Estrogen-induced breast cancer: Alterations in breast morphology and oxidative stress as a function of estrogen exposure

Toxicology and Applied Pharmacology

Volumn 232, Issue 1, 2008, Pages 78-85

  Mense, Sarah M ^a   Remotti, Fabrizio ^b   Bhan, Ashima ^a   Singh, Bhupendra ^a   El Tamer, Mahmoud ^c   Hei, Tom K ^a   Bhat, Hari K ^a  

^a Public Health Columbia University   (United States)

^b Department of Medicine   (United States)

^c New York Presbyterian Columbia University Medical Center   (United States)

Author keywords

17 estradiol; ACI rat; Animal model of breast cancer; Breast cancer; Estrogen; Histopathology; Mammary tumor; Oxidative stress

Indexed keywords

8 ISOPROSTANE; CATALASE; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; FORMALDEHYDE; GLUTATHIONE PEROXIDASE; LIQUID NITROGEN; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER RISK; CELL PROLIFERATION; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVITY; FEMALE; FROZEN SECTION; HISTOPATHOLOGY; INVASIVE CARCINOMA; MORPHOLOGY; NONHUMAN; OXIDATIVE STRESS; QUANTITATIVE ANALYSIS; RAT; TIME; TISSUE FIXATION;

ANIMALS; CATALASE; CELL PROLIFERATION; DINOPROST; DISEASE MODELS, ANIMAL; DRUG IMPLANTS; ESTRADIOL; FEMALE; GLUTATHIONE PEROXIDASE; LIPID PEROXIDATION; MAMMARY GLANDS, ANIMAL; MAMMARY NEOPLASMS, EXPERIMENTAL; NEOPLASM INVASIVENESS; NEOPLASMS, HORMONE-DEPENDENT; OXIDATIVE STRESS; RATS; RATS, INBRED ACI; SUPEROXIDE DISMUTASE; TIME FACTORS; UP-REGULATION;

ANIMALIA; RATTUS;

EID: 51549099366     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2008.06.007     Document Type: Article

References (55)

1. Arnerlov C., Emdin S.O., Cajander S., Bengtsson N.O., Tavelin B., and Roos G. Intratumoral variations in DNA ploidy and s-phase fraction in human breast cancer. Anal. Cell. Pathol. 23 (2001) 21-28
2. Badawi A.F., Cavalieri E.L., and Rogan E.G. Role of human cytochrome P450 1A1, 1A2, 1B1, and 3A4 in the 2-, 4-, and 16alpha-hydroxylation of 17beta-estradiol. Metabolism 50 (2001) 1001-1003
3. Bhat H.K., Calaf G., Hei T.K., Loya T., and Vadgama J.V. Critical role of oxidative stress in estrogen-induced carcinogenesis. Proc. Natl. Acad. Sci. U. S. A 100 (2003) 3913-3918
4. Brueggemeier R.W., Bhat A.S., Lovely C.J., Coughenour H.D., Joomprabutra S., Weitzel D.H., Vandre D.D., Yusuf F., and Burak Jr. W.E. 2-Methoxymethylestradiol: a new 2-methoxy estrogen analog that exhibits antiproliferative activity and alters tubulin dynamics. J. Steroid Biochem. Mol. Biol. 78 (2001) 145-156
5. Cao K., Stack D.E., Ramanathan R., Gross M.L., Rogan E.G., and Cavalieri E.L. Synthesis and structure elucidation of estrogen quinones conjugated with cysteine, N-acetylcysteine, and glutathione. Chem. Res. Toxicol. 11 (1998) 909-916
6. Cavalieri E., Chakravarti D., Guttenplan J., Hart E., Ingle J., Jankowiak R., Muti P., Rogan E., Russo J., Santen R., and Sutter T. Catechol estrogen quinones as initiators of breast and other human cancers: implications for biomarkers of susceptibility and cancer prevention. Biochim. Biophys. Acta 1766 (2006) 63-78
7. Cavalieri E.L., and Rogan E.G. A unifying mechanism in the initiation of cancer and other diseases by catechol quinones. Ann. N.Y. Acad. Sci. 1028 (2004) 247-257
8. 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. Molecular origin of cancer: catechol estrogen-3,4-quinones as endogenous tumor initiators. Proc. Natl. Acad. Sci. U. S. A 94 (1997) 10937-10942
9. Clemons M., and Goss P. Estrogen and the risk of breast cancer. N. Engl. J. Med. 344 (2001) 276-285
10. Cracowski J.L., Durand T., and Bessard G. Isoprostanes as a biomarker of lipid peroxidation in humans: physiology, pharmacology and clinical implications. Trends Pharmacol. Sci. 23 (2002) 360-366
11. di Ilio C., Sacchetta P., del Boccio G., la Rovere G., and Federici G. Glutathione peroxidase, glutathione S-transferase and glutathione reductase activities in normal and neoplastic human breast tissue. Cancer Lett. 29 (1985) 37-42
12. Er T.K., Hou M.F., Tsa E.M., Lee J.N., and Tsai L.Y. Differential expression of manganese containing superoxide dismutase in patients with breast cancer in Taiwan. Ann. Clin. Lab. Sci. 34 (2004) 159-164
13. Felty Q., Singh K.P., and Roy D. Estrogen-induced G1/S transition of G0-arrested estrogen-dependent breast cancer cells is regulated by mitochondrial oxidant signaling. Oncogene 24 (2005) 4883-4893
14. Felty Q., Xiong W.C., Sun D., Sarkar S., Singh K.P., Parkash J., and Roy D. Estrogen-induced mitochondrial reactive oxygen species as signal-transducing messengers. Biochemistry 44 (2005) 6900-6909
15. Galati G., and O'Brien P.J. Potential toxicity of flavonoids and other dietary phenolics: significance for their chemopreventive and anticancer properties. Free Radic. Biol. Med. 37 (2004) 287-303
16. Gromadzinska J., Wasowicz W., Andrijewski M., Sklodowska M., Quispe O.Z., Wolkanin P., Olborski B., and Pluzanska A. Glutathione and glutathione metabolizing enzymes in tissues and blood of breast cancer patients. Neoplasma 44 (1997) 45-51
17. Han X., and Liehr J.G. DNA single-strand breaks in kidneys of Syrian hamsters treated with steroidal estrogens: hormone-induced free radical damage preceding renal malignancy. Carcinogenesis 15 (1994) 997-1000
18. Harvell D.M., Strecker T.E., Tochacek M., Xie B., Pennington K.L., McComb R.D., Roy S.K., and Shull J.D. Rat strain-specific actions of 17β-estradiol in the mammary gland: correlation between estrogen-induced lobuloalveolar hyperplasia and susceptibility to estrogen-induced mammary cancers. Proc. Natl. Acad. Sci. U. S. A 97 (2000) 2779-2784
19. IARC. Cancer incidence in five continents. Volume 9 (2007), International Agency for Research on Cancer, Lyon
20. IARC. IARC monographs on the evaluation of carcinogenic risks to humans: overall evaluations of carcinogenicity, an updating of IARC monographs volumes 1 to 42. Supplement 7 (1987), International Agency for Research on Cancer, Lyon
21. IARC. IARC monographs on the evaluation of carcinogenic risks to humans: hormonal contraception and postmenopausal hormone therapy 72 (1999), International Agency for Research on Cancer, Lyon 474-530
22. Iscan M., Coban T., Bulbul D., Eke B.C., Aygormez S., and Berberoglu U. Xenobiotic metabolizing and antioxidant enzymes in normal and neoplastic human breast tissue. Eur. J. Drug Metab. Pharmacokinet. 23 (1998) 497-500
23. Ju Y.H., Allred K.F., Allred C.D., and Helferich W.G. Genistein stimulates growth of human breast cancer cells in a novel, postmenopausal animal model, with low plasma estradiol concentrations. Carcinogenesis 27 (2006) 1292-1299
24. Kattan Z., Minig V., Leroy P., Dauca M., and Becuwe P. Role of manganese superoxide dismutase on growth and invasive properties of human estrogen-independent breast cancer cells. Breast Cancer Res. Treat. 108 (2008) 203-215
25. Key T., Appleby P., Barnes I., and Reeves G. Endogenous sex hormones and breast cancer in postmenopausal women: reanalysis of nine prospective studies. J. Natl. Cancer Inst. 94 (2002) 606-616
26. Kumaraguruparan R., Kabalimoorthy J., and Nagini S. Correlation of tissue lipid peroxidation and antioxidants with clinical stage and menopausal status in patients with adenocarcinoma of the breast. Clin. Biochem. 38 (2005) 154-158
27. LaVallee T.M., Zhan X.H., Herbstritt C.J., Kough E.C., Green S.J., and Pribluda V.S. 2-Methoxyestradiol inhibits proliferation and induces apoptosis independently of estrogen receptors alpha and beta. Cancer Res. 62 (2002) 3691-3697
28. Li J.J., and Li S.A. Estrogen carcinogenesis in Syrian hamster tissues: role of metabolism. Fed. Proc. 46 (1987) 1858-1863
29. Li J.J., Papa D., Davis M.F., Weroha S.J., Aldaz C.M., El-Bayoumy K., Ballenger J., Tawfik O., and Li S.A. Ploidy differences between hormone- and chemical carcinogen-induced rat mammary neoplasms: comparison to invasive human ductal breast cancer. Mol. Carcinog. 33 (2002) 56-65
30. Li J.J., Weroha S.J., Lingle W.L., Papa D., Salisbury J.L., and Li S.A. Estrogen mediates Aurora-A overexpression, centrosome amplification, chromosomal instability, and breast cancer in female ACI rats. Proc. Natl. Acad. Sci. U. S. A 101 (2004) 18123-18128
31. Li S.A., Weroha S.J., Tawfik O., and Li J.J. Prevention of solely estrogen-induced mammary tumors in female aci rats by tamoxifen: evidence for estrogen receptor mediation. J. Endocrinol. 175 (2002) 297-305
32. Liehr J.G., Fang W.F., Sirbasku D.A., and Ari-Ulubelen A. Carcinogenicity of catechol estrogens in Syrian hamsters. J. Steroid Biochem. 24 (1986) 353-356
33. 32P-postlabelling in studies of hormonal carcinogenesis. IARC Scientific Publications 124 (1993) 149-155
34. Makris A., Allred D.C., Powles T.J., Dowsett M., Fernando I.N., Trott P.A., Ashley S.E., Ormerod M.G., Titley J.C., and Osborne C.K. Cytological evaluation of biological prognostic markers from primary breast carcinomas. Breast Cancer Res. Treat. 44 (1997) 65-74
35. McPherson K., Steel C.M., and Dixon J.M. ABC of breast diseases. Breast cancer-epidemiology, risk factors, and genetics. BMJ. 321 (2000) 624-628
36. Milne G.L., Sanchez S.C., Musiek E.S., and Morrow J.D. Quantification of F2-isoprostanes as a biomarker of oxidative stress. Nat. Protoc. 2 (2007) 221-226
37. Milne G.L., Yin H., and Morrow J.D. Human biochemistry of the isoprostane pathway. J. Biol. Chem. 283 (2008) 15533-15537
38. Montuschi P., Barnes P.J., and Roberts II L.J. Isoprostanes: markers and mediators of oxidative stress. FASEB J. 18 (2004) 1791-1800
39. Mukhopadhyay S., Das S.K., and Mukherjee S. Expression of Mn-superoxide dismutase gene in nontumorigenic and tumorigenic human mammary epithelial cells. J. Biomed. Biotechnol. 2004 (2004) 195-202
40. Naiki-Ito A., Asamoto M., Hokaiwado N., Takahashi S., Yamashita H., Tsuda H., Ogawa K., and Shirai T. Gpx2 is an overexpressed gene in rat breast cancers induced by three different chemical carcinogens. Cancer Res. 67 (2007) 11353-11358
41. Nelson H.D., Humphrey L.L., Nygren P., Teutsch S.M., and Allan J.D. Postmenopausal hormone replacement therapy: scientific review. JAMA 288 (2002) 872-881
42. NTP. Report on Carcinogens (2002), National Toxicology Program, Research Triangle Park
43. Patel M.M., and Bhat H.K. Differential oxidant potential of carcinogenic and weakly carcinogenic estrogens: involvement of metabolic activation and cytochrome P450. J. Biochem. Mol. Toxicol. 18 (2004) 37-42
44. Ries L., Melbert D., Krapcho M., Mariotto A., Miller B.A., Feuer E.J., Clegg L., Horner M.J., Howlader N., Eisner M.P., Reichman M., and Edwards B.K. SEER Cancer Statistics Review, 1975-2004 (2007), National Cancer Institute, Bethesda
45. Rossouw J.E., Anderson G.L., Prentice R.L., LaCroix A.Z., Kooperberg C., Stefanick M.L., Jackson R.D., Beresford S.A., Howard B.V., Johnson K.C., Kotchen J.M., and Ockene J. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA 288 (2002) 321-333
46. Roy D., Cai Q., Felty Q., and Narayan S. Estrogen-induced generation of reactive oxygen and nitrogen species, gene damage, and estrogen-dependent cancers. J. Toxicol. Environ. Health B. Crit. Rev. 10 (2007) 235-257
47. Shull J.D., Spady T.J., Snyder M.C., Johansson S.L., and Pennington K.L. Ovary-intact, but not ovariectomized female ACI rats treated with 17beta-estradiol rapidly develop mammary carcinoma. Carcinogenesis 18 (1997) 1595-1601
48. Singh S.V., Brunnert S.R., Roberts B., and Krishan A. Differential expression of glutathione S-transferase, glutathione peroxidase and glutathione reductase in normal and malignant human breast tissues. Cancer Lett. 51 (1990) 43-48
49. Tsanou E., Ioachim E., Briasoulis E., Damala K., Charchanti A., Karavasilis V., Pavlidis N., and Agnantis N.J. Immunohistochemical expression of superoxide dismutase (MnSOD) anti-oxidant enzyme in invasive breast carcinoma. Histol. Histopathol. 19 (2004) 807-813
50. Wang M.Y., and Liehr J.G. Induction by estrogens of lipid peroxidation and lipid peroxide-derived malonaldehyde-DNA adducts in male Syrian hamsters: role of lipid peroxidation in estrogen-induced kidney carcinogenesis. Carcinogenesis 16 (1995) 1941-1945
51. Weroha S.J., Li S.A., Tawfik O., and Li J.J. Overexpression of cyclins D1 and D3 during estrogen-induced breast oncogenesis in female ACI rats. Carcinogenesis 27 (2006) 491-498
52. Weydert C.J., Waugh T.A., Ritchie J.M., Iyer K.S., Smith J.L., Li L., Spitz D.R., and Oberley L.W. Overexpression of manganese or copper-zinc superoxide dismutase inhibits breast cancer growth. Free Radic. Biol. Med. 41 (2006) 226-237
53. Yager J.D. Endogenous estrogens as carcinogens through metabolic activation. J. Natl. Cancer Inst. Monogr. 27 (2000) 67-73
54. Yager J.D., and Davidson N.E. Estrogen carcinogenesis in breast cancer. N. Engl. J. Med. 354 (2006) 270-282
55. Ziegler R.G., Rossi S.C., Fears T.R., Bradlow H.L., Adlercreutz H., Sepkovic D., Kiuru P., Wahala K., Vaught J.B., Donaldson J.L., Falk R.T., Fillmore C.M., Siiteri P.K., Hoover R.N., and Gail M.H. Quantifying estrogen metabolism: an evaluation of the reproducibility and validity of enzyme immunoassays for 2-hydroxyestrone and 16alpha-hydroxyestrone in urine. Environ. Health Perspect. 105 Suppl. 3 (1997) 607-614