The biological role of estrogen receptors α and β in cancer

Critical Reviews in Oncology/Hematology

Volumn 50, Issue 1, 2004, Pages 3-22

  Pearce, Sandra Timm ^a   Jordan, V Craig ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Cancer; Coregulator; Estrogen receptor; Knockout mice

Indexed keywords

2,3 BIS(4 HYDROXYPHENYL)PROPIONITRILE; ANASTROZOLE; ANTIESTROGEN; AROMATASE INHIBITOR; CONTRACEPTIVE AGENT; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FULVESTRANT; LIGAND; MEDROXYPROGESTERONE ACETATE; PHYTOESTROGEN; PROPIONITRILE; PROPYLPYRAZOLE TRIOL; PYRAZOLE DERIVATIVE; RALOXIFENE; SELECTIVE ESTROGEN RECEPTOR MODULATOR; STEROID HORMONE; STEROID RECEPTOR; TAMOXIFEN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

BIOLOGICAL PHENOMENA AND FUNCTIONS CONCERNING THE ENTIRE ORGANISM; BONE DENSITY; BREAST CANCER; BREAST DEVELOPMENT; CANCER; CANCER RISK; CARDIOVASCULAR DISEASE; COLON CANCER; COLORECTAL CARCINOMA; CRYSTAL STRUCTURE; DRUG ACTIVITY; ENDOCRINE FUNCTION; ENDOMETRIUM CANCER; GENE; GENETIC TRANSCRIPTION; GENITAL SYSTEM; GROWTH; HORMONAL THERAPY; HORMONE RESPONSE; HORMONE SUBSTITUTION; HUMAN; IMMUNOHISTOCHEMISTRY; INTERPERSONAL COMMUNICATION; KNOCKOUT MOUSE; LIGAND BINDING; MUTATION; NONHUMAN; ORGANOGENESIS; OVARY CANCER; POSTMENOPAUSE; PROSTATE CANCER; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REPRODUCTION; REVIEW; SIDE EFFECT; TISSUE DISTRIBUTION; TISSUE SPECIFICITY; TRANSCRIPTION INITIATION; TUMOR;

ANIMALS; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FEMALE; HUMANS; LIGANDS; NEOPLASMS; TISSUE DISTRIBUTION; TRANSCRIPTION, GENETIC;

EID: 8344275588     PISSN: 10408428     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.critrevonc.2003.09.003     Document Type: Review

References (194)

1. Jordan V.C. Antiestrogens and selective estrogen receptor modulators as multifunctional medicines. 1. Receptor interactions. J Med Chem. 46:2003;883-908.
2. Jordan V.C. Antiestrogens and selective estrogen receptor modulators as multifunctional medicines. 2. Clinical considerations and new agents. J Med Chem. 46:2003;1081-1111.
3. Beatson G. On the treatment of inoperable cases of the carcinoma of the mamma: suggestions for a new method of treatment, with illustrative cases. The Lancet. 2:1896;104-107.
4. Boyd S. On oophorectomy in cancer of the breast. Br Med J. 2:1900;1161-1167.
5. Jensen E.V., Jacobson H.I. Basic guides to the mechanism of estrogen action. Recent Prog Hormone Res. 18:1962;387-414.
6. Jensen E.V., Block G.E., Smith S., Kyser K., DeSombre E.R. Estrogen receptors and breast cancer response to adrenalectomy. Natl Cancer Inst Monogr. 34:1971;55-70.
7. McGuire WL, Carbone PP, Vollmer EP. In: McGuire, WL, Carbone, PP, Sears, ME, Escher, GC, editors. Estrogen receptors in human breast cancer. New York: Raven Press; 1975. p. 1-7.
8. Knight W.A., Livingston R.B., Gregory E.J., McGuire W.L. Estrogen receptor as an independent prognostic factor for early recurrence in breast cancer. Cancer Res. 37:1977;4669-4671.
9. Jordan V.C., Gapstur S., Morrow M. Selective estrogen receptor modulation and reduction in risk of breast cancer, osteoporosis, and coronary heart disease. J Natl Cancer Inst. 93:2001;1449-1457.
10. Osborne C.K., Pippen J., Jones S.E.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. 20:2002;3386-3395.
11. Howell A., Robertson J.F., Quaresma Albano J.et al. 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. 20:2002;3396-3403.
12. 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 randomised trial, Lancet 2002;359:2131-9.
13. Bonneterre J., Thurlimann B., Robertson J.F.et al. Anastrozole versus tamoxifen as first-line therapy for advanced breast cancer in 668 postmenopausal women: results of the Tamoxifen or Arimidex Randomized Group Efficacy and Tolerability study. J Clin Oncol. 18:2000;3748-3757.
14. Nabholtz J.M., Buzdar A., Pollak M.et al. Anastrozole is superior to tamoxifen as first-line therapy for advanced breast cancer in postmenopausal women: results of a North American multicenter randomized trial. Arimidex Study Group. J Clin Oncol. 18:2000;3758-3767.
15. Mouridsen H., Gershanovich M., Sun Y.et al. Superior efficacy of letrozole versus tamoxifen as first-line therapy for postmenopausal women with advanced breast cancer: results of a phase III study of the International Letrozole Breast Cancer Group. J Clin Oncol. 19:2001;2596-2606.
16. Rossouw J.E., Anderson G.L., Prentice R.L.et al. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results From the Women's Health Initiative randomized controlled trial. JAMA. 288:2002;321-333.
17. Collaborative Group on Hormonal Factors in Breast Cancer. Breast cancer and hormone replacement therapy: collaborative reanalysis of data from 51 epidemiological studies of 52,705 women with breast cancer and 108,411 women without breast cancer. Lancet 1997;350:1047-59.
18. Walter P., Green S., Greene G.et al. Cloning of the human estrogen receptor cDNA. Proc Natl Acad Sci USA. 82:1985;7889-7893.
19. Greene G.L., Gilna P., Waterfield M., Baker A., Hort Y., Shine J. Sequence and expression of human estrogen receptor complementary DNA. Science. 231:1986;1150-1154.
20. Green S., Walter P., Kumar V.et al. Human oestrogen receptor cDNA: sequence. Nature. 320:1986;134-139.
21. Flouriot G., Brand H., Denger S. Identification of a new isoform of the human estrogen receptor-alpha (hER-alpha) that is encoded by distinct transcripts and that is able to repress hER-alpha activation function 1. EMBO J. 19:2000;4688-4700.
22. Murphy L.C., Dotzlaw H., Leygue E., Douglas D., Coutts A., Watson P.H. Estrogen receptor variants and mutations. J Steroid Biochem Mol Biol. 62:1997;363-372.
23. Poola I., Koduri S., Chatra S., Clarke R. Identification of twenty alternatively spliced estrogen receptor alpha mRNAs in breast cancer cell lines and tumors using splice targeted primer approach. J Steroid Biochem Mol Biol. 72:2000;249-258.
24. Kuiper G.G., Enmark E., Pelto-Huikko M., Nilsson S., Gustafsson J.A. Cloning of a novel receptor expressed in rat prostate and ovary. Proc Natl Acad Sci USA. 93:1996;5925-5930.
25. Tremblay G.B., Tremblay A., Copeland N.G.et al. Cloning, chromosomal localization, and functional analysis of the murine estrogen receptor beta. Mol Endocrinol. 11:1997;353-365.
26. Mosselman S., Polman J., Dijkema R. ER beta: identification and characterization of a novel human estrogen receptor. FEBS Lett. 392:1996;49-53.
27. Enmark E., Pelto-Huikko M., Grandien K.et al. Human estrogen receptor beta-gene structure, chromosomal localization, and expression pattern. J Clin Endocrinol Metab. 82:1997;4258-4265.
28. Ogawa S., Inoue S., Watanabe T.et al. The complete primary structure of human estrogen receptor beta (hER beta) and its heterodimerization with ER alpha in vivo and in vitro. Biochem Biophys Res Commun. 243:1998;122-126.
29. Lewandowski S., Kalita K., Kaczmarek L. Estrogen receptor beta. Potential functional significance of a variety of mRNA isoforms. FEBS Lett. 524:2002;1-5.
30. Nilsson S., Makela S., Treuter E.et al. Mechanisms of estrogen action. Physiol Rev. 81:2001;1535-1565.
31. Hall J.M., McDonnell D.P. The estrogen receptor beta-isoform (ERbeta) of the human estrogen receptor modulates ERalpha transcriptional activity and is a key regulator of the cellular response to estrogens and antiestrogens. Endocrinology. 140:1999;5566-5578.
32. Kuiper G.G., Carlsson B., Grandien K.et al. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta. Endocrinology. 138:1997;863-870.
33. Kuiper G.G., Lemmen J.G., Carlsson B.et al. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology. 139:1998;4252-4263.
34. Gustafsson J.A. Estrogen receptor beta - a new dimension in estrogen mechanism of action. J Endocrinol. 163:1999;379-383.
35. Taylor A.H., Al-Azzawi F. Immunolocalisation of oestrogen receptor beta in human tissues. J Mol Endocrinol. 24:2000;145-155.
36. Hiroi H., Inoue S., Watanabe T.et al. Differential immunolocalization of estrogen receptor alpha and beta in rat ovary and uterus. J Mol Endocrinol. 22:1999;37-44.
37. Sar M., Welsch F. Differential expression of estrogen receptor-beta and estrogen receptor-alpha in the rat ovary. Endocrinology. 140:1999;963-971.
38. Weihua Z., Warner M., Gustafsson J.A. Estrogen receptor beta in the prostate. Mol. Cell Endocrinol. 193:2002;1-5.
39. Kumar V., Green S., Stack G., Berry M., Jin J.R., Chambon P. Functional domains of the human estrogen receptor. Cell. 51:1987;941-951.
40. Tora L., White J., Brou C.et al. The human estrogen receptor has two independent nonacidic transcriptional activation functions. Cell. 59:1989;477-487.
41. Berry M., Metzger D., Chambon P. Role of the two activating domains of the oestrogen receptor in the cell-type and promoter-context dependent agonistic activity of the anti- oestrogen 4-hydroxytamoxifen. EMBO J. 9:1990;2811-2818.
42. Danielian P.S., White R., Lees J.A., Parker M.G. Identification of a conserved region required for hormone dependent transcriptional activation by steroid hormone receptors. EMBO J. 11:1992;1025-1033.
43. Tzukerman M.T., Esty A., Santiso-Mere D.et al. Human estrogen receptor transactivational capacity is determined by both cellular and promoter context and mediated by two functionally distinct intramolecular regions. Mol. Endocrinol. 8:1994;21-30.
44. Kraus W.L., McInerney E.M., Katzenellenbogen B.S. Ligand-dependent, transcriptionally productive association of the amino- and carboxyl-terminal regions of a steroid hormone nuclear receptor. Proc. Natl. Acad. Sci. USA. 92:1995;12314-12318.
45. Fawell S.E., White R., Hoare S., Sydenham M., Page M., Parker M.G. Inhibition of estrogen receptor-DNA binding by the "pure" antiestrogen ICI 164,384 appears to be mediated by impaired receptor dimerization. Proc. Natl. Acad. Sci. USA. 87:1990;6883-6887.
46. Dauvois S., Danielian P.S., White R., Parker M.G. Antiestrogen ICI 164,384 reduces cellular estrogen receptor content by increasing its turnover. Proc. Natl. Acad. Sci. USA. 89:1992;4037-4041.
47. McKenna N.J., Lanz R.B., O'Malley B.W. Nuclear receptor coregulators: cellular and molecular biology. Endocr. Rev. 20:1999;321-344.
48. Klinge C.M. Estrogen receptor interaction with co-activators and co-repressors. Steroids. 65:2000;227-251.
49. Tremblay G.B., Giguere V. Coregulators of estrogen receptor action. Crit. Rev. Eukaryot. Gene Exp. 12:2002;1-22.
50. Heery D.M., Kalkhoven E., Hoare S., Parker M.G. A signature motif in transcriptional co-activators mediates binding to nuclear receptors. Nature. 387:1997;733-736.
51. Montano M.M., Ekena K., Delage-Mourroux R., Chang W., Martini P., Katzenellenbogen B.S. An estrogen receptor-selective coregulator that potentiates the effectiveness of antiestrogens and represses the activity of estrogens. Proc. Natl. Acad. Sci. USA. 96:1999;6947-6952.
52. Katzenellenbogen B.S., Montano M.M., Ediger T.R.et al. Estrogen receptors: selective ligands, partners, and distinctive pharmacology. Recent Prog. Horm. Res. 55:2000;163-193.
53. Endoh H., Maruyama K., Masuhiro Y.et al. Purification and identification of p68 RNA helicase acting as a transcriptional coactivator specific for the activation function 1 of human estrogen receptor alpha. Mol. Cell Biol. 19:1999;5363-5372.
54. Suen C.S., Berrodin T.J., Mastroeni R., Cheskis B.J., Lyttle C.R., Frail D.E. A transcriptional coactivator, steroid receptor coactivator-3, selectively augments steroid receptor transcriptional activity. J. Biol. Chem. 273:1998;27645-27653.
55. Watanabe T., Inoue S., Ogawa S.et al. Agonistic effect of tamoxifen is dependent on cell type, ERE-promoter context, and estrogen receptor subtype: functional difference between estrogen receptors alpha and beta. Biochem. Biophys. Res. Commun. 236:1997;140-145.
56. McInerney E.M., Weis K.E., Sun J., Mosselman S., Katzenellenbogen B.S. Transcription activation by the human estrogen receptor subtype beta (ER beta) studied with ER beta and ER alpha receptor chimeras. Endocrinology. 139:1998;4513-4522.
57. Adlercreutz H. Phyto-oestrogens and cancer. Lancet Oncol. 3:2002;364-373.
58. Mishra S.I., Dickerson V., Najm W. Phytoestrogens and breast cancer prevention: what is the evidence? Am. J. Obstet. Gynecol. 188:2002;S66-S70.
59. Adlercreutz H., Mazur W. Phyto-oestrogens and Western diseases. Ann Med. 29:1997;95-120.
60. Shiau A.K., Barstad D., Radek J.T.et al. Structural characterization of a subtype-selective ligand reveals a novel mode of estrogen receptor antagonism. Nat. Struct. Biol. 9:2002;359-364.
61. Sun J., Huang Y.R., Harrington W.R., Sheng S., Katzenellenbogen J.A., Katzenellenbogen B.S. Antagonists selective for estrogen receptor alpha. Endocrinology. 143:2002;941-947.
62. Brzozowski A.M., Pike A.C., Dauter Z.et al. Molecular basis of agonism and antagonism in the oestrogen receptor. Nature. 389:1997;753-758.
63. Pike A.C., Brzozowski A.M., Hubbard R.E. A structural biologist's view of the oestrogen receptor. J. Steroid Biochem. Mol. Biol. 74:2000;261-268.
64. Jordan V.C., Collins M.M., Rowsby L., Prestwich G. A monohydroxylated metabolite of tamoxifen with potent antioestrogenic activity. J. Endocrinol. 75:1977;305-316.
65. Shiau A.K., Barstad D., Loria P.M.et al. The structural basis of estrogen receptor/coactivator recognition and the antagonism of this interaction by tamoxifen. Cell. 95:1998;927-937.
66. Pike A.C., Brzozowski A.M., Hubbard R.E.et al. Structure of the ligand-binding domain of oestrogen receptor beta in the presence of a partial agonist and a full antagonist. EMBO J. 18:1999;4608-4618.
67. Pike A.C., Brzozowski A.M., Walton J.et al. Structural insights into the mode of action of a pure antiestrogen. Structure (Camb). 9:2001;145-153.
68. van Hoorn W.P. Identification of a second binding site in the estrogen receptor. J. Med. Chem. 45:2002;584-589.
69. Zhang Z., Maier B., Santen R.J., Song R.X. Membrane association of estrogen receptor alpha mediates estrogen effect on MAPK activation. Biochem. Biophys. Res. Commun. 294:2002;926-933.
70. Levin E.R. Cellular functions of plasma membrane estrogen receptors. Steroids. 67:2002;471-475.
71. Santen R.J., Song R.X., McPherson R.et al. The role of mitogen-activated protein (MAP) kinase in breast cancer. J. Steroid. Biochem. Mol. Biol. 80:2002;239-256.
72. Razandi M., Pedram A., Greene G.L., Levin E.R. Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript: studies of ERalpha and ERbeta expressed in Chinese hamster ovary cells. Mol Endocrinol. 13:1999;307-319.
73. Lannigan D.A. Estrogen receptor phosphorylation. Steroids. 68:2003;1-9.
74. Kato S. Estrogen receptor-mediated cross-talk with growth factor signaling pathways. Breast Cancer. 8:2001;3-9.
75. Denton R.R., Koszewski N.J., Notides A.C. Estrogen receptor phosphorylation. Hormonal dependence and consequence on specific DNA binding. J. Biol. Chem. 267:1992;7263-7268.
76. Le Goff P., Montano M.M., Schodin D.J., Katzenellenbogen B.S. Phosphorylation of the human estrogen receptor. Identification of hormone-regulated sites and examination of their influence on transcriptional activity. J. Biol. Chem. 269:1994;4458-4466.
77. Ali S., Metzger D., Bornert J.M., Chambon P. Modulation of transcriptional activation by ligand-dependent phosphorylation of the human oestrogen receptor A/B region. EMBO J. 12:1993;1153-1160.
78. Joel P.B., Traish A.M., Lannigan D.A. Estradiol and phorbol ester cause phosphorylation of serine 118 in the human estrogen receptor. Mol. Endocrinol. 9:1995;1041-1052.
79. Bunone G., Briand P.A., Miksicek R.J., Picard D. Activation of the unliganded estrogen receptor by EGF involves the MAP kinase pathway and direct phosphorylation. EMBO J. 15:1996;2174-2183.
80. Kato S., Endoh H., Masuhiro Y.et al. Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science. 270:1995;1491-1494.
81. Joel P.B., Traish A.M., Lannigan D.A. Estradiol-induced phosphorylation of serine 118 in the estrogen receptor is independent of p42/p44 mitogen-activated protein kinase. J. Biol. Chem. 273:1998;13317-13323.
82. Chen D., Washbrook E., Sarwar N.et al. Phosphorylation of human estrogen receptor alpha at serine 118 by two distinct signal transduction pathways revealed by phosphorylation-specific antisera. Oncogene. 21:2002;4921-4931.
83. Arnold S.F., Obourn J.D., Jaffe H., Notides A.C. Serine 167 is the major estradiol-induced phosphorylation site on the human estrogen receptor. Mol. Endocrinol. 8:1994;1208-1214.
84. Joel P.B., Smith J., Sturgill T.W., Fisher T.L., Blenis J., Lannigan D.A. pp90rsk1 regulates estrogen receptor-mediated transcription through phosphorylation of Ser-167. Mol. Cell Biol. 18:1998;1978-1984.
85. Simoncini T., Hafezi-Moghadam A., Brazil D.P., Ley K., Chin W.W., Liao J.K. Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature. 407:2000;538-541.
86. Sun M., Paciga J.E., Feldman R.I.et al. Phosphatidylinositol-3-OH Kinase (PI3K)/AKT2, activated in breast cancer, regulates and is induced by estrogen receptor alpha (ERalpha) via interaction between ERalpha and PI3K. Cancer Res. 61:2001;5985-5991.
87. Campbell R.A., Bhat-Nakshatri P., Patel N.M., Constantinidou D., Ali S., Nakshatri H. Phosphatidylinositol 3-kinase/AKT-mediated activation of estrogen receptor alpha: a new model for anti-estrogen resistance. J. Biol. Chem. 276:2001;9817-9824.
88. Rogatsky I., Trowbridge J.M., Garabedian M.J. Potentiation of human estrogen receptor alpha transcriptional activation through phosphorylation of serines 104 and 106 by the cyclin A-CDK2 complex. J. Biol. Chem. 274:1999;22296-22302.
89. Chen D., Pace P.E., Coombes R.C., Ali S. Phosphorylation of human estrogen receptor alpha by protein kinase A regulates dimerization. Mol. Cell Biol. 19:1999;1002-1015.
90. Arnold S.F., Obourn J.D., Jaffe H., Notides A.C. Phosphorylation of the human estrogen receptor on tyrosine 537 in vivo and by src family tyrosine kinases in vitro. Mol. Endocrinol. 9:1995;24-33.
91. Tremblay A., Tremblay G.B., Labrie F., Giguere V. Ligand-independent recruitment of SRC-1 to estrogen receptor beta through phosphorylation of activation function AF-1. Mol. Cell. 3:1999;513-519.
92. Gee J.M., Robertson J.F., Ellis I.O., Nicholson R.I. Phosphorylation of ERK1/2 mitogen-activated protein kinase is associated with poor response to anti-hormonal therapy and decreased patient survival in clinical breast cancer. Int J Cancer. 95:2001;247-254.
93. Kushner P.J., Agard D.A., Greene G.L.et al. Estrogen receptor pathways to AP-1. J. Steroid Biochem. Mol. Biol. 74:2000;311-317.
94. Paech K., Webb P., Kuiper G.G.et al. Differential ligand activation of estrogen receptors ERalpha and ERbeta at AP1 sites. Science. 277:1997;1508-1510.
95. Webb P., Lopez G.N., Uht R.M., Kushner P.J. Tamoxifen activation of the estrogen receptor/AP-1 pathway: potential origin for the cell-specific estrogen-like effects of antiestrogens. Mol. Endocrinol. 9:1995;443-456.
96. Webb P., Nguyen P., Valentine C.et al. The estrogen receptor enhances AP-1 activity by two distinct mechanisms with different requirements for receptor transactivation functions. Mol. Endocrinol. 13:1999;1672-1685.
97. Weatherman R.V., Scanlan T.S. Unique protein determinants of the subtype-selective ligand responses of the estrogen receptors (ERalpha and ERbeta ) at AP-1 sites. J. Biol. Chem. 276:2001;3827-3832.
98. Safe S. Transcriptional activation of genes by 17 beta-estradiol through estrogen receptor-Sp1 interactions. Vitam. Horm. 62:2001;231-252.
99. Saville B., Wormke M., Wang F.et al. Ligand-, cell-, and estrogen receptor subtype (alpha/beta)-dependent activation at GC-rich (Sp1) promoter elements. J. Biol. Chem. 275:2000;5379-5387.
100. Cowley S.M., Hoare S., Mosselman S., Parker M.G. Estrogen receptors alpha and beta form heterodimers on DNA. J. Biol. Chem. 272:1997;19858-19862.
101. Pettersson K., Grandien K., Kuiper G.G., Gustafsson J.A. Mouse estrogen receptor beta forms estrogen response element-binding heterodimers with estrogen receptor alpha. Mol. Endocrinol. 11:1997;1486-1496.
102. Curtis Hewitt S., Couse J.F., Korach K.S. Estrogen receptor transcription and transactivation: Estrogen receptor knockout mice: what their phenotypes reveal about mechanisms of estrogen action. Breast Cancer Res. 2:2000;345-352.
103. Couse J.F., Curtis Hewitt S., Korach K.S. Receptor null mice reveal contrasting roles for estrogen receptor alpha and beta in reproductive tissues. J. Steroid Biochem. Mol. Biol. 74:2000;287-296.
104. Curtis S.H., Korach K.S. Steroid receptor knockout models: phenotypes and responses illustrate interactions between receptor signaling pathways in vivo. Adv. Pharmacol. 47:2000;357-380.
105. Couse J.F., Korach K.S. Estrogen receptor null mice: what have we learned and where will they lead us? Endocr. Rev. 20:1999;358-417.
106. Lubahn D.B., Moyer J.S., Golding T.S., Couse J.F., Korach K.S., Smithies O. Alteration of reproductive function but not prenatal sexual development after insertional disruption of the mouse estrogen receptor gene. Proc. Natl. Acad. Sci. USA. 90:1993;11162-11166.
107. Bocchinfuso W.P., Korach K.S. Mammary gland development and tumorigenesis in estrogen receptor knockout mice. J. Mammary Gland Biol. Neoplasia. 2:1997;323-334.
108. Day J.K., Besch-Williford C., McMann T.R., Hufford M.G., Lubahn D.B., MacDonald R.S. Dietary genistein increased DMBA-induced mammary adenocarcinoma in wild-type, but not ER alpha KO, mice. Nutr. Cancer. 39:2001;226-232.
109. Eddy E.M., Washburn T.F., Bunch D.O.et al. Targeted disruption of the estrogen receptor gene in male mice causes alteration of spermatogenesis and infertility. Endocrinology. 137:1996;4796-4805.
110. Ogawa S., Lubahn D.B., Korach K.S., Pfaff D.W. Behavioral effects of estrogen receptor gene disruption in male mice. Proc. Natl. Acad. Sci. USA. 94:1997;1476-1481.
111. Krege J.H., Hodgin J.B., Couse J.F.et al. Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc. Natl. Acad. Sci. USA. 95:1998;15677-15682.
112. Ogawa S., Chan J., Chester A.E., Gustafsson J.A., Korach K.S., Pfaff D.W. Survival of reproductive behaviors in estrogen receptor beta gene-deficient (betaERKO) male and female mice. Proc. Natl. Acad. Sci. USA. 96:1999;12887-12892.
113. Dupont S., Krust A., Gansmuller A., Dierich A., Chambon P., Mark M. Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development. 127:2000;4277-4291.
114. Wang L., Andersson S., Warner M., Gustafsson J.A. Morphological abnormalities in the brains of estrogen receptor beta knockout mice. Proc. Natl. Acad. Sci. USA. 98:2001;2792-2796.
115. Couse J.F., Hewitt S.C., Bunch D.O.et al. Postnatal sex reversal of the ovaries in mice lacking estrogen receptors alpha and beta. Science. 286:1999;2328-2331.
116. Ogawa S., Chester A.E., Hewitt S.C.et al. From the cover: abolition of male sexual behaviors in mice lacking estrogen receptors alpha and beta (alpha beta ERKO). Proc. Natl. Acad. Sci. USA. 97:2000;14737-14741.
117. Iafrati M.D., Karas R.H., Aronovitz M.et al. Estrogen inhibits the vascular injury response in estrogen receptor alpha-deficient mice. Nat. Med. 3:1997;545-548.
118. Karas R.H., Hodgin J.B., Kwoun M.et al. Estrogen inhibits the vascular injury response in estrogen receptor beta-deficient female mice. Proc. Natl. Acad. Sci. USA. 96:1999;15133-15136.
119. Karas R.H., Schulten H., Pare G.et al. Effects of estrogen on the vascular injury response in estrogen receptor alpha, beta (double) knockout mice. Circ. Res. 89:2001;534-539.
120. Couse J.F., Curtis S.W., Washburn T.F.et al. Analysis of transcription and estrogen insensitivity in the female mouse after targeted disruption of the estrogen receptor gene. Mol. Endocrinol. 9:1995;1441-1454.
121. Mendelsohn M.E. Protective effects of estrogen on the cardiovascular system. Am. J. Cardiol. 89:2002;12E-17E. discussion 17E-18E.
122. Rubanyi G.M., Freay A.D., Kauser K.et al. Vascular estrogen receptors and endothelium-derived nitric oxide production in the mouse aorta. Gender difference and effect of estrogen receptor gene disruption. J. Clin. Invest. 99:1997;2429-2437.
123. Johnson B.D., Zheng W., Korach K.S., Scheuer T., Catterall W.A., Rubanyi G.M. Increased expression of the cardiac L-type calcium channel in estrogen receptor-deficient mice. J. Gen. Physiol. 110:1997;135-140.
124. Smith E.P., Boyd J., Frank G.R.et al. Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. N. Engl. J. Med. 331:1994;1056-1061.
125. Sudhir K., Chou T.M., Chatterjee K.et al. Premature coronary artery disease associated with a disruptive mutation in the estrogen receptor gene in a man. Circulation. 96:1997;3774-3777.
126. Sudhir K., Chou T.M., Messina L.M.et al. Endothelial dysfunction in a man with disruptive mutation in oestrogen-receptor gene. Lancet. 349:1997;1146-1147.
127. Jensen EV, Jordan VC. The estrogen receptor: a model for molecular medicine. The Dorothy P. Landon AACR Prize for Translational Research. Clin Cancer Res 2003, in press.
128. Horwitz K.B. The central role of progesterone receptors and progestational agents in the management and treatment of breast cancer. Semin Oncol. 15:1988;14-19.
129. Clark G.M., McGuire W.L. Steroid receptors and other prognostic factors in primary breast cancer. Semin Oncol. 15:1988;20-25.
130. Early Breast Cancer Trialists' Collaborative Group. Tamoxifen for early breast cancer: an overview of the randomised trials. Lancet 1998;351:1451-67.
131. Fisher B., Costantino J.P., Wickerham D.L.et al. Tamoxifen for prevention of breast cancer: report of the National Surgical Adjuvant Breast and Bowel Project P-1 Study. J. Natl. Cancer Inst. 90:1998;1371-1388.
132. Jordan V.C. Selective estrogen receptor modulation: a personal perspective. Cancer Res. 61:2001;5683-5687.
133. Powles T.J., Hickish T., Kanis J.A., Tidy A., Ashley S. Effect of tamoxifen on bone mineral density measured by dual-energy X-ray absorptiometry in healthy premenopausal and postmenopausal women. J. Clin. Oncol. 14:1996;78-84.
134. Shang Y., Brown M. Molecular determinants for the tissue specificity of SERMs. Science. 295:2002;2465-2468.
135. Berns E.M., van Staveren I.L., Klijn J.G., Foekens J.A. Predictive value of SRC-1 for tamoxifen response of recurrent breast cancer. Breast Cancer Res. Treat. 48:1998;87-92.
136. Anzick S.L., Kononen J., Walker R.L.et al. AIB1, a steroid receptor coactivator amplified in breast and ovarian cancer. Science. 277:1997;965-968.
137. List H.J., Reiter R., Singh B., Wellstein A., Riegel A.T. Expression of the nuclear coactivator AIB1 in normal and malignant breast tissue. Breast Cancer Res. Treat. 68:2001;21-28.
138. Osborne C.K., Bardou V., Hopp T.A.et al. Role of the estrogen receptor coactivator AIB1 (SRC-3) and HER-2/neu in tamoxifen resistance in breast cancer. J. Natl. Cancer Inst. 95:2003;353-361.
139. Clarke R., Skaar T.C., Bouker K.B.et al. Molecular and pharmacological aspects of antiestrogen resistance. J. Steroid Biochem. Mol. Biol. 76:2001;71-84.
140. Clarke R., Leonessa F., Welch J.N., Skaar T.C. Cellular and molecular pharmacology of antiestrogen action and resistance. Pharmacol. Rev. 53:2001;25-71.
141. Ali S., Coombes R.C. Endocrine-responsive breast cancer and strategies for combating resistance. Nat. Rev. Cancer. 2:2002;101-115.
142. Schiff R., Massarweh S., Shou J., Osborne C.K. Breast cancer endocrine resistance: how growth factor signaling and estrogen receptor coregulators modulate response. Clin Cancer Res. 9:2003;447S-454S.
143. Johnston S.R.D., Saccanti-Jotti G., Smith I.E., Newby J., Dowsett M. Change in estrogen receptor expression and function in tamoxifen-resistant breast cancer. Endocr. Relat. Cancer. 2:1995;105-110.
144. Vignon F., Lippman M.E., Nawata H., Derocq D., Rochefort H. Induction of two estrogen-responsive proteins by antiestrogens in R27, a tamoxifen-resistant clone of MCF7 cells. Cancer Res. 44:1984;2084-2088.
145. Westley J., Steiner D.F., Westley B. Effects of antiestrogens on the estrogen-regulated pS2 RNA and the 52- and 160-kilodalton proteins in MCF7 cells and two tamoxifen-resistant sublines. J Biol Chem. 259:1984;6641-6649.
146. MacGregor J.I., Jordan V.C. Basic guide to the mechanisms of antiestrogen action. Pharmacol. Rev. 50:1998;151-196.
147. Fuqua S.A., Wiltschke C., Zhang Q.X.et al. A hypersensitive estrogen receptor-alpha mutation in premalignant breast lesions. Cancer Res. 60:2000;4026-4029.
148. Zhang Q.X., Borg A., Wolf D.M., Oesterreich S., Fuqua S.A. An estrogen receptor mutant with strong hormone-independent activity from a metastatic breast cancer. Cancer Res. 57:1997;1244-1249.
149. Wolf D.M., Jordan V.C. The estrogen receptor from a tamoxifen stimulated MCF-7 tumor variant contains a point mutation in the ligand binding domain. Breast Cancer Res. Treat. 31:1994;129-138.
150. Levenson A.S., Tonetti D.A., Jordan V.C. The oestrogen-like effect of 4-hydroxytamoxifen on induction of transforming growth factor alpha mRNA in MDA-MB-231 breast cancer cells stably expressing the oestrogen receptor. Br. J. Cancer. 77:1998;1812-1819.
151. Liu H., Lee E.S., de los Reyes A., Zapf J.W., Jordan V.C. Silencing and reactivation of the selective estrogen receptor modulator-estrogen receptor alpha complex. Cancer Res. 61:2001;3632-3639.
152. Bilimoria M.M., Assikis V.J., Muenzner H.D., Wolf D.M., Satyaswaroop P.G., Jordan V.C. An analysis of tamoxifen-stimulated human carcinomas for mutations in the AF-2 region of the estrogen receptor. J. Steroid Biochem. Mol. Biol. 58:1996;479-488.
153. Herman M.E., Katzenellenbogen B.S. Response-specific antiestrogen resistance in a newly characterized MCF-7 human breast cancer cell line resulting from long-term exposure to trans-hydroxytamoxifen. J Steroid Biochem Mol Biol. 59:1996;121-134.
154. Mullick A., Chambon P. Characterization of the estrogen receptor in two antiestrogen-resistant cell lines, LY2 and T47D. Cancer Res. 50:1990;333-338.
155. Karnik P.S., Kulkarni S., Liu X.P., Budd G.T., Bukowski R.M. Estrogen receptor mutations in tamoxifen-resistant breast cancer. Cancer Res. 54:1994;349-353.
156. Jiang S.Y., Wolf D.M., Yingling J.M., Chang C., Jordan V.C. An estrogen receptor positive MCF-7 clone that is resistant to antiestrogens and estradiol. Mol. Cell Endocrinol. 90:1992;77-86.
157. Liu H., Park W.C., Bentrem D.J.et al. Structure-function relationships of the raloxifene-estrogen receptor-alpha complex for regulating transforming growth factor-alpha expression in breast cancer cells. J. Biol. Chem. 277:2002;9189-9198.
158. Speirs V., Malone C., Walton D.S., Kerin M.J., Atkin S.L. Increased expression of estrogen receptor beta mRNA in tamoxifen-resistant breast cancer patients. Cancer Res. 59:1999;5421-5424.
159. Yamamoto Y., Wada O., Suzawa M.et al. The tamoxifen-responsive estrogen receptor alpha mutant D351Y shows reduced tamoxifen-dependent interaction with corepressor complexes. J. Biol. Chem. 276:2001;42684-42691.
160. Dumont J.A., Bitonti A.J., Wallace C.D., Baumann R.J., Cashman E.A., Cross-Doersen D.E. Progression of MCF-7 breast cancer cells to antiestrogen-resistant phenotype is accompanied by elevated levels of AP-1 DNA-binding activity. Cell Growth Differ. 7:1996;351-359.
161. Johnston S.R., Lu B., Scott G.K.et al. Increased activator protein-1 DNA binding and c-Jun NH2-terminal kinase activity in human breast tumors with acquired tamoxifen resistance. Clin. Cancer Res. 5:1999;251-256.
162. Smith L.M., Wise S.C., Hendricks D.T.et al. cJun overexpression in MCF-7 breast cancer cells produces a tumorigenic. Oncogene. 18:1999;6063-6070.
163. Schiff R., Reddy P., Ahotupa M.et al. Oxidative stress and AP-1 activity in tamoxifen-resistant breast tumors in vivo. J. Natl. Cancer Inst. 92:2000;1926-1934.
164. Chung Y.L., Sheu M.L., Yang S.C., Lin C.H., Yen S.H. Resistance to tamoxifen-induced apoptosis is associated with direct interaction between Her2/neu and cell membrane estrogen receptor in breast cancer. Int. J. Cancer. 97:2002;306-312.
165. Kurokawa H., Lenferink A.E., Simpson J.F.et al. Inhibition of HER2/neu (erbB-2) and mitogen-activated protein kinases enhances tamoxifen action against HER2-overexpressing, tamoxifen-resistant breast cancer cells. Cancer Res. 60:2000;5887-5894.
166. Pietras R.J., Arboleda J., Reese D.M.et al. HER-2 tyrosine kinase pathway targets estrogen receptor and promotes hormone-independent growth in human breast cancer cells. Oncogene. 10:1995;2435-2446.
167. Parisot J.P., Hu X.F., DeLuise M., Zalcberg J.R. Altered expression of the IGF-1 receptor in a tamoxifen-resistant human breast cancer cell line. Br. J. Cancer. 79:1999;693-700.
168. Rabenoelina F., Semlali A., Duchesne M.J., Freiss G., Pons M., Badia E. Effect of prolonged hydroxytamoxifen treatment of MCF-7 cells on mitogen activated kinase cascade. Int. J. Cancer. 98:2002;698-706.
169. Palmieri C., Cheng G.J., Saji S.et al. Estrogen receptor beta in breast cancer. Endocr. Relat. Cancer. 9:2002;1-13.
170. Gustafsson J.A., Warner M. Estrogen receptor beta in the breast: role in estrogen responsiveness and development of breast cancer. J. Steroid Biochem. Mol. Biol. 74:2000;245-248.
171. Mann S., Laucirica R., Carlson N.et al. Estrogen receptor beta expression in invasive breast cancer. Hum. Pathol. 32:2001;113-118.
172. Jarvinen T.A., Pelto-Huikko M., Holli K., Isola J. Estrogen receptor beta is coexpressed with ERalpha and PR and associated with nodal status, grade, and proliferation rate in breast cancer. Am. J. Pathol. 156:2000;29-35.
173. Omoto Y., Inoue S., Ogawa S.et al. Clinical value of the wild-type estrogen receptor beta expression in breast cancer. Cancer Lett. 163:2001;207-212.
174. Roger P., Sahla M.E., Makela S., Gustafsson J.A., Baldet P., Rochefort H. Decreased expression of estrogen receptor beta protein in proliferative preinvasive mammary tumors. Cancer Res. 61:2001;2537-2541.
175. Speirs V., Parkes A.T., Kerin M.J.et al. Coexpression of estrogen receptor alpha and beta: poor prognostic factors in human breast cancer? Cancer Res. 59:1999;525-528.
176. Leygue E., Dotzlaw H., Watson P.H., Murphy L.C. Altered estrogen receptor alpha and beta messenger RNA expression during human breast tumorigenesis. Cancer Res. 58:1998;3197-3201.
177. Chang W.Y., Prins G.S. Estrogen receptor-beta: implications for the prostate gland. Prostate. 40:1999;115-124.
178. Fiorelli G., Picariello L., Martineti V., Tonelli F., Brandi M.L. Functional estrogen receptor beta in colon cancer cells. Biochem. Biophys. Res. Commun. 261:1999;521-527.
179. Arai N., Strom A., Rafter J.J., Gustafsson J.A. Estrogen receptor beta mRNA in colon cancer cells: growth effects of estrogen and genistein. Biochem. Biophys. Res. Commun. 270:2000;425-431.
180. Qiu Y., Waters C.E., Lewis A.E., Langman M.J., Eggo M.C. Oestrogen-induced apoptosis in colonocytes expressing oestrogen receptor beta. J. Endocrinol. 174:2002;369-377.
181. Foley E.F., Jazaeri A.A., Shupnik M.A., Jazaeri O., Rice L.W. Selective loss of estrogen receptor beta in malignant human colon. Cancer Res. 60:2000;245-248.
182. Witte D., Chirala M., Younes A., Li Y., Younes M. Estrogen receptor beta is expressed in human colorectal adenocarcinoma. Hum. Pathol. 32:2001;940-944.
183. Hulley S., Furberg C., Barrett-Connor E.et al. Noncardiovascular disease outcomes during 6.8 years of hormone therapy: Heart and Estrogen/progestin Replacement Study follow-up (HERS II). Jama. 288:2002;58-66.
184. Grodstein F., Newcomb P.A., Stampfer M.J. Postmenopausal hormone therapy and the risk of colorectal cancer: a review and meta-analysis. Am. J. Med. 106:1999;574-582.
185. Campbell-Thompson M., Lynch I.J., Bhardwaj B. Expression of estrogen receptor (ER) subtypes and ERbeta isoforms in colon cancer. Cancer Res. 61:2001;632-640.
186. Makar A.P. Hormone therapy in epithelial ovarian cancer. Endocr. Relat. Cancer. 7:2000;85-93.
187. Hankinson S.E., Colditz G.A., Hunter D.J., Spencer T.L., Rosner B., Stampfer M.J. A quantitative assessment of oral contraceptive use and risk of ovarian cancer. Obstet. Gynecol. 80:1992;708-714.
188. Pujol P., Rey J.M., Nirde P.et al. Differential expression of estrogen receptor-alpha and -beta messenger RNAs as a potential marker of ovarian carcinogenesis. Cancer Res. 58:1998;5367-5373.
189. Rutherford T., Brown W.D., Sapi E., Aschkenazi S., Munoz A., Mor G. Absence of estrogen receptor-beta expression in metastatic ovarian cancer. Obstet. Gynecol. 96:2000;417-421.
190. Sakaguchi H., Fujimoto J., Aoki I., Toyoki H., Khatun S., Tamaya T. Expression of oestrogen receptor alpha and beta in uterine endometrial and ovarian cancers. Eur. J. Cancer. 38(Suppl 6):2002;S74-S75.
191. Lau K.M., Mok S.C., Ho S.M. Expression of human estrogen receptor-alpha and -beta, progesterone receptor, and androgen receptor mRNA in normal and malignant ovarian epithelial cells. Proc. Natl. Acad. Sci. USA. 96:1999;5722-5727.
192. Lazennec G., Bresson D., Lucas A., Chauveau C., Vignon F. ER beta inhibits proliferation and invasion of breast cancer cells. Endocrinology. 142:2001;4120-4130.
193. Meyers M.J., Sun J., Carlson K.E., Marriner G.A., Katzenellenbogen B.S., Katzenellenbogen J.A. Estrogen receptor-beta potency-selective ligands: structure-activity relationship studies of diarylpropionitriles and their acetylene and polar analogues. J. Med. Chem. 44:2001;4230-4251.
194. Harris H.A., Katzenellenbogen J.A., Katzenellenbogen B.S. Characterization of the biological roles of the estrogen receptors, ERalpha and ERbeta, in estrogen target tissues in vivo through the use of an ERalpha-selective ligand. Endocrinology. 143:2002;4172-4177.