Nile red is a fluorescent allosteric substrate of cytochrome P450 3A4

Biochemistry

Volumn 47, Issue 2, 2008, Pages 509-516

  Lampe, Jed N ^a   Fernandez, Cristina ^a   Nath, Abhinav ^a   Atkins, William M ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FLUORESCENT ALLOSTERIC SUBSTRATE; NILE RED;

CONCENTRATION (PROCESS); DRUG PRODUCTS; FLUORESCENCE; IRON; MASS SPECTROMETRY; METABOLISM;

PROTEINS;

CYTOCHROME P450 3A4; DRUG METABOLITE; FLUORESCENT DYE; HEME; IRON; ITRACONAZOLE; NILE RED; UNCLASSIFIED DRUG;

ALLOSTERISM; ARTICLE; BINDING AFFINITY; BINDING SITE; DIELECTRIC CONSTANT; ENZYME KINETICS; ENZYME SUBSTRATE COMPLEX; FLUORESCENCE SPECTROSCOPY; IN VITRO STUDY; LIGAND BINDING; MASS SPECTROMETRY; OXIDATION; PRIORITY JOURNAL; STEADY STATE;

ALLOSTERIC REGULATION; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYTOCHROME P-450 ENZYME SYSTEM; KINETICS; OXAZINES; OXIDATION-REDUCTION; SPECTROMETRY, FLUORESCENCE; SPECTROPHOTOMETRY, ULTRAVIOLET; SUBSTRATE SPECIFICITY; TIME FACTORS;

EID: 38849187174     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi7013807     Document Type: Article

References (48)

1. Ortiz de Montellano, P. R. (2005) Cytochrome P450: Structure, Mechanism, and Biochemistry, 3rd ed., Kluwer Academic/Plenum Publishers, New York.
2. Guengerich, F. P. (2002) Cytochrome P450 enzymes in the generation of commercial products, Nat. Rev. Drug Discovery 1, 359-366.
3. Verras, A., and Ortiz de Montellano, P. R. (2006) Protein dynamics and imidazole binding in cytochrome P450 enzymes, Biochem. Soc. Trans. 34, 1170-1172.
4. Johnson, E. F., and Stout, C. D. (2005) Structural diversity of human xenobiotic-metabolizing cytochrome P450 monooxygenases, Biochem. Biophys. Res. Commun. 338, 331-336.
5. Guengerich, F. P. (2006) Cytochrome P450s and other enzymes in drug metabolism and toxicity, AAPS J. 8, E101-E111.
6. Atkins, W. M. (2005) Non-Michaelis-Menten kinetics in cytochrome P450-catalyzed reactions, Annu. Rev. Pharmacol. Toxicol. 45, 291-310.
7. Shou, M. (2004) The impact of cytochrome P450 allosterism on pharmacokinetics and drug-drug interactions, Drug Discovery Today 9, 636-637.
8. Shou, M., Grogan, J., Mancewicz, J. A., Krausz, K. W., Gonzalez, F. J., Gelboin, H. V., and Korzekwa, K. R. (1994) Activation of CYP3A4: Evidence for the simultaneous binding of two substrates in a cytochrome P450 active site, Biochemistry 33, 6450-6455.
9. Korzekwa, K. R., Krishnamachary, N., Shou, M., Ogai, A., Parise, R. A., Rettie, A. E., Gonzalez, F. J., and Tracy, T. S. (1998) Evaluation of atypical cytochrome P450 kinetics with two-substrate models: Evidence that multiple substrates can simultaneously bind to cytochrome P450 active sites, Biochemistry 37, 4137-4147.
10. Wrighton, S. A., Campanile, C., Thomas, P. E., Maines, S. L., Watkins, P. B., Parker, G., Mendez-Picon, G., Haniu, M., Shively, J. E., Levin, W., et al. (1986) Identification of a human liver cytochrome P-450 homologous to the major isosafrole-inducible cytochrome P-450 in the rat, Mol. Pharmacol. 29, 405-410.
11. Schwab, G. E., Raucy, J. L., and Johnson, E. F. (1988) Modulation of rabbit and human hepatic cytochrome P-450-catalyzed steroid hydroxylations by α-naphthoflavone, Mol. Pharmacol. 33, 493-499.
12. Lampe, J. N., and Atkins, W. M. (2006) Time-resolved fluorescence studies of heterotropic ligand binding to cytochrome P450 3A4, Biochemistry 45, 12204-12215.
13. 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.
14. 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.
15. Isin, E. M., and Guengerich, F. P. (2006) Kinetics and thermodynamics of ligand binding by cytochrome P450 3A4, J. Biol. Chem. 281, 9127-9136.
16. Shou, M., Dai, R., Cui, D., Korzekwa, K. R., Baillie, T. A., and Rushmore, T. H. (2001) A kinetic model for the metabolic interaction of two substrates at the active site of cytochrome P450 3A4, J. Biol. Chem. 276, 2256-2262.
17. 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.
18. Dabrowski, M. J., Schrag, M. L., Wienkers, L. C., and Atkins, W. M. (2002) Pyrene-pyrene complexes at the active site of cytochrome P450 3A4: Evidence for a multiple substrate binding site, J. Am. Chem. Soc. 124, 11866-11867.
19. Khan, K. K., Liu, H., and Halpert, J. R. (2003) Homotropic versus heterotopic cooperativity of cytochrome P450eryF: A substrate oxidation and spectral titration study, Drug Metab. Dispos. 31, 356-359.
20. 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.
21. Koley, A. P., Buters, J. T., Robinson, R. C., Markowitz, A., and Friedman, F. K. (1995) CO binding kinetics of human cytochrome P450 3A4. Specific interaction of substrates with kinetically distinguishable conformers, J. Biol. Chem. 270, 5014-5018.
22. Davydov, D. R., Halpert, J. R., Renaud, J. P., and Hui Bon Hoa, G. (2003) Conformational heterogeneity of cytochrome P450 3A4 revealed by high pressure spectroscopy, Biochem. Biophys. Res. Commun. 312, 121-130.
23. 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.
24. He, Y. A., Gajiwala, K. S., Wu, M., Parge, H., Burke, B., Lee, C. A., and Wester, M. R. (2006) The crystal structure of human CYP3A4 in complex with testosterone, in Abstracts, 16th International Symposium on Microsomal Drug Oxidations (MDO 2006), p 114, Diamond Congress, Ltd., Budapest, Hungary.
25. 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.
26. Stortelder, A., Keizers, P. H., Oostenbrink, C., De Graaf, C., De Kruijf, P., Vermeulen, N. P., Gooijer, C., Commandeur, J. N., and Van der Zwan, G. (2006) Binding of 7-methoxy-4-(aminomethyl)-coumarin to wild-type and W128F mutant cytochrome P450 2D6 studied by time-resolved fluorescence spectroscopy, Biochem. J. 393, 635-643.
27. Omura, T., and Sato, R. (1962) A new cytochrome in liver microsomes, J. Biol. Chem. 237, 1375-1376.
28. Hill, A. V. (1913) XLVII. The combinations of haemoglobin with oxygen and with carbon monoxide, Biochem. J. 7, 471-480.
29. Rushmore, T. H., Reider, P. J., Slaughter, D., Assang, C., and Shou, M. (2000) Bioreactor systems in drug metabolism: Synthesis of cytochrome P450-generated metabolites, Metab. Eng. 2, 115-125.
30. Otey, C. R., Bandara, G., Lalonde, J., Takahashi, K., and Arnold, F. H. (2006) Preparation of human metabolites of propranolol using laboratory-evolved bacterial cytochromes P450, Biotechnol. Bioeng. 93, 494-499.
31. Parikh, A., Gillam, E. M., and Guengerich, F. P. (1997) Drug metabolism by Escherichia coli expressing human cytochromes P450, Nat. Biotechnol. 15, 784-788.
32. Jones, E., Oliphant, T., Peterson P., et al. (2001) SciPy: Open Source Scientific Tools for Python.
33. Mendes, P. (1993) GEPASI: A software package for modelling the dynamics, steady states and control of biochemical and other systems, Comput. Appl. Biosci. 9, 563-571.
34. Mendes, P. (1997) Biochemistry by numbers: Simulation of biochemical pathways with Gepasi 3, Trends Biochem. Sci. 22, 361-363.
35. Mendes, P., and Kell, D. (1998) Non-linear optimization of biochemical pathways: Applications to metabolic engineering and parameter estimation, Bioinformatics 14, 869-883.
36. Roberts, A. G., and Atkins, W. M. (2007) Energetics of heterotropic cooperativity between α-naphthoflavone and testosterone binding to CYP3A4, Arch. Biochem. Biophys. (in press).
37. Shaw, P. M., Hosea, N. A., Thompson, D. V., Lenius, J. M., and Guengerich, F. P. (1997) Reconstitution premixes for assays using purified recombinant human cytochrome P450, NADPH-cytochrome P450 reductase, and cytochrome b5, Arch. Biochem. Biophys. 348, 107-115.
38. Sackett, D. L., and Wolff, J. (1987) Nile red as a polarity-sensitive fluorescent probe of hydrophobic protein surfaces, Anal. Biochem. 167, 228-234.
39. Ruvinov, S. B., Yang, X. J., Parris, K. D., Banik, U., Ahmed, S. A., Miles, E. W., and Sackett, D. L. (1995) Ligand-mediated changes in the tryptophan synthase indole tunnel probed by nile red fluorescence with wild type, mutant, and chemically modified enzymes, J. Biol. Chem. 270, 6357-6369.
40. Brown, M. B., Miller, J. N., and Seare, N. J. (1995) An investigation of the use of nile red as a long-wavelength fluorescent probe for the study of α1-acid glycoprotein-drug interactions, J. Pharm. Biomed. Anal. 13, 1011-1017.
41. Santra, M. K., Banerjee, A., Krishnakumar, S. S., Rahaman, O., and Panda, D. (2004) Multiple-probe analysis of folding and unfolding pathways of human serum albumin. Evidence for a framework mechanism of folding, Eur. J. Biochem. 271, 1789-1797.
42. Polverini, E., Cugini, G., Annoni, F., Abbruzzetti, S., Viappiani, C., and Gensch, T. (2006) Molten globule formation in apomyoglobin monitored by the fluorescent probe Nile Red, Biochemistry 45, 5111-5121.
43. Hungerford, G., Rei, A., and Ferreira, M. I. (2005) Studies on the interaction of Nile red with horseradish peroxidase in solution, FEBS J. 272, 6161-6169.
44. Sackett, D. L., Knutson, J. R., and Wolff, J. (1990) Hydrophobic surfaces of tubulin probed by time-resolved and steady-state fluorescence of nile red, J. Biol. Chem. 265, 14899-14906.
45. Pearson, J. T., Hill, J. J., Swank, J., Isoherranen, N., Kunze, K. L., and Atkins, W. M. (2006) Surface plasmon resonance analysis of antifungal azoles binding to CYP3A4 with kinetic resolution of multiple binding orientations, Biochemistry 45, 6341-6353.
46. Kunze, K. L., Nelson, W. L., Kharasch, E. D., Thummel, K. E., and Isoherranen, N. (2006) Stereochemical aspects of itraconazole metabolism in vitro and in vivo, Drug Metab. Dispos. 34, 583-590.
47. Locuson, C. W., Hutzler, J. M., and Tracy, T. S. (2007) Visible spectra of type II cytochrome P450-drug complexes: Evidence that "incomplete" heme coordination is common, Drug Metab. Dispos. 35, 614-622.
48. Fernando, H., Halpert, J. R., and Davydov, D. R. (2006) Resolution of multiple substrate bindingsites in cytochrome P450 3A4: The stoichiometry of the enzyme-substrate complexes probed by FRET and Job's titration, Biochemistry 45, 4199-4209.