Pivotal role of P450-P450 interactions in CYP3A4 allostery: The case of α-naphthoflavone

Biochemical Journal

Volumn 453, Issue 2, 2013, Pages 219-230

  Davydov, Dmitri R ^a   Davydova, Nadezhda Y ^a   Sineva, Elena V ^a   Kufareva, Irina ^a   Halpert, James R ^a  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

naphthoflavone; Cytochrome P450 3A4; Luminescence resonance energy transfer (LRET); Microsome; Oligomerization; Protein protein interaction

Indexed keywords

[7 BENZYLOXY 4 (TRIFLUOROMETHYL)COUMARIN]; ALPHA NAPHTHOFLAVONE; CYTOCHROME P450; CYTOCHROME P450 3A4; ENZYME; LIPID; OLIGOMER; PROTEOLIPOSOME; RECOMBINANT ENZYME; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; UNCLASSIFIED DRUG;

ALLOSTERISM; ARTICLE; CONCENTRATION (PARAMETERS); ENERGY TRANSFER; LIVER MICROSOME; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

ALLOSTERIC REGULATION; BENZOFLAVONES; BIOPOLYMERS; CYTOCHROME P-450 CYP3A; HUMANS; MICROSOMES; PROTEIN BINDING;

EID: 84879577472     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20130398     Document Type: Article

References (54)

1. Davydov, D. R. and Halpert, J. R. (2008) Allosteric P450 mechanisms: multiple binding sites, multiple conformers or both? Expert Opin. Drug Metab. Toxicol. 4, 1523-1535
2. Denisov, I. G., Frank, D. J. and Sligar, S. G. (2009) Cooperative properties of cytochromes P450. Pharmacol. Ther. 124, 151-167
3. Denisov, I. G. and Sligar, S. G. (2012) A novel type of allosteric regulation: functional cooperativity in monomeric proteins. Arch. Biochem. Biophys. 519, 91-102
4. Fernando, H., Halpert, J. R. and Davydov, D. R. (2006) Resolution of multiple substrate binding sites in cytochrome P450 3A4: the stoichiometry of the enzyme-substrate complexes probed by FRET and Job's titration. Biochemistry 45, 4199-4209
5. Roberts, A. G., Campbell, A. P. and Atkins, W. M. (2005) The thermodynamic landscape of testosterone binding to cytochrome P450 3A4: ligand binding and spin state equilibria. Biochemistry 44, 1353-1366 (Pubitemid 40209015)
6. Denisov, I. G., Baas, B. J., Grinkova, Y. V. and Sligar, S. G. (2007) Cooperativity in cytochrome P450 3A4: linkages in substrate binding, spin state, uncoupling, and product formation. J. Biol. Chem. 282, 7066-7076 (Pubitemid 47093646)
7. Houston, J. B. and Galetin, A. (2005) Modelling atypical CYP3A4 kinetics: principles and pragmatism. Arch. Biochem. Biophys. 433, 351-360 (Pubitemid 39610415)
8. Galetin, A., Clarke, S. E. and Houston, J. B. (2002) Quinidine and haloperidol as modifiers of CYP3A4 activity: multisite kinetic model approach. Drug Metab. Dispos. 30, 1512-1522 (Pubitemid 35397061)
9. Egnell, A. C., Houston, J. B. and Boyer, C. S. (2005) Predictive models of CYP3A4 heteroactivation: in vitro-in vivo scaling and pharmacophore modeling. J. Pharm. Exp. Ther. 312, 926-937 (Pubitemid 40293750)
10. Kenworthy, K. E., Clarke, S. E., Andrews, J. and Houston, J. B. (2001) Multisite kinetic models for CYP3A4: simultaneous activation and inhibition of diazepam and testosterone metabolism. Drug Metab. Dispos. 29, 1644-1651 (Pubitemid 33111598)
11. Kenworthy, K. E., Bloomer, J. C., Clarke, S. E. and Houston, J. B. (1999) CYP3A4 drug interactions: correlation of 10 in vitro probe substrates. Br. J. Clin. Pharmacol. 48, 716-727 (Pubitemid 29520596)
12. Lee, C. A., Kadwell, S. H., Kost, T. A. and Serabjitsingh, C. J. (1995) CYP3A4 expressed by insect cells infected with a recombinant baculovirus containing both CYP3A4 and human NADPH-cytochrome P450 reductase is catalytically similar to human liver microsomal CYP3A4. Arch. Biochem. Biophys. 319, 157-167
13. Domanski, T. L., He, Y. A., Harlow, G. R. and Halpert, J. R. (2000) Dual role of human cytochrome P450 3A4 residue Phe-304 in substrate specificity and cooperativity. J. Pharmacol. Exp. Ther. 293, 585-591 (Pubitemid 30244111)
14. Domanski, T. L., He, Y. A., Khan, K. K., Roussel, F., Wang, Q. and Halpert, J. R. (2001) Phenylalanine and tryptophan scanning mutagenesis of CYP3A4 substrate recognition site residues and effect on substrate oxidation and cooperativity. Biochemistry 40, 10150-10160 (Pubitemid 32800121)
15. Borek-Dohalska, L. and Stiborova, M. (2010) Cytochrome P450 3A activities and their modulation by α-naphthoflavone in vitro are dictated by the efficiencies of model experimental systems. Collect. Czech. Chem. Commun. 75, 201-220
16. Frank, D. J., Denisov, I. G. and Sligar, S. G. (2011) Analysis of heterotropic cooperativity in cytochrome P450 3A4 using α-naphthoflavone and testosterone. J. Biol. Chem. 286, 5540-5545
17. Sai, Y., Dai, R., Yang, T. J., Krausz, K. W., Gonzalez, F. J., Gelboin, H. V. and Shou, M. (2000) Assessment of specificity of eight chemical inhibitors using cDNA-expressed cytochromes P450. Xenobiotica 30, 327-343 (Pubitemid 30251243)
18. Nakajima, M., Kobayashi, K., Oshima, K., Shimada, N., Tokudome, S., Chiba, K. and Yokoi, T. (1999) Activation of phenacetin O-deethylase activity by α-naphthoflavone in human liver microsomes. Xenobiotica 29, 885-898 (Pubitemid 29454382)
19. Koley, A. P., Buters, J. T. M., Robinson, R. C., Markowitz, A. and Friedman, F. K. (1997) Differential mechanisms of cytochrome P450 inhibition and activation by α-naphthoflavone. J. Biol. Chem. 272, 3149-3152 (Pubitemid 27066801)
20. Nakamura, H., Nakasa, H., Ishii, I., Ariyoshi, N., Igarashi, T., Ohmori, S. and Kitada, M. (2002) Effects of endogenous steroids on CYP3A4-mediated drug metabolism by human liver microsomes. Drug Metab. Dispos. 30, 534-540 (Pubitemid 34456975)
21. Ngui, J. S., Tang, W., Stearns, R. A., Shou, M. G., Miller, R. R., Zhang, Y., Lin, J. H. and Baillie, T. (2000) Cytochrome P450 3A4-mediated interaction of diclofenac and quinidine. Drug Metab. Dispos. 28, 1043-1050 (Pubitemid 30660358)
22. Ludwig, E., Schmid, J., Beschke, K. and Ebner, T. (1999) Activation of human cytochrome P-450 3A4-catalyzed meloxicam 5′-methylhydroxylation by quinidine and hydroquinidine in vitro. J. Pharm. Exp. Ther. 290, 1-8 (Pubitemid 29302296)
23. Ngui, J. S., Chen, Q., Shou, M. G., Wang, R. W., Stearns, R. A., Baillie, T. A. and Tang, W. (2001) In vitro stimulation of warfarin metabolism by quinidine: increases in the formation of 4′- and 10-hydroxywarfarin. Drug Metab. Dispos. 29, 877-886 (Pubitemid 32488645)
24. Zhang, Z., Li, Y., Shou, M., Zhang, Y., Ngui, J. S., Stearns, R. A., Evans, D. C., Baillie, T. A. and Tang, W. (2004) Influence of different recombinant systems on the cooperativity exhibited by cytochrome P4503A4. Xenobiotica 34, 473-486 (Pubitemid 38901457)
25. 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)
26. Reed, J. R. and Backes, W. L. (2012) Formation of P450. P450 complexes and their effect on P450 function. Pharmacol. Ther. 133, 299-310
27. Davydov, D. R. (2011) Microsomal monooxygenase as a multienzyme system: the role of P450-P450 interactions. Expert Opin. Drug Metab. Toxicol. 7, 543-558
28. Tsalkova, T. N., Davydova, N. Y., Halpert, J. R. and Davydov, D. R. (2007) Mechanism of interactions of α-naphthoflavone with cytochrome P450 3A4 explored with an engineered enzyme bearing a fluorescent probe. Biochemistry 46, 106-119 (Pubitemid 46075020)
29. Davydov, D. R., Rumfeldt, J. A. O., Sineva, E. V., Fernando, H., Davydova, N. Y. and Halpert, J. R. (2012) Peripheral ligand-binding site in cytochrome P450 3A4 located with fluorescence resonance energy transfer (FRET). J. Biol. Chem. 287, 6797-6809
30. Davydov, D. R., Baas, B. J., Sligar, S. G. and Halpert, J. R. (2007) Allosteric mechanisms in cytochrome P450 3A4 studied by high-pressure spectroscopy: pivotal role of substrate-induced changes in the accessibility and degree of hydration of the heme pocket. Biochemistry 46, 7852-7864 (Pubitemid 47016068)
31. 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
32. Fernando, H., Halpert, J. R. and Davydov, D. R. (2008) Kinetics of electron transfer in the complex of cytochrome P450 3A4 with the flavin domain of cytochrome P450BM-3 as evidence of functional heterogeneity of the heme protein. Arch. Biochem. Biophys. 471, 20-31
33. Bartlett, G. R. (1959) Phosphorus assay in column chromatography. J. Biol. Chem. 234, 466-468
34. Davydov, D. R., Kumar, S. and Halpert, J. R. (2002) Allosteric mechanisms in P450eryF probed with 1-pyrenebutanol, a novel fluorescent substrate. Biochem. Biophys. Res. Commun. 294, 806-812 (Pubitemid 34692603)
35. Davydov, D. R., Deprez, E., Hoa, G. H., Knyushko, T. V., Kuznetsova, G. P., Koen, Y. M. and Archakov, A. I. (1995) High-pressure-induced transitions in microsomal cytochrome P450 2B4 in solution: evidence for conformational inhomogeneity in the oligomers. Arch. Biochem. Biophys. 320, 330-344
36. Davydov, D. R., Femando, H. and Halpert, J. R. (2006) Variable path length and counter-flow continuous variation methods for the study of the formation of high-affinity complexes by absorbance spectroscopy. An application to the studies of substrate binding in cytochrome P450. Biophys. Chem. 123, 95-101 (Pubitemid 44279169)
37. Abagyan, R. and Totrov, M. (1994) Biased probability Monte Carlo conformational searches and electrostatic calculations for peptides and proteins. J. Mol. Biol. 235, 983-1002 (Pubitemid 24047836)
38. Kufareva, I., Ilatovskiy, A. V. and Abagyan, R. (2012) Pocketome: an encyclopedia of small-molecule binding sites in 4D. Nucleic Acids Res. 40, D535-D540
39. An, J. H., Totrov, M. and Abagyan, R. (2005) Pocketome via comprehensive identification and classification of ligand binding envelopes. Mol. Cell. Proteomics 4, 752-761 (Pubitemid 40873004)
40. Pauli, J., Vag, T., Haag, R., Spieles, M., Wenzel, M., Kaiser, W. A., Resch-Genger, U. and Hilger, I. (2009) An in vitro characterization study of new near infrared dyes for molecular imaging. Eur. J. Med. Chem. 44, 3496-3503
41. Nagle, J. F. and Tristram-Nagle, S. (2000) Structure of lipid bilayers. Biochim. Biophys. Acta 1469, 159-195
42. Hardt, S. L. (1979) Rates of diffusion controlled reactions in one, 2 and 3 dimensions. Biophys. Chem. 10, 239-243
43. Melo, E. and Martins, J. (2006) Kinetics of bimolecular reactions in model bilayers and biological membranes. A critical review. Biophys. Chem. 123, 77-94 (Pubitemid 44279173)
44. Wibo, M., Amar-Costesec, A., Berthet, J. and Beayfay, H. (1971) Electron microscope examination of subcellular fractions III. Quantitative analysis of the microsomal fraction isolated from rat liver. J. Cell. Biol. 51, 52-71
45. Wilson, Z. E., Ellis, S. W., Edwards, R. J., Tucker, G. T. and Rostami-Hodjegan, A. (2005) Implications of the disparity in relative holo: apo-protein contents of different standards used for immuno-quantification of hepatic cytochrome P450 3A4 (CYP3A4). Drug Metab. Rev. 37, 77-77
46. Perrett, H. F., Barter, Z. E., Jones, B. C., Yamazaki, H., Tucker, G. T. and Rostami-Hodjegan, A. (2007) Disparity in holoprotein/apoprotein ratios of different standards used for immunoquantification of hepatic cytochrome P450 enzymes. Drug Metab. Dispos. 35, 1733-1736 (Pubitemid 47481563)
47. Yu, A. M., Qu, J., Felmlee, M. A., Cao, J. and Jiang, X. L. (2009) Quantitation of human cytochrome P450 2D6 protein with immunoblot and mass spectrometry analysis. Drug Metab. Dispos. 37, 170-177
48. Fernando, H., Davydov, D. R., Chin, C. C. and Halpert, J. R. (2007) Role of subunit interactions in P450 oligomers in the loss of homotropic cooperativity in the cytochrome P450 3A4 mutant L211F/D214E/F304W. Arch. Biochem. Biophys. 460, 129-140 (Pubitemid 46482417)
49. Yamada, M., Ohta, Y., Bachmanova, G. I., Nishimoto, Y., Archakov, A. I. and Kawato, S. (1995) Dynamic interactions of rabbit liver cytochromes P450IA2 and P450IIB4 with cytochrome b5 and NADPH-cytochrome P450 reductase in proteoliposomes. Biochemistry 34, 10113-10119
50. 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)
51. Williams, P. A., Cosme, J., Vinkovic, D. M., Ward, A., Angove, H. C., Day, P. J., Vonrhein, C., Tickle, I. J. and Jhoti, H. (2004) Crystal structures of human cytochrome P450 3A4 bound to metyrapone and progesterone. Science 305, 683-686 (Pubitemid 39006760)
52. Roberts, A. G. and Atkins, W. M. (2007) Energetics of heterotropic cooperativity between α-naphthoflavone and testosterone binding to CYP3A4. Arch. Biochem. Biophys. 463, 89-101 (Pubitemid 46879710)
53. Grinkova, Y. V., Denisov, I. G., McLean, M. A. and Sligar, S. G. (2013) Oxidase uncoupling in heme monooxygenases: human cytochrome P450 CYP3A4 in nanodiscs. Biochem. Biophys. Res. Commun. 430, 1223-1227
54. Ekroos, M. and Sjogren, T. (2006) Structural basis for ligand promiscuity in cytochrome P450 3A4. Proc. Natl. Acad. Sci. U.S.A. 103, 13682-13687 (Pubitemid 44413967)