The new biology of estrogen-induced apoptosis applied to treat and prevent breast cancer

Endocrine-Related Cancer

Volumn 22, Issue 1, 2015, Pages R1-R31

  Jordan, V Craig ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Acquired resistance; Aromatase inhibitors; Modulators; Raloxifene; Selective estrogen receptor; Tamoxifen

Indexed keywords

BISPHENOL TRIPHENYLETHYLENE; DEATH RECEPTOR; ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR; GESTAGEN; GLUCOCORTICOID; PACLITAXEL; PHYTOESTROGEN; PROTEIN CSRC INHIBITOR; PROTEIN TYROSINE KINASE INHIBITOR; TAMOXIFEN; UNCLASSIFIED DRUG; ESTRADIOL DERIVATIVE;

ADJUVANT THERAPY; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BREAST CANCER; BREAST METASTASIS; CANCER CELL; CANCER THERAPY; CELL CYCLE G2 PHASE; CELL POPULATION; DRUG MECHANISM; DRUG RECEPTOR BINDING; ENDOPLASMIC RETICULUM STRESS; ESTROGEN THERAPY; HORMONE SUBSTITUTION; HUMAN; HYSTERECTOMY; INFLAMMATION; MITOCHONDRION; MORTALITY; NONHUMAN; ONCOGENE SRC; POSTMENOPAUSE; REVIEW; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; ANIMAL; BREAST NEOPLASMS; DRUG EFFECTS; FEMALE; PATHOLOGY;

ANIMALS; APOPTOSIS; BREAST NEOPLASMS; ESTRADIOL CONGENERS; FEMALE; HUMANS;

EID: 84923595903     PISSN: 13510088     EISSN: 14796821     Source Type: Journal    
DOI: 10.1530/ERC-14-0448     Document Type: Review

References (208)

1. Anderson GL, Limacher M, Assaf AR, Bassford T, Beresford SA, Black H, Bonds D, Brunner R, Brzyski R, Caan B et al. 2004 Effects of conjugated equine estrogen in postmenopausal women with hysterectomy: the Women's Health Initiative randomized controlled trial. Journal of the American Medical Association 291 1701-1712. (doi:10.1001/jama.291.14.1701)
2. Anderson GL, Chlebowski RT, Aragaki AK, Kuller LH, Manson JE, Gass M, Bluhm E, Connelly S, Hubbell FA, Lane D et al. 2012 Conjugated equine oestrogen and breast cancer incidence and mortality in postmeno-pausal women with hysterectomy: extended follow-up of the Women's Health Initiative randomised placebo-controlled trial. Lancet Oncology 13 476-486. (doi:10.1016/S1470-2045(12)70075-X)
3. Ariazi EA, Cunliffe HE, Lewis-Wambi JS, Slifker MJ, Willis AL, Ramos P, Tapia C, Kima HR, Yerrum S, Sharma CGN et al. 2011 Estrogen induces apoptosis in estrogen deprivation-resistant breast cancer through stress responses as identified by global gene expression across time. PNAS 108 18879-18886. (doi:10.1073/pnas.1115188108)
4. Arnold SF, Obourn JD, Jaffe H & Notides AC 1995 Phosphorylation of the human estrogen receptor on tyrosine 537 in vivo and by src family tyrosine kinases in vitro. Molecular Endocrinology 9 24-33. (doi:10.1210/mend.9.1.7539106)
5. Assender JW, Gee JM, Lewis I, Ellis IO, Robertson JF & Nicholson RI 2007 Protein kinase C isoform expression as a predictor of disease outcome on endocrine therapy in breast cancer. Journal of Clinical Pathology 60 1216-1221. (doi:10.1136/jcp.2006.041616)
6. Balaburski GM, Dardes RC, Johnson M, Haddad B, Zhu F, Ross EA, Sengupta S, Klein-Szanto A, Liu H, Lee ES et al. 2010 Raloxifene-stimulated experimental breast cancer with the paradoxical actions of estrogen to promote or prevent tumor growth: a unifying concept in anti-hormone resistance. International Journal of Oncology 37 387-398. (doi:10.3892/ijo-00000687)
7. Baumler E 1984 Paul Ehrlich: Scientist for Life. First Edition. New York: Holmes & Meier.
8. Beatson GT 1896 On the treatment of inoperable cases of carcinoma of the mamma: suggestions for a new method of treatment, with illustrative cases. Lancet 2 104-107. (doi:10.1016/S0140-6736(01)72307-0)
9. Becker MA, Ibrahim YH, Cui X, Lee AV & Yee D 2011 The IGF pathway regulates ERa through a S6K1-dependent mechanism in breast cancer cells. Molecular Endocrinology 25 516-528. (doi:10.1210/me.2010-0373)
10. Beral V, Banks E, Reeves G & Bull D 2003 Breast cancer and hormone-replacement therapy in the Million Women Study. Lancet 362 419-427. (doi:10.1016/S0140-6736(03)14596-5)
11. Beral V, Reeves G, Bull D et al. 2011 Breast cancer risk in relation to the interval between menopause and starting hormone therapy. Journal of the National Cancer Institute 103 296-305. (doi:10.1093/jnci/djq527)
12. Bergh J, Jonsson PE, Lidbrink EK, Trudeau M, Eiermann W, Brattström D, Lindemann JP, Wiklund F & Henriksson R 2012 FACT: an open-label randomized phase III study of fulvestrant and anastrozole in combination compared with anastrozole alone as first-line therapy for patients with receptor-positive postmenopausal breast cancer. Journal of Clinical Oncology 30 1919-1925. (doi:10.1200/JCO.2011.38.1095)
13. Berthois Y, Katzenellenbogen JA & Katzenellenbogen BS 1986 Phenol red in tissue culture media is a weak estrogen: implications concerning the study of estrogen-responsive cells in culture. PNAS 83 2496-2500. (doi:10.1073/pnas.83.8.2496)
14. Bindal RD & Katzenellenbogen JA 1988 Bis(4-hydroxyphenyl)[2-(phenox-ysulfonyl)phenyl]methane: isolation and structure elucidation of a novel estrogen from commercial preparations of phenol red (phenolsulfonphthalein). Journal of Medicinal Chemistry 31 1978-1983. (doi:10.1021/jm00118a020)
15. C-dependent protein kinase of human mammary carcinoma cells: inverse relationship to estrogen receptors. International Journal of Cancer 40 344-348. (doi:10.1002/ijc.2910400310)
16. Bourgoin-Voillard S, Gallo D, Laios I, Cleeren A, Bali LE, Jacquot Y, Nonclercq D, Laurent G, Tabet JC & Leclercq G 2010 Capacity of type I and II ligands to confer to estrogen receptor a an appropriate conformation for the recruitment of coactivators containing a LxxLL motif-relationship with the regulation of receptor level and ERE-dependent transcription in MCF-7 cells. Biochemical Pharmacology 79 746-757. (doi:10.1016/j.bcp.2009.10.015)
17. Boyd S 1900 On oophorectomy in cancer of the breast. BMJ 2 1161-1187.
18. Brauch H & Schwab M 2014 Prediction of tamoxifen outcome by genetic variation of CYP2D6 in post-menopausal women with early breast cancer. British Journal of Clinical Pharmacology 77 695-703. (doi:10.1111/bcp.12229)
19. Brooks SC, Locke ER & Soule HD 1973 Estrogen receptor in a human cell line (MCF-7) from breast carcinoma. Journal of Biological Chemistry 248 6251-6253.
20. Brzozowski AM, Pike ACW, Dauter Z, Hubbard RE, Bonn T, Engström O, Ohman L, Greene GL, Gustafsson JA & Carlquist M 1997 Molecular basis of agonism and antagonism in the oestrogen receptor. Nature 389 753-758. (doi:10.1038/39645)
21. Catherino WH, Jeng MH & Jordan VC 1993 Norgestrel and gestodene stimulate breast cancer cell growth through an oestrogen receptor mediated mechanism. British Journal of Cancer 67 945-952. (doi:10.1038/bjc.1993.175)
22. Chisamore MJ, Ahmed Y, Bentrem DJ, Jordan VC & Tonetti DA 2001 Novel antitumor effect of estradiol in athymic mice injected with a T47D breast cancer cell line overexpressing protein kinase Ca. Clinical Cancer Research 7 3156-3165.
23. Chu I, Arnaout A, Loiseau S, Sun J, Seth A, McMahon C, Chun K, Hennessy B, Mills GB, Nawaz Z et al. 2007 Src promotes estrogen-dependent estrogen receptor a proteolysis in human breast cancer. Journal of Clinical Investigation 117 2205-2215. (doi:10.1172/JCI21739)
24. Cole MP, Jones CT & Todd ID 1971 A new anti-oestrogenic agent in late breast cancer. An early clinical appraisal of ICI46474. British Journal of Cancer 25 270-275. (doi:10.1038/bjc.1971.33)
25. Courtin A, Communal L, Vilasco M, Cimino D, Mourra N, de Bortoli M, Taverna D, Faussat AM, Chaouat M, Forgez P et al. 2012 Glucocorticoid receptor activity discriminates between progesterone and medroxy-progesterone acetate effects in breast cells. Breast Cancer Research and Treatment 131 49-63. (doi:10.1007/s10549-011-1394-5)
26. Cuzick J, Forbes JF, Sestak I, Cawthorn S, Hamed H, Holli K & Howell A 2007 Long-term results of tamoxifen prophylaxis for breast cancer-96-month follow-up of the randomized IBIS-I trial. Journal of the National Cancer Institute 99 272-282. (doi:10.1093/jnci/djk049)
27. Cuzick J, Sestak I, Baum M, Buzdar A, Howell A, Dowsett M & Forbes JF 2010 ATAC/LATTE investigators. Effect of anastrozole and tamoxifen as adjuvant treatment for early-stage breast cancer: 10-year analysis of the ATAC trial. Lancet Oncology 11 1135-1141. (doi:10.1016/S1470-2045(10)70257-6)
28. Davies C, Godwin J, Gray R, Clarke M, Cutter D, Darby S, McGale P, Pan HC, Taylor C, Wang YC et al. 2011 Relevance of breast cancer hormone receptors and other factors to the efficacy of adjuvant tamoxifen: patient-level meta-analysis of randomised trials. Lancet 378 771-784. (doi:10.1016/S0140-6736(11)60993-8)
29. Davies C, Pan H, Godwin J, Gray R, Arriagada R, Raina V, Abraham M, Medeiros Alencar VH, Badran A, Bonfill X et al. 2013 Long-term effects of continuing adjuvant tamoxifen to 10 years versus stopping at 5 years after diagnosis of oestrogen receptor-positive breast cancer: ATLAS, a randomised trial. Lancet 381 805-816. (doi:10.1016/S0140-6736(12)61963-1)
30. Dodds EC, Lawson W & Noble RL 1938 Biological effects of the synthetic oestrogenic substance 4:4'-dihydroxy-α:β. Lancet 232 1389-1391. (doi:10.1016/S0140-6736(00)89468-4)
31. Dowsett M, Cuzick J, Ingle J, Coates A, Forbes J, Bliss J, Buyse M, Baum M, Buzdar A, Colleoni M et al. 2010 Meta-analysis of breast cancer outcomes in adjuvant trials of aromatase inhibitors versus tamoxifen. Journal of Clinical Oncology 28 509-518. (doi:10.1200/JCO.2009.23.1274)
32. Early Breast Cancer Trialists' Collaborative Group 1998 Tamoxifen for early breast cancer: an overview of the randomised trials. Lancet 351 1451-1467. (doi:10.1016/S0140-6736(97)11423-4)
33. Early Breast Cancer Trialists' Collaborative Group 2005 Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet 365 1687-1717. (doi:10.1016/S0140-6736(05)66544-0)
34. Ellis MJ, Gao F, Dehdashti F, Jeffe DB, Marcom PK, Carey LA, Dickler MN, Silverman P, Fleming GF, Kommareddy A et al. 2009 Lower-dose vs high-dose oral estradiol therapy of hormone receptor-positive, aromatase inhibitor-resistant advanced breast cancer: a phase 2 randomized study. Journal of the American Medical Association 302 774-780. (doi:10.1001/jama.2009.1204)
35. Fagan DH, Uselman RR, Sachdev D & Yee D 2012 Acquired resistance to tamoxifen is associated with loss of the type I insulin-like growth factor receptor: implications for breast cancer treatment. Cancer Research 72 3372-3380. (doi:10.1158/0008-5472.CAN-12-0684)
36. Fan P & Jordan VC 2014 Acquired resistance to selective estrogen receptor modulators (SERMs) in clinical practice (tamoxifen & raloxifene) by selection pressure in breast cancer cell populations. Steroids 90 44-52. (doi:10.1016/j.steroids.2014.06.002)
37. Fan P, McDaniel RE, Kim HR, Clagett D, Haddad B & Jordan VC 2012 Modulating therapeutic effects of the c-Src inhibitor via oestrogen receptor and human epidermal growth factor receptor 2 in breast cancer cell lines. European Journal of Cancer 48 3488-3498. (doi:10.1016/j.ejca.2012.04.020)
38. Fan P, Griffith OL, Agboke FA, Anur P, Zou X, McDaniel RE, Creswell K, Kim SH, Katzenellenbogen JA, Gray JW et al. 2013 c-Src modulates estrogen-induced stress and apoptosis in estrogen-deprived breast cancer cells. Cancer Research 73 4510-4520. (doi:10.1158/0008-5472.CAN-12-4152)
39. Fan P, Agboke FA, McDaniel RE, Sweeney EE, Zou X, Creswell K & Jordan VC 2014a Inhibition of c-Src blocks oestrogen-induced apoptosis and restores oestrogen-stimulated growth in long-term oestrogen-deprived breast cancer cells. European Journal of Cancer 50 457-468. (doi:10.1016/j.ejca.2013.10.001)
40. Fan P, Agboke FA, Cunliffe H, Ramos P & Jordan VC 2014b A molecular model for the mechanism of acquired tamoxifen resistance in breast cancer. European Journal of Cancer 50 2866-2876. (doi:10.1016/j.ejca.2014.08.011)
41. 2-and tamoxifen-stimulated cell growth through global gene expression profiling in br east cancer cells. European Journal of Cancer 50 2877-2886. (doi:10.1016/j.ejca.2014.08.010)
42. Feherty P, Farrer-Brown G & Kellie AE 1971 Oestradiol receptors in carcinoma and benign disease of the breast: an in vitro assay. British Journal of Cancer 25 697-710. (doi:10.1038/bjc.1971.85)
43. Fisher B, Brown A, Wolmark N, Redmond C, Wickerham DL, Wittliff J, Dimitrov N, Poisson SL, Schipper H & Prager D 1987 Prolonging tamoxifen therapy for primary breast cancer. Findings from the National Surgical Adjuvant Breast and Bowel Project clinical trial. Annals of Internal Medicine 106 649-654. (doi:10.7326/0003-4819-106-5-649)
44. Fisher B, Costantino JP, Wickerham DL, Redmond CK, Kavanah M, Cronin WM, Vogel V, Robidoux A, Dimitrov N, Atkins J et al. 1998 Tamoxifen for prevention of breast cancer: report of the National Surgical Adjuvant Breast and Bowel Project P-1 Study. Journal of the National Cancer Institute 90 1371-1388. (doi:10.1093/jnci/90.18.1371)
45. Fisher B, Costantino JP, Wickerham DL, Cecchini RS, Cronin WM, Robidoux A, Bevers TB, Kavanah MT, Atkins JN, Margolese RG et al. 2005 Tamoxifen for the prevention of breast cancer: current status of the National Surgical Adjuvant Breast and Bowel Project P-1 study. Journal of the National Cancer Institute 97 1652-1662. (doi:10.1093/jnci/dji372)
46. Folca PJ, Glascock RF & Irvine WT 1961 Studies with tritium-labelled hexoestrol in advanced breast cancer. Comparison of tissue accumulation of hexoestrol with response to bilateral adrenalectomy and oophorectomy. Lancet 2 796-798. (doi:10.1016/S0140-6736(61)91088-1)
47. Forbes JF, Cuzick J, Buzdar A, Howell A, Tobias JS & Baum M 2008 Effect of anastrozole and tamoxifen as adjuvant treatment for early-stage breast cancer: 100-month analysis of the ATAC trial. Lancet Oncology 9 45-53. (doi:10.1016/S1470-2045(07)70385-6)
48. Fournier DB, Chisamore M, Lurain JR, Rademaker AW, Jordan VC & Tonetti DA 2001 Protein kinase Ca expression is inversely related to ER status in endometrial carcinoma: possible role in AP-1-mediated proliferation of ER-negative endometrial cancer. Gynecologic Oncology 81 366-372. (doi:10.1006/gyno.2001.6164)
49. Frankel LB, Lykkesfeldt AE, Hansen JB & Stenvang J 2007 Protein Kinase Ca is a marker for antiestrogen resistance and is involved in the growth of tamoxifen resistant human breast cancer cells. Breast Cancer Research and Treatment 104 165-179. (doi:10.1007/s10549-006-9399-1)
50. Giovanella BC, Stehlin JS & Williams LJ Jr 1974 Heterotransplantation of human malignant tumors in "nude" thymusless mice. II. Malignant tumors induced by injection of cell cultures derived from human solid tumors. Journal of the National Cancer Institute 52 921-930. (doi:10.1093/jnci/52.3.921)
51. Giovanella BC, Stehlin JS Jr, Williams LJ Jr, Lee SS & Shepard RC 1978 Heterotransplantation of human cancers into nude mice: a model system for human cancer chemotherapy. Cancer 42 2269-2281. (doi:10.1002/1097-0142(197811)42:5<2269::AID-CNCR2820420527>3.0.CO;2-F)
52. Glascock RF & Hoekstra WG 1959 Selective accumulation of tritiumlabelled hexoestrol by the reproductive organs of immature female goats and sheep. Biochemical Journal 72 673-682.
53. Gottardis MM & Jordan VC 1988 Development of tamoxifen-stimulated growth of MCF-7 tumors in athymic mice after long-term antiestrogen administration. Cancer Research 48 5183-5187.
54. Gottardis MM, Robinson SP & Jordan VC 1988 Estradiol-stimulated growth of MCF-7 tumors implanted in athymic mice: a model to study the tumoristatic action of tamoxifen. Journal of Steroid Biochemistry 30 311-314. (doi:10.1016/0022-4731(88)90113-6)
55. Gottardis MM, Wagner RJ, Borden EC & Jordan VC 1989a Differential ability of antiestrogens to stimulate breast cancer cell (MCF-7) growth in vivo and in vitro. Cancer Research 49 4765-4769.
56. Gottardis MM, Jiang SY, Jeng MH & Jordan VC 1989b Inhibition of tamoxifen-stimulated growth of an MCF-7 tumor variant in athymic mice by novel steroidal antiestrogens. Cancer Research 49 4090-4093.
57. Haddow A 1970 David A Karnofsky memorial lecture. Thoughts on chemical therapy. Cancer 26 737-754. (doi:10.1002/1097-0142(197010)26:4<737::AID-CNCR2820260402>3.0.CO;2-T)
58. Haddow A & Robinson AM 1939 The association of carcinogenicity and growth-inhibitory power in the polycyclic hydrocarbons and other substances. Proceedings of the Royal Society of London. Series B, Biological Sciences 127 277-287. (doi:10.1098/rspb.1939.0022)
59. Haddow A, Watkinson JM, Paterson E & Koller PC 1944 Influence of synthetic oestrogens on advanced malignant disease. BMJ 2 393-398. (doi:10.1136/bmj.2.4368.393)
60. Harper MJ & Walpole AL 1967 A new derivative of triphenylethylene: effect on implantation and mode of action in rats. Journal of Reproduction and Fertility 13 101-119. (doi:10.1530/jrf.0.0130101)
61. Harrington WR, Kim SH, Funk CC, Madak-Erdogan Z, Schiff R, Katzenellenbogen JA & Katzenellenbogen BS 2006 Estrogen dendrimer conjugates that preferentially activate extranuclear, nongenomic versus genomic pathways of estrogen action. Molecular Endocrinology 20 491-502. (doi:10.1210/me.2005-0186)
62. Howell A, Dodwell DJ, Anderson H & Redford J 1992 Response after withdrawal of tamoxifen and progestogens in advanced breast cancer. Annals of Oncology 3 611-617.
63. Howell A, Robertson JF, Quaresma Albano J, Aschermannova A, Mauriac L, Kleeberg UR, Vergote I, Erikstein B, Webster A & Morris C 2002 Fulvestrant, formerly ICI 182, 780, is as effective as anastrozole in postmenopausal women with advanced breast cancer progressing after prior endocrine treatment. Journal of Clinical Oncology 20 3396-3403. (doi:10.1200/JCO.2002.10.057)
64. Hu ZZ, Kagan BL, Ariazi EA et al. 2011 Proteomic analysis of pathways involved in estrogen-induced growth and apoptosis of breast cancer cells. PLoS ONE 6 e20410. (doi:10.1371/journal.pone.0020410)
65. Hunter T & Sefton BM 1980 Transforming gene product of Rous sarcoma virus phosphorylates tyrosine. PNAS 77 1311-1315. (doi:10.1073/pnas. 77.3.1311)
66. Huseby RA, Maloney TM & McGrath CM 1984 Evidence for a direct growth-stimulating effect of estradiol on human MCF-7 cells in vivo. Cancer Research 44 2654-2659.
67. Ingle JN, Ahmann DL, Green SJ, Edmonson JH, Bisel HF, Kvols LK, Nichols WC, Creagan ET, Hahn RG, Rubin J et al. 1981 Randomized clinical trial of diethylstilbestrol versus tamoxifen in postmenopausal women with advanced breast cancer. New England Journal of Medicine 304 16-21. (doi:10.1056/NEJM198101013040104)
68. Jeng MH, Parker CJ & Jordan VC 1992 Estrogenic potential of progestins in oral contraceptives to stimulate human breast cancer cell proliferation. Cancer Research 52 6539-6546.
69. Jeng MH, Langan-Fahey SM & Jordan VC 1993 Estrogenic actions of RU486 in hormone-responsive MCF-7 human breast cancer cells. Endocrinology 132 2622-2630. (doi:10.1210/endo.132.6.8504763)
70. Jeng MH, Shupnik MA, Bender TP, Westin EH, Bandyopadhyay D, Kumar R, Masamura S & Santen RJ 1998 Estrogen receptor expression and function in long-term estrogen-deprived human breast cancer cells. Endocrinology 139 4164-4174. (doi:10.1210/endo.139.10.6229)
71. Jensen EV & Jacobson HI 1962 Basic guides to the mechanism of estrogen action. Recent Progress in Hormone Research 18 387-414.
72. Jensen EV & Jordan VC 2003 The estrogen receptor: a model for molecular medicine. Clinical Cancer Research 9 1980-1989.
73. Jiang SY, Wolf DM, Yingling JM, Chang C & Jordan VC 1992 An estrogen receptor positive MCF-7 clone that is resistant to antiestrogens and estradiol. Molecular and Cellular Endocrinology 90 77-86. (doi:10.1016/0303-7207(92)90104-E)
74. Johansson H, Terenius L & Thoren L 1970 The binding of estradiol-17b to human breast cancers and other tissues in vitro. Cancer Research 30 692-698.
75. Jordan VC 1976a Antiestrogenic and antitumor properties of tamoxifen in laboratory animals. Cancer Treatment Reports 60 1409-1419.
76. Jordan VC 1976b Effect of tamoxifen (ICI 46, 474) on initiation and growth of DMBA-induced rat mammary carcinomata. European Journal of Cancer 12 419-424. (doi:10.1016/0014-2964(76)90030-X)
77. Jordan VC 1983 Laboratory studies to develop general principles for the adjuvant treatment of breast cancer with antiestrogens: problems and potential for future clinical applications. Breast Cancer Research and Treatment 3 (Suppl) S73-S86. (doi:10.1007/BF01855131)
78. Jordan VC 1984 Biochemical pharmacology of antiestrogen action. Pharmacological Reviews 36 245-276.
79. Jordan VC 2003a Tamoxifen: a most unlikely pioneering medicine. Nature Reviews. Drug Discovery 2 205-213. (doi:10.1038/nrd1031)
80. Jordan VC 2003b Antiestrogens and selective estrogen receptor modulators as multifunctional medicines. 1. Receptor interactions. Journal of Medicinal Chemistry 46 883-908. (doi:10.1021/jm020449y)
81. Jordan VC 2003c Antiestrogens and selective estrogen receptor modulators as multifunctional medicines. 2. Clinical considerations and new agents. Journal of Medicinal Chemistry 46 1081-1111. (doi:10.1021/jm020450x)
82. Jordan VC 2004 Selective estrogen receptor modulation: concept and consequences in cancer. Cancer Cell 5 207-213. (doi:10.1016/S1535-6108(04)00059-5)
83. Jordan VC 2008a Tamoxifen: catalyst for the change to targeted therapy. European Journal of Cancer 44 30-38. (doi:10.1016/j.ejca.2007.11.002)
84. Jordan VC 2008b The 38th David A. Karnofsky lecture: the paradoxical actions of estrogen in breast cancer - survival or death? Journal of Clinical Oncology 26 3073-3082. (doi:10.1200/JCO.2008.17.5190)
85. Jordan VC 2014a Proven value of translational research with appropriate animal models to advance breast cancer treatment and save lives: the Tamoxifen Tale. British Journal of Clinical Pharmacology [in press]. (doi:10.1111/bcp.12440)
86. Jordan C 2014b Tamoxifen as the first targeted long term adjuvant therapy for breast cancer. Endocrine-Related Cancer 21 R235-R246. (doi:10.1530/ERC-14-0092)
87. Jordan VC 2014c Avoiding the bad and enhancing the good of soy supplements in breast cancer. Journal of the National Cancer Institute 106 dju233. (doi:10.1093/jnci/dju233)
88. Jordan VC 2014d Linking estrogen-induced apoptosis with decreases in mortality following long term adjuvant tamoxifen therapy. Journal of the National Cancer Institute 106 dju296. (doi:10.1093/jnci/dju296)
89. Jordan VC 2014e A(nother) scientific strategy to prevent breast cancer in postmenopausal women by enhancing estrogen-induced apoptosis? Menopause 21 1160-1164. (doi:10.1097/GME.0000000000000220)
90. Jordan VC & Allen KE 1980 Evaluation of the antitumour activity of the non-steroidal antioestrogen monohydroxytamoxifen in the DMBA-induced rat mammary carcinoma model. European Journal of Cancer 16 239-251. (doi:10.1016/0014-2964(80)90156-5)
91. Jordan VC & Brodie AM 2007 Development and evolution of therapies targeted to the estrogen receptor for the treatment and prevention of breast cancer. Steroids 72 7-25. (doi:10.1016/j.steroids.2006.10.009)
92. Jordan VC & Dowse LJ 1976 Tamoxifen as an anti-tumour agent: effect on oestrogen binding. Journal of Endocrinology 68 297-303. (doi:10.1677/joe.0.0680297)
93. Jordan VC & Ford LG 2011 Paradoxical clinical effect of estrogen on breast cancer risk: a 'new' biology of estrogen-induced apoptosis. Cancer Prevention Research 4 633-637. (doi:10.1158/1940-6207.CAPR-11-018)
94. Jordan VC & Jaspan T 1976 Tamoxifen as an anti-tumour agent: oestrogen binding as a predictive test for tumour response. Journal of Endocrinology 68 453-460. (doi:10.1677/joe.0.0680453)
95. Jordan VC & Koerner S 1975 Tamoxifen (ICI 46, 474) and the human carcinoma 8S oestrogen receptor. European Journal of Cancer 11 205-206. (doi:10.1016/0014-2964(75)90119-X)
96. Jordan VC & Koerner S 1976 Tamoxifen as an anti-tumour agent: role of oestradiol and prolactin. Journal of Endocrinology 68 305-311. (doi:10.1677/joe.0.0680305)
97. 3H]tamoxifen in rat uterine cytosols: a comparison of swinging bucket and vertical tube rotor sucrose density gradient analysis. Molecular and Cellular Endocrinology 8 179-188. (doi:10.1016/0303-7207(77)90090-9)
98. Jordan VC, Dix CJ, Rowsby L & Prestwich G 1977 Studies on the mechanism of action of the nonsteroidal antioestrogen tamoxifen (I.C.I. 46, 474) in the rat. Molecular and Cellular Endocrinology 7 177-192. (doi:10.1016/0303-7207(77)90066-1)
99. Jordan VC, Koch R, Mittal S & Schneider MR 1986 Oestrogenic and antioestrogenic actions in a series of triphenylbut-1-enes: modulation of prolactin synthesis in vitro. British Journal of Pharmacology 87 217-223. (doi:10.1111/j.1476-5381.1986.tb10174.x)
100. Jordan VC, Wolf M, Mirecki DM, Whitford DA & Welshons WV 1988 Hormone receptor assays: clinical usefulness in the management of carcinoma of the breast. CRC Critical Reviews in Clinical Laboratory Sciences 26 97-152. (doi:10.3109/10408368809106860)
101. Jordan VC, Schafer JM, Levenson AS, Liu H, Pease KM, Simons LA & Zapf JW 2001 Molecular classification of estrogens. Cancer Research 61 6619-6623.
102. Jordan VC, Liu H & Dardes R 2002 Re: Effect of long-term estrogen deprivation on apoptotic responses of breast cancer cells to 17 β-estradiol and the two faces of Janus: sex steroids as mediators of both cell proliferation and cell death. Journal of the National Cancer Institute 94 1173-1175 author reply 1173-1175. (doi:10.1093/jnci/94.15.1173)
103. Katzenellenbogen BS, Kendra KL, Norman MJ & Berthois Y 1987 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 Research 47 4355-4360.
104. Kennedy BJ 1965 Hormone therapy for advanced breast cancer. Cancer 18 1551-1557. (doi:10.1002/1097-0142(196512)18:12<1551::AID-CNCR2820181206>3.0.CO;2-1)
105. Kiang DT & Kennedy BJ 1977 Tamoxifen (antiestrogen) therapy in advanced breast cancer. Annals of Internal Medicine 87 687-690. (doi:10.7326/0003-4819-87-6-687)
106. Komm BS & Mirkin S 2012 Incorporating bazedoxifene/conjugated estrogens into the current paradigm of menopausal therapy. International Journal of Women's Health 4 129-140. (doi:10.2147/IJWH. S29346)
107. Koubovec D, Ronacher K, Stubsrud E, Louw A & Hapgood JP 2005 Synthetic progestins used in HRT have different glucocorticoid agonist properties. Molecular and Cellular Endocrinology 242 23-32. (doi:10.1016/j.mce.2005.07.001)
108. Lacassagne A 1936a A comparative study of the carcinogenic action of certain oestrogenic hormones. American Journal of Cancer 28 735-740.
109. Lacassagne A 1936b Hormonal pathogenesis of adenocarcinoma of the breast. American Journal of Cancer 27 217-228. (doi:10.1158/ajc.1936.217)
110. LaCroix AZ, Chlebowski RT, Manson JE, Aragaki AK, Johnson KC, Martin L, Margolis KL, Stefanick ML, Brzyski R, Curb JD et al. 2011 Health outcomes after stopping conjugated equine estrogens among post-menopausal women with prior hysterectomy: a randomized controlled trial. Journal of the American Medical Association 305 1305-1314. (doi:10.1001/jama.2011.382)
111. Langan-Fahey SM, Tormey DC & Jordan VC 1990 Tamoxifen metabolites in patients on long-term adjuvant therapy for breast cancer. European Journal of Cancer 26 883-888. (doi:10.1016/0277-5379(90)90191-U)
112. Lathrop AE & Loeb L 1915a Further investigations on the origin of tumors in mice: I. Tumor incidence and tumor age in various strains of mice. Journal of Experimental Medicine 22 646-673. (doi:10.1084/jem.22.5.646)
113. Lathrop AE & Loeb L 1915b Further investigations on the origin of tumors in mice: II. Tumor incidence and tumor age in hybrids. Journal of Experimental Medicine 22 713-731. (doi:10.1084/jem.22.6.713)
114. Lathrop AE & Loeb L 1916 Further investigations on the origin of tumors in mice. III. On the part played by internal secretion in the spontaneous development of tumors. Journal of Cancer Research 1 1-19. (doi:10.1158/jcr.1916.1)
115. Leclercq G, Heuson JC, Schoenfeld R et al. 1973 Estrogen receptors in human breast cancer. European Journal of Cancer 9 665-673. (doi:10.1016/0014-2964(73)90009-1)
116. Levenson AS & Jordan VC 1997 MCF-7: the first hormone-responsive breast cancer cell line. Cancer Research 57 3071-3078.
117. Levenson AS & Jordan VC 1998 The key to the antiestrogenic mechanism of raloxifene is amino acid 351 (aspartate) in the estrogen receptor. Cancer Research 58 1872-1875.
118. Levenson AS, Catherino WH & Jordan VC 1997 Estrogenic activity is increased for an antiestrogen by a natural mutation of the estrogen receptor. Journal of Steroid Biochemistry and Molecular Biology 60 261-268. (doi:10.1016/S0960-0760(96)00184-7)
119. Levenson AS, Kwaan HC, Svoboda KM, Weiss IM, Sakurai S & Jordan VC 1998 Oestradiol regulation of the components of the plasminogen-plasmin system in MDA-MB-231 human breast cancer cells stably expressing the oestrogen receptor. British Journal of Cancer 78 88-95. (doi:10.1038/bjc.1998.447)
120. Lewis JS, Cheng D & Jordan VC 2004 Targeting oestrogen to kill the cancer but not the patient. British Journal of Cancer 90 944-949. (doi:10.1038/sj.bjc.6601627)
121. Lewis JS, Osipo C, Meeke K & Jordan VC 2005a Estrogen-induced apoptosis in a breast cancer model resistant to long-term estrogen withdrawal. Journal of Steroid Biochemistry and Molecular Biology 94 131-141. (doi:10.1016/j.jsbmb.2004.12.032)
122. Lewis JS, Meeke K, Osipo C, Ross EA, Kidawi N, Li T, Bell E, Chandel NS & Jordan VC 2005b Intrinsic mechanism of estradiol-induced apoptosis in breast cancer cells resistant to estrogen deprivation. Journal of the National Cancer Institute 97 1746-1759. (doi:10.1093/jnci/dji400)
123. Lewis-Wambi JS & Jordan VC 2009 Estrogen regulation of apoptosis: how can one hormone stimulate and inhibit? Breast Cancer Research 11 206. (doi:10.1186/bcr2255)
124. Lewis-Wambi JS, Kim HR, Wambi C, Patel R, Pyle JR, Klein-Szanto AJ & Jordan VC 2008 Buthionine sulfoximine sensitizes antihormone-resistant human breast cancer cells to estrogen-induced apoptosis. Breast Cancer Research 10 R104. (doi:10.1186/bcr2208)
125. Lewis-Wambi JS, Swaby R, Kim H & Jordan VC 2009 Potential of L-buthionine sulfoximine to enhance the apoptotic action of estradiol to reverse acquired antihormonal resistance in metastatic breast cancer. Journal of Steroid Biochemistry and Molecular Biology 114 33-39. (doi:10.1016/j.jsbmb.2008.12.016)
126. Lewis-Wambi JS, Kim H, Curpan R, Grigg R, Sarker MA & Jordan VC 2011 The selective estrogen receptor modulator bazedoxifene inhibits hormone-independent breast cancer cell growth and down-regulates estrogen receptor a and cyclin D1. Molecular Pharmacology 80 610-620. (doi:10.1124/mol.111.072249)
127. Lippman ME & Bolan G 1975 Oestrogen-responsive human breast cancer in long term tissue culture. Nature 256 592-593. (doi:10.1038/256592a0)
128. Liu H, Lee ES, Deb Los Reyes A, Zapf JW & Jordan VC 2001 Silencing and reactivation of the selective estrogen receptor modulator-estrogen receptor α complex. Cancer Research 61 3632-3639.
129. Liu H, Park WC, Bentrem DJ, McKian KP, ReyesAde L, Loweth JA, SchaferJM, Zapf JW & Jordan VC 2002 Structure-function relationships of the raloxifene-estrogen receptor-a complex for regulating transforming growth factor-α expression in breast cancer cells. Journal of Biological Chemistry 277 9189-9198. (doi:10.1074/jbc.M108335200)
130. Liu H, Lee ES, Gajdos C, Pearce ST, Chen B, Osipo C, Loweth J, McKian K, De Los Reyes A, Wing L et al. 2003 Apoptotic action of 17β-estradiol in raloxifene-resistant MCF-7 cells in vitro and in vivo. Journal of the National Cancer Institute 95 1586-1597. (doi:10.1093/jnci/djg080)
131. Liu H, Cheng D, Weichel AK, Osipo C, Wing LK, Chen B, Louis TE & Jordan VC 2006 Cooperative effect of gefitinib and fumitremorgin c on cell growth and chemosensitivity in estrogen receptor alpha negative fulvestrant-resistant MCF-7 cells. International Journal of Oncology 29 1237-1246. (doi:10.3892/ijo.29.5.1237)
132. Lonning PE 2009 Additive endocrine therapy for advanced breast cancer - back to the future. Acta Oncologica 48 1092-1101. (doi:10.3109/02841860903117816)
133. Lonning PE, Taylor PD, Anker G, Iddon J, Wie L, Jørgensen LM, Mella O & Howell A 2001 High-dose estrogen treatment in postmenopausal breast cancer patients heavily exposed to endocrine therapy. Breast Cancer Research and Treatment 67 111-116. (doi:10.1023/A:1010619225209)
134. Lubczyk V, Bachmann H & Gust R 2002 Investigations on estrogen receptor binding. The estrogenic, antiestrogenic, and cytotoxic properties of C2-alkyl-substituted 1, 1-bis(4-hydroxyphenyl)-2-phenylethenes. Journal of Medicinal Chemistry 45 5358-5364. (doi:10.1021/jm0209230)
135. Maass H, Engel B, Hohmeister H, Lehmann F & Trams G 1972 Estrogen receptors in human breast cancer tissue. American Journal of Obstetrics and Gynecology 113 377-382.
136. MacGregor Schafer J, Liu H, Bentrem DJ, Zapf JW & Jordan VC 2000 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 Research 60 5097-5105.
137. Masamura S, Santner SJ, Heitjan DF & Santen RJ 1995 Estrogen deprivation causes estradiol hypersensitivity in human breast cancer cells. Journal of Clinical Endocrinology and Metabolism 80 2918-2925. (doi:10.1210/jcem.80.10.7559875)
138. Massarweh S, Osborne CK, Jiang S, Wakeling AE, Rimawi M, Mohsin SK, Hilsenbeck S & Schiff R 2006 Mechanisms of tumor regression and resistance to estrogen deprivation and fulvestrant in a model of estrogen receptor-positive, HER-2/neu-positive breast cancer. Cancer Research 66 8266-8273. (doi:10.1158/0008-5472.CAN-05-4045)
139. Massarweh S, Osborne CK, Creighton CJ, Qin L, Tsimelzon A, Huang S, Weiss H, Rimawi M & Schiff R 2008 Tamoxifen resistance in breast tumors is driven by growth factor receptor signaling with repression of classic estrogen receptor genomic function. Cancer Research 68 826-833. (doi:10.1158/0008-5472.CAN-07-2707)
140. Maximov PY, Fernandes DJ, McDaniel RE, Myers CB, Curpan RF & Jordan VC 2014a Influence of the length and positioning of the antiestrogenic side chain of endoxifen and 4-hydroxytamoxifen on gene activation and growth of estrogen receptor positive cancer cells. Journal of Medicinal Chemistry 57 4569-4583. (doi:10.1021/jm500569h)
141. Maximov PY, McDaniel RE, Fernandes DJ, Bhatta P, Korostyshevskiy VR, Curpan RF & Jordan VC 2014b Pharmacological relevance of endoxifen in a laboratory simulation of breast cancer in postmenopausal patients. Journal of the National Cancer Institute 106 dju283. (doi:10.1093/jnci/dju283)
142. Maximov PY, McDaniel RE, Fernandes DJ et al. 2014c Simulation with cells in vitro of tamoxifen treatment in premenopausal breast cancer patients with different CYP2D6 genotypes. British Journal of Pharmacology 171 5624-5635. (doi:10.1111/bph.12864)
143. McGuire WL, Carbone PP & Vollmer EP (Eds) 1975a Estrogen Receptors in Human Breast Cancer. New York: Raven Press.
144. McGuire WL, Carbone PP, Sears ME et al. 1975b Estrogen receptors in human breast cancer: an overview. In Estrogen Receptors and Human Breast Cancer, pp 1-15. eds WL McGuire, PP Carbone & EP Vollmer. New York: Raven Press.
145. Mehta RS, Barlow WE, Albain KS, Vandenberg TA, Dakhil SR, Tirumali NR, Lew DL, Hayes DF, Gralow JR, Livingston RB et al. 2012 Combination anastrozole and fulvestrant in metastatic breast cancer. New England Journal of Medicine 367 435-444. (doi:10.1056/NEJMoa1201622)
146. Miranda TB, Voss TC, Sung MH, Baek S, John S, Hawkins M, Grøntved L, Schiltz RL & Hager GL 2013 Reprogramming the chromatin landscape: interplay of the estrogen and glucocorticoid receptors at the genomic level. Cancer Research 73 5130-5139. (doi:10.1158/0008-5472.CAN-13-0742)
147. Molloy ME, Perez White BE, Gherezghiher T, Michalsen BT, Xiong R, Patel H, Zhao H, Maximov PY, Jordan VC, Thatcher GR et al. 2014 Novel selective estrogen mimics for the treatment of tamoxifen-resistant breast cancer. Molecular Cancer Therapeutics 13 2515-2526. (doi:10.1158/1535-7163.MCT-14-0319)
148. Morgan LR Jr, Schein PS, Woolley PV, Hoth D, Macdonald J, Lippman M, Posey LE & Beazley RW 1976 Therapeutic use of tamoxifen in advanced breast cancer: correlation with biochemical parameters. Cancer Treatment Reports 60 1437-1443.
149. Murphy CS, Meisner LF, Wu SQ & Jordan VC 1989 Short- and long-term estrogen deprivation of T47D human breast cancer cells in culture. European Journal of Cancer and Clinical Oncology 25 1777-1788. (doi:10.1016/0277-5379(89)90348-9)
150. Murphy CS, Pink JJ & Jordan VC 1990 Characterization of a receptor-negative, hormone-nonresponsive clone derived from a T47D human breast cancer cell line kept under estrogen-free conditions. Cancer Research 50 7285-7292.
151. Nabha SM, Glaros S, Hong M, Lykkesfeldt AE, Schiff R, Osborne K & Reddy KB 2005 Upregulation of PKC-d contributes to antiestrogen resistance in mammary tumor cells. Oncogene 24 3166-3176. (doi:10.1038/sj.onc. 1208502)
152. Obiorah I & Jordan VC 2013 2012 NAMS/PFIZER-Wulf H. Utian endowed lecture. The scientific rationale for a delay after menopause in the use of conjugated equine estrogens in postmenopausal women that causes a reduction in breast cancer incidence and mortality. Menopause 20 372-382. (doi:10.1097/GME.0b013e31828865a5)
153. Obiorah IE & Jordan VC 2014 Differences in the rate of oestrogen-induced apoptosis in breast cancer by estradiol and the triphenylethylene bisphenol. British Journal of Pharmacology 17 4062-4072. (doi:10.1111/bph.12762)
154. Obiorah I, Sengupta S, Fan P & Jordan VC 2014a Delayed triggering of oestrogen induced apoptosis that contrasts with rapid paclitaxel-induced breast cancer cell death. British Journal of Cancer 110 1488-1496. (doi:10.1038/bjc.2014.50)
155. Obiorah IE, Fan P & Jordan VC 2014b Breast cancer cell apoptosis with phytoestrogens is dependent on an estrogen deprived state. Cancer Prevention Research 7 939-949. (doi:10.1158/1940-6207.CAPR-14-0061)
156. Obiorah I, Sengupta S, Curpan R & Jordan VC 2014c Defining the conformation of the estrogen receptor complex that controls estrogen-induced apoptosis in breast cancer. Molecular Pharmacology 85 789-799. (doi:10.1124/mol.113.089250)
157. Obiorah IE, Fan P, Sengupta S & Jordan VC 2014d Selective estrogen-induced apoptosis in breast cancer. Steroids 90C 60-70. (doi:10.1016/j.steroids.2014.06.003)
158. Osborne CK, Hobbs K & Clark GM 1985 Effect of estrogens and antiestrogens on growth of human breast cancer cells in athymic nude mice. Cancer Research 45 584-590.
159. Osborne CK, Coronado EB & Robinson JP 1987 Human breast cancer in the athymic nude mouse: cytostatic effects of long-term antiestrogen therapy. European Journal of Cancer and Clinical Oncology 23 1189-1196. (doi:10.1016/0277-5379(87)90154-4)
160. Osborne CK, Pippen J, Jones SE, Parker LM, Ellis M, Come S, Gertler SZ, May JT, Burton G, Dimery I et al. 2002 Double-blind, randomized trial comparing the efficacy and tolerability offulvestrant versus anastrozole in postmenopausal women with advanced breast cancer progressing on prior endocrine therapy: results of a North American trial. Journal of Clinical Oncology 20 3386-3395. (doi:10.1200/JCO.2002.10.058)
161. Osipo C, Gajdos C, Liu H, Chen B & Jordan VC 2003 Paradoxical action of fulvestrant in estradiol-induced regression of tamoxifen-stimulated breast cancer. Journal of the National Cancer Institute 95 1597-1608. (doi:10.1093/jnci/djg079)
162. Osipo C, Gajdos C, Cheng D & Jordan VC 2005 Reversal of tamoxifen resistant breast cancer by low dose estrogen therapy. Journal of Steroid Biochemistry and Molecular Biology 93 249-256. (doi:10.1016/j.jsbmb.2004.12.005)
163. Osipo C, Meeke K, Cheng D, Weichel A, Bertucci A, Liu H & Jordan VC 2007 Role for HER2/neu and HER3 in fulvestrant-resistant breast cancer. International Journal of Oncology 30 509-520. (doi:10.3892/ijo.30.2.509)
164. Peethambaram PP, Ingle JN, Suman VJ, Hartmann LC & Loprinzi CL 1999 Randomized trial of diethylstilbestrol vs. tamoxifen in postmenopausal women with metastatic breast cancer. An updated analysis. Breast Cancer Research and Treatment 54 117-122. (doi:10.1023/A:1006185805079)
165. Perez White B, Molloy ME, Zhao H et al. 2013 Extranuclear ERa is associated with regression of T47D PKCa-overexpressing, tamoxifen-resistant breast cancer. Molecular Cancer 12 34. (doi:10.1186/1476-4598-12-34)
166. Pink JJ & Jordan VC 1996 Models of estrogen receptor regulation by estrogens and antiestrogens in breast cancer cell lines. Cancer Research 56 2321-2330.
167. Pink JJ, Jiang SY, Fritsch M & Jordan VC 1995 An estrogen-independent MCF-7 breast cancer cell line which contains a novel 80-kilodalton estrogen receptor-related protein. Cancer Research 55 2583-2590.
168. Pink JJ, Wu SQ, Wolf DM, Bilimoria MM & Jordan VC 1996a A novel 80 kDa human estrogen receptor containing a duplication of exons 6 and 7. Nucleic Acids Research 24 962-969. (doi:10.1093/nar/24.5.962)
169. Pink JJ, Bilimoria MM, Assikis J & Jordan VC 1996b Irreversible loss of the oestrogen receptor in T47D breast cancer cells following prolonged oestrogen deprivation. British Journal of Cancer 74 1227-1236. (doi:10.1038/bjc.1996.521)
170. Pink JJ, Fritsch M, Bilimoria MM, Assikis VJ & Jordan VC 1997 Cloning and characterization of a 77-kDa oestrogen receptor isolated from a human breast cancer cell line. British Journal of Cancer 75 17-27. (doi:10.1038/bjc.1997.4)
171. Powles TJ, Ashley S, Tidy A, Smith IE & Dowsett M 2007 Twenty-year follow-up of the Royal Marsden randomized, double-blinded tamox-ifen breast cancer prevention trial. Journal of the National Cancer Institute 99 283-290. (doi:10.1093/jnci/djk050)
172. Pradhan M, Baumgarten SC, Bembinster LA & Frasor J 2012 CBP mediates NF-κB-dependent histone acetylation and estrogen receptor recruitment to an estrogen response element in the BIRC3 promoter. Molecular and Cellular Biology 32 569-575. (doi:10.1128/MCB.05869-11)
173. Robson JM 1937 Oestrous reactions, including mating, produced by triphenyl ethylene. Nature 140 196. (doi:10.1038/140196b0)
174. Robson JM & Schonberg JM 1938 Duration of action of natural and synthetic oestrogens. Nature 142 292-293. (doi:10.1038/142292a0)
175. Robson J & Schonberg A 1942 A new synthetic oestrogen with prolonged action when given orally. Nature 150 22-23. (doi:10.1038/150022a0)
176. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, Stefanick ML, Jackson RD, Beresford SA, Howard BV, Johnson KC et al. 2002 Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women's Health Initiative randomized controlled trial. Journal of the American Medical Association 288 321-333. (doi:10.1001/jama.288.3.321)
177. Rygaard J & Povlsen CO 1969 Heterotransplantation of a human malignant tumour to "Nude" mice. Acta Pathologica et Microbiologica Scandinavica 77 758-760. (doi:10.1111/j.1699-0463.1969.tb04520.x)
178. Schafer JI, Liu H, Tonetti DA & Jordan VC 1999 The interaction of raloxifene and the active metabolite of the antiestrogen EM-800 (SC 5705) with the human estrogen receptor. Cancer Research 59 4308-4313.
179. Schinzinger A 1889 Ueber carcinoma mammae [abstract]. Beilage zum Centralblatt fur Chirurgie.18th Congress of the German Society for Surgery. 16 55-56.
180. Schrek R 1959 Fashions in cancer research. In The Year Book of Pathology and Clinical Pathology, pp 26-39. Chicago: The Year Book Publishers.
181. Scottish Cancer Trials Office (MRC) 1987 Adjuvant tamoxifen in the management of operable breast cancer: the Scottish Trial. Report from the Breast Cancer Trials Committee, Edinburgh. Lancet 2 171-175. (doi:10.1016/S0140-6736(87)90762-8)
182. Sengupta S, Obiorah I, Maximov PY, Curpan R & Jordan VC 2013 Molecular mechanism of action of bisphenol and bisphenol A mediated by oestrogen receptor alpha in growth and apoptosis of breast cancer cells. British Journal of Pharmacology 169 167-178. (doi:10.1111/bph.12122)
183. Shafie SM 1980 Estrogen and the growth of breast cancer: new evidence suggests indirect action. Science 209 701-702. (doi:10.1126/science.6994231)
184. Shafie SM & Grantham FH 1981 Role of hormones in the growth and regression of human breast cancer cells (MCF-7) transplanted into athymic nude mice. Journal of the National Cancer Institute 67 51-56. (doi:10.1093/jnci/67.1.51)
185. Shang Y, Hu X, DiRenzo J, Lazar MA & Brown M 2000 Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 103 843-852. (doi:10.1016/S0092-8674(00)00188-4)
186. Shiau AK, Barstad D, Loria P, Cheng L, Kushner PJ, Agard DA & Greene GL 1998 The structural basis of estrogen receptor/coactivator recognition and the antagonism of this interaction by tamoxifen. Cell 95 927-937. (doi:10.1016/S0092-8674(00)81717-1)
187. Shike M, Doane A, Russo L et al. 2014 The effects of soy supplementation on gene expression in breast cancer: a randomized placebo-controlled study. Journal of the National Cancer Institute 106 dju189. (doi:10.1093/jnci/dju189)
188. Sledge GW, Mamounas EP, Hortobagyi GN, Burstein HJ, Goodwin PJ & Wolff AC 2014 Past, present, and future challenges in breast cancer treatment. Journal of Clinical Oncology 32 1979-1986. (doi:10.1200/JCO.2014.55.4139)
189. Song RX & Santen RJ 2003 Apoptotic action of estrogen. Apoptosis 8 55-60. (doi:10.1023/A:1021649019025)
190. Song RX, Mor G, Naftolin F, McPherson RA, Song J, Zhang Z, Yue W, Wang J & Santen RJ 2001 Effect of long-term estrogen deprivation on apoptotic responses of breast cancer cells to 17β-estradiol. Journal of the National Cancer Institute 93 1714-1723. (doi:10.1093/jnci/93.22.1714)
191. C breast cancer cells. Apoptosis 10 667-678. (doi:10.1007/s10495-005-1903-2)
192. Soule HD & McGrath CM 1980 Estrogen responsive proliferation of clonal human breast carcinoma cells in athymic mice. Cancer Letters 10 177-189. (doi:10.1016/0304-3835(80)90042-7)
193. Soule HD, Vazguez J, Long A, Albert S & Brennan M 1973 A human cell line from a pleural effusion derived from a breast carcinoma. Journal of the National Cancer Institute 51 1409-1416. (doi:10.1093/jnci/51.5.1409)
194. Stoll B 1977 Palliation by castration or hormone ablation. In Breast Cancer Management Early and Late, pp 135-149. Ed BA Stoll. London: William Herman Medical Books Ltd.
195. Sweeney EE, McDaniel RE, Maximov PY, Fan P & Jordan VC 2012 Models and mechanisms of acquired antihormone resistance in breast cancer: significant clinical progress despite limitations. Hormone Molecular Biology and Clinical Investigation 9 143-163. (doi:10.1515/hmbci-2011-0004)
196. Sweeney EE, Fan P & Jordan VC 2014a Mechanisms underlying differential response to estrogen-induced apoptosis in long-term estrogen-deprived breast cancer cells. International Journal of Oncology 44 1529-1538. (doi:10.3892/ijo.2014.2329)
197. Sweeney EE, Fan P & Jordan VC 2014b Molecular modulation of estrogen-induced apoptosis by synthetic progestins in hormone replacement therapy: an insight into the Women's Health Initiative study. Cancer Research 74 7060-7068. (doi:10.1158/0008-5472.CAN-14-1784)
198. Terenius L 1971 Structure-activity relationships of anti-oestrogens with regard to interaction with 17-β-oestradiol in the mouse uterus and vagina. Acta Endocrinologica 66 431-447. (doi:10.1530/acta.0.0660431)
199. Toft D & Gorski J 1966 A receptor molecule for estrogens: isolation from the rat uterus and preliminary characterization. PNAS 55 1574-1581. (doi:10.1073/pnas.55.6.1574)
200. Toft D, Shyamala G & Gorski J 1967 A receptor molecule for estrogens: studies using a cell-free system. PNAS 57 1740-1743.
201. Tonetti DA, Chisamore MJ, Grdina W, Schurz H & Jordan VC 2000 Stable transfection of protein kinase C alpha cDNA in hormone-dependent breast cancer cell lines. British Journal of Cancer 83 782-791. (doi:10.1054/bjoc.2000.1326)
202. Uht RM, Anderson CM, Webb P & Kushner PJ 1997 Transcriptional activities of estrogen and glucocorticoid receptors are functionally integrated at the AP-1 response element. Endocrinology 138 2900-2908. (doi:10.1210/endo.138.7.5244)
203. Walpole AL & Paterson E 1949 Synthetic oestrogens in mammary cancer. Lancet 2 783-786. (doi:10.1016/S0140-6736(49)91370-7)
204. Wardell SE, Nelson ER, Chao CA & McDonnell DP 2013 Bazedoxifene exhibits antiestrogenic activity in animal models of tamoxifen-resistant breast cancer: implications for treatment of advanced disease. Clinical Cancer Research 19 2420-2431. (doi:10.1158/1078-0432.CCR-12-3771)
205. Welshons WV & Jordan VC 1987 Adaptation of estrogen-dependent MCF-7 cells to low estrogen (phenol red-free) culture. European Journal of Cancer and Clinical Oncology 23 1935-1939. (doi:10.1016/0277-5379(87)90062-9)
206. Wolf DM & Jordan VC 1993 A laboratory model to explain the survival advantage observed in patients taking adjuvant tamoxifen therapy. Recent Results in Cancer Research 127 23-33.
207. Yao K, Lee ES, Bentrem DJ, England G, Schafer JI, O'Regan RM & Jordan VC 2000 Antitumor action of physiological estradiol on tamoxifen-stimulated breast tumors grown in athymic mice. Clinical Cancer Research 6 2028-2036.
208. Zhang Y, Zhao H, Asztalos S, Chisamore M, Sitabkhan Y & Tonetti DA 2009 Estradiol-induced regression in T47D:A18/PKCa tumors requires the estrogen receptor and interaction with the extracellular matrix. Molecular Cancer Research 7 498-510. (doi:10.1158/1541-7786.MCR-08-0415)