Vibrio harveyi flavin reductase-luciferase fusion protein mimics a single-component bifunctional monooxygenase

Biochemistry

Volumn 47, Issue 1, 2008, Pages 368-377

  Jawanda, Navneet ^a   Ahmed, Kamran ^a   Tu, Shiao Chun ^a  

^a University of Houston   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYSIS; NUCLEOTIDES; REACTION KINETICS;

FLAVIN REDUCTASE; FUSION ENZYMES; MONOOXYGENASE;

ENZYMES;

HYBRID PROTEIN; LUCIFERASE; OXIDOREDUCTASE; OXYGEN; QUERCETIN; UNSPECIFIC MONOOXYGENASE;

ARTICLE; BIOLUMINESCENCE; CATALYSIS; COMPLEX FORMATION; DIFFUSION; ENZYME ACTIVE SITE; ENZYME SUBSTRATE; ENZYME SUBUNIT; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; QUANTUM MECHANICS; REDUCTION; VIBRIO HARVEYI;

BACTERIAL PROTEINS; FLAVIN MONONUCLEOTIDE; FMN REDUCTASE; KINETICS; LUCIFERASES; MIXED FUNCTION OXYGENASES; NADP; OXYGEN; PROTEIN BINDING; RECOMBINANT FUSION PROTEINS; VIBRIO;

VIBRIO HARVEYI;

EID: 37849017720     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701392b     Document Type: Article

References (61)

1. Ziegler, D. M. (2002) An overview of the mechanism, substrate specificities, and structure of FMOs, Drug Metab. Rev. 34, 503-511.
2. Cole, L. J., Entsch, B., Ortiz-Maldonado, M., and Ballou, D. P. (2005) Properties of p-hydroxybenzoate hydroxylase when stabilized in its open conformation, Biochemistry 44, 14807-14817.
3. Wang, L.-H., and Tu, S.-C. (1984) The kinetic mechanism of salicylate hydroxylase as studied by initial rate measurement, rapid reaction kinetics, and isotope effects, J. Biol. Chem. 259, 10682-10688.
4. Yu, Y., Wang, L.-H., and Tu, S.-C. (1987) Pseudomonas cepacia 3-hydroxybenzoate 6-hydroxylase: stereochemistry, isotope effects, and kinetic mechanism, Biochemistry 26, 1105-1110.
5. Tu, S.-C. (2001) Reduced flavin: donor and acceptor enzymes and mechanisms of channeling, Antioxid. Redox Signal. 3, 881-897.
6. van Berkel, W. J., Kamerbeek, N. M., and Fraaije, M. W. (2006) Flavoprotein monooxygenases, a diverse class of oxidative biocatalysts, J. Biotechnol. 124, 670-689.
7. Hastings, J. W., and Nealson, K. H. (1977) Bacterial bioluminescence, Annu. Rev. Microbiol. 31, 549-595.
8. Lei, B., and Tu, S.-C. (1996) Gene overexpression, purification, and identification of a desulfurization enzyme from Rhodococcus sp. strain IGTS8 as a sulfide/sulfoxide monooxygenase, J. Bacteriol. 178, 5699-5705.
9. Gray, K. A., Pogrebinsky, O. S., Mrachko, G. T., Xi, L., Monticello, D. J., and Squires, C. H. (1996) Molecular mechanisms of biocatalytic desulfurization of fossil fuels, Nat. Biotechnol. 14, 1705-1709.
10. Kendrew, S. G., Hopwood, D. A., and Marsh, E. N. (1997) Identification of a monooxygenase from Streptomyces coelicolor A3(2) involved in biosynthesis of actinorhodin: purification and characterization of the recombinant enzyme, J. Bacteriol. 179, 4305-4310.
11. Valton, J., Filisetti, L., Fontecave, M., and Nivière, V. (2004) A two-component flavin-dependent monooxygenase involved in actinorhodin biosynthesis in Streptomyces coelicolor, J. Biol. Chem. 279, 44362-44369.
12. Blanc, V., Lagneaux, D., Didier, P., Gil, P., Lacroix, P., and Crouzet, J. (1995) Cloning and analysis of structural genes from Streptomyces pristinaespiralis encoding enzymes involved in the conversion of pristinamycin IIB to pristinamycin IIA (PIIA): PIIA synthase and NADH:riboflavin 5′-phosphate oxidoreductase, J. Bacteriol. 177, 5206-5214.
13. Thibaut, D., Ratet, N., Bisch, D., Faucher, D., Debussche, L., and Blanche, F. (1995) Purification of the two-enzyme system catalyzing the oxidation of the D-proline residue of pristinamycin I1HB during the last step of pristinamycin IIA biosynthesis, J. Bacteriol. 177, 5199-5205.
14. Parry, R. J., and Li, W. (1997) Purification and characterization of isobutylamine N-hydroxylase from the valanimycin producer Streptomyces viridifaciens MG456-hF10, Arch. Biochem. Biophys. 339, 47-54.
15. Arunachalam, U., Massey, V., and Vaidyanathan, C. S. (1992) p-Hydroxyphenylacetate-3-hydroxylase. A two-protein component enzyme, J. Biol. Chem. 267, 25848-25855.
16. Chaiyen, P., Suadee, C., and Wilairat, P. (2001) A novel two-protein component flavoprotein hydroxylase, Eur. J. Biochem. 268, 5550-5561.
17. Prieto, M. A., and Garcia, J. L. (1994) Molecular characterization of 4-hydroxyphenylacetate 3-hydroxylase of Escherichia coli. A two-protein component enzyme, J. Biol. Chem. 269, 22823-22829.
18. 2 by NAD(P)H-flavin oxidoreductase and 4-hydroxyphenylacetate 3-monooxygenase, Biochemistry 42, 7509-7517.
19. Becker, D., Schrader, T., and Andreesen, J. R. (1997) Two-component flavin-dependent pyrrole-2-carboxylate monooxygenase from Rhodococcus sp, Eur. J. Biochem. 249, 739-747.
20. Xu, Y., Mortimer, M. W., Fisher, T. S., Kahn, M. L., Brockman, F. J., and Xun, L. (1997) Cloning, sequencing, and analysis of a gene cluster from Chelatobacter heintzii ATCC 29600 encoding nitrilotriacetate monooxygenase and NADH:flavin mononucleotide oxidoreductase, J. Bacteriol. 179, 1112-1116.
21. Uetz, T., Schneider, R., Snozzi, M., and Egli, T. (1992) Purification and characterization of a two-component monooxygenase that hydroxylates nitrilotriacetate from "Chelatobacter" strain ATCC 29600, J. Bacteriol. 174, 1179-1188.
22. Russell, T. R., Demeler, B., and Tu, S.-C. (2004) Kinetic mechanism and quaternary structure of Aminobacter aminovorans NADH:flavin oxidoreductase: an unusual flavin reductase with bound flavin, Biochemistry 43, 1580-1590.
23. Payne, J. W., Bolton, H., Jr., Campbell, J. A., and Xun, L. (1998) Purification and characterization of EDTA monooxygenase from the EDTA- degrading bacterium BNC1 [published erratum appears in J Bacteriol 1998 Nov;180(21):5808], J. Bacteriol. 180, 3823-3827.
24. Witschel, M., Nagel, S., and Egli, T. (1997) Identification and characterization of the two-enzyme system catalyzing oxidation of EDTA in the EDTA-degrading bacterial strain DSM 9103, J. Bacteriol. 179, 6937-6943.
25. Gisi, M. R., and Xun, L. (2003) Characterization of chlorophenol 4-monooxygenase (TftD) and NADH:flavin adenine dinucleotide oxidoreductase (TftC) of Burkholderia cepacia AC1100, J. Bacteriol. 185, 2786-2792.
26. Garrec, G. M., Artaud, I., and Capeillère-Blandin, C. (2001) Purification and catalytic properties of the chlorophenol 4-monooxygenase from Burkholderia cepacia strain AC1100, Biochim. Biophys. Acta 1547, 288-301.
27. Pessione, E., Divari, S., Griva, E., Cavaletto, M., Rossi, G. L., Gilardi, G., and Giunta, C. (1999) Phenol hydroxylase from Acinetobacter radioresistens is a multicomponent enzyme. Purification and characterization of the reductase moiety, Eur. J. Biochem. 265, 549-555.
28. Kirchner, U., Westphal, A. H., Mueller, R., and Van Berkel, W. J. H. (2003) Phenol hydroxylase from Bacillus thermoglucosidasius A7, a two-protein component monooxygenase with a dual Role for FAD, J. Biol. Chem. 278, 47545-47553.
29. Divari, S., Valetti, F., Caposio, P., Pessione, E., Cavaletto, M., Griva, E., Gribaudo, G., Gilardi, G., and Giunta, C. (2003) The oxygenase component of phenol hydroxylase from Acinetobacter radioresistens S13, Eur. J. Biochem. 270, 2244-2253.
30. Eichhorn, E., van der Ploeg, J. R., and Leisinger, T. (1999) Characterization of a two-component alkanesulfonate monooxygenase from Escherichia coli, J. Biol. Chem. 274, 26639-26646.
31. Otto, K., Hofstetter, K., Rothlisberger, M., Witholt, B., and Schmid, A. (2004) Biochemical characterization of StyAB from Pseudomonas sp. strain VLB120 as a two-component flavin-diffusible monooxygenase, J. Bacteriol. 186, 5292-5302.
32. Lei, B., Liu, M., Huang, S., and Tu, S.-C. (1994) Vibrio harveyi NADPH-flavin oxidoreductase: cloning, sequencing and overexpression of the gene and purification and characterization of the cloned enzyme, J. Bacteriol. 176, 3552-3558.
33. Inouye, S. (1994) NAD(P)H-flavin oxidoreductase from the bioluminescent bacterium, Vibrio fischeri ATCC 7744, is a flavoprotein, FEBS Lett. 347, 163-168.
34. Lei, B., and Tu, S.-C. (1998) Mechanism of reduced flavin transfer from Vibrio harveyi NADPH-FMN oxidoreductase to luciferase, Biochemistry 37, 14623-14629.
35. Jeffers, C. E., and Tu, S.-C. (2001) Differential transfers of reduced flavin cofactor and product by bacterial flavin reductase to luciferase, Biochemistry 40, 1749-1754.
36. Jeffers, C. E., Nichols, J. C., and Tu, S.-C. (2003) Complex formation between Vibrio harveyi luciferase and monomeric NADPH:FMN oxidoreductase, Biochemistry 42, 529-534.
37. Low, J. C., and Tu, S.-C. (2003) Energy transfer evidence for in vitro and in vivo complexes of Vibrio harveyi flavin reductase P and luciferase, Photochem. Photobiol. 77, 446-452.
38. Li, X., and Tu, S.-C. (2006) Activity Coupling of Vibrio harveyi luciferase and flavin reductase (FRP): Oxygen as a probe, Arch. Biochem. Biophys. 454, 26-31.
39. Gao, B., and Ellis, H. R. (2005) Altered mechanism of the alkanesulfonate FMN reductase with the monooxygenase enzyme, Biochem. Biophys. Res. Commun. 331, 1137-1145.
40. Abdurachim, K., and Ellis, H. R. (2006) Detection of protein-protein interactions in the alkanesulfonate monooxygenase system from Escherichia coli, J. Bacteriol. 188, 8153-8159.
41. Galán, B., Díaz, E., Prieto, M. A., and García, J. L. (2000) Functional analysis of the small component of the 4-hydroxyphenyl- acetate 3-monooxygenase of Escherichia coli W: a prototype of a new flavin:NAD(P)H reductase subfamily, J. Bacteriol. 182, 627-636.
42. Sucharitakul, J., Phongsak, T., Entsch, B., Svasti, J., Chaiyen, P., and Ballou, D. P. (2007) Kinetics of a two-component p-hydroxyphenylacetate hydroxylase explain how reduced flavin is transferred from the reductase to the oxygenase, Biochemistry, DOI: 10.1021/bi7006614.
43. Kantz, A., Chin, F., Nallamothu, N., Nguyen, T., and Gassner, G. T. (2005) Mechanism of flavin transfer and oxygen activation by the two-component flavoenzyme styrene monooxygenase, Arch. Biochem. Biophys. 442, 102-116.
44. Tu, S.-C., and Hastings, J. W. (1980) Physical interaction and activity coupling between two enzymes induced by immobilization of one, Proc. Natl. Acad. Sci. U.S.A. 77, 249-252.
45. Lowry, O. H., Rosebrough, N. J., Fair, A. L., and Randall, R. J. (1951) Protein measurement with the Folin phenol reagent, J. Biol. Chem. 193, 265-275.
46. Wang, H., Lei, B., and Tu, S.-C. (2000) Vibrio harveyi NADPH-FMN oxidoreductase Arg203 as a critical residue for NADPH recognition and binding, Biochemistry 39, 7813-7819.
47. Li, C.-H., and Tu, S.-C. (2005) Active site hydrophobicity is critical to the bioluminescence activity of Vibrio harveyi luciferase, Biochemistry 44, 12970-12977.
48. Huston, J. S., Levinson, D., Mudgett-Hunter, M., Tai, M. S., Novotny, J., Margolies, M. N., Ridge, R. J., Bruccoleri, R. E., Haber, E., Crea, R., and Oppermann, H. (1988) Protein engineering of antibody binding sites: recovery of specific activity in an anti-digoxin single-chain Fv analogue produced in Escherichia coli, Proc. Natl. Acad. Sci U.S.A. 85, 5879-5883.
49. Robinson, C. R., and Sauer, R. T. (1998) Optimizing the stability of single-chain proteins by linker length and composition mutagenesis, Proc. Natl. Acad. Sci. U.S.A 95, 5929-5934.
50. Lei, B., Cho, K. W., and Tu, S.-C. (1994) Mechanism of aldehyde inhibition of Vibrio harveyi luciferase. Identification of two aldehyde sites and relationship between aldehyde and flavin binding, J. Biol. Chem. 269, 5612-5618.
51. Tu, S.-C., and McCormick, D. B. (1974) Conformation of porcine D-amino acid oxidase as studied by protein fluorescence and optical rotatory dispersion, Biochemistry 13, 893-899.
52. Liu, M., Lei, B., Ding, Q., Lee, J. C., and Tu, S.-C. (1997) Vibrio harveyi NADPH:FMN oxidoreductase: preparation and characterization of the apoenzyme and monomer-dimer equilibrium, Arch. Biochem. Biophys. 337, 89-95.
53. Jablonski, E., and DeLuca, M. (1978) Studies of the control of luminescence in Beneckea harveyi: properties of the NADH and NADPH:FMN oxidoreductases, Biochemistry 17, 672-678.
54. Baldwin, T. O., Nicoli, M. Z., Becvar, J. E., and Hastings, J. W. (1975) Bacterial luciferase. Binding of oxidized flavin mononucleotide, J. Biol. Chem. 250, 2763-2768.
55. Duane, W., and Hastings, J. W. (1975) Flavin mononucleotide reductase of luminous bacteria, Mol. Cell. Biochem. 6, 53-64.
56. Ballou, D. P., Entsch, B., and Cole, L. J. (2005) Dynamics involved in catalysis by single-component and two-component flavin-dependent aromatic hydroxylases, Biochem. Biophys. Res. Commun. 338, 590-598.
57. Brender, J. R., Dertouzos, J., Ballou, D. P., Massey, V., Palfey, B. A., Entsch, B., Steel, D. G., and Gafni, A. (2005) Conformational dynamics of the isoalloxazine in substrate-free p-hydroxybenzoate hydroxylase: single-molecule studies, J. Am. Chem. Soc. 127, 18171-18178.
58. Tu, S.-C., Romero, F. A., and Wang, L. H. (1981) Uncoupling of the substrate monooxygenation and reduced pyridine nucleotide oxidation activities of salicylate hydroxylase by flavins, Arch. Biochem. Biophys. 209, 423-432.
59. Kourtz, L., Dillon, K., Daughtry, S., Madison, L. L., Peoples, O., and Snell, K. D. (2005) A novel thiolase-reductase gene fusion promotes the production of polyhydroxybutyrate in Arabidopsis, Plant Biotechnol. J. 3, 435-447.
60. Hastings, J. W., and Morin, J. G. (2006) Photons for reporting molecular events: green fluorescent protein and four luciferase systems, Methods Biochem. Anal. 47, 15-38.
61. Roda, A., Guardigli, M., Pasini, P., and Mirasoli, M. (2003) Bioluminescence and chemiluminescence in drug screening, Anal. Bioanal. Chem. 377, 826-833.