Metabolism of equilenin in MCF-7 and MDA-MB-231 human breast cancer cells

Chemical Research in Toxicology

Volumn 14, Issue 5, 2001, Pages 572-581

  Spink, David C ^a,b   Zhang, Fagan ^c   Hussain, Mirza M ^a   Katz, Barbara H ^a   Liu, Xuemei ^c   Hilker, David R ^a   Bolton, Judy L ^c  

^a WADSWORTH CENTER   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

^c UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; 3,4,4',5 TETRACHLOROBIPHENYL; AROMATIC HYDROCARBON RECEPTOR; CYTOCHROME P450 1A1; CYTOCHROME P450 1B1; DIHYDROEQUILIN; EQUILENIN;

ARTICLE; BREAST CANCER; CANCER CELL CULTURE; CELL STRAIN MCF 7; CONTROLLED STUDY; DRUG HYDROXYLATION; DRUG METABOLISM; GAS CHROMATOGRAPHY; HUMAN; HUMAN CELL; MASS SPECTROMETRY;

ARYL HYDROCARBON HYDROXYLASES; BREAST NEOPLASMS; CYTOCHROME P-450 CYP1A1; CYTOCHROME P-450 ENZYME SYSTEM; EQUILENIN; FEMALE; HUMANS; HYDROXYLATION; POLYCHLORINATED BIPHENYLS; RECEPTORS, ARYL HYDROCARBON; TETRACHLORODIBENZODIOXIN; TUMOR CELLS, CULTURED;

MINK CELL FOCUS-FORMING VIRUS;

EID: 0035012529     PISSN: 0893228X     EISSN: None     Source Type: Journal    
DOI: 10.1021/tx000219r     Document Type: Article

References (45)

1. Grodstein, F., Stampfer, M. J., Colditz, G. A., Willett, W. C., Manson, J. E., Joffe, M., Rosner, B., Fuchs, C., Hankinson, S. E., Hunter, D. J., Hennekens, C. H., and Speizer, F. E. (1997) Postmenopausal hormone therapy and mortality. N. Eng. J. Med. 336, 1769-1775.
2. Wickelgren, I. (1997) Estrogen: A new weapon against Alzheimer's. Science 276, 676-677.
3. Colditz, G. A. (1998) Relationship between estrogen levels, use of hormone replacement therapy, and breast cancer. J. Natl. Cancer Inst. 90, 814-823.
4. Bhavnani, B. R. (1988) The saga of the ring B unsaturated equine estrogens. Endocr. Rev. 9, 396-416.
5. Bhavnani, B. R. (1998) Pharmacokinetics and pharmacodynamics of conjugated equine estrogens: chemistry and metabolism. Proc. Soc. Exp. Biol. Med. 217, 6-16.
6. Li, J. J., Li, S. A., Oberley, T. D., and Parsons, J. A. (1995) Carcinogenic activities of various steroidal and nonsteroidal estrogens in the hamster kidney: relation to hormonal activity and cell proliferation. Cancer Res. 55, 4347-4351.
7. 3H]17ß-dihydroequilin sulfate in normal postmenopausal women. Steroids 59, 389-394.
8. Purdy, R. H., Moore, P. H., Williams, M. C., Goldzheher, H. W., and Paul, S. M. (1982) Relative rates of 2- and 4-hydroxylation synthesis are dependent on both substrate and tissue. FEBS Lett. 138, 40-44.
9. Li, S. A., Klicka, J. K., and Li, J. J. (1985) Estrogen 2- and 4-hydroxylase activity, catechol estrogen formation, and implication for carcinogenesis in the hamster kidney. Cancer Res. 45, 181-185.
10. Sarabia, S. F., Zhu, B. T., Kurosawa, T., Thoma, M., and Liehr, J. G. (1997) Mechanism of cytochrome P450-catalyzed aromatic hydroxylation of estrogens. Chem. Res. Toxicol. 10, 767-771.
11. Zhang, V., Chen, Y., Pisha, E., Shen, L., Xiong, Y., van Breemen, R. B., and Bolton, J. L. (1999) The major metabolite of equilin, 4-hydroxyequilin, autoxidizes to an o-quinone which isomerizes to the potent cytotoxin 4-hydroxyequilenin-o-quinone. Chem. Res. Toxicol. 12, 204-213.
12. Liehr, J. G., Ulubelen, A. A., and Strobel, H. W. (1986) Cytochrome P-450-mediated redox cycling of estrogens. J. Biol Chem. 261, 16865-16870.
13. Liehr, J. G., and Roy, D. (1990) Free radical generation by redox cycling of estrogens. Free Radical Biol. Med. 8, 415-423.
14. Nutter, L. M., Ngo, E., and Abdul-Hajj, Y. J. (1991) Characterization of DNA damage by 3,4-estrone-o-quinone in human cells. J. Biol. Chem. 266, 16380-16386.
15. Nutter, L. M., Wu., Y.-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.
16. Cavalieri, E. L., Stack, D. E., Devanesan, P. D., Todorovic, R., Dwivedy, I., Higginbotham, S., Johansson, S. L., Patil, K. D., Gross, M. L., Gooden, J. K., Ramanathan, R., Cerny, R. L., and Rogan E. G. (1997) Molecular origin of cancer: Catechol estrogen-3,4-quinones as endogenous tumor initiators. Proc. Natl. Acad. Sci. U.S.A. 94, 10937-10942.
17. Han, X., and Liehr, J. G. (1995) Microsome-mediated 8-hydroxylation of guanine bases of DNA by steroid estrogens: correlation of DNA damage by free radicals with metabolic activation to quinones. Carcinogenesis 16, 2571-2574.
18. Shen, L., Pisha, E., Huang, Z., Pezzuto, J. M., Krol, E., Alam, Z., van Breemen, R. B., and Bolton, J. L. (1997) Bioreductive activation of catechol estrogen-ortho-quinones: aromatization of the B ring in 4-hydroxyequilenin markedly alters quinoid formation and reactivity. Carcinogenesis 18, 1093-1101.
19. Chen, Y., Shen, L., Zhang, F., Lau, S., van Breemen, R. B., Nikolic, D., and Bolton, J. L. (1998) The equine estrogen metabolite 4-hydroxyequilenin causes DNA single strand breaks and oxidation of DNA bases in vitro. Chem. Res. Toxicol. 11, 1105-1111.
20. Chen, Y., Liu, X., Pisha, E., Constantinou, A. I., Hua, Y., Shen, L., van Breemen, R. B., Eliguindi, E. C., Blond, S. Y., Zhang, F., and Bolton, J. L. (2000) A metabolite of equine estrogens, 4-hydroxyequilenin, induces DNA damage and apoptosis in breast cancer cell lines. Chem. Res. Toxicol. 13, 342-350.
21. Shen, L., Qiu, S., van Breemen, R. B., Zhang, F., Chen, Y., and Bolton, J. L. (1998) Reaction of the premarin metabolite 4-hydroxyequilenin semiquinone radical with 2′-deoxyguanosine: formation of unusual cyclic adducts. J. Am. Chem. Soc. 119, 11126-11127.
22. Shen, L., Qiu, S., Chen, Y., Zhang, F., van Breemen, R. B., Nikolic, D., and Bolton, J. L. (1998) Alkylation of 2′-deoxyribonucleosides and DNA by the Premarin metabolite 4-hydroxyequilenin semiquinone radical. Chem. Res. Toxicol. 11, 94-101.
23. Bolton, J. L., Pisha, E., Zhang, F., and Qiu, S. (1998) Role of quinoids in estrogen carcinogenesis. Chem. Res. Toxicol. 11, 1113-1127.
24. Spink D. C., Lincoln D. W., II, Dickerman, H. W., and Gierthy, J. F. (1990) 2,3,7,8-Tetrachlorodibenzo-p-dioxin causes an extensive alteration of 17ß-estradiol metabolism in MCF-7 breast tumor cells. Proc. Natl. Acad. Sci. U.S.A. 87, 6917-6921.
25. Spink, D. C., Eugster, H.-P., Lincoln, D. W., II, Schuetz, J. D., Schuetz, E. G., Johnson, J. A., Kaminsky, L. S., and Gierthy, J. F. (1992) 17ß-Estradiol hydroxylation catalyzed by human cytochrome P450 1A1: a comparison of the activities induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin in MCF-7 cells with those from heterologous expression of the cDNA. Arch. Biochem. Biophys. 293, 342-348.
26. Spink, D. C, Hayes, C. L., Young, N. R., Christou, M., Sutter, T. R., Jefcoate, C. R., and Gierthy, J. F. (1994) The effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on estrogen metabolism in MCF-7 breast cancer cells: evidence for induction of a novel 17ß-estradiol 4-hydroxylase. J. Steroid Biochem. Mol. Biol. 51, 251-258.
27. Hayes, C. L., Spink D. C., Spink B. C., Cao, J. Q., Walker, N. J., and Sutter T. R. (1996) 17ß-Estradiol hydroxylation catalyzed by human cytochrome P450 1B1. Proc. Natl. Acad. Sci. U.S.A. 93, 9778-9781.
28. Shimada, T., Hayes, C. L., Yamazaki, H., Amin, S., Hect, S. S., Guengerich, F. P., and Sutter, T. R. (1996) Activation of chemically diverse procarcinogens by human cytochrome P450 1B1. Cancer Res. 56, 2979-2985.
29. Larsen, M. C., Angus, W. G. R., Brake, P. B., Eltom, S. E., Sukow, K. A., and Jefcoate, C. R. (1998) Characterization of CYP1B1 and CYP1A1 expression in human mammary epithelial cells: role of the aryl hydrocarbon receptor in polycyclic aromatic hydrocarbon metabolism. Cancer Res. 58, 2366-2374.
30. Spink, B. C., Fasco, M. J., Gierthy, J. F., and Spink, D. C. (1998) 12-O-tetradecanoylphorbol-13-acetate upregulates the Ah receptor and differentially alters CYP1A1 and CYP1B1 expression in MCF-7 breast cancer cells. J. Cell. Biochem. 70, 289-296.
31. Döhr, O., Vogel, C., and Abel, J. (1995) Different response of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)-sensitive genes in human breast cancer MCF-7 and MDA-MB-231 cells. Arch. Biochem. Biophys. 321, 405-412.
32. Spink, D. C., Spink, B. C., Cao, J. Q., DePasquale, J. A., Pentecost, B. T., Fasco, M. J., Li, Y., and Sutter, T. R. (1998) Differential expression of CYP1A1 and CYP1B1 in human breast epithelial cells and breast tumor cells. Carcinogenesis 19, 291-298.
33. Angus, W. G. R., Larsen, M. C., and Jefcoate, C. R. (1999) Expression of CYP1A1 and CYP1B1 depends on cell-specific factors in human breast cancer cell lines: role of estrogen receptor status. Carcinogenesis 20, 947-955.
34. Pang, S., Cao, J. Q., Katz, B. H., Hayes, C. L., Sutter, T. R., and Spink, D. C. (1999) Inductive and inhibitory effects of non-ortho-substituted polychlorinated biphenyls on estrogen metabolism and cytochromes P450 1A1 and 1B1. Biochem. Pharmacol. 58, 29-38.
35. Teuber, H. J. (1953) Reakionen mit nitrosodisulfonat (III). Equilenin-Chinon. Chem. Ber. 86, 1495-1499.
36. Rao, P. N., and Somawardhana, C. W. (1987) Synthesis of 2-methoxy and 4-methoxy equine estrogens. Steroids 49, 419-432.
37. Zhang, F., and Bolton, J. L. (1999) Synthesis of the equine estrogen metabolites 2-hydroxyequilin and 2-hydroxyequilenin. Chem. Res. Toxicol. 12, 200-203.
38. Hylarides, M. D., Wilbur, D. S., and Mettler, F. A., Jr. (1983) B-ring aromatization of estrogen derivatives. Steroids 41, 657-662.
39. Chang, M., Zhang F., Shen L., Pauss N., Alam I., van Breemen, R. B., Blond, S. Y., and Bolton, J. L. (1998) Inhibition of glutathione S-transferase activity by the quinoid metabolites of equine estrogens. Chem. Res. Toxicol. 11, 758-65.
40. Murphy, R. C. (1974) Facile synthesis of deuterated estrogens. Steroids 24, 343-349.
41. Hoffman, A. R., Paul, S. M., and Axelrod, J. (1979) Catecholestrogen synthesis and metabolism by human breast tumors. Cancer Res. 39, 4584-4587.
42. Liehr, J. G., Fang, W. F., Sirbasku, D. A., and Ari-Ulubelen, A. (1986) Carcinogenicity of catechol estrogens in Syrian hamsters. J. Steroid Biochem. 24, 353-356.
43. Li, J. J., and Li, S. A. (1987) Estrogen carcinogenesis in Syrian hamster tissues: role of metabolism. Fed. Proc. 46, 1858-1863.
44. Newbold, R. R., and Liehr, J. G. (2000) Induction of uterine adenocarcinoma in CD-1 mice by catechol estrogens. Cancer Res. 60, 235-237.
45. Liehr, J. G., Ricci, M. J., Jefcoate, C. R., Hannigan, E. V., Hokanson, J. A., and Zhu, B. T. (1995) 4-Hydroxylation of estradiol by human uterine myometrium and myoma microsomes: Implications for the mechanism of uterine tumorigenesis. Proc. Natl. Acad. Sci. U.S.A. 92, 9220-9224.