Cooperative binding of acetaminophen and caffeine within the P450 3A4 active site

Chemical Research in Toxicology

Volumn 20, Issue 10, 2007, Pages 1434-1441

  Cameron, Michael D ^a   Wen, Bo ^a   Roberts, Arthur G ^a   Atkins, William M ^a   Campbell, A Patricia ^a   Nelson, Sidney D ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAFFEINE; CYTOCHROME P450 3A4; GLUTATHIONE; HEME; LIPOSOME; PARACETAMOL; PROTON;

ARTICLE; DRUG OXIDATION; DRUG PROTEIN BINDING; ELECTRON SPIN RESONANCE; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME PURIFICATION; ESCHERICHIA COLI; MICHAELIS CONSTANT; NUCLEAR MAGNETIC RESONANCE; PROTEIN EXPRESSION;

ACETAMINOPHEN; ANALGESICS, NON-NARCOTIC; BINDING SITES; CAFFEINE; CENTRAL NERVOUS SYSTEM STIMULANTS; CYTOCHROME P-450 ENZYME SYSTEM; ESCHERICHIA COLI; GLUTATHIONE; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; OXIDATION-REDUCTION; RECOMBINANT PROTEINS;

ESCHERICHIA COLI;

EID: 35848962279     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx7000702     Document Type: Article

References (40)

1. Prescott, L. F. (1996) Paracetamol (Acetaminophen): A Critical Bibliographic Review. Taylor & Francis, London.
2. Nelson, S. D. and Bruschi, S. (2003) in Mechanisms of Acetaminophen-Induced Liver Disease. Drug-Induced Liver Disease (Kaplowitz, N., and DeLeve, L. D., Eds.) 1st ed., pp 287-326, Marcel Dekker, New York.
3. Raucy, J. L., Lasker, J. M., Lieber, C. S., and Black, M. (1989) Acetaminophen activation by human liver cytochromes P450IIE1 and P450IA2. Arch. Biochem. Biophys. 271, 270-283.
4. Patten, C. J., Thomas, P. E., Guy, R. L., Lee, M., Gonzalez, F. J., Guengerich, F. P., and Yang, C. S. (1993) Cytochrome P450 enzymes involved in acetaminophen activation by rat and human liver microsomes and their kinetics. Chem. Res. Toxicol. 6, 511-518.
5. Lee, S. S., Buters, J. T., Pineau, T., Femandez-Salguero, P., and Gonzalez, F. J. (1996) Role of CYP2E1 in the hepatotoxicity of acetaminophen. J. Biol. Chem. 271, 12063-12067.
6. Tonge, R. P., Kelly, E. J., Bruschi, S. A., Kalhorn, T., Eaton, D. L., Nebert, D. W., and Nelson, S. D. (1998) Role of CYP1A2 in the hepatotoxicity of acetaminophen: investigations using CYP1A2 null mice. Toxicol. Appl. Pharmacol. 153, 102-108.
7. Chen, W., Koenigs, L. L., Thompson, S. J., Peter, R. M., Rettie, A. E., Trager, W. F., and Nelson, S. D. (1998) Oxidation of acetaminophen to its toxic quinone imine and nontoxic catechol metabolites by baculovirus-expressed and purified human cytochromes P450 2E1 and 2A6. Chem. Res. Toxicol. 11, 295-301.
8. Dong, H., Haining, R. L., Thummel, K. E., Rettie, A. E., and Nelson, S. D. (2000) Involvement of human cytochrome P450 2D6 in the bioactivation of acetaminophen. Drug Metab. Dispos. 28, 1397-1400.
9. Thummel, K. E., Lee, C. A., Kunze, K. L., Nelson, S. D., and Slattery, J. T. (1993) Oxidation of acetaminophen to N-acetyl-p-aminobenzo-quinone imine by human CYP3A4. Biochem. Pharmacol. 45, 1563-1569.
10. Lee, C. A., Manyike, P. T., Thummel, K. E., Nelson, S. D., and Slattery, J. T. (1997) Mechanism of cytochrome P450 activation by caffeine and 7,8-benzoflavone in rat liver microsomes. Drug Metab. Dispos. 25, 1150-1156.
11. Li, Y., Wang, E., Patten, C. J., Chen, L., and Yang, C. S. (1994) Effects of flavonoids on cytochrome P450-dependent acetaminophen metabolism in rats and human liver microsomes. Drug Metab. Dispos. 22, 566-571.
12. 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.
13. 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.
14. 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.
15. 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.
16. Shou, M., Mei, Q., Ettore, M. W., Jr., Dai, R., Baillie, T. A., and Rushmore, T. H. (1999) Sigmoidal kinetic model for two co-operative substrate-binding sites in a cytochrome P450 3A4 active site: an example of the metabolism of diazepam and its derivatives. Biochem. J. 340, 845-853.
17. 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.
18. Yano, J. K., Wester, M. R., Schoch, G. A., Griffin, K. J., Stout, C. D., and Johnson, E. F. (2004) The structure of human microsomal cytochrome P450 3A4 determined by X-ray crystallography to 2.05-A resolution. J Biol. Chem. 279, 38091-38094.
19. 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.
20. Ha, H. R., Chen, J., Krahenbuhl, S., and Follath, F. (1996) Biotransformation of caffeine by cDNA-expressed human cytochromes P-450. Eur. J. Clin. Pharmacol. 49, 309-315.
21. Myers, T. G., Thummel, K. E., Kalhom, T. F., and Nelson, S. D. (1994) Preferred orientations in the binding of 4′-hydroxyacetanilide (acetaminophen) to cytochrome P450 1A1 and 2B1 isoforms as determined by 13C- and 15N-NMR relaxation studies. J. Med. Chem. 37, 860-867.
22. van de Straat, R., de Vries, J., de Boer, H. J., Vromans, R. M., and Vermeulen, N. P. (1987) Relationship between paracetamol binding to and its oxidation by two cytochromes P-450 isozymes: a proton nuclear magnetic resonance and spectrophotometric study. Xenobiotica 17, 1-9.
23. Regal, K. A., and Nelson, S. D. (2000) Orientation of caffeine within the active site of human cytochrome P450 1A2 based on NMR longitudinal (T1) relaxation measurements. Arch. Biochem. Biophys. 384, 47-58.
24. Hummel, M. A., Gannett, P. M., Aguilar, J. S., and Tracy, T. S. (2004) Effector-mediated alteration of substrate orientation in cytochrome P450 2C9. Biochemistry 43, 7207-7214.
25. Cameron, M. D., Wen, B., Allen, K. E., Roberts, A. G., Schuman, J. T., Campbell, A. P., Kunze, K. L., and Nelson, S. D. (2005) Cooperative binding of midazolam with testosterone and alpha-naphthoflavone within the CYP3A4 active site: a NMR Tl paramagnetic relaxation study. Biochemistry 44, 14143-14151.
26. Buettner, G. R. (1988) In the absence of catalytic metals ascorbate does not autoxidize at pH 7: ascorbate as a test for catalytic metals. J. Biochem. Biophys. Methods 16, 27-40.
27. Gillam, E. M., Baba, T., Kim, B. R., Ohmori, S., and Guengerich, F. P. (1993) Expression of modified human cytochrome P450 3A4 in Escherichia coli and purification and reconstitution of the enzyme. Arch. Biochem. Biophys. 305, 123-131.
28. Holmans, P. L., Shet, M. S., Martin-Wixtrom, C. A., Fisher, C. W., and Estabrook, R. W. (1994) The high-level expression in Escherichia coli of the membrane-bound form of human and rat cytochrome b5 and studies on their mechanism of function. Arch. Biochem. Biophys. 312, 554-565.
29. Shen, A. L., Christensen, M. J., and Kasper, C. B. (1991) NADPH-cytochrome P450 oxidoreductase. The role of cysteine 566 in catalysis and cofactor binding. J. Biol. Chem. 266, 19976-19980.
30. 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.
31. Harlow, G. R., and Halpert, J. R. (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. U.S.A. 95, 6636-6641.
32. Guengerich, F. P. (1983) Oxidation-reduction properties of rat liver cytochromes P-450 and NADPH-cytochrome p-450 reductase related to catalysis in reconstituted systems. Biochemistry 22, 2811-2820.
33. Piotto, M., Saudek, V., and Sklenar, V. (1992) Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR 2, 661-665.
34. Villafranca, J. J. (1989) Paramagnetic probes of macromolecules. Methods Enzymol. 177, 403-413.
35. Solomon, I. (1955) Relaxation processes in a system of two spins. Phys. Rev. 99, 559-565.
36. Modi, S., Primrose, W. U., Boyle, J. M., Gibson, C. F., Lian, L. Y., and Roberts, G. C. (1995) NMR studies of substrate binding to cytochrome P450 BM3: comparisons to cytochrome P450 cam. Biochemistry 34, 8982-8988.
37. Segel, I. H. (1975) Enzyme Kinetics: Behavior and Analysis of Rapid Equilibrium and Steady-State Enzyme Systems, John-Wiley & Sons, New York.
38. Domanski, T. L., Liu, J., Harlow, G. R., and Halpert, J. R. (1998) Analysis of four residues within substrate recognition site 4 of human cytochrome P450 3A4: role in steroid hydroxylase activity and alpha-naphthoflavone stimulation. Arch. Biochem. Biophys. 350, 223-232.
39. Harlow, G. R., and Halpert, J. R. (1997) Alanine-scanning mutagenesis of a putative substrate recognition site in human cytochrome P450 3A4. Role of residues 210 and 211 in flavonoid activation and substrate specificity. J. Biol. Chem. 272, 5396-5402.
40. 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.