Oxygen-18 tracer studies of enzyme reactions with radical/cation diagnostic probes

Biochemical and Biophysical Research Communications

Volumn 338, Issue 1, 2005, Pages 240-249

  Moe, Luke A ^a   Fox, Brian G ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Catalysis; Diiron enzyme; Hydroxylation mechanism; Norcarane; Oxygen 18; Radical clock

Indexed keywords

CATION; CYCLOPROPANE; CYTOCHROME P450; OXYGEN 18; RADICAL; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; TOLUENE DERIVATIVE; TRACER;

ANALYTIC METHOD; CATALYSIS; CATALYST; COMPARATIVE STUDY; DIAGNOSTIC TEST; ENZYME ENGINEERING; ENZYME MECHANISM; ENZYME SUBSTRATE; HYDROXYLATION; PRIORITY JOURNAL; REVIEW;

CATIONS; DIMYRISTOYLPHOSPHATIDYLCHOLINE; DIOXYGENASES; ENZYMES; MOLECULAR PROBES; OXYGEN; OXYGEN ISOTOPES; REACTIVE OXYGEN SPECIES; TERPENES;

EID: 27544477398     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2005.08.217     Document Type: Review

References (58)

1. R.Y. Stanier, O. Hayaishi, and M. Tsuchida The bacterial oxidation of tryptophan. I. A general survey of the pathways J. Bacteriol. 62 1951 355 366
2. H.N. Fernley, and W.C. Evans Oxidative metabolism of polycyclic hydrocarbons by soil pseudomonads Nature 182 1958 373 375
3. S. Dagley, W.C. Evans, and D.W. Ribbons New pathways in the oxidative metabolism of aromatic compounds by microorganisms Nature 188 1960 560 566
4. H.S. Mason, W.L. Fowlks, and E. Peterson Oxygen transfer and electron transport by the phenolase complex J. Am. Chem. Soc. 77 1955 2914 2915
5. O. Hayaishi, M. Katagiri, and S. Rothberg Mechanism of the pyrocatechase reaction J. Am. Chem. Soc. 77 1955 5450 5451
6. 18O studies of pyrogallol cleavage by catechol 1,2-dioxygenase J. Biol. Chem. 259 1984 13056 13060
7. D.T. Gibson, M. Hensley, H. Yoshioka, and T.J. Mabry Formation of (+)-cis-2,3-dihydroxy-1-methylcyclohexa-4,6-diene from toluene by Pseudomonas putida Biochemistry 9 1970 1626 1630
8. D.T. Gibson, G.E. Cardini, F.C. Maseles, and R.E. Kallio Incorporation of oxygen-18 into benzene by Pseudomonas putida Biochemistry 9 1970 1631 1635
9. D.T. Gibson, S.M. Resnick, K. Lee, J.M. Brand, D.S. Torok, L.P. Wackett, M.J. Schocken, and B.E. Haigler Desaturation, dioxygenation, and monooxygenation reactions catalyzed by naphthalene dioxygenase from Pseudomonas sp. strain 9816-4 J. Bacteriol. 177 1995 2615 2621
10. O. Hayaishi Fifty years of oxygen activation J. Biol. Inorg. Chem. 10 2005 1 2
11. D. Prockop, A. Kaplan, and S. Udenfriend Oxygen-18 studies on the conversion of proline to collagen hydroxyproline Arch. Biochem. Biophys. 101 1963 499 503
12. I.J. Higgins, and J.R. Quayle Oxygenation of methane by methane-grown Pseudomonas methanica and Methylomonas methanooxidans Biochem. J. 118 1970 201 208
13. T. Madhok, H. Schnoes, and H.F. DeLuca Mechanism of 25- hydroxycholecalciferol 1α-hydroxylation. Incorporation of oxygen-18 into the 1α position of 25-hydroxycholecalciferol Biochemistry 12 1970 2555 2558
14. J.D. Pikus, J.M. Studts, K. McClay, R.J. Steffan, and B.G. Fox Changes in the regiospecificity of aromatic hydroxylation produced by active site engineering in the diiron enzyme toluene 4-monooxygenase Biochemistry 36 1997 9283 9289
15. J.D. Pikus, K.H. Mitchell, J.M. Studts, K. McClay, R.J. Steffan, and B.G. Fox Threonine 201 in the diiron enzyme toluene 4-monooxygenase is not required for catalysis Biochemistry 39 2000 791 799
16. K.H. Mitchell, J.M. Studts, and B.G. Fox Combined participation of effector protein binding and hydroxylase active site residues provide toluene 4-monooxygenase regiospecificity Biochemistry 41 2002 3176 3188
17. L.A. Moe, Z. Hu, D. Deng, R.N. Austin, J.T. Groves, and B.G. Fox 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 43 2004 15688 15701
18. K.H. Mitchell, C.E. Rogge, T. Gierahn, and B.G. Fox Insight into the mechanism of aromatic hydroxylation by toluene 4-monooxygenase through the use of specifically deuterated toluene and p-xylene Proc. Natl. Acad. Sci. USA 100 2003 3784 3789
19. G.A. Hamilton Mechanisms of biological oxidation reactions involving oxygen and reduced oxygen derivatives C.C. Reddy G.A. Hamilton K.M. Madyastha Biological Oxidation Systems 1990 Academic Press New York
20. B.J. Wallar, and J.D. Lipscomb Dioxygen activation by enzymes containing binuclear non-heme iron clusters Chem. Rev. 96 1996 2625 2657
21. M. Merkx, D.A. Kopp, M.H. Sazinsky, J.L. Blazyk, J. Muller, and S.J. Lippard Dioxygen activation and methane hydroxylation by soluble methane monooxygenase: a tale of two irons and three proteins Angew. Chem. Int. Ed. Engl. 40 2001 2782 2807
22. S. Shaik, S. Cohen, S.P. de Visser, P.K. Sharma, D. Kumar, S. Kozuch, F. Ogliaro, and D. Danovich The rebound controversy: an overview and theoretical modeling of the rebound step in C-H hydroxylation by cytochrome P450 Eur. J. Inorg. Chem. 2 2004 207 226
23. V. Guallar, B.F. Gherman, W.H. Miller, S.J. Lippard, and R.A. Friesner Dynamics of alkane hydroxylation at the non-heme diiron center in methane monooxygenase J. Am. Chem. Soc. 124 2002 3377 3384
24. J.T. Groves, and G.A. McCluskey Aliphatic hydroxylation via oxygen rebound: oxygen transfer catalyzed by iron J. Am. Chem. Soc. 98 1976 859 861
25. J.T. Groves The bioinorganic chemistry of iron in oxygenases and supramolecular assemblies Proc. Natl. Acad. Sci. USA 100 2003 3569 3574
26. D. Griller, and K.U. Ingold Free-radical clocks Acc. Chem. Res. 13 1980 317 323
27. M. Newcomb, M.-H. Le Tadic-Biadatti, D.L. Chesney, E.F. Roberts, and P.F. Hollenberg A nonsynchronous concerted mechanism for cytochrome P-450 catalyzed hydroxylation J. Am. Chem. Soc. 117 1995 12085 12091
28. M. Newcomb, and D.L. Chestney A hypersensitive mechanistic probe for distinguishing between radical and carbocation intermediates J. Am. Chem. Soc. 116 1994 9753 9754
29. M. Newcomb, C.C. Johnson, M.B. Manek, and T.R. Varick Picosecond radical kinetics. Ring openings of phenyl substituted cyclopropylcarbinyl radicals J. Am. Chem. Soc. 114 1992 10915 10921
30. J.K. Atkinson, and K.U. Ingold Cytochrome P450 hydroxylation of hydrocarbons: variation in the rate of oxygen rebound using cyclopropyl radical clocks including two new ultrafast probes J. Am. Chem. Soc. 32 1993 9209 9214
31. Y. Jin, and J.D. Lipscomb Mechanistic insights into C-H activation from radical clock chemistry: oxidation of substituted methylcyclopropanes catalyzed by soluble methane monooxygenase from Methylosinus trichosporium OB3b Biochim. Biophys. Acta 1543 2000 47 59
32. V.W. Bowry, and K.U. Ingold A radical clock investigation of microsomal cytochrome P-450 hydroxylation of hydrocarbons. Rate of oxygen rebound J. Am. Chem. Soc. 113 1991 5699 5707
33. P.R. Ortiz de Montellano, and R.A. Stearns Timing of the radical recombination step in cytochrome P-450 catalysis with ring-strained probes J. Am. Chem. Soc. 109 1987 3415 3420
34. K.B. Wiberg, V.Z. Williams Jr., and L.E. Friedrich Solvolysis of bicyclo[2.1.O]pentyl 2- (3,5-dinitrobenzoates) J. Am. Chem. Soc. 92 1970 564 567
35. M. Newcomb, R. Shen, S.-Y. Choi, P.H. Toy, P.F. Hollenberg, A.D.N. Vaz, and M.J. Coon 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 2000 2677 2686
36. K. Auclair, Z. Hu, D.M. Little, P.R. Ortiz de Montellano, and J.T. Groves Revisiting the mechanism of P450 enzymes with the radical clocks norcarane and spiro[2,5]octane J. Am. Chem. Soc. 124 2002 6020 6027
37. F. Ruzicka, D.-S. Huang, M.I. Donnelly, and P.A. Frey Methane monooxygenase catalyzed oxygenation of 1,1-dimethylcyclopropane. Evidence for radical and carbocationic intermediates Biochemistry 29 1990 1696 1700
38. E.C. Friedrich, and R.L. Holmstead Cyclopropylcarbinyl-allylcarbinyl radical rearrangements in the simple bicyclo[3.1.0]hexyl and-[4.1.0]heptyl systems J. Org. Chem. 37 1972 2550 2554
39. M. Newcomb, and P.H. Toy Hypersensitive radical probes and the mechanisms of cytochrome P450-catalyzed hydroxylation reactions Acc. Chem. Res. 33 2000 449 455
40. J.T. Groves, J.W. Kruper, and R.C. Haushalter Hydrocarbon oxidation with oxometalloporphinates. Isolation and reaction of a porphinatomanganese(V) complex J. Am. Chem. Soc. 102 1980 6375
41. E.C. Friedrich, and J.D. Cooper Jassawalla Methyl substituent effects on cyclopropylcarbinyl-cyclopropylcarbinyl cation rearrangements in the 2-bicyclo[4.1.0]heptyl system Tetrahedron Lett. 11 1978 953 956
42. E.C. Friedrich, and J.D. Cooper Jassawalla Methyl substituent effects upon the chemistry of 2-bicyclo[4.1.0]heptyl 3,5-dinitrobenzoates J. Org. Chem. 44 1979 4224 4229
43. M. Newcomb, R. Shen, Y. Lu, M.J. Coon, P.F. Hollenberg, D.A. Kopp, and S.J. Lippard Evaluation of norcarane as a probe for radicals in cytochrome P450- and soluble methane monooxygenase-catalyzed hydroxylation reactions J. Am. Chem. Soc. 122 2002 2677 2686
44. B.J. Brazeau, R.N. Austin, C. Tarr, J.T. Groves, and J.D. Lipscomb Intermediate Q from soluble methane monooxygenase hydroxylates the mechanistic substrate probe norcarane: evidence for a stepwise reaction J. Am. Chem. Soc. 123 2001 11831 11837
45. S.-K. Lee, J.C. Nesheim, and J.D. Lipscomb Transient intermediates of the methane monooxygenase catalytic cycle J. Biol. Chem. 268 1993 21569 21577
46. M.P. Hendrich, E. Münck, B.G. Fox, and J.D. Lipscomb Integer-spin EPR studies of the fully reduced methane monooxygenase hydroxylase component J. Am. Chem. Soc. 112 1990 5861 5865
47. B.G. Fox, W.A. Froland, J.E. Dege, and J.D. Lipscomb Methane monooxygenase from Methylosinus trichosporium OB3b: purification and properties of a three-component system with high specific activity from a Type II methanotroph J. Biol. Chem. 264 1989 10023 10033
48. K.E. Liu, A.M. Valentine, D. Qui, D.E. Edmondson, E.H. Appelman, T.G. Spiro, and S.J. Lippard Characterization of a diiron(III) peroxo intermediate in the reaction cycle of methane monooxygenase hydroxylase from Methylococcus capsulatus (Bath) J. Am. Chem. Soc. 119 1997 11134 11136
49. IV cluster J. Am. Chem. Soc. 115 1993 6450 6451
50. M.-H. Baik, M. Newcomb, R.A. Friesner, and S.J. Lippard Mechanistic studies on the hydroxylation of methane by methane monooxygenase Chem. Rev. 103 2003 2385 2419
51. E.J. McKenna, and M.J. Coon Enzymatic ω-oxidation IV. Purification and properties of the ω-hydroxylase of Pseudomonas oleovorans J. Biol. Chem. 245 1970 3882 3889
52. J. Shanklin, C. Achim, H. Schmidt, B.G. Fox, and E. Münck Mössbauer studies of alkane ω-hydroxylase: evidence for a diiron cluster in an integral membrane enzyme Proc. Natl. Acad. Sci. USA 94 1997 2981 2986
53. S. Harayama, M. Rekik, M. Wubbolts, K. Rose, R.A. Leppik, and K.N. Timmis Characterization of five genes in the upper-pathway operon of TOL plasmid pWW0 from Pseudomonas putida and identification of the gene products J. Bacteriol. 171 1989 5048 5055
54. R.N. Austin, H.-K. Chang, G.J. Zylstra, and J.T. Groves The non-heme diiron alkane monooxygenase of Pseudomonas oleovorans (AlkB) hydroxylates via a substrate radical intermediate J. Am. Chem. Soc. 122 2000 11747 11748
55. R.N. Austin, J. Buzzi, E. Kim, G.J. Zylstra, and J.T. Groves Xylene monooxygenase: a membrane-spanning non-heme diiron enzyme that hydroxylates hydrocarbons via a substrate radical intermediate J. Biol. Inorg. Chem. 8 2003 733 740
56. J.T. Groves, G.A. McClusky, R.E. White, and M.J. Coon Aliphatic hydroxylation by highly purified liver microsomal cytochrome P-450: evidence for a carbon radical intermediate Biochem. Biophys. Res. Commun. 81 1978 154 160
57. J.T. Groves, and D.V. Subramanian Hydroxylation by cytochrome P-450 and metalloporphyrin models. Evidence for allylic rearrangement J. Am. Chem. Soc. 106 1984 2177 2181
58. 9 desaturase complex Biochemistry 39 2000 10507 10513