The consequences of exhaustive antiestrogen therapy in breast cancer: Estrogen-induced tumor cell death

Experimental Biology and Medicine

Volumn 229, Issue 8, 2004, Pages 722-731

  Osipo, Clodia ^a   Liu, Hong ^a   Meeke, Kathleen ^a   Jordan, V Craig ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Apoptosis; Aromatase inhibitor; HER2 neu; Phytoestrogens; Raloxifene; Selective estrogen receptor modulator; Tamoxifen

Indexed keywords

AMINOGLUTETHIMIDE; ANTIESTROGEN; AROMATASE INHIBITOR; DIETHYLSTILBESTROL; ESTRADIOL; ESTROGEN; FULVESTRANT; GONADORELIN AGONIST; LETROZOLE; RALOXIFENE; TAMOXIFEN;

BREAST CANCER; CANCER COMBINATION CHEMOTHERAPY; CANCER PALLIATIVE THERAPY; CANCER PATIENT; CANCER PREVENTION; CANCER RISK; CANCER STAGING; CELL DEATH; CLINICAL TRIAL; DRUG EFFICACY; DRUG MECHANISM; DRUG SCREENING; ENDOMETRIUM CANCER; ESTROGEN ACTIVITY; ESTROGEN THERAPY; HIGH RISK POPULATION; HORMONAL REGULATION; HUMAN; NONHUMAN; OSTEOPOROSIS; POSTMENOPAUSE; PREDICTION; PREMENOPAUSE; REVIEW; SHORT SURVEY; SIDE EFFECT; TREATMENT PLANNING; TUMOR CELL; TUMOR CELL DESTRUCTION;

EID: 4444364541     PISSN: 15353702     EISSN: None     Source Type: Journal    
DOI: 10.1177/153537020422900804     Document Type: Short Survey

References (81)

1. Kennedy BJ. Hormone therapy for advanced breast cancer. Cancer 18:1551-1557, 1965.
2. Jordan VC. Tamoxifen: a most unlikely pioneering medicine. Nature Rev Drug Discov 2:205-213, 2003.
3. Jordan VC, Morrow M. Tamoxifen, raloxifene, and the prevention of breast cancer. Endocr Rev 20:253-278, 1999.
4. Jensen EV, Jordan VC. The estrogen receptor: a model for molecular medicine. The Dorothy P. Landon AACR Prize for Translational Research. Clin Cancer Res 9:1980-1989, 2003.
5. McGuire WL, Carbone PP, Vollmer EP. Estrogen Receptors in Human Breast Cancer. New York: Raven Press, 1975.
6. Harper MJ, Walpole AL. A new derivative of triphenylethylene: effect on implantation and mode of action in rats. J Reprod Fertil 13:101-119, 1967.
7. Lerner LI, Jordan VC. The development of antiestrogens for the treatment of breast cancer: Eighth Cain Memorial Award Lecture. Cancer Res 50:4177-4189, 1990.
8. Cole MP, Jones CT, Todd ID. A new anti-oestrogenic agent in late breast cancer. An early clinical appraisal of ICI 46474. Br J Cancer 25:270-275, 1971.
9. Jordan VC, Koerner S. Tamoxifen (ICI 46,474) and the human carcinoma 8S oestrogen receptor. Eur J Cancer 11:205-206, 1975.
10. Jordan VC, Dowse LJ. Tamoxifen as an antitumour agent: effect on oestrogen binding. J Endocrinol 68:297-303, 1976.
11. Jordan VC, Jaspan T. Tamoxifen as an antitumour agent: oestrogen binding as a predictive test for tumour response. J Endocrinol 68:453-460, 1976.
12. Jordan VC, Allen KE. Evaluation of the antitumour activity of the nonsteroidal antioestrogen monohydroxytamoxifen in the DMBA-induced rat mammary carcinoma model. Eur J Cancer 16:239-251, 1980.
13. Mandlekar S, Kong AN. Mechanisms of tamoxifen-induced apoptosis. Apoptosis 6:469-477, 2001.
14. Early Breast Cancer Trialists' Collaborative Group. Tamoxifen for early breast cancer: an overview of the randomised trials. Lancet 354:1451-1467, 1998.
15. Jordan VC. Effect of tamoxifen (ICI 46,474) on initiation and growth of DMBA-induced rat mammary carcinomata. Eur J Cancer 12:419-424, 1976.
16. Fisher B, Costantino JP, Wickerham DL, Redmond CK, Kavanah M, Cronin WM, Vogel V, Robidoux A, Dimitrov N, Atkins J, Daly M, Wieand S, Tan-Chiu E, Ford L, Wolmark N. Tamoxifen for prevention of breast cancer: report of the National Surgical Adjuvant Breast and Bowel Project P-1 Study. J Natl Cancer Inst 90:1371-1388, 1998.
17. Cuzick J, Powles T, Veronesi U, Forbes J, Edwards R, Ashley S, Boyle P. Overview of the main outcomes in breast-cancer prevention trials. Lancet 361:296-300, 2003.
18. Jordan VC, Fritz NF, Langan-Fahey S, Thompson M, Tormey DC. Alteration of endocrine parameters in premenopausal women with breast cancer during long-term adjuvant therapy with tamoxifen as the single agent. J Natl Cancer Inst 83:1488-1491, 1991.
19. Jakesz R, Hausmaninger H, Kubista E, Gnant M, Menzel C, Bauernhofer T, Seifert M, Haider M, Mlineritsch B, Steindorfer P, Kwasny W, Fridrik M, Steger G, Wette V, Samonigg H. Randomized adjuvant trial of tamoxifen and goserelin versus cyclophosphamide, methotrexate, and fluorouracil: evidence for the superiority of treatment with endocrine blockade in premenopausal patients with hormone-responsive breast cancer - Austrian breast and colorectal cancer study group trial 5. J Clin Oncol 15:4621-4627, 2002.
20. The ATAC Trialist Group. Anastrozole alone or in combination with tamoxifen versus tamoxifen alone for adjuvant treatment of postmenopausal women with early breast cancer: first results of the ATAC randomized trial. Lancet 359:2131-2139, 2002.
21. Fisher B, Dignam J, Bryant J, Wolmark N. Five versus more than five years of tamoxifen for lymph node-negative breast cancer: updated findings from the National Surgical Adjuvant Breast and Bowel Project B-14 randomized trial. J Natl Cancer Inst 93:684-690, 2001.
22. Goss PE, Ingle JN, Marino S, Robert NJ, Muss HB, Piccart MJ, Castiglione M, Tu D, Shepherd LE, Pritchard KI, Livingston RB, Davidson NE, Norton L, Perez EA, Abrams JS, Therasse P, Palmer MJ, Pater JL. A randomized trial of letrozole in postmenopausal women after five years of tamoxifen therapy for early-stage breast cancer. N Engl J Med 349:1-10, 2003.
23. Jordan VC. Antiestrogens and selective estrogen receptor modulators as multifunctional medicines. Part I: receptor interactions. J Med Chem 46:883-908, 2003.
24. Jordan VC. Antiestrogens and selective estrogen receptor modulators as multifunctional medicines Part II: clinical considerations and new agents. J Med Chem 46:1082-1111, 2003.
25. Jordan VC. Selective estrogen receptor modulation: a personal perspective. Cancer Res 61:5683-5687, 2001.
26. Barrett-Connor E, Grady D. Hormone replacement therapy, heart disease, and other considerations. Annu Rev Public Health 19:55-72, 1998.
27. Fisher B, Costantino JP, Redmond CK, Fisher ER, Wickerham DL, Cronin WM. Endometrial cancer in tamoxifen-treated breast cancer patients: findings from the National Surgical Adjuvant Breast and Bowel Project (NSABP) B-14. J Natl Cancer Inst 86:527-537, 1994.
28. Ettinger B, Black DM, Mitlak BH, Knickerbocker RK, Nickelsen T, Genant HK, Christiansen C, Delmas PD, Zanchetta JR, Stakkestad J, Gluer CC, Krueger K, Cohen FJ, Eckert S, Ensrud KE, Avioli LV, Lips P, Cummings SR. Reduction of vertebral fracture risk in postmenopausal women with osteoporosis treated with raloxifene: results from a 3-year randomized clinical trial. Multiple Outcomes of Raloxifene Evaluation (MORE) Investigators [see comments]. JAMA 282:637-645, 1999.
29. Cummings SR, Eckert S, Krueger KA, Grady D, Powles TJ, Cauley JA, Norton L, Nickelsen T, Bjarnason NH, Morrow M, Lippman ME, Black D, Glusman JE, Costa A, Jordan VC. The effect of raloxifene on risk of breast cancer in postmenopausal women: results from the MORE randomized trial. Multiple Outcomes of Raloxifene Evaluation. JAMA 281:2189-2197, 1999.
30. Walsh BW, Kuller LH, Wild RA, Paul S, Farmer M, Lawrence JB, Shah AS, Anderson PW. Effects of raloxifene on serum lipids and coagulation factors in healthy postmenopausal women. JAMA 279:1445-1451, 1998.
31. Barrett-Connor E, Grady D, Sashegyi A, Anderson PW, Cox DA, Hoszowski K, Rautaharju P, Harper KD. Raloxifene and cardiovascular events in osteoporotic postmenopausal women. JAMA 287:847-857, 2002.
32. Benz CC, Scott GK, Sarup JC, Johnson RM, Tripathy D, Coronado E, Shepard HM, Osborne CK. Estrogen-dependent, tamoxifen-resistant tumorigenic growth of MCF-7 cells transfected with HER2/neu. Breast Cancer Res Treat 24:85-95, 1993.
33. Osborne CK, Bardou V, Hopp TA, Chamness GC, Hilsenbeck SG, Fuqua SA, Wong J, Allred DC, Clark GM, Schiff R. Role of the estrogen receptor coactivator AIB1 (SRC-3) and HER-2/neu in tamoxifen resistance in breast cancer. J Natl Cancer Inst 95:353-361, 2003.
34. Osborne CK, Hobbs K, Clark GM. Effect of estrogens and antiestrogens on growth of human breast cancer cells in athymic nude mice. Cancer Res 45:584-591, 1985.
35. Dardes RC, MacGregor Schafer J, Timm Pearce S, Osipo C, Chen B, Jordan VC. Regulation of estrogen target genes and growth by selective estrogen receptor modulators in endometrial cancer cells. Gynecol Oncol 85:498-506, 2002.
36. Satyaswaroop PG, Zaino RJ, Mortel R. Human endometrial adenocarcinoma transplanted into nude mice: growth regulation by estradiol. Science 219:58-60, 1983.
37. Gottardis MM, Jordan VC. Development of tamoxifen-stimulated growth of MCF-7 tumors in athymic mice after long-term antiestrogen administration. Cancer Res 48:5183-5187, 1988.
38. MacGregor-Schafer JI, Lee ES, O'Regan RM, Yao K, Jordan VC. Rapid development of tamoxifen stimulated mutant p53 breast tumors (T47D) in athymic mice. Clin Cancer Res 6:4373-4380, 2000.
39. Satyaswaroop PG, Zaino RJ, Mortel R. Estrogen-like effects of tamoxifen on human endometrial carcinoma transplanted into nude mice. Cancer Res 44:4006-4010, 1984.
40. O'Regan RM, Gajdos C, Dardes RC, De Los Reyes A, Park W, Rademaker AW, Jordan VC. Effects of raloxifene after tamoxifen on breast and endometrial tumor growth in athymic mice. J Natl Cancer Inst 94:274-283, 2002.
41. Wijayaratne AL, McDonnell DP. The human estrogen receptor-alpha is a ubiquitinated protein whose stability is affected differentially by agonists, antagonists, and selective estrogen receptor modulators. J Biol Chem 276:35684-35692, 2001.
42. Osborne CK, Coronado-Heinsohn EB, Hilsenbeck SG, McCue BL, Wakeling AE, McClelland RA, Manning DL, Nicholson RI. Comparison of the effects of a pure steroidal antiestrogen with those of tamoxifen in a model of human breast cancer. J Natl Cancer Inst 87:746-750, 1995.
43. Lee ES, Schafer JM, Yao K, England G, O'Regan RM, De Los Reyes A, Jordan VC. Cross-resistance of triphenylethylene-type antiestrogens but not ICI 182,780 in tamoxifen-stimulated breast tumors grown in athymic mice. Clin Cancer Res 6:4893-4899, 2000.
44. Howell A, Dodwell DJ, Anderson H, Redford J. Response after withdrawal of tamoxifen and progestogens in advanced breast cancer [see comments]. Ann Oncol 3:611-617, 1992.
45. Brodie A, Lu Q, Long B. Aromatase and its inhibitors. J Steroid Biochem Mol Biol 69:205-210, 1999.
46. Buzdar A. Exemestane in advanced breast cancer. Anticancer Drugs 11:609-616, 2000.
47. Goss PE, Strasser K. Aromatase inhibitors in the treatment and prevention of breast cancer. J Clin Oncol 19:881-894, 2001.
48. Howell A, Robertson JFR, Quaresma Albano J, Aschermannova A, Mauriac L, Kleeberg UR, Vergot I, Erikstein B, Webster A, Morris C. Fulvestrant, formerly ICI 182,780, is as effective as anastrozole in postmenopausal women with advanced breast cancer progressing after prior endocrine treatment. J Clin Oncol 20:3396-3403, 2002.
49. Osborne CK, Pippen J, Jones SE, Parker LM, Ellis M, Come S, Gertler SZ, May JT, Burton G, Dimery I, Webster A, Morris C, Elledge R, Buzdar A. J Clin Oncol Double-blind, randomized trial comparing the efficacy and tolerability of fulvestrant versus anastrozole in postmenopausal women with advanced breast cancer progressing on prior endocrine therapy: results of a North American trial. J Clin Oncol 20:3386-3395, 2002.
50. Wolf DM, Jordan VC. A laboratory model to explain the survival advantage observed in patients taking adjuvant tamoxifen therapy. Recent Results Cancer Res 127:23-33, 1993.
51. Yao K, Lee ES, Bentrem DJ, England G, Schafer JI, O'Regan R, Jordan VC. Antitumor action of physiological estradiol on tamoxifen-stimulated breast tumors grown in athymic mice. Clin Cancer Res 6:2028-2036, 2000.
52. Gottardis MM, Robinson SP, Satyaswaroop PG, Jordan VC. Contrasting actions of tamoxifen on endometrial and breast tumor growth in the athymic mouse. Cancer Res 48:812-815, 1988.
53. MacGregor Shafer JI, Lee ES, Dardes RC, Bentrem DJ, O'Regan RM, de los Reyes A, Jordan VC. Analysis of cross-resistance of the selective estrogen receptor modulators arzoxifene (LY353381) and LY117018 in tamoxifen-stimulated breast cancer xenografts. Clin Cancer Res 7:2505-2512, 2001.
54. Osipo C, Gajdos C, Liu H, Chen B, Jordan VC. Paradoxical action of fulvestrant on estradiol-induced regression of tamoxifen-stimulated breast cancer. J Natl Cancer Inst 95:1597-1607, 2003.
55. Chisamore MJ, Ahmed Y, Bentrem DJ, Jordan VC, Tonetti DA. Novel antitumor effect of estradiol in athymic mice injected with a T47D breast cancer cell line overexpressing protein kinase C alpha. Clin Cancer Res 7:3156-3165, 2001.
56. Jordan VC, Osipo C, MacGregor Schafer J, Fox JE, Cheng D, Liu H. Changing role of the oestrgoen receptor (ER) in the life and death of breast cancer. Breast 12:432-441, 2003.
57. Dardes RC, Liu H, Gajdos C, O'Regan R, de los Reyes A, Jordan VC. Raloxifene stimulated endometrial cancer grown in athymic mice: cross resistance with ICI 182,780 and antitumor action of estradiol. Breast Cancer Res Treat 69:228 Abstract 447, 2001.
58. Santen RJ, Worgul TJ, Lipton A, Harvey H, Boucher A, Samojlik E, Wells SA. Aminoglutethimide as treatment of postmenopausal women with advanced breast carcinoma. Ann Intern Med 96:94-101, 1982.
59. Welshons WV, Jordan VC. Adaptation of estrogen-dependent MCF-7 cells to low estrogen (phenol red-free) culture. Eur J Cancer 232:1935-1939, 1987.
60. Katzenellenbogen BS, Kendra KL, Norman MJ, Berthois Y. Proliferation, hormonal responsiveness, and estrogen receptor content of MCF-7 human breast cancer cells grown in the short-term and long-term absence of estrogens. Cancer Res 47:4355-4360, 1987.
61. Jiang SY, Wolf DM, Yingling JM, Chang C, Jordan VC. An estrogen receptor positive MCF-7 clone that is resistant to antiestrogens and estradiol. Mol Cell Endocrinol 90:77-80, 1992.
62. Pink JJ, Jiang SY, Fritsch M, Jordan VC. An estrogen-independent MCF-7 breast cancer cell line which contains a novel 80-kilodalton estrogen receptor-related protein. Cancer Res 55:2583-2590, 1995.
63. Song RX, Mor G, Naftolin F, McPherson RA, Song J, Zhang Z, Yue W, Wang J, Santen RJ. Effect of long-term estrogen deprivation on apoptotic responses of breast cancer cells to 17beta-estradiol. J Natl Cancer Inst 93:1714-1723, 2001.
64. Haddow A, Watkinson JM, Patersonm E. Influence of synthetic oestrogens upon advanced malignant disease. BMJ 2:393-398, 1944.
65. Ingle JN, Ahmann DL, Green SJ, Edmonson JH, Bisel HF, Kvols LK, Nichols WC, Creagan ET, Hahn RG, Rubin J, Frytak S. Randomized clinical trial of diethylstilbestrol versus tamoxifen in postmenopausal women with advanced breast cancer. N Engl J Med 304:16-21, 1981.
66. Ingle JN. Estrogen as therapy for breast cancer. Breast Cancer Res 4:133-136, 2002.
67. Lonning PE, Taylor PD, Anker G, Iddon J, Wie L, Jorgensen LM, Mella O, Howell A. High-dose estrogen treatment in postmenopausal breast cancer patients heavily exposed to endocrine therapy. Breast Cancer Res Treat 67:111-116, 2001.
68. Black LJ, Jones CD, Falcone JF. Antagonism of estrogen action with a new benzothiophene derived antiestrogen. Life Sci 32:1031-1036, 1983.
69. Jordan VC, Collins MM, Rowsby L, Prestwich GA. monohydroxylated metabolite of tamoxifen with potent antiestrogenic activity. J Endocrinol 75:305-316, 1977.
70. MacGregor Schafer J, Liu H, Bentrem DJ, Zapf JW, Jordan VC. Allosteric silencing of activating function 1 in the 4-hydroxytamoxifen estrogen receptor complex is induced by substituting glycine for aspartate at amino acid 351. Cancer Res 60:5097-5105, 2000.
71. Liu H, Park WC, Bentrem DJ, McKian KP, de los Reyes A, Loweth JA, Schafer JM, Zapf JW, Jordan VC. Structure-function relationships of the raloxifene-estrogen receptor-alpha complex for regulating transforming growth factor-alpha expression in breast cancer cells. J Biol Chem 277:9189-9198, 2002.
72. Newman SP, Bates NP, Vernimmen D, Parker MG, Hurst HC. Cofactor competition between the ligand-bound oestrogen receptor and an intron 1 enhancer leads to oestrogen repression of ERBB2 expression in breast cancer. Oncogene 19:490-497, 2000.
73. Liu H, Lee ES, Gajdos C, Pearce ST, Chen B, Osipo C, Loweth J, McKian K, De los Reyes A, Wing L, Jordan VC. Apoptotic action of 17 beta-estradiol in raloxifene resistant MCF-7 cells in vitro and in vivo. J Natl Cancer Inst 95:1586-1596, 2003.
74. McDonnell DP, Clemm DL, Hermann T, Goldman ME, Pike JW. Analysis of estrogen receptor function in vitro reveals three distinct classes of antiestrogens. Mol Endocrinol 9:659-669, 1995.
75. Jordan VC, MacGregor Schafer JI, Levenson AS, Liu H, Pease KM, Simons LA, Zapf JW. Molecular classification of estrogens. Cancer Res 61:6619-6623, 2001.
76. Gust R, Keilitz R, Schmidt K. Investigations of new lead structures for the design of selective estrogen receptor modulators. J Med Chem 44:1963-1970, 2001.
77. Bentrem D, Fox JE, Pearce ST, Liu H, Pappas S, Kupfer D, Zapf JW, Jordan VC. Distinct molecular conformations of the estrogen receptor alpha complex exploited by environmental estrogens. Cancer Res 63:7490-7496, 2003.
78. Jordan VC, Mittal S, Gosden B, Koch R, Lieberman ME. Structure-activity relationships of estrogens. Environmental Health Perspectives (NIH special issue) 61:97-110, 1985.
79. Liu H, Lee ES, De los Reyes A, Zapf JW, Jordan VC. Silencing and reactivation of the selective estrogen receptor modulator-estrogen receptor alpha complex. Cancer Res 61:3632-3639, 2001.
80. Jiang SY, Jordan VC. Growth regulation of estrogen receptor negative breast cancer cells transfected with cDNA's for estrogen receptor. J Natl Cancer Inst 84:580-591, 1992.
81. Levenson AS, Jordan VC. Transfection of human estrogen receptor (ER) cDNA in ER-negative mammalian cell lines. J Steroid Biochem Mol Biol 51:229-239, 1994.