Multiple roles of component proteins in bacterial multicomponent monooxygenases: Phenol hydroxylase and toluene/ o-xylene monooxygenase from Pseudomonas sp. OX1

Biochemistry

Volumn 50, Issue 11, 2011, Pages 1788-1798

  Tinberg, Christine E ^a   Song, Woon Ju ^a   Izzo, Viviana ^a   Lippard, Stephen J ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOSTERY; AROMATIC SUBSTRATES; COMPLETE SYSTEM; DIOXYGENS; ELECTRON-TRANSFER; ELECTRON-TRANSFER STEP; HYDROCARBON OXIDATION; HYDROXYLASES; MONOOXYGENASES; MULTICOMPONENTS; O-XYLENE; PHENOL HYDROXYLASE; PRODUCT YIELDS; PROTEIN COMPONENTS; PSEUDOMONAS SP; REACTIVITY MECHANISM; REGULATORY EFFECTS; REGULATORY PROTEIN; STEADY STATE; SUBSTRATE OXIDATION;

AROMATIC HYDROCARBONS; CARBOXYLATION; CATALYSTS; ELECTRONS; ENZYMES; HYDROXYLATION; OXIDATION; PHENOLS; XYLENE;

SUBSTRATES;

CATECHOL; HYDROCARBON; HYDROLASE; OXYGENASE; PHENOL HYDROXYLASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; TOLUENE; TOLUENE XYLENE MONOOXYGENASE; UNCLASSIFIED DRUG; XYLENE;

ALLOSTERISM; ARTICLE; CONTROLLED STUDY; ELECTRON TRANSPORT; ESCHERICHIA COLI; HYDROXYLATION; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN PURIFICATION; PSEUDOMONAS; REGULATORY MECHANISM; STEADY STATE;

BINDING SITES; CATECHOLS; KINETICS; MIXED FUNCTION OXYGENASES; MODELS, MOLECULAR; NAD; OXIDATION-REDUCTION; OXYGENASES; PHENOL; PROTEIN CONFORMATION; PSEUDOMONAS; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS); PSEUDOMONAS SP.;

EID: 79952786487     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200028z     Document Type: Article

References (58)

1. Murray, L. J. and Lippard, S. J. (2007) Substrate Trafficking and Dioxygen Activation in Bacterial Multicomponent Monooxygenases Acc. Chem. Res. 40, 466-474
2. Sazinsky, M. H. and Lippard, S. J. (2006) Correlating Structure with Function in Bacterial Multicomponent Monooxygenases and Related Diiron Proteins Acc. Chem. Res. 39, 558-566
3. Leahy, J. G., Batchelor, P. J., and Morcomb, S. M. (2003) Evolution of the Soluble Diiron Monooxygenases FEMS Microbiol. Rev. 27, 449-479 (Pubitemid 37205164)
4. Notomista, E., Lahm, A., Di Donato, A., and Tramontano, A. (2003) Evolution of Bacterial and Archaeal Multicomponent Monooxygenases J. Mol. Evol. 56, 435-445 (Pubitemid 36390774)
5. Wallar, B. J. and Lipscomb, J. D. (1996) Dioxygen Activation by Enzymes Containing Binuclear Non-Heme Iron Clusters Chem. Rev. 96, 2625-2657 (Pubitemid 126641115)
6. Brazeau, B. J. and Lipscomb, J. D. (2000) Kinetics and Activation Thermodynamics of Methane Monooxygenase Compound Q Formation and Reaction with Substrates Biochemistry 39, 13503-13515
7. Tinberg, C. E. and Lippard, S. J. (2009) Revisiting the Mechanism of Dioxygen Activation in Soluble Methane Monooxygenase from M. capsulatus (Bath): Evidence for a Multi-Step, Proton-Dependent Reaction Pathway Biochemistry 48, 12145-12158
8. Liu, K. E., Valentine, A. M., Wang, D., Huynh, B. H., Edmondson, D. E., Salifoglou, A., and Lippard, S. J. (1995) Kinetic and Spectroscopic Characterization of Intermediates and Component Interactions in Reactions of Methane Monooxygenase from Methylococcus capsulatus (Bath) J. Am. Chem. Soc. 117, 10174-10185
9. Liu, K. E., Wang, D., Huynh, B. H., Edmondson, D. E., Salifoglou, A., and Lippard, S. J. (1994) Spectroscopic Detection of Intermediates in the Reaction of Dioxygen with Reduced Methane Monooxygenase Hydroxylase from Methylococcus capsulatus (Bath) J. Am. Chem. Soc. 116, 7465-7466 (Pubitemid 24981465)
10. Valentine, A. M., Stahl, S. S., and Lippard, S. J. (1999) Mechanistic Studies of the Reaction of Reduced Methane Monooxygenase Hydroxylase with Dioxygen and Substrates J. Am. Chem. Soc. 121, 3876-3887
11. Lee, S.-K. and Lipscomb, J. D. (1999) Oxygen Activation Catalyzed by Methane Monooxygenase Hydroxylase Component: Proton Delivery during the O-O Bond Cleavage Steps Biochemistry 38, 4423-4432
12. IV Cluster J. Am. Chem. Soc. 115, 6450-6451
13. Lee, S.-K., Nesheim, J. C., and Lipscomb, J. D. (1993) Transient Intermediates of the Methane Monooxygenase Catalytic Cycle J. Biol. Chem. 268, 21569-21577 (Pubitemid 23320647)
14. 2 Diamond Core Structure for the Key Intermediate Q of Methane Monooxygenase Science 275, 515-518 (Pubitemid 27051903)
15. Murray, L. J., Naik, S. G., Ortillo, D. O., García-Serres, R., Lee, J. K., Huynh, B. H., and Lippard, S. J. (2007) Characterization of the Arene-Oxidizing Intermediate in ToMOH as a Diiron(III) Species J. Am. Chem. Soc. 129, 14500-14510 (Pubitemid 350171479)
16. Murray, L. J., García-Serres, R., Naik, S., Huynh, B. H., and Lippard, S. J. (2006) Dioxygen Activation at Non-Heme Diiron Centers: Characterization of Intermediates in a Mutant Form of Toluene/ o -Xylene Monooxygenase Hydroxylase J. Am. Chem. Soc. 128, 7458-7459 (Pubitemid 43877517)
17. Izzo, V., Tinberg, C. E., García-Serres, R., Naik, S., Huynh, B. H., and Lippard, S. J., manuscript in preparation.
18. Merkx, M., Kopp, D. A., Sazinsky, M. H., Blazyk, J. L., Müller, J., and Lippard, S. J. (2001) Dioxygen Activation and Methane Hydroxylation by Soluble Methane Monooxygenase: A Tale of Two Irons and Three Proteins Angew. Chem., Int. Ed. 40, 2782-2807 (Pubitemid 32783348)
19. Fox, B. G., Liu, Y., Dege, J. E., and Lipscomb, J. D. (1991) Complex Formation between the Protein Components of Methane Monooxygenase from Methylosinus trichosporium OB3b: Identification of Sites of Component Interaction J. Biol. Chem. 266, 540-550 (Pubitemid 21906157)
20. Gassner, G. T. and Lippard, S. J. (1999) Component Interactions in the Soluble Methane Monooxygenase System from Methylococcus capsulatus (Bath) Biochemistry 38, 12768-12785
21. Green, J. and Dalton, H. (1985) Protein B of Soluble Methane Monooxygenase from Methylococcus capsulatus (Bath): A Novel Regulatory Protein of Enzyme Activity J. Biol. Chem. 260, 15795-15801 (Pubitemid 16173210)
22. Pikus, J. D., Studts, J. M., Achim, C., Kauffmann, K. E., Münck, E., Steffan, R. J., McClay, K., and Fox, B. G. (1996) Recombinant Toluene-4-monooxygenase: Catalytic and Mössbauer Studies of the Purified Diiron and Rieske Components of a Four-Protein Complex Biochemistry 35, 9106-9119 (Pubitemid 26249858)
23. Liu, K. E. and Lippard, S. J. (1991) Redox Properties of the Hydroxylase Component of Methane Monooxygenase from Methylococcus capsulatus (Bath): Effects of Protein B, Reductase, and Substrate J. Biol. Chem. 266, 12836-12839 (Pubitemid 21907273)
24. Paulsen, K. E., Liu, Y., Fox, B. G., Lipscomb, J. D., Münck, E., and Stankovich, M. T. (1994) Oxidation-Reduction Potentials of the Methane Monooxygenase Hydroxylase Component from Methylosinus trichosporium OB3b Biochemistry 33, 713-722 (Pubitemid 24064110)
25. DeWitt, J. G., Rosenzweig, A. C., Salifoglou, A., Hedman, B., Lippard, S. J., and Hodgson, K. O. (1995) X-ray Absorption Spectroscopic Studies of the Diiron Center in Methane Monooxygenase in the Presence of Substrate and the Coupling Protein of the Enzyme System Inorg. Chem. 34, 2505-2515
26. Fox, B. G., Hendrich, M. P., Surerus, K. K., Andersson, K. K., Froland, W. A., Lipscomb, J. D., and Münck, E. (1993) Mössbauer, EPR, and ENDOR Studies of the Hydroxylase and Reductase Components of Methane Monooxygenase from Methylosinus trichosporium OB3b J. Am. Chem. Soc. 115, 3688-3701
27. Froland, W. A., Andersson, K. K., Lee, S.-K., Liu, Y., and Lipscomb, J. D. (1992) Methane Monooxgenase Component B and Reductase Alter the Regioselectivity of the Hydroxylase Component-catalyzed Reactions: A Novel Role for Protein-Protein Interactions in an Oxygenase Mechanism J. Biol. Chem. 267, 17588-17597
28. Mitić, N., Schwartz, J. K., Brazeau, B. J., Lipscomb, J. D., and Solomon, E. I. (2008) CD and MCD Studies of the Effects of Component B Variant Binding on the Biferrous Active Site of Methane Monooxygenase Biochemistry 47, 8386-8397
29. Pulver, S. C., Froland, W. A., Lipscomb, J. D., and Solomon, E. I. (1997) Ligand Field Circular Dichroism and Magnetic Circular Dichroism Studies of Component B and Substrate Binding to the Hydroxylase Component of Methane Monooxygenase J. Am. Chem. Soc. 119, 387-395 (Pubitemid 27079489)
30. Bailey, L. J., McCoy, J. G., Phillips, G. N., Jr., and Fox, B. G. (2008) Structural Consequences of Effector Protein Complex Formation in a Diiron Hydroxylase Proc. Natl. Acad. Sci. U.S.A. 105, 19194-19198
31. Sazinsky, M. H., Dunten, P. W., McCormick, M. S., Di Donato, A., and Lippard, S. J. (2006) X-ray Structure of a Hydroxylase-Regulatory Protein Complex from a Hydrocarbon-Oxidizing Multicomponent Monooxygenase, Pseudomonas sp. OX1 Phenol Hydroxylase Biochemistry 45, 15392-15404 (Pubitemid 46032464)
32. Blazyk, J. L., Gassner, G. T., and Lippard, S. J. (2005) Intermolecular Electron-Transfer Reactions in Soluble Methane Monooxygenase: A Role for Hysteresis in Protein Function J. Am. Chem. Soc. 127, 17364-17376 (Pubitemid 41791055)
33. Gallagher, S. C., Callaghan, A. J., Zhao, J., Dalton, H., and Trewhella, J. (1999) Global Conformational Changes Control the Reactivity of Methane Monooxygenase Biochemistry 38, 6752-6760
34. Wallar, B. J. and Lipscomb, J. D. (2001) Methane Monooxygenase Component B Mutants Alter the Kinetics of Steps Throughout the Catalytic Cycle Biochemistry 40, 2220-2233 (Pubitemid 32165693)
35. Mitchell, K. H., Studts, J. M., and Fox, B. G. (2002) Combined Participation of Hydroxylase Active Site Residues and Effector Protein Binding in a Para to Ortho Modulation of Toluene 4-Monooxygenase Regiospecificity Biochemistry 41, 3176-3188 (Pubitemid 34184649)
36. Zheng, H. and Lipscomb, J. D. (2006) Regulation of Methane Monooxygenase Catalysis Based on Size Exclusion and Quantum Tunneling Biochemistry 45, 1685-1692 (Pubitemid 43222112)
37. Liu, Y., Nesheim, J. C., Lee, S.-K., and Lipscomb, J. D. (1995) Gating Effects of Component B on Oxygen Activation by the Methane Monooxygenase Hydroxylase Component J. Biol. Chem. 270, 24662-24665
38. Liu, Y., Nesheim, J. C., Paulsen, K. E., Stankovich, M. T., and Lipscomb, J. D. (1997) Roles of the Methane Monooxygenase Reductase Component in the Regulation of Catalysis Biochemistry 36, 5223-5233 (Pubitemid 27199739)
39. Cafaro, V., Izzo, V., Scognamiglio, R., Notomista, E., Capasso, P., Casbarra, A., Pucci, P., and Di Donato, A. (2004) Phenol Hydroxylase and Toluene/ o -Xylene Monooxygenase from Pseudomonas stutzeri OX1: Interplay between Two Enzymes Appl. Environ. Microbiol. 70, 2211-2219 (Pubitemid 38500522)
40. Powlowski, J. and Shingler, V. (1994) Genetics and Biochemistry of Phenol Degradation by Pseudomonas sp. CF600 Biodegradation 5, 219-236
41. Arenghi, F. L. G., Berlanda, D., Galli, E., Sello, G., and Barbieri, P. (2001) Organization and Regulation of meta Cleavage Pathway Genes for Toluene and o -Xylene Derivative Degradation in Pseudomonas stutzeri OX1 Appl. Environ. Microbiol. 67, 3304-3308 (Pubitemid 33644808)
42. Cafaro, V., Scognamiglio, R., Viggiani, A., Izzo, V., Passaro, I., Notomista, E., Dal Piaz, F., Amoresano, A., Casbarra, A., Pucci, P., and Di Donato, A. (2002) Expression and Purification of the Recombinant Subunits of Toluene/ o -Xylene Monooxygeanse and Reconsitution of the Active Complex Eur. J. Biochem. 269, 5689-5699 (Pubitemid 35365558)
43. Bertoni, G., Martino, M., Galli, E., and Barbieri, P. (1998) Analysis of the Gene Cluster Encoding Toluene/ o -Xylene Monooxygenase from Pseudomonas stutzeri OX1 Appl. Environ. Microbiol. 64, 3626-3632 (Pubitemid 28462950)
44. Scognamiglio, R., Notomista, E., Barbieri, P., Pucci, P., Dal Piaz, F., Tramontano, A., and Di Donato, A. (2001) Conformational Analysis of Putative Regulatory Subunit D of the Toluene/ o -Xylene-Monooxygenase Complex from Pseudomonas stutzeri OX1 Protein Sci. 10, 482-490 (Pubitemid 32221139)
45. Song, W. J., Behan, R. K., Naik, S. G., Huynh, B. H., and Lippard, S. J. (2009) Characterization of a Peroxodiiron(III) Intermediate in the T201S Variant of Toluene/ o -Xylene Monooxygenase Hydroxylase from Pseudomonas sp. OX1 J. Am. Chem. Soc. 131, 6074-6075
46. Murray, L. J., García-Serres, R., McCormick, M. S., Davydov, R., Naik, S. G., Kim, S.-H., Hoffman, B. M., Huynh, B. H., and Lippard, S. J. (2007) Dioxygen Activation at Non-Heme Diiron Centers: Oxidation of a Proximal Residue in the I100W Variant of Toluene/ o -Xylene Monooxygenase Hydroxylase Biochemistry 46, 14795-14809 (Pubitemid 350308871)
47. Gibbs, C. R. (1976) Characterization and Application of FerroZine Iron Reagent as a Ferrous Iron Indicator Anal. Chem. 48, 1197-1201
48. Lambeth, D. O. and Palmer, G. (1973) The Kinetics and Mechanism of Reduction of Electron Transfer Proteins and Other Compounds of Biological Interest by Dithionite J. Biol. Chem. 248, 6095-6103
49. Switala, J. and Loewen, P. C. (2002) Diversity of Properties Among Catalases Arch. Biochem. Biophys. 401, 145-154 (Pubitemid 34848616)
50. Elsen, N. L., Bailey, L. J., Hauser, A. D., and Fox, B. G. (2009) Role for Threonine 201 in the Catalytic Cycle of the Soluble Diiron Hydroxylase Toluene 4-Monooxygenase Biochemistry 48, 3838-3846
51. Hildebrandt, A. G. and Roots, I. (1975) Reduced Nicotinamide Adenine Dinucleotide Phosphate (NADPH)-Dependent Formation and Breakdown of Hydrogen Peroxide during Mixed Function Oxidation Reactions in Liver Microsomes Arch. Biochem. Biophys. 171, 385-397
52. Messner, K. R. and Imlay, J. A. (2002) In Vitro Quantitation of Biological Superoxide and Hydrogen Peroxide Generation Methods Enzymol. 349, 354-361 (Pubitemid 34229523)
53. Yang, X. and Ma, K. (2005) Determination of Hydrogen Peroxide Generated by Reduced Nicotinamide Adenine Dinucleotide Oxidase Anal. Biochem. 344, 130-134 (Pubitemid 41569386)
54. Newman, L. M. and Wackett, L. P. (1995) Purification and Characterization of Toluene 2-Monooxygenase from Burkholderia cepacia G4 Biochemistry 34, 14066-14076
55. Cadieux, E., Vrajmasu, V., Achim, C., Powlowski, J., and Münck, E. (2002) Biochemical, Mössbauer, and EPR Studies of the Diiron Cluster of Phenol Hydroxylase from Pseudomonas sp. Strain CF 600 Biochemistry 41, 10680-10691 (Pubitemid 34913328)
56. Song, W. J. and Lippard, S. J. (2011) unpublished results.
57. McCormick, M. S. (2008) Structural Investigations of Hydroxylase Proteins and Complexes in Bacterial Multicomponent Monooxygenase Systems. Ph.D. Thesis, Massachusetts Institute of Technology, Cambridge, MA.
58. Lund, J., Woodland, M. P., and Dalton, H. (1985) Electron Transfer Reactions in the Soluble Methane Monooxygenase of Methylococcus capsulatus (Bath) Eur. J. Biochem. 147, 297-305