7,8-benzoflavone binding to human cytochrome P450 3A4 reveals complex fluorescence quenching, suggesting binding at multiple protein sites

References

• Atkins, W. M. (2004). Implications of the allosteric kinetics of cytochrome P450s. Drug Discovery Today, 9, 478–484.
   PubMed Web of Science ®Google Scholar
• Busby Jr., W. F., Ackerman, J. M., & Crespi, C. L. (1999). Effect of methanol, ethanol, dimethyl sulfoxide, and acetonitrile on in vitro activities of cDNA-expressed human cytochromes P-450. Drug Metabolism and Disposition, 27, 246–249.
   PubMed Web of Science ®Google Scholar
• Callis, P. R., & Burgess, B. K. (1997). Tryptophan fluorescence shifts in proteins from hybrid simulations: An electrostatic approach. The Journal of Physical Chemistry B, 101, 9429–9432.10.1021/jp972436f
   Web of Science ®Google Scholar
• Callis, P. R., & Liu, T. (2004). Quantitative prediction of fluorescence quantum yields for tryptophan in proteins. The Journal of Physical Chemistry B, 108, 4248–4259.10.1021/jp0310551
   Web of Science ®Google Scholar
• Cantor, C. R., & Schimmel, P. R. (1980). Fluorescence spectroscopy, in Biophysical Chemistry. Part II: Techniques for the Study of Biological Structure and Function (1st ed., pp. 433–455). New York, NY: W. H. Freeman.
   Google Scholar
• Dabrowski, M. J., Schrag, M. L., Wienkers, L. C., & Atkins, W. M. (2002). Pyrene·pyrene complexes at the active site of cytochrome P450 3A4: Evidence for a multiple substrate binding site. Journal of the American Chemical Society, 124, 11866–11867.10.1021/ja027552x
   PubMed Web of Science ®Google Scholar
• Davydov, D. R., Davydova, N. Y., Sineva, E. V., & Halpert, J. R. (2015). Interactions among cytochromes P450 in microsomal membranes. Journal of Biological Chemistry, 290, 3850–3864.10.1074/jbc.M114.615443
   PubMed Web of Science ®Google Scholar
• Davydov, D. R., Davydova, N. Y., Sineva, E. V., Kufareva, I., & Halpert, J. R. (2013). Pivotal role of P450-P450 interactions in CYP3A4 allostery: The case of α-naphthoflavone. Biochemical Journal, 453, 219–230.10.1042/BJ20130398
   PubMed Web of Science ®Google Scholar
• Davydov, D. R., Fernando, H., Baas, B. J., Sligar, S. G., & Halpert, J. R. (2005). Kinetics of dithionite-dependent reduction of cytochrome P450 3A4: Heterogeneity of the enzyme caused by its oligomerization. Biochemistry, 44, 13902–13913.10.1021/bi0509346
   PubMed Web of Science ®Google Scholar
• Davydov, D. R., Rumfeldt, J. A., Sineva, E. V., Fernando, H., Davydova, N. Y., & Halpert, J. R. (2012). Peripheral ligand-binding site in cytochrome P450 3A4 located with fluorescence resonance energy transfer (FRET). Journal of Biological Chemistry, 287, 6797–6809.10.1074/jbc.M111.325654
   PubMed Web of Science ®Google Scholar
• Denisov, I. G., Frank, D. J., & Sligar, S. G. (2009). Cooperative properties of cytochromes P450. Pharmacology and Therapeutics, 124, 151–167.10.1016/j.pharmthera.2009.05.011
   PubMed Web of Science ®Google Scholar
• Denisov, I. G., Grinkova, Y. V., Baylon, J. L., Tajkhorshid, E., & Sligar, S. G. (2015). Mechanism of drug–drug interactions mediated by human cytochrome P450 CYP3A4 monomer. Biochemistry, 54, 2227–2239.10.1021/acs.biochem.5b00079
   PubMed Web of Science ®Google Scholar
• Denisov, I. G., & Sligar, S. G. (2012). A novel type of allosteric regulation: Functional cooperativity in monomeric proteins. Archives of Biochemistry and Biophysics, 519, 91–102.10.1016/j.abb.2011.12.017
   PubMed Web of Science ®Google Scholar
• Easterbrook, J., Lu, C., Sakai, Y., & Li, A. P. (2001). Effects of organic solvents on the activities of cytochrome P450 isoforms, UDP-dependent glucuronyl transferase, and phenol sulfotransferase in human hepatocytes. Drug Metabolism and Disposition, 2, 141–144.
   Google Scholar
• Eftink, M. R. (1991). Fluorescence quenching reactions: Probing biological macromolecular structures. In T. G. Dewey (Ed.), Biophysical and biochemical aspects of fluorescence spectroscopy (pp. 1–41). New York, NY: Plenum.10.1007/978-1-4757-9513-4
   Google Scholar
• Eftink, M. R., & Ghiron, C. A. (1981). Fluorescence quenching studies with proteins. Analytical Biochemistry, 114, 199–227.10.1016/0003-2697(81)90474-7
   PubMed Web of Science ®Google Scholar
• Ekroos, M., & Sjogren, T. (2006). Structural basis for ligand promiscuity in cytochrome P450 3A4. Proceedings of the National Academy of Sciences, 103, 13682–13687.10.1073/pnas.0603236103
   PubMed Web of Science ®Google Scholar
• Fernando, H., Rumfeldt, J. A., Davydova, N. Y., Halpert, J. R., & Davydov, D. R. (2011). Multiple substrate-binding sites are retained in cytochrome P450 3A4 mutants with decreased cooperativity. Xenobiotica, 41, 281–289.10.3109/00498254.2010.538748
   PubMed Web of Science ®Google Scholar
• Förster, T. (1948). Intermolecular energy migration and fluorescence. Annals Physics, 2, 55–75.10.1002/(ISSN)1521-3889
   Web of Science ®Google Scholar
• Galetin, A., Clarke, S. E., & Houston, J. B. (2002). Quinidine and haloperidol as modifiers of CYP3A4 activity: Multisite kinetic model approach. Drug Metabolism and Disposition, 30, 1512–1522.10.1124/dmd.30.12.1512
   PubMed Web of Science ®Google Scholar
• Gillam, E. M., Baba, T., Kim, B. R., Ohmori, S., & Guengerich, F. P. (1993). Expression of modified human cytochrome P450 3A4 in Escherichia coli and purification and reconstitution of the enzyme. Archives of Biochemistry and Biophysics, 305, 123–131.10.1006/abbi.1993.1401
   PubMed Web of Science ®Google Scholar
• Gryczynski, I., Wiczk, W., Johnson, M. L., & Lakowicz, J. R. (1988). Lifetime distributions and anisotropy decays of indole fluorescence in cyclohexane/ethanol mixtures by frequency-domain fluorometry. Biophysical Chemistry, 32, 173–185.10.1016/0301-4622(88)87005-4
   PubMed Web of Science ®Google Scholar
• Guengerich, F. P. (1999). Cytochrome P-450 3A4: Regulation and role in drug metabolism. Annual Review of Pharmacology and Toxicology, 39, 1–17.10.1146/annurev.pharmtox.39.1.1
   PubMed Web of Science ®Google Scholar
• Guengerich, F. P. (2001). Common and uncommon cytochrome P450 reactions related to metabolism and chemical toxicity. Chemical Research in Toxicology, 14, 611–650.10.1021/tx0002583
   PubMed Web of Science ®Google Scholar
• Guengerich, F. P. (2006). A malleable catalyst dominates the metabolism of drugs. Proceedings of the National Academy of Sciences, 103, 13565–13566.10.1073/pnas.0606333103
   PubMed Web of Science ®Google Scholar
• Guengerich, F. P. (2015). Human cytochrome P450 enzymes. In P. R. Ortiz de Montellano (Ed.), Cytochrome P450: Structure, mechanism, and biochemistry (4th ed., Vol. 2, pp. 523–785). New York, NY: Springer.
   Google Scholar
• Guengerich, F. P., Martin, M. V., Sohl, C. D., & Cheng, Q. (2009). Measurement of cytochrome P450 and NADPH-cytochrome P450 reductase. Nature Protocols, 4, 1245–1251.10.1038/nprot.2009.121
   PubMed Web of Science ®Google Scholar
• Guengerich, F. P., & Munro, A. W. (2013). Unusual cytochrome P450 enzymes and reactions. Journal of Biological Chemistry, 288, 17065–17073.10.1074/jbc.R113.462275
   PubMed Web of Science ®Google Scholar
• Guengerich, F. P., Waterman, M. R., & Egli, M. (2016). Recent structural insights into cytochrome P450 function. Trends in Pharmacological Sciences, 37, 625–640.10.1016/j.tips.2016.05.006
   PubMed Web of Science ®Google Scholar
• Hays, M. D., Ryan, D. K., & Pennell, S. (2004). A modified multisite Stern−Volmer equation for the determination of conditional stability constants and ligand concentrations of soil fulvic acid with metal ions. Analytical Chemistry, 76, 848–854.10.1021/ac0344135
   PubMed Web of Science ®Google Scholar
• Hosea, N. A., Miller, G. P., & Guengerich, F. P. (2000). Elucidation of distinct ligand binding sites for cytochrome P450 3A4. Biochemistry, 39, 5929–5939.10.1021/bi992765t
   PubMed Web of Science ®Google Scholar
• Isin, E. M., & Guengerich, F. P. (2006). Kinetics and thermodynamics of ligand binding by cytochrome P450 3A4. Journal of Biological Chemistry, 281, 9127–9136.10.1074/jbc.M511375200
   PubMed Web of Science ®Google Scholar
• Isin, E. M., & Guengerich, F. P. (2007). Multiple sequential steps involved in the binding of inhibitors to cytochrome P450 3A4. The Journal of Biological Chemistry, 282, 6863–6874.
   PubMed Web of Science ®Google Scholar
• Isin, E. M., Sohl, C. D., Eoff, R. L., & Guengerich, F. P. (2008). Cooperativity of cytochrome P450 1A2: Interactions of 1,4-phenylene diisocyanide and 1-isopropoxy-4-nitrobenzene. Archives of Biochemistry and Biophysics, 473, 69–75. doi:10.1016/j.abb.2008.02.033
   PubMed Web of Science ®Google Scholar
• Kaur, P., Chamberlin, A. R., Poulos, T. L., & Sevrioukova, I. F. (2016). Structure-based inhibitor design for evaluation of a CYP3A4 pharmacophore model. Journal of Medicinal Chemistry, 59, 4210–4220.10.1021/acs.jmedchem.5b01146
   PubMed Web of Science ®Google Scholar
• Koley, A. P., Buters, J. T. M., Robinson, R. C., Markowitz, A., & Friedman, F. K. (1995). Co binding kinetics of human cytochrome P450 3A4: Specific interaction of substrates with kinetically distinguishable conformers. Journal of Biological Chemistry, 270, 5014–5018.10.1074/jbc.270.10.5014
   PubMed Web of Science ®Google Scholar
• Koley, A. P., Robinson, R. C., & Friedman, F. K. (1996). Cytochrome P450 conformation and substrate interactions as probed by CO binding kinetics. Biochimie, 78, 706–713.10.1016/S0300-9084(97)82528-X
   PubMed Web of Science ®Google Scholar
• Lakowicz, J. R. (2006). Principles of fluorescence spectroscopy (3rd ed., pp. 278–330). New York, NY: Springer.10.1007/978-0-387-46312-4
   Google Scholar
• Lampe, J. N., Fernandez, C., Nath, A., & Atkins, W. M. (2008). Nile red is a fluorescent allosteric substrate of cytochrome P450 3A4. Biochemistry, 47, 509–516.10.1021/bi7013807
   PubMed Web of Science ®Google Scholar
• Lehrer, S. S. (1971). Solute perturbation of protein fluorescence. Quenching of the tryptophyl fluorescence of model compounds and of lysozyme by iodide ion. Biochemistry, 10, 3254–3263.10.1021/bi00793a015
   PubMed Web of Science ®Google Scholar
• Lehrer, S. S., & Leavis, P. C. (1978). Solute quenching of protein fluorescence. Methods in Enzymology, 49, 222–236.10.1016/S0076-6879(78)49012-3
   PubMedGoogle Scholar
• Ménard, A., Huang, Y., Karam, P., Cosa, G., & Auclair, K. (2012). Site-specific fluorescent labeling and oriented immobilization of a triple mutant of CYP3A4 via C64. Bioconjugate Chemistry, 23, 826–836.10.1021/bc200672s
   PubMed Web of Science ®Google Scholar
• Nath, A., Fernández, C., Lampe, J. N., & Atkins, W. M. (2008). Spectral resolution of a second binding site for Nile Red on cytochrome P4503A4. Archives of Biochemistry and Biophysics, 474, 198–204.10.1016/j.abb.2008.03.017
   PubMed Web of Science ®Google Scholar
• Omura, T., & Sato, R. (1964). The carbon monoxide-binding pigment of liver microsomes. I. Evidence for its hemoprotein nature. The Journal of Biological Chemistry, 239, 2370–2378.
   PubMed Web of Science ®Google Scholar
• Roberts, A. G., Yang, J., Halpert, J. R., Nelson, S. D., Thummel, K. T., & Atkins, W. M. (2011). The structural basis for homotropic and heterotropic cooperativity of midazolam metabolism by human cytochrome P450 3A4. Biochemistry, 50, 10804–10818.10.1021/bi200924t
   PubMed Web of Science ®Google Scholar
• Seidel, C. A. M., Schulz, A., & Sauer, M. H. M. (1996). Nucleobase-specific quenching of fluorescent dyes. 1. Nucleobase one-electron redox potentials and their correlation with static and dynamic quenching efficiencies. The Journal of Physical Chemistry, 100, 5541–5553.10.1021/jp951507c
   Web of Science ®Google Scholar
• Sevrioukova, I. F., & Poulos, T. L. (2012). Interaction of human cytochrome P4503A4 with ritonavir analogs. Archives of Biochemistry and Biophysics, 520, 108–116.10.1016/j.abb.2012.02.018
   PubMed Web of Science ®Google Scholar
• Sevrioukova, I. F., & Poulos, T. L. (2013a). Dissecting cytochrome P450 3A4-ligand interactions using ritonavir analogues. Biochemistry, 52, 4474–4481.10.1021/bi4005396
   PubMed Web of Science ®Google Scholar
• Sevrioukova, I. F., & Poulos, T. L. (2013b). Understanding the mechanism of cytochrome P450 3A4: recent advances and remaining problems. Dalton Trans, 42, 3116–3126.10.1039/C2DT31833D
   PubMed Web of Science ®Google Scholar
• Sevrioukova, I. F., & Poulos, T. L. (2014). Ritonavir analogues as a probe for deciphering the cytochrome P450 3A4 inhibitory mechanism. Current Topics in Medicinal Chemistry, 14, 1348–1355.10.2174/1568026614666140506120647
   PubMed Web of Science ®Google Scholar
• Sevrioukova, I. F., & Poulos, T. L. (2015). Anion-dependent stimulation of CYP3A4 monooxygenase. Biochemistry, 54, 4083–4096.10.1021/acs.biochem.5b00510
   PubMed Web of Science ®Google Scholar
• Shimada, T., & Guengerich, F. P. (1989). Evidence for cytochrome P-450NF, the nifedipine oxidase, being the principal enzyme involved in the bioactivation of aflatoxins in human liver. Proceedings of the National Academy of Sciences, 86, 462–465.10.1073/pnas.86.2.462
   PubMed Web of Science ®Google Scholar
• Stryer, L., & Haugland, R. P. (1967). Energy transfer: A spectroscopic ruler. Proceedings of the National Academy of Sciences, 58, 719–726.10.1073/pnas.58.2.719
   PubMed Web of Science ®Google Scholar
• Sun, M., & Song, P.-S. (1977). Solvent effects on the fluorescent states of indole derivatives-dipole moments. Photochemistry and Photobiology, 25, 3–9.10.1111/php.1977.25.issue-1
   Web of Science ®Google Scholar
• Tsalkova, T. N., Davydova, N. Y., Halpert, J. R., & 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, 106–119.10.1021/bi061944p
   PubMed Web of Science ®Google Scholar
• Ueng, Y. F., Kuwabara, T., Chun, Y. J., & Guengerich, F. P. (1997). Cooperativity in oxidations catalyzed by cytochrome P450 3A4. Biochemistry, 36, 370–381.10.1021/bi962359z
   PubMed Web of Science ®Google Scholar
• Ueng, Y.-F., Shimada, T., Yamazaki, H., & Guengerich, F. P. (1995). Oxidation of aflatoxin B1 by bacterial recombinant human cytochrome P450 enzymes. Chemical Research in Toxicology, 8, 218–225.10.1021/tx00044a006
   PubMed Web of Science ®Google Scholar
• Vivian, J. T., & Callis, P. R. (2001). Mechanisms of tryptophan fluorescence shifts in proteins. Biophysical Journal, 80, 2093–2109.10.1016/S0006-3495(01)76183-8
   PubMed Web of Science ®Google Scholar
• Weber, G. (1960). Fluorescence-polarization spectrum and electronic-energy transfer in tyrosine, tryptophan and related compounds. Biochemical Journal, 75, 335–345.10.1042/bj0750335
   PubMed Web of Science ®Google Scholar
• Williams, P. A., Cosme, J., Vinkovic, D. M., Ward, A., Angove, H. C., Day, P. J., … Jhoti, H. (2004). Crystal structures of human cytochrome P450 3A4 bound to metyrapone and progesterone. Science, 305, 683–686.10.1126/science.1099736
   PubMed Web of Science ®Google Scholar
• Witherow, L. E., & Houston, J. B. (1999). Sigmoidal kinetics of CYP3A substrates: An approach for scaling dextromethorphan metabolism in hepatic microsomes and isolated hepatocytes to predict in vivo clearance in rat. Journal of Pharmacology and Experimental Therapeutics, 290, 58–65.
   PubMed Web of Science ®Google Scholar
• Woods, C. M., Fernandez, C., Kunze, K. L., & Atkins, W. M. (2011). Allosteric activation of cytochrome P450 3A4 by α-naphthoflavone: branch point regulation revealed by isotope dilution analysis. Biochemistry, 50, 10041–10051.10.1021/bi2013454
   PubMed Web of Science ®Google Scholar
• Yano, J. K., Wester, M. R., Schoch, G. A., Griffin, K. J., Stout, C. D., & Johnson, E. F. (2004). The structure of human microsomal cytochrome P450 3A4 determined by X-ray crystallography to 2.05 Å resolution. Journal of Biological Chemistry, 279, 38091–38094.10.1074/jbc.C400293200
   PubMed Web of Science ®Google Scholar
• Yoshida, M., Fujino, Y., Saito, K., & Doi, T. (2011). Regioselective synthesis of flavone derivatives via DMAP-catalyzed cyclization of o-alkynoylphenols. Tetrahedron, 67, 9993–9997.10.1016/j.tet.2011.09.063
   Web of Science ®Google Scholar