Resolution of two substrate-binding sites in an engineered cytochrome P450eryF bearing a fluorescent probe

Biophysical Journal

Volumn 89, Issue 1, 2005, Pages 418-432

  Davydov, Dmitri R ^a   Botchkareva, Alexandra E ^a,b   Davydova, Nadezhda E ^a   Halpert, James R ^a  

^a University of Texas Medical Branch School of Medicine   (United States)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

1 PYRENEBUTANOL; CYSTEINE; CYTOCHROME P450; CYTOCHROME P450ERYF; FLUORESCENT DYE; SERINE PROTEINASE; UNCLASSIFIED DRUG;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; CONFORMATIONAL TRANSITION; COOPERATIVE BINDING; ENZYME ACTIVE SITE; ENZYME ENGINEERING; ENZYME SUBSTRATE COMPLEX; FLUORESCENCE RESONANCE ENERGY TRANSFER; IONIC STRENGTH; NONHUMAN; SITE DIRECTED MUTAGENESIS;

EID: 23244465885     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.104.058479     Document Type: Article

References (49)

1. Ekins, S., D. M. Stresser, and J. A. Williams. 2003. In vitro and pharmacophore insights into CYP3A enzymes. Trends Pharmacol. Sci. 24:161-166.
2. Guengerich, F. P. 1999. Cytochrome P-450 3A4: regulation and role in drug metabolism. Annu. Rev. Pharmacol. Toxicol. 39:1-17.
3. Lin, Y., P. Lu, C. Tang, Q. Mei, G. Sandig, A. D. Rodrigues, T. H. Rushmore, and M. Shou. 2001. Substrate inhibition kinetics for cytochrome P450-catalyzed reactions. Drug Metab. Dispos 29:368-374.
4. Tang, W., and R. A. Stearns. 2001. Heterotropic cooperativity of cytochrome P450 3A4 and potential drug-drug interactions. Curr. Drug Metab. 2:185-198.
5. Shou, M., J. Grogan, J. A. Mancewicz, K. W. Krausz, F. J. Gonzalez, H. V. Gelboin, and K. R. Korzekwa. 1994. Activation of CYP3A4 - evidence for the simultaneous binding of 2 substrates. Biochemistry. 33:6450-6455.
6. Korzekwa, K. R., N. Krishnamachary, M. Shou, A. Ogai, R. A. Parise, A. E. Rettie, F. J. Gonzalez, and T. S. Tracy. 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.
7. Ueng, Y. F., T. Kuwabara, Y. J. Chun, and F. P. Guengerich. 1997. Cooperativity in oxidations catalyzed by cytochrome P450 3A4. Biochemistry. 36:370-381.
8. Harlow, G. R., and J. R. Halpert. 1998. Analysis of human cytochrome P450 3A4 cooperativity: construction and characterization of a site-directed mutant that displays hyperbolic steroid hydroxylation kinetics. Proc. Natl. Acad. Sci. USA. 95:6636-6641.
9. Schrag, M. L., and L. C. Wienkers. 2000. Topological alteration of the CYP3A4 active site by the divalent cation Mg2+. Drug Metab. Dispos. 28:1198-1201.
10. Atkins, W. M., R. W. Wang, and A. Y. H. Lu. 2001. Allosteric behavior in cytochrome P450-dependent in vitro drug-drug interactions: A prospective based on conformational dynamics. Chem. Res. Toxicol. 14:338-347.
11. Davydov, D. R., J. R. Halpert, J. P. Renaud, and G. Hui Bon Hoa. 2003. Conformational heterogeneity of cytochrome P450 3A4 revealed by high pressure spectroscopy. Biochem. Biophys. Res. Commun. 312:121-130.
12. Davydov, D. R., A. E. Botchkareva, S. Kumar, Y. Q. He, and J. R. Halpert. 2004. An electrostatically driven conformational transition is involved in the mechanisms of substrate binding and cooperativity in cytochrome P450eryF. Biochemistry. 43:6475-6485.
13. Schoch, G. A., J. K. Yano, M. R. Wester, K. J. Griffin, C. D. Stout, and E. F. Johnson. 2004. Structure of human microsomal cytochrome P4502C8 - Evidence for a peripheral fatty acid binding site. J. Biol. Chem. 279:9497-9503.
14. Williams, P. A., J. Cosme, D. M. Vinkovic, A. Ward, H. C. Angove, P. J. Day, C. Vonrhein, I. J. Tickle, and H. Jhoti. 2004. Crystal structures of human cytochrome P450 3A4 bound to metyrapone and progesterone. Science. 305:683-686.
15. Hosea, N. A., G. P. Miller, and F. P. Guengerich, 2000. Elucidation of distinct ligand binding sites for cytochrome P450 3A4. Biochemistry. 39:5929-5939.
16. Boek-Dohalska, L., P. Hodek, M. Sulc, and M. Stiborova. 2001. alpha-naphthoflavone acts as activator and reversible or irreversible inhibitor of rabbit microsomal CYP3A6. Chem. Biol. Interact. 138:85-106.
17. Galetin, A., S. E. Clarke, and J. B. Houston. 2003. Multisite kinetic analysis of interactions between prototypical CYP3A4 subgroup substrates: Midazolam, testosterone, and nifedipine. Drug Metab. Dispos. 31:1108-1116.
18. He, Y. A., F. Roussel, and J. R. Halpert. 2003. Analysis of homotropic and heterotropic cooperativity of diazepam oxidation. Arch. Biochem. Biophys. 409:92-101.
19. Koley, A. P., J. T. M. Buters, R. C. Robinson, A. Markowitz, and F. K. Friedman. 1997. Differential mechanisms of cytochrome P450 inhibition and activation by alpha-naphthoflavone. J. Biol. Chem. 272:3149-3152.
20. Koley, A. P., R. C. Robinson, A. Markowitz, and F. K. Friedman. 1997. Drug-drug interactions: effect of quinidine on nifedipine binding to human cytochrome P450 3A4. Biochem. Pharmacol. 53:455-460.
21. Koley, A. P., J. T. M. Buters, R. C. Robinson, A. Markowitz, and F. K. Friedman. 1996. Cytochrome P450 conformation and substrate interactions as probed by CO binding kinetics. Biochimie. 78:706-713.
22. 5. J. Inorg. Biochem. 93:152-160.
23. Hlavica, P., and D. F. V. Lewis. 2001. Allosteric phenomena in cytochrome P450-catalyzed monooxygenations. Eur. J. Biochem. 268:4817-4832.
24. Blanck, J., O. Ristau, A. A. Zhukov, A. I. Archakov, H. Rein, and K. Ruckpaul. 1991. Cytochrome P-450 spin state and leakiness of the monooxygenase pathway. Xenobiotica. 21:121-135.
25. Rein, H., O. Ristau, R. Misselwitz, E. Buder, and K. Ruckpaul. 1979. The importance of the spin equilibrium in cytochrome P-450 for the reduction rate of the heme iron. Acta Biol. Med. Ger. 38:187-200.
26. Sligar, S. G., D. L. Cinti, G. G. Gibson, and J. B. Schenkman. 1979. Spin state control of the hepatic cytochrome P450 redox potential. Biochem. Biophys. Res. Commun. 90:925-932.
27. Sligar, S. G. 1976. Coupling of spin, substrate, and redox equilibria in cytochrome P450. Biochemistry. 15:5399-5406.
28. Cupp-Vickery, J. R., C. Garcia, A. Hofacre, and K. McGee-Estrada. 2001. Ketoconazole-induced conformational changes in the active site of cytochrome P450eryF. J. Mol. Biol. 311:101-110.
29. Davydov, D. R., S. Kumar, and J. R. Halpert. 2002. Allosteric mechanisms in P450eryF probed with 1-pyrenebutanol, a novel fluorescent substrate. Biochem. Biophys. Res. Commun. 294:806-812.
30. Khan, K. K., H. Liu, and J. R. Halpert. 2003. Homotropic versus heterotropic cooperativity of cytochrome P450eryF: A substrate oxidation and spectral titration study. Drug Metab. Dispos. 31:356-359.
31. Khan, K. K., and J. Halpert. 2002. 7-benzyloxyquinoline oxidation by P450eryF A245T: Finding of a new fluorescent substrate probe. Chem. Res. Toxicol. 15:806-814.
32. Xiang, H., R. A. Tschirret-Guth, and P. R. Ortiz De Montellano. 2000. An A245T mutation conveys on cytochrome P450eryF the ability to oxidize alternative substrates. J. Biol. Chem. 275:35999-36006.
33. Baas, B. J., I. G. Denisov, and S. G. Sligar. 2004. Homotropic cooperativity of monomeric cytochrome P450 3A4 in a nanoscale native bilayer environment. Arch. Biochem. Biophys. 430:218-228.
34. Yoon, M. Y., A. P. Campbell, and W. M. Atkins. 2004. " Allosterism" in the elementary steps of the cytochrome P450 reaction cycle. Drug Metab. Rev. 36:219-230.
35. Davydov, D. R., G. Hui Bon Hoa, and J. A. Peterson. 1999. Dynamics of protein-bound water in the heme domain of P450BM3 studied by high-pressure spectroscopy: Comparison with P450cam and P450 2B4. Biochemistry. 38:751-761.
36. Hui Bon Hoa, G., M. A. Mclean, and S. G. Sligar. 2002. High pressure, a tool for exploring heme protein active sites. Biochim. Biophys. Acta. 1595:297-308.
37. Kornblatt, J. A., and M. J. Komblatt. 2002. The effects of osmotic and hydrostatic pressures on macromolecular systems. Biochim. Biophys. Acta. 1595:30-47.
38. Davydov, D. R., E. Deprez, G. Hui Bon Hoa, T. V. Knyushko, G. P. Kuznetsova, Y. M. Koen, and A. I. Archakov. 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.
39. Molecular Probes, Inc. 2003. Handbook of Fluorescent Probes and Research Products. Web edition: http://www.probes.com/handbook/. Molecular Probes, Eugene, OR.
40. Renaud, J. P., D. R. Davydov, K. P. M. Heirwegh, D. Mansuy, and G. Hui Bon Hoa. 1996. Thermodynamic studies of substrate binding and spin transitions in human cytochrome P-450 3A4 expressed in yeast microsomes. Biochem. J. 319:675-681.
41. Peyser, Y. M., K. Ajtai, T. P. Burghardt, and A. Muhlrad. 2001. Effect of ionic strength on the conformation of myosin subfragment 1-nucleotide complexes. Biophys. J. 81:1101-1114.
42. Segel, I. H. 1975. Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady-State Enzyme Systems. Wiley-Interscience, New York.
43. Radzicka, A., and R. Wolfenden. 1988. Comparing the polarities of the amino acids: Side-chain distribution coefficients between the vapor phase, cyclohexane, 1-octanol, and neutral aqueous solution. Biochemistry. 27:1664-1670.
44. Zimmerman, J. M., N. Eliezer, and R. Simha. 1968. The characterization of amino acid sequences in proteins by statistical methods. J. Theor. Biol. 21:170-201.
45. Cupp-Vickery, J. R., and T. L. Poulos. 1995. Structure of cytochrome P450eryF involved in erythromycin biosynthesis. Nat. Struct. Biol. 2:144-153.
46. Cupp-Vickery, J., R. Anderson, and Z. Hatziris. 2000. Crystal structures of ligand complexes of P450eryF exhibiting homotropic cooperativity. Proc. Natl. Acad. Sci. USA. 97:3050-3055.
47. Krepps, M. K., S. Parkin, and D. A. Atwood. 2001. Hydrogen bonding with sulfur. Cryst. Growth Design. 1:291-297.
48. Pal, D., and P. Chakrabarti. 1999. Different types of interactions involving cysteine sulfhydryl group in proteins. J. Biomol. Struct. Dyn. 15:1059-1072.
49. Adman, E., K. D. Watenpaugh, and L. H. Jensen. 1975. NH...S hydrogen-bonds in Peptococcus aerogenes ferredoxin, Clostridium pasteurianum rubredoxin, and Chromatium high potential iron protein. Proc. Natl. Acad. Sci. USA. 72:4854-4858.