Oxygen activation by cytochrome P450 monooxygenase

Photosynthesis Research

Volumn 98, Issue 1-3, 2008, Pages 657-666

  Hamdane, Djemel ^a   Zhang, Haoming ^a   Hollenberg, Paul ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Hydroxylation; Oxygen intermediate; Oxygen splitting; P450; P450 reductase

Indexed keywords

CYTOCHROME P450; OXYGEN; PROTON; WATER;

CLASSIFICATION; ELECTRON TRANSPORT; METABOLISM; OXIDATION REDUCTION REACTION; REVIEW;

CYTOCHROME P-450 ENZYME SYSTEM; ELECTRON TRANSPORT; OXIDATION-REDUCTION; OXYGEN; PROTONS; WATER;

EID: 57849111310     PISSN: 01668595     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11120-008-9322-1     Document Type: Review

References (65)

1. M Akhtar MR Calder DL Corina JN Wright 1982 Mechanistic studies on C-19 demethylation in oestrogen biosynthesis Biochem J 201 569 580
2. CB Brewer JA Peterson 1988 Single turnover kinetics of the reaction between oxycytochrome P-450cam and reduced putidaredoxin J Biol Chem 263 791 798
3. SN Daff SK Chapman KL Turner RA Holt S Govindaraj TL Poulos 1997 Redox control of the catalytic cycle of flavocytochrome P-450 BM3 Biochemistry 36 13816 13823 10.1021/bi971085s
4. R Davydov ID Macdonald TM Makris S Sligar BM Hoffman 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 10.1021/ja9918829
5. R Davydov TM Makris V Kofman DE Werst SG Sligar BM Hoffman 2001 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 1403 1415 10.1021/ja003583l
6. IG Denisov TM Makris SG Sligar 2001 Cryotrapped reaction intermediates of cytochrome p450 studied by radiolytic reduction with phosphorus-32 J Biol Chem 276 11648 11652 10.1074/jbc.M010219200
7. IG Denisov TM Makris SG Sligar I Schlichting 2005 Structure and chemistry of cytochrome P450 Chem Rev 105 2253 2277 10.1021/cr0307143
8. IG Denisov YV Grinkova BJ Baas SG Sligar 2006 The ferrous-dioxygen intermediate in human cytochrome P450 3A4. Substrate dependence of formation and decay kinetics J Biol Chem 281 23313 23318 10.1074/jbc.M605511200
9. C Di Primo E Deprez GH Hoa P Douzou 1995 Antagonistic effects of hydrostatic pressure and osmotic pressure on cytochrome P-450cam spin transition Biophys J 68 2056 2061
10. D Dolphin A Forman DC Borg J Fajer RH Felton 1971 Compounds I of catalase and horse radish peroxidase: pi-cation radicals Proc Natl Acad Sci USA 68 614 618 10.1073/pnas.68.3.614
11. T Egawa H Shimada Y Ishimura 1994 Evidence for compound I formation in the reaction of cytochrome P450cam with m-chloroperbenzoic acid Biochem Biophys Res Commun 201 1464 1469 10.1006/bbrc.1994.1868
12. Y Furukawa I Morishima 2001 The role of water molecules in the association of cytochrome P450cam with putidaredoxin. An osmotic pressure study J Biol Chem 276 12983 12990 10.1074/jbc.M010217200
13. N Gerber S Sligar 1992 Catalytic mechanism of cytochrome-P450: evidence for a distal charge relay J Am Chem Soc 114 8742 8743 10.1021/ja00048a081
14. JT Groves GA McClusky 1976 Aliphatic hydroxylation via oxygen rebound. Oxygen transfer catalyzed by iron. J Am Chem Soc 98 859 861 10.1021/ja00419a049
15. FP Guengerich 2001 Uncommon P450-catalyzed reactions Curr Drug Metab 2 93 115 10.2174/1389200013338694
16. FP Guengerich JA Krauser WW Johnson 2004 Rate-limiting steps in oxidations catalyzed by rabbit cytochrome P450 1A2 Biochemistry 43 10775 10788 10.1021/bi0491393
17. DL Harris G Loew 1998 Theoretical investigation of the proton assisted pathway to formation of cytochrome P450 compound I J Am Chem Soc 120 8941 8948 10.1021/ja981059x
18. DL Harris G Loew L Waskell 1998 Structure and spectra of ferrous dioxygen and reduced ferrous dioxygen model cytochrome P450 J Am Chem Soc 120 4308 4318 10.1021/ja974110q
19. X He PR de Montellano 2004 Radical rebound mechanism in cytochrome P-450-catalyzed hydroxylation of the multifaceted radical clocks alpha- and beta-thujone J Biol Chem 279 39479 39484 10.1074/jbc.M406838200
20. MJ Hintz JA Peterson 1981 The kinetics of reduction of cytochrome P-450cam by reduced putidaredoxin J Biol Chem 256 6721 6728
21. FM Ho S Styring 2008 Access channels and methanol binding site to the CaMn4 cluster in Photosystem II based on solvent accessibility simulations, with implications for substrate water access Biochim Biophys Acta 1777 140 153 10.1016/j.bbabio.2007.08.009
22. PF Hollenberg UM Kent NN Bumpus 2008 Mechanism-based inactivation of human cytochromes p450s: experimental characterization, reactive intermediates, and clinical implications Chem Res Toxicol 21 189 205 10.1021/tx7002504
23. S Jin TM Makris TA Bryson SG Sligar JH Dawson 2003 Epoxidation of olefins by hydroperoxo-ferric cytochrome P450 J Am Chem Soc 125 3406 3407 10.1021/ja029272n
24. WH Koppenol 2007 Oxygen activation by cytochrome p450: a thermodynamic analysis J Am Chem Soc 129 9686 9690 10.1021/ja071546p
25. VY Kuznetsov TL Poulos IF Sevrioukova 2006 Putidaredoxin-to-cytochrome P450cam electron transfer: differences between the two reductive steps required for catalysis Biochemistry 45 11934 11944 10.1021/bi0611154
26. JD Lipscomb 1980 Electron paramagnetic resonance detectable states of cytochrome P-450cam Biochemistry 19 3590 3599 10.1021/bi00556a027
27. JD Lipscomb SG Sligar MJ Namtvedt IC Gunsalus 1976 Autooxidation and hydroxylation reactions of oxygenated cytochrome P-450cam J Biol Chem 251 1116 1124
28. PJ Mak IG Denisov D Victoria TM Makris T Deng SG Sligar 2007 Resonance Raman detection of the hydroperoxo intermediate in the cytochrome P450 enzymatic cycle J Am Chem Soc 129 6382 6383 10.1021/ja071426h
29. TM Makris K von Koenig I Schlichting SG Sligar 2007 Alteration of P450 distal pocket solvent leads to impaired proton delivery and changes in heme geometry Biochemistry 46 14129 14140 10.1021/bi7013695
30. SA Martinis WM Atkins PS Stayton S Sligar 1989 A conserved residue of cytochrome P-450 is involved in heme-oxygen stability and activation J Am Chem Soc 111 9252 9253 10.1021/ja00208a031
31. J Murray J Barber 2007 Structural characteristics of channels and pathways in photosysyem II including the identification of an oxygen channel J Struct Biol 159 228 237 10.1016/j.jsb.2007.01.016
32. S Nagano JR Cupp-Vickery TL Poulos 2005 Crystal structures of the ferrous dioxygen complex of wild-type cytochrome P450eryF and its mutants, A245S and A245T: investigation of the proton transfer system in P450eryF J Biol Chem 280 22102 22107 10.1074/jbc.M501732200
33. DR Nelson 2006 Cytochrome P450 nomenclature, 2004 Methods Mol Biol 320 1 10
34. M Newcomb R Zhang RE Chandrasena JA Halgrimson JH Horner TM Makris 2006 Cytochrome p450 compound I J Am Chem Soc 128 4580 4581 10.1021/ja060048y
35. Newcomb M, Halgrimson JA, Horner JH, Wasinger EC, Chen LX, Sligar SG (2008) X-ray absorption spectroscopic characterization of a cytochrome P450 compound II derivative. Proc Natl Acad Sci USA
36. F Ogliaro N Harris MS Cohen M Filatov SP de Visser S Shaik 2000 A model "rebound" mechanism of hydroxylation of hydroxylation by cytochrome p450: a theoretical investigation of the iron(III)-hydroperoxo species and its epoxidation pathways J Am Chem Soc 122 8977 8989 10.1021/ja991878x
37. F Ogliaro SP de Visser S Cohen PK Sharma S Shaik 2002 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 2806 2817 10.1021/ja0171963
38. Ortiz de Montellano P (2005) Cytochrome P450: structure, mechanism, and biochemistry, Third edn. Kluwer Academic/Plenum Publishers, New York
39. P Ortiz de Montellano RA Stearns 1987 Timing of the radical recombination step in cytochrome P-450 catalysis with ring-strained probes J Am Chem Soc 109 3415 3420 10.1021/ja00245a037
40. TW Ost CS Miles AW Munro J Murdoch GA Reid SK Chapman 2001 Phenylalanine 393 exerts thermodynamic control over the heme of flavocytochrome P450 BM3 Biochemistry 40 13421 13429 10.1021/bi010716m
41. SS Pochapsky TC Pochapsky JW Wei 2003 A model for effector activity in a highly specific biological electron transfer complex: the cytochrome P450(cam)-putidaredoxin couple Biochemistry 42 5649 5656 10.1021/bi034263s
42. D Pompon MJ Coon 1984 On the mechanism of action of cytochrome P-450. Oxidation and reduction of the ferrous dioxygen complex of liver microsomal cytochrome P-450 by cytochrome b5 J Biol Chem 259 15377 15385
43. TD Porter 2002 The roles of cytochrome b5 in cytochrome P450 reactions J Biochem Mol Toxicol 16 311 316 10.1002/jbt.10052
44. TL Poulos BC Finzel IC Gunsalus GC Wagner J Kraut 1985 The 2.6-A crystal structure of Pseudomonas putida cytochrome P-450 J Biol Chem 260 16122 16130
45. R Raag SA Martinis SG Sligar TL Poulos 1991 Crystal structure of the cytochrome P-450CAM active site mutant Thr252Ala Biochemistry 30 11420 11429 10.1021/bi00112a008
46. F Rappaport M Guergova-Kuras PJ Nixon BA Diner J Lavergne 2002 Kinetics and pathways of charge recombination in photosystem II Biochemistry 41 8518 8527 10.1021/bi025725p
47. I Schlichting J Berendzen K Chu AM Stock SA Maves DE Benson 2000 The catalytic pathway of cytochrome p450cam at atomic resolution Science 287 1615 1622 10.1126/science.287.5458.1615
48. V Schunemann C Jung AX Trautwein D Mandon R Weiss 2000 Intermediates in the reaction of substrate-free cytochrome P450cam with peroxy acetic acid FEBS Lett 479 149 154 10.1016/S0014-5793(00)01886-X
49. V Schunemann C Jung J Terner AX Trautwein R Weiss 2002 Spectroscopic studies of peroxyacetic acid reaction intermediates of cytochrome P450cam and chloroperoxidase J Inorg Biochem 91 586 596 10.1016/S0162-0134(02)00476-2
50. H Shimada S Nagano Y Ariga M Unno T Egawa T Hishiki 1999 Putidaredoxin-cytochrome p450cam interaction. Spin state of the heme iron modulates putidaredoxin structure J Biol Chem 274 9363 9369 10.1074/jbc.274.14. 9363
51. H Shimada S Nagano H Hori Y Ishimura 2001 Putidaredoxin-cytochrome P450cam interaction J Inorg Biochem 83 255 260 10.1016/S0162-0134(00)00173-2
52. SG Sligar 1976 Coupling of spin, substrate, and redox equilibria in cytochrome P450 Biochemistry 15 5399 5406 10.1021/bi00669a029
53. SG Sligar IC Gunsalus 1976 A thermodynamic model of regulation: modulation of redox equilibria in camphor monoxygenase Proc Natl Acad Sci USA 73 1078 1082 10.1073/pnas.73.4.1078
54. M Sono MP Roach ED Coulter JH Dawson 1996 Heme-containing oxygenases Chem Rev 96 2841 2888 10.1021/cr9500500
55. T Spolitak JH Dawson DP Ballou 2006 Rapid kinetics investigations of peracid oxidation of ferric cytochrome P450cam: nature and possible function of compound ES J Inorg Biochem 100 2034 2044 10.1016/j.jinorgbio.2006.09.026
56. T Tosha N Kagawa M Arase MR Waterman T Kitagawa 2008 Interaction between substrate and oxygen ligand responsible for effective O-O bond cleavage in bovine cytochrome P450 steroid 21-hydroxylase proved by Raman spectroscopy J Biol Chem 283 3708 3717 10.1074/jbc.M707338200
57. M Unno H Shimada Y Toba R Makino Y Ishimura 1996 Role of Arg112 of cytochrome p450cam in the electron transfer from reduced putidaredoxin. Analyses with site-directed mutants J Biol Chem 271 17869 17874 10.1074/jbc.271.30.17869
58. AD Vaz SJ Pernecky GM Raner MJ Coon 1996 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 4644 4648 10.1073/pnas.93.10.4644
59. AD Vaz DF McGinnity MJ Coon 1998 Epoxidation of olefins by cytochrome P450: evidence from site-specific mutagenesis for hydroperoxo-iron as an electrophilic oxidant Proc Natl Acad Sci USA 95 3555 3560 10.1073/pnas.95.7.3555
60. M Vidakovic SG Sligar H Li TL Poulos 1998 Understanding the role of the essential Asp251 in cytochrome p450cam using site-directed mutagenesis, crystallography, and kinetic solvent isotope effect Biochemistry 37 9211 9219 10.1021/bi980189f
61. H Zhang L Gruenke D Arscott DL Harris M Glavanovich R Johnson 2003 Determination of the rate of reduction of oxyferrous cytochrome P450 2B4 by 5-deazaFAD T491 V cytochrome P450 reductase Biochemistry 42 11594 11603 10.1021/bi034968u
62. H Zhang E Myshkin L Waskell 2005 Role of cytochrome b5 in catalysis by cytochrome P450 2B4 Biochem Biophys Res Commun 338 499 506 10.1016/j.bbrc.2005. 09.022
63. H Zhang D Hamdane SC Im L Waskell 2008 Cytochrome b5 inhibits electron transfer from NADPH-cytochrome P450 reductase to ferric cytochrome P450 2B4 J Biol Chem 283 5217 5225 10.1074/jbc.M709094200
64. B Zhao FP Guengerich A Bellamine DC Lamb M Izumikawa L Lei 2005 Binding of two flaviolin substrate molecules, oxidative coupling, and crystal structure of Streptomyces coelicolor A3(2) cytochrome P450 158A2 J Biol Chem 280 11599 11607 10.1074/jbc.M410933200
65. B Zhao FP Guengerich M Voehler MR Waterman 2005 Role of active site water molecules and substrate hydroxyl groups in oxygen activation by cytochrome P450 158A2: a new mechanism of proton transfer J Biol Chem 280 42188 42197 10.1074/jbc.M509220200