Dynamics involved in catalysis by single-component and two-component flavin-dependent aromatic hydroxylases

Biochemical and Biophysical Research Communications

Volumn 338, Issue 1, 2005, Pages 590-598

  Ballou, David P ^a   Entsch, Barrie ^b   Cole, Lindsay J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF NEW ENGLAND   (Australia)

Author keywords

Flavin hydroperoxide; Flavoprotein hydroxylase; Halogenase; Monooxygenase; Protein dynamics; Two component flavin dependent monooxygenase

Indexed keywords

4 HYDROXYBENZOATE 3 MONOOXYGENASE; ANTIBIOTIC AGENT; AROMATIC COMPOUND; DIMETHYLANILINE MONOOXYGENASE; HYDROGEN PEROXIDE; OXIDOREDUCTASE; OXYGEN; REBECCAMYCIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; SIDEROPHORE; SOLVENT; UNSPECIFIC MONOOXYGENASE;

ACINETOBACTER BAUMANNII; BIODEGRADATION; CHEMICAL COMPOSITION; CHLORINATION; DRUG DETOXIFICATION; DRUG SYNTHESIS; ENVIRONMENT; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME CONFORMATION; ENZYME RELEASE; ENZYME STABILITY; ENZYME SUBSTRATE; EXPOSURE; HYDROXYLATION; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; MOTION; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN TRANSPORT; PSEUDOMONAS AERUGINOSA; REVIEW;

4-HYDROXYBENZOATE-3-MONOOXYGENASE; BACTERIAL PROTEINS; CATALYSIS; FLAVINS; FLAVOPROTEINS; MIXED FUNCTION OXYGENASES; THERMODYNAMICS;

ACINETOBACTER BAUMANNII; PSEUDOMONAS AERUGINOSA;

EID: 27544432463     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2005.09.081     Document Type: Review

References (48)

1. M. Katagiri, H. Maeno, S. Yamamoto, O. Hayaishi, T. Kitao, and S. Oae Salicylate hydroxylase, a monooxygenase requiring flavin adenine dinucleotide. II. The mechanism of salicylate hydroxylation to catechol J. Biol. Chem. 240 1965 3414 3417
2. J.R. Cashman The implications of polymorphisms in mammalian flavin-containing monooxygenases in drug discovery and development Drug Discov. Today 9 2004 574 581
3. Y. Zhao, S.K. Christensen, C. Fankhauser, J.R. Cashman, J.D. Cohen, D. Weigel, and J. Chory A role for flavin monooxygenase-like enzymes in auxin biosynthesis Science 291 2001 306 309
4. B.P. Laden, Y. Tang, and T.D. Porter Cloning, heterologous expression, and enzymological characterization of human squalene monooxygenase Arch. Biochem. Biophys. 374 2000 381 388
5. W.W. Poon, D.E. Davis, H.T. Ha, T. Jonassen, P.N. Rather, and C.F. Clarke Identification of Escherichia coli ubiB, a gene required for the first monooxygenase step in ubiquinone biosynthesis J. Bacteriol. 182 2000 5139 5146
6. C. Ambrosi, L. Leoni, L. Putignani, N. Orsi, and P. Visca Pseudobactin biogenesis in the plant growth-promoting rhizobacterium pseudomonas strain B10: identification and functional analysis of the l-ornithine N5-oxygenase (psbA) gene J. Bacteriol. 182 2000 6233 6238
7. B.A. Palfey, D.P. Ballou, and V. Massey Oxygen activation by flavins and pterins J.S. Valentine C.S. Foote A. Greenberg J.F. Liebman Active Oxygen in Biochemistry 1995 Blackie Academic and Professional New York 37 83
8. B.A. Palfey, and V. Massey Flavin-dependent enzymes M. Sinnott Comprehensive Biological Catalysis 1998 Academic Press New York 83 154
9. B. Entsch, B.A. Palfey, D.P. Ballou, and V. Massey Catalytic function of tyrosine residues in para-hydroxybenzoate hydroxylase as determined by the study of site-directed mutants J. Biol. Chem. 266 1991 17341 17349
10. D.L. Gatti, B.A. Palfey, M.S. Lah, B. Entsch, V. Massey, D.P. Ballou, and M.L. Ludwig The mobile flavin of 4-OH benzoate hydroxylase Science 266 1994 110 114
11. G.R. Moran, B. Entsch, B.A. Palfey, and D.P. Ballou Electrostatic effects on substrate activation in para-hydroxybenzoate hydroxylase: studies of the mutant lysine 297 methionine Biochemistry 36 1997 7548 7556
12. B.A. Palfey, B. Entsch, D.P. Ballou, and V. Massey Changes in the catalytic properties of p-hydroxybenzoate hydroxylase caused by the mutation Asn300Asp Biochemistry 33 1994 1545 1554
13. B. Entsch, L.J. Cole, and D.P. Ballou Protein dynamics and electrostatics in the function of p-hydroxybenzoate hydroxylase Arch. Biochem. Biophys. 433 2005 297 311
14. B. Entsch, L.J. Cole, D.P. Ballou, in: T. Nishino, R. Miura, M. Tanokura (Eds.), Flavins and Flavoproteins, Small World Internet Publishing, Japan, 2005 (in press).
15. B. Entsch, and W.J.H. van Berkel Structure and mechanism of para-hydroxybenzoate hydroxylase FASEB J. 9 1995 476 483
16. B. Galan, E. Diaz, M.A. Prieto, and J.L. Garcia 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 2000 627 636
17. J. Valton, L. Filisetti, S.G. Kendrew, M. Fontecave, V. Niviere, in: T. Nishino, R. Miura, M. Tanokura (Eds.), Flavins and Flavoproteins, Small World Internet Publishing, Japan, 2005 (in press).
18. K. Otto, K. Hofstetter, M. Rothlisberger, B. Witholt, and A. Schmid Biochemical characterization of StyAB from Pseudomonas sp. strain VLB120 as a two-component flavin-diffusible monooxygenase J. Bacteriol. 186 2004 5292 5302
19. D.J. Manstein, E.F. Pai, L.M. Schopfer, and V. Massey Absolute stereochemistry of flavins in enzyme-catalyzed reactions Biochemistry 25 1986 6807 6816
20. C.C. Ryerson, D.P. Ballou, and C. Walsh Kinetic isotope effects in the oxidation of isotopically labeled NAD(P)H by bacterial flavoprotein monooxygenases Biochemistry 21 1982 1144 1151
21. D. Sheng, D.P. Ballou, and V. Massey Mechanistic studies of cyclohexanone monooxygenase: chemical properties of intermediates involved in catalysis Biochemistry 40 2001 11156 11167
22. K.C. Jones, and D.P. Ballou Reactions of the 4a-hydroperoxide of liver microsomal flavin-containing monooxygenase with nucleophilic and electrophilic substrates J. Biol. Chem. 261 1986 2553 2559
23. N.B. Beaty, and D.P. Ballou The oxidative half-reaction of liver microsomal FAD-containing monooxygenase J. Biol. Chem. 256 1981 4619 4625
24. B. Entsch, D.P. Ballou, and V. Massey Flavin-oxygen derivatives involved in hydroxylation by p-hydroxybenzoate hydroxylase J. Biol. Chem. 251 1976 2550 2563
25. G.R. Moran, B. Entsch, B.A. Palfey, and D.P. Ballou Evidence for flavin movement in the function of p-hydroxybenzoate hydroxylase from studies of the mutant Arg220Lys Biochemistry 35 1996 9278 9285
26. B.A. Palfey, D.P. Ballou, and V. Massey Flavin conformational changes in the catalytic cycle of p-hydroxybenzoate hydroxylase substituted with 6-azido- and 6-aminoflavin adenine dinucleotide Biochemistry 36 1997 15713 15723
27. B.A. Palfey, G.R. Moran, B. Entsch, D.P. Ballou, and V. Massey Substrate recognition by 'password' in p-hydroxybenzoate hydroxylase Biochemistry 38 1999 1153 1158
28. H.A. Schreuder, A. Mattevi, G. Obmolova, K.H. Kalk, W.G. Hol, F.J. van der Bolt, and W.J. van Berkel Crystal structures of wild-type p-hydroxybenzoate hydroxylase complexed with 4-aminobenzoate, 2,4-dihydroxybenzoate, and 2-hydroxy-4-aminobenzoate and of the Tyr222Ala mutant complexed with 2-hydroxy-4-aminobenzoate. Evidence for a proton channel and a new binding mode of the flavin ring Biochemistry 33 1994 10161 10170
29. G.R. Moran, B. Entsch, B.A. Palfey, and D.P. Ballou Mechanistic insights into p-hydroxybenzoate hydroxylase from studies of the mutant Ser212Ala Biochemistry 38 1999 6292 6299
30. J. Wang, M. Ortiz-Maldonado, B. Entsch, V. Massey, D. Ballou, and D.L. Gatti Protein and ligand dynamics in 4-hydroxybenzoate hydroxylase Proc. Natl. Acad. Sci. USA 99 2002 608 613
31. L.J. Cole, D.L. Gatti, B. Entsch, and D.P. Ballou Removal of a methyl group causes global changes in p-hydroxybenzoate hydroxylase Biochemistry 44 2005 8047 8058
32. M. Husain, and V. Massey Kinetic studies on the reaction of p-hydroxybenzoate hydroxylase. Agreement of steady state and rapid reaction data J. Biol. Chem. 254 1979 6657 6666
33. K.K. Frederick, D.P. Ballou, and B.A. Palfey Protein dynamics control proton transfers to the substrate on the His72Asn mutant of p-hydroxybenzoate hydroxylase Biochemistry 40 2001 3891 3899
34. B.A. Palfey, R. Basu, K.K. Frederick, B. Entsch, and D.P. Ballou Role of protein flexibility in the catalytic cycle of p-hydroxybenzoate hydroxylase elucidated by the Pro293Ser mutant Biochemistry 41 2002 8438 8446
35. M. Ortiz-Maldonado, D.P. Ballou, and V. Massey Use of free energy relationships to probe the individual steps of hydroxylation of p-hydroxybenzoate hydroxylase: studies with a series of 8-substituted flavins Biochemistry 38 1999 8124 8137
36. M. Ortiz-Maldonado, B. Entsch, and D.P. Ballou Oxygen reactions in p-hydroxybenzoate hydroxylase utilize the H-bond network during catalysis Biochemistry 43 2004 15246 15257
37. M. Ortiz-Maldonado, L.J. Cole, S.M. Dumas, B. Entsch, and D.P. Ballou Increased positive electrostatic potential in p-hydroxybenzoate hydroxylase accelerates hydroxylation but slows turnover Biochemistry 43 2004 1569 1579
38. M. Fontecave, R. Eliasson, and P. Reichard Enzymatic regulation of the radical content of the small subunit of Escherichia coli ribonucleotide reductase involving reduction of its redox centers J. Biol. Chem. 264 1989 9164 9170
39. F. Xu, K.S. Quandt, and D.E. Hultquist Characterization of NADPH-dependent methemoglobin reductase as a heme-binding protein present in erythrocytes and liver Proc. Natl. Acad. Sci. USA 89 1992 2130 2134
40. T. Wilson, and J.W. Hastings Bioluminescence Annu. Rev. Cell Dev. Biol. 14 1998 197 230
41. L. Xun, and E.R. Sandvik Characterization of 4-hydroxyphenylacetate 3-hydroxylase (HpaB) of Escherichia coli as a reduced flavin adenine dinucleotide-utilizing monooxygenase Appl. Environ. Microbiol. 66 2000 481 486
42. B. Entsch, S. Chakraborty, M. Ortiz, D. Ballou, in: T. Nishino, R. Miura, M. Tanokura, (Eds). Flavins and Flavoproteins, Small World Internet Publishing, Japan, 2005 (in press).
43. J. Sucharitakul, P. Chaiyen, B. Entsch, and D.P. Ballou The reductase of p-hydroxyphenylacetate 3-hydroxylase from Acinetobacter baumannii requires p-hydroxyphenylacetate for effective catalysis Biochemistry 44 2005 10434 10442
44. R.H. vanden Heuvel, A.H. Westphal, A.J. Heck, M.A. Walsh, S. Rovida, W.J. van Berkel, and A. Mattevi 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 2004 12860 12867
45. 2 by NAD(P)H-flavin oxidoreductase and 4-hydroxyphenylacetate 3-monooxygenase Biochemistry 42 2003 7509 7517
46. K. Thotsaporn, J. Sucharitakul, J. Wongratana, C. Suadee, and P. Chaiyen 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 2004 60 66
47. E. Yeh, S. Garneau, and C.T. Walsh Robust in vitro activity of RebF and RebH, a two-component reductase/halogenase, generating 7-chlorotryptophan during rebeccamycin biosynthesis Proc. Natl. Acad. Sci. USA 102 2005 3960 3965
48. C. Dong, S. Flecks, S. Unversucht, C. Haupt, K.H. van Pee, J.H. Naismith, The structure of tryptophan 7-halogenase (PrnA), a member of the flavin-dependent halogenase superfamily, suggests chlorine incorporation proceeds by an unexpected electrophilic mechanism, Science (2005), in press.