An electrostatically driven conformational transition is involved in the mechanisms of substrate binding and cooperativity in cytochrome P450eryF

Biochemistry

Volumn 43, Issue 21, 2004, Pages 6475-6485

  Davydov, Dmitri R ^a   Botchkareva, Alexandra E ^a   Kumar, Santosh ^a   He, You Qun ^a   Halpert, James R ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOLS; CONFORMATIONS; DISSOCIATION; ELECTROSTATICS; IONIC STRENGTH; PIGMENTS;

CYTOCHROMES;

BIOCHEMICAL ENGINEERING;

1 PYRENEBUTANOL; 7 (DIETHYLAMINO) 3 (4' MALEIMIDYLPHENYL) 4 METHYLCOUMARIN; ARGININE; ASPARTIC ACID; BUTANOL; COUMARIN DERIVATIVE; CYSTEINE; CYTOCHROME P450; CYTOCHROME P450 ERYF; GLUTAMIC ACID; HEME DERIVATIVE; ISOLEUCINE; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SUBSTITUTION; ARTICLE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; DISSOCIATION; ELECTRICITY; ENZYME SUBSTRATE COMPLEX; FLUORESCENCE RESONANCE ENERGY TRANSFER; HELIX D; HELIX E; HELIX F; HELIX G; HYDRATION; IONIC STRENGTH; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN INTERACTION; PROTEIN MODIFICATION; SPIN TRAPPING;

ALLOSTERIC SITE; AMINO ACID SUBSTITUTION; BINDING SITES; CYSTEINE; CYTOCHROME P-450 ENZYME SYSTEM; ELECTROSTATICS; FLUORESCENCE RESONANCE ENERGY TRANSFER; GLUTAMIC ACID; HEME; MIXED FUNCTION OXYGENASES; OSMOLAR CONCENTRATION; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; PYRENES;

EID: 2542623028     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi036260l     Document Type: Article

References (70)

1. Makris, T. M., Davydov, R., Denisov, I. G., Hoffman, B. M., and Sligar, S. G. (2002) Mechanistic enzymology of oxygen activation by the cytochromes P450, Drug Metab. Rev. 34, 691-708.
2. Atkins, W. M., and Sligar, S. G. (1990) Tyrosine-96 as a natural spectroscopic probe of the cytochrome P-450cam active site, Biochemistry 29, 1271-1275.
3. Raag, R., and Poulos, T. L. (1991) Crystal structures of cytochrome P-450CAM complexed with camphane, thiocamphor, and adamantane: factors controlling P-450 substrate hydroxylation, Biochemistry 30, 2674-2684.
4. Gerber, N. C., and Sligar, S. G. (1994) A role for Asp-251 in cytochrome P-450cam oxygen activation, J. Biol. Chem. 269, 4260-4266.
5. Loida, P. J., and Sligar, S. G. (1993) Molecular recognition in cytochrome P-450: mechanism for the control of uncoupling reactions, Biochemistry 32, 11530-11538.
6. Deprez, E., Gerber, N. C., Di Primo, C., Douzou, P., Sligar, S. G., and Hui Bon Hoa, G. (1994) Electrostatic control of the substrate access channel in cytochrome P-450cam, Biochemistry 33, 14464-14468.
7. Li, H. Y., Narasimhulu, S., Havran, L. M., Winkler, J. D., and Poulos, T. L. (1995) Crystal structure of cytochrome P450(cam) complexed with its catalytic product, 5-exo-hydroxycamphor, J. Am. Chem. Soc. 117, 6297-6299.
8. Schlichting, I., Berendzen, J., Chu, K., Stock, A. M., Maves, S. A., Benson, D. E., Sweet, B. M., Ringe, D., Petsko, G. A., and Sligar, S. G. (2000) The catalytic pathway of cytochrome P450cam at atomic resolution, Science 287, 1615-1622.
9. Di Primo, C., Deprez, E., Hui Bon Hoa, G., and Douzou, P. (1995) Antagonistic effects of hydrostatic pressure and osmotic pressure on cytochrome P-450(cam) spin transition, Biophys. J. 68, 2056-2061.
10. Poulos, T. L., Finzel, B. C., and Howard, A. J. (1987) High-resolution crystal structure of cytochrome P450cam, J. Mol. Biol. 195, 687-700.
11. Prasad, S., and Mitra, S. (2002) Role of protein and substrate dynamics in catalysis by Pseudomonas putida cytochrome P450(cam), Biochemistry 41, 14499-14508.
12. Schulze, H., Hui Bon Hoa, G., Helms, V., Wade, R. C., and Jung, C. (1996) Structural changes in cytochrome P-450cam effected by the binding of the enantiomers (1R)-camphor and (1S)-camphor, Biochemistry 35, 14127-14138.
13. Lounnas, V., and Wade, R. C. (1997) Exceptionally stable salt bridges in cytochrome P450cam have functional roles, Biochemistry 36, 5402-5417.
14. Deprez, E., Di Primo, C., Hui Bon Hoa, G., and Douzou, P. (1994) Effects of monovalent cations on cytochrome-P-450 camphor-evidence for preferential binding of potassium, FEBS Lett. 347, 207-210.
15. Deprez, E., Gill, E., Helms, V., Wade, R. C., and Hui Bon Hoa, G. (2002) Specific and nonspecific effects of potassium cations on substrate-protein interactions in cytochromes P450cam and P450lin, J. Inorg. Biochem. 91, 597-606.
16. Di Primo, C., Deprez, E., Sligar, S. G., and Hui Bon Hoa, G. (1997) Origin of the photoacoustic signal in cytochrome P-450(cam): Role of the Arg186-Asp251-Lys178 bifurcated salt bridge, Biochemistry 36, 112-118.
17. Kuthan, H., and Ullrich, V. (1982) Oxidase and oxygenase function of the microsomal cytochrome P450 monooxygenase system, Eur. J. Biochem. 126, 583-588.
18. Gorsky, L. D., Koop, D. R., and Coon, M. J. (1984) On the stoichiometry of the oxidase and monooxygenase reactions catalyzed by liver microsomal cytochrome P-450. Products of oxygen reduction, J. Biol. Chem. 259, 6812-6817.
19. Zhukov, A. A., and Archakov, A. I. (1985) Stoichiometry of microsomal oxidation reactions. Distribution of redox-equivalents in monooxygenase and oxidase reactions catalyzed by cytochrome P-450, Biochemistry (Moscow) 50, 1659-1672.
20. Mansuy, D., Carlier, M., Bertrand, J. C., and Azoulay, E. (1980) Spectral characterization of cytochrome P-450 of a strain of Candida tropicalis grown on tetradecane, Eur. J. Biochem. 109, 103-108.
21. Yun, C. H., Ahn, T., and Guengerich, F. P. (1998) Conformational change and activation of cytochrome P450 2B1 induced by salt and phospholipid, Arch. Biochem. Biophys. 356, 229-238.
22. Yun, C. H., Song, M., and Kim, H. (1997) Conformational change of cytochrome P450 1A2 induced by phospholipids and detergents, J. Biol. Chem. 272, 19725-19730.
23. Gemzik, B., Halvorson, M. R., and Parkinson, A. (1990) Pronounced and differential effects of ionic strength and pH on testosterone oxidation by membrane-bound and purified forms of rat liver microsomal cytochrome P-450, J. Steroid Biochem. 35, 429-440.
24. 5 in the process, Arch. Biochem. Biophys. 314, 234-241.
25. Harlow, G. R., and Halpert, J. R. (1996) Mutagenesis study of Asp-290 in cytochrome P450 2B11 using a fusion protein with rat NADPH-cytochrome P450 reductase, Arch. Biochem. Biophys. 326, 85-92.
26. Guengerich, F. P. (1999) Cytochrome P-450 3A4: regulation and role in drug metabolism, Annu. Rev. Pharmacol. Toxicol. 39, 1-17.
27. Hosea, N. A., Miller, G. P., and Guengerich, F. P. (2000) Elucidation of distinct ligand binding sites for cytochrome P450 3A4, Biochemistry 39, 5929-5939.
28. Houston, J. B., and Kenworthy, K. E. (2000) In vitro-in vivo scaling of CYP kinetic data not consistent with the classical Michaelis-Menten model, Drug Metab. Dispos. 28, 246-254.
29. Shou, M. G., 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.
30. Miller, G. P., and Guengerich, F. P. (2000) A simple Michaelis-Menten scheme fails to describe the demethylation of p-nitroanisole by rabbit liver P450 1A2, FASEB J. 14, A1435-A1435.
31. Miller, G. P., and Guengerich, F. P. (2001) Binding and oxidation of alkyl 4-nitrophenyl ethers by rabbit cytochrome P450 1A2: Evidence for two binding sites, Biochemistry 40, 7262-7272.
32. Ekins, S., Ring, B. J., Binkley, S. N., Hall, S. D., and Wrighton, S. A. (1998) Autoactivation and activation of the cytochrome P450s, Int. J. Clin. Pharm. Ther. 36, 642-651.
33. 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.
34. Hutzler, J. M., Hauer, M. J., and Tracy, T. S. (2001) Dapsone activation of CYP2C9-mediated metabolism: Evidence for activation of multiple substrates and a two-site model, Drug Metab. Dispos. 29, 1029-1034.
35. Hutzler, J. M., Wienkers, L. C., Wahlstrom, J. L., Carlson, T. J., and Tracy, T. S. (2003) Activation of cytochrome P450 2C9-mediated metabolism: mechanistic evidence in support of kinetic observations, Arch. Biochem. Biophys. 410, 16-24.
36. Ariyoshi, N., Miyazaki, M., Toide, K., Sawamura, Y., and Kamataki, T. (2001) A single nucleotide polymorphism of CYP2B6 found in Japanese enhances catalytic activity by autoactivation, Biochem. Biophys. Res. Commun. 281, 1256-1260.
37. Kiselev, P. A., Garda, G., Finch, S. A., Stir, A., Khatyleva, S. I., and Akhrem, A. A. (1990) Regulation of the catalytic activity of the monooxygenase enzyme system depending of the substrate structure and phospholipid composition of the model membrane, Biochemistry (Moscow) 55, 1535-1544.
38. Cupp-Vickery, J., Anderson, R., and Hatziris, Z. (2000) Crystal structures of ligand complexes of P450eryF exhibiting homotropic cooperativity, Proc. Natl. Acad. Sci. U.S.A. 97, 3050-3055.
39. Khan, K. K., He, Y. A., He, Y. Q., and Halpert, J. R. (2002) Site-directed mutagenesis of cytochrome P450eryF: Implications for substrate oxidation, cooperativity, and topology of the active site, Chem. Res. Toxicol. 15, 843-853.
40. 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.
41. 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.
42. Williams, P. A., Cosme, J., Ward, A., Agnove, H. C., Vinkovic, D. M., and Jhoti, H. (2003) Crystal structure of human cytochrome P450 2C9 with bound warfarin, Nature 424, 464-468.
43. He, Y. A., Roussel, F., and Halpert, J. R. (2003) Analysis of homotropic and heterotropic cooperativity of diazepam oxidation, Arch. Biochem. Biophys. 409, 92-101.
44. Atkins, W. M., Wang, R. W., and Lu, A. Y. H. (2001) Allosteric behavior in cytochrome P450-dependent in vitro drug-drug interactions: A prospective based on conformational dynamics, Chem. Res. Toxicol. 14, 338-347.
45. Shou, M. (2002) Kinetic analysis for multiple substrate interaction at the active site of cytochrome P450, in Methods in Enzymology, pp 261-276, Academic Press, New York.
46. Helms, V., Deprez, E., Gill, E., Barret, C., Hui Bon Hoa, G., and Wade, R. C. (1996) Improved binding of cytochrome P450cam substrate analogues designed to fill extra space in the substrate binding pocket, Biochemistry 35, 1485-1499.
47. Wade, R. C., Gabdoulline, R. R., Ludemann, S. K., and Lounnas, V. (1998) Electrostatic steering and ionic tethering in enzyme-ligand binding-Insights from Simulations, Proc. Natl. Acad. Sci. U.S.A. 95, 5942-5949.
48. Davydov, D. R., Knyushko, T. V., Kanaeva, I. P., Koen, Y. M., Samenkova, N. F., Archakov, A. I., and Hui Bon Hoa, G. (1996) Interactions of cytochrome P450 2B4 with NADPH-cytochrome P450 reductase studied by fluorescent probe, Biochimie 78, 734-743.
49. Molecular Probes Inc. (2003) http://www.probes.com/servlets/datatable?item=244&id=28833.
50. Johnson, W. C. (1999) Analyzing protein circular dichroism spectra for accurate secondary structures, Proteins 35, 307-312.
51. Provencher, S. W., and Glockner, J. (1981) Estimation of globular protein secondary structure from circular dichroism, Biochemistry 20, 33-37.
52. Davydov, D. R., Deprez, E., Hui Bon Hoa, G., 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.
53. Renaud, J. P., Davydov, D. R., Heirwegh, K. P. M., Mansuy, D., and Hui Bon Hoa, G. (1996) Thermodynamic studies of substrate binding and spin transitions in human cytochrome P-450 3A4 expressed in yeast microsomes, Biochem. J. 319, 675-681.
54. Yun, C. H., Song, M., Ahn, T., and Kim, H. (1996) Conformational change of cytochrome P450 1A2 induced by sodium chloride, J. Biol. Chem. 271, 31312-31316.
55. Cupp-Vickery, J. R., Garcia, C., Hofacre, A., and Mcgee-Estrada, K. (2001) Ketoconazole-induced conformational changes in the active site of cytochrome P450eryF, J. Mol. Biol. 311, 101-110.
56. Cupp-Vickery, J. R., Li, H., and Poulos, T. L. (1994) Preliminary crystallographic analysis of an enzyme involved in erythromycin biosynthesis: cytochrome P450eryF, Proteins 20, 197-201.
57. Cupp-Vickery, J. R., and Poulos, T. L. (1997) Structure of cytochrome P450eryF: substrate, inhibitors, and model compounds bound in the active site, Steroids 62, 112-116.
58. Kornblatt, J. A., and Kornblatt, M. J. (2002) Water as it applies to the function of enzymes, Int. Rev. Cytol. 215, 49-73.
59. Hlavica, P., Schulze, J., and Lewis, D. F. V. (2003) Functional interaction of cytochrome P450 with its redox partners: a critical assessment and update of the topology of predicted contact regions, J. Inorg. Biochem. 96, 279-297.
60. Gotoh, O. (1992) Substrate recognition sites in cytochrome P450 family 2 (CYP2) proteins inferred from comparative analyses of amino acid and coding nucleotide sequences, J. Biol. Chem. 267, 83-90.
61. Domanski, T. L., and Halpert, J. R. (2001) Analysis of mammalian cytochrome P450 structure and function by site-directed mutagenesis, Curr. Drug Metab. 2, 117-137.
62. Williams, P. A., Cosme, J., Sridhar, V., Johnson, E. F., and Mcree, D. E. (2000) Mammalian microsomal cytochrome P450 monooxygenase: Structural adaptations for membrane binding and functional diversity, Mol. Cell 5, 121-131.
63. Wester, M. R., Johnson, E. F., Marques-Soares, C., Dijols, S., Dansette, P. M., Mansuy, D., and Stout, C. D. (2003) Structure of mammalian cytochrome P450 2C5 complexed with diclofenac at 2.1 Å resolution: evidence for an induced fit model of substrate binding, Biochemistry 42, 9335-9345.
64. 5 binding to the terminal hemoprotein, J. Biol. Chem. 258, 13444-13452.
65. Gibson, G. G., and Tamburini, P. P. (1984) Cytochrome P-450 spin state: inorganic biochemistry of haem iron ligation and functional significance, Xenobiotica 14, 27-47.
66. Bosterling, B., and Trudell, J. R. (1982) Association of cytochrome b5 and cytochrome P-450 reductase with cytochrome P-450 in the membrane of reconstituted vesicles, J. Biol. Chem. 257, 4783-4787.
67. Winn, P. J., Ludemann, S. K., Gauges, R., Lounnas, V., and Wade, R. C. (2002) Comparison of the dynamics of substrate access channels in three cytochrome P450s reveals different opening mechanisms and a novel functional role for a buried arginine, Proc. NatL Acad. Sci. U.S.A. 99, 5361-5366.
68. Sligar, S. G. (1976) Coupling of spin, substrate, and redox equilibria in cytochrome P450, Biochemistry 15, 5399-5406.
69. Davydov, D. R., Hui Bon Hoa, G., and Peterson, J. A. (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.
70. Helms, V., and Wade, R. C. (1995) Thermodynamics of water mediating protein-ligand interactions in cytochrome P450cam: a molecular dynamics study, Biophys. J. 3, 810-824.