Human cytochrome P450 1A1 structure and utility in understanding drug and xenobiotic metabolism

Journal of Biological Chemistry

Volumn 288, Issue 18, 2013, Pages 12932-12943

  Walsh, Agnes A ^a   Szklarz, Grazyna D ^b   Scott, Emily E ^a  

^a UNIVERSITY OF KANSAS   (United States)

^b WEST VIRGINIA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BENZO [A] PYRENE; CYTOCHROME P450; DOCKING STUDIES; ENVIRONMENTAL POLLUTANTS; FUNCTIONAL SIMILARITY; HUMAN CYTOCHROME; STRUCTURAL BASIS; XENOBIOTIC METABOLISM;

ENZYMES; PHYSIOLOGY; PYRENE;

METABOLISM;

ALPHA NAPHTHOFLAVONE; BENZOCHROMEN 4 ONE; CHROMENE DERIVATIVE; CYTOCHROME P450 1A1; HEME; POLYCYCLIC AROMATIC HYDROCARBON; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG METABOLISM; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INHIBITOR INTERACTION; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; HUMAN; IN VITRO STUDY; MOLECULAR DOCKING; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; SEQUENCE ANALYSIS; XENOBIOTIC METABOLISM;

CYTOCHROME P450; CYTOCHROME P450 1A1; DOCKING; DRUG METABOLISM; MEMBRANE PROTEINS; X-RAY CRYSTALLOGRAPHY; XENOBIOTICS;

CRYSTALLOGRAPHY, X-RAY; CYTOCHROME P-450 CYP1A1; ENZYME INHIBITORS; HUMANS; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY; XENOBIOTICS;

NICOTIANA TABACUM;

EID: 84877134071     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.452953     Document Type: Article

References (66)

1. Shimada, T., Yun, C. H., Yamazaki, H., Gautier, J. C., Beaune, P. H., and Guengerich, F. P. (1992) Characterization of human lung microsomal cytochrome P-450 1A1 and its role in the oxidation of chemical carcinogens. Mol. Pharmacol. 41, 856-864 (Pubitemid 23023328)
2. Yengi, L. G., Xiang, Q., Pan, J., Scatina, J., Kao, J., Ball, S. E., Fruncillo, R., Ferron, G., and Roland Wolf, C. (2003) Quantitation of cytochrome P450 mRNA levels in human skin. Anal. Biochem. 316, 103-110 (Pubitemid 36407636)
3. van de Kerkhof, E. G., de Graaf, I. A., Ungell, A. L., and Groothuis, G. M. (2008) Induction of metabolism and transport in human intestine. Validation of precision-cut slices as a tool to study induction of drug metabolism in human intestine in vitro. Drug Metab. Dispos. 36, 604-613
4. Nishimura, M., Yaguti, H., Yoshitsugu, H., Naito, S., and Satoh, T. (2003) Tissue distribution of mRNA expression of human cytochrome P450 isoforms assessed by high-sensitivity real-time reverse transcription PCR. Yakugaku zasshi 123, 369-375 (Pubitemid 41327466)
5. Hakkola, J., Raunio, H., Purkunen, R., Pelkonen, O., Saarikoski, S., Cresteil, T., and Pasanen, M. (1996) Detection of cytochrome P450 gene expression in human placenta in first trimester of pregnancy. Biochem. Pharmacol. 52, 379-383 (Pubitemid 26233768)
6. Schwarz, D., Kisselev, P., Ericksen, S. S., Szklarz, G. D., Chernogolov, A., Honeck, H., Schunck, W. H., and Roots, I. (2004) Arachidonic and eicosapentaenoic acid metabolism by human CYP1A1. Highly stereoselective formation of 17(R),18(S)-epoxyeicosatetraenoic acid. Biochem. Pharmacol. 67, 1445-1457 (Pubitemid 38388207)
7. Arnold, C., Konkel, A., Fischer, R., and Schunck, W. H. (2010) Cytochrome P450-dependent metabolism of omega-6 and omega-3 long-chain polyunsaturated fatty acids. Pharmacol. Rep. 62, 536-547
8. Lee, A. J., Cai, M. X., Thomas, P. E., Conney, A. H., and Zhu, B. T. (2003) Characterization of the oxidative metabolites of 17β-estradiol and estrone formed by 15 selectively expressed human cytochrome p450 isoforms. Endocrinology 144, 3382-3398 (Pubitemid 36904414)
9. Ma, X., Idle, J. R., Krausz, K. W., and Gonzalez, F. J. (2005) Metabolism of melatonin by human cytochromes p450. Drug Metab. Dispos. 33, 489-494 (Pubitemid 40393190)
10. Rendic, S., and Guengerich, F. P. (2012) Contributions of human enzymes in carcinogen metabolism. Chem. Res. Toxicol. 25, 1316-1383
11. Wogan, G. N., Hecht, S. S., Felton, J. S., Conney, A. H., and Loeb, L. A. (2004) Environmental and chemical carcinogenesis. Semin. Cancer Biol. 14, 473-486 (Pubitemid 39360995)
12. Shimada, T., and Fujii-Kuriyama, Y. (2004) Metabolic activation of polycyclic aromatic hydrocarbons to carcinogens by cytochromes P450 1A1 and 1B1. Cancer Sci. 95, 1-6 (Pubitemid 38208399)
13. Kim, D., and Guengerich, F. P. (2005) Cytochrome P450 activation of arylamines and heterocyclic amines. Annu. Rev. Pharmacol. Toxicol. 45, 27-49 (Pubitemid 40261797)
14. Hankinson, O. (1995) The aryl hydrocarbon receptor complex. Annu. Rev. Pharmacol. Toxicol. 35, 307-340
15. Willey, J. C., Coy, E. L., Frampton, M. W., Torres, A., Apostolakos, M. J., Hoehn, G., Schuermann, W. H., Thilly, W. G., Olson, D. E., Hammersley, J. R., Crespi, C. L., and Utell, M. J. (1997) Quantitative RT-PCR measurement of cytochromes p450 1A1, 1B1, and 2B7, microsomal epoxide hydrolase, and NADPH oxidoreductase expression in lung cells of smokers and nonsmokers. Am. J. Respir. Cell Mol. Biol. 17, 114-124 (Pubitemid 127500828)
16. Kim, J. H., Sherman, M. E., Curriero, F. C., Guengerich, F. P., Strickland, P. T., and Sutter, T. R. (2004) Expression of cytochromes P450 1A1 and 1 in human lung from smokers, non-smokers, and ex-smokers. Toxicol. Appl. Pharmacol. 199, 210-219
17. Suter, M., Abramovici, A., Showalter, L., Hu, M., Shope, C. D., Varner, M., and Aagaard-Tillery, K. (2010) In utero tobacco exposure epigenetically modifies placental CYP1A1 expression. Metabolism 59, 1481-1490
18. Chi, A. C., Appleton, K., Henriod, J. B., Krayer, J. W., Marlow, N. M., Bandyopadhyay, D., Sigmon, R. C., and Kurtz, D. T. (2009) Differential induction of CYP1A1 and CYP1B1 by benzo[a]pyrene in oral squamous cell carcinoma cell lines and by tobacco smoking in oral mucosa. Oral Oncol. 45, 980-985
19. Androutsopoulos, V. P., Tsatsakis, A. M., and Spandidos, D. A. (2009) Cytochrome P450 CYP1A1. Wider roles in cancer progression and prevention. BMC Cancer 9, 187
20. Doostdar, H., Burke, M. D., and Mayer, R. T. (2000) Bioflavonoids. Selective substrates and inhibitors for cytochrome P450 CYP1A and CYP1B1. Toxicology 144, 31-38 (Pubitemid 30201617)
21. Lautraite, S., Musonda, A. C., Doehmer, J., Edwards, G. O., and Chipman, J. K. (2002) Flavonoids inhibit genetic toxicity produced by carcinogens in cells expressing CYP1A2 and CYP1A1. Mutagenesis 17, 45-53 (Pubitemid 34083385)
22. Reid, J. M., Kuffel, M. J., Miller, J. K., Rios, R., and Ames, M. M. (1999) Metabolic activation of dacarbazine by human cytochromes P450. The role of CYP1A1, CYP1A2, and CYP2E1. Clin. Cancer Res. 5, 2192-2197 (Pubitemid 29399277)
23. Leong, C. O., Gaskell, M., Martin, E. A., Heydon, R. T., Farmer, P. B., Bibby, M. C., Cooper, P. A., Double, J. A., Bradshaw, T. D., and Stevens, M. F. (2003) Antitumour 2-(4-aminophenyl)benzothiazoles generate DNA adducts in sensitive tumour cells in vitro and in vivo. Br. J. Cancer 88, 470-477 (Pubitemid 36308161)
24. Sansen, S., Yano, J. K., Reynald, R. L., Schoch, G. A., Griffin, K. J., Stout, C. D., and Johnson, E. F. (2007) Adaptations for the oxidation of polycyclic aromatic hydrocarbons exhibited by the structure of human P450 1A2. J. Biol. Chem. 282, 14348-14355 (Pubitemid 47100434)
25. Wang, A., Savas, U., Stout, C. D., and Johnson, E. F. (2011) Structural characterization of the complex between alpha-naphthoflavone and human cytochrome P450 1B1. J. Biol. Chem. 286, 5736-5743
26. Hammons, G. J., Milton, D., Stepps, K., Guengerich, F. P., Tukey, R. H., and Kadlubar, F. F. (1997) Metabolism of carcinogenic heterocyclic and aromatic amines by recombinant human cytochrome P450 enzymes. Carcinogenesis 18, 851-854 (Pubitemid 28132477)
27. Turesky, R. J., Constable, A., Richoz, J., Varga, N., Markovic, J., Martin, M. V., and Guengerich, F. P. (1998) Activation of heterocyclic aromatic amines by rat and human liver microsomes and by purified rat and human cytochrome P450 1A2. Chem. Res. Toxicol. 11, 925-936 (Pubitemid 28390194)
28. Rendic, S. (2002) Summary of information on human CYP enzymes. Human P450 metabolism data. Drug Metab. Rev. 34, 83-448
29. Zhou, S. F., Yang, L. P., Zhou, Z. W., Liu, Y. H., and Chan, E. (2009) Insights into the substrate specificity, inhibitors, regulation, and polymorphisms and the clinical impact of human cytochrome P450 1A2. AAPS J. 11, 481-494
30. Shimada, T., Hayes, C. L., Yamazaki, H., Amin, S., Hecht, S. S., Guengerich, F. P., and Sutter, T. R. (1996) Activation of chemically diverse procarcinogens by human cytochrome P-450 1B1. Cancer Res. 56, 2979-2984 (Pubitemid 26199741)
31. Hayes, C. L., Spink, D. C., Spink, B. C., Cao, J. Q., Walker, N. J., and Sutter, T. R. (1996) 17β-Estradiol hydroxylation catalyzed by human cytochrome P450 1B1. Proc. Natl. Acad. Sci. U.S.A. 93, 9776-9781 (Pubitemid 26296685)
32. Porubsky, P. R., Battaile, K. P., and Scott, E. E. (2010) Human cytochrome P450 2E1 structures with fatty acid analogs reveal a previously unobserved binding mode. J. Biol. Chem. 285, 22282-22290
33. Wang, A., Savas, U., Hsu, M. H., Stout, C. D., and Johnson, E. F. (2012) Crystal structure of human cytochrome P450 2D6 with prinomastat bound. J. Biol. Chem. 287, 10834-10843
34. Liu, J., Ericksen, S. S., Besspiata, D., Fisher, C. W., and Szklarz, G. D. (2003) Characterization of substrate binding to cytochrome P450 1A1 using molecular modeling and kinetic analyses. Case of residue 382. Drug Metab. Dispos. 31, 412-420 (Pubitemid 36378518)
35. DeVore, N. M., Smith, B. D., Wang, J. L., Lushington, G. H., and Scott, E. E. (2009) Key residues controlling binding of diverse ligands to human cytochrome P450 2A enzymes. Drug Metab. Dispos. 37, 1319-1327
36. Leslie, A. G. (2006) The integration of macromolecular diffraction data. Acta Crystallogr. D Biol. Crystallogr. 62, 48-57
37. Collaborative Computational Project, Number 4 (1994) The CCP4 suite. Programs for protein crystallography. Acta Crystallogr.DBiol. Crystallogr. 50, 760-763
38. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
39. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (Pubitemid 27235885)
40. Guex, N., and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-Pdb-Viewer. An environment for comparative protein modeling. Electrophoresis 18, 2714-2723 (Pubitemid 28059943)
41. Kabsch, W., and Sander, C. (1983) Dictionary of protein secondary structure. Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22, 2577-2637
42. Kleywegt, G. J., and Jones, T. A. (1994) Detection, delineation, measurement and display of cavities in macromolecular structures. Acta Crystallogr D. Biol. Crystallogr. 50, 178-185 (Pubitemid 2054290)
43. Delano, W. L. (2002) The PyMOL Molecular Graphics System, Delano Scientific, Palo Alto, CA
44. Needleman, S. B., and Wunsch, C. D. (1970) A general method applicable to the search for similarities in the amino acid sequence of two proteins. J. Mol. Biol. 48, 443-453
45. Paulsen, M. D., and Ornstein, R. L. (1991) A 175-psec molecular dynamics simulation of camphor-bound cytochrome P-450cam. Proteins 11, 184-204
46. Paulsen, M. D., and Ornstein, R. L. (1992) Predicting the product specificity and coupling of cytochrome P450cam. J. Comput. Aided Mol. Des. 6, 449-460
47. Huang, Q., and Szklarz, G. D. (2010) Significant increase in phenacetin oxidation on L382V substitution in human cytochrome P450 1A2. Drug Metab. Dispos. 38, 1039-1045
48. Ericksen, S. S., and Szklarz, G. D. (2005) Regiospecificity of human cytochrome P450 1A1-mediated oxidations. The role of steric effects. J. Biomol. Struct. Dyn. 23, 243-256 (Pubitemid 41642429)
49. Tu, Y., Deshmukh, R., Sivaneri, M., and Szklarz, G. D. (2008) Application of molecular modeling for prediction of substrate specificity in cytochrome P450 1A2 mutants. Drug Metab. Dispos. 36, 2371-2380
50. Sandhu, P., Guo, Z., Baba, T., Martin, M. V., Tukey, R. H., and Guengerich, F. P. (1994) Expression of modified human cytochrome P450 1A2 in Escherichia coli. Stabilization, purification, spectral characterization, and catalytic activities of the enzyme. Arch. Biochem. Biophys. 309, 168-177 (Pubitemid 24171457)
51. Shimada, T., Wunsch, R. M., Hanna, I. H., Sutter, T. R., Guengerich, F. P., and Gillam, E. M. (1998) Recombinant human cytochrome P450 1B1 expression in Escherichia coli. Arch. Biochem. Biophys. 357, 111-120 (Pubitemid 28402591)
52. Shah, M. B., Wilderman, P. R., Pascual, J., Zhang, Q., Stout, C. D., and Halpert, J. R. (2012) Conformational adaptation of human cytochrome P450 2B6 and rabbit cytochrome P450 2B4 revealed upon binding multiple amlodipine molecules. Biochemistry 51, 7225-7238
53. Honma, W., Li, W., Liu, H., Scott, E. E., and Halpert, J. R. (2005) Functional role of residues in the helix B′ region of cytochrome P450 2B1. Arch. Biochem. Biophys. 435, 157-165 (Pubitemid 40170026)
54. Mast, N., White, M. A., Bjorkhem, I., Johnson, E. F., Stout, C. D., and Pikuleva, I. A. (2008) Crystal structures of substrate-bound and substrate-free cytochrome P450 46A1, the principal cholesterol hydroxylase in the brain. Proc. Natl. Acad. Sci. U.S.A. 105, 9546-9551 (Pubitemid 352031338)
55. Zhao, Y., Sun, L., Muralidhara, B. K., Kumar, S., White, M. A., Stout, C. D., and Halpert, J. R. (2007) Structural and thermodynamic consequences of 1-(4-chlorophenyl)imidazole binding to cytochrome P450 2B4. Biochemistry 46, 11559-11567 (Pubitemid 47585501)
56. Iba, M. M., Shin, M., and Caccavale, R. J. (2010) Cytochromes P4501 (CYP1). Catalytic activities and inducibility by diesel exhaust particle extract and benzo[a]pyrene in intact human lung ex vivo. Toxicology 273, 35-44
57. Shimada, T., Gillam, E. M., Sutter, T. R., Strickland, P. T., Guengerich, F. P., and Yamazaki, H. (1997) Oxidation of xenobiotics by recombinant human cytochrome P450 1B1. Drug Metab. Dispos. 25, 617-622 (Pubitemid 27213104)
58. Shimada, T., Tanaka, K., Takenaka, S., Murayama, N., Martin, M. V., Foroozesh, M. K., Yamazaki, H., Guengerich, F. P., and Komori, M. (2010) Structure-function relationships of inhibition of human cytochromes P450 1A1, 1A2, 1B1, 2C9, and 3A4 by 33 flavonoid derivatives. Chem. Res. Toxicol. 23, 1921-1935
59. Chun, Y. J., Ryu, S. Y., Jeong, T. C., and Kim, M. Y. (2001) Mechanism-based inhibition of human cytochrome P450 1A1 by rhapontigenin. Drug Metab. Dispos. 29, 389-393 (Pubitemid 32275551)
60. Chun, Y. J., Kim, M. Y., and Guengerich, F. P. (1999) Resveratrol is a selective human cytochrome P450 1A1 inhibitor. Biochem. Biophys. Res. Commun. 262, 20-24 (Pubitemid 29412616)
61. Shimada, T. (2006) Xenobiotic-metabolizing enzymes involved in activation and detoxification of carcinogenic polycyclic aromatic hydrocarbons. Drug Metab. Pharmacokinet. 21, 257-276
62. Bauer, E., Guo, Z., Ueng, Y. F., Bell, L. C., Zeldin, D., and Guengerich, F. P. (1995) Oxidation of benzo[a]pyrene by recombinant human cytochrome P450 enzymes. Chem. Res. Toxicol. 8, 136-142
63. Huang, Q., Deshmukh, R. S., Ericksen, S. S., Tu, Y., and Szklarz, G. D. (2012) Preferred binding orientations of phenacetin in CYP1A1 and CYP1A2 are associated with isoform-selective metabolism. Drug Metab. Dispos. 40, 2324-2331
64. Liu, J., Ericksen, S. S., Sivaneri, M., Besspiata, D., Fisher, C. W., and Szklarz, G. D. (2004) The effect of reciprocal active site mutations in human cytochromes P450 1A1 and 1A2 on alkoxyresorufin metabolism. Arch. Biochem. Biophys. 424, 33-43 (Pubitemid 38326852)
65. Szklarz, G. D., and Paulsen, M. D. (2002) Molecular modeling of cytochrome P450 1A1. Enzyme-substrate interactions and substrate binding affinities. J. Biomol. Struct. Dyn. 20, 155-162 (Pubitemid 35265925)
66. Piver, B., Fer, M., Vitrac, X., Merillon, J. M., Dreano, Y., Berthou, F., and Lucas, D. (2004) Involvement of cytochrome P450 1A2 in the biotransformation of trans-resveratrol in human liver microsomes. Biochem. Pharmacol. 68, 773-782 (Pubitemid 38953459)