Redox and functional analysis of the Rieske ferredoxin component of the toluene 4-monooxygenase

Biochemistry

Volumn 46, Issue 4, 2007, Pages 976-986

  Elsen, Nathaniel L ^a   Moe, Luke A ^a   McMartin, Lea A ^a   Fox, Brian G ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYTIC SPECIALIZATION; FERREDOXIN; PROTEIN PROTEIN INTERACTIONS; REDOX POTENTIAL;

BIOCATALYSTS; CATALYST ACTIVITY; ELECTROSTATICS; HYDROXYLATION; MUTAGENESIS; PURIFICATION;

ENZYME KINETICS;

FERREDOXIN; OXIDOREDUCTASE; OXYGEN; OXYGENASE; PARA CRESOL; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; RIESKE FERREDOXIN; TOLUENE 4 MONOOXYGENASE; TOLUENE 4 MONOOXYGENASE TBUB; UNCLASSIFIED DRUG; UNSPECIFIC MONOOXYGENASE;

ARTICLE; BURKHOLDERIA CEPACIA; CATALYSIS; ENZYME MECHANISM; HYDROXYLATION; MUTAGENESIS; NONHUMAN; OXIDATION REDUCTION REACTION; PHYLOGENY; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RALSTONIA PICKETTII; THERMUS;

AMINO ACID SEQUENCE; BURKHOLDERIA CEPACIA; ELECTRON TRANSPORT COMPLEX III; ELECTROSTATICS; FERREDOXINS; GENETIC COMPLEMENTATION TEST; HYDROGEN BONDING; IRON-SULFUR PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; OXIDATION-REDUCTION; OXYGENASES; PSEUDOMONAS; RALSTONIA PICKETTII; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SPECTROPHOTOMETRY; THERMUS THERMOPHILUS;

RALSTONIA PICKETTII; THERMUS;

EID: 33846687102     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0616145     Document Type: Article

References (69)

1. Kuznetsov, V. Y., Blair, E., Farmer, P. J., Poulos, T. L., Pifferitti, A., and Sevrioukova, I. F. (2005) The putidaredoxin reductase-putidaredoxin electron transfer complex: theoretical and experimental studies, J. Biol. Chem. 280, 16135-16142.
2. Tollin, G., Cheddar, G., Watkins, J. A., Meyer, T. E., and Cusanovich, M. A. (1984) Electron transfer between flavodoxin semiquinone and c-type cytochromes: correlations between electrostatically corrected rate constants, redox potentials, and surface topologies, Biochemistry 23, 6345-6349.
3. Ludden, P. W., Okon, Y., and Burris, R. H. (1978) The nitrogenase system of Spirillum lipoferum, Biochem. J. 173, 1001-1003.
4. Johnson, D. C., Dean, D. R., Smith, A. D., and Johnson, M. K. (2005) Structure, function, and formation of biological iron-sulfur clusters, Annu. Rev. Biochem. 74, 247-281.
5. Stephens, P. J., Jollie, D. R., and Warshel, A. (1996) Protein control of redox potentials of iron-sulfur proteins, Chem. Rev. 96, 2491-2514.
6. Trumpower, B. L., and Gennis, R. B. (1994) Energy transduction by cytochrome complexes in mitochondrial and bacterial respiration: the enzymology of coupling electron transfer reactions to transmembrane proton translocation, Annu. Rev. Biochem. 63, 675-716.
7. Berry, E. A., Guergovas-Kuras, M., Huang, L. S., and Crofts, A. R. (2000) Structure and function of cytochrome bc complexes, Annu. Rev. Biochem. 69, 1005-1075.
8. Mason, J. R., and Cammack, R. (1992) The electron-transport proteins of hydroxylating bacterial dioxygenases, Annu. Rev. Microbiol. 46, 277-305.
9. Harayama, S., Kok, M., and Neidle, E. L. (1992) Functional and evolutionary relationships among diverse oxygenases, Annu. Rev. Microbiol. 46, 565-601.
10. Harborne, N. R., Griffiths, L., Busby, S. J., and Cole, J. A. (1992) Transcriptional control, translation and function of the products of the five open reading frames of the Escherichia coli nir operon, Mol. Microbiol. 6, 2805-2813.
11. Ellis, P. J., Conrads, T., Hille, R., and Kuhn, P. (2001) Crystal structure of the 100 kDa arsenite oxidase from Alcaligenes faecalis in two crystal forms at 1.64 Å and 2.03 Å, Structure 9, 125-132.
12. Gibson, D. T., and Parales, R. E. (2000) Aromatic hydrocarbon dioxygenases in environmental biotechnology, Curr. Opin. Biotechnol. 11, 236-43.
13. Leahy, J. G., Batchelor, P. J., and Morcomb, S. M. (2003) Evolution of the soluble diiron monooxygenases, FEMS Microbiol. Rev. 27, 449-479.
14. Batie, C. J., Ballou, D. P., and Correll, C. C. (1992) Phthalate dioxygenase reductase and related flavin-iron-sulfur containing electron transferases, in Chemistry and Biochemistry of the Flavoenzymes (Mueller, F., Ed.) pp 543-556, CRC Press, Boca Raton, FL.
15. Colbert, C. L., Couture, M. M., Eltis, L. D., and Bolin, J. T. (2000) A cluster exposed: structure of the Rieske ferredoxin from biphenyl dioxygenase and the redox properties of Rieske Fe-S proteins, Structure 8, 1267-1278.
16. Link, T. (1999) The structures of Rieske and Rieske-type proteins, Adv. Inorg. Chem. 47, 83-157.
17. Hunsicker-Wang, L. M., Heine, A., Chen, Y., Luna, E. P., Todaro, T., Zhang, Y. M., Williams, P. A., McRee, D. E., Hirst, J., Stout, C. D., and Fee, J. A. (2003) High-resolution structure of the soluble, respiratory-type Rieske protein from Thermus thermophilus: analysis and comparison, Biochemistry 42, 7303-7317.
18. 1 complex, Biochim. Biophys. Acta 1275, 54-60.
19. Nam, J. W., Noguchi, H., Zui, Fujimoto, Mizuno, H., Ashikawa, Y., Abo, M., Fushinobu, S., Kobashi, N., Wakagi, T., Iwata, K., Yoshida, T., Habe, H., Yamane, H., Omori, T., and Nojiri, H. (2005) Crystal structure of the ferredoxin component of carbazole 1,9a-dioxygenase of Pseudomonas resinovorans strain CA10, a novel Rieske non-heme iron oxygenase system, Proteins: Struct., Funct., Bioinf. 58, 779-789.
20. Bonisch, H., Schmidt, C. L., Schafer, G., and Ladenstein, R. (2002) The structure of the soluble domain of an archaeal Rieske iron-sulfur protein at 1.1 Å resolution, J. Mol. Biol. 319, 791-805.
21. 1 complex determined by MAD phasing at 1.5 Å resolution, Structure 4, 567-579.
22. Moe, L., Bingman, C. A., Wesenberg, G. E., Phillips, G. N., and Fox, B. G. (2006) Structure of T4moC, the Rieske-type ferredoxin component of toluene 4-monooxygenase, Acta Crystallogr., Sect. D: Biol. Crystallogr. 62, 476-482.
23. Whited, G. M., and Gibson, D. T. (1991) Toluene 4-monooxygenase, a three component enzyme system that catalyzes the oxidation of toluene to p-cresol in Pseudomonas mendocina KR1, J. Bacteriol. 173, 3010-3016.
24. 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.
25. Couture, M. M., Colbert, C. L., Babini, E., Rosell, F. I., Mauk, A. G., Bolin, J. T., and Elus, L. D. (2001) Characterization of BphF, a Rieske-type ferredoxin with a low reduction potential, Biochemistry 40, 84-92.
26. Olsen, R. H., Kukor, J. J., and Kaphammer, B. (1994) A novel toluene-3-monooxygenase pathway cloned from Pseudomonas pickettii PK01, J. Bacteriol. 176, 3749-3756.
27. Pikus, J. D., Studts, J. M., McClay, K., Steffan, R. J., and Fox, B. G. (1997) Changes in the regiospecificity of aromatic hydroxylation produced by active site engineering in the diiron enzyme toluene 4-monooxygenase, Biochemistry 36, 9283-9289.
28. Studts, J. M., and Fox, B. G. (1999) Application of fed-batch fermentation to the preparation of isotopically labeled or selenomethionine- labeled proteins, Protein Expression Purif. 16, 109-119.
29. 15N resonances of the Rieske ferredoxin component from toluene 4-monooxygenase, Biochemistry 38, 727-739.
30. Mitchell, K. H., Studts, J. M., and Fox, B. G. (2002) Combined participation of effector protein binding and hydroxylase active site residues provide toluene 4-monooxygenase regiospecificity, Biochemistry 41, 3176-3188.
31. Hinckley, G. T., and Frey, P. A. (2006) An adaptable spectroelectrochemical titrator: The midpoint reduction potential of the iron-sulfur center in lysine 2,3-aminomutase, Anal. Biochem. 349, 103-111.
32. Bailey, S. I., and Ritchie, I. M. (1985) A cyclic voltammetric study of the aqueous electrochemistry of some quinines, Electrochim. Acta 30, 3-12.
33. Clark, W. M. (1960) Oxidation-reduction potentials of organic systems, Williams and Wilkins, Baltimore, MD.
34. Neese, F. (2004) Orca-An ab initio, Density Functional, and Semiempirical Program Package, Version 2.4, revision 2, July 2004. Max-Planck-Institut für Bioanorganische Chemie, Mülheim, Germany.
35. Schäfer, A., Horn, H., and Ahlrichs, R. (1992) Fully optimized contracted Gaussian-basis sets for atoms Li to Kr, J. Chem. Phys. 97, 2571-2577.
36. Becke, A. (1993) A new mixing of Hartree-Fock and local density-functional theories, J. Chem. Phys. 98, 1372-1377.
37. Lee, C., Yang, W., and Parr, R. (1988) Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density, Phys. Rev. B 37, 785-789.
38. Laaksonen, L. (1992) A graphics program for the analysis and display of molecular dynamics trajectories, J. Mol. Graphics 10, 33-34.
39. Chen, J., Anderson, J. B., DeWeese-Scott, C., Fedorova, N. D., Geer, L. Y., He, S., Hurwitz, D. I., Jackson, J. D., Jacobs, A. R., Lanczycki, C. J., Liebert, C. A., Liu, C., Madej, T., Marchler-Bauer, A., Marchler, G. H., Mazumder, R., Nikolskaya, A. N., Rao, B. S., Panchenko, A. R., Shoemaker, B. A., Simonyan, V., Song, J. S., Thiessen, P. A., Vasudevan, S., Wang, Y., Yamashita, R. A., Yin, J. J., and Bryant, S. H. (2003) MMDB: Entrez's 3D-structure database, Nucleic Acids Res. 31, 474-477.
40. Lambert, C., Leonard, N., De, Bolle, X., and Depiereux, E. (2002) ESyPred3D: Prediction of proteins 3D structures, Bioinformatics 18, 1250-1256.
41. Baker, N. A., Sept, D., Joseph, S., Holst, M. J., and McCammon, J. A. (2001) Electrostatics of nanosystems: application to microtubules and the ribosome, Proc. Natl. Acad. Sci. U.S.A. 98, 10037-10041.
42. Holst, M., and Saied, F. (1995) Numerical solution of the nonlinear Poisson-Boltzmann equation: Developing more robust and efficient methods, J. Comput. Chem. 16, 337-364.
43. Skjeldal, L., Peterson, F. A., Doreleijers, J. F., Moe, L. A., Pikus, J. D., Volkman, B. F., Westler, W. M., Markley, J. L., and Fox, B. G. (2004) Solution structure of T4moC, the Rieske ferredoxin component of the toluene 4-monooxygenase complex, J. Biol. Inorg. Chem. 9, 945-953.
44. Nam, J. W., Nojiri, H., Yoshida, T., Habe, H., Yamane, H., and Omori, T. (2001) New classification system for oxygenase components involved in ring-hydroxylating oxygenations, Biosci., Biotechnol., Biochem. 65, 254-263.
45. Denke, E., Merbitz-Zahradnik, T., Hatzfeld, O. M., Snyder, C. H., Link, T. A., and Trumpower, B. L. (1998) Alteration of the midpoint potential and catalytic activity of the Rieske iron-sulfur protein by changes of amino acids forming hydrogen bonds to the iron-sulfur cluster, J. Biol. Chem. 273, 9085-9093.
46. 1 complex in Paracoccus denitrificans, Eur. J. Biochem. 255, 100-106.
47. a values of Rieske iron-sulfur proteins, Biochemistry 43, 12383-12389.
48. Zu, Y., Couture, M. M., Kolling, D. R., Crofts, A. R., Eltis, L. D., Fee, J. A., and Hirst, J. (2003) Reduction potentials of Rieske clusters: importance of the coupling between oxidation state and histidine protonation state, Biochemistry 42, 12400-12408.
49. Brugna, M., Nitschke, W., Asso, M., Guigliarelli, B., Lemesle-Meunier, D., and Schmidt, C. (1999) Redox components of cytochrome bc-type enzymes in acidophilic prokaryotes, J. Biol. Chem. 274, 16766-16772.
50. Carrell, C. J., Zhang, H., Cramer, W. A., and Smith, J. L. (1997) Biological identity and diversity in photosynthesis and respiration: structure of the lumen-side domain of the chloroplast Rieske protein, Structure 5, 1613-1625.
51. Flint, D. H., Tuminello, J. F., and Emptage, M. H. (1993) The inactivation of Fe-S cluster containing hydro-lyases by superoxide, J. Biol. Chem. 268, 22369-22376.
52. Ding, H., and Demple, B. (1998) Thiol-mediated disassembly and reassembly of [2Fe-2S] clusters in the redox-regulated transcription factor SoxR, Biochemistry 37, 17280-17286.
53. 2+ cluster of FNR from Escherichia coli, Biochemistry 43, 791-798.
54. Cardinale, G. J., and Abeles, R. H. (1968) Purification and mechanism of action of proline reacemase, Biochemistry 7, 3970-3978.
55. Itzhaki, L. S., and Evans, P. A. (1996) Solvent isotope effects on the refolding kinetics of hen egg-white lysozyme, Protein Sci. 5, 140-146.
56. Kauppi, B., Lee, K., Carredano, E., Parales, R. E., Gibson, D. T., Eklund, H., and Ramaswamy, S. (1998) Structure of an aromatic-ring-hydroxylating dioxygenase-naphthalene 1,2-dioxygenase, Structure 6, 571-586.
57. Bertoni, G., Bolognesi, F., Galli, E., and Barbieri, P. (1996) Cloning of the genes for and characterization of the early stages of toluene catabolism in Pseudomonas stutzeri OX1, Appl. Environ. Microbiol. 62, 3704-3711.
58. Hoke, K., Cobb, N., Armstrong, F., and Hille, R. (2004) Electrochemical studies of arsenite oxidase: an unusual example of a highly cooperative two-electron molybdenum center, Biochemistry 43, 1667-1674.
59. Zhang, H., Carrell, C., Huang, D., Sled, V., Ohnishi, T., Smith, J., and Cramer, W. (1996) Characterization and crystallization of the lumen side domain of the chloroplast Rieske iron-sulfur protein, J. Biol. Chem. 271, 31360-31366.
60. 1 complex and in bacterial dioxygenases by circular dichroism spectroscopy and cyclic voltammetry, Biochemistry 35, 7546-7552.
61. 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.
62. + reductase is a critical residue for binding ferredoxin and flavodoxin during electron transfer, Biochemistry 37, 13604-13613.
63. Sobrado, P., Lyle, K., Kaul, S., Turco, M., Arabshahi, I., Marwah, A., and Fox, B. (2006) Indentification of the binding region of the [2Fe-2S] ferredoxin in stearoyl-acyl carrier protein desaturase: Insight into the catalytic complex and mechanism of action, Biochemistry 45, 4848-4858.
64. Morales, R., Charon, M. H., Kachalova, G., Serre, L., Medina, M., Gomez-Moreno, C., and Frey, M. (2000) A redox-dependent interaction between two electron-transfer partners involved in photosynthesis, EMBO Rep. 1, 271-276.
65. Martins, B. M., Svetlitchnaia, T., and Dobbek, H. (2005) 2-oxo-quinoline 8-monooxygenase oxygenase component: Active site modulation by Rieske-[2Fe-2S] center oxidation/reduction, Structure 13, 817-824.
66. Beharry, Z. M., Eby, D. M., Coulter, E. D., Viswanathan, R., Neidle, E. L., Phillips, R. S., and Kurtz, D. M., Jr. (2003) Histidine ligand protonation and redox potential in the Rieske dioxygenases: role of a conserved aspartate in anthranilate 1,2-dioxygenase, Biochemistry 42, 13625-13636.
67. Pinto, A., Tarasev, M., and Ballou, D. P. (2006) Substitutions of the "bridging" aspartate 178 result in profound changes in the reactivity of the Rieske center of phthalate dioxygenase, Biochemistry 45, 9032-9041.
68. Tarasev, M., Pinto, A., Kim, D., Elliott, S. J., and Ballou, D. P. (2006) The "bridging" aspartate 178 in phthalate dioxygenase facilitates interactions between the Rieske center and the iron-(II)-mononuclear center, Biochemistry 45, 10208-10216.
69. Moe, L., McMartin, L., and Fox, B. (2006) Component interactions and implications for complex formation in the multicomponent toluene 4-monooxygenase, Biochemistry 45, 5478-5485.