Organization of multiple cytochrome P450s with NADPH-cytochrome P450 reductase in membranes

Pharmacology and Therapeutics

Volumn 98, Issue 2, 2003, Pages 221-233

  Backes, Wayne L ^a   Kelley, Rusty W ^a  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aggregation state of P450; Complementary charge pairing; Functional complex formation; NADPH cytochrome P450 reductase P450 interactions; P450 reduction; P450 P450 interactions

Indexed keywords

CYTOCHROME P450; CYTOCHROME P450 1A2; CYTOCHROME P450 2B4; ISOENZYME; PHOSPHOLIPID; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE FERRIHEMOPROTEIN REDUCTASE; UNCLASSIFIED DRUG; UNSPECIFIC MONOOXYGENASE;

AMINO TERMINAL SEQUENCE; COMPLEX FORMATION; DRUG DISPOSITION; DRUG SCREENING; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME RECONSTITUTION; ENZYME SUBSTRATE; HUMAN; MICROSOME MEMBRANE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVIEW;

EID: 0037408258     PISSN: 01637258     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0163-7258(03)00031-7     Document Type: Review

References (72)

1. Alston K., Robinson R.C., Park S.S., Gelboin H.V., Friedman F.K. Interactions among cytochromes P-450 in the endoplasmic reticulum. Detection of chemically cross-linked complexes with monoclonal antibodies. J Biol Chem. 266:1991;735-739.
2. Backes W.L., Eyer C.S. Cytochrome P-450 LM2 reduction. Substrate effects on the rate of reductase-LM2 association. J Biol Chem. 264:1989;6252-6259.
3. Backes W.L., Batie C.J., Cawley G.F. Interactions among P450 enzymes when combined in reconstituted systems: formation of a 2B4-1A2 complex with a high affinity for NADPH-cytochrome P450 reductase. Biochemistry. 37:1998;12852-12859.
4. Bernhardt R. Cytochrome P450: structure, function, and generation of reactive oxygen species. Rev Physiol Biochem Pharmacol. 127:1996;137-221.
5. Bernhardt R., Makower A., Janig G.R., Ruckpaul K. Selective chemical modification of a functionally linked lysine in cytochrome P-450 LM2. Biochim Biophys Acta. 785:1984;186-190.
6. Bernhardt R., Pommerening K., Ruckpaul K. Modification of carboxyl groups on NADPH-cytochrome P-450 reductase involved in binding of cytochromes c and P-450 LM2. Biochem Int. 14:1987;823-832.
7. Bernhardt R., Kraft R., Otto A., Ruckpaul K. Electrostatic interactions between cytochrome P-450 LM2 and NADPH-cytochrome P-450 reductase. Biomed Biochim Acta. 47:1988;581-592.
8. Bernhardt R., Kraft R., Ruckpaul K. Molecular mechanism of P450/reductase interaction. Schuster I. Cytochrome P450: Biochemistry and Biophysics. 1989;320-323 Taylor and Francis, New York.
9. Black S.D., French J.S., Williams C.H. Jr., Coon M.J. Role of a hydrophobic polypeptide in the N-terminal region of NADPH-cytochrome P-450 reductase in complex formation with P-450LM. Biochem Biophys Res Commun. 91:1979;1528-1535.
10. Causey K.M., Eyer C.S., Backes W.L. Dual role of phospholipid in the reconstitution of cytochrome P-450 LM2-dependent activities. Mol Pharmacol. 38:1990;134-142.
11. Cawley G.F., Batie C.J., Backes W.L. Substrate-dependent competition of different P450 isozymes for limiting NADPH-cytochrome P450 reductase. Biochemistry. 34:1995;1244-1247.
12. Cawley G.F., Zhang S., Kelley R., Backes W.L. Evidence supporting the interaction of P450 2B4 and P450 1A2 in microsomal preparations. Drug Metab Dispos. 29:2001;1529-1534.
13. Cosme J., Johnson E.F. Engineering microsomal cytochrome P450 2C5 to be a soluble, monomeric enzyme. Mutations that alter aggregation, phospholipid dependence of catalysis, and membrane binding. J Biol Chem. 275:2000;2545-2553.
14. Cvrk T., Strobel H.W. Role of LYS271 and LYS279 residues in the interaction of cytochrome P4501A1 with NADPH-cytochrome P450 reductase. Arch Biochem Biophys. 385:2001;290-300.
15. Davydov D.R., Kariakin A.A., Petushkova N.A., Peterson J.A. Association of cytochromes P450 with their reductases: opposite sign of the electrostatic interactions in P450BM-3 as compared with the microsomal 2B4 system. Biochemistry. 39:2000;6489-6497.
16. Davydov D.R., Petushkova N.A., Archakov A.I., Hoa G.H. Stabilization of P450 2B4 by its association with P450 1A2 revealed by high-pressure spectroscopy. Biochem Biophys Res Commun. 276:2000;1005-1012.
17. Dean W.L., Gray R.D. Relationship between state of aggregation and catalytic activity for cytochrome P-450LM2 and NADPH-cytochrome P-450 reductase. J Biol Chem. 257:1982;14679-14685.
18. Dong M.S., Yamazaki H., Guo Z.Y., Guengerich F.P. Recombinant human cytochrome P450 1A2 and an N-terminal-truncated form: construction, purification, aggregation properties, and interactions with flavodoxin, ferredoxin, and NADPH-cytochrome P450 reductase. Arch Biochem Biophys. 327:1996;11-19.
19. Dutton D.R., McMillen S.K., Sonderfan A.J., Thomas P.E., Parkinson A. Studies on the rate-determining factor in testosterone hydroxylation by rat liver microsomal cytochrome P-450: evidence against cytochrome P-450 isozyme:isozyme interactions. Arch Biochem Biophys. 255:1987;316-328.
20. Estabrook R.W., Franklin M.R., Cohen B., Shigamatzu A., Hildebrandt A.G. Biochemical and genetic factors influencing drug metabolism. Influence of hepatic microsomal mixed function oxidation reactions on cellular metabolic control. Metabolism. 20:1971;187-199.
21. Estabrook R.W., Shet M.S., Fisher C.W., Jenkins C.M., Waterman M.R. The interaction of NADPH-P450 reductase with P450: an electrochemical study of the role of the flavin mononucleotide-binding domain. Arch Biochem Biophys. 333:1996;308-315.
22. Eyer C.S., Backes W.L. Relationship between the rate of reductase-cytochrome P450 complex formation and the rate of first electron transfer. Arch Biochem Biophys. 293:1992;231-240.
23. French J.S., Guengerich F.P., Coon M.J. Interactions of cytochrome P-450, NADPH-cytochrome P-450 reductase, phospholipid, and substrate in the reconstituted liver microsomal enzyme system. J Biol Chem. 255:1980;4112-4119.
24. Gigon P.L., Gram T.E., Gillette J.R. Studies on the rate of reduction of hepatic microsomal cytochrome P-450 by reduced nicotinamide adenine dinucleotide phosphate: effect of drug substrates. Mol Pharmacol. 5:1969;109-122.
25. Gut J., Richter C., Cherry R.J., Winterhalter K.H., Kawato S. Rotation of cytochrome P-450: II. Specific interactions of cytochrome P-450 with NADPH-cytochrome P-450 reductase in phospholipid vesicles. J Biol Chem. 257:1982;7030-7036.
26. Gut J., Richter C., Cherry R.J., Winterhalter K.H., Kawato S. Rotation of cytochrome P-450. Complex formation of cytochrome P-450 with NADPH-cytochrome P-450 reductase in liposomes demonstrated by combining protein rotation with antibody-induced cross-linking. J Biol Chem. 258:1983;8588-8594.
27. Hildebrandt A., Estabrook R.W. Evidence for the participation of cytochrome b5 in hepatic microsomal mixed-function oxidation reactions. Arch Biochem Biophys. 143:1971;66-79.
28. Imaoka S., Terano Y., Funae Y. Constitutive testosterone 6 beta-hydroxylase in rat liver. J Biochem (Tokyo). 104:1988;481-487.
29. Imaoka S., Imai Y., Shimada T., Funae Y. Role of phospholipids in reconstituted cytochrome P450 3A form and mechanism of their activation of catalytic activity. Biochemistry. 31:1992;6063-6069.
30. Ingelman-Sundberg M. Phospholipids and detergents as effectors in the liver microsomal hydroxylase system. Biochim Biophys Acta. 488:1977;225-234.
31. Ingelman-Sundberg M., Haaparanta T., Rydstrom J. Membrane charge as effector of cytochrome P-450LM2 catalyzed reactions in reconstituted liposomes. Biochemistry. 20:1981;4100-4106.
32. Ingelman-Sundberg M., Blanck J., Smettan G., Ruckpaul K. Reduction of cytochrome P-450 LM2 by NADPH in reconstituted phospholipid vesicles is dependent on membrane charge. Eur J Biochem. 134:1983;157-162.
33. Johnson E.F., Muller-Eberhard U. Resolution of two forms of cytochrome P-450 from liver microsomes of rabbits treated with 2,3,7,8-tetrachlorodibenz-p-dioxin. J Biol Chem. 252:1977;2839-2845.
34. Kaminsky L.S., Guengerich F.P. Cytochrome P-450 isozyme/isozyme functional interactions and NADPH-cytochrome P-450 reductase concentrations as factors in microsomal metabolism of warfarin. Eur J Biochem. 149:1985;479-489.
35. Kanaeva I.P., Dedinskii I.R., Skotselyas E.D., Krainev A.G., Guleva I.V., Sevryukova I.F., Koen Y.M., Kuznetsova G.P., Bachmanova G.I., Archakov A.I. Comparative study of monomeric reconstituted and membrane microsomal monooxygenase systems of the rabbit liver: I. Properties of NADPH-cytochrome P450 reductase and cytochrome P450 LM2 (2B4) monomers. Arch Biochem Biophys. 298:1992;395-402.
36. Kanaeva I.P., Nikityuk O.V., Davydov D.R., Dedinskii I.R., Koen Y.M., Kuznetsova G.P., Skotselyas E.D., Bachmanova G.I., Archakov A.I. Comparative study of monomeric reconstituted and membrane microsomal monooxygenase systems of the rabbit liver: II. Kinetic parameters of reductase and monooxygenase reactions. Arch Biochem Biophys. 298:1992;403-412.
37. Kawato S., Gut J., Cherry R.J., Winterhalter K.H., Richter C. Rotation of cytochrome P-450: I. Investigations of protein-protein interactions of cytochrome P-450 in phospholipid vesicles and liver microsomes. J Biol Chem. 257:1982;7023-7029.
38. Kawato S., Ashikawa I., Iwase T., Hara E. Drug-induction decreases the mobility of cytochrome P-450 in rat liver microsomes: protein rotation study. J Biochem (Tokyo). 109:1991;587-593.
39. Li D.N., Pritchard M.P., Hanlon S.P., Burchell B., Wolf C.R., Friedberg T. Competition between cytochrome P-450 isozymes for NADPH-cytochrome P-450 oxidoreductase affects drug metabolism. J Pharmacol Exp Ther. 289:1999;661-667.
40. Lu A.Y.H., Junk K.W., Coon M.J. Resolution of the cytochrome P-450-containing omega-hydroxylation system of liver microsomes into three components. J Biol Chem. 244:1969;3714-3721.
41. Miwa G.T., Lu A.Y.H. The association of cytochrome P-450 and NADPH-cytochrome P-450 reductase in phospholipid membranes. Arch Biochem Biophys. 234:1984;161-166.
42. Miwa G.T., West S.B., Huang M.T., Lu A.Y.H. Studies on the association of cytochrome P-450 and NADPH-cytochrome c reductase during catalysis in a reconstituted hydroxylating system. J Biol Chem. 254:1979;5695-5700.
43. Muller-Enoch D., Churchill P., Fleischer S., Guengerich F.P. Interaction of liver microsomal cytochrome P-450 and NADPH-cytochrome P-450 reductase in the presence and absence of lipid. J Biol Chem. 259:1984;8174-8182.
44. Myasoedova K.N., Berndt P. Immobilized cytochrome P-450LM2. Dissociation and reassociation of oligomers. FEBS Lett. 270:1990;177-180.
45. Nadler S.G., Strobel H.W. Role of electrostatic interactions in the reaction of NADPH-cytochrome P-450 reductase with cytochromes P-450. Arch Biochem Biophys. 261:1988;418-429.
46. Nadler S.G., Strobel H.W. Identification and characterization of an NADPH-cytochrome P450 reductase derived peptide involved in binding to cytochrome P450. Arch Biochem Biophys. 290:1991;277-284.
47. Nelson D.R., Koymans L., Kamataki T., Stegeman J.J., Feyereisen R., Waxman D.J., Waterman M.R., Gotoh O., Coon M.J., Estabrook R.W., Gunsalus I.C., Nebert D.W. The P450 superfamily: update on new sequences, gene mapping, accession numbers, and nomenclature. Pharmacogenetics. 6:1996;1-42.
48. 2-terminal region on localization in cytosol and membranes. Proc Natl Acad Sci USA. 90:1993;2651-2655.
49. 2-terminal region and expressed in Escherichia coli. Arch Biochem Biophys. 318:1995;446-456.
50. Peterson J.A., Ebel R.E., O'Keeffe D.H., Matsubara T., Estabrook R.W. Temperature dependence of cytochrome P-450 reduction. A model for NADPH-cytochrome P-450 reductase:cytochrome P-450 interaction. J Biol Chem. 251:1976;4010-4016.
51. Sevrukova I.F., Kanaeva I.P., Koen Y.M., Samenkova N.F., Bachmanova G.I., Archakov A.I. Catalytic activity of cytochrome P4501A2 in reconstituted system with Emulgen 913. Arch Biochem Biophys. 311:1994;133-143.
52. Shen A.L., Kasper C.B. Role of acidic residues in the interaction of NADPH-cytochrome P450 oxidoreductase with cytochrome P450 and cytochrome c. J Biol Chem. 270:1995;27475-27480.
53. Shimizu T., Tateishi T., Hatano M., Fujii-Kuriyama Y. Probing the role of lysines and arginines in the catalytic function of cytochrome P450d by site-directed mutagenesis. Interaction with NADPH-cytochrome P450 reductase. J Biol Chem. 266:1991;3372-3375.
54. Strobel H.W., Lu A.Y.H., Heidema J., Coon M.J. Phosphatidylcholine requirement in the enzymatic reduction of hemoprotein P-450 and in fatty acid, hydrocarbon, and drug hydroxylation. J Biol Chem. 245:1970;4851-4854.
55. Tamburini P.P., Schenkman J.B. Differences in the mechanism of functional interaction between NADPH-cytochrome P-450 reductase and its redox partners. Mol Pharmacol. 30:1986;178-185.
56. Tamburini P.P., Gibson G.G., Backes W.L., Sligar S.G., Schenkman J.B. Reduction kinetics of purified rat liver cytochrome P-450. Evidence for a sequential reaction mechanism dependent on the hemoprotein spin state. Biochemistry. 23:1984;4526-4533.
57. Tamburini P.P., MacFarquhar S., Schenkman J.B. Evidence of binary complex formations between cytochrome P-450, cytochrome b5, and NADPH-cytochrome P-450 reductase of hepatic microsomes. Biochem Biophys Res Commun. 134:1986;519-526.
58. Tan Y.Z., Patten C.J., Smith P., Yang C.S. Competitive interactions between cytochromes P450 2A6 and 2E1 for NADPH-cytochrome P450 oxidoreductase in the microsomal membranes produced by a baculovirus expression system. Arch Biochem Biophys. 342:1997;82-91.
59. Taniguchi H., Pyerin W. Phospholipid bilayer membranes play decisive roles in the cytochrome P-450-dependent monooxygenase system. J Cancer Res Clin Oncol. 114:1988;335-340.
60. Taniguchi H., Imai Y., Iyanagi T., Sato R. Interaction between NADPH-cytochrome P-450 reductase and cytochrome P-450 in the membrane of phosphatidylcholine vesicles. Biochim Biophys Acta. 550:1979;341-356.
61. Taniguchi H., Imai Y., Sato R. Protein-protein and lipid-protein interactions in a reconstituted cytochrome P-450 dependent microsomal monooxygenase. Biochemistry. 26:1987;7084-7090.
62. Tsuprun V.L., Myasoedova K.N., Berndt P., Sograf O.N., Orlova E.V., Chernyak V.Y., Archakov A.I., Skulachev V.P. Quaternary structure of the liver microsomal cytochrome P-450. FEBS Lett. 205:1986;35-40.
63. von Wachenfeldt C., Richardson T.H., Cosme J., Johnson E.F. Microsomal P450 2C3 is expressed as a soluble dimer in Escherichia coli following modification of its N-terminus. Arch Biochem Biophys. 339:1997;107-114.
64. Voznesensky A.I., Schenkman J.B. The cytochrome P450 2B4-NADPH cytochrome P450 reductase electron transfer complex is not formed by charge-pairing. J Biol Chem. 267:1992;14669-14676.
65. Voznesensky A.I., Schenkman J.B. Quantitative analyses of electrostatic interactions between NADPH-cytochrome P450 reductase and cytochrome P450 enzymes. J Biol Chem. 269:1994;15724-15731.
66. 2-terminal region of rabbit CYP2E1 is not essential for interaction with NADPH-cytochrome P450 reductase. Biochem Biophys Res Commun. 203:1994;156-161.
67. Wagner S.L., Dean W.L., Gray R.D. Effect of a zwitterionic detergent on the state of aggregation and catalytic activity of cytochrome P-450LM2 and NADPH-cytochrome P-450 reductase. J Biol Chem. 259:1984;2390-2395.
68. Wagner S.L., Dean W.L., Gray R.D. Zwitterionic detergent mediated interaction of purified cytochrome P-450LM4 from 5,6-benzoflavone-treated rabbits with NADPH-cytochrome P-450 reductase. Biochemistry. 26:1987;2343-2348.
69. West S.B., Lu A.Y.H. Reconstituted liver microsomal enzyme system that hydroxylates drugs, other foreign compounds and endogenous substrates: V. Competition between cytochromes P-450 and P-448 for reductase in 3,4-benzpyrene hydroxylation. Arch Biochem Biophys. 153:1972;298-303.
70. Yamada M., Ohta Y., Bachmanova G.I., Nishimoto Y., Archakov A.I., Kawato S. Dynamic interactions of rabbit liver cytochromes P450IA2 and P450IIB4 with cytochrome b5 and NADPH-cytochrome P450 reductase in proteoliposomes. Biochemistry. 34:1995;10113-10119.
71. Yamazaki H., Gillam E.M.J., Dong M.S., Johnson W.W., Guengerich F.P., Shimada T. Reconstitution of recombinant cytochrome P450 2C10(2C9) and comparison with cytochrome P450 3A4 and other forms: effects of cytochrome P450-P450 and cytochrome P450-B5 interactions. Arch Biochem Biophys. 342:1997;329-337.
72. Yamazaki H., Inoue K., Shaw P.M., Checovich W.J., Guengerich F.P., Shimada T. Different contributions of cytochrome P450 2C19 and 3A4 in the oxidation of omeprazole by human liver microsomes: effects of contents of these two forms in individual human samples. J Pharmacol Exp Ther. 283:1997;434-442.