Reactive intermediates in cytochrome P450 catalysis

Journal of Biological Chemistry

Volumn 288, Issue 24, 2013, Pages 17074-17081

  Krest, Courtney M ^a,b   Onderko, Elizabeth L ^a   Yosca, Timothy H ^a   Calixto, Julio C ^a   Karp, Richard F ^a   Livada, Jovan ^a   Rittle, Jonathan ^a,c   Green, Michael T ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b STANFORD UNIVERSITY   (United States)

^c California Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATALYTIC CYCLES; CYTOCHROME P450; ENZYME PURIFICATION; KINETIC CHARACTERIZATION; LASER FLASH PHOTOLYSIS; PEROXYNITRITES; PRODUCTION OF; REACTIVE INTERMEDIATE;

BIOCHEMISTRY; BIOLOGY;

REACTION INTERMEDIATES;

CYTOCHROME P450; CYTOCHROME P450 I; CYTOCHROME P450 II; UNCLASSIFIED DRUG;

BINDING AFFINITY; CHEMICAL BOND; ENZYME BINDING; ENZYME MECHANISM; ENZYME METABOLISM; ENZYME PURIFICATION; ENZYME SUBSTRATE; ENZYME SYNTHESIS; HYDROXYLATION; PHOTOLYSIS; PRIORITY JOURNAL; SHORT SURVEY;

CYTOCHROME P450; ENZYME CATALYSIS; ENZYME PURIFICATION; HEME; P450 COMPOUND I; SPECTROSCOPY;

ARCHAEAL PROTEINS; BIOCATALYSIS; CYTOCHROME P-450 ENZYME SYSTEM; HUMANS; HYDROXYLATION; IRON; OXIDATION-REDUCTION; THERMODYNAMICS;

EID: 84879049215     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.R113.473108     Document Type: Short Survey

References (54)

1. Rittle, J., and Green, M. T. (2010) Cytochrome P450 compound I: capture, characterization, and C-H bond activation kinetics. Science 330, 933-937
2. Moss, T. H., Ehrenberg, A., and Bearden, A. J. (1969) Mössbauer spectroscopic evidence for electronic configuration of iron in horseradish peroxidase and its peroxide derivatives. Biochemistry 8, 4159-4162
3. Schonbaum, G. R., and Lo, S. (1972) Interaction of peroxidases with aromatic peracids and alkyl peroxides. Product analysis. J. Biol. Chem. 247, 3353-3360
4. Sheng, X., Zhang, H., Im, S. C., Horner, J. H., Waskell, L., Hollenberg, P. F., and Newcomb, M. (2009) Kinetics of oxidation of benzphetamine by compounds I of cytochrome P450 2B4 and its mutants. J. Am. Chem. Soc. 131, 2971-2976
5. Jung, C. (2011) The mystery of cytochrome P450 compound I: a minireview dedicated to Klaus Ruckpaul. Biochim. Biophys. Acta 1814, 46-57
6. Wang, Q., Sheng, X., Horner, J. H., and Newcomb, M. (2009) Quantitative production of compound I from a cytochrome P450 enzyme at low temperatures. Kinetics, activation parameters, and kinetic isotope effects for oxidation of benzyl alcohol. J. Am. Chem. Soc. 131, 10629-10636
7. Groves, J. T., and McClusky, G. A. (1976) Aliphatic hydroxylation via oxygen rebound. Oxygen transfer catalyzed by iron. J. Am. Chem. Soc. 98, 859-861
8. Groves, J. T., McClusky, G. A., White, R. E., and Coon, M. J. (1978) Aliphatic hydroxylation by highly purified liver microsomal cytochrome-P-450- evidence for a carbon radical intermediate. Biochem. Biophys. Res. Commun. 81, 154-160 (Pubitemid 8307814)
9. Green, M. T. (2009) C-H bond activation in heme proteins: the role of thiolate ligation in cytochrome P450. Curr. Opin. Chem. Biol. 13, 84-88
10. Green, M. T., Dawson, J. H., and Gray, H. B. (2004) Oxoiron(IV) in chloroperoxidase compound II is basic: implications for P450 chemistry. Science 304, 1653-1656 (Pubitemid 38765853)
11. Chen, X., Su, Z., Horner, J. H., and Newcomb, M. (2011) Oxidation of 10-undecenoic acid by cytochrome P450BM-3 and its compound I transient. Org. Biomol. Chem. 9, 7427-7433
12. Newcomb, M., Zhang, R., Chandrasena, R. E. P., Halgrimson, J. A., Horner, J. H., Makris, T. M., and Sligar, S. G. (2006) Cytochrome P450 compound I. J. Am. Chem. Soc. 128, 4580-4581
13. Sheng, X., Horner, J. H., and Newcomb, M. (2008) Spectra and kinetic studies of the compound I derivative of cytochrome P450 119. J. Am. Chem. Soc. 130, 13310-13320
14. Sheng, X., Zhang, H., Hollenberg, P. F., and Newcomb, M. (2009) Kinetic isotope effects in hydroxylation reactions effected by cytochrome P450 compounds I implicate multiple electrophilic oxidants for P450-catalyzed oxidations. Biochemistry 48, 1620-1627
15. Yuan, X., Wang, Q., Horner, J. H., Sheng, X., and Newcomb, M. (2009) Kinetics and activation parameters for oxidations of styrene by compounds I from the cytochrome P450BM-3 (CYP102A1) heme domain and from CYP119. Biochemistry 48, 9140-9146
16. Denisov, I. G., Makris, T. M., Sligar, S. G., and Schlichting, I. (2005) Structure and chemistry of cytochrome P450. Chem. Rev. 105, 2253-2277 (Pubitemid 40951784)
17. Ortiz de Montellano, P. R. (ed) (2005) Cytochrome P450 Structure, Mechanism, and Biochemistry, Kluwer Academic/Plenum Publishers, New York.
18. BM3) variant. Dalton Trans. 40, 10383-10396
19. Egawa, T., Shimada, H., and Ishimura, Y. (1994) Evidence for compound I formation in the reaction of cytochrome-P450cam with m-chloroperbenzoic acid. Biochem. Biophys. Res. Commun. 201, 1464-1469
20. Kellner, D. G., Hung, S. C., Weiss, K. E., and Sligar, S. G. (2002) Kinetic characterization of compound I formation in the thermostable cytochrome P450 CYP119. J. Biol. Chem. 277, 9641-9644 (Pubitemid 34968061)
21. Spolitak, T., Dawson, J. H., and Ballou, D. P. (2005) Reaction of ferric cytochrome P450cam with peracids. Kinetic characterization of intermediates on the reaction pathway. J. Biol. Chem. 280, 20300-20309 (Pubitemid 40776727)
22. Davydov, R., Hoffman, B. M., Valentine, A. M., Lippard, S. J., Sligar, S. G., and Ikeda-Saito, M. (1999) EPR and ENDOR studies on cryoreduced metalloproteins. J. Inorg. Biochem. 74, 110
23. Davydov, R., Macdonald, I. D. G., Makris, T. M., Sligar, S. G., and Hoffman, B. M. (1999) 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, 10654-10655
24. Davydov, R., Perera, R., Jin, S., Yang, T. C., Bryson, T. A., Sono, M., Dawson, J. H., and Hoffman, B. M. (2005) Substrate modulation of the properties and reactivity of the oxy-ferrous and hydroperoxo-ferric intermediates of cytochrome P450cam as shown by cryoreduction-EPR/ENDOR spectroscopy. J. Am. Chem. Soc. 127, 1403-1413 (Pubitemid 40204515)
25. 2 activation intermediates by cryoreduction and electron paramagnetic resonance. Biochemistry 47, 9661-9666
26. Denisov, I. G., Makris, T. M., and Sligar, S. G. (2001) Cryotrapped reaction intermediates of cytochrome P450 studied by radiolytic reduction with phosphorus-32. J. Biol. Chem. 276, 11648-11652
27. Schlichting, I., Berendzen, J., Chu, K., Stock, A. M., Maves, S. A., Benson, D. E., Sweet, R. M., Ringe, D., Petsko, G. A., and Sligar, S. G. (2000) The catalytic pathway of cytochrome P450cam at atomic resolution. Science 287, 1615-1622 (Pubitemid 30127756)
28. Ener, M. E., Lee, Y. T., Winkler, J. R., Gray, H. B., and Cheruzel, L. (2010) Photooxidation of cytochrome P450-BM3. Proc. Natl. Acad. Sci. U.S.A. 107, 18783-18786
29. Wilker, J. J., Dmochowski, I. J., Dawson, J. H., Winkler, J. R., and Gray, H. B. (1999) Substrates for rapid delivery of electrons and holes to buried active sites in proteins. Angew Chem. Int. Ed. 38, 89-92
30. Eble, K. S., and Dawson, J. H. (1984) Novel reactivity of cytochrome P-450-CAM. Methyl hydroxylation of 5,5-difluorocamphor. J. Biol. Chem. 259, 14389-14393
31. Kadkhodayan, S., Coulter, E. D., Maryniak, D. M., Bryson, T. A., and Dawson, J. H. (1995) Uncoupling oxygen transfer and electron transfer in the oxygenation of camphor analogs by cytochrome P450-CAM. Direct observation of an intermolecular isotope effect for substrate C-H activation. J. Biol. Chem. 270, 28042-28048
32. Cherepanov, A. V., and de Vries, S. (2004) Microsecond freeze-hyperquenching: development of a new ultrafast micro-mixing and sampling technology and application to enzyme catalysis. Biochim. Biophys. Acta 1656, 1-31 (Pubitemid 38609194)
33. Rittle, J., Younker, J. M., and Green, M. T. (2010) Cytochrome P450: the active oxidant and its spectrum. Inorg. Chem. 48, 3610-3617
34. McLean, M. A., Maves, S. A., Weiss, K. E., Krepich, S., and Sligar, S. G. (1998) Characterization of a cytochrome P450 from the acidothermophilic archaea Sulfolobus solfataricus. Biochem. Biophys. Res. Commun. 252, 166-172 (Pubitemid 28534645)
35. Rabe, K. S., Kiko, K., and Niemeyer, C. M. (2008) Characterization of the peroxidase activity of CYP119, a thermostable P450 from Sulfolobus acidocaldarius. ChemBioChem. 9, 420-425
36. Wright, R. L., Harris, K., Solow, B., White, R. H., and Kennelly, P. J. (1996) Cloning of a potential cytochrome P450 from the archaeon Sulfolobus solfataricus. FEBS Lett. 384, 235-239 (Pubitemid 26125228)
37. Oku, Y., Ohtaki, A., Kamitori, S., Nakamura, N., Yohda, M., Ohno, H., and Kawarabayasi, Y. (2004) Structure and direct electrochemistry of cytochrome P450 from the thermoacidophilic crenarchaeon, Sulfolobus tokodaii strain 7. J. Inorg. Biochem. 98, 1194-1199 (Pubitemid 38833597)
38. Lee, D. S., Yamada, A., Sugimoto, H., Matsunaga, I., Ogura, H., Ichihara, K., Adachi, S., Park, S. Y., and Shiro, Y. (2003) Substrate recognition and molecular mechanism of fatty acid hydroxylation by cytochrome P450 from Bacillus subtilis. Crystallographic, spectroscopic, and mutational studies. J. Biol. Chem. 278, 9761-9767 (Pubitemid 36800475)
39. SPα with its bound fatty acid substrate insight into the regioselective hydroxylation of fatty acids at the alpha position. J. Biol. Chem. 286, 29941-29950
40. Schoch, G. A., Yano, J. K., Wester, M. R., Griffin, K. J., Stout, C. D., and Johnson, E. F. (2004) Structure of human microsomal cytochrome P4502C8. Evidence for a peripheral fatty acid binding site. J. Biol. Chem. 279, 9497-9503 (Pubitemid 38296017)
41. Mayer, J. M. (1998) Hydrogen atom abstraction by metal-oxo complexes: understanding the analogy with organic radical reactions. Acc. Chem. Res. 31, 441-450
42. Mayer, J. M. (2004) Proton-coupled electron transfer: a reaction chemist's view. Annu. Rev. Phys. Chem. 55, 363-390
43. Stone, K. L., Behan, R. K., and Green, M. T. (2006) Resonance Raman spectroscopy of chloroperoxidase compound II provides direct evidence for the existence of an iron(IV)-hydroxide. Proc. Natl. Acad. Sci. U.S.A. 103, 12307-12310 (Pubitemid 44267255)
44. Stone, K. L., Hoffart, L. M., Behan, R. K., Krebs, C., and Green, M. T. (2006) Evidence for two ferryl species in chloroperoxidase compound II. J. Am. Chem. Soc. 128, 6147-6153
45. Behan, R. K., Hoffart, L. M., Stone, K. L., Krebs, C., and Green, M. T. (2006) Evidence for basic ferryls in cytochromes P450. J. Am. Chem. Soc. 128, 11471-11474 (Pubitemid 44338839)
46. Green, M. T. (2006) Application of Badger's rule to heme and non-heme iron-oxygen bonds: an examination of ferryl protonation states. J. Am. Chem. Soc. 128, 1902-1906
47. Behan, R. K., and Green, M. T. (2006) On the status of ferryl protonation. J. Inorg. Biochem. 100, 448-459
48. BM-3 by peroxynitrite-stopped-flow measurements prove ferryl intermediates. Eur. J. Biochem. 267, 6729-6739
49. Lambeir, A. M., Dunford, H. B., and Pickard, M. A. (1987) Kinetics of the oxidation of ascorbic-acid, ferrocyanide and para-phenolsulfonic acid by chloroperoxidase compound-I and compound-II. Eur. J. Biochem. 163, 123-127
50. Behan, R. K., Hoffart, L. M., Stone, K. L., Krebs, C., and Green, M. T. (2007) Reaction of cytochrome P450BM3 and peroxynitrite yields nitrosyl complex. J. Am. Chem. Soc. 129, 5855-5859 (Pubitemid 46748489)
51. Ortiz de Montellano, P. R. (2010) Hydrocarbon hydroxylation by cytochrome P450 enzymes. Chem. Rev. 110, 932-948
52. Palcic, M. M., Rutter, R., Araiso, T., Hager, L. P., and Dunford, H. B. (1980) Spectrum of chloroperoxidase compound-I. Biochem. Biophys. Res. Commun. 94, 1123-1127
53. Su, Z., Horner, J. H., and Newcomb, M. (2012) Cytochrome P450 119 compounds I formed by chemical oxidation and photooxidation are the same species. Chemistry 10.1002/chem.201202254
54. Dunford, H. B., and Stillman, J. S. (1976) On the function and mechanism of action of peroxidases. Coord. Chem. Rev. 19, 187-251