D. P., and Massey, V. (2001) Mechanistic studies of cyclohexanone monooxygenase: chemical properties of intermediates involved in catalysis. Biochemistry 40, 11156-11167
14. Orru, R., Dudek, H. M., Martinoli, C, Torres Pazmino, D. E., Royant, A., Weik, M., Fraaije, M. W., and Mattevi, A. (2011) Snapshots of enzymatic Baeyer-Villiger catalysis. Oxygen activation and intermediate stabilization. J. Biol. Chem 286, 29284-29291
15. Mirza, I. A., Yachnin, B. J., Wang, S., Grosse, S., Bergeron, H., Imura, A., Iwaki, H., Hasegawa, Y., Lau, P. C, and Berghuis, A. M. (2009) Crystal structures of cyclohexanone monooxygenase reveal complex domain movements and a sliding cofactor. J. Am. Chem. Soc. 131, 8848-8854
16. Romero, E., Fedkenheuer, M., Chocklett, S. W., Qi, J., Oppenheimer, M., and Sobrado, P. (2012) Dual role of NADP(H) in the reaction of a flavin dependent AT-hydroxylating monooxygenase. Biochim. Biophys. Acta 1824, 850-857
17. Robinson, R., and Sobrado, P. (2011) Substrate binding modulates the activity of Mycobacterium smegmatis G, a flavin-dependent monooxygenase involved in the biosynthesis of hydroxamate-containing sidero-phores. Biochemistry 50, 8489-8496
18. Jeong, S. S., and Gready, J. E. (1994) A method of preparation and purification of (4R)-deuterated-reduced nicotinamide adenine dinucleotide phosphate. Anal. Biochem. 221, 273-277
19. Hess, B. (2008) P-LINCS: a parallel linear constraint solver for molecular simulation. J. Chem. Theory Comput 4, 116-122
20. Oostenbrink, C, Villa, A, Mark, A. E., and van Gunsteren, W. F. (2004) A biomolecular force field based on the free enthalpy of hydration and solvation: the GROMOS force-field parameter sets 53A5 and 53A6. J. Comput. Chem. 25, 1656-1676
21. Han, A, Robinson, R. M., Badieyan, S., Ellerbrock, J., and Sobrado, P. (2013) Tryptophan-47 in the active site of Methylophaga sp. strain SKI flavin-monooxygenase is important for hydride transfer. Arch, Biochem. Biophys. 532, 46-53
22. Anandakrishnan, R., Aguilar, B., and Onufriev, A. V. (2012) H++ 3.0: automating pK prediction and the preparation of biomolecular structures for atomistic molecular modeling and simulations. Nucleic Acids Res. 40, W537-W541
23. Berendsen, H. J. C, Postma, J. P. M., van Gunsteren, W. F., DiNola, A, and Haak, J. R. (1984) Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81, 3684-3690
24. Badieyan, S., Bevan, D. R, and Zhang, C. (2012) A salt-bridge controlled by ligand binding modulates the hydrolysis reaction in a GH5 endoglucanase. Protein Eng. Des. Set 25, 223-233
25. Darden, T., York, D., and Pedersen, L. (1993) Particle mesh Ewald: an N.log(N) method for Ewald sums in large systems. J. Chem, Phys. 98, 10089-10092
26. Mayfield, J. A., Frederick, R. E., Streit, B. R., Wencewicz, T. A., Ballou, D. P., and DuBois, J. L. (2010) Comprehensive spectroscopic, steady state, and transient kinetic studies of a representative siderophore-associated flavin monooxygenase. J. Biol. Chem. 285, 30375-30388
27. Romero, E., Robinson, R., and Sobrado, P. (2012) Monitoring the reductive and oxidative half-reactions of a flavin-dependent monooxygenase using stopped-flowspectrophotometry. J. Vis. Exp. 61, e3803 doi: 10.3791/3803
28. Eppink, M. H., Boeren, S. A, Vervoort, J., and van Berkel, W. J. (1997) Purification and properties of 4-hydroxybenzoate 1-hydroxylase (decar-boxylating), a novel flavin adenine dinucleotide-dependent monooxygenase from Candida parapsilosis CBS604. J. Bacterial. V79, 6680-6687
29. Romero, E., Avila, D., and Sobrado, P. (2013) in Flavins and Flavoproteins (Miller, S., Hille, R., and Palfey, B., eds) pp. 289-294, Lulu, Raleigh, NC
30. Mattevi, A. (2006) To be or not to be an oxidase: challenging the oxygen reactivity of flavoenzymes. Trends Biochem. Sci. 31, 276-283
31. Meneely, K. M., Barr, E. W., Bollinger, J. M., Jr., and Lamb, A. L. (2009) Kinetic mechanism of ornithine hydroxylase (PvdA) from Pseudomonas aeruginosa: substrate triggering of 02 addition but not flavin reduction. Biochemistry 48, 4371-4376
32. Meneely, K. M., and Lamb, A. L. (2007) Biochemical characterization of a flavin adenine dinucleotide-dependent monooxygenase, ornithine hydroxylase from Pseudomonas aeruginosa, suggests a novel reaction mechanism. Biochemistry 46, 11930-11937
33. Olucha, J., Meneely, K. M., Chilton, A. S., and Lamb, A. L. (2011) Two structures of an N-hydroxylating flavoprotein monooxygenase: ornithine hydroxylase from Pseudomonas aeruginosa. J. Biol. Chem. 286, 31789-31798
34. Alfleri, A, Malito, E., Orru, R., Fraaije, M. W., and Mattevi, A. (2008) Revealing the moonlighting role of NADP in the structure of a flavin-containing monooxygenase. Proc Natl. Acad. Sci. U.S.A. 105, 6572-6577
35. Orru, R., Torres Pazmino, D. E., Fraaije, M. W., and Mattevi, A. (2010) Joint functions of protein residues and NADP(H) in oxygen activation by flavin-containing monooxygenase. J. Biol. Chem. 285, 35021-35028
36. 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
37. Olucha, J., and Lamb, A. L. (2011) Mechanistic and structural studies of the AT-hydroxylating flavoprotein monooxygenases. Bioorg. Chem. 39, 171-177