Dietary indole-3-carbinol promotes endometrial adenocarcinoma development in rats initiated with N-ethyl-N′ -nitro-N-nitrosoguanidine, with induction of cytochrome P450s in the liver and consequent modulation of estrogen metabolism

Carcinogenesis

Volumn 25, Issue 11, 2004, Pages 2257-2264

  Yoshida, Midori ^a   Katashima, Sayumi ^a   Ando, Jin ^a   Tanaka, Takuji ^b   Uematsu, Fumiyuki ^a   Nakae, Dai ^a   Maekawa, Akihiko ^a  

^a SASAKI INSTITUTE   (Japan)

^b KANAZAWA MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

3 INDOLEMETHANOL; 4 HYDROXYESTRADIOL; ANTIESTROGEN; CYTOCHROME P450; CYTOCHROME P450 1A1; CYTOCHROME P450 1A2; CYTOCHROME P450 1B1; ESTRADIOL; ESTROGEN; ETHYLNITRONITROSOGUANIDINE; MESSENGER RNA; STEROID 16ALPHA MONOOXYGENASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CANCER PREVENTION; CARCINOGENESIS; CONTROLLED STUDY; CRUCIFERA; ENDOMETRIUM CARCINOMA; ENZYME ACTIVITY; ENZYME INDUCTION; ESTROGEN ACTIVITY; ESTROGEN METABOLISM; FEMALE; IMMUNOHISTOCHEMISTRY; LIVER METABOLISM; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; RAT; STEROID HYDROXYLATION; UTERUS HORN; VEGETABLE;

ADENOCARCINOMA; ANIMALS; CARCINOGENS; CYTOCHROME P-450 ENZYME SYSTEM; DISEASE MODELS, ANIMAL; ENDOMETRIAL NEOPLASMS; ENZYME INDUCTION; ESTROGEN ANTAGONISTS; ESTROGENS; FEMALE; INDOLES; LIVER; RATS;

EID: 8844252309     PISSN: 01433334     EISSN: None     Source Type: Journal    
DOI: 10.1093/carcin/bgh225     Document Type: Article

References (55)

1. Jongen,W. (1996) Glucosinolates in brassica: occurrence and significance as cancer-modulating agents. Proc. Nutr. Soc., 55 433-446.
2. Meng,Q., Yuan,F., Goldberg,I.D., Rosen,E.M., Auborn,K. and Fan,S. (2000) Indole-3-carbinol is a negative regulator of estrogen receptor-α signaling in human tumor cells. J. Nutr., 130, 2927-2931.
3. Michnovicz,J.J. and Bradlow,H.L. (1990) Induction of estradiol metabolism by dietary indole-3-carbinol in humans. J. Natl Cancer Inst., 82, 947-949.
4. Michnovicz,J.J., Adlecreutz,H. and Bradlow,H.L. (1997) Changes in levels of urinary estrogen metabolites after oral indole-3-carbinol treatment in humans. J. Natl Cancer Inst., 89 718-823.
5. Bonnesen,C., Eggleston,I.M. and Hayes,J.D. (2001) Dietary indoles and isothiocyanates that are generated from cruciferous vegetables can both stimulate apoptosis and confer protection against DNA damage in human colon cell lines. Cancer Res., 61, 6120-6130.
6. Bradlow,H.L., Michnovicz,J.J., Telang,N.T. and Osborne,M.P. (1991) Effects of dietary indole-3-carbinol on estradiol metabolism and spontaneous mammary tumors in mice. Carcinogenesis, 12, 1571-1574.
7. Kojima,T., Tanaka,T. and Mori,H. (1994) Chemoprevention of spontaneous endometrial cancer in female Donryu rats by dietary indole-3-carbinol. Cancer Res., 54, 1446-1449.
8. Wattenberg,L.W. and Loub,W.D. (1978) Inhibition of polycystic aromatic hydrocarbon induced neoplasia by naturally occurring indoles. Cancer Res., 38, 1410-1413.
9. Babich,B.S., Borenfreund,E. and Stem,A. (1993) Comparative cytotoxicities of selected minor dietary non-nutrients with chemopreventive properties. Cancer Lett., 73, 1410-1413.
10. Reddy,B.S., Hanson,D., Mathews,L. and Sharma,C. (1983) Effects of micronutrients, antioxidants and related compounds on the mutagenicity of 3,2′-dimethyl-4-aminobiphenyl, a colon and breast carcinogen. Food Chem. Toxicol., 21, 129-132.
11. Exon,J.H., South,E.H., Magnuson,B.A. and Hendrix,K. (2001) Effects of indole-3-carbinol on immune response, aberrant crypt foci and colonic crypt cell proliferation in rats. J. Toxicol. Environ. Health Part A, 62, 561-573.
12. Stoner,G., Casto,B., Ralston,S., Roebuck,B., Pereira,C. and Bailey,G. (2002) Development of a multi-organ rat model for evaluating chemopreventive agents: efficacy of indole-3-carbinol. Carcinogenesis 23, 265-272.
13. Dashwood,R.H. and Xu,M. (2003) The disposition and metabolism of 2-amino-3-methylimidazo[4,5-f]quinoline in the F344 rat at high versus low doses of indole-3-carbinol. Food Chem. Toxicol., 41, 1185-1192.
14. Nho,C.W. and Jeffery,E. (2001) The synergistic upregulation of phase II detoxication enzymes by glucosinolate breakdown products in cruciferous vegetables. Toxicol. Appl. Pharmacol., 174, 146-152.
15. Ritter,C.L., Prigge,W.F., Reichert,M.A. and Malejka-Giganti,D. (2001) Oxidations of 17β-estradiol and estrone and their interconversions catalyzed by liver, mammary gland and mammary tumor after acute and chronic treatment of rats with indole-3-carbinol or β-naphthoflavone. Can. J. Physiol. Pharmacol., 79, 519-532.
16. He,Y.H., Friesen,M.D., Ruch,R.J. and Schut,H.A. (2000) Indole-3-carbinol as a chemopreventive agent in 2-amino-1-methyl-6-phenyl-imidazo [4,5-b]pyridine (PhIP) carcinogenesis: inhibition of PhIP-DNA adduct formation, acceleration of PhIP metabolism and induction of cytochrome P450 in female F344 rats. Food Chem. Toxicol., 38, 15-23.
17. Park,J.Y. and Bjeldanes,L.F. (1992) Organ-selective induction of cytochrome P-450-dependent activities by indole-3-carbinol-derived products: influence on covalent binding of benzo[a]pyrene to hepatic and pulmonary DNA in the rat. Chem. Biol. Interact., 83, 235-247.
18. Stresser,D.M., Bailey,G.S. and Williams,D.E. (1994) Indole-3-carbinol and β-naphthoflavone induction of aflatoxin B1 metabolism and cytochrome P-450 associated with bioactivation and detoxication of aflatoxin B1 in the rat. Drug Metab. Dipos., 22 383-391.
19. Xu,M., Schut,H.A., Bfeldanes,L.F., Williams,D.E., Bailey,G..S. and Dashwood,R.H. (1997) Inhibition of 2-amino-3-methylimidazo[4,5-f]quinoline-DNA adducts by indole-3-carbinol: dose-response studies in the rat colon. Carcinogenesis, 18, 2149-2153.
20. Horn,T.L., Reichert,M.A., Bliss,R.L. and Malejka-Giganti,D. (2002) Modulations of P450 mRNA in liver and mammary gland and P450 activities and metabolism of estrogen in liver by treatment of rats with indole-3-carbinol. Biochem. Pharmacol., 64, 393-404.
21. Leibelt,D.A., Hedstrom,O.R., Fischer,K.A., Pereira,C.B. and Williams,D.E. (2003) Evaluation of chronic dietary exposure to indole-3-carbinol and absorption-enhanced 3,3′-diindolylmethane in Sprague-Dawley rats. Toxicol. Sci., 74, 10-21.
22. Dannan,G.A., Porubek,D.J., Nelson,S.D., Waxman,D.J. and Guencerich,E.P. (1986) 17β-Estradiol 2- and 4-hydroxylation catalyzed by rat hepatic cytochrome P-450: roles of individual forms, inductive effects, developmental patterns and alterations by gonadectomy and hormone replacement. Endocrinology, 118, 1952-1960.
23. Hammond,D.K., Zhu,B.T., Wang,M.Y., Ricci,M.J. and Liehr,J.G. (1997) Cytochrome P450 metabolism of estradiol in hamster liver and kidney. Toxicol. Appl. Pharmacol., 145, 54-60.
24. Zhu,B.T. and Conney,A.H. (1998) Functional role of estrogen metabolism in target cells: review and perspectives. Carcinogenesis 19, 1-27.
25. Wilson,A.M. and Reed,G.A. (2001) Predominant 4-hydroxylation of estradiol by constitutive cytochrome P450s in the female ACI rat liver. Carcinogenesis, 22, 257-263.
26. Badawi,A.F., Cavalieri,E.L. and Rogan,E.G. (2000) Effect of chlorinated hydrocarbons on expression of cytochrome P450 1A1, 1A2 and 1B1 and 2- and 4-hydroxylation of 17β-estradiol in female Sprague-Dawley rats. Carcinogenesis, 21, 1593-1599.
27. Van Aswegen,C.H., Purdy,R.H. and Wittliff,J.L. (1989) Binding to 2-hydroxyestradiol and 4-hydroxyestradiol to estrogen receptor human breast cancers. J. Steroid Biochem., 32, 485-492.
28. MacLusky,N.J., Barnea,E.R., Clark,C.R. and Naftolin,F. (1983) Catechol estrogens and estrogen receptors. In Merrian,G.R. and Lipsett,M.B. (eds) Catechol Estrogens. Raven Press, New York, pp. 151-165.
29. Liehr,J.G. (2000) Is estradiol a genotoxic mutagenic carcinogen? Endocrine Rev., 21, 40-54.
30. Marticci,C.P. and Fishman,J. (1993) P450 enzymes of estrogen metabolism. Pharmacol. Ther., 57, 237-257.
31. Liehr,J.G., Fang,W.F., Sirbasku,D.A. and Ari-Ulubelen,A. (1986) Carcinogenicity of catechol estrogens in Syrian hamster. J. Steroid Biochem., 24, 353-356.
32. 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. USA, 92, 9220-9224.
33. Liehr,J.G. and Ricci,M.J. (1996) 4-Hydroxylation of estrogens and markers of human mammary tumors. Proc. Natl Acad. Sci. USA, 93, 3294-3296.
34. Segura-Aguilar,J., Castro,V. and Bergman,A. (1997) Effects of four organohalogen environmental contaminants on cytochrome P450 forms that catalyze 4- and 2-hydroxylation of estradiol in the rat liver. Biochem. Mol. Med., 60, 149-154.
35. Suchar,L.A., Chang,R.L., Thomas,P.E., Rosen,R.T., Lech,J. and Conney,A.H. (1996) Effects of phenobarbital, dexamethasone and 3-methylcholanthrene administration on the metabolism of 17β -estradiol by liver microsomes from female rats. Endocrinology, 137, 663-676.
36. Maekawa,A., Onodera,H., Tanigawa,H., Furuta,K., Kanno,J., Matsuoka,C., Ogiu,T. and Hayashi,Y. (1986) Spontaneous neoplastic and non-neoplastic lesions in aging Donryu rats. Jpn. J. Cancer Res., 77, 882-890.
37. Nagaoka,T., Onodera,H., Matsushima,Y. Todate,A., Shibutani,M., Ogasawara,H. and Meakawa,A. (1990) Spontaneous uterine adenocarcinomas in aged rats and their relation to endocrine imbalance. J. Cancer Res. Clin. Oncol., 116, 623-628.
38. Nagaoka,T., Takeuchi,M., Onodera,H., Matsushima,Y., Ando-Lu,J. and Maekawa,A. (1994) A sequential observation of spontaneous endometrial adenocarcinoma development in Donryu rats. Toxicol. Pathol., 22, 261-269.
39. Ando-Lu,J., Takahashi,M., Imai,S., Ishihara,R., Kitamura,T., Iijima,T., Takano,S., Nishiyama,K., Suzuki,K. and Maekawa,A. (1994) High-yield induction of endometrial adenocarcinomas in Donryu rats by a single intra-uterine administration of N-ethyl-N′-nitro-N-nitrosoguanidine. Jpn. J. Cancer Res., 85 789-793.
40. Maekawa,A., Takahashi,M., Ando,J. and Yoshida,M. (1999) Uterine carcinogenesis by chemicals/hormones in rodents. J. Toxicol. Pathol., 12, 1-11.
41. Nishiyama,K., Ando-Lu,J., Nishimura,S., Takahashi,M., Yoshida,M., Sasahara,K., Miyajima,K. and Maekawa,A. (1998) Initiating and promoting effects of concurrent oral administration of ethylenethiourea and sodium nitrite on uterine endometrial adenocarcinoma development in Donryu rats. In Vivo, 12, 363-368.
42. Yoshida,M., Kudoh,K., Katsuda,S., Takahashi,M., Ando,J. and Maekawa,A. (1998) Inhibitory effects of uterine endometrial carcinogenesis in Donryu rats by tamoxifen. Cancer Lett., 134 43-51.
43. Pecorelli,S., Benedet,J.L., Creasman,W.T. and Shepherd,J.H. (1999) FIGO staging of gynecologic cancer. Int. J. Gynecol. Obstet. 64, 5-10.
44. Shimada,T., Sugie,A., Shindo,A., Nakajima,J., Azuma,E., Hashimoto,M. and Inoue,K. (2003) Tissue-specific induction of cytochrome P450 1A1 and 1B1 by polycyclic aromatic hydrocarbons and polychlorinated biphenyls in engineered C57BL/6 J mice of arylhydrocarbon gene. Toxicol. Appl. Pharmacol., 187, 1-10.
45. Walker,N.J., Portier,C.J., Lax,S.F., Crofits,F.G., Li,Y., Lucier,G.W. and Sutter,T.R. (1999) Characterization of the dose-response of CYP1B1, CYP1A1 and CYP1A2 in the liver of female Sprague-Dawley rats following chronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxiol. Appl. Pharmacol., 154, 279-286.
46. Chen,I., Safe,S. and Bjeldances,L. (1996) Indole-3-carbinol and diindolylmethane as aryl hydrocarbon (Ah) receptor agnosits and antagonists in T47D human breast cancer cells. Biochem. Pharmacol., 51, 1069-1076.
47. Chen,I., AcDougal,A., Wang,F. and Safe,S. (1998) Aryl hydrocarbon receptor-mediated antiestrogenic and antitumorigenic activity of diindolylmethane. Carcinogenesis, 19, 1631-1639.
48. Newbold,R.R. and Lier,J.G. (2000) Induction of uterine adenocarcinoma in CD-1 mice by catechol estrogens. Cancer Res., 60, 235-237.
49. Katsuda,S., Yoshida,M., Kuroda,H., Ando,J., Takahashi,M., Kurokawa,Y., Watanabe,G., Taya,K. and Maekawa,A. (2002) Uterine adenocarcinoma in N-ethyl-N′-nitro-N-nitrosoguanidine-treated rats with high-dose exposure to p-tert-octylphenol during adulthood. Jpn. J. Cancer Res., 93, 117-124.
50. Yoshida,M., Katsuda,S., Tanimoto,T., Asai,S., Nakae,D., Kurokawa,Y., Taya,K. and Maekawa,A. (2002) Induction of different types of uterine adenocarcinornas in Donryu rats due to neonatal exposure to high-dose p-t-octylphenol for different periods. Carcinogenesis, 23, 1745-1750.
51. Hatanaka,N., Yamazaki,H., Kizu,R., Hayakawa,K., Aoki,Y., Iwanari,M., Nakajima,M. and Yokoi,T. (2001) Induction of cytochrome P450 1B1 in lung, liver and kidney of rats exposed to diesel exhaust. Carcinogenesis, 22, 2033-2038.
52. Santostefano,M.J., Richardson,V.M., Walker,N.J., Blanton,J., Lindros,K.O., Lucier,G.W., Alcasey,S.K. and Birnbaum,L.S. (1999) Dose-dependent localization of TCDD in isolated centrilobular and periportal hepatocytes. Toxicol. Sci., 52, 9-19.
53. Counmoul,X., Diry,M., Robillot,C. and Barouki,R. (2001) Differential regulation of cytochrome P450 1A1 and 1B1 by a combination of dioxin and pesticides in the breast tumor cell line MCF-7. Cancer Res., 61, 3942-3948.
54. Shimada,T., Hayes,C.H., Yamazaki,H., Amin,S., Hecht,S.S., Guengerich,P.F. and Sutter,T.R. (1996) Activation of chemically diverse procarcinogens by human cytochrome P-450 1B1. Cancer Res., 56 2979-2984.
55. Parkinson,A. (1996) An overview of current cytochrome P450 technology for assessing the safety and efficacy of new materials. Toxicol. Pathol., 24, 45-57.