Oestrogen-receptor-mediated transcription and the influence of co-factors and chromatin state

Nature Reviews Cancer

Volumn 7, Issue 9, 2007, Pages 713-722

  Green, Kelly A ^a   Carroll, Jason S ^a  

^a CANCER RESEARCH UK CAMBRIDGE RESEARCH INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATASE INHIBITOR; CYCLIN D1; ESTROGEN RECEPTOR ALPHA; HEPATOCYTE NUCLEAR FACTOR 3ALPHA; TAMOXIFEN; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR GATA 4;

ACETYLATION; BREAST CANCER; BREAST CARCINOGENESIS; CHROMATIN CONDENSATION; CHROMATIN STRUCTURE; CODON; ENZYME ACTIVITY; GENETIC TRANSCRIPTION; HUMAN; IN VITRO STUDY; METHYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; TRANSCRIPTION REGULATION;

AMINO ACID SEQUENCE; CARRIER PROTEINS; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; ESTROGEN RECEPTOR ALPHA; HUMANS; MODELS, BIOLOGICAL; NUCLEAR PROTEINS; P300-CBP TRANSCRIPTION FACTORS; REPRESSOR PROTEINS; TAMOXIFEN; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEINS;

EID: 34548248572     PISSN: 1474175X     EISSN: 14741768     Source Type: Journal    
DOI: 10.1038/nrc2211     Document Type: Review

References (178)

1. Krege, J.H. et al. Generation and reproductive phenotypes of mice lacking estrogen receptor β. Proc. Natl Acad. Sci. USA 95, 15677-15682 (1998).
2. Weihua, Z. et al. Estrogen receptor (ER) β, a modulator of ERα in the uterus. Proc. Natl Acad. Sci. USA 97, 5936-5941 (2000).
3. Saji, S. et al. Estrogen receptors α and β in the rodent mammary gland. Proc. Natl Acad. Sci. USA 97, 337-342 (2000).
4. Andersen, J. & Poulsen, H. S. Immunohistochemical estrogen receptor determination in paraffin-embedded tissue. Prediction of response to hormonal treatment in advanced breast cancer. Cancer 64, 1901-1908 (1989).
5. Stierer, M. et al. Immunohistochemical and biochemical measurement of estrogen and progesterone receptors in primary breast cancer. Correlation of histopathology and prognostic factors. Ann. Surg. 218, 13-21 (1993).
6. Perou, C.M. et al. Molecular portraits of human breast tumours. Nature 406, 747-752 (2000).
7. Sorlie, T. et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl Acad. Sci. USA 98, 10869-10874 (2001).
8. van 't Veer, L. J. et al. Gene expression profiling predicts clinical outcome of breast cancer. Nature 415, 530-536 (2002).
9. Sorlie, T. et al. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc. Natl Acad. Sci. USA 100, 8418-8423 (2003).
10. Howell, A. & Dowsett, M. Endocrinology and hormone therapy in breast cancer: aromatase inhibitors versus antioestrogens. Breast Cancer Res. 6, 269-274 (2004).
11. Fisher, B. 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, 1371-1388 (1998).
12. Fisher, B. et al. Tamoxifen for the prevention of breast cancer: current status of the National Surgical Adjuvant Breast and Bowel Project P-1 study. J. Natl Cancer Inst. 97, 1652-1662 (2005).
13. Jordan, V. C. Tamoxifen: a most unlikely pioneering medicine. Nature Rev. Drug Discov, 2, 205-213 (2003).
14. Howell, A., DeFriend, D., Robertson, J., Blamey, R. & Walton, P. Response to a specific antioestrogen (ICI 182780) in tamoxifen-resistant breast cancer. Lancet 345, 29-30 (1995).
15. Clarke, R., Leonessa, F., Welch, J. N. & Skaar, T. C. Cellular and molecular pharmacology of antiestrogen action and resistance. Pharmacol. Rev. 53, 25-71 (2001).
16. Fisher, B., Dignam, J., Bryant, J. & Wolmark, N. Five versus more than five years of tamoxifen for lymph node-negative breast cancer: updated findings from the National Surgical Adjuvant Breast and Bowel Project B-14 randomized trial. J. Natl Cancer Inst. 93, 684-690 (2001).
17. Johnston, S. R. Acquired tamoxifen resistance in human breast cancer - potential mechanisms and clinical implications. Anticancer Drugs 8, 911-930 (1997).
18. Hopp, T. A. & Fuqua, S. A. Estrogen receptor variants. J. Mammary Gland Biol. Neoplasia 3, 73-83 (1998).
19. Howell, A. et al. Pharmacokinetics, pharmacological and anti-tumour effects of the specific anti-oestrogen ICI 182780 in women with advanced breast cancer. Br. J. Cancer 74, 300-308 (1996).
20. Johnston, S. R. et al. Changes in estrogen receptor, progesterone receptor, and pS2 expression in tamoxifen-resistant human breast cancer. Cancer Res. 55, 3331-3338 (1995).
21. Linja, M. J. & Visakorpi, T. Alterations of androgen receptor in prostate cancer. J. Steroid Biochem. Mol. Biol. 92, 255-264 (2004).
22. Holst, F. et al. Estrogen receptor α (ESR1) gene amplification is frequent in breast cancer. Nature Genet. 39, 655-660 (2007).
23. Hall, J. M. & McDonnell, D. P. Coregulators in nuclear estrogen receptor action: from concept to therapeutic targeting. Mol. Interv. 5, 343-357 (2005).
24. Green, S., Kumar, V., Theulaz, I., Wahli, W. & Chambon, P. The N-terminal DNA-binding 'zinc finger' of the oestrogen and glucocorticoid receptors determines target gene specificity. EMBO J. 7, 3037-3044 (1988).
25. Mader, S., Kumar, V., de Verneuil, H. & Chambon, P. Three amino acids of the oestrogen receptor are essential to its ability to distinguish an oestrogen from a glucocorticoid-responsive element. Nature 338, 271-274 (1989).
26. Ruff, M., Gangloff, M., Wurtz, J. M. & Moras, D. Estrogen receptor transcription and transactivation: structure-function relationship in DNA- and ligand-binding domains of estrogen receptors. Breast Cancer Res. 2, 353-359 (2000).
27. Klinge, C. M. Estrogen receptor interaction with estrogen response elements. Nucleic Acids Res. 29, 2905-2919 (2001).
28. Maynard, A. T. & Covell, D. G. Reactivity of zinc finger cores: analysis of protein packing and electrostatic screening. J. Am. Chem. Soc. 123, 1047-1058 (2001).
29. Cheung, E., Schwabish, M. A. & Kraus, W. L. Chromatin exposes intrinsic differences in the transcriptional activities of estrogen receptors alpha and beta. EMBO J. 22, 600-611 (2003).
30. Bourguet, W. et al. Purification, functional characterization, and crystallization of the ligand binding domain of the retinoid X receptor. Protein Expr. Purif. 6, 604-608 (1995).
31. Bourguet, W., Ruff, M., Chambon, P., Gronemeyer, H. & Moras, D. Crystal structure of the ligand-binding domain of the human nuclear receptor RXR-α. Nature 375, 377-382 (1995).
32. Brzozowski, A. M. et al. Molecular basis of agonism and antagonism in the oestrogen receptor. Nature 389, 753-758 (1997).
33. Shiau, A. K. et al. The structural basis of estrogen receptor/coactivator recognition and the antagonism of this interaction by tamoxifen. Cell 95, 927-937 (1998).
34. Tanenbaum, D. M., Wang, Y., Williams, S. P. & Sigler, P. B. Crystallographic comparison of the estrogen and progesterone receptor's ligand binding domains. Proc. Natl Acad. Sci. USA 95, 5998-6003 (1998).
35. Celik, L., Lund, J. D. & Schiott, B. Conformational dynamics of the estrogen receptor α: molecular dynamics simulations of the influence of binding site structure on protein dynamics. Biochemistry 46, 1743-1758 (2007).
36. 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, 1025-1033 (1992).
37. Wrenn, C. K. & Katzenellenbogen, B. S. Structure-function analysis of the hormone binding domain of the human estrogen receptor by region-specific mutagenesis and phenotypic screening in yeast. J. Biol. Chem. 268, 24089-24098 (1993).
38. Henttu, P. M., Kalkhoven, E. & Parker, M. G. AF-2 activity and recruitment of steroid receptor coactivator 1 to the estrogen receptor depend on a lysine residue conserved in nuclear receptors. Mol. Cell Biol. 17, 1832-1839 (1997).
39. Feng, W. et al. Hormone-dependent coactivator binding to a hydrophobic cleft on nuclear receptors. Science 280, 1747-1749 (1998).
40. Onate, S. A., Tsai, S. Y., Tsai, M. J. & O'Malley, B. W. Sequence and characterization of a coactivator for the steroid hormone receptor superfamily. Science 270, 1354-1357 (1995).
41. Hong, H., Kohli, K., Garabedian, M. J. & Stallcup, M. R. GRIP1, a transcriptional coactivator for the AF-2 transactivation domain of steroid, thyroid, retinoid, and vitamin D receptors. Mol. Cell Biol. 17, 2735-2744 (1997).
42. Anzick, S. L. et al. AIB1, a steroid receptor coactivator amplified in breast and ovarian cancer. Science 277, 965-968 (1997).
43. Torchia, J. et al. The transcriptional co-activator p/CIP binds CBP and mediates nuclear-receptor function. Nature 387, 677-684 (1997).
44. Huang, H. J., Norris, J. D. & McDonnell, D. P. Identification of a negative regulatory surface within estrogen receptor alpha provides evidence in support of a role for corepressors in regulating cellular responses to agonists and antagonists. Mol. Endocrinol. 16, 1778-1792 (2002).
45. Horlein, A. J. et al. Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor. Nature 377, 397-404 (1995).
46. Chen, J. D. & Evans, R. M. A transcriptional corepressor that interacts with nuclear hormone receptors. Nature 377, 454-457 (1995).
47. Shang, Y., Hu, X., DiRenzo, J., Lazar, M. A. & Brown, M. Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 103, 843-852 (2000).
48. Metivier, R. et al. Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 115, 751-763 (2003).
49. 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, 21-28 (2001).
50. Osborne, C. K. 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, 353-361 (2003).
51. Cirillo, L. A. et al. Binding of the winged-helix transcription factor HNF3 to a linker histone site on the nucleosome. EMBO J. 17, 244-254 (1998).
52. Cirillo, L. A. et al. Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4. Mol. Cell 9, 279-289 (2002).
53. Carroll, J. S. et al. Chromosome-wide mapping of estrogen receptor binding reveals long-range regulation requiring the forkhead protein FoxA1. Cell 122, 33-43 (2005).
54. Laganiere, J. et al. Location analysis of estrogen receptor alpha target promoters reveals that FOXA1 defines a domain of the estrogen response. Proc. Natl Acad. Sci. USA 102, 11651-11656 (2005).
55. Eeckhoute, J., Carroll, J. S., Geistlinger, T. R., Torres-Arzayus, M. I. & Brown, M. A cell-type-specific transcriptional network required for estrogen regulation of cyclin D1 and cell cycle progression in breast cancer. Genes Dev. 20, 2513-2526 (2006).
56. Carroll, J. S. et al. Genome-wide analysis of estrogen receptor binding sites. Nature Genet. 38, 1289-1297 (2006).
57. Bourdeau, V. et al. Genome-wide identification of high-affinity estrogen response elements in human and mouse. Mol. Endocrinol. 18, 1411-1427 (2004).
58. Vega, V. B. et al. Multi-platform genome-wide identification and modeling of functional human estrogen receptor binding sites. Genome Biol. 7, R82 (2006).
59. Lin, C. Y. et al. Whole-genome cartography of estrogen receptor α binding sites. PLoS Genet. 3, e87 (2007).
60. Kouros-Mehr, H., Slorach, E. M., Sternlicht, M. D. & Werb, Z. GATA-3 maintains the differentiation of the luminal cell fate in the mammary gland. Cell 127, 1041-1055 (2006).
61. Eeckhoute, J. et al. Positive cross-regulatory loop ties GATA-3 to Estrogen Receptor alpha expression in breast cancer. Cancer Res. 67, 6477-6483 (2007).
62. Wang, Q. et al. A hierarchical network of transcription factors governs androgen receptor-dependent prostate cancer growth. Mol. Cell 27, 380-392 (2007).
63. Kassabov, S. R., Zhang, B., Persinger, J. & Bartholomew, B. SWI/SNF unwraps, slides, and rewraps the nucleosome. Mol. Cell 11, 391-403 (2003).
64. Kadam, S. & Emerson, B. M. Transcriptional specificity of human SWI/SNF BRG1 and BRM chromatin remodeling complexes. Mol. Cell 11, 377-389 (2003).
65. Owen-Hughes, T., Utley, R. T., Cote, J., Peterson, C. L. & Workman, J. L. Persistent site-specific remodeling of a nucleosome array by transient action of the SWI/SNF complex. Science 273, 513-516 (1996).
66. Ichinose, H., Garnier, J. M., Chambon, P. & Losson, R. Ligand-dependent interaction between the estrogen receptor and the human homologues of SWI2/SNF2. Gene 188, 95-100 (1997).
67. DiRenzo, J. et al. BRG-1 is recruited to estrogen-responsive promoters and cooperates with factors involved in histone acetylation. Mol. Cell Biol. 20, 7541-7549 (2000).
68. Chiba, H., Muramatsu, M., Nomoto, A. & Kato, H. Two human homologues of Saccharomyces cerevisiae SWI2/SNF2 and Drosophila brahma are transcriptional coactivators cooperating with the estrogen receptor and the retinoic acid receptor. Nucleic Acids Res. 22, 1815-1820 (1994).
69. Belandia, B., Orford, R. L., Hurst, H. C. & Parker, M. G. Targeting of SWI/SNF chromatin remodelling complexes to estrogen-responsive genes. EMBO J. 21, 4094-4103 (2002).
70. Garcia-Pedrero, J. M., Kiskinis, E., Parker, M. G. & Belandia, B. The SWI/SNF chromatin remodeling subunit BAF57 is a critical regulator of estrogen receptor function in breast cancer cells. J. Biol. Chem. 281, 22656-22664 (2006).
71. Kiskinis, E., Garcia-Pedrero, J. M., Villaronga, M. A., Parker, M. G. & Belandia, B. Identification of BAF57 mutations in human breast cancer cell lines. Breast Cancer Res. Treat. 98, 191-198 (2006).
72. Narlikar, G. J., Fan, H. Y. & Kingston, R. E. Cooperation between complexes that regulate chromatin structure and transcription. Cell 108, 475-487 (2002).
73. Wu, R. C. et al. Selective phosphorylations of the SRC-3/AIB1 coactivator integrate genomic reponses to multiple cellular signaling pathways. Mol. Cell 15, 937-949 (2004).
74. Pollard, K. J. & Peterson, C. L. Chromatin remodeling: a marriage between two families? Bioessays 20, 771-780 (1998).
75. Kouzarides, T. Chromatin modifications and their function. Cell 128, 693-705 (2007).
76. Kamei, Y. et al. A CBP integrator complex mediates transcriptional activation and AP-1 inhibition by nuclear receptors. Cell 85, 403-414 (1996).
77. Torchia, J., Glass, C. & Rosenfeld, M. G. Co-activators and co-repressors in the integration of transcriptional responses. Curr. Opin. Cell Biol. 10, 373-383 (1998).
78. Chen, H. et al. Nuclear receptor coactivator ACTR is a novel histone acetyltransferase and forms a multimeric activation complex with P/CAF and CBP/p300. Cell 90, 569-580 (1997).
79. Demarest, S. J. et al. Mutual synergistic folding in recruitment of CBP/p300 by p160 nuclear receptor coactivators. Nature 415, 549-553 (2002).
80. Martinez-Balbas, M. A. et al. The acetyltransferase activity of CBP stimulates transcription. EMBO J. 17, 2886-2893 (1998).
81. Spencer, T. E. et al. Steroid receptor coactivator-1 is a histone acetyltransferase. Nature 389, 194-198 (1997).
82. Schiltz, R. L. et al. Overlapping but distinct patterns of histone acetylation by the human coactivators p300 and PCAF within nucleosomal substrates. J. Biol. Chem. 274, 1189-1192 (1999).
83. Webb, P. et al. Estrogen receptor activation function 1 works by binding p160 coactivator proteins. Mol. Endocrinol. 12, 1605-1618 (1998).
84. Kobayashi, Y. et al. p300 mediates functional synergism between AF-1 and AF-2 of estrogen receptor α and β by interacting directly with the N-terminal A/B domains. J. Biol. Chem. 275, 15645-15651 (2000).
85. Kim, M. Y., Hsiao, S. J. & Kraus, W. L. A role for coactivators and histone acetylation in estrogen receptor α-mediated transcription initiation. EMBO J. 20, 6084-6094 (2001).
86. Sewack, G. F., Ellis, T. W. & Hansen, U. Binding of TATA binding protein to a naturally positioned nucleosome is facilitated by histone acetylation. Mol. Cell Biol. 21, 1404-1415 (2001).
87. Kraus, W. L. & Kadonaga, J. T. p300 and estrogen receptor cooperatively activate transcription via differential enhancement of initiation and reinitiation. Genes Dev. 12, 331-342 (1998).
88. Hudelist, G. et al. Expression of sex steroid receptors and their co-factors in normal and malignant breast tissue: AIB1 is a carcinoma-specific co-activator. Breast Cancer Res. Treat. 78, 193-204 (2003).
89. Shou, J. et al. Mechanisms of tamoxifen resistance: increased estrogen receptor-HER2/neu cross-talk in ER/HER2-positive breast cancer. J. Natl Cancer Inst. 96, 926-935 (2004).
90. Fu, M. et al. p300 and p300/cAMP-response element-binding protein-associated factor acetylate the androgen receptor at sites governing hormone-dependent transactivation. J. Biol. Chem. 275, 20853-20860 (2000).
91. Debes, J. D. et al. p300 in prostate cancer proliferation and progression. Cancer Res. 63, 7638-7640 (2003).
92. Heemers, H. V. et al. Androgen deprivation increases p300 expression in prostate cancer cells. Cancer Res. 67, 3422-3430 (2007).
93. Wang, Q., Carroll, J. S. & Brown, M. Spatial and temporal recruitment of androgen receptor and its coactivators involves chromosomal looping and polymerase tracking. Mol. Cell 19, 631-642 (2005).
94. Yang, X. J., Ogryzko, V. V., Nishikawa, J., Howard, B. H. & Nakatani, Y. A p300/CBP-associated factor that competes with the adenoviral oncoprotein E1A. Nature 382, 319-324 (1996).
95. Xu, W., Edmondson, D. G. & Roth, S. Y. Mammalian GCN5 and P/CAF acetyltransferases have homologous amino-terminal domains important for recognition of nucleosomal substrates. Mol. Cell Biol. 18, 5659-5669 (1998).
96. Santos-Rosa, H., Valls, E., Kouzarides, T. & Martinez-Balbas, M. Mechanisms of P/CAF autoacetylation. Nucleic Acids Res. 31, 4285-4292 (2003).
97. Cheng, A. S. et al. Combinatorial analysis of transcription factor partners reveals recruitment of c-MYC to estrogen receptor-α responsive promoters. Mol. Cell 21, 393-404 (2006).
98. Cascio, S. et al. Insulin-like growth factor 1 differentially regulates estrogen receptor-dependent transcription at estrogen response element and AP-1 sites in breast cancer cells. J. Biol. Chem. 282, 3498-3506 (2007).
99. Qi, C. et al. Identification of protein arginine methyltransferase 2 as a coactivator for estrogen receptor α. J. Biol. Chem. 277, 28624-28630 (2002).
100. Bedford, M. T. & Richard, S. Arginine methylation an emerging regulator of protein function. Mol. Cell 18, 263-272 (2005).
101. Strahl, B. D. et al. Methylation of histone H4 at arginine 3 occurs in vivo and is mediated by the nuclear receptor coactivator PRMT1. Curr. Biol. 11, 996-1000 (2001).
102. Wang, H. et al. Methylation of histone H4 at arginine 3 facilitating transcriptional activation by nuclear hormone receptor. Science 293, 853-857 (2001).
103. Wagner, S., Weber, S., Kleinschmidt, M. A., Nagata, K. & Bauer, U. M. SET-mediated promoter hypoacetylation is a prerequisite for coactivation of the estrogen-responsive pS2 gene by PRMT1. J. Biol. Chem. 281, 27242-27250 (2006).
104. Chen, D. et al. Regulation of transcription by a protein methyltransferase. Science 284, 2174-2177 (1999).
105. Chen, D., Huang, S. M. & Stallcup, M. R. Synergistic, p160 coactivator-dependent enhancement of estrogen receptor function by CARM1 and p300. J. Biol. Chem. 275, 40810-40816 (2000).
106. Teyssier, C., Chen, D. & Stallcup, M. R. Requirement for multiple domains of the protein arginine methyltransferase CARM1 in its transcriptional coactivator function. J. Biol. Chem. 277, 46066-46072 (2002).
107. Klinge, C. M., Jernigan, S. C., Mattingly, K. A., Risinger, K. E. & Zhang, J. Estrogen response element-dependent regulation of transcriptional activation of estrogen receptors α and β by coactivators and corepressors. J. Mol. Endocrinol. 33, 387-410 (2004).
108. Xu, W. et al. A methylation-mediator complex in hormone signaling. Genes Dev. 18, 144-156 (2004).
109. Ma, H. et al. Hormone-dependent, CARM1-directed, arginine-specific methylation of histone H3 on a steroid-regulated promoter. Curr. Biol. 11, 1981-1985 (2001).
110. Schurter, B. T. et al. Methylation of histone H3 by coactivator-associated arginine methyltransferase 1. Biochemistry 40, 5747-5756 (2001).
111. Bauer, U. M., Daujat, S., Nielsen, S. J., Nightingale, K. & Kouzarides, T. Methylation at arginine 17 of histone H3 is linked to gene activation. EMBO Rep. 3, 39-44 (2002).
112. Daujat, S. et al. Crosstalk between CARM1 methylation and CBP acetylation on histone H3. Curr. Biol. 12, 2090-2097 (2002).
113. Shi, Y. et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 119, 941-953 (2004).
114. Metzger, E. et al. LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 437, 436-439 (2005).
115. Garcia-Bassets, I. et al. Histone methylation-dependent mechanisms impose ligand dependency for gene activation by nuclear receptors. Cell 128, 505-518 (2007).
116. 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, 1153-1160 (1993).
117. 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, 4458-4466 (1994).
118. 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, 1208-1214 (1994).
119. Kato, S. et al. Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science 270, 1491-1494 (1995).
120. Joel, P. B. et al. pp90rsk1 regulates estrogen receptor-mediated transcription through phosphorylation of Ser-167. Mol. Cell Biol. 18, 1978-1984 (1998).
121. Shao, D. & Lazar, M. A. Modulating nuclear receptor function: may the phos be with you. J. Clin. Invest. 103, 1617-1618 (1999).
122. Martin, M. B. et al. A role for Akt in mediating the estrogenic functions of epidermal growth factor and insulin-like growth factor I. Endocrinology 141, 4503-4511 (2000).
123. Campbell, R. A. et al. Phosphatidylinositol 3-kinase/AKT-mediated activation of estrogen receptor α: a new model for anti-estrogen resistance. J. Biol. Chem. 276, 9817-9824 (2001).
124. Chen, D. et al. Phosphorylation of human estrogen receptor alpha at serine 118 by two distinct signal transduction pathways revealed by phosphorylation-specific antisera. Oncogene 21, 4921-4931 (2002).
125. Glaros, S., Atanaskova, N., Zhao, C., Skafar, D. F. & Reddy, K. B. Activation function-1 domain of estrogen receptor regulates the agonistic and antagonistic actions of tamoxifen. Mol. Endocrinol. 20, 996-1008 (2006).
126. Font de Mora, J. & Brown, M. AIB1 is a conduit for kinase-mediated growth factor signaling to the estrogen receptor. Mol. Cell Biol. 20, 5041-5047 (2000).
127. Bautista, S. et al. In breast cancer, amplification of the steroid receptor coactivator gene AIB1 is correlated with estrogen and progesterone receptor positivity. Clin. Cancer Res. 4, 2925-2929 (1998).
128. Torres-Arzayus, M. I. et al. High tumor incidence and activation of the PI3K/AKT pathway in transgenic mice define AIB1 as an oncogene. Cancer Cell 6, 263-274 (2004).
129. Yi, P. et al. Peptidyl-prolyl isomerase 1 (Pin1) serves as a coactivator of steroid receptor by regulating the activity of phosphorylated steroid receptor coactivator 3 (SRC-3/AIB1). Mol. Cell Biol. 25, 9687-9699 (2005).
130. Benz, C. C. et al. Estrogen-dependent, tamoxifen-resistant tumorigenic growth of MCF-7 cells transfected with HER2/neu. Breast Cancer Res. Treat. 24, 85-95 (1992).
131. Witters, L., Engle, L. & Lipton, A. Restoration of estrogen responsiveness by blocking the HER-2/neu pathway. Oncol. Rep. 9, 1163-1166 (2002).
132. Knowlden, J. M. et al. Elevated levels of epidermal growth factor receptor/c-erbB2 heterodimers mediate an autocrine growth regulatory pathway in tamoxifen-resistant MCF-7 cells. Endocrinology 144, 1032-1044 (2003).
133. Larsen, S. S., Egeblad, M., Jaattela, M. & Lykkesfeldt, A. E. Acquired antiestrogen resistance in MCF-7 human breast cancer sublines is not accomplished by altered expression of receptors in the ErbB-family. Breast Cancer Res. Treat. 58, 41-56 (1999).
134. Park, K. J., Krishnan, V., O'Malley, B. W., Yamamoto, Y. & Gaynor, R. B. Formation of an IKKα-dependent transcription complex is required for estrogen receptor-mediated gene activation. Mol. Cell 18, 71-82 (2005).
135. Prall, O. W., Rogan, E. M., Musgrove, E. A., Watts, C. K. & Sutherland, R. L. c-Myc or cyclin D1 mimics estrogen effects on cyclin E-Cdk2 activation and cell cycle reentry. Mol. Cell Biol. 18, 4499-4508 (1998).
136. Keeton, E. K. & Brown, M. Cell cycle progression stimulated by tamoxifen-bound estrogen receptor-α and promoter-specific effects in breast cancer cells deficient in N-CoR and SMRT. Mol. Endocrinol. 19, 1543-1554 (2005).
137. Yamamoto, Y. et al. The tamoxifen-responsive estrogen receptor alpha mutant D351Y shows reduced tamoxifen-dependent interaction with corepressor complexes. J. Biol. Chem. 276, 42684-42691 (2001).
138. Hu, X. & Lazar, M. A. The CoRNR motif controls the recruitment of corepressors by nuclear hormone receptors. Nature 402, 93-96 (1999).
139. Liu, X. F. & Bagchi, M. K. Recruitment of distinct chromatin-modifying complexes by tamoxifen-complexed estrogen receptor at natural target gene promoters in vivo. J. Biol. Chem. 279, 15050-15058 (2004).
140. 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, 129-138 (1994).
141. Catherino, W. H., Wolf, D. M. & Jordan, V. C. A naturally occurring estrogen receptor mutation results in increased estrogenicity of a tamoxifen analog. Mol. Endocrinol. 9, 1053-1063 (1995).
142. Levenson, A. S., Catherino, W. H. & Jordan, V. C. Estrogenic activity is increased for an antiestrogen by a natural mutation of the estrogen receptor. J. Steroid Biochem. Mol. Biol. 60, 261-268 (1997).
143. MacGregor Schafer, J., Liu, H., Bentrem, D. J., Zapf, J. W. & Jordan, V. C. Allosteric silencing of activating function 1 in the 4-hydroxytamoxifen estrogen receptor complex is induced by substituting glycine for aspartate at amino acid 351. Cancer Res. 60, 5097-5105 (2000).
144. Pakdel, F. & Katzenellenbogen, B. S. Human estrogen receptor mutants with altered estrogen and antiestrogen ligand discrimination. J. Biol. Chem. 267, 3429-3437 (1992).
145. Mahfoudi, A., Roulet, E., Dauvois, S., Parker, M. G. & Wahli, W. Specific mutations in the estrogen receptor change the properties of antiestrogens to full agonists. Proc. Natl Acad. Sci. USA 92, 4206-4210 (1995).
146. Montano, M. M., Ekena, K., Krueger, K. D., Keller, A. L. & Katzenellenbogen, B. S. Human estrogen receptor ligand activity inversion mutants: receptors that interpret antiestrogens as estrogens and estrogens as antiestrogens and discriminate among different antiestrogens. Mol. Endocrinol. 10, 230-242 (1996).
147. McInerney, E. M. & Katzenellenbogen, B. S. Different regions in activation function-1 of the human estrogen receptor required for antiestrogen- and estradiol-dependent transcription activation. J. Biol. Chem. 271, 24172-24178 (1996).
148. Kurebayashi, J. et al. Expression levels of estrogen receptor-alpha, estrogen receptor-beta, coactivators, and corepressors in breast cancer. Clin. Cancer Res. 6, 512-518 (2000).
149. Lavinsky, R. M. et al. Diverse signaling pathways modulate nuclear receptor recruitment of N-CoR and SMRT complexes. Proc. Natl Acad. Sci. USA 95, 2920-2925 (1998).
150. Carroll, J. S. et al. p27(Kip1) induces quiescence and growth factor insensitivity in tamoxifen-treated breast cancer cells. Cancer Res. 63, 4322-4326 (2003).
151. Frasor, J., Danes, J. M., Funk, C. C. & Katzenellenbogen, B. S. Estrogen down-regulation of the corepressor N-CoR: mechanism and implications for estrogen derepression of N-CoR-regulated genes. Proc. Natl Acad. Sci. USA 102, 13153-13157 (2005).
152. Perissi, V., Aggarwal, A., Glass, C. K., Rose, D. W. & Rosenfeld, M. G. A corepressor/coactivator exchange complex required for transcriptional activation by nuclear receptors and other regulated transcription factors. Cell 116, 511-526 (2004).
153. Naeem, H. et al. The activity and stability of the transcriptional coactivator p/CIP/SRC-3 are regulated by CARM1-dependent methylation. Mol. Cell Biol. 27, 120-134 (2007).
154. Feng, Q., Yi, P., Wong, J. & O'Malley, B. W. Signaling within a coactivator complex: methylation of SRC-3/AIB1 is a molecular switch for complex disassembly. Mol. Cell Biol. 26, 7846-7857 (2006).
155. Lee, Y. H., Coonrod, S. A., Kraus, W. L., Jelinek, M. A. & Stallcup, M. R. Regulation of coactivator complex assembly and function by protein arginine methylation and demethylimination. Proc. Natl Acad. Sci. USA 102, 3611-3616 (2005).
156. Hong, H. et al. Aberrant expression of CARM1, a transcriptional coactivator of androgen receptor, in the development of prostate carcinoma and androgen-independent status. Cancer 101, 83-89 (2004).
157. Frasor, J. et al. Selective estrogen receptor modulators: discrimination of agonistic versus antagonistic activities by gene expression profiling in breast cancer cells. Cancer Res. 64, 1522-1533 (2004).
158. Frasor, J. et al. Gene expression preferentially regulated by tamoxifen in breast cancer cells and correlations with clinical outcome. Cancer Res. 66, 7334-7340 (2006).
159. Hodges, L. C. et al. Tamoxifen functions as a molecular agonist inducing cell cycle-associated genes in breast cancer cells. Mol. Cancer Res. 1, 300-311 (2003).
160. Stossi, F., Likhite, V. S., Katzenellenbogen, J. A. & Katzenellenbogen, B. S. Estrogen-occupied estrogen receptor represses cyclin G2 gene expression and recruits a repressor complex at the cyclin G2 promoter. J. Biol. Chem. 281, 16272-16278 (2006).
161. 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, 5925-5930 (1996).
162. Palmieri, C. et al. Estrogen receptor beta in breast cancer. Endocr. Relat. Cancer 9, 1-13 (2002).
163. Palmieri, C. et al. The expression of oestrogen receptor (ER)-beta and its variants, but not ERα, in adult human mammary fibroblasts. J. Mol. Endocrinol. 33, 35-50 (2004).
164. Liu, M. M. et al. Opposing action of estrogen receptors α and β on cyclin D1 gene expression. J. Biol. Chem. 277, 24353-24360 (2002).
165. Lindberg, M. K. et al. Estrogen receptor (ER)-β reduces ERα-regulated gene transcription, supporting a "ying yang" relationship between ERα and ERβ in mice. Mol. Endocrinol. 17, 203-208 (2003).
166. Faulds, M. H., Olsen, H., Helguero, L. A., Gustafsson, J. A. & Haldosen, L. A. Estrogen receptor functional activity changes during differentiation of mammary epithelial cells. Mol. Endocrinol. 18, 412-421 (2004).
167. Strom, A. et al. Estrogen receptor β inhibits 17beta-estradiol-stimulated proliferation of the breast cancer cell line T47D. Proc. Natl Acad. Sci. USA 101, 1566-1571 (2004).
168. Matthews, J. et al. Estrogen receptor (ER) β modulates ERα-mediated transcriptional activation by altering the recruitment of c-Fos and c-Jun to estrogen-responsive promoters. Mol. Endocrinol. 20, 534-543 (2006).
169. Kumar, V. et al. Functional domains of the human estrogen receptor. Cell 51, 941-951 (1987).
170. Stack, G. et al. Structure and function of the pS2 gene and estrogen receptor in human breast cancer cells. Cancer Treat. Res. 40, 185-206 (1988).
171. Sewack, G. F. & Hansen, U. Nucleosome positioning and transcription-associated chromatin alterations on the human estrogen-responsive pS2 promoter. J. Biol. Chem. 272, 31118-31129 (1997).
172. Metivier, R. et al. Transcriptional complexes engaged by apo-estrogen receptor-alpha isoforms have divergent outcomes. EMBO J. 23, 3653-3666 (2004).
173. Muller, W. & Borchard, F. pS2 protein in gastric carcinoma and normal gastric mucosa: association with clincopathological parameters and patient survival. J. Pathol. 171, 263-269 (1993).
174. Katoh, M. Trefoil factors and human gastric cancer [Dave: should review be deleted?] (review). Int. J. Mol. Med. 12, 3-9 (2003).
175. Karam, S. M., Tomasetto, C. & Rio, M. C. Trefoil factor 1 is required for the commitment programme of mouse oxyntic epithelial progenitors. Gut 53, 1408-1415 (2004).
176. Kwon, Y. S. et al. Sensitive ChIP-DSL technology reveals an extensive estrogen receptor α-binding program on human gene promoters. Proc. Natl Acad. Sci. USA 104, 4852-4857 (2007).
177. Montano, M. M. et al. An estrogen receptor-selective coregulator that potentiates the effectiveness of antiestrogens and represses the activity of estrogens. Proc. Natl Acad. Sci. USA 96, 6947-6952 (1999).
178. Deblois, G. & Giguere, V. Ligand-independent coactivation of ERα AF-1 by steroid receptor RNA activator (SRA) via MAPK activation. J. Steroid Biochem. Mol. Biol. 85, 123-131 (2003).