The St. Gallen Prize Lecture 2011: Evolution of long-term adjuvant anti-hormone therapy: Consequences and opportunities

Breast

Volumn 20, Issue SUPPL. 3, 2011, Pages

  Jordan, V Craig ^a   Obiorah, Ifeyinwa ^a   Fan, Ping ^a   Kim, Helen R ^a   Ariazi, Eric ^b   Cunliffe, Heather ^c   Brauch, Hiltrud ^d  

^a GEORGETOWN UNIVERSITY   (United States)

^b FOX CHASE CANCER CENTER   (United States)

^c Translational Cenomics   (United States)

^d DR MARGARETE FISCHER BOSCH INSTITUTE OF CLINICAL PHARMACOLOGY   (Germany)

Author keywords

Acquired drug resistance Chemoprevention; Raloxifene Apoptosis Oestrogen; Tamoxifen Selective oestrogen receptor modulators (SERMs)

Indexed keywords

AROMATASE INHIBITOR; DIETHYLSTILBESTROL; ESTRADIOL; ESTROGEN RECEPTOR; LASOFOXIFENE; LETROZOLE; RALOXIFENE; SELECTIVE ESTROGEN RECEPTOR MODULATOR; SEROTONIN UPTAKE INHIBITOR; TAMOXIFEN; TAMOXIFEN CITRATE; VENLAFAXINE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; BREAST CANCER; CANCER ADJUVANT THERAPY; CANCER GROWTH; CANCER INCIDENCE; CANCER MORTALITY; CANCER RESISTANCE; CANCER RISK; CANCER SURVIVAL; CLINICAL TRIAL (TOPIC); DRUG APPROVAL; DRUG CHOICE; DRUG EFFICACY; DRUG INHIBITION; DRUG MEGADOSE; DRUG METABOLISM; DRUG RECEPTOR BINDING; DRUG SAFETY; DRUG STRUCTURE; DRUG TARGETING; EARLY INTERVENTION; ESTROGEN THERAPY; HUMAN; LONG TERM CARE; LOW DRUG DOSE; MOLECULAR INTERACTION; NONHUMAN; OSTEOPOROSIS; POSTMENOPAUSE; PREMENOPAUSE; PRIORITY JOURNAL; REVIEW; RISK BENEFIT ANALYSIS; RISK REDUCTION; SIGNAL TRANSDUCTION; SURVIVAL RATE; TREATMENT DURATION;

EID: 80051691488     PISSN: 09609776     EISSN: 15323080     Source Type: Journal    
DOI: 10.1016/S0960-9776(11)70287-9     Document Type: Review

References (88)

1. Jordan VC Tamoxifen: a most unlikely pioneering medicine. Nat Rev Drug Discov 2003, 2:205-213.
2. Jordan VC Tamoxifen: catalyst for the change to targeted therapy. EurJ Cancer 2008, 44:30-38.
3. Jordan VC Selective estrogen receptor modulation: a personal perspective. Cancer Res 2001, 61:5683-5687.
4. Jordan VC The 38th David A. Karnofsky lecture: the paradoxical actions of estrogen in breast cancer - survival or death?. J Clin Oncol 2008, 26:3073-3082.
5. EBCTCG Tamoxifen for early breast cancer: an overview of the randomised trials. Lancet 1998, 351:1451-1467.
6. EBCTCG Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet 2005, 365:1687-1717.
7. Jordan VC, Koerner S Tamoxifen (ICI 46,474) and the human carcinoma 8S oestrogen receptor. EurJ Cancer 1975, 11:205-206.
8. Jordan V, Dix CJ, Allen KE The effectiveness of long term tamoxifen treatment in a laboratory model for adjuvant hormone therapy of breast cancer. Adjuvant Ther Cancer 1979, 2:19-26.
9. Jordan VC, Allen KE Evaluation of the antitumour activity of the non-steroidal antioestrogen monohydroxytamoxifen in the DMBA-induced rat mammary carcinoma model. EurJ Cancer 1980, 16:239-251.
10. Jordan VC, Collins MM, Rowsby L, Prestwich G A monohydroxylated metabolite of tamoxifen with potent antioestrogenic activity. J Endocrmo 1977, 75:305-316.
11. Jordan VC, Dix CJ, Naylor KE, Prestwich G, Rowsby L Nonsteroidal antiestrogens: their biological effects and potential mechanisms of action. J Toxicol Environ Health 1978, 4:363-390.
12. Allen KE, Clark ER, Jordan VC Evidence for the metabolic activation of non-steroidal antioestrogens: a study of structure-activity relationships. Br J Pharmacol 1980, 71:83-91.
13. NATO Controlled trial of tamoxifen as adjuvant agent in management of early breast cancer. Interim analysis at four years by Nolvadex Adjuvant Trial Organisation. Lancet 1983, 1:257-261.
14. NATO Controlled trial of tamoxifen as single adjuvant agent in management of early breast cancer. Analysis at six years by Nolvadex Adjuvant Trial Organisation. Lancet 1985, 1:836-840.
15. Cole MP, Jones CT, Todd ID A new anti-oestrogenic agent in late breast cancer. An early clinical appraisal of ICI46474. BrJ Cancer 1971, 25:270-275.
16. Jordan VC, Brodie AM Development and evolution of therapies targeted to the estrogen receptor for the treatment and prevention of breast cancer. Steroids 2007, 72:7-25.
17. Howell A, Cuzick J, Baum M, Buzdar A, Dowsett M, Forbes JF, et al. Results of the ATAC (Arimidex, Tamoxifen, Alone or in Combination) trial after completion of 5 years' adjuvant treatment for breast cancer. Lancet 2005, 365:60-62.
18. Hershman DL, Kushi LH, Shao T, Buono D, Kershenbaum A, Tsai WY, et al. Early discontinuation and nonadherence to adjuvant hormonal therapy in a cohort of 8,769 early-stage breast cancer patients. J Clin Oncol 2010, 28:4120-4128.
19. Partridge AH, LaFountain A, Mayer E, Taylor BS, Winer E, Asnis-Alibozek A Adherence to initial adjuvant anastrozole therapy among women with early-stage breast cancer. J Clin Oncol 2008, 26:556-562.
20. Lash TL, Fox MP, Westrup JL, Fink AK, Silliman RA Adherence to tamoxifen over the five-year course. Breast Cancer Res Treat 2006, 99:215-220.
21. McCowan C, Shearer J, Donnan FT, Dewar JA, Crilly M, Thompson AM, et al. Cohort study examining tamoxifen adherence and its relationship to mortality in women with breast cancer. BrJ Cancer 2008, 99:1763-1768.
22. Geiger AM, Thwin SS, Lash TL, Buist DS, Prout MN, Wei F, et al. Recurrences and second primary breast cancers in older women with initial early-stage disease. Cancer 2007, 109:966-974.
23. Yood MU, Owusu C, Buist DS, Geiger AM, Field TS, Thwin SS, et al. Mortality impact of less-than-standard therapy in older breast cancer patients. J Am Coll Surg 2008, 206:66-75.
24. Brauch H, Jordan VC Targeting of tamoxifen to enhance antitumour action for the treatment and prevention of breast cancer: the 'personalised' approach?. Eur J Cancer 2009, 45:2274-2283.
25. Dezentje VO, van Blijderveen NJ, Gelderblom H, Putter H, van Herk-Sukel MP, Casparie MK, et al. Effect of concomitant CYP2D6 inhibitor use and tamoxifen adherence on breast cancer recurrence in early-stage breast cancer. J Clin Oncol 2010, 28:2423-2429.
26. Lash TL, Cronin-Fenton D, Ahern TP, Rosenberg CL, Lunetta KL, Silliman RA, et al. Breast cancer recurrence risk related to concurrent use of SSRI antidepressants and tamoxifen. Acta Oncol 2010, 49:305-312.
27. Kelly CM, Juurlink DN, Gomes T, Duong-Hua M, Pritchard KI, Austin PC, et al. Selective serotonin reuptake inhibitors and breast cancer mortality in women receiving tamoxifen: a population based cohort study. BMJ 2010, 340-693.
28. SCTO Adjuvant tamoxifen in the management of operable breast cancer: the Scottish Trial. Report from the Breast Cancer Trials Committee, Scottish Cancer Trials Office (MRC), Edinburgh. Lancet 1987, 2:171-175.
29. Levenson AS, Jordan VC MCF-7: the first hormone-responsive breast cancer cell line. Cancer Res 1997, 57:3071-3078.
30. Osborne CK, Coronado EB, Robinson JP Human breast cancer in the athymic nude mouse: cytostatic effects of long-term antiestrogen therapy. Eur J Cancer Clin Oncol 1987, 23:1189-1196.
31. Jordan VC Selective estrogen receptor modulation: concept and consequences in cancer. Cancer Cell 2004, 5:207-213.
32. Gottardis MM, Jordan VC Development of tamoxifen-stimulated growth of MCF-7 tumors in athymic mice after long-term antiestrogen administration. Cancer Res 1988, 48:5183-5187.
33. Gottardis MM, Jiang SY, Jeng MH, Jordan VC Inhibition of tamoxifen-stimulated growth of an MCF-7 tumor variant in athymic mice by novel steroidal antiestrogens. Cancer Res 1989, 49:4090-4093.
34. Wakeling AE, Dukes M, Bowler J A potent specific pure antiestrogen with clinical potential. Cancer Res 1991, 51:3867-3873.
35. Osborne CK, Pippen J, Jones SE, Parker LM, Ellis M, Come S, et al. 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 2002, 20:3386-3395.
36. Howell A, Robertson JF, Quaresma Albano J, Aschermannova A, Mauriac L, Kleeberg UR, et al. Fulvestrant, formerly ICI 182,780, is as effective as anastrozole in postmenopausal women with advanced breast cancer progressing after prior endocrine treatment.;. Clin Oncol 2002, 20:3396-3403.
37. Wolf DM, Jordan VC A laboratory model to explain the survival advantage observed in patients taking adjuvant tamoxifen therapy. Recent Results Cancer Res 1993, 127:23-33.
38. Yao K, Lee ES, Bentrem DJ, England G, Schafer JI, O'Regan RM, et al. Antitumor action of physiological estradiol on tamoxifen-stimulated breast tumors grown in athymic mice. Clin Cancer Res 2000, 6:2028-2036.
39. Song RX, Mor G, Naftolin F, McPherson RA, Song J, Zhang Z, et al. Effect of long-term estrogen deprivation on apoptotic responses of breast cancer cells to 17beta-estradiol. J Natl Cancer Inst 2001, 93:1714-1723.
40. Liu H, Lee ES, Gajdos C, Pearce ST, Chen B, Osipo C, et al. Apoptotic action of 17beta-estradiol in raloxifene-resistant MCF-7 cells in vitro and in vivo. J Nati Cancer Inst 2003, 95:1586-1597.
41. Osipo C, Gajdos C, Liu H, Chen B, ordan VC Paradoxical action of fulvestrant in estradiol-induced regression of tamoxifen-stimulated breast cancerJNar/. Cancer Inst 2003, 95:1597-1608.
42. Lewis JS, Meeke K, Osipo C, Ross EA, Kidawi N, Li T, et al. Intrinsic mechanism of estradiol-induced apoptosis in breast cancer cells resistant to estrogen deprivation. J Nati Cancer Inst 2005, 97:1746-1759.
43. Lonning PE, Taylor PD, Anker G, Iddon J, Wie L, Jorgensen LM, et al. High-dose estrogen treatment in postmenopausal breast cancer patients heavily exposed to endocrine therapy. Breast Cancer Res Treat 2001, 67:111-116.
44. Ellis MJ, Gao F, Dehdashti F, Jeffe DB, Marcom PK, Carey LA, et al. Lower-dose vs high-dose oral estradiol therapy of hormone receptor-positive, aromatase inhibitor-resistant advanced breast cancer: a phase 2 randomized study. JAMA 2009, 302:774-780.
45. Balaburski GM, Dardes RC, Johnson M, Haddad B, Zhu F, Ross EA, et al. Raloxifene-stimulated experimental breast cancer with the paradoxical actions of estrogen to promote or prevent tumor growth: a unifying concept in anti-hormone resistance. IntJ Oncol 2010, 37:387-398.
46. Lewis JS, Osipo C, Meeke K, Jordan VC Estrogen-induced apoptosis in a breast cancer model resistant to long-term estrogen withdrawal./. Steroid Biochem Mol Biol 2005, 94:131-141.
47. Haddow A, Watkinson JM, Paterson E, Koller PC Influence of synthetic oestrogens on advanced malignant disease. Br MedJ 1944, 2:393-398.
48. Haddow A David A. Karnofsky memorial lecture. Thoughts on chemical therapy. Cancer 1970, 26:737-754.
49. Lewis-Wambi JS, Kim HR, Wambi C, Patel R, Pyle JR Klein-Szanto AJ, et al. Buthionine sulfoximine sensitizes antihormone-resistant human breast cancer cells to estrogen-induced apoptosis. Breast Cancer Res 2008, 10:R104.
50. Shiau AK, Barstad D, Loria PM, Cheng L, Kushner PJ, Agard DA, et al. The structural basis of estrogen receptor/coactivator recognition and the antagonism of this interaction by tamoxifen. Cell 1998, 95:927-937.
51. Brzozowski AM, Pike AC, Dauter Z, Hubbard RE, Bonn T, Engstrom o, et al. Molecular basis of agonism and antagonism in the oestrogen receptor. Nature 1997, 389:753-758.
52. Levenson AS, Jordan VC The key to the antiestrogenic mechanism of raloxifene is amino acid 351 (aspartate) in the estrogen receptor. Cancer Res 1998, 58:1872-1875.
53. 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 2000, 60:5097-5105.
54. Liu H, Lee ES, Deb Los Reyes A, Zapf JW, Jordan VC Silencing and reactivation of the selective estrogen receptor modulator-estrogen receptor alpha complex. Cancer Res 2001, 61:3632-3639.
55. Liu H, Park WC, Bentrem DJ, McKian KP, Reyes Ade L, Loweth JA, et al. Structure-function relationships of the raloxifene-estrogen receptor-alpha complex for regulating transforming growth factor-alpha expression in breast cancer cells. JBiol Chem 2002, 277:9189-9198.
56. Jordan VC, Schafer JM, Levenson AS, Liu H, Pease KM, Simons LA, et al. Molecular classification of estrogens. Cancer Res 2001, 61:6619-6623.
57. Maximov PY, Myers CB, Curpan RF, Lewis-Wambi JS, Jordan VC Structure-function relationships of estrogenic triphenylethylenes related to endoxifen and 4-hydroxytamoxifen. J Med Chem 2010, 53:3273-3283.
58. Sengupta S, Sharma CG, Jordan VC Estrogen regulation of X-box binding protein-1 and its role in estrogen induced growth of breast and endometrial cancer cells. Horm Mol Biol Clin Investig 2010, 2:235-243.
59. Bourgoin-Voillard S, Gallo D, Laios I, Cleeren A, Bali LE, Jacquot Y, et al. Capacity of type I and II ligands to confer to estrogen receptor alpha 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. Biochem Pharmacol 2010, 79:746-757.
60. Lonning PE Additive endocrine therapy for advanced breast cancer - back to the future. Acta Oncol 2009, 48:1092-1101.
61. Stefanick ML, Anderson GL, Margolis KL, Hendrix SL, Rodabough RJ, Paskett ED, et al. Effects of conjugated equine estrogens on breast cancer and mammography screening in postmenopausal women with hysterectomy. JAMA 2006, 295:1647-1657.
62. Beral V, Reeves G, Bull D, Green J Breast cancer risk in relation to the interval between menopause and starting hormone therapy. JNar/. Cancer Inst 2011, 103:296-305.
63. Lewis-Wambi JS, Jordan VC Estrogen regulation of apoptosis: how can one hormone stimulate and inhibit?. Breast Cancer Res 2009, 11:206.
64. Maximov PY, Lewis-Wambi JS, Jordan VC The paradox of oestradiol-induced breast cancer cell growth and apoptosis. Curr Signal Transduct Ther 2009, 4:88-102.
65. Berger MF, Lawrence MS, Demichelis F, Drier Y, Cibulskis K, Sivachenko AY, et al. The genomic complexity of primary human prostate cancer. Nature 2011, 470:214-220.
66. Pfeifer GP, Hainaut P Next-generation sequencing: emerging lessons on the origins of human cancer. Curr Opin Oncol 2011, 23:62-68.
67. Ottenhoff-Kalff AE, Rijksen G, van Beurden EA, Hennipman A, Michels AA, Staal GE Characterization of protein tyrosine kinases from human breast cancer: involvement of the c-Src oncogene product. Cancer Res 1992, 52:4773-4778.
68. Jordan VC Tamoxifen (ICI46.474) as a targeted therapy to treat and prevent breast cancer. BrJ Pharmacol 2006, 147(Suppl l):S269-S276.
69. Jordan VC, Robinson SP Species-specific pharmacology of antiestrogens: role of metabolism. Fed Proc 1987, 46:1870-1874.
70. Jordan VC, Phelps E, Lindgren JU Effects of anti-estrogens on bone in castrated and intact female rats. Breast Cancer Res Treat 1987, 10:31-35.
71. Love RR, Mazess RB, Barden HS, Epstein S, Newcomb PA, Jordan VC, et al. Effects of tamoxifen on bone mineral density in postmenopausal women with breast cancer. N Engl J Med 1992, 326:852-856.
72. Love RR, Wiebe DA, Newcomb PA, Cameron L, Leventhal H, Jordan VC, et al. Effects of tamoxifen on cardiovascular risk factors in postmenopausal women. Ann Intern Med 1991, 115:860-864.
73. Gottardis MM, Robinson SP, Satyaswaroop PG, Jordan VC Contrasting actions of tamoxifen on endometrial and breast tumor growth in the athymic mouse. Cancer Res 1988, 48:812-815.
74. Fornander T, Cedermark B, Mattsson A, Skoog L, Theve T, Askergren J, et al. Adjuvant tamoxifen in early breast-cancer - occurrence of new primary cancers. Lancet 1989, 1:117-120.
75. Fisher B, Costantino JP, Wickerham DL, Redmond CK, Kavanah M, Cronin WM, et al. Tamoxifen for prevention of breast cancer: report of the National Surgical Adjuvant Breast and Bowel Project P-l Study. J Nati Cancer Inst 1998, 90:1371-1388.
76. Smith CL, O'Malley BW Coregulator function: a key to understanding tissue specificity of selective receptor modulators. Endocr Rev 2004, 25:45-71.
77. Black LJ, Jones CD, Falcone JF Antagonism of estrogen action with a new benzothiophene derived antiestrogen. Life Sci 1983, 32:1031-1036.
78. Gottardis MM, Ricchio ME, Satyaswaroop PG, Jordan VC Effect of steroidal and nonsteroidal antiestrogens on the growth of a tamoxifen-stimulated human endometrial carcinoma (EnCalOl) in athymic mice. Cancer Res 1990, 50:3189-3192.
79. Lerner LJ, Jordan VC Development of antiestrogens and their use in breast cancer: eighth Cain memorial award lecture. Cancer Res 1990, 50:4177-4189.
80. Cummings SR, Eckert S, Krueger KA, Grady D, Powles TJ, Cauley JA, et al. The effect of raloxifene on risk of breast cancer in postmenopausal women: results from the MORE randomized trial. Multiple Outcomes of Raloxifene Evaluation. JAMA 1999, 281:2189-2197.
81. Cummings SR, Ensrud K, Delmas PD, LaCroix AZ, Vukicevic S, Reid DM, et al. Lasofoxifene in postmenopausal women with osteoporosis. N Engl J Med 2010, 362:686-696.
82. Vogel VG, Costantino JP, Wickerham DL, Cronin WM, Cecchini RS, Atkins JN, et al. Effects of tamoxifen vs raloxifene on the risk of developing invasive breast cancer and other disease outcomes: the NSABP Study of Tamoxifen and Raloxifene (STAR) P-2 trial. JAMA 2006, 295:2727-2741.
83. Vogel VG, Costantino JP, Wickerham DL, Cronin WM, Cecchini RS, Atkins JN, et al. Update of the National Surgical Adjuvant Breast and Bowel Project Study of Tamoxifen and Raloxifene (STAR) P-2 Trial: Preventing breast cancer. Cancer Prev Res (Phila) 2010, 3:696-706.
84. Fisher B, Costantino JP, Wickerham DL, Cecchini RS, Cronin WM, Robidoux A, et al. Tamoxifen for the prevention of breast cancer: current status of the National Surgical Adjuvant Breast and Bowel Project P-l study. J Nati Cancer Inst 2005, 97:1652-1662.
85. Powles TJ, Ashley S, Tidy A, Smith IE, Dowsett M Twenty-year follow-up of the Royal Marsden randomized, double-blinded tamoxifen breast cancer prevention trial. J. Nati Cancer Inst 2007, 99:283-290.
86. Jordan VC Chemosuppression of breast cancer with tamoxifen: laboratory evidence and future clinical investigations. Cancer Invest 1988, 6:589-595.
87. Gail MH, Brinton LA, Byar DP, Corle DK, Green SB, Schairer C, et al. Projecting individualized probabilities of developing breast cancer for white females who are being examined annually. J Nati Cancer Inst 1989, 81:1879-1886.
88. Jordan VC A century of deciphering the control mechanisms of sex steroid action in breast and prostate cancer: the origins of targeted therapy and chemoprevention. Cancer Res 2009, 69:1243-1254.