Remarkable aliphatic hydroxylation by the diiron enzyme toluene 4-monooxygenase in reactions with radical or cation diagnostic probes norcarane, 1,1-dimethylcyclopropane, and 1,1-diethylcyclopropane

Biochemistry

Volumn 43, Issue 50, 2004, Pages 15688-15701

  Moe, Luke A ^a   Hu, Zhengbo ^c   Deng, Dayi ^c   Austin, Rachel N ^b   Groves, John T ^c   Fox, Brian G ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b BATES COLLEGE   (United States)

^c PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; CATALYSIS; HYDROXYLATION; OXIDATION; POSITIVE IONS; TOLUENE;

ALIPHATIC HYDROXYLATION; ISOMERIC NONCARANOLS; RADICAL OXIDATION;

ENZYMES;

1,1 DIETHYLCYCLOPROPANE; CATION; CRESOL; CYCLOHEX 2 ENYL METHANOL; CYCLOPROPANE DERIVATIVE; DIIRON ENZYME; ENZYME; METHANOL DERIVATIVE; NORCARANE (BICYCLO[4.1.0]HEPTANE) 1,1 DIMETHYLCYCLOPROPANE; OXYGENASE; RADICAL; TOLUENE 4 MONOOXYGENASE; TOLUENE DERIVATIVE; UNCLASSIFIED DRUG; WATER;

ARTICLE; CATALYSIS; HYDROXYLATION; ISOMERISM; OXIDATION; OXYGENATION; PRIORITY JOURNAL;

CATIONS; CYCLOPROPANES; HYDROXYLATION; IRON; ISOENZYMES; MUTATION; OXIDATION-REDUCTION; OXYGEN; OXYGENASES; PSEUDOMONAS MENDOCINA; SUBSTRATE SPECIFICITY; TERPENES; TOLUENE; XENOBIOTICS;

EID: 10844228235     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi040033h     Document Type: Article

References (78)

1. Kelly, S. L., Lamb, D. C., Jackson, C. J., Warrilow, A. G., and Kelly, D. E. (2003) The biodiversity of microbial cytochromes P450, Adv. Microb. Physiol. 47, 131-186.
2. Sullivan, J. P., Dickinson, D., and Chase, H. A. (1998) Methanotrophs, Methylosinus trichosporium OB3b, sMMO, and their application to bioremediation, Crit. Rev. Microbiol. 24, 335-373.
3. Knief, C., Lipski, A., and Dunfield, P. F. (2003) Diversity and activity of methanotrophic bacteria in different upland soils, Appl. Environ. Microbiol. 69, 6703-6714.
4. Shively, J. M., English, R. S., Baker, S. H., and Cannon, G. C. (2001) Carbon cycling: the prokaryotic contribution, Curr. Opin. Microbiol. 4, 301-306.
5. Williams, P. A., and Sayers, J. R. (1994) The evolution of pathways for aromatic hydrocarbon oxidation in Pseudomonas, Biodegradation 5, 195-217.
6. Gottschalk, G. (1986) in Bacterial Metabolism, p 359, Springer-Verlag, New York.
7. Ortiz de Montellano, P. R. (2004) in Cytochrome P450: Structure, Mechanism, and Biochemistry (Ortiz de Montellano, P. R., Ed.), in press, Kluwer Academic/Plenum Press, New York.
8. Groves, J. T. (2004) Models and Mechanisms of Cytochrome P450 Action in Cytochrome P450: Structure, Mechanism, and Biochemistry (Ortiz de Montellano, P. R., Ed.) pp 1-44, Kluwer Academic/Plenum Press, New York.
9. Groves, J. T. (2003) The bioinorganic chemistry of iron in oxygenases and supramolecular assemblies. Proc. Natl. Acad. Sci. U.S.A. 100, 3569-3574.
10. Auclair, K., Hu, Z., Little, D. M., Ortiz de Montellano, P. R., and Groves, J. T. (2002) Revisiting the mechanism of P450 enzymes with the radical clocks norcarane and spiro[2,5]octane, J. Am. Chem. Soc. 124, 6020-6027.
11. Wallar, B. J., and Lipscomb, J. D. (1996) Dioxygen activation by enzymes containing binuclear non-heme iron clusters, Chem. Rev. 96, 2625-2657.
12. Kopp, D., and Lippard, S. J. (2002) Soluble methane monooxygenase: activation of dioxygen and methane, Curr. Opin. Chem. Biol. 6, 568-576.
13. Baik, M.-H., Newcomb, M., Freisner, R. A., and Lippard, S. J. (2003) Mechanistic studies on the hydroxylation of methane by methane monooxygenase, Chem. Rev. 103, 2385-2419.
14. Austin, R. N., Buzzi, J., Kim, E., Zylstra, G. J., and Groves, J. T. (2003) Xylene monooxygenase: a membrane-spanning non-heme diiron enzyme that hydroxylates hydrocarbons via a substrate radical intermediate, J. Biol. Inorg. Chem. 8, 733-740.
15. Austin, R. N., Chang, H.-K., Zylstra, G. J., and Groves, J. T. (2000) The non-heme diiron alkane monooxygenase of Pseudomonas oleovorans (AlkB) hydroxylates via a substrate radical intermediate, J. Am. Chem. Soc. 122, 11747-11748.
16. Shanklin, J., Achim, C., Schmidt, H., Fox, B. G., and Münck, E. (1997) Mössbauer studies of alkane ω-hydroxylase: Evidence for a diiron cluster in an integral membrane enzyme, Proc. Natl. Acad. Sci. U.S.A. 94, 2981-2986.
17. 2+ sites in pMMO from Methylococcus capsulatus (Bath) and Methylmicrobium album BG8, Biophys. J. 79, 1085-1094.
18. Murrell, J. C., McDonald, I. R., and Gilbert, B. (2000) Regulation of expression of methane monooxygenases by copper ions, Trends Microbiol. 8, 221-225.
19. Chan, S. I., Chen, K. H. C., Yu, S. S. F., Chen, C. L., and Kuo, S. S. J. (2004) Toward delineating the structure and function of the particulate methane monooxygenase from methanotrophic bacteria, Biochemistry 43, 4421-4430.
20. Yu, S. S. F., Wu, L. Y., Chen, K. H. C., Luo, W. I., Huang, D. S., and Chan, S. I. (2003) The stereospecific hydroxylation of [2,2-H-2(2)]butane and chiral dideuteriobutanes by the particulate methane monooxygenase from Methylococcus capsulatus (Bath). J. Biol. Chem. 278, 40658-40669.
21. Lieberman, R. L., Shrestha, D. B., Doan, P. E., Hoffman, B. M., Stemmler, T. L., and Rosenzweig, A. C. (2003) Purified particulate methane monooxygenase from Methylococcus capsulatus (Bath) is a dimer with both mononuclear copper and a copper-containing cluster, Proc. Natl. Acad. Sci. U.S.A. 100, 3820-3825.
22. Basu, P., Katterle, B., Andersson, K. K., and Dalton, H. (2003) The membrane-associated form of methane monooxygenase from Methylococcus capsulatus (Bath) is a copper/iron protein, Biochem. J. 369, 417-427.
23. Choi, D. W., Kunz, R. C., Boyd, E. S., Semrau, J. D., Antholine, W. E., Han, J. I., Zahn, J. A., Boyd, J. M., de la Mora, A. M., and DiSpirito, A. A. (2003) The membrane-associated methane monooxygenase (pMMO) and pMMO-NADH:quinone oxidoreductase complex from Methylococcus capsulatus (Bath), J. Bacteriol. 185, 5755-5764.
24. Shaik, S., de Visser, S. P., Ogliaro, F., Schwarz, H., and Schroder, D. (2002) Two-state reactivity mechanisms of hydroxylation and epoxidation by cytochrome P-450 revealed by theory, Curr. Opin. Chem. Biol. 6, 556-567.
25. Groves, J. T., and McCluskey, G. A. (1976) Aliphatic hydroxylation via oxygen rebound: Oxygen transfer catalyzed by iron, J. Am. Chem. Soc. 98, 859-861.
26. Rataj, M. J., Knauth, J. E., and Donnelly, M. I. (1991) Oxidation of deuterated compounds by high specific activity methane monooxygenase from Methylosinus trichosporium OB3b, J. Biol. Chem. 266, 18684-18690.
27. Nesheim, J. C., and Lipscomb, J. D. (1996) Large kinetic isotope effects in methane oxidation catalyzed by methane monooxygenase: Evidence for C-H bond cleavage in a reaction cycle intermediate, Biochemistry 35, 10240-10247.
28. Priestly, N. D., Floss, H. D., Froland, W. A., Lipscomb, J. D., Williams, P. G., and Morimoto, H. (1992) Cryptic stereochemistry of the methane monooxygenase reaction, J. Am. Chem. Soc. 114, 7561-7562.
29. Valentine, A. M., Wilkinson, B., Liu, K. E., Komar-Panicucci, S., Priestly, N. D., Williams, P. D., Morimoto, H., Floss, H. G., and Lippard, S. J. (1997) Tritiated chiral alkanes as substrates for soluble methane monooxygenase from Methylococcus capsulatus (Bath): Probes for the mechanism of hydroxylation, J. Am. Chem. Soc. 119, 1818-1827.
30. Wilkins, P. C., Dalton, H., Samuel, C. J., and Green, J. (1994) Further evidence for multiple pathways in soluble methane-monooxygenase-catalysed oxidations from the measurement of deuterium kinetic isotope effects, Eur. J. Biochem. 226, 555-560.
31. Dunietz, B. D., Beachy, M. D., Cao, Y., Whittington, D. A., Lippard, S. J., and Friesner, R. A. (2000) Large scale ab initio quantum chemical calculation of the intermediates in the soluble methane monooxygenase catalytic cycle, J. Am. Chem. Soc. 122, 2828-2839.
32. Guallar, V., Gherman, B. F., Miller, W. H., Lippard, S. J., and Friesner, R. A. (2002) Dynamics of alkane hydroxylation at the non-heme diiron center in methane monooxygenase, J. Am. Chem. Soc. 124, 3377-3384.
33. Musaev, D. G., Basch, H., and Morokuma, K. (2002) Theoretical study of the mechanism of alkane hydroxylation and ethylene epoxidation reactions catalyzed by diiron bis-oxo complexes. The effect of substrate molecules, J. Am. Chem. Soc. 124, 4135-4148.
34. Siegbahn, P. E. (2001) O-O bond cleavage and alkane hydroxylation in methane monooxygenase, J. Biol. Inorg. Chem. 6, 27-45.
35. Siegbahn, P. E. M., and Crabtree, R. H. (1997) Mechanism of C-H activation by diiron methane monooxygenases: Quantum chemical studies, J. Am. Chem. Soc. 119, 3103-3113.
36. Stearns, R. A., and Ortiz de Montellano, P. R. (1985) Cytochrome P-450 catalyzed oxidation of quadricyclane. Evidence for a radical cation intermediate, J. Am. Chem. Soc. 107, 4081-4082.
37. Ortiz de Montellano, P. R., and Stearns, R. A. (1987) Timing of the radical recombination step in cytochrome P-450 catalysis with ring-strained probes, J. Am. Chem. Soc. 109, 3415-3420.
38. Choi, S.-Y., Eaton, P. E., Kopp, D. A., Newcomb, M., Lippard, S. J., and Shen, R. (1999) Cationic species can be produced in soluble methane monooxygenase-catalyzed hydroxylation reactions; radical intermediates are not, J. Am. Chem. Soc. 121, 12198-12199.
39. Newcomb, M., and Toy, P. H. (2000) Hypersensitive radical probes and the mechanisms of cytochrome P450-catalyzed hydroxylation reactions, Acc. Chem. Res. 33, 449-455.
40. Newcomb, M., Shen, R., Choi, S.-Y., Toy, P. H., Hollenberg, P. F., Vaz, A. D. N., and Coon, M. J. (2000) Cytochrome P450-catalyzed hydroxylation of mechanistic probes that distinguish between radicals and cations. Evidence for cationic but not for radical intermediates, J. Am. Chem. Soc. 122, 2677-2686.
41. Brazeau, B. J., Austin, R. N., Tarr, C., Groves, J. T., and Lipscomb, J. D. (2001) Intermediate Q from soluble methane monooxygenase hydroxylates the mechanistic substrate probe norcarane: evidence for a stepwise reaction, J. Am. Chem. Soc. 123, 11831-11837.
42. Griller, D., and Ingold, K. U. (1980) Free-radical clocks, Acc. Chem. Res. 13, 317-323.
43. Ingold, K. U., and Walton, J. C. (1986) Small, strained bicycloalkyl radicals and some homolytic reactions involving their parent bicycloalkanes, Acc. Chem. Res. 19, 72-77.
44. Bowry, V. W., Lustzk, J., and Ingold, K. U. (1991) Calibration of a new horologery of fast radical "clocks". Ring-opening rates for ring- and α-alkyl-substituted cyclopropylcarbinyl radicals and for the bicyclo[2.1.0]pent-2-yl radical, J. Am. Chem. Soc. 113, 5687-5698.
45. Bowry, V. W., Lusztyk, J., and Ingold, K. U. (1989) Calibration of the bicyclo[2.1.0]pent-2-yl radical ring opening and an oxygen rebound rate constant for cytochrome P-450, J. Am. Chem. Soc. 111, 1927-1928.
46. Choi, S.-Y., Eaton, P. E., Hollenberg, P. F., Liu, K. E., Lippard, S. J., Newcomb, M., Putt, D. A., Upadhyaya, S., and Xiong, Y. (1996) Regiochemical variations in reactions of methylcubane with tert-butoxyl radical, cytochrome P-450 enzymes, and a methane monooxygenase system, J. Am. Chem. Soc. 118, 6547-6555.
47. 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.
48. Whited, G. M., and Gibson, D. T. (1991) Separation and partial characterization of the enzymes of the toluene-4-monooxygenase catabolic pathway in Pseudomonas mendocina KR1, J. Bacteriol. 173, 3017-3020.
49. McClay, K., Fox, B. G., and Steffan, R. J. (1996) Chloroform mineralization by toluene-oxidizing bacteria, Appl. Environ. Microbiol. 62, 2716-2722.
50. McClay, K., Fox, B. G., and Steffan, R. J. (2000) Toluene monooxygenase catalyzed epoxidation of alkenes, Appl. Environ. Microbiol. 66, 1877-1882.
51. 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.
52. 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.
53. Groves, J. T., Kruper, J. W., and Haushalter, R. C. (1980) Hydrocarbon oxidation with oxometalloporphinates. Isolation and reaction of a (porphinato)manganese(V) complex, J. Am. Chem. Soc. 102, 6375-6377.
54. Pikus, J. D., Mitchell, K. H., Studts, J. M., McClay, K., Steffan, R. J., and Fox, B. G. (2000) Threonine 201 in the diiron enzyme toluene 4-monooxygenase is not required for catalysis. Biochemistry 39, 791-799.
55. Mitchell, K. H., Rogge, C. E., Gierahn, T., and Fox, B. G. (2003) Insight into the mechanism of aromatic hydroxylation by toluene 4-monooxygenase through the use of specificially deuterated toluene and p-xylene, Proc. Natl. Acad. Sci. U.S.A. 100, 3784-3789.
56. van Leusen, D., and van Leusen, A. (1980) A simple synthesis of cyclobutanone, Synthesis 4, 325-326.
57. Bloomquist, A. T., Passer, M., and Schollenberger, C. S. (1957) Thermal Condensation of Formaldehyde with Acyclic Olefins, J. Am. Chem. Soc. 79, 4972-4976.
58. Marvel, C. S., Myers, R. L., and Saunders, J. H. (1948) The Preparation of 2-Alkylbutadienes, J. Am. Chem. Soc. 70, 1694-1699.
59. 15N resonances of the Rieske ferredoxin component from toluene 4-monooxygenase, Biochemistry 38, 727-739.
60. Studts, J. M., Mitchell, K. H., Pikus, J. D., McClay, K., Steffan, R. J., and Fox, B. G. (2000) Optimized expression and purification of toluene 4-monooxygenase hydroxylase, Protein Expression Purif. 20, 58-65.
61. Hemmi, H., Studts, J. M., Chae, Y. K., Song, J., Markley, J. L., and Fox, B. G. (2001) Solution structure of the toluene 4-monooxygenase effector protein (T4moD), Biochemistry 40, 3512-3524.
62. Ruzicka, F., Huang, D.-S., Donnelly, M. I., and Frey, P. A. (1990) Methane monooxygenase catalyzed oxidation of 1,1-dimethyl-cyclopropane. Evidence for radical and carbocationic intermediates, Biochemistry 29, 1696-1700.
63. 9 desaturase complex, Biochemistry 39, 10507-10513.
64. Newcomb, M., Shen, R., Lu, Y., Coon, M. J., Hollenberg, P. F., Kopp, D. A., and Lippard, S. J. (2002) Evaluation of norcarane as a probe for radicals in cytochrome P450- and soluble methane monooxygenase-catalyzed hydroxylation reactions, J. Am. Chem. Soc. 124, 6879-6886.
65. Canada, K. A., Iwashita, S., Shim, H., and Wood, T. K. (2002) Directed evolution of toluene ortho-monooxygenase for enhanced 1-naphthol synthesis and chlorinated ethene degradation, J. Bacteriol. 184, 344-349.
66. Rui, L., Kwon, Y. K., Fishman, A., Reardon, K. F., and Wood, T. K. (2004) Saturation Mutagenesis of Toluene ortho-Monooxygenase of Burkholderia cepacia G4 for Enhanced 1-Naphthol Synthesis and Chloroform Degradation, Appl. Environ. Microbiol. 70, 3246-3252.
67. Vardar, G., and Wood, T. K. (2004) Protein Engineering of Toluene-o-Xylene Monooxygenase from Pseudomonas stutzeri OX1 for Synthesizing 4-Methylresorcinol, Methylhydroquinone, and Pyrogallol, Appl. Environ. Microbiol 70, 3253-3262.
68. Åberg, A., Ormö, M., Nordlund, P., and Sjöberg, B.-M. (1993) Autocatalytic generation of dopa in the engineered protein R2 F208Y from Escherichia coli ribonucleotide reductase and crystal structure of the dopa-208 protein, Biochemistry 32, 9845-9850.
69. Logan, D. T., deMaré, F., Persson, B. O., Slaby, A., Sjöberg, B.-M., and Nordlund, P. (1998) Crystal structure of two self-hydroxylating ribonucleotide reductase protein R2 mutants: structural basis for the oxygen-insertion step catalyzed by the diiron proteins, Biochemistry 37, 10798-10807.
70. Ormö, M., deMaré, F., Regnström, K., Åberg, A., Sahlin, M., Ling, J., Loehr, T. M., Sanders-Loehr, J., and Sjöberg, B.-M. (1992) Engineering of the iron site in ribonucleotide reductase to a self-hydroxylating monooxygenase, J. Biol. Chem. 267, 8711-8714.
71. Ling, J., Sahlin, M., Sjöberg, B.-M., Loehr, T. M., and Sanders-Loehr, J. (1994) Dioxygen is the source of the oxo bridge in ribonucleotide reductase, J. Biol. Chem. 269, 5596-5601.
72. Baldwin, J., Voegtli, W. C., Khidekel, N., Moënne-Loccoz, P., Krebs, C., Pereira, A. S., Ley, B. A., Huynh, B. H., Loehr, T. M., Riggs-Gelasco, P. J., Rosenzweig, A. C., and Bollinger, J. M., Jr. (2001) Rational reprogramrning of the R2 subunit of Escherichia coli ribonucleotide reductase into a self-hydroxylating monooxygenase, J. Am. Chem. Soc. 123, 7017-7030.
73. Voegtli, W. C., Khidekel, N., Baldwin, J., Ley, B. A., Bollinger, J. M., Jr., and Rosenzweig, A. C. (2000) Crystal structure of the ribonucleotide reductase R2 mutant that accumulates a μ-1,2-peroxodiiron(III) intermediate during oxygen activation, J. Am. Chem. Soc. 122, 3255-3261.
74. White, R. D., and Fox, B. G. (2003) Chain cleavage and sulfoxidation of thiastearoyl-ACP upon reaction with stearoyl-ACP desaturase, Biochemistry 42, 7828-7835.
75. Rogge, C. E., and Fox, B. G. (2002) Desaturation, chain scission, and register-shift of oxygen-substituted fatty acids during reaction with stearoyl-ACP desaturase, Biochemistry 41, 10141-10148.
76. Fox, B. G., Lyle, K. S., and Rogge, C. E. (2004) Reactions of the diiron enzyme stearoyl-ACP desaturase, Acc. Chem. Res. 37, 421-429.
77. Nordlund, P., and Eklund, H. (1993) Structure and function of the Escherichia coli ribonucleotide reductase protein R2, J. Mol. Biol. 232, 123-164.
78. 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.