Role of human hepatic cytochrome P450 1A2 and 3A4 in the metabolic activation of estrone

Carcinogenesis

Volumn 18, Issue 1, 1997, Pages 207-214

  Shou, Magang ^a   Korzekwa, Kenneth R ^b   Brooks, Ericka N ^a,c   Krausz, Kristopher W ^a   Gonzalez, Frank J ^a   Gelboin, Harry V ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^c CLARK ATLANTA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAFFEINE; CYTOCHROME P450; ESTROGEN; ESTRONE; LIVER ENZYME; MONOCLONAL ANTIBODY; RECOMBINANT ENZYME; TESTOSTERONE;

ADULT; ARTICLE; CARCINOGENESIS; DEMETHYLATION; FEMALE; GAS CHROMATOGRAPHY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN TISSUE; HYDROXYLATION; LIVER MICROSOME; MALE; MASS SPECTROMETRY; METABOLIC ACTIVATION; MICHAELIS MENTEN KINETICS; NORMAL HUMAN; ORGAN DONOR; PRIORITY JOURNAL;

ADULT; BIOTRANSFORMATION; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYTOCHROME P-450 CYP1A2; CYTOCHROME P-450 ENZYME SYSTEM; ESTRONE; FEMALE; GENETIC VECTORS; HUMANS; MALE; MIDDLE AGED; MIXED FUNCTION OXYGENASES; VACCINIA VIRUS;

EID: 0031418653     PISSN: 01433334     EISSN: None     Source Type: Journal    
DOI: 10.1093/carcin/18.1.207     Document Type: Article

References (62)

1. Henderson,B.E., Ross,R.K. and Pike,M.C. (1991) Toward the primary prevention of cancer. Science, 254, 1131-1138.
2. Lippman,M.E. and Dickson,R.B. (1989) Mechanism of normal and malignant breast epithelial growth regulation. J. Steroid Biochem., 34, 107-121.
3. Li,J.J., Li,S.A., Klicka,J.K, Parson,J.A. and Lam,L.K. (1983) Relative carcinogenic activity of various synthetic and natural estrogens in the hamster kidney. Cancer Res., 43, 5200-5204.
4. Kirkman,H. (1959) Estrogen-induced tumors of the kidney in the Syrian hamster. Natl Cancer Inst. Monogr., 1, 1-59.
5. Vana,J., Murphy,G.P., Aronoff,B.L. and Baker,H.W. (1979) Survey of primary liver tumors and oral contraceptive use. J. Toxicol. Environ. Health, 5, 255-273.
6. Kirkman,H. and Wurster,D.H. (1957) Steroid tumorigenesis. Proc. Am. Assoc. Cancer Res., 2, 221-222.
7. Liehr,J.G., Randerath,K. and Randerath,E. (1985) Target organ-specific covalent DNA binding preceding dethylstilbestrol-induced carcinogenesis. Carcinogenesis, 6, 1067-1069.
8. Liehr,J.G. (1986) Modulation of estrogen-induced carcinogenesis by chemical modifications. Arch. Toxicol., 55, 119-122.
9. Dwinedy,I., Devanesan,P., Cremonesi,P., Rogan,E. and Cavalieri,E. (1992) Synthesis and characterization of estrone 2,3- and 3,4-quinones. Comparison of DNA adducts formed by the quinones versus horseradish peroxidase-activated catechol estrogens. Chem. Res. Toxicol., 5, 828-833.
10. Nutter,L.M., Wu,Y., Ngo,E.O., Sierra,E.E., Gutierrez,P.L. and Abul-Hajj,Y.J. (1994) An O-quinone form of estrogen produces free radicals in human breast cancer cells: Correlation with DNA damage. Chem. Res. Toxicol., 7, 23-28.
11. Antonio,P., Gabolden,M., Lacomba,T. and Juan,A. (1976) Effect of the antiestrongen nafoxidine on the occurrence of estrogen-induced renal tumorigenesis in the Syrian hamsters. Horm. Metab. Res., 6, 522-525.
12. Li,J.J. and Li,S.A. (1981) Inhibition of estrogen-induced renal tumorigenesis in the Syrian golden hamster by BHA, β- and α-naphthoflavone. Proc. Am. Assoc. Cancer Res., 22, 11-12.
13. Liehr,J.G. and Wheeler,S.A. (1983) Inhibition of estrogen-induced renal carcinoma in Syrian hamsters by vitamin C. Cancer Res., 43, 4638-4642.
14. Gelboin,H.V. (1980) Benzo[a]pyrene metabolism, activation, and carcinogenesis: Role and regulation of mixed-function oxidases and related enzymes. Physiol. Rev., 60, 1107-1166.
15. Conney,A.M. (1982) Induction of microsomal enzymes by foreign chemicals and carcinogenesis by polycyclic aromatic hydrocarbons. G.H.A. Clowes Memorial Lecture. Cancer Res., 42, 4875-4917.
16. Gonzalez,F.J. (1988) The molecular biology of cytochrome P450s. Pharmacol. Rev., 40, 243-288.
17. Guengerich,T.P., Gillam,E.M.J., Martin,M.V., Baba,T., Kim,B.R., Raney,K.D. and Yun,C.H. (1994) The importance of cytochrome P450 3A enzymes in drug metabolism. In Waterman,M.R. and Hildebrand,M. (eds), Assessment of the Use of Single Cytochrome P450 Enzymes in Drug Research. Springer, Berlin, Germany, pp. 161-186.
18. Ryan,K.J. (1958) Conversion of androstenedione to estrone by placental microsomes. Biochim. Biophys. Acta, 27, 658-662.
19. Lemon,H.M., Heidel,J.W. and Rodriguez-Sierra,J.F. (1992) Increased catechol estrogen metabolism as a risk factor for nonfamilial breast cancer. Cancer, 69, 457-465.
20. Li,J.J. and Li,S.A. (1987) Estrogen carcinogenesis in hamster tissues: role of metabolism. Fed. Proc., 46, 1858-1863.
21. Liehr,J.G., Fang,W.F., Sibasku,D.A. and Ulubelen,A.A. (1986) Carcinogenicity of catechol estrogens in Syrian hamsters. J. Steroid Biochem., 24, 353-356.
22. Martucci,C.P. and Fishman,J. (1993) P450 enzymes of estrogen metabolism. Pharmacol. Ther., 57, 237-257.
23. Ball,P. and Knuppen,R. (1990) Formation, metabolism and physiologic importance of catecholestrogens. Am. J. Obstet. Gynecol., 163, 2163-2170.
24. Aoyama,T., Korzekwa,K.R., Nagata,K., Gillette,J., Gelboin,H.V. and Gonzalez,F.J. (1990) Estradiol metabolism by complementary deoxyribonucleic acid-expressed human cytochrome P450s. Endocrinology, 126, 3101-3106.
25. Brueggemeier,R.W., Tseng,K., Katlic,N.E., Beleh,M.A. and Lin,Y.C. (1990) Estrogen metabolism in primary kidney cell cultures from Syrian hamsters. J. Steroid Biochem., 36, 325-332.
26. 14C]estrone in hamster and rat hepatic and renal microsomes: species-, sex- and age-specific differences. J. Steroid Biochem. Mol. Biol., 42, 389-397.
27. Zhu,B.T., Bui,Q.D., Weisz,J. and Liehr,J.G. (1994) Conversion of estrone to 2- and 4- hydroxyestrone by hamster kidney and liver microsomes: Implications for the mechanism of estrogen-induced carcinogenesis. Endocrinology, 135, 1355-1772.
28. Dannan,G.A., Porurek,D.J., Nelson,S.D., Waxman,D.J. and Guengerich,F.P. (1986) 17β-Estradiol 2- and 4-hydroxylation catalyzed by rat hepatic cytochrome P450: roles of individual forms, inductive effects, developmental patterns and alterations by fonadectomy and hormone replacement. Endocrinology, 118, 1952-1960.
29. Graham,M.J., Lucier,G.W., Linko,P., Maronpot,R.R. and Goldstein,J.A. (1988) Increase in cytochrome P450 mediated 17β-estradiol 2-hydroxylase activity in rat liver microsomes after both acute administration and subchronic administration of 2,3,7,8-tetrachlorodibenzo-p-dioxin in a two-stage hepatocarcinogenesis model. Carcinogenesis, 9, 1935-1941.
30. Namkung,M.J., Yang,H.L., Hulla,J.E. and Juchau,M.R. (1988) On the substrate specificity of cytochrome P450IIIA1. Mol. Pharmacol., 34, 628-637.
31. Swaneck,G.E. and Fishman,J. (1991) Estrogen actions on target cells: evidence for different effects by products of two alternative pathways of estradiol metabolism. In Hochberg, R.B. and Naftolin, F. (eds), The New Biology of Steroid Hormones. Raven Press, New York, pp. 45-36
32. Gonzalez,F.J., Aoyama,T., and Gelboin,H.V. (1991) Expression of mammalian cytochrome P450 using vaccinia virus. Methods Enzymol., 206, 85-92.
33. Gelboin,H.V., Krausz,K.W., Goldfarb,I., Buters,J.T.M., Yang,S.K., Gonzalez,F.J., Korzekwa,K.R. and Shou,M. (1995) An inhibitory monoclonal antibody to human cytochrome P450 3A4. Biochem. Pharmacol., 50, 1841-1850.
34. Wang,P.P., Beaune,P., Kaminsky,L.S., Dannan,G.A., Kadlubar,F.F., Larrey,D. and Guengerich,F.P. (1983) Purification and characterization of six cytochrome P450 isozymes from human liver microsomes. Biochemistry, 22, 5375-5383.
35. 3450 and P450a. Mol. Carcinogen., 1, 253-259.
36. Yamano,S., Nhamburo,P.T., Aoyama,T., Meyer,U.A., Inaba,T., Kalow,W., Gelboin,H.V., McBride,O.W. and Gonzalez,F.J. (1989) cDNA cloning and sequence, and cDNA-directed expression of human P450 IIB1: identification of a normal and two variant cDNAs derived from the CYP2B locus on chromosome 19 and differential expression of IIB mRNAs in human liver. Biochemistry, 28, 7340-7348.
37. Relling,M.V., Aoyama,T., Gonzalez,F.J. and Meyer,U.A. (1990) Tolbutamide and mephytoin hydroxylation by human cytochrome P450s in the CYP2C subfamily. J. Pharmacol. Exp. Ther., 252, 442.
38. Rettie,A.E., Wienkers,L.C., Gonzalez,F.J., Trager,W.F. and Korzekwa,K.R. (1994) Impaired (S)-warfarin metabolism catalyzed by the R144C allelic variant of CYP2C9. Pharmacogenetics, 4, 39-42.
39. Umeno,M., McBride,O.W., Yang,C.S., Gelboin,H.V. and Gonzalez,F.J. (1988) Human ethanol-inducible P450IIE1: complete gene sequence, promoter characterization, chromosome mapping, and cDNA-directed expression. Biochemistry, 27, 9006-9013.
40. Aoyama,T., Yamano,S., Waxman,D.J., Meyer,U.A., Fisher,V., Lapenson,D.P., Tyndale,R., Inaba,T., Kalow,W., Gelboin,H.V. and Gonzalez,F.J. (1989) Cytochrome P450hPCN3, a novel P450 IIA gene product that is deferentially expressed in adult human liver: cDNA and deduced amino acid sequence and distinct specificities of cDNA-expressed hPCN1 and hPCN3 for the metabolism of steroid hormones and cyclosporin. J. Biol. Chem., 264, 10388-10389.
41. Omura,T. and Sato,R. (1964) The carbon monooxide-binding pigment of liver microsomes: I. Evidence for its hemoprotein nature. J. Biol. Chem., 239, 2370-2378.
42. Cleland.W.W. (1979) Statistical analysis of enzyme kinetic data. Methods Enzymol., 63, 103-159.
43. Fuhr,U., Doehmer,J., Battula,N., Wölfel,C., Kudla,C., Keita,Y. and Staib,A.H. (1992) Biotransformation of caffeine and theophylline in mammalian cell lines genetically engineered for expression of single cytochrome P450 isoforms. Biochem. Pharmacol., 43, 225-235.
44. Weaver,R.J., Dickins,M. and Burke,M.D. (1995) Hydroxylation of the antimalarial drug 58C80 by CYP2C9 in human liver microsomes: Comparison with mephenytoin and tolbutamide hydroxylations. Biochem. Pharmacol., 49, 997-1004.
45. Hanioka,N., Korzekwa,K. and Gonzalez,F.J. (1990) Sequence requirements for cytochromes P450IIA1 and P450IIA2 catalytic activity: Evidence for both specific and non-specific substrate binding interactions through use of chimeric cDNAs and cDNA expression. Protein Eng., 3, 571-575.
46. Peter,R., Böcker,R., Beaune,P.H., Iwasaki,M., Guengerich,F.P. and Yang,C.S. (1990) Hydroxylation of chlorzoxazone as a specific probe for human liver cytochrome P-450IIE1. Chem. Res. Toxicol., 3, 566-573.
47. Gonzalez,F.J. and Korzekwa,K.R. (1995) Cytochromes P450 expression systems. Annu. Rev. Pharmacol. Toxicol., 35, 369-390.
48. Rettie,A.E., Korzekwa,K.R., Kunze,K.L., Lawrence,R.F., Eddy,A.C., Aoyam,T., Gelboin,H.V., Gonzalez,F.J. and Trager, W.F. (1992) Hydroxylation of warfarin by human cDNA-expressed cytochrome P-450: A role for CYP2C9 in the etiology of S-warfarin-drug interactions. Chem. Res. Toxicol., 5, 54-59.
49. Nelson,S.D., Mitchell,J.R., Dybrig,E. and Sasame,H. (1976) Cytochrome P450-mediated oxidation of 2-hydroxy-estrogens to reactive intermediates. Biochem. Biophys. Res. Commun., 70, 1157-1165.
50. Ball,P. and Knuppen,R. (1980) Catecholestrogens. Acta Endocr. (Suppl.), 232, 1-127.
51. Fishman,J. (1983) Aromatic hydroxylation of estrogens. Annu. Rev. Physiol., 45, 61-72.
52. Fishman,J., Naftolin,F., Davies,I.J., Ryan,K.J. and, Petro,Z. (1976) Catechol estrogen formation by the hamster brain and pituitary. J. Clin. Endocrinol. Metab., 4, 177-180.
53. Shupnik,M.A., Klibanski,A., Longcope,C. and Rigeway,E.C. (1985) Catecholestrogen regulation of prolactin synthesis in pituitary cell culture. Endocrinology, 117, 939-946.
54. Paria,B.C., Charkraborty,C. and Des,S.K. (1990) Catechol estrogen formation in mouse uterus and its role in implantation. Mol. Cell. Endocrinol., 69, 25-31.
55. Li,J.J. and Li,S.A. (1987) Estrogen carcinogenesis in Syrian hamster tissues: role of metabolism. Fed. Proc., 46, 1858-1863.
56. Metzler,M. (1984) Metabolism of stilbene estrogens and steroidal estrogens in relation to carcinogenicity. Arch. Toxicol., 55, 104-109.
57. Liehr,J.G. and Roy,D. (1990) Free radical generation by redox cycling of estrogens. Free Radical Biol. Med., 8, 415-423.
58. Haaf,H., Li,S.A. and Li,J.J. (1987) Covalent binding of estrogen metabolites to hamster liver microsomal proteins: inhibition by ascorbic acid and catechol-O-methyltransferase. Carcinogenesis, 8, 209-215.
59. Li,S.A., Klicka,J.K. and Li,J.J. (1986) Effect of androgen and estrogen treatment on hamster liver and kidney estrogen 2-/4-hydrolase activity. Free Radical Biol. Med., 8, 415-423.
60. Liehr,J.G., Ulubelen,A.A. and Strobel,H.W. (1986) Cytochrome P450-mediated redox cycling of estrogens. J. Biol. Chem., 261, 16865-16870.
61. Lonning,P.E., Skulstad,P., Sunde,A. and Thorsen,T. (1989) Separation of urinary metabolites of radiolabelled estrogens in man by HPLC. J. Steroid Biochem., 32, 91-97.
62. Swaneck,G. and Fishman,J. (1988) Covalent binding of the endogenous estrogen 16α- hydroxyestrone to estradiol receptor in human breast cancer cells: characterization and intranuclear localization. Proc. Natl Acad. Sci USA, 85, 7831-7835.