17-Beta-estradiol induces transformation and tumorigenesis in human breast epithelial cells

FASEB Journal

Volumn 20, Issue 10, 2006, Pages 1622-1634

  Russo, Jose ^a   Fernandez, Sandra V ^a   Russo, Patricia A ^a   Fernbaugh, Rachael ^a   Sheriff, Fathima S ^a   Lareef, Hasan M ^a   Garber, James ^a   Russo, Irma H ^a  

^a FOX CHASE CANCER CENTER   (United States)

Author keywords

Breast cancer; CGH; Estrogen; Invasiveness

Indexed keywords

ESTRADIOL; ESTROGEN RECEPTOR ALPHA; KERATIN; MATRIGEL; PROGESTERONE RECEPTOR; UVOMORULIN;

ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CARCINOGENESIS; CHROMOSOME DELETION; CHROMOSOME LOSS; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; GENE MUTATION; GENE SEQUENCE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; BREAST TUMOR; CANCER INVASION; CELL LINE; CELL TRANSFORMATION; CHEMICALLY INDUCED DISORDER; CHROMOSOME ABERRATION; GENETICS; PATHOLOGY;

BREAST NEOPLASMS; CELL LINE; CELL TRANSFORMATION, NEOPLASTIC; CHROMOSOME ABERRATIONS; EPITHELIAL CELLS; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; HUMANS; NEOPLASM INVASIVENESS; RECEPTORS, PROGESTERONE;

EID: 33749321931     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.05-5399com     Document Type: Article

References (82)

1. Beatson, G. (1896) On the treatment of inoperable cases of carcinoma of the mammary. Suggestions for a new method of treatment with illustrative cases. Lancet 2, 104-107
2. Boyd, S. (1900) An oophorectomy in cancer of the breast. Br. Med. J. 2, 1161-1167
3. Block, G. (1958) Estrogen excretion following operative and irradiation castration in cases of mammary cancer. Surgery 43, 415-422
4. Toft, D., Shyamala, G., and Gorski, J. (1967) A receptor molecule for estrogens: studies using a cell free system. Proc. Natl. Acad. Sci. USA 57, 1740-1743
5. Green, S., Walter, P., Greene, G., Krust, A., Goffin, C., Jensen, E., Scrace, G., Waterfield, M., and Chambon, P. (1986) Cloning of the human estrogen receptor cDNA. J. Steroid Biochem. 24, 77-83
6. Dorgan, J. F., Longcope, C., Stephenson, H. E., Jr., Falk, R. T., Miller, R., Franz, C., Kahle, L., Campbell, W. S., Tangrea, J. A., and Schatzkin, A. (1996) Relation of prediagnostic serum estrogen and androgen levels to breast cancer risk. Cancer Epidemiol. Biomarkers Prev. 5, 533-539
7. Dorgan, J. F., Stanczyk, F. Z., Longcope, C., Stephenson, H. E., Jr., Chang, L., Miller, R., Franz, C., Falk, R. T., and Kahle, L. (1997) Relationship of serum dehydroepiandrosterone (DHEA), DHEA sulfate, and 5-androstate-3β, 17β-diol to risk of breast cancer in postmenopausal women. Cancer Epidemiol. Biomarkers Prev. 6, 177-181
8. Thomas, H. V., Key, T. J., Allen, D. S., Moore, J. W., Dowsett, M., Fentiman, I. S., and Wang, D. Y. (1997) A prospective study of endogenous serum hormone concentrations and breast cancer risk in postmenopausal women on the island of Guernsey. Br. J. Cancer. 76, 401-405
9. Hankinson, S. E., Willett, W. C., Manson, J. E., Colditz, G. A., Hunter, D. J., Spiegelman, D., Barbieri, R. L., and Speizer, F. E. (1998) Plasma sex steroid hormone levels and risk of breast cancer in postmenopausal women. J. Natl. Cancer Inst. 90, 1292-1299
10. Toniolo, P. G., Levitz, M., Zeleniuch-Jacquotte, A., Banerjee, S., Koenig, K. L., Shore, R. E., Strax, P., and Pasternack, B. S. (1995) A prospective study of endogenous estrogens and breast cancer in postmenopausal women. J. Natl. Cancer Inst. 87, 190-197
11. Berrino, F., Muti, P., Micheli, A., Bolelli, G., Krogh, V., Sciajno, R., Pisani, P., Panico, S., and Secreto, G. (1996) Serum sex hormone levels after menopause and subsequent breast cancer. J. Natl. Cancer Inst. 88, 291-296
12. Garland, C. F., Friedlander, N. J., Barrett-Connor, E., and Khaw, K.-T. (1992) Sex hormones and postmenopausal breast cancer: a prospective study in an adult community. Am. J. Epidemiol. 135, 1220-1230
13. Kabuto, M., Akiba, S., Stevens, R. G., Neriiski, K., and Land, C. E. (2000) A prospective study of estradiol and breast cancer in Japanese women. Cancer Epidemiol. Biomarkers Prev. 9, 575-579
14. Cauley, J. A., Lucas, F. L., Kuller, L. H., Stone, K., Browner, W., and Cummings, S. R., for the Study of Osteoporotic Fractures Research Group. (1999) Elevated serum estradiol and testosterone concentrations are associated with a high risk for breast cancer. Ann. Intern. Med. 130, 270-277
15. Helzlsouer, K. J., Alberg, A. J., Bush, T. L., Longcope, C., Gordon, G. B., and Comstock, G. W. (1994) A prospective study of endogenous hormones and breast cancer. Cancer Detect. Prev. 18, 79-85
16. Endogenous Hormones and Breast Cancer Collaborative Group. (2002) Endogenous sex hormones and breast cancer in postmenopausal women: reanalysis of nine prospective studies. J. Natl. Cancer Inst. 94, 606-616
17. Henderson, B. E., Ross, R., and Bernstein, L. (1988) Estrogens as a cause of human cancer: the Richard and Hinda Rosenthal Foundation award lecture. Cancer Res. 48, 246-253
18. Pike, M. C., Spicer, D. V., Dahmoush, L., and Press, M. F. (1993) Estrogens, progestagens, normal breast cell proliferation, and breast cancer risk. Epidemiol. Rev. 15, 17-35
19. Kelsey, J. L., Gammon, M. D., and John, E. M. (1993) Reproductive factors and breast cancer. Epidemiol. Rev. 15, 36-47
20. Bernstein, L., and Ross, R. K. (1993) Endogenous hormones and breast cancer risk. Epidemiol. Rev. 15, 48-65
21. Russo, J., Ao, X., Grill, C., and Russo, I. H. (1999) Pattern of distribution of cells positive for estrogen receptor alpha and progesterone receptor in relation to proliferating cells in the mammary gland. Breast Cancer Res. Treat. 53, 217-227
22. Russo, I. H., and Russo, J. (2005) The role of estrogen in breast cancer. In Molecular Basis of Breast Cancer Prevention and Treatment (Russo, J., and Russo, I. H., eds) pp. 89-136, Springer-Verlag, Heidelberg
23. Miller, W. R., and O'Neill, J. (1987) The importance of local synthesis of estrogen within the breast. Steroids 50, 537-548
24. Russo, J., Hu, Y. F., and Russo, I. H. (2000) Estrogens and breast cancer in humans. In Endocrine Disrupters of the Environment (Metzler, M., ed) pp. 1-26, Springer-Verlag, Heidelberg
25. Li, J. J., Li, S. A., Klicka, J. K., Parsons, J. A., and Lam, L. K. (1983) Relative carcinogenic activity of various synthetic and natural estrogens in the Syrian hamster kidney. Cancer Res. 43, 5200-5204
26. 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
27. Yager, J. D. (2000) Endogenous estrogens as carcinogens through metabolic activation. J. Natl. Cancer Institute Monogr. 27, 67-73
28. Russo, I. H., and Russo, J. (1996) Mammary gland neoplasia in long-term rodent studies. Environ. Health Perspect. 104, 938-967
29. Meites, J. (1972) Relation of prolactin and estrogen to mammary tumorigenesis in the rat. J. Natl. Cancer Inst. 48, 1217-1223
30. Bocchinfuso, W. P., and Korach, K. S. (1997) Mammary gland development and tumorigenesis in estrogen receptor knockout mice. J. Mammary Gland Biol. Neoplasia 2, 323-334
31. Bocchinfuso, W. P., Hively, W. P., Couse, J. F., Varmus, H. E., and Korach, K. S. (1999) A mouse mammary tumor virus-Wnt1 transgene induces mammary gland hyperplasia and tumorigenesis in mice lacking estrogen receptor-alpha. Cancer Res. 59, 1869-1876
32. Cavalieri, E. L., Kumar, S., Todorovic, R., Higginbotham, S., Badawi, A. F., and Rogan, E. G. (2001) Imbalance of estrogen homeostasis in kidney and liver of hamsters treated with estradiol: implications for estrogen-induced initiation of renal tumors. Chem. Res. Toxicol. 14, 1041-1050
33. Rogan, E. G., Badawi, A. F., Devanesan, P. D., Meza, J. L., Edney, J. A., West, W. W., Higginbotham, S. M., and Cavalieri, E. L. (2003) Relative imbalances in estrogen metabolism and conjugation in breast tissue of women with carcinoma: Potential biomarkers of susceptibility to cancer. Carcinogenesis 24, 697-702
34. 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. USA,. 99, 10937-10942
35. Liehr, J. G., Fang, W. F., Sirbasku, D. A., and Ari-Ulubelen, A. (1986) Carcinogenicity of catecholestrogens in Syrian hamsters. J. Steroid Biochem. 24, 353-356
36. Li, J. J., and Li, S. A. (1987) Estrogen carcinogenesis in Syrian hamster tissue: Role of metabolism. Federation Proc. 46, 1858-1863
37. Newbold, R. R., and Liehr, J. G. (2000) Induction of uterine adenocarcinoma in CD-1 mice by catechol estrogens. Cancer Res. 60, 235-237
38. Chakravarti, D., Mailander, P., Li, K-M., Higginbotham, S., Zhang, H. L., Gross, M. L., Meza, J. L., Cavalieri, E. L., and Rogan, E. G. (2001) Evidence that a burst of DNA depurination in SENCAR mouse skin induces error-prone repair and forms mutations in the H-ras gene. Oncogene 20, 7945-7953
39. Russo, J., Lareef, M. H., Tahin, Q., Hu, Y. F., Slater, C., Ao, X., and Russo, I. H. (2002) 17β-Estradiol is carcinogenic in human breast epithelial cells. J. Steroid Biochem. Mol. Biol. 80, 149-162
40. Russo, J., Lareef, M. H., Balogh, G., Guo, S., and Russo, I. H. (2003) Estrogen and its metabolites are carcinogenic agents in human breast epithelial cells. J. Steroid Biochem. Mol. Biol. 87, 1-25
41. Lareef, M. H., Garber, J., Russo, P. A., Russo, I. H., Heulings, R., and Russo, J. (2005) The estrogen antagonist ICI-182,780 does not inhibit the transformation phenotypes induced by 17-beta-estradiol and 4-OH estradiol in human breast epithelial cells. Int. J. Oncol. 26, 423-429
42. Fernandez, S. V., Russo, I. H., Lareef, M. H., Balsara, B., and Russo, J. (2005) Comparative genomic hybridization of human breast epithelial cells transformed by estrogen and its metabolites. Int. J. Oncol. 26, 691-695
43. Cavalieri, E., Rogan, E., and Chakravarti, D. (2004) The role of endogenous catechol quinones in the initiation of cancer and neurodegenerative diseases. In Methods in Enzymology, Quinones and Quinone Enzymes (Sies, H., and Packer, L., eds) Vol. 382, pp. 293-319, Elsevier, Duesseldorf, Germany
44. Russo, J., Hu, Y. F., Tahin, Q., Mihaila, D., Slater, C., Lareef, M. H., and Russo, I. H. (2001) Carcinogenicity of estrogens in human breast epithelial cells. APMIS 109, 39-52
45. Calaf, G., and Russo, J. (1993) Transformation of human breast epithelial cells by chemical carcinogens. Carcinogenesis 14, 483-492
46. Calaf, G., Zhang, P. L., Alvarado, M. V., Estrada, S., and Russo, J. (1995) C-Ha-ras enhances the neoplastic transformation of human breast epithelial cells treated with chemical carcinogens. Int. J. Oncol. 6, 5-11
47. Forozan, F., Mahlamaki, E. H., Monni, O., Chen, Y., Veldman, R., Jiang, Y., Gooden, G. C., Ethier, S. P., Kallioniemi, A., and Kallioniemi, O. P. (2000) Comparative genomic hybridization analysis of 38 breast cancer cell lines: a basis for interpreting complementary DNA microarray data. Cancer Res. 60, 4519-4525
48. Russo, J. (2005) Estrogens as carcinogens in the human breast. Proc. Am. Assoc. Cancer Res. 46, SY14-1
49. Liu, S., and Lin, Y. C. (2004) Transformation of MCF-10A human breast epithelial cells by zeranol and estradiol-17beta. Breast J. 10, 514-521
50. Cuendet, M., Liu, X., Pisha, E., Li, Y., Yao, J., Yu, L., and Bolton, J. L. (2004) Equine estrogen metabolite 4-hydroxyequilenin induces anchorage-independent growth of human mammary epithelial MCF-10A cells: differential gene expression. Mutat. Res. 550, 109-121
51. Fernandez, S. V., Russo, I. H., and Russo, J. (2006) Estradiol and its metabolites 4-hydroxyestradiol and 2-hydroxyestradiol induce mutations in human breast epithelial cells. Int. J. Cancer 118, 1862-1868
52. Marsit, C. J., Okpukpara, C., Danaee, H., and Kelsey, K. T. (2005) Epigenetic silencing of the PRSS3 putative tumor suppressor gene in non-small cell lung cancer. Mol. Carcinog. 44, 146-150
53. Zhang, L. H., Qin, L. X., Ma, Z. C., Ye, S. L., Liu, Y. K., Ye, Q. H., Wu, X., Huang, W., and Tang, Z. Y. (2003) Allelic imbalance regions on chromosomes 8p, 17p and 19p related to metastasis of hepatocellular carcinoma: comparison between matched primary and metastatic lesions in 22 patients by genome-wide microsatellite analysis. J. Cancer Res. Clin. Oncol. 129, 279-286
54. Hopman, A. H., Kamps, M. A., Speel, E. J., Schapers, R. F., Sauter, G., and Ramaekers, F. C. (2002) Identification of chromosome 9 alterations and p53 accumulation in isolated carcinoma in situ of the urinary bladder versus carcinoma in situ associated with carcinoma. Am. J. Pathol. 161, 1119-1125
55. Verdorfer, I., Hobisch, A., Hittmair, A., Duba, H. C., Bartsch, G., Utermann, G., and Erdel, M. (1999) Cytogenetic characterization of 22 human renal cell tumors in relation to a histopathological classification. Cancer Genet. Cytogenet. 111, 61-70
56. Sarkar, S., Roy, B. C., Hatano, N., Aoyagi, T., Gohji, K., and Kiyama, R. (2002) A novel ankyrin repeat-containing gene (Kank) located at 9p24 is a growth suppressor of renal cell carcinoma. J. Biol. Chem. 277, 36585-36591
57. Zettl, A., Rudiger, T., Konrad, M. A., Chott, A., Simonitsch-Klupp, I., Sonnen, R., Muller-Hermelink, H. K., and Ott, G. (2004) Genomic profiling of peripheral T-cell lymphoma, unspecified, and anaplastic large T-cell lymphoma delineates novel recurrent chromosomal alterations. Am. J. Pathol. 164, 1837-1848
58. Adam, Z., Adany, R., Ladanyi, A., Timar, J., and Balazs, M. (2000) Liver metastatic ability of human melanoma cell line is associated with losses of chromosomes 4, 9p21-pter and 10p. Clin. Exp. Metastasis 18, 295-302
59. Simons, A., Schepens, M., Jeuken, J., Sprenger, S., van de Zande, G., Bjerkehagen, B., Forus, A., Weibolt, V., Molenaar, I., van den Berg, E., Myklebost, O., Bridge, J., van Kessel, A. G., and Suijkerbuijk, R. (2000) Frequent loss of 9p21 (p16(INK4A)) and other genomic imbalances in human malignant fibrous histiocytoma. Cancer Genet. Cytogenet. 118, 89-98
60. Tahara, H., Smith, A. P., Gaz, R. D., and Arnold, A. (1996) Loss of chromosome arm 9p DNA and analysis of the p16 and p15 cyclin-dependent kinase inhibitor genes in human parathyroid adenomas. J. Clin. Endocrinol. Metab. 81, 3663-3667
61. Johannsdottir, H. K., Johannesdottir, G., Agnarsson, B. A., Eerola, H., Arason, A., Johannsson, O. T., Heikkila, P., Egilsson, V., Olsson, H., Borg, A., Nevanlinna, H., and Barkardottir, R. B. (2004) Deletions on chromosome 4 in sporadic and BRCA mutated tumors and association with pathological variables. Anticancer Res. 24, 2681-2687
62. Zinn-Justin, A., Ziegler, A., and Abel, L. (2001) Multipoint development of the weighted pairwise correlation (WPC) linkage method for pedigrees of arbitrary size and application to the analysis of breast cancer and alcoholism familial data. Genet. Epidemiol. 21, 40-52
63. Shivapurkar, N., Sood, S., Wistuba, I. I., Virmani, A. K., Maitra, A., Milchgrub, S., Minna, J. D., and Gazdar, A. F. (1999) Multiple regions of chromosome 4 demonstrating allelic losses in breast carcinomas. Cancer Res. 59, 3576-3580
64. Dallol, A., Da Silva, N. F., Viacava, P., Minna, J. D., Bieche, I., Maher, E. R., and Latif, F. (2002) SLIT2, a human homologue of the Drosophila Slit2 gene, has tumor suppressor activity and is frequently inactivated in lung and breast cancers. Cancer Res. 62, 5874-5880
65. Achuthan, R., Bell, S. M., Roberts, P., Leek, J. P., Horgan, K., Markham, A. F., MacLennan, K. A., and Speirs, V. (2001) Genetic events during the transformation of a tamoxifen-sensitive human breast cancer cell line into a drug-resistant clone. Cancer Genet. Cytogenet. 130, 166-172
66. Ugolini, F., Adelaide, J., Charafe-Jauffret, E., Nguyen, C., Jacquemier, J., Jordan, B., Birnbaum, D., and Pebusque, M. J. (1999) Differential expression assay of chromosome arm 8p genes identifies frizzled-related (FRP1/FRZB) and fibroblast growth factor receptor 1 (FGFR1) as candidate breast cancer genes. Oncogene 18, 1903-1910
67. Gelsi-Boyer, V., Orsetti, B., Cervera, N., Finetti, P., Sircoulomb, F., Rouge, C., Lasorsa, L., Letessier, A., Ginestier, C., Monville, F., Esteyries, S., Adelaide, J., Esterni, B., Henry, C., Ethier, S. P., Bibeau, F., Mozziconacci, M. J., Charafe-Jauffret, E., Jacquemier, J., Bertucci, F., Birnbaum, D., Theillet, C., and Chaffanet, M. (2005) Comprehensive profiling of 8p11-12 amplification in breast cancer. Mol. Cancer Res. 3, 655-667
68. Jakob, J., Nagase, S., Gazdar, A., Chien, M., Morozova, I., Russo, J. J., Nandula, S. V., Murty, V. V., Li, C. M., Tycko, B., and Parsons, R. (2005) Two somatic biallelic lesions within and near SMAD4 in a human breast cancer cell line. Genes Chromosomes Cancer 42, 372-383
69. Weber-Mangal, S., Sinn, H. P., Popp, S., Klaes, R., Emig, R., Bentz, M., Mansmann, U., Bastert, G., Bartram, C. R., and Jauch, A. (2003) Breast cancer in young women (< or = 35 years): Genomic aberrations detected by comparative genomic hybridization. Int. J. Cancer 107, 583-592
70. Richard, F., Pacyna-Gengelbach, M., Schluns, K., Fleige, B., Winzer, K. J., Szymas, J., Dietel, M., Petersen, I., and Schwendel, A. (2000) Patterns of chromosomal imbalances in invasive breast cancer. Int. J. Cancer 89, 305-310
71. Dellas, A., Torhorst, J., Schultheiss, E., Mihatsch, M. J., and Moch, H. (2002) DNA sequence losses on chromosomes 11p and 18q are associated with clinical outcome in lymph nodenegative ductal breast cancer. Clin. Cancer Res. 8, 1210-1216
72. Yokota, T., Matsumoto, S., Yoshimoto, M., Kasumi, F., Akiyama, F., Sakamoto, G., Nakamura, Y., and Emi, M. (1997) Mapping of a breast cancer tumor suppressor gene locus to a 4-cM interval on chromosome 18q21. Jpn. J. Cancer Res. 88, 959-964
73. Kaneko, M., Arihiro, K., Takeshima, Y., Fujii, S., and Inai, K. (2002) Loss of heterozygosity and microsatellite instability in epithelial hyperplasia of the breast. J. Exp. Ther. Oncol. 2, 9-18
74. Forozan, F., Veldman, R., Ammerman, C. A., Parsa, N. Z., Kallioniemi, A., Kallioniemi, O. P., and Ethier, S. P. (1999) Molecular cytogenetic analysis of 11 new breast cancer cell lines. Br. J. Cancer 81, 1328-1334
75. Nessling, M., Richter, K., Schwaenen, C., Roerig, P., Wrobel, G., Wessendorf, S., Fritz, B., Bentz, M., Sinn, H. P., Radlwimmer, B., and Lichter, P. (2005) Candidate genes in breast cancer revealed by microarray-based comparative genomic hybridization of archived tissue. Cancer Res. 65, 439-447
76. Loveday, R. L., Greenman, J., Simcox, D. L., Speirs, V., Drew, P. J., Monson, J. R., and Kerin, M. J. (2000) Genetic changes in breast cancer detected by comparative genomic hybridisation. Int. J. Cancer 86, 494-500
77. Bieche, I., Khodja, A., and Lidereau, R. (1999) Deletion mapping of chromosomal region 1p32-pter in primary breast cancer. Genes Chromosomes Cancer 24, 255-263
78. Ragnarsson, G., Eiriksdottir, G., Johannsdottir, J. T., Jonasson, J. G., Egilsson, V., and Ingvarsson, S. (1999) Loss of heterozygosity at chromosome 1p in different solid human tumours: association with survival. Br. J. Cancer 79, 1468-1474
79. Bieche, I., Khodja, A., and Lidereau, R. (1998) Deletion mapping in breast tumor cell lines points to two distinct tumor-suppressor genes in the 1p32-pter region, one of deleted regions (1p36.2) being located within the consensus region of LOH in neuroblastoma. Oncol. Rep. 5, 267-272
80. Tsao, S. W., Wong, N., Wang, X., Liu, Y., Wan, T. S., Fung, L. F., Lancaster, W. D., Gregoire, L., and Wong, Y. C. (2001) Nonrandom chromosomal imbalances in human ovarian surface epithelial cells immortalized by HPV16-E6E7 viral oncogenes. Cancer Genet. Cytogenet. 130, 141-149
81. Melcher, R., Steinlein, C., Feichtinger, W., Muller, C. R., Menzel, T., Luhrs, H., Scheppach, W., and Schmid, M. (2000) Spectral karyotyping of the human colon cancer cell lines SW480 and SW620. Cytogenet. Cell Genet. 88, 145-152
82. Muleris, M., Almeida, A., Gerbault-Seureau, M., Malfoy, B., and Dutrillaux, B. (1994) Detection of DNA amplification in 17 primary breast carcinomas with homogeneously staining regions by a modified comparative genomic hybridization technique. Genes Chromosomes Cancer 10, 160-170