Studies on the mechanism of p-hydroxyphenylacetate 3-hydroxylase from Pseudomonas aeruginosa: A system composed of a small flavin reductase and a large flavin-dependent oxygenase

Biochemistry

Volumn 49, Issue 2, 2010, Pages 372-385

  Chakraborty, Sumita ^a   Ortiz Maldonado, Mariliz ^a,c   Entsch, Barrie ^a,b   Ballou, David P ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF NEW ENGLAND   (Australia)

^c GENENCOR INTERNATIONAL INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACINETOBACTERS; BAUMANNII; CONCENTRATION OF; FLAVIN REDUCTASE; FLAVIN-DEPENDENT; HIS-TAGGED PROTEINS; HYDROPEROXIDES; HYDROXYLASES; MOLECULAR ORIGINS; MONOOXYGENASES; OXYGENASES; P.AERUGINOSA; PSEUDOMONAS AERUGINOSA; RATE DETERMINING STEP; THERMUS THERMOPHILUS; TWO-COMPONENT; YELLOW PROTEINS;

CATALYSIS; COMPLEXATION; ENZYMES; ESCHERICHIA COLI; GROUP TECHNOLOGY; OXYGENATION; OXYGENATORS; PURIFICATION;

ENZYME ACTIVITY;

4 HYDROXYPHENYLACETATE 3 HYDROXYLASE; ACETIC ACID DERIVATIVE; BACTERIAL ENZYME; OXIDOREDUCTASE; OXYGEN; OXYGENASE; POLYHISTIDINE TAG; QUERCETIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; UNCLASSIFIED DRUG; WATER; 3 HYDROXYPHENYLACETATE 6 HYDROXYLASE; 3-HYDROXYPHENYLACETATE 6-HYDROXYLASE; BACTERIAL PROTEIN; DIMETHYLANILINE MONOOXYGENASE; DIMETHYLANILINE MONOOXYGENASE (N-OXIDE FORMING); FLAVINE MONONUCLEOTIDE REDUCTASE; HPAA PROTEIN, BACTERIA; LECTIN; LIPOPROTEIN; MIXED FUNCTION OXIDASE; PRIMER DNA;

ACINETOBACTER BAUMANNII; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME BINDING; ENZYME MECHANISM; ENZYME PURIFICATION; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSEUDOMONAS AERUGINOSA; SPECIES; THERMUS THERMOPHILUS; CHEMISTRY; ENZYMOLOGY; GENE AMPLIFICATION; GENETICS; KINETICS; METABOLISM; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION;

ACINETOBACTER BAUMANNII; ESCHERICHIA COLI; PSEUDOMONAS AERUGINOSA; THERMUS THERMOPHILUS;

ACINETOBACTER BAUMANNII; BACTERIAL PROTEINS; BASE SEQUENCE; DNA PRIMERS; FMN REDUCTASE; GENE AMPLIFICATION; KINETICS; LECTINS; LIPOPROTEINS; MIXED FUNCTION OXYGENASES; OXYGENASES; POLYMERASE CHAIN REACTION; PSEUDOMONAS AERUGINOSA;

EID: 75349094072     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi901454u     Document Type: Article

References (28)

1. 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.
2. Campbell, Z. T., and Baldwin, T. O. (2009) Fre is the major flavin reductase supporting bioluminescence from Vibrio harveyi luciferase in Escherichia coli. J. Biol. Chem. 284, 8322-8328.
3. Entsch, B., Cole, L. J., and Ballou, D. P. (2005) Protein dynamics and electrostatics in the function of p-hydroxybenzoate hydroxylase. Arch. Biochem. Biophys. 433, 297-311.
4. Arunachalam, U., Massey, V., and Miller, S. M. (1994) Mechanism of p-hydroxyphenylacetate 3-hydroxylase, a two-protein enzyme. J. Biol. Chem. 269, 150-155.
5. 2 byNAD(P)H-flavin oxidoreductase and 4-hydroxyphenylacetate 3-monooxygenase. Biochemistry 42, 7509-7517.
6. 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 46, 8611-8623.
7. Alfieri, A., Fersini, F., Ruangchan, N., Prongjit, M., Chaiyen, P., and Mattevi, A. (2007) Structure of the monooxygenase component of a two-component flavoprotein monooxygenase. Proc. Natl. Acad. Sci. U.S.A. 104, 1177-1182.
8. Kim, S.-H., Hisano, T., Takeda, K., Iwasaki, W., Ebihara, A., and Miki, K. (2007) Crystal structure of the oxygenase component (HpaB) of the 4-hydroxyphenylacetate 3-monooxygenase from Thermus thermophilus HB8. J. Biol. Chem. 282, 33107-33117.
9. Kim, S.-H., Hisano, T., Iwasaki, W., Ebihara, A., and Miki, K. (2008) Crystal structure of the flavin reductase component (HpaC) of 4-hydroxyphenylacetate 3-monooxygenase from Thermus thermophilus HB8: Structural basis for the flavin affinity. Proteins 70, 718-730.
10. 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.
11. Sucharitakul, J., Chaiyen, P., Entsch, B., and Ballou, D. P. (2005) The reductase of p-hydroxyphenylacetate 3-hydroxylase from Acinetobacter baumannii requires p-hydroxyphenylacetate for effective catalysis. Biochemistry 44, 10434-10442.
12. Valton, J., Mathevon, C., Fontecave, M., Nivière, V., and Ballou, D. P. (2008) Mechanism and regulation of the two-component FMNdependent monooxygenase ActVA-ActVB from Streptomyces coelicolor. J. Biol. Chem. 283, 10287-10296.
13. Entsch, B., Cole, L. J., and Ballou, D. P. (2005) Protein dynamics in catalysis by flavoprotein hydroxylases. In Flavins and Flavoproteins 2005 (Nishino, T., Miura, R., Tanokura, M., and Fukui, K., Eds.) pp 143-154, ARchiTect, Tokyo.
14. Chakraborty, S., Ortiz-Maldonado, M., Eschenburg, K., Entsch, B., and Ballou, D. P. (2005) p-Hydroxyphenylacetate 3-hydroxylase from Pseudomonas aeruginosa. In Flavins and Flavoproteins 2005 (Nishino, T., Miura, R., Tanokura, M., and Fukui, K., Eds.) pp 161-166, ARchiTect, Tokyo.
15. Van den Heuvel, R. H. H., Westphal, A. H., Hecks, A. J. R., Walsh, M. A., Rovida, S., van Berkel, W. J. H., and Mattevi, A. (2004) Structural studies on flavin reductase PheA2 reveal binding of NAD in an unusual folded conformation and support novel mechanism of action. J. Biol. Chem. 279, 12860-12867.
16. Duch, D. S., and Laskowski, M., Sr. (1971) A sensitive method for the determination of RNA in DNA and vice versa. Anal. Biochem. 44, 42-48.
17. Arunachalam, U., Massey, V., and Vaidyanathan, C. S. (1992) p-Hydroxyphenylacetate-3-hydroxylase. A two-protein component enzyme. J. Biol. Chem. 267, 25848-25855.
18. Galán, B., Díaz, E., Prieto, M. A., and García, J. L. (2000) Functional analysis of the small component of the 4- hydroxyphenylacetate 3-monooxygenase of Escherichia coli W: A prototype of a new flavin:NAD(P)H reductase subfamily. J. Bacteriol. 182, 627-636.
19. Gibian, M. J., and Rynd, J. A. (1969) Oxidation of reduced flavins by quinones. Biochem. Biophys. Res. Commun. 34, 594-599.
20. 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.
21. Gibson, Q. H., Swoboda, B. E., and Massey, V. (1964) Kinetics and mechanism of action of glucose oxidase. J. Biol. Chem. 239, 3927-3934.
22. Moran, G. R., Entsch, B., Palfey, B. A., and Ballou, D. P. (1996) Evidence for flavin movement in the function of p-hydroxybenzoate hydroxylase from studies of the mutant Arg220Lys. Biochemistry 35, 9278-9285.
23. Fischer, M., and Bacher, A. (2005) Biosynthesis of flavocoenzymes. Nat. Prod. Rep. 22, 324-350.
24. Entsch, B., and Ballou, D. P. (2009) Flavin-mediated hydroxylation reactions. In Wiley Encyclopedia of Chemical Biology (Dagley, T. P., Ed.) Vol. 2, pp 8-17, Wiley & Sons, New York.
25. Thatsaporn, K., Sucharitakul, J., Wongratana, J., Suadee, C., and Chaiyen, P. (2004) Cloning and expression of p-hydroxyphenylacetate 3-hydroxylase from Acinetobacter baumannii: Evidence of the divergence of enzymes in the class of two-protein component aromatic hydroxylases. Biochim. Biophys. Acta 1680, 60-66.
26. Schreuder, H. A., Prick, P. A., Wieringa, R. K., Vriend, G., Wilson, K. S., Hol, W. G., and Drenth, J. (1989) Crystal structure of the p-hydroxybenzoate hydroxylase-substrate complex refined at 1.9 Å resolution. Analysis of the enzyme-substrate and enzyme-product complexes. J. Mol. Biol. 208, 679-696.
27. Alfieri, 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.
28. Entsch, B., Ballou, D. P., Husain, M., and Massey, V. (1976) Catalytic mechanism of p-hydroxybenzoate hydroxylase with p-mercaptobenzoate as substrate. J. Biol. Chem. 251, 7367-7379.