A bi-faceted role of estrogen receptor β in breast cancer

Endocrine-Related Cancer

Volumn 20, Issue 3, 2013, Pages

  Leygue, Etienne ^a   Murphy, Leigh C ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Breast; Endocrine therapy resistance; Estrogen receptor; Estrogen therapy

Indexed keywords

ANTIESTROGEN; CELL NUCLEUS RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; PROGESTERONE RECEPTOR;

ALTERNATIVE RNA SPLICING; APOPTOSIS; BREAST CANCER; BREAST CARCINOGENESIS; BREAST EPITHELIUM; CANCER INHIBITION; CELL COUNT; CELL CULTURE; CELL DIFFERENTIATION; CELL SURVIVAL; CELLULAR DISTRIBUTION; DNA SEQUENCE; ENHANCER REGION; EPITHELIAL MESENCHYMAL TRANSITION; ESTROGEN ACTIVITY; ESTROGEN RESPONSIVE ELEMENT; GENETIC TRANSCRIPTION; GROWTH STIMULATION; HORMONAL THERAPY; HUMAN; IMMUNODETECTION; IMMUNOHISTOCHEMISTRY; LIGAND BINDING; MAMMARY GLAND; MUTAGENESIS; MYOEPITHELIUM CELL; PREDICTIVE VALUE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN STRUCTURE; REVIEW; TRANSIENT EXPRESSION; TUMOR MICROENVIRONMENT;

BREAST; ENDOCRINE THERAPY RESISTANCE; ESTROGEN RECEPTOR; ESTROGEN THERAPY;

ANIMALS; BREAST NEOPLASMS; ESTROGEN RECEPTOR BETA; FEMALE; HUMANS;

EID: 84879495316     PISSN: 13510088     EISSN: 14796821     Source Type: Journal    
DOI: 10.1530/ERC-12-0389     Document Type: Review

References (122)

1. Antal M, Krust A, Chambon P & Mark M 2008 Sterility and absence of histopathological defects in nonreproductive organs of a mouse ERbnull mutant. PNAS 105 2433-2438. (doi:10.1073/pnas.0712029105)
2. Bardin A, Boulle N, Lazennec G, Vignon F & Pujol P 2004 Loss of ERb expression as a common step in estrogen-dependent tumor progression. Endocrine-Related Cancer 11 537-551. (doi:10.1677/erc.1.00800)
3. Bhat R, Harnish DC, Stevis P, Lyttle C & Komm B 1998 A novel human estrogen receptor β: identification and functional analysis of additional N-terminal amino acids. Journal of Steroid Biochemistry and Molecular Biology 67 233-240. (doi:10.1016/S0960-0760(98)00115-0)
4. Bhat-Nakshatri P, Wang G, Appaiah H, Luktuke N, Carroll JS, Geistlinger TR, Brown M, Badve S, Liu Y & Nakshatri H 2008 AKT alters genome-wide estrogen receptor α binding and impacts estrogen signaling in breast cancer. Molecular and Cellular Biology 28 7487-7503. (doi:10.1128/MCB.00799-08)
5. Bocchinfuso W & Korach K 1997 Mammary gland development and tumorigenesis in estrogen receptor knockout mice. Journal of Mammary Gland Biology and Neoplasia 2 323-334. (doi:10.1023/A:1026339111278)
6. Chang EC, Frasor J, Komm B & Katzenellenbogen BS 2006 Impact of estrogen receptor β on gene networks regulated by estrogen receptor α in breast cancer cells. Endocrinology 147 4831-4842. (doi:10.1210/en.2006-0563)
7. Charn TH, Liu ET, Chang EC, Lee YK, Katzenellenbogen JA & Katzenellenbogen BS 2010 Genome-wide dynamics of chromatin binding of estrogen receptors α and β: mutual restriction and competitive site selection. Molecular Endocrinology 24 47-59. (doi:10.1210/me.2009-0252)
8. Cheng G, Weihua Z, Warner M & Gustafsson J 2004a Estrogen receptors ERα and ERβ in proliferation in the rodent mammary gland. PNAS 101 3739-3746. (doi:10.1073/pnas.0307864100)
9. Cheng J, Lee E, Madison L & Lazennec G 2004b Expression of estrogen receptor b in prostate carcinoma cells inhibits invasion and proliferation and triggers apoptosis. FEBS Letters 566 169-172. (doi:10.1016/j.febslet.2004.04. 025)
10. Cheng G, Li Y, Omoto Y, Wang Y, Berg T, Nord M, Vihko P, Warner M, Piao Y & Gustafsson J 2005 Differential regulation of estrogen receptor (ER)α and ERβ in primate mammary gland. Journal of Clinical Endocrinology and Metabolism 90 435-444. (doi:10.1210/jc.2004-0861)
11. Cheng L, Li J, Han Y, Lin J, Niu C, Zhou Z, Yuan B, Huang K, Jiang K, Zhang H et al. 2012 PES1 promotes breast cancer by differentially regulating ERα and ERβ. Journal of Clinical Investigation 122 2857-2870. (doi:10.1172/JCI62676)
12. Choi Y & Pinto M 2005 Estrogen receptor b in breast cancer: associations between ERβ, hormonal receptors, and other prognostic biomarkers. Applied Immunohistochemistry & Molecular Morphology 13 19-24. (doi:10.1097/00129039-200503000-00004)
13. Cleveland AG, Oikarinen SI, Bynote KK, Marttinen M, Rafter JJ, Gustafsson JA, Roy SK, Pitot HC, Korach KS, Lubahn DB et al. 2009 Disruption of estrogen receptor signaling enhances intestinal neoplasia in Apc(Min/+) mice. Carcinogenesis 30 1581-1590. (doi:10.1093/carcin/bgp132)
14. Cooper C, Vincett D, Yan Y, Hamedani MK, Myal Y & Leygue E 2011 Steroid receptor RNA activator bi-faceted genetic system: heads or tails? Biochimie 93 1973-1980. (doi:10.1016/j.biochi.2011.07.002)
15. Cotrim CZ, Fabris V, Doria ML, Lindberg K, Gustafsson JA, Amado F, Lanari C & Helguero LA 2013 Estrogen receptor b growth-inhibitory effects are repressed through activation of MAPK and PI3K signalling inmammary epithelial and breast cancer cells. Oncogene 32 2390-2402. (doi:10.1038/onc.2012.261)
16. Couse J & Korach K 1999 Estrogen receptor null mice: what have we learned and where will they lead us? Endocrine Reviews 20 358-417. (doi:10.1210/er.20.3.358)
17. Cvoro A, Tatomer D, Tee M, Zogovic T, Harris H & Leitman D 2008 Selective estrogen receptor-β agonists repress transcription of proinflammatory genes. Journal of Immunology 180 630-636.
18. Deblois G & Giguere V 2013 Oestrogen-related receptors in breast cancer: control of cellular metabolism and beyond. Nature Reviews. Cancer 13 27-36. (doi:10.1038/nrc3396)
19. DuSell CD & McDonnell DP 2008 27-Hydroxycholesterol: a potential endogenous regulator of estrogen receptor signaling. Trends in Pharmacological Sciences 29 510-514. (doi:10.1016/j.tips.2008.07.003)
20. Esslimani-Sahla M, Simony-Lafontaine J, Kramar A, Lavaill R, Mollevi C, Warner M, Gustafsson J-A & Rochefort H 2004 Estrogen receptor b (ERβ) level but not its ERβ-cx variant helps to predict tamoxifen resistance in breast cancer. Clinical Cancer Research 10 5769-5776. (doi:10.1158/1078-0432. CCR-04-0389)
21. Feng Y, Manka D, Wagner KU & Khan SA 2007 Estrogen receptor-α expression in the mammary epithelium is required for ductal and alveolar morphogenesis in mice. PNAS 104 14718-14723. (doi:10.1073/pnas.0706933104)
22. Finan B, Yang B, Ottaway N, Stemmer K, Muller TD, Yi CX, Habegger K, Schriever SC, Garcia-Caceres C, Kabra DG et al. 2012 Targeted estrogen delivery reverses the metabolic syndrome. Nature Medicine 18 1847-1856. (doi:10.1038/nm.3009)
23. Fisher B, Costantino J, Wickerham D, Cecchini R, Cronin W, Robidoux A, Bevers T, Kavanah M, Atkins J, Margolese R 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)
24. Fleming F, Hill A, McDermott E, O'Higgins N & Young L 2004 Differential recruitment of coregulator proteins steroid receptor coactivator-1 and silencing mediator for retinoid and thyroid receptors to the estrogen receptor-estrogen response element by β-estradiol and 4-hydroxytamoxifen in human breast cancer. Journal of Clinical Endocrinology and Metabolism 89 375-383. (doi:10.1210/jc.2003-031048)
25. Forster C, Makela S, Warri A, Kietz S, Becker D, Hultenby K, Warner M & Gustafsson J 2002 Involvement of estrogen receptor b in terminal differentiation of mammary gland epithelium. PNAS 99 15578-15583. (doi:10.1073/pnas.192561299)
26. Fox E, Davis R & Shupnik M 2008 ERβ in breast cancer - onlooker, passive player, or active protector? Steroids 73 1039-1051. (doi:10.1016/j.steroids.2008.04.006)
27. Giroux V, Lemay F, Bernatchez G, Robitaille Y & Carrier J 2008 Estrogen receptor β deficiency enhances small intestinal tumorigenesis in ApcMin/+ mice. International Journal of Cancer 123 303-311. (doi:10.1002/ijc. 23532)
28. Grober OM, Mutarelli M, Giurato G, Ravo M, Cicatiello L, De Filippo MR, Ferraro L, Nassa G, Papa MF, Paris O et al. 2011 Global analysis of estrogen receptor b binding to breast cancer cell genome reveals an extensive interplay with estrogen receptor a for target gene regulation. BMC Genomics 12 36. (doi:10.1186/1471-2164-12-36)
29. Gruvberger-Saal S, Bendahl P, Saal L, Laakso M, Hegardt C, Edén P, Peterson C, Malmström P, Isola J, Borg A et al. 2007 Estrogen receptor b expression is associated with tamoxifen response in ERα-negative breast carcinoma. Clinical Cancer Research 13 1987-1994. (doi:10.1158/1078-0432.CCR-06- 1823)
30. Guerini V, Sau D, Scaccianoce E, Rusmini P, Ciana P, Maggi A, Martini P, Katzenellenbogen B, Martini L, Motta M et al. 2005 The androgen derivative 5α-androstane-3β,17β-diol inhibits prostate cancer cell migration through activation of the estrogen receptor b subtype. Cancer Research 65 5445-5453. (doi:10.1158/0008-5472.CAN-04-1941)
31. Hall J, Couse J & Korach K 2001 The multifaceted mechanisms of estradiol and estrogen receptor signaling. Journal of Biological Chemistry 276 36869-36872. (doi:10.1074/jbc.R100029200)
32. Hamilton-Burke W, Coleman L, Cummings M, Green CA, Holliday DL, Horgan K, Maraqa L, Peter MB, Pollock S, Shaaban AM et al. 2010 Phosphorylation of estrogen receptor b at serine 105 is associated with good prognosis in breast cancer. American Journal of Pathology 177 1079-1086. (doi:10.2353/ajpath.2010. 090886)
33. Hammes SR & Levin ER 2011 Minireview: recent advances in extranuclear steroid receptor actions. Endocrinology 152 4489-4495. (doi:10.1210/en.2011- 1470)
34. Hammond ME, Hayes DF, Dowsett M, Allred DC, Hagerty KL, Badve S, Fitzgibbons PL, Francis G, Goldstein NS, Hayes M et al. 2010 American Society of Clinical Oncology/College Of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. Journal of Clinical Oncology 28 2784-2795. (doi:10.1200/JCO.2009.25. 6529)
35. Haring J, Schuler S, Lattrich C, Ortmann O & Treeck O 2012 Role of estrogen receptor b in gynecological cancer. Gynecologic Oncology 127 673-676. (doi:10.1016/j.ygyno.2012.09.006)
36. Harrington W, Sheng S, Barnett D, Petz L, Katzenellenbogen J & Katzenellenbogen B 2003 Activities of estrogen receptor α- and β-selective ligands at diverse estrogen responsive gene sites mediating transactivation or transrepression. Molecular and Cellular Endocrinology 206 13-22. (doi:10.1016/S0303-7207(03)00255-7)
37. Helguero LA, Faulds MH, Gustafsson JA & Haldosen LA 2005 Estrogen receptors alfa (ERα) and β (ERβ) differentially regulate proliferation and apoptosis of the normal murine mammary epithelial cell line HC11. Oncogene 24 6605-6616. (doi:10.1038/sj.onc.1208807)
38. Herynk M & Fuqua S 2004 Estrogen receptor mutations in human disease. Endocrine Reviews 25 869-898. (doi:10.1210/er.2003-0010)
39. Hickey TE, Robinson JL, Carroll JS & Tilley WD 2012 Minireview: the androgen receptor in breast tissues: growth inhibitor, tumor suppressor, oncogene? Molecular Endocrinology 26 1252-1267. (doi:10.1210/me.2012-1107)
40. Hodges-Gallagher L, Valentine CD, El Bader S & Kushner PJ 2008 Estrogen receptor b increases the efficacy of antiestrogens by effects on apoptosis and cell cycling in breast cancer cells. Breast Cancer Research and Treatment 109 241-250. (doi:10.1007/s10549-007-9640-6)
41. Honma N, Horii R, Iwase T, Saji S, Younes M, Takubo K, Matsuura M, Ito Y, Akiyama F & Sakamoto G 2008 Clinical importance of estrogen receptor-β evaluation in breast cancer patients treated with adjuvant tamoxifen therapy. Journal of Clinical Oncology 26 3727-3734. (doi:10.1200/JCO.2007.14.2968)
42. Hou Y, Yuan S, Li H, Wu J, Lu J, Liu G, Lu L, Shen Z, Ding J & Shao Z 2004 ERβ exerts multiple stimulative effects on human breast carcinoma cells. Oncogene 23 5799-5806. (doi:10.1038/sj.onc.1207765)
43. Kuiper G, Enmark E, Pelto-Huikko M, Nilsson S & Gustafsson J-A 1996 Cloning of a novel estrogen receptor expressed in rat prostate and ovary. PNAS 93 5925-5930. (doi:10.1073/pnas.93.12.5925)
44. Kuiper G, Lemmen J, Carlsson B, Corton J, Safe S & Saag PVD 1998 Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor b. Endocrinology 139 4252-4263. (doi:10.1210/en.139.10.4252)
45. Kumar R & McEwan IJ 2012 Allosteric modulators of steroid hormone receptors: structural dynamics and gene regulation. Endocrine Reviews 33 271-299. (doi:10.1210/er.2011-1033)
46. Lazennec G, Bresson D, Lucas A, Chauveau C & Vignon F 2001 ERβ inhibits proliferation and invasion of breast cancer cells. Endocrinology 142 4120-4130. (doi:10.1210/en.142.9.4120)
47. Le Romancer M, Poulard C, Cohen P, Sentis S, Renoir JM & Corbo L 2011 Cracking the estrogen receptor's posttranslational code in breast tumors. Endocrine Reviews 32 597-622. (doi:10.1210/er.2010-0016)
48. Leung Y, Mak P, Hassan S & Ho S 2006 Estrogen receptor (ER)-β isoforms: a key to understanding ER-β signaling. PNAS 103 13162-13167. (doi:10.1073/pnas.0605676103)
49. Leung YK, Lee MT, Lam HM, Tarapore P & Ho SM 2012 Estrogen receptor-β and breast cancer: translating biology into clinical practice. Steroids 77 727-737. (doi:10.1016/j.steroids.2012.03.008)
50. Levin ER 2012 Elusive extranuclear estrogen receptors in breast cancer. Clinical Cancer Research 18 6-8. (doi:10.1158/1078-0432.CCR-11-2547)
51. Levin ER & Pietras RJ 2008 Estrogen receptors outside the nucleus in breast cancer. Breast Cancer Research and Treatment 108 351-361. (doi:10.1007/s10549-007-9618-4)
52. Lewandowski S, Thiery J, Jalil A, Leclercq G, Szczylik C & Chouaib S 2005 Opposite effects of estrogen receptors α and β on MCF-7 sensitivity to the cytotoxic action of TNF and p53 activity. Oncogene 24 4789-4798. (doi:10.1038/sj.onc.1208595)
53. Leygue E & Murphy L 2011 Comparative evaluation of ERα and ERβ significance in breast cancer: state of the art. Expert Review of Endocrinology & Metabolism 6 333-343. (doi:10.1586/eem.11.27)
54. Leygue E, Dotzlaw H, Watson P & Murphy L 1998 Altered estrogen receptor a and b mRNA expression during human breast tumorigenesis. Cancer Research 58 3197-3201.
55. Leygue E, Dotzlaw H, Watson P & Murphy L 1999 Expression of estrogen receptor β1, β2, and β5 messenger RNAs in human breast tissue. Cancer Research 59 1175-1179.
56. Liu Y, Gao H, Marstrand TT, Strom A, Valen E, Sandelin A, Gustafsson JA & Dahlman-Wright K 2008 The genome landscape of ERα- and ERβ-binding DNA regions. PNAS 105 2604-2609. (doi:10.1073/pnas.0712085105)
57. Lonard DM, Lanz RB & O'Malley BW 2007 Nuclear receptor coregulators and human disease. Endocrine Reviews 28 575-587. (doi:10.1210/er.2007-0012)
58. von Maillot K, Gentsch HH & Gunselmann W 1980 Steroid receptors and response to endocrine treatment and chemotherapy of advanced breast cancer. Journal of Cancer Research and Clinical Oncology 98 301-313. (doi:10.1007/BF00410792)
59. Mak P, Leav I, Pursell B, Bae D, Yang X, Taglienti CA, Gouvin LM, Sharma VM & Mercurio AM 2010 ERβ impedes prostate cancer EMT by destabilizing HIF-1α and inhibiting VEGF-mediated snail nuclear localization: implications for Gleason grading. Cancer Cell 17 319-332. (doi:10.1016/j.ccr. 2010.02.030)
60. Mak P, Chang C, Pursell B & Mercurio AM 2013 Estrogen receptor b sustains epithelial differentiation by regulating prolyl hydroxylase 2 transcription. PNAS 110 4708-4713. (doi:10.1073/pnas.1221654110)
61. McKenna N, Lanz R & O'Malley B 1999 Nuclear receptor coregulators: cellular and molecular biology. Endocrine Reviews 20 321-344. (doi:10.1210/er.20.3.321)
62. Michael Miller KK, Al-Rayyan N, Ivanova MM, Mattingly KA, Ripp SL, Klinge CM & Prough RA 2012 DHEA metabolites activate estrogen receptors α and β. Steroids 78 15-25. (doi:10.1016/j.steroids. 2012.10.002)
63. Miller W, Anderson T, Dixon J & Saunders P 2006 Oestrogen receptor b and neoadjuvant therapy with tamoxifen: prediction of response and effects of treatment. British Journal of Cancer 94 1333-1338. (doi:10.1038/sj.bjc.6603082)
64. Monroe D, Secreto F, Subramaniam M, Getz B, Khosla S & Spelsberg T 2005 Estrogen receptor a and b heterodimers exert unique effects on estrogen- and tamoxifen-dependent gene expression in human U2OS osteosarcoma cells. Molecular Endocrinology 19 1555-1568. (doi:10.1210/me.2004-0381)
65. Murphy L & Watson P 2006 Is oestrogen receptor-β a predictor of endocrine therapy responsiveness in human breast cancer? Endocrine-Related Cancer 13 327-334. (doi:10.1677/erc.1.01141)
66. Murphy LC & Leygue E 2012 The role of estrogen receptor-β in breast cancer. Seminars in Reproductive Medicine 30 5-13. (doi:10.1055/s-0031- 1299592)
67. Murphy L, Cherlet T, Lewis A, Banu Y & Watson P 2003 New insights into estrogen receptor function in human breast cancer. Annals of Medicine 35 614-631. (doi:10.1080/07853890310014579)
68. Murphy L, Peng B, Lewis A, Davie J, Leygue E, Kemp A, Ung K, Vendetti M & Shiu R 2005 Inducible upregulation of oestrogen receptor-β1 affects oestrogen and tamoxifen responsiveness in MCF7 human breast cancer cells. Journal of Molecular Endocrinology 34 553-566. (doi:10.1677/jme.1.01688)
69. Muscat GE, Eriksson NA, Byth K, Loi S, Graham D, Jindal S, Davis MJ, Clyne C, Funder JW, Simpson ER et al. 2013 Research resource: nuclear receptors as transcriptome: discriminant and prognostic value in breast cancer. Molecular Endocrinology 27 350-365. (doi:10.1210/me.2012-1265)
70. Nassa G, Tarallo R, Ambrosino C, Bamundo A, Ferraro L, Paris O, Ravo M, Guzzi PH, Cannataro M, Baumann M et al. 2011 A large set of estrogen receptor b-interacting proteins identified by tandem affinity purification in hormone-responsive human breast cancer cell nuclei. Proteomics 11 159-165. (doi:10.1002/pmic.201000344)
71. Ni M, Chen Y, Lim E, Wimberly H, Bailey ST, Imai Y, Rimm DL, Liu XS & Brown M 2011 Targeting androgen receptor in estrogen receptornegative breast cancer. Cancer Cell 20 119-131. (doi:10.1016/j.ccr. 2011.05.026)
72. Novelli F, Milella M, Melucci E, Di Benedetto A, Sperduti I, Perrone-Donnorso R, Perracchio L, Venturo I, Nistico C, Fabi A et al. 2008 A divergent role for estrogen receptor-β in node-positive and nodenegative breast cancer classified according to molecular subtypes: an observational prospective study. Breast Cancer Research 10 R74. (doi:10.1186/bcr2139)
73. Ogawa S, Inoue S, Watanabe T, Orimo A, Hosoi T, Ouchi Y & Muramatsu M 1998 Molecular cloning and characterization of human estrogen receptor bcx: potential inhibitor of estrogen action in human. Nucleic Acids Research 26 3505-3512. (doi:10.1093/nar/26.15.3505)
74. O'Neill P, Davies M, Shaaban A, Innes H, Torevell A, Sibson D & Foster C 2004 Wild-type oestrogen receptor b (ERβ1) mRNA and protein expression in Tamoxifen-treated post-menopausal breast cancers. British Journal of Cancer 91 1694-1702.
75. Paech K, Webb P, Kuiper G, Nilsson S, Gustafsson J, Kushner PJ & Scanlan TS 1997 Differential ligand activation of estrogen receptors ERα and ERβ at AP1 sites. Science 277 1508-1510. (doi:10.1126/science.277.5331. 1508)
76. Palmieri G, Cheng G, Saji S, Zelada-Hedman M, Warri A, Weihua Z, Noorden AV, Wahlstrom T, Coombes R, Warner M et al. 2002 Estrogen receptor b in breast cancer. Endocrine-Related Cancer 9 1-13. (doi:10.1677/erc.0.0090001)
77. Paruthiyil S, Parmar H, Kerekatte V, Cunha G, Firestone G & Leitman D 2004 Estrogen receptor b inhibits human breast cancer cell proliferation and tumor formation by causing a G2 cell cycle arrest. Cancer Research 64 423-428. (doi:10.1158/0008-5472.CAN-03-2446)
78. Paruthiyil S, Cvoro A, Tagliaferri M, Cohen I, Shtivelman E & Leitman DC 2011 Estrogen receptor b causes a G2 cell cycle arrest by inhibiting CDK1 activity through the regulation of cyclin B1, GADD45A, and BTG2. Breast Cancer Research and Treatment 129 777-784. (doi:10.1007/s10549-010-1273-5)
79. Pedram A, Razandi M, Wallace D & Levin E 2006 Functional estrogen receptors in the mitochondria of breast cancer cells. Molecular Biology of the Cell 17 2125-2137. (doi:10.1091/mbc.E05-11-1013)
80. Peng B, Lu B, Leygue E & Murphy L 2003 Putative functional characteristics of human estrogen receptor-β isoforms. Journal of Molecular Endocrinology 30 13-29. (doi:10.1677/jme.0.0300013)
81. Picard N, Caron V, Bilodeau S, Sanchez M, Mascle X, Aubry M & Tremblay A 2012 Identification of estrogen receptor b as a SUMO-1 target reveals a novel phosphorylated sumoylation motif and regulation by glycogen synthase kinase 3β. Molecular and Cellular Biology 32 2709-2721. (doi:10.1128/MCB.06624-11)
82. Powell E, Shanle E, Brinkman A, Li J, Keles S, Wisinski KB, Huang W & Xu W 2012 Identification of estrogen receptor dimer selective ligands reveals growth-inhibitory effects on cells that co-express ERα and ERβ. PLoS ONE 7 e30993. (doi:10.1371/journal.pone.0030993)
83. Prins GS & Korach KS 2008 The role of estrogens and estrogen receptors in normal prostate growth and disease. Steroids 73 233-244. (doi:10.1016/j.steroids.2007.10.013)
84. Rae JM, Creighton CJ, Meck JM, Haddad BR & Johnson MD 2007 MDA-MB-435 cells are derived from M14 melanoma cells - a loss for breast cancer, but a boon for melanoma research. Breast Cancer Research and Treatment 104 13-19. (doi:10.1007/s10549-006-9392-8)
85. Razandi M, Pedram A, Jordan VC, Fuqua S & Levin ER 2012 Tamoxifen regulates cell fate through mitochondrial estrogen receptor b in breast cancer. Oncogene [in press]. (doi:10.1038/onc.2012.335)
86. Roger P, Sahla M, Makela S, Gustafsson JA, Baldet P & Rochefort H 2001 Decreased expression of estrogen receptor b protein in proliferative preinvasive mammary tumors. Cancer Research 61 2537-2541.
87. Rousseau C, Nichol J, Pettersson F, Couture M & Miller W 2004 ERβ sensitizes breast cancer cells to retinoic acid: evidence of transcriptional crosstalk. Molecular Cancer Research 2 523-531.
88. Saijo K, Collier JG, Li AC, Katzenellenbogen JA & Glass CK 2011 An ADIOL-ERβ-CtBP transrepression pathway negatively regulates microglia-mediated inflammation. Cell 145 584-595. (doi:10.1016/j.cell.2011.03. 050)
89. Saji S, Jensen E, Nilsson S, Rylander T, Warner M & Gustafsson J-A 2000 Estrogen receptors α and β in the rodent mammary gland. PNAS 97 337-342. (doi:10.1073/pnas.97.1.337)
90. Saji S, Omoto Y, Shimizu C, Horiguchi S, Watanabe T, Funata N, Hayash S, Gustafsson J & Toi M 2002a Clinical impact of assay of estrogen receptor b cx in breast cancer. Breast Cancer Research and Treatment 9 303-307.
91. Saji S, Omoto Y, Shimizu C, Warner M, Hayashi Y, Horiguchi S, Watanabe T, Hayashi S & Gustafsson J 2002b Expression of estrogen receptor (ER) (β)cx protein in ER(α)-positive breast cancer: specific correlation with progesterone receptor. Cancer Research 62 4849-4853.
92. Sanchez M, Picard N, Sauve K & Tremblay A 2010 Challenging estrogen receptor b with phosphorylation. Trends in Endocrinology and Metabolism 21 104-110. (doi:10.1016/j.tem.2009.09.007)
93. Sanchez M, Picard N, Sauve K & Tremblay A 2012 Coordinate regulation of estrogen receptor b degradation by Mdm2 and CREB-binding protein in response to growth signals. Oncogene 32 117-126. (doi:10.1038/onc.2012.19)
94. 2-terminal domain of the estrogen receptor b correlates with the survival of breast cancer patients. Cancer Research 66 2716-2724. (doi:10.1158/0008-5472.CAN-05-3592)
95. Secreto FJ, Monroe DG, Dutta S, Ingle JN & Spelsberg TC 2007 Estrogen receptor α/β isoforms, but not βcx, modulate unique patterns of gene expression and cell proliferation in Hs578T cells. Journal of Cellular Biochemistry 101 1125-1147. (doi:10.1002/jcb.21205)
96. Shaaban AM, Green AR, Karthik S, Alizadeh Y, Hughes TA, Harkins L, Ellis IO, Robertson JF, Paish EC, Saunders PT et al. 2008 Nuclear and cytoplasmic expression of ERβ1, ERβ2, and ERβ5 identifies distinct prognostic outcome for breast cancer patients. Clinical Cancer Research 14 5228-5235. (doi:10.1158/1078-0432.CCR-07-4528)
97. Shanle EK & Xu W 2010 Selectively targeting estrogen receptors for cancer treatment. Advanced Drug Delivery Reviews 62 1265-1276. (doi:10.1016/j.addr.2010.08.001)
98. Shanle EK, Hawse JR & Xu W 2011 Generation of stable reporter breast cancer cell lines for the identification of ER subtype selective ligands. Biochemical Pharmacology 82 1940-1949. (doi:10.1016/j.bcp. 2011.08.026)
99. Skliris G, Leygue E, Curtis-Snell L, Watson P & Murphy L 2006 Expression of oestrogen receptor-β in oestrogen receptor-α negative human breast tumours. British Journal of Cancer 95 616-626. (doi:10.1038/sj.bjc. 6603295)
100. Skliris G, Lewis A, Emberley E, Peng B, Weebadda W, Kemp A, Davie J, Shiu R, Watson P, Murphy L et al. 2007 Estrogen receptor-β regulates psoriasin (S100A7) in human breast cancer. Breast Cancer Research and Treatment 104 75-85. (doi:10.1007/s10549-006-9390-x)
101. Skliris GP, Nugent ZJ, Rowan BG, Penner CR, Watson PH & Murphy LC 2010 A phosphorylation code for oestrogen receptor-α predicts clinical outcome to endocrine therapy in breast cancer. Endocrine-Related Cancer 17 589-597. (doi:10.1677/ERC-10-0030)
102. Speirs V, Skliris G, Burdall S & Carder P 2002 Distinct expression patterns of ERα and ERβ in normal human mammary gland. Journal of Clinical Pathology 255 371-374. (doi:10.1136/jcp.55.5.371)
103. Stewart J, King R, Hayward J & Rubens R 1982 Estrogen and progesterone receptors: correlation of response rates, site and timing of receptor analysis. Breast Cancer Research and Treatment 2 243-250. (doi:10.1007/BF01806937)
104. Strom A, Hartman J, Foster J, Kietz S, Wimalasena J & Gustafsson J-A 2004 Estrogen receptor b inhibits 17b-estradiol-stimulated proliferation of the breast cancer cell line T-47D. PNAS 101 1566-1571. (doi:10.1073/pnas.0308319100)
105. Tateishi Y, Sonoo R, Sekiya Y, Sunahara N, Kawano M, Wayama M, Hirota R, Kawabe Y, Murayama A, Kato S et al. 2006 Turning off estrogen receptor b-mediated transcription requires estrogen-dependent receptor proteolysis. Molecular and Cellular Biology 26 7966-7976. (doi:10.1128/MCB.00713-06)
106. Thomas C & Gustafsson JA 2011 The different roles of ER subtypes in cancer biology and therapy. Nature Reviews. Cancer 11 597-608. (doi:10.1038/nrc3093)
107. Thomas C & Gustafsson JA 2012 Targeting PES1 for restoring the ERα/ERβ ratio in breast cancer. Journal of Clinical Investigation 122 2771-2773. (doi:10.1172/JCI65133)
108. Thomas C, Rajapaksa G, Nikolos F, Hao R, Katchy A, McCollum CW, Bondesson M, Quinlan P, Thompson A, Krishnamurthy S et al. 2012 ERβ1 represses basal breast cancer epithelial to mesenchymal transition by destabilizing EGFR. Breast Cancer Research 14 R148. (doi:10.1186/bcr3358)
109. Tonetti D, Rubenstein R, Deleon M, Zhao H, Pappas S, Bentrem D, Chen B, Constantinou A & Jordan V 2003 Stable transfection of an estrogen receptor b cDNA isoform into MDAMB231 breast cancer cells. Journal of Steroid Biochemistry and Molecular Biology 87 47-55. (doi:10.1016/j.jsbmb.2003.07.003)
110. Treeck O, Lattrich C, Springwald A & Ortmann O 2010 Estrogen receptor b exerts growth-inhibitory effects on human mammary epithelial cells. Breast Cancer Research and Treatment 120 557-565. (doi:10.1007/s10549-009-0413-2)
111. Trialists' EBC 1992 Systemic treatment of early breast cancer by hormonal, cytotoxic, or immune therapy, 133 randomised trials involving 31 000 recurrences and 24 000 deaths among 75 000 women. Early Breast Cancer Trialists'. Lancet 339 1-15.
112. Trialists' EBC 1998 Tamoxifen for early breast cancer: an overview of the randomised trials. Early Breast Cancer Trialists' Collaborative Group. Lancet 351 1451-1467. (doi:10.1016/S0140-6736(97)11423-4)
113. Vivar OI, Zhao X, Saunier EF, Griffin C, Mayba OS, Tagliaferri M, Cohen I, Speed TP & Leitman DC 2010 Estrogen receptor b binds to and regulates three distinct classes of target genes. Journal of Biological Chemistry 285 22059-22066. (doi:10.1074/jbc.M110.114116)
114. Weihua Z, Saji S, Makinen S, Cheng G, Jensen E, Warner M & Gustaffson J-A 2000 Estrogen receptor (ER) b, a modulator of ERα in the uterus. PNAS 97 5936-5941. (doi:10.1073/pnas.97.11.5936)
115. Welsh AW, Lannin DR, Young GS, Sherman ME, Figueroa JD, Henry NL, Ryden L, Kim C, Love RR, Schiff R et al. 2012 Cytoplasmic estrogen receptor in breast cancer. Clinical Cancer Research 18 118-126. (doi:10.1158/1078-0432.CCR-11-1236)
116. Williams C, Edvardsson K, Lewandowski SA, Strom A & Gustafsson JA 2008 A genome-wide study of the repressive effects of estrogen receptor b on estrogen receptor a signaling in breast cancer cells. Oncogene 27 1019-1032. (doi:10.1038/sj.onc.1210712)
117. Wu X, Subramaniam M, Grygo SB, Sun Z, Negron V, Lingle WL, Goetz MP, Ingle JN, Spelsberg TC & Hawse JR 2011 Estrogen receptor-β sensitizes breast cancer cells to the anti-estrogenic actions of endoxifen. Breast Cancer Research 13 R27. (doi:10.1186/bcr2844)
118. Yan M, Rayoo M, Takano EA & Fox SB 2011 Nuclear and cytoplasmic expressions of ERβ1 and ERβ2 are predictive of response to therapy and alters prognosis in familial breast cancers. Breast Cancer Research and Treatment 126 395-405. (doi:10.1007/s10549-010-0941-9)
119. Yan Y, Li X, Blanchard A, Bramwell VHC, Pritchard KI, Tu D, Shepherd L, Myal Y, Penner C, Watson PH et al. 2013 Expression of both estrogen receptor-β 1 (ER-β1) and its co-regulator steroid receptor RNA activator protein (SRAP) are predictive for benefit from tamoxifen therapy in patients with estrogen receptor-α (ER-α) negative early breast cancer (EBC). Annals of Oncology [in press]. (doi:10.1093/annonc/mdt132)
120. Zhao C, Matthews J, Tujague M, Wan J, Strom A, Toresson G, Lam EW, Cheng G, Gustafsson JA & Dahlman-Wright K 2007 Estrogen receptor b2 negatively regulates the transactivation of estrogen receptor a in human breast cancer cells. Cancer Research 67 3955-3962. (doi:10.1158/0008-5472.CAN-06-3505)
121. Zhao C, Gao H, Liu Y, Papoutsi Z, Jaffrey S, Gustafsson JA & Dahlman-Wright K 2010 Genome-wide mapping of estrogen receptor-β-binding regions reveals extensive cross-talk with transcription factor activator protein-1. Cancer Research 70 5174-5183. (doi:10.1158/0008-5472. CAN-09-4407)
122. Zwart W, Theodorou V & Carroll JS 2011 Estrogen receptor-positive breast cancer: a multidisciplinary challenge. Wiley Interdisciplinary Reviews. Systems Biology and Medicine 3 216-230. (doi:10.1002/wsbm.109)