Highly reactive electrophilic oxidants in cytochrome P450 catalysis

Biochemical and Biophysical Research Communications

Volumn 338, Issue 1, 2005, Pages 394-403

  Newcomb, Martin ^a   Chandrasena, R Esala P ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Compound I; Cytochrome P450 enzymes; Iron oxo; Oxidation

Indexed keywords

CATION; CYTOCHROME P450; HYDROGEN PEROXIDE; IRON DERIVATIVE; OXIDIZING AGENT; PORPHYRIN DERIVATIVE;

CATALYSIS; CATALYST; CHEMICAL BOND; CHEMICAL REACTION KINETICS; ENERGY; ENZYME ACTIVITY; ENZYME MECHANISM; HYDROXYLATION; ISOMERISM; OXIDATION; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; REVIEW;

ANIMALS; CATALYSIS; CYTOCHROME P-450 ENZYME SYSTEM; HUMANS; OXIDANTS; SUBSTRATE SPECIFICITY;

EID: 27544462035     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2005.08.208     Document Type: Review

References (74)

1. T. Omura, R. Sato, D.Y. Cooper, O. Rosenthal, and R.W. Estabrook Function of cytochrome P450 of microsomes Fed. Proc. 24 1965 1181 1189
2. A.Y.H. Lu, and M.J. Coon Role of hemoprotein P450 in fatty acid ω-hydroxylation in a soluble enzyme system from liver microsomes J. Biol. Chem. 243 1968 1331 1332
3. M. Katagiri, B.N. Ganguli, and I.C. Gunsalus A soluble cytochrome P450 functional in methylene hydroxylation J. Biol. Chem. 243 1968 3543 3546
4. R.A. Sheldon Metalloprophyrins in Catalytic Oxidations 1994 Marcel Dekker New York
5. B. Meunier Metal-oxo and Metal-Peroxo Species in Catalytic Oxidations 2000 Springer-Verlag Berlin
6. B. Meunier Metalloporphyrins as versatile catalysts for oxidation reactions and oxidative DNA cleavage Chem. Rev. 92 1992 1411 1456
7. A.D.N. Vaz Multiple oxidants in cytochrome P450 catalyzed reactions: implications for drug metabolism Curr. Drug Metab. 2 2001 1 16
8. M. Newcomb, P.F. Hollenberg, and M.J. Coon Multiple mechanisms and multiple oxidants in P450-catalyzed hydroxylations Arch. Biochem. Biophys. 409 2003 72 79
9. M.J. Coon Multiple oxidants and multiple mechanisms in cytochrome P450 catalysis Biochem. Biophys. Res. Commun. 312 2003 163 168
10. S.X. Jin, T.A. Bryson, and J.H. Dawson Hydroperoxoferric heme intermediate as a second electrophilic oxidant in cytochrome P450-catalyzed reactions J. Biol. Inorg. Chem. 9 2004 644 653
11. P. Hlavica Models and mechanisms of OO bond activation by cytochrome P450. A critical assessment of the potential role of multiple active intermediates in oxidative catalysis Eur. J. Biochem. 271 2004 4335 4360
12. J.T. Groves Models and mechanisms of cytochrome P450 action P.R. Ortiz de Montellano Cytochrome P450 structure mechanism and biochemistry third ed. 2005 Kluwer Academic/Plenum New York 1 43
13. T.L. Poulos Intermediates in P450 catalysis Philos. Trans. R. Soc. Lond. A Biol. Sci. 363 2005 793 806
14. P.R. Ortiz de Montellano Cytochrome P450 Structure, Mechanism and Biochemistry third ed. 2005 Kluwer Academic/Plenum New York
15. M. Akhtar, M.R. Calder, D.L. Corina, and J.N. Wright Mechanistic studies on C-19 demethylation in oestrogen biosynthesis Biochem. J. 201 1982 569 580
16. A.D.N. Vaz, S.J. Pernecky, G.M. Raner, and M.J. Coon Peroxo-iron and oxenoid-iron species as alternative oxygenating agents in cytochrome P450-catalyzed reactions: switching by threonine-302 to alanine mutagenesis of cytochrome P450 2B4 Proc. Natl. Acad. Sci. USA 93 1996 4644 4648
17. R. Davydov, I.D.G. Macdonald, T.M. Makris, S.G. Sligar, and B.M. Hoffman EPR and ENDOR of catalytic intermediates in cryoreduced native and mutant oxy-cytochromes P450cam: mutation-induced changes in the proton delivery system J. Am. Chem. Soc. 121 1999 10654 10655
18. R. Davydov, T.M. Makris, V. Kofman, D.E. Werst, S.G. Sligar, and B.M. Hoffman Hydroxylation of camphor by reduced oxy-cytochrome P450cam: mechanistic implications of EPR and ENDOR studies of catalytic intermediates in native and mutant enzymes J. Am. Chem. Soc. 123 2001 1403 1415
19. D.L. Harris, and G.H. Loew Theoretical investigation of the proton assisted pathway to formation of cytochrome P450 Compound I J. Am. Chem. Soc. 120 1998 8941 8948
20. G.D. Nordblom, R.E. White, and M.J. Coon Studies on hydroperoxide- dependent substrate hydroxylation by purified liver microsomal cytochrome P450 Arch. Biochem. Biophys. 175 1976 524 533
21. J.H. Dawson Probing structure-function relations in heme-containing oxygenases and peroxidases Science 240 1988 433 439
22. A.N.P. Hiner, E.L. Raven, R.N.F. Thorneley, F. Garcia-Canovas, and J.N. Rodriguez-Lopez Mechanisms of Compound I formation in heme peroxidases J. Inorg. Biochem. 91 2002 27 34
23. J.T. Groves, R.C. Haushalter, M. Nakamura, T.E. Nemo, and B.J. Evans High-valent iron-porphyrin complexes related to peroxidase and cytochrome P450 J. Am. Chem. Soc. 103 1981 2884 2886
24. I.G. Denisov, T.M. Makris, and S.G. Sligar Cryotrapped reaction intermediates of cytochrome P450 studied by radiolytic reduction with phosphorus-32 J. Biol. Chem. 276 2001 11648 11652
25. T. Egawa, H. Shimada, and Y. Ishimura Evidence for Compound I formation in the reaction of cytochrome P450cam with m-chloroperbenzoic acid Biochem. Biophys. Res. Commun. 201 1994 1464 1469
26. T. Spolitak, J.H. Dawson, and D.P. Ballou Reaction of ferric cytochrome P450cam with peracids. Kinetic characterization of intermediates on the reaction pathway J. Biol. Chem. 280 2005 20300 20309
27. D.G. Kellner, S.C. Hung, K.E. Weiss, and S.G. Sligar Kinetic characterization of Compound I formation in the thermostable cytochrome P450 CYP119 J. Biol. Chem. 277 2002 9641 9644
28. V. Schünemann, C. Jung, A.X. Trautwein, D. Mandon, and R. Weiss Intermediates in the reaction of substrate-free cytochrome P450(cam) with peroxy acetic acid FEBS Lett. 479 2000 149 154
29. V. Schünemann, A.X. Trautwein, C. Jung, and J. Terner Mossbauer and EPR study of reaction intermediates of cytochrome P450 Hyperfine Interact. 141 2002 279 284
30. V. Schünemann, F. Lendzian, C. Jung, J. Contzen, A.L. Barra, S.G. Sligar, and A.X. Trautwein Tyrosine radical formation in the reaction of wild type and mutant cytochrome P450cam with peroxy acids-a multifrequency EPR study of intermediates on the millisecond time scale J. Biol. Chem. 279 2004 10919 10930
31. S.I. Ozaki, M.P. Roach, T. Matsui, and Y. Watanabe Investigations of the roles of the distal heme environment and the proximal heme iron ligand in peroxide activation by heme enzymes via molecular engineering of myoglobin Acc. Chem. Res. 34 2001 818 825
32. T. Egawa, H. Shimada, and Y. Ishimura Formation of Compound I in the reaction of native myoglobins with hydrogen peroxide J. Biol. Chem. 275 2000 34858 34866
33. R. Zhang, R.E.P. Chandrasena, E. Martinez II, J.H. Horner, and M. Newcomb Formation of Compound I by photo-oxidation of Compound II Org. Lett. 7 2005 1193 1195
34. R. Zhang, and M. Newcomb Laser flash photolysis formation and direct kinetic studies of manganese(V)-oxo porphyrin intermediates J. Am. Chem. Soc. 125 2003 12418 12419
35. IV-oxo species J. Am. Chem. Soc. 127 2005 6573 6582
36. R. Zhang, D.N. Harischandra, and M. Newcomb Laser flash photolysis generation and kinetic studies of corrole-manganese(V)-oxo intermediates Chem. Eur. J. 11 2005 5713 5720
37. D.N. Harischandra, R. Zhang, and M. Newcomb Photochemical generation of a highly reactive iron-oxo intermediate. A true iron(V)-oxo species? J. Am. Chem. Soc. 127 2005
38. 3+ complex J. Chem. Soc. Chem. Commun. 1995 2297 2298
39. T.L. Poulos, B.C. Finzel, and A.J. Howard High-resolution crystal structure of cytochrome P450cam J. Mol. Biol. 195 1987 687 700
40. K.G. Ravichandran, S.S. Boddupalli, C.A. Hasemann, J.A. Peterson, and J. Deisenhofer Crystal structure of hemoprotein domain of P450 BM3, a prototype for microsomal P450s Science 261 1993 731 736
41. C.A. Hasemann, K.G. Ravichandran, J.A. Peterson, and J. Deisenhofer Crystal structure and refinement of cytochrome P450(Terp) at 2.3 Angstrom resolution J. Mol. Biol. 236 1994 1169 1185
42. J.R. Cupp-Vickery, and T.L. Poulos Structure of cytochrome P450eryf involved in erythromycin biosynthesis Nat. Struct. Biol. 2 1995 144 153
43. D.R. Nelson, and H.W. Strobel Secondary structure prediction of 52 membrane-bound cytochromes P450 shows a strong structural similarity to P450cam Biochemistry 28 1989 656 660
44. S.A. Martinis, W.M. Atkins, P.S. Stayton, and S.G. Sligar A conserved residue of cytochrome P450 is involved in heme oxygen stability and activation J. Am. Chem. Soc. 111 1989 9252 9253
45. M. Imai, H. Shimada, Y. Watanabe, Y. Matsushima-Hibiya, R. Makino, H. Koga, T. Horiuchi, and Y. Ishimura Uncoupling of the cytochrome P450cam monooxygenase reaction by a single mutation, threonine-252 to alanine or valine-a possible role of the hydroxy amino acid in oxygen activation Proc. Natl. Acad. Sci. USA 86 1989 7823 7827
46. H. Yeom, S.G. Sligar, H. Li, T.L. Poulos, and A.J. Fulco The role of Thr268 in oxygen activation of cytochrome P450 BM3 Biochemistry 34 1995 14733 14740
47. A.D.N. Vaz, D.F. McGinnity, and M.J. Coon Epoxidation of olefins by cytochrome P450: evidence from site-specific mutagenesis for hydroperoxo-iron as an electrophilic oxidant Proc. Natl. Acad. Sci. USA 95 1998 3555 3560
48. P.H. Toy, M. Newcomb, M.J. Coon, and A.D.N. Vaz Two distinct electrophilic oxidants effect hydroxylation in cytochrome P450-catalyzed reactions J. Am. Chem. Soc. 120 1998 9718 9719
49. T.A. Halgren, J.D. Roberts, J.H. Horner, F.N. Martinez, C. Tronche, and M. Newcomb Kinetics and equilibrium constants for reactions of α-phenyl-substituted cyclopropylcarbinyl radicals J. Am. Chem. Soc. 122 2000 2988 2994
50. K.P. Vatsis, and M.J. Coon ipso-substitution by cytochrome P450 with conversion of p-hydroxybenzene derivatives to hydroquinone: evidence for hydroperoxo-iron as the active oxygen species Arch. Biochem. Biophys. 397 2002 119 129
51. S. Jin, T.M. Makris, T.A. Bryson, S.G. Sligar, and J.H. Dawson Epoxidation of olefins by hydroperoxo-ferric cytochrome P450 J. Am. Chem. Soc. 125 2003 3406 3407
52. T.J. Volz, D.A. Rock, and J.P. Jones Evidence for two different active oxygen species in cytochrome P450 BM3 mediated sulfoxidation and N-dealkylation reactions J. Am. Chem. Soc. 124 2002 9724 9725
53. J.K. Atkinson, P.F. Hollenberg, K.U. Ingold, C.C. Johnson, M.-H. Le Tadic, M. Newcomb, and D.A. Putt Cytochrome P450-catalyzed hydroxylation of hydrocarbons: kinetic deuterium isotope effects for the hydroxylation of an ultrafast radical clock Biochemistry 33 1994 10630 10637
54. M. Newcomb, D. Aebisher, R. Shen, R.E.P. Chandrasena, P.F. Hollenberg, and M.J. Coon Kinetic isotope effects implicate two electrophilic oxidants in cytochrome P450-catalyzed hydroxylations J. Am. Chem. Soc. 125 2003 6064 6065
55. R.E.P. Chandrasena, K.P. Vatsis, M.J. Coon, P.F. Hollenberg, and M. Newcomb Hydroxylation by the hydroperoxy-iron species in cytochrome P450 enzymes J. Am. Chem. Soc. 126 2004 115 126
56. J.M. Hutzler, F.J. Powers, M.A. Wynalda, and L.C. Wienkers Effect of carbonate anion on cytochrome P450 2D6-mediated metabolism in vitro: the potential role of multiple oxygenating species Arch. Biochem. Biophys. 417 2003 165 175
57. M. Newcomb, M.H. Le Tadic-Biadatti, D.L. Chestney, E.S. Roberts, and P.F. Hollenberg A nonsynchronous concerted mechanism for cytochrome P-450 catalyzed hydroxylation J. Am. Chem. Soc. 117 1995 12085 12091
58. S.Y. Choi, P.E. Eaton, P.F. Hollenberg, K.E. Liu, S.J. Lippard, M. Newcomb, D.A. Putt, S.P. Upadhyaya, and Y. Xiong Regiochemical variations in reactions of methylcubane with tert-butoxyl radical, cytochrome P-450 enzymes, and a methane monooxygenase system J. Am. Chem. Soc. 118 1996 6547 6555
59. P.H. Toy, M. Newcomb, and P.F. Hollenberg Hypersensitive mechanistic probe studies of cytochrome P450-catalyzed hydroxylation reactions. Implications for the cationic pathway J. Am. Chem. Soc. 120 1998 7719 7729
60. 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
61. A. Dey, and A. Ghosh True iron(V) and iron(VI) porphyrins: a first theoretical exploration J. Am. Chem. Soc. 124 2002 3206 3207
62. G.A. Olah, D.G. Parker, and N. Yoneda Oxyfunctionalization of hydrocarbons. 9. Superacid-catalyzed oxygenation of alkanes Angew. Chem. Int. Ed. Engl. 17 1978 909 931
63. F. Ogliaro, S.P. de Visser, S. Cohen, P.K. Sharma, and S. Shaik Searching for the second oxidant in the catalytic cycle of cytochrome P450: a theoretical investigation of the iron(III)-hydroperoxo species and its epoxidation pathways J. Am. Chem. Soc. 124 2002 2806 2817
64. R.D. Bach, and M.D. Su The transition state for the hydroxylation of saturated hydrocarbons with hydroperoxonium ion J. Am. Chem. Soc. 116 1994 10103 10109
65. + with halogenated alkanes Chem. Eur. J. 11 2005 152 159
66. P.R. Ortiz de Montellano Heme oxygenase mechanism: evidence for an electrophilic, ferric peroxide species Acc. Chem. Res. 31 1998 543 549
67. S. Shaik, M. Filatov, D. Schroder, and H. Schwarz Electronic structure makes a difference: cytochrome P450 mediated hydroxylations of hydrocarbons as a two-state reactivity paradigm Chem. Eur. J. 4 1998 193 199
68. S. Shaik, D. Kumar, S.P. de Visser, A. Altun, and W. Thiel Theoretical perspective on the structure and mechanism of cytochrome P450 enzymes Chem. Rev. 105 2005 2279 2328
69. T. Kamachi, and K. Yoshizawa A theoretical study on the mechanism of camphor hydroxylation by Compound I of cytochrome P450 J. Am. Chem. Soc. 125 2003 4652 4661
70. V. Guallar, M.H. Baik, S.J. Lippard, and R.A. Friesner Peripheral heme substituents control the hydrogen-atom abstraction chemistry in cytochromes P450 Proc. Natl. Acad. Sci. USA 100 2003 6998 7002
71. V. Guallar, and R.A. Friesner Cytochrome P450CAM enzymatic catalysis cycle: a quantum mechanics/molecular mechanics study J. Am. Chem. Soc. 126 2004 8501 8508
72. R.D. Bach, A.L. Owensby, C. Gonzalez, H.B. Schlegel, and J.J.W. McDouall Nature of the transition structure for oxygen atom transfer from a hydroperoxide. Theoretical comparison between water oxide and ammonia oxide J. Am. Chem. Soc. 113 1991 6001 6011
73. M. Hata, T. Hoshino, and M. Tsuda An ultimate species in the substrate oxidation process by cytochrome P450 Chem. Commun. 2000 2037 2038
74. M.J. Coon, A.D.N. Vaz, D.F. McGinnity, and H.-M. Peng Multiple activated oxygen species in P450 catalysis: contributions to specificity in drug metabolism Drug Metab. Dispos. 26 1998 1190 1193