Effect of homomeric P450-P450 complexes on P450 function

Biochemical Journal

Volumn 446, Issue 3, 2012, Pages 489-497

  Reed, James R ^a   Connick, J Patrick ^a   Cheng, Dongmei ^a   Cawley, George F ^a   Backes, Wayne L ^a  

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

Author keywords

Bioluminescence resonance energy transfer (BRET); Cytochrome P450; Enzyme kinetics; Homomeric P450 P450 complexes; Protein cross linking; Protein protein interactions

Indexed keywords

CYTOCHROME P450; CYTOCHROME P450 1A2; CYTOCHROME P450 2B4; CYTOCHROME P450 2E1; CYTOCHROME P450 REDUCTASE;

ARTICLE; BIOLOGICAL ACTIVITY; BIOLUMINESCENCE RESONANCE ENERGY TRANSFER; CATALYSIS; CELL STRAIN HEK293; CONTROLLED STUDY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MICHAELIS MENTEN KINETICS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CROSS LINKING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MODIFICATION;

ANIMALS; BIOLUMINESCENCE RESONANCE ENERGY TRANSFER TECHNIQUES; CATALYSIS; CYTOCHROME P-450 CYP1A2; CYTOCHROME P-450 ENZYME SYSTEM; HEK293 CELLS; HUMANS; KINETICS; PROTEIN INTERACTION DOMAINS AND MOTIFS; RABBITS;

EID: 84865599017     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20120636     Document Type: Article

References (54)

1. Lu, A. Y., Strobel, H. W. and Coon, M. J. (1969) Hydroxylation of benzphetamine and other drugs by a solubilized form of cytochrome P-450 from liver microsomes: lipid requirement for drug demethylation Biochem. Biophys. Res. Commun. 36, 545-551
2. Lu, A. Y. H. and Coon, M. J. (1968) Role of hemoprotein P-450 in fatty acid ω-hydroxylation in a soluble enzyme system from liver microsomes J. Biol. Chem. 243, 1331-1332
3. Miwa, G. T. and Lu, A. Y. H. (1984) The association of cytochrome P-450 and NADPH-cytochrome P-450 reductase in phospholipid membranes Arch. Biochem. Biophys. 234, 161-166 (Pubitemid 15203704)
4. Miwa, G. T., West, S. B., Huang, M. T. and Lu, A. Y. H. (1979) Studies on the association of cytochrome P-450 and NADPH-cytochrome c reductase during catalysis in a reconstituted hydroxylating system. J. Biol. Chem. 254, 5695-5700
5. Backes, W. L. (1993) NADPH-cytochrome P450 reductase: function in cytochrome P450. In Cytochrome P450 (Schenkman, J. B. and Greim, H., eds), pp. 15-34, Springer-Verlag, Berlin
6. Reed, J. R. and Backes, W. L. (2012) Formation of P450-P450 complexes and their effect on P450 function. Pharmacol. Ther. 133, 299-310
7. Backes, W. L., Batie, C. J. and Cawley, G. F. (1998) 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, 12852-12859 (Pubitemid 28433517)
8. Backes, W. L. and Kelley, R. W. (2003) Organization of multiple cytochrome P450s with NADPH-cytochrome P450 reductase in membranes. Pharmacol. Ther. 98, 221-233 (Pubitemid 36513776)
9. Davydov, D. R., Petushkova, N. A., Bobrovnikova, E. V., Knyushko, T. V. and Dansette, P. (2001) Association of cytochromes P450 1A2 and 2B4: are the interactions between different P450 species involved in the control of the monooxygenase activity and coupling? Adv. Exp. Med. Biol. 500, 335-338 (Pubitemid 34107025)
10. Hazai, E. and Kupfer, D. (2005) Interactions between CYP2C9 and CYP2C19 in reconstituted binary systems influence their catalytic activity: possible rationale for the inability of CYP2C19 to catalyze methoxychlor demethylation in human liver microsomes Drug Metab. Dispos. 33, 157-164 (Pubitemid 40023527)
11. Kelley, R. W., Reed, J. R. and Backes, W. L. (2005) Effects of ionic strength on the functional interactions between CYP2B4 and CYP1A2. Biochemistry 44, 2632-2641 (Pubitemid 40279567)
12. Kelley, R. W., Cheng, D. and Backes, W. L. (2006) Heteromeric complex formation between CYP2E1 and CYP1A2: evidence for the involvement of electrostatic interactions. Biochemistry 45, 15807-15816 (Pubitemid 46032501)
13. Reed, J. R., Eyer, M. and Backes, W. L. (2010) Functional interactions between cytochromes P450 1A2 and 2B4 require both enzymes to reside in the same phospholipid vesicle: evidence for physical complex formation. J. Biol. Chem. 285, 8942-8952
14. Subramanian, M., Zhang, H. and Tracy, T. S. (2010) CYP2C9-CYP3A4 protein-protein interactions in a reconstituted expressed enzyme system. Drug Metab. Dispos. 38, 1003-1009
15. Subramanian, M., Low, M., Locuson, C. W. and Tracy, T. S. (2009) CYP2D6-CYP2C9 protein-protein interactions and isoform-selective effects on substrate binding and catalysis. Drug Metab. Dispos. 37, 1682-1689
16. Cawley, G. F., Batie, C. J. and Backes, W. L. (1995) Substrate-dependent competition of different P450 isozymes for limiting NADPH-cytochrome P450 reductase. Biochemistry 34, 1244-1247
17. Saribas, A. S., Gruenke, L. and Waskell, L. (2001) Overexpression and purification of the membrane-bound cytochrome P450 2B4. Protein Expression Purif. 21, 303-309 (Pubitemid 34161454)
18. Yasukochi, Y. and Masters, B. S. (1976) Some properties of a detergent-solubilized NADPH-cytochrome c (cytochrome P-450) reductase purified by biospecific affinity chromatography. J. Biol. Chem. 251, 5337-5344
19. Shen, A. L., Porter, T. D., Wilson, T. E. and Kasper, C. B. (1989) Structural analysis of the FMN binding domain of NADPH-cytochrome P-450 oxidoreductase by site-directed mutagenesis. J. Biol. Chem. 264, 7584-7589 (Pubitemid 19119176)
20. Coon, M. J., Van Der Hoeven, T. A., Dahl, S. B. and Haugen, D. A. (1984) Two forms of liver microsomal cytochrome P-450, P-450LM2 and P-450LM4 (rabbit liver). Methods Enzymol. 52, 109-117
21. Cheng, D., Kelley, R. W., Cawley, G F. and Backes, W. L. (2004) High-level expression of recombinant rabbit cytochrome P450 2E1 in Escherichia coli C41 and its purification/Protein. Expression Purif. 33, 66-71 (Pubitemid 38069816)
22. Causey, K. M., Eyer, C. S. and Backes, W. L. (1990) Dual role of phospholipid in the reconstitution of cytochrome P-450 LM2-dependent activities. Mol. Pharmacol. 38, 134-142 (Pubitemid 20231495)
23. Beebe, L. E., Roberts, E. S., Fornwald, L. W., Hollenberg, P. F. and Alworth, W. L. (1996) Mechanism-based inhibition of mouse P4502b-10 by selected arylalkynes. Biochem. Pharmacol. 52, 1507-1513 (Pubitemid 26375456)
24. Burke, M. D., Thompson, S., Elcombe, J. R., Halpert, J., Haaparanta, T. and Mayer, R. T. (1985) Ethoxy-, pentoxy- and benzyloxyphenoxazones and homologues: a series of substrates to distinguish between different induced cytochromes P-450. Biochem. Pharmacol. 34, 3337-3345 (Pubitemid 16215699)
25. Roberts, E. S., Ballou, D. P., Hopkins, N. E., Alworth, W. L. and Hollenberg, P. F. (1995) Mechanistic studies of 9-ethynylphenanthrene- inactivated cytochrome P450 2B1 Arch. Biochem. Biophys. 323, 303-312
26. Hayashi, S., Omata, Y., Sakamoto, H., Hara, T. and Noguchi, M. (2003) Purification and characterization of a soluble form of rat liver NADPH-cytochrome P-450 reductase highly expressed in Escherichia coli. Protein Expression Purif. 29, 1-7 (Pubitemid 36599788)
27. Cheng, D., Reed, J. R., Harris, D. and Backes, W. L. (2007) Inhibition of CYP2B4 by the mechanism-based inhibitor 2-ethynylnaphthalene: inhibitory potential of 2EN is dependent on the size of the substrate Arch. Biochem. Biophys. 462, 28-37 (Pubitemid 46755142)
28. Netter, K. J. and Seidel, G. (1964) An adaptively stimulated O-demethylating system in rat liver microsomes and its kinetic properties. J. Pharmacol. Exp. Ther. 146, 61-65
29. de Andrade, J. B., Bispo, M. S., Reboucas, M. V., Carvalho, M. L. S. M. and Pinheiro, H. L. C. (1996) Spectrofluorimetric determination of formaldehyde in liquid samples. Am. Lab. 28, 56-58
30. Hanna, I. H., Reed, J. R., Guengerich, F. P. and Hollenberg, P. F. (2000) Expression of human cytochrome P450 2B6 in Escherichia coli: characterization of catalytic activity and expression levels in human liver. Arch. Biochem. Biophys. 376, 206-216 (Pubitemid 30205131)
31. Backes, W. L. and Eyer, C. S. (1989) Cytochrome P-450 LM2 reduction. Substrate effects on the rate of reductase-LM2 association. J. Biol. Chem. 264, 6252-6259 (Pubitemid 19106700)
32. Eyer, C. S. and Backes, W. L. (1992) Relationship between the rate of reductase-cytochrome P450 complex formation and the rate of first electron transfer Arch. Biochem. Biophys. 293, 231-240
33. Hu, G., Johnson, E. F. and Kemper, B. (2010) CYP2C8 exists as a dimer in natural membranes. Drug Metab. Dispos. 38, 1976-1983
34. Ozalp, C., Szczesna-Skorupa, E. and Kemper, B. (2005) Bimolecular fluorescence complementation analysis of cytochrome p450 2c2, 2e1, and NADPH-cytochrome p450 reductase molecular interactions in living cells. Drug Metab. Dispos. 33, 1382-1390 (Pubitemid 41196983)
35. Szczesna-Skorupa, E., Mallah, B. and Kemper, B. (2003) Fluorescence resonance energy transfer analysis of cytochromes P450 2C2 and 2E1 molecular interactions in living cells J. Biol. Chem. 278, 31269-31276 (Pubitemid 36994644)
36. Hwang, H. W., Lee, J. R., Chou, K. Y., Suen, C. S., Hwang, M. J., Chen, C., Shieh, R. C. and Chau, L. Y. (2009) Oligomerization is crucial for the stability and function of heme oxygenase-1 in the endoplasmic reticulum. J. Biol. Chem. 284, 22672-22679
37. Marohnic, C. C., Huber, III, W. J., Patrick, C. J., Reed, J. R., McCammon, K., Panda, S. P., Martasek, P., Backes, W. L. and Masters, B. S. (2011) Mutations of human cytochrome P450 reductase differentially modulate heme oxygenase-1 activity and oligomerization. Arch. Biochem. Biophys. 513, 42-50
38. James, J. R., Oliveira, M. I., Carmo, A. M., Iaboni, A. and Davis, S. J. (2006) A rigorous experimental framework for detecting protein oligomerization using bioluminescence resonance energy transfer. Nat. Methods 3, 1001-1006 (Pubitemid 44782699)
39. Yamazaki, H., Gillam, E. M. J., Dong, M. S., Johnson, W. W., Guengerich, F. P. and Shimada, T. (1997) 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, 329-337 (Pubitemid 27251255)
40. Davydov, D. R., Fernando, H., Baas, B. J., Sligar, S. G. and Halpert, J. R. (2005) Kinetics of dithionite-dependent reduction of cytochrome P450 3A4: heterogeneity of the enzyme caused by its oligomerization. Biochemistry 44, 13902-13913 (Pubitemid 41507470)
41. Davydov, D. R., Sineva, E. V., Sistla, S., Davydova, N. Y., Frank, D. J., Sligar, S. G. and Halpert, J. R. (2010) Electron transfer in the complex of membrane-bound human cytochrome P450 3A4 with the flavin domain of P450BM-3: the effect of oligomerization of the heme protein and intermittent modulation of the spin equilibrium. Biochim. Biophys. Acta 1797, 378-390
42. Myasoedova, K. N. and Berndt, P. (1990) Cytochrome P-450LM2 oligomers in proteoliposomes. FEBS Lett. 275, 235-238
43. Kawato, S., Gut, J., Cherry, R. J., Winterhalter, K. H. and Richter, C. (1982) 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, 7023-7029
44. Gut, J., Richter, C., Cherry, R. J., Winterhalter, K. H. and Kawato, S. (1982) 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, 7030-7036
45. Schwarz, D., Pirrwitz, J. and Ruckpaul, K. (1982) Rotational diffusion of cytochrome P-450 in the microsomal membrane-evidence for a clusterlike organization from saturation transfer electron paramagnetic resonance spectroscopy. Arch. Biochem. Biophys. 216, 322-328
46. Guengerich, F. P. and Holladay, L. A. (1979) Hydrodynamic characterization of highly purified and functionally active liver microsomal cytochrome P-450. Biochemistry 18, 5442-5449
47. Tsuprun, V. L., Myasoedova, K. N., Berndt, P., Sograf, O. N., Orlova, E. V., Chernyak, V. Y., Archakov, A. I. and Skulachev, V. P. (1986) Quaternary structure of the liver microsomal cytochrome P-450. FEBS Lett. 205, 35-40 (Pubitemid 16031344)
48. Autor, A. P., Kaschnitz, R. M., Heidema, J. K. and Coon, M. J. (1973) Sedimentation and other properties of the reconstituted liver microsomal mixed-function oxidase system containing cytochrome P-450, reduced triphosphopyridine nucleotide-cytochrome P-450 reductase, and phosphatidylcholine. Mol. Pharmacol. 9, 93-104
49. Myasoedova, K. N. and Tsuprun, V. L. (1993) Cytochrome P-450: hexameric structure of the purified LM4 form. FEBS Lett. 325, 251-254 (Pubitemid 23186487)
50. French, J. S., Guengerich, F. P. and Coon, M. J. (1980) Interactions of cytochrome P-450, NADPH-cytochrome P-450 reductase, phospholipid, and substrate in the reconstituted liver microsomal enzyme system. J. Biol. Chem. 255, 4112-4119
51. Jamakhandi, A. P., Kuzmic, P., Sanders, D. E. and Miller, G. P. (2007) Global analysis of protein-protein interactions reveals multiple CYP2E1-reductase complexes. Biochemistry 46, 10192-10201 (Pubitemid 47381277)
52. Shimada, T., Mernaugh, R. L. and Guengerich, F. P. (2005) Interactions of mammalian cytochrome P450, NADPH-cytochrome P450 reductase, and cytochrome b5 enzymes. Arch. Biochem. Biophys. 435, 207-216 (Pubitemid 40170032)
53. Tan, Y. Z., Patten, C. J., Smith, P. and Yang, C. S. (1997) 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, 82-91 (Pubitemid 27217104)
54. Cawley, G. F., Zhang, S., Kelley, R. W. and Backes, W. L. (2001) Evidence supporting the interaction of CYP2B4 and CYP1A2 in microsomal preparations. Drug Metab. Dispos. 29, 1529-1534 (Pubitemid 33111584)