Formation of catechol estrogen glutathione conjugates and γ-glutamyl transpeptidase-dependent nephrotoxicity of 17β-estradiol in the golden Syrian hamster

Carcinogenesis

Volumn 18, Issue 3, 1997, Pages 561-567

  Butterworth, Michael ^a,b   Lau, Serrine S ^a   Monks, Terrence J ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; CARBON 14; CARBONYL DERIVATIVE; CATECHOL ESTROGEN; ESTRADIOL; GAMMA GLUTAMYLTRANSFERASE; GLUCOSE; GLUTATHIONE; GLUTATHIONE TRANSFERASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONJUGATION; CONTROLLED STUDY; HORMONAL CARCINOGENESIS; HORMONE METABOLISM; KIDNEY CARCINOMA; NEPHROTOXICITY; NONHUMAN; PRIORITY JOURNAL; SYRIAN HAMSTER; URINARY EXCRETION;

ALKALINE PHOSPHATASE; ANIMALS; BILE; BIOTRANSFORMATION; CARCINOMA, RENAL CELL; CRICETINAE; ESTRADIOL; ESTROGENS, CATECHOL; GAMMA-GLUTAMYLTRANSFERASE; GLUTATHIONE; GLUTATHIONE TRANSFERASE; GLYCOSURIA; KIDNEY NEOPLASMS; KIDNEY TUBULES, PROXIMAL; MALE; MESOCRICETUS; MICROVILLI; OXIDATION-REDUCTION; SULFIDES;

EID: 0031417558     PISSN: 01433334     EISSN: None     Source Type: Journal    
DOI: 10.1093/carcin/18.3.561     Document Type: Article

References (61)

1. Thomas, D.B. (1978) Role of exogenous female hormones in altering the risk of benign and malignant neoplasms in humans. Cancer Res., 38, 3991-4000.
2. Bernstein, L. and Ross, R.K. (1993) Endogenous hormones and breast cancer risk. Epidemiol. Rev., 15, 48-65.
3. Matthews, V.S., Kirkman, H. and Bacon, R.L. (1947) Kidney damage in the golden hamster following chronic administration of diethylstilbestrol and sesame oil. Proc. Soc. Exp. Biol. Med., 66, 195-196.
4. Kirkman, H. and Bacon, R.L. (1952) Estrogen-induced tumors of the kidney. 1. Incidence of renal tumors in intact and gonadectomized male golden hamsters treated with diethylstilbestrol. J. Natl Cancer Inst., 13, 745-755.
5. Kirkman, H. (1959) Estrogen-induced tumors of the kidney III. Growth characteristics in the Syrian hamster. Natl Cancer Inst. Monogr., 1, 1-57.
6. Liehr, J.G. and Roy, D. (1990) Free radical generation of cycling estrogens. Free Rad. Biol. Med., 8, 415-423.
7. Monks, T.J., Anders, M.W., Dekant, W., Stevens, J.L., Lau, S.S. and van Bladeren, P.J. (1990) Contemporary issues in toxicology. Glutathione conjugate mediated toxicities. Toxicol. Appl. Pharmacol., 106, 1-19.
8. Monks, T.J. and Lau, S.S (1992) Toxicology of quinone-thioethers. Crit. Rev. Toxicol., 22, 243-270.
9. Monks, T.J. and Lau, S.S. (1994) Glutathione conjugation as a mechanism for the transport of reactive metabolites. In Anders, M.W. and Dekant, W. (eds), Advances in Pharmacology, Vol. 27: Conjugation-dependent Carcinogenicity and Toxicology of Foreign Compounds, Academic Press, New York, pp. 183-210.
10. Monks, T.J. and Lau, S.S. (1994) Glutathione conjugate mediated toxicities. In Kauffman, F.C. (ed.), Handbook of Experimental Pharmacology, Vol. 112: Conjugation-Deconjugation Reactions in Drug Metabolism and Toxicity, Springer-Verlag, New York, pp. 459-509.
11. Lau, S.S., Hill, B.A., Highet, R.J. and Monks, T.J. (1988) Sequential oxidation and glutathione addition to 1,4-benzoquinone: Correlation of toxicity with increased glutathione substitution. Molec. Pharmacol., 34, 829-836.
12. Lau, S.S., Kleiner, H.E. and Monks, T.J. (1995) Metabolism as a determinant of species susceptibility to 2,3,5-(triglutathion-S-yl)hydroquinone mediated nephrotoxicity. The role of N-acetylation and N-deacetylation. Drug Metab. Disp., 23, 1136-1142.
13. Rehwoldt, R. (1986) Tracking the use of antioxidants through industry surveys. Food Chem. Toxicol., 24, 1039-1041.
14. Clayson, D.B., Iverson, F., Nera, E.A. and Lok, E. (1990) The significance of induced forestomach tumors. Ann. Rev. Toxicol., 30, 441-446.
15. Tsuda, H., Fukushima, S., Imaida, K., Sakata, T. and Ito, N. (1984) Modification of carcinogenesis by antioxidants and other compounds. Acta Pharmacol. Toxicol., 2(Suppl.), 125-143.
16. Imaida, K., Fukushima, S., Shirai, T., Ohtani, M., Nakanishi, K. and Ito, N. (1983) Promoting activities of butylated hydroxyanisole and butylated hydroxytoluene on 2-stage urinary bladder carcinogenesis and inhibition of γ-glutamyl transpeptidase-positive foci development in the rat. Carcinogenesis, 4, 895-899.
17. Nera, E.A., Iverson, F., Lok, E., Armstrong, C.L., Karpinski, K. and Clayson, D.B. (1988) A carcinogenesis reversibility study of the effects of butylated hydroxyanisole on the forestomach and urinary bladder in male Fischer 344 rats. Toxicology, 53, 251-268.
18. Ito, N., Hirose, M., Fukushima, S., Tsuda, H., Shirai, T. and Tatematsu, M. (1986) Studies on antioxidants: their carcinogenic and modifying effects on chemical carcinogenesis. Food Chem. Toxicol., 24, 1071-1082.
19. Verhagen, H., Thijssen, H.H.W., Ten Hoor, F. and Kleinjans, J.C.S. (1989) Disposition of single oral doses of butylated hydroxyanisole in man and rat. Food Chem. Toxicol., 27, 151-158.
20. Shibata, M.A., Asakawa, E., Hagiwara, A., Kurata, Y. and Fukushima, S. (1991) DNA synthesis and scanning electron microscopic lesions in renal pelvic epithelium of rats treated with bladder cancer promoters. Toxicol. Lett., 55, 263-272.
21. Tamano, S., Fukushima, S., Shirai, T., Hirose, M. and Ito, N. (1987) Modification by α-tocopherol, propyl gallate and tertiary butylhydroquinone of urinary bladder carcinogenesis in Fischer 344 rats pretreated with N-butyl-N-(4-hydroxybutyl)nitrosamine. Cancer Lett., 35, 39-46.
22. Fukushima, S., Shibata, M.A., Kurata, Y., Tamano, S. and Masui, T. (1986) Changes in the urine and scanning electron microscopically observed appearance of the rat bladder following treatment with tumor promoters. Japan. J. Cancer Res., 77, 1074-1082.
23. Kurata, Y., Fukushima, S., Hasegawa, R., Hirose, M., Shibata, M.A., Shirai, T. and Ito, N. (1990) Structure-activity relations in promotion of rat urinary bladder carcinogenesis by phenolic antioxidants. Japan. J. Cancer Res., 81, 754-759.
24. Peters, M.M., Lau, S.S., Dulik, D.M., Murphy, D., van Ommen, B., van Bladeren, P.J. and Monks, T.J. (1996) Metabolism of 2-tert-butylhydroquinone to S-substituted conjugates in the male Fischer 344 rat. Chem. Res. Toxicol. 9, 133-139.
25. Peters, M.M., Jones, T.W., Monks, T.J. and Lau, S.S. (1996) Glutathione conjugates of 2-tert-butylhydroquinone, metabolites of the renal tumor promoter tert-butylhydroxyanisole, are toxic to kidney and bladder. Cancer Res., 56, 1006-1011.
26. Nelson, S.D., Mitchell, J.R., Dybing, E. and Sasame, H.A. (1976) Cytochrome P-450-mediated oxidation of 2-hydroxyestrogens to reactive intermediates. Biochem. Biophys. Res. Commun., 70, 1157-1165.
27. Marks, F. and Hecker, E. (1969) Metabolism and mechanism of action of estrogens. XII. Structure and mechanism of formation of water-soluble and protein-bound metabolites of estrone in rat liver microsomes in vitro and in vivo. Biochim. Biophys. Acta, 187, 250-265.
28. Kuss, E. (1969) Water-soluble metabolites of oestradiol-17β. III Separation and identification of 1-and 4-glutathione thioethers of 2,3-dihydroxyoestratrienes. Hoppe-Seylers, Z. Physiol Chem., 350, 95-97.
29. Kuss, E. (1971) Microsomal oxidation of estradiol-17β. 2-Hydroxylation and 1-or 4-thioether formation with and without 17-hydroxyl dehydrogenation. Hoppe-Seylers, Z. Physiol Chem. 352, 817-836.
30. Elce, J.S. (1970) Metabolism of a glutathione conjugate of 2-hydroxyestradiol by rat liver and kidney preparations in vitro. Biochem. J., 116, 913-917.
31. Elce, J.S. and Harris, J. (1971) Conjugation of 2-hydroxy-estradiol-17β[1,3,5 (10)-estratriene-2,3-17β-triol] with glutathione in the rat. Steroids, 18, 583-591.
32. Elce, J.S. (1972) Metabolism of a glutathione conjugate of 2-hydroxyoestradiol-17β in the adult male rat. Biochem. J., 126, 1067-1071.
33. Elce, J.S. and Chandra, J. (1973) Estrogen mercapturic acids in the adult male rat. Steroids, 22, 699-705.
34. Butterworth, M., Lau, S.S. and Monks, T.J. (1996) 17β-Estradiol metabolism in hamster liver microsomes. Implications for the catechol O-methyltransferase mediated detoxication of catechol estrogens. Drug Metab. Disp., 24, 588-594.
35. Jellinck, P.H. and Elce, J.S. (1969) Synthesis of estrogen glutathione and cysteine derivatives. Steroids, 13, 711-718.
36. Stalford, A.C., Maggs, J.L., Gilchrist, T.L. and Park, B.K. (1994) Catechol estrogens as mediators of carcinogenesis: Correlation of aromatic hydroxylation of estradiol and its fluorinated analogs with tumor induction in Syrian hamsters. Mol. Pharmacol., 45, 1259-1267.
37. Roy, D., Floyd, R.A. and Liehr, J.G. (1991) Elevated 8-hydroxy-deoxyguanosine levels in DNA of diethylstilbestrol-treated Syrian hamsters: Covalent DNA damage by free radicals generated by redox cycling of diethylstilbestrol. Cancer Res., 51, 3882-3885.
38. Buege, J.A and Aust, S.D. (1978) Microsomal lipid peroxidation. Meth. Enzymol., 52, 302-310.
39. Pryor, W.A. and Castle, L. (1984) Chemical methods for the detection of lipid hydroperoxides. Meth. Enzymol., 103, 293-299.
40. Oliver, C.N., Ahn, B.W., Moerman, E.J., Goldstein, S. and Stadtman, E.R., (1987) Age-related changes in oxidized proteins. J. Biol. Chem., 262, 55488-55491.
41. Habig, W.H., Pabst, M.J. and Jakoby, W.B. (1974) Glutathione-S-transferase, the first step in mercapturic acid formation. J. Biol. Chem., 249, 7130-7139.
42. Wicoxon, F. (1945) Individual comparisons by ranking methods. Biomet. Bull., 1, 80-83.
43. Mann, H.B. and Whitney, D.R. (1947) On a test of whether one of two random variables is stochastically larger than the other. Ann. Math. Statist., 18, 50-60.
44. Monks, T.J., Lau, S.S., Highet, R.J. and Gillette, J.R. (1985) Glutathione conjugates of 2-bromohydroquinone are nephrotoxic. Drug Metab. Dispos., 13, 533-559.
45. Monks, T.J., Highet, R.J. and Lau, S.S. (1988) 2-Bromo-(diglutatmon-S-yl)hydroquinone nephrotoxicity: Physiological, biochemical and electrochemical determinants. Mol. Pharmacol., 34, 492-500.
46. Monks, T.J. and Lau, S.S. (1990) Glutathione conjugation, γ-glutamyl transpeptidase and the mercapturic acid pathway as modulators of 2-bromohydroquinone oxidation. Toxicol. Appl. Pharmacol., 103, 557-563.
47. Li, J.J., Gonzalez, A., Banerjee, S., Banerjee, S.K. and Li, S.A. (1993) Estrogen carcinogenicity in hamster kidney: Role of cytotoxicity and cell proliferation. Environ. Health Perspect., 101, 259-264.
48. Gonzalez, A., Oberley, T.O. and Li, J.J. (1989) Morphological and immunohistochemical studies of the estrogen-induced Syrian hamster renal tumor: Probable cell of origin. Cancer Res., 49, 1020-1028.
49. Lau, S.S., Jones, T.W., Sioco, R., Hill, B.A., Pinon, R.K. and Monks, T.J. (1990) Species differences in renal γ-glutamyl transpeptidase activity do not correlate with susceptibility to 2-bromo-(diglutathion-S-yl)hydroquinone mediated nephrotoxicity. Toxicology, 64, 291-311.
50. Butterworth, M., Lau, S.S. and Monks, T.J. (1996) 17β-Estradiol metabolism by hamster liver microsomes. Comparison of catechol estrogen O-methylation with catechol estrogen oxidation and glutathione conjugation. Chem. Res. Toxicol., 9, 793-799.
51. Li, S.I., Purdy, R.H. and Li, S.A. (1989) Variations in catechol O-methyl transferase activity in rodent tissue. Carcinogenesis, 10, 63-67.
52. Rivera, M.I., Hinojosa, L.M., Hill, B.A., Lau, S.S. and Monks, T.J. (1994) Metabolism and toxicity of 2-bromo-(diglutathion-S-yl)hydroquinone and 2-bromo-3-(glutathion-S-yl)-hydroquinone in the in situ perfused rat kidney. Drug Metab. Disp., 22, 503-510.
53. Hill, B.A., Davison, K.L., Dulik, D.M., Monks, T.J. and Lau, S.S. (1994) Metabolism of 2-(glutathion-S-yl)-hydroquinone and 2,3,5-(triglutathion-S-yl)hydroquinone in the in situ perfused rat kidney: Relationship to nephrotoxicity. Toxicol. Appl. Pharm., 129, 121-132.
54. 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, 457-165.
55. Adlercreutz, H., Gorbach, S.L., Goldin, B.R., Woods, M.N., Dwyer, J.T. and Hämäläinen, E. (1994) Estrogen metabolism and excretion in Oriental and Caucasian women. J. Natl Cancer Inst., 86, 1076-1082.
56. Ball, P., Gelbke, H.P. and Knuppen, R. (1975) The excretion of 2-hydroxyestrone during the menstrual cycle. J. Clin. Endocrinol. Metab., 40, 406-408.
57. Williams, J.G., Longcope, C. and Williams, K.I.H. (1974) 4-Hydroxyestrone: A new metabolite of estradiol-17β from humans. Steroids, 24, 687-701.
58. 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.
59. Liehr, J.G. and Ricci, M.J. (1996) 4-Hydroxylation of estrogens as markers of human mammary tumors. Proc. Natl Acad. Sci. USA, 93, 3294-3296.
60. Dwivedy, I., Devanesan, P., Cremonesi, P., Rogan, E. and Cavalieri, E. (1992) Synthesis and characterization of estrogen 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.
61. Iverson, S.L., Shen, L., Anlar, N. and Bolton, J.L. (1996) Bioactivation of estrone and its catechol metabolites to quinoid-glutathione conjugates in rat liver microsomes. Chem. Res. Toxicol., 9, 492-499.