Pathophysiological roles of ERα in the ER signaling mediated oncogenesis of breast cancer
DOI:
https://doi.org/10.15584/ejcem.2020.4.6Keywords:
breast, cancer, estrogen receptor alpha, oncogenesisAbstract
Introduction. Estrogen receptors (ER) are members of nuclear receptors that act in the ER signaling pathway regulating the pathophysiology of hormone-responsive target cells including breast tissue.
Aim. This detailled review literature was written on the pathophysiology of ER signaling as well as the effect altered ERα and associated pathway derangement in the oncogenesis of breast cancer.
Material and methods. This review was performed according to systematic literature search of three major bibliographic databases (Scopus, PubMed, and Cochran).
Analysis of the literature. In this pathway, estrogen receptor alpha (ERα) is a key estradiol-17β (E2) induced transcription factor that has been implicated in the initiation and development of the major fraction of breast cancers. Hence understanding the ERα-mediated ER signaling that results in alterations from normal phenotypic features of breast tissue to the oncogenic features of breast cancer is important. The oncogenic effect of ERα in ER signaling is driven by combinations of molecular assets within the cancer cells. Normally, the transcriptional activity of ERα is controlled by tight regulation of its protein level inside the cells. Altered stability and activity of ERα due to its phosphorylation, ubiquitination, glycosylation, sumoylation, and acetylation events can trigger oncogenic ER signaling.
Conclusion. The function and activity of ERα is also modulated by its interaction with coregulators as well as crosstalk with oncogenic factors from other oncogenic pathways. These all events increase the complexity of the progression of ER+ breast cancer and its response to endocrine therapy.
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Vlahopoulos SA, Cen O, Hengen N, et al. Dynamic aberrant NF-kappaB spurs tumorigenesis: a new model encompassing the microenvironment. Cytokine Growth Factor Rev. 2015;26(4):389-403.
Wang K, Grivennikov SI, Karin M. Implications of anti-cytokine therapy in colorectal cancer and autoimmune diseases. Ann Rheum Dis. 2013;72, 2:ii100-103.
Sanchez-Vega F, Mina M, Armenia J, et al. Oncogenic Signaling Pathways in The Cancer Genome Atlas. Cell. 2018;173(2):321-337 e310.
Sawyers C. Targeted cancer therapy. Nature. 2004;432(7015):294-297.
Gruber CJ, Tschugguel W, Schneeberger C, Huber JC. Production and actions of estrogens. N Engl J Med. 2002;346(5):340-352.
Nelson LR, Bulun SE. Estrogen production and action. J Am Acad Dermatol. 2001;45(3):116-124.
Feng Q, Zhang Y. The NuRD complex: linking histone modification to nucleosome remodeling. Curr Top Microbiol Immunol. 2003;274:269-290.
Sharma D, Blum J, Yang X, Beaulieu N, Macleod AR, Davidson NE. Release of methyl CpG binding proteins and histone deacetylase 1 from the Estrogen receptor alpha (ER) promoter upon reactivation in ER-negative human breast cancer cells. Mol Endocrinol. 2005;19(7):1740-1751.
Garcia-Becerra R, Santos N, Diaz L, Camacho J. Mechanisms of resistance to endocrine therapy in breast cancer: focus on signaling pathways, miRNAs and genetically based resistance. Int J Mol Sci. 2012;14(1):108-145.
Barone I, Cui Y, Herynk MH, et al. Expression of the K303R estrogen receptor-alpha breast cancer mutation induces resistance to an aromatase inhibitor via addiction to the PI3K/Akt kinase pathway. Cancer Res. 2009;69(11):4724-4732.
Li Y, Meeran SM, Patel SN, Chen H, Hardy TM, Tollefsbol TO. Epigenetic reactivation of estrogen receptor-alpha (ERalpha) by genistein enhances hormonal therapy sensitivity in ERalpha-negative breast cancer. Mol Cancer. 2013;12:9.
Robinson DR, Wu YM, Vats P, et al. Activating ESR1 mutations in hormone-resistant metastatic breast cancer. Nat Genet. 2013;45(12):1446-1451.
Giuliano M, Trivedi MV, Schiff R. Bidirectional Crosstalk between the Estrogen Receptor and Human Epidermal Growth Factor Receptor 2 Signaling Pathways in Breast Cancer: Molecular Basis and Clinical Implications. Breast Care (Basel). 2013;8(4):256-262.
Levin ER. Bidirectional signaling between the estrogen receptor and the epidermal growth factor receptor. Molecular endocrinology. 2003;17(3):309-317.
Trevino LS, Weigel NL. Phosphorylation: a fundamental regulator of steroid receptor action. Trends Endocrinol Metab. 2013;24(10):515-524.
Anbalagan M, Huderson B, Murphy L, Rowan BG. Post-translational modifications of nuclear receptors and human disease. Nucl Recept Signal. 2012;10:e001.
Le Romancer M, Poulard C, Cohen P, Sentis S, Renoir JM, Corbo L. Cracking the estrogen receptor's posttranslational code in breast tumors. Endocr Rev. 2011;32(5):597-622.
Zhou W, Slingerland JM. Links between oestrogen receptor activation and proteolysis: relevance to hormone-regulated cancer therapy. Nat Rev Cancer. 2014;14(1):26-38.
Leung YK, Lee MT, Lam HM, Tarapore P, Ho SM. Estrogen receptor-beta and breast cancer: translating biology into clinical practice. Steroids. 2012;77(7):727-737.
Green KA, Carroll JS. Oestrogen-receptor-mediated transcription and the influence of co-factors and chromatin state. Nat Rev Cancer. 2007;7(9):713-722.
Lonard DM, O'Malley BW. The expanding cosmos of nuclear receptor coactivators. Cell. 2006;125(3):411-414.
Yamnik RL, Digilova A, Davis DC, Brodt ZN, Murphy CJ, Holz MK. S6 kinase 1 regulates estrogen receptor alpha in control of breast cancer cell proliferation. J Biol Chem. 2009;284(10):6361-6369.
Mann M, Krishnan S, Vadlamudi RK. Emerging significance of estrogen cancer coregulator signaling in breast cancer. Minerva Ginecol. 2012;64(1):75-88.
Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61(2):69-90.
Clegg LX, Reichman ME, Miller BA, et al. Impact of socioeconomic status on cancer incidence and stage at diagnosis: selected findings from the surveillance, epidemiology, and end results: National Longitudinal Mortality Study. Cancer Causes Control. 2009;20(4):417-435.
Ghoncheh M, Pournamdar Z, Salehiniya H. Incidence and Mortality and Epidemiology of Breast Cancer in the World. Asian Pac J Cancer Prev. 2016;17(3):43-46.
Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65(2):87-108.
Pruthi S. Detection and evaluation of a palpable breast mass. Mayo Clin Proc. 2001;76(6):641-647;647-648.
Bevers TB, Anderson BO, Bonaccio E, et al. NCCN clinical practice guidelines in oncology: breast cancer screening and diagnosis. J Natl Compr Canc Netw. 2009;7(10):1060-1096.
Malhotra GK, Zhao X, Band H, Band V. Histological, molecular and functional subtypes of breast cancers. Cancer Biol Ther. 2010;10(10):955-960.
Recommendations for the reporting of breast carcinoma. Association of Directors of Anatomic and Surgical Pathology. Am J Clin Pathol. 1995;104(6):614-619.
Hon JD, Singh B, Sahin A, et al. Breast cancer molecular subtypes: from TNBC to QNBC. Am J Cancer Res. 2016;6(9):1864-1872.
Sorlie T, Perou CM, Tibshirani R, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proceedings of the National Academy of Sciences of the United States of America. 2001;98(19):10869-10874.
Sorlie T, Tibshirani R, Parker J, et al. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proceedings of the National Academy of Sciences of the United States of America. 2003;100(14):8418-8423.
Perou CM, Sorlie T, Eisen MB, et al. Molecular portraits of human breast tumours. Nature. 2000;406(6797):747-752.
Pfefferle AD, Spike BT, Wahl GM, Perou CM. Luminal progenitor and fetal mammary stem cell expression features predict breast tumor response to neoadjuvant chemotherapy. Breast Cancer Res Treat. 2015;149(2):425-437.
Visvader JE. Keeping abreast of the mammary epithelial hierarchy and breast tumorigenesis. Genes Dev. 2009;23(22):2563-2577.
Spike BT, Engle DD, Lin JC, Cheung SK, La J, Wahl GM. A mammary stem cell population identified and characterized in late embryogenesis reveals similarities to human breast cancer. Cell Stem Cell. 2012;10(2):183-197.
Brough R, Frankum JR, Sims D, et al. Functional viability profiles of breast cancer. Cancer Discov. 2011;1(3):260-273.
Riggins RB, Schrecengost RS, Guerrero MS, Bouton AH. Pathways to tamoxifen resistance. Cancer Lett. 2007;256(1):1-24.
Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet. 2005;365(9472):1687-1717.
Forbes JF, Cuzick J, Buzdar A, Howell A, Tobias JS, Baum M. Effect of anastrozole and tamoxifen as adjuvant treatment for early-stage breast cancer: 100-month analysis of the ATAC trial. Lancet Oncol. 2008;9(1):45-53.
Thurlimann B, Keshaviah A, Coates AS, et al. A comparison of letrozole and tamoxifen in postmenopausal women with early breast cancer. N Engl J Med. 2005;353(26):2747-2757.
Early Breast Cancer Trialists' Collaborative G. Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet. 2005;365(9472):1687-1717.
Pagani O, Price KN, Gelber RD, et al. Patterns of recurrence of early breast cancer according to estrogen receptor status: a therapeutic target for a quarter of a century. Breast Cancer Res Treat. 2009;117(2):319-324.
Osborne CK, Bardou V, Hopp TA, 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. 2003;95(5):353-361.
Zhang Y, Moerkens M, Ramaiahgari S, et al. Elevated insulin-like growth factor 1 receptor signaling induces antiestrogen resistance through the MAPK/ERK and PI3K/Akt signaling routes. Breast Cancer Res. 2011;13(3):R52.
Turner N, Pearson A, Sharpe R, et al. FGFR1 amplification drives endocrine therapy resistance and is a therapeutic target in breast cancer. Cancer Res. 2010;70(5):2085-2094.
Gilani RA, Kazi AA, Shah P, et al. The importance of HER2 signaling in the tumor-initiating cell population in aromatase inhibitor-resistant breast cancer. Breast Cancer Res Treat. 2012;135(3):681-692.
Burris HA, 3rd. Overcoming acquired resistance to anticancer therapy: focus on the PI3K/AKT/mTOR pathway. Cancer Chemother Pharmacol. 2013;71(4):829-842.
Planas-Silva MD, Bruggeman RD, Grenko RT, Smith JS. Overexpression of c-Myc and Bcl-2 during progression and distant metastasis of hormone-treated breast cancer. Exp Mol Pathol. 2007;82(1):85-90.
van Agthoven T, van Agthoven TL, Dekker A, van der Spek PJ, Vreede L, Dorssers LC. Identification of BCAR3 by a random search for genes involved in antiestrogen resistance of human breast cancer cells. Embo J. 1998;17(10):2799-2808.
Schroth W, Goetz MP, Hamann U, et al. Association between CYP2D6 polymorphisms and outcomes among women with early stage breast cancer treated with tamoxifen. JAMA. 2009;302(13):1429-1436.
Liu L, Bai YX, Zhou JH, et al. A polymorphism at the 3'-UTR region of the aromatase gene is associated with the efficacy of the aromatase inhibitor, anastrozole, in metastatic breast carcinoma. Int J Mol Sci. 2013;14(9):18973-18988.
Michalides R, Griekspoor A, Balkenende A, et al. Tamoxifen resistance by a conformational arrest of the estrogen receptor alpha after PKA activation in breast cancer. Cancer Cell. 2004;5(6):597-605.
Berry DA, Cirrincione C, Henderson IC, et al. Estrogen-receptor status and outcomes of modern chemotherapy for patients with node-positive breast cancer. JAMA. 2006;295(14):1658-1667.
Petit T, Wilt M, Velten M, et al. Semi-quantitative evaluation of estrogen receptor expression is a strong predictive factor of pathological complete response after anthracycline-based neo-adjuvant chemotherapy in hormonal-sensitive breast cancer. Breast Cancer Res Treat. 2010;124(2):387-391.
Sui M, Huang Y, Park BH, Davidson NE, Fan W. Estrogen receptor alpha mediates breast cancer cell resistance to paclitaxel through inhibition of apoptotic cell death. Cancer Res. 2007;67(11):5337-5344.
Tabuchi Y, Matsuoka J, Gunduz M, et al. Resistance to paclitaxel therapy is related with Bcl-2 expression through an estrogen receptor mediated pathway in breast cancer. Int J Oncol. 2009;34(2):313-319.
Green S, Walter P, Kumar V, et al. Human oestrogen receptor cDNA: sequence, expression and homology to v-erb-A. Nature. 1986;320(6058):134-139.
Mosselman S, Polman J, Dijkema R. ER beta: identification and characterization of a novel human estrogen receptor. FEBS Lett. 1996;392(1):49-53.
Evans RM. The steroid and thyroid hormone receptor superfamily. Science. 1988;240(4854):889-895.
Ribeiro RC, Kushner PJ, Baxter JD. The nuclear hormone receptor gene superfamily. Annu Rev Med. 1995;46:443-453.
Zhou Z, Qiao JX, Shetty A, et al. Regulation of estrogen receptor signaling in breast carcinogenesis and breast cancer therapy. Cell Mol Life Sci. 2014;71(8):1549.
Marino M, Ascenzi P, Acconcia F. S-palmitoylation modulates estrogen receptor alpha localization and functions. Steroids. 2006;71(4):298-303.
Galluzzo P, Ascenzi P, Bulzomi P, Marino M. The nutritional flavanone naringenin triggers antiestrogenic effects by regulating estrogen receptor alpha-palmitoylation. Endocrinology. 2008;149(5):2567-2575.
Razandi M, Pedram A, Park ST, Levin ER. Proximal events in signaling by plasma membrane estrogen receptors. The Journal of biological chemistry. 2003;278(4):2701-2712.
Sanchez AM, Flamini MI, Baldacci C, Goglia L, Genazzani AR, Simoncini T. Estrogen receptor-alpha promotes breast cancer cell motility and invasion via focal adhesion kinase and N-WASP. Molecular endocrinology. 2010;24(11):2114-2125.
Adlanmerini M, Solinhac R, Abot A, et al. Mutation of the palmitoylation site of estrogen receptor alpha in vivo reveals tissue-specific roles for membrane versus nuclear actions. Proceedings of the National Academy of Sciences of the United States of America. 2014;111(2):E283-290.
Pedram A, Razandi M, Lewis M, Hammes S, Levin ER. Membrane-localized estrogen receptor alpha is required for normal organ development and function. Dev Cell. 2014;29(4):482-490.
Chen JQ, Cammarata PR, Baines CP, Yager JD. Regulation of mitochondrial respiratory chain biogenesis by estrogens/estrogen receptors and physiological, pathological and pharmacological implications. Biochim Biophys Acta. 2009;1793(10):1540-1570.
Klinge CM. Estrogenic control of mitochondrial function and biogenesis. J Cell Biochem. 2008;105(6):1342-1351.
Monje P, Boland R. Subcellular distribution of native estrogen receptor alpha and beta isoforms in rabbit uterus and ovary. J Cell Biochem. 2001;82(3):467-479.
Simpkins JW, Yang SH, Sarkar SN, Pearce V. Estrogen actions on mitochondria--physiological and pathological implications. Mol Cell Endocrinol. 2008;290(1-2):51-59.
Chen JQ, Yager JD, Russo J. Regulation of mitochondrial respiratory chain structure and function by estrogens/estrogen receptors and potential physiological/pathophysiological implications. Biochim Biophys Acta. 2005;1746(1):1-17.
Pedram A, Razandi M, Wallace DC, Levin ER. Functional estrogen receptors in the mitochondria of breast cancer cells. Mol Biol Cell. 2006;17(5):2125-2137.
Papa L, Germain D. Estrogen receptor mediates a distinct mitochondrial unfolded protein response. J Cell Sci. 2011;124(Pt 9):1396-1402.
Germain D. Estrogen carcinogenesis in breast cancer. Endocrinol Metab Clin North Am. 2011;40(3):473-484, vii.
Echeverria PC, Picard D. Molecular chaperones, essential partners of steroid hormone receptors for activity and mobility. Biochim Biophys Acta. 2010;1803(6):641-649.
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. 1988;7(10):3037-3044.
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. 1989;338(6212):271-274.
Kumar V, Green S, Stack G, Berry M, Jin JR, Chambon P. Functional domains of the human estrogen receptor. Cell. 1987;51(6):941-951.
Schwabe JW, Chapman L, Rhodes D. The oestrogen receptor recognizes an imperfectly palindromic response element through an alternative side-chain conformation. Structure. 1995;3(2):201-213.
Hall JM, McDonnell DP, Korach KS. Allosteric regulation of estrogen receptor structure, function, and coactivator recruitment by different estrogen response elements. Molecular endocrinology. 2002;16(3):469-486.
Freedman LP, Luisi BF. On the mechanism of DNA binding by nuclear hormone receptors: a structural and functional perspective. J Cell Biochem. 1993;51(2):140-150.
Shang Y, Hu X, DiRenzo J, Lazar MA, Brown M. Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell. 2000;103(6):843-852.
Yasar P, Ayaz G, User SD, Gupur G, Muyan M. Molecular mechanism of estrogen-estrogen receptor signaling. Reprod Med Biol. 2017;16(1):4-20.
Cui J, Shen Y, Li R. Estrogen synthesis and signaling pathways during aging: from periphery to brain. Trends Mol Med. 2013;19(3):197-209.
Huang J, Li X, Hilf R, Bambara RA, Muyan M. Molecular basis of therapeutic strategies for breast cancer. Curr Drug Targets Immune Endocr Metabol Disord. 2005;5(4):379-396.
Hall JM, Couse JF, Korach KS. The multifaceted mechanisms of estradiol and estrogen receptor signaling. The Journal of biological chemistry. 2001;276(40):36869-36872.
Kushner PJ, Agard DA, Greene GL, et al. Estrogen receptor pathways to AP-1. J Steroid Biochem Mol Biol. 2000;74(5):311-317.
Safe S. Transcriptional activation of genes by 17 beta-estradiol through estrogen receptor-Sp1 interactions. Vitam Horm. 2001;62:231-252.
Bjornstrom L, Sjoberg M. Mutations in the estrogen receptor DNA-binding domain discriminate between the classical mechanism of action and cross-talk with Stat5b and activating protein 1 (AP-1). The Journal of biological chemistry. 2002;277(50):48479-48483.
Cheung E, Acevedo ML, Cole PA, Kraus WL. Altered pharmacology and distinct coactivator usage for estrogen receptor-dependent transcription through activating protein-1. Proceedings of the National Academy of Sciences of the United States of America. 2005;102(3):559-564.
Karin M, Liu Z, Zandi E. AP-1 function and regulation. Curr Opin Cell Biol. 1997;9(2):240-246.
Safe S, Abdelrahim M. Sp transcription factor family and its role in cancer. Eur J Cancer. 2005;41(16):2438-2448.
Nott SL, Huang Y, Li X, et al. Genomic responses from the estrogen-responsive element-dependent signaling pathway mediated by estrogen receptor alpha are required to elicit cellular alterations. The Journal of biological chemistry. 2009;284(22):15277-15288.
Ahlbory-Dieker DL, Stride BD, Leder G, et al. DNA binding by estrogen receptor-alpha is essential for the transcriptional response to estrogen in the liver and the uterus. Molecular endocrinology. 2009;23(10):1544-1555.
Walker VR, Korach KS. Estrogen receptor knockout mice as a model for endocrine research. Ilar J. 2004;45(4):455-461.
Wang LH, Yang XY, Zhang X, Mihalic K, Xiao W, Farrar WL. The cis decoy against the estrogen response element suppresses breast cancer cells via target disrupting c-fos not mitogen-activated protein kinase activity. Cancer research. 2003;63(9):2046-2051.
Gibson DA, Saunders PT. Estrogen dependent signaling in reproductive tissues - a role for estrogen receptors and estrogen related receptors. Mol Cell Endocrinol. 2012;348(2):361-372.
Muyan M, Gupur G, Yasar P, et al. Modulation of Estrogen Response Element-Driven Gene Expressions and Cellular Proliferation with Polar Directions by Designer Transcription Regulators. PLoS One. 2015;10(8):e0136423.
Kumar R, Thompson EB. Transactivation functions of the N-terminal domains of nuclear hormone receptors: protein folding and coactivator interactions. Molecular endocrinology. 2003;17(1):1-10.
Tora L, White J, Brou C, et al. The human estrogen receptor has two independent nonacidic transcriptional activation functions. Cell. 1989;59(3):477-487.
Metzger D, Ali S, Bornert JM, Chambon P. Characterization of the amino-terminal transcriptional activation function of the human estrogen receptor in animal and yeast cells. The Journal of biological chemistry. 1995;270(16):9535-9542.
Bocquel MT, Kumar V, Stricker C, Chambon P, Gronemeyer H. The contribution of the N- and C-terminal regions of steroid receptors to activation of transcription is both receptor and cell-specific. Nucleic acids research. 1989;17(7):2581-2595.
Tasset D, Tora L, Fromental C, Scheer E, Chambon P. Distinct classes of transcriptional activating domains function by different mechanisms. Cell. 1990;62(6):1177-1187.
Rajbhandari P, Finn G, Solodin NM, et al. Regulation of estrogen receptor alpha N-terminus conformation and function by peptidyl prolyl isomerase Pin1. Mol Cell Biol. 2012;32(2):445-457.
Yi P, Bhagat S, Hilf R, Bambara RA, Muyan M. Differences in the abilities of estrogen receptors to integrate activation functions are critical for subtype-specific transcriptional responses. Molecular endocrinology. 2002;16(8):1810-1827.
Cowley SM, Parker MG. A comparison of transcriptional activation by ER alpha and ER beta. J Steroid Biochem Mol Biol. 1999;69(1-6):165-175.
Delaunay F, Pettersson K, Tujague M, Gustafsson JA. Functional differences between the amino-terminal domains of estrogen receptors alpha and beta. Mol Pharmacol. 2000;58(3):584-590.
Huang J, Li X, Maguire CA, Hilf R, Bambara RA, Muyan M. Binding of estrogen receptor beta to estrogen response element in situ is independent of estradiol and impaired by its amino terminus. Molecular endocrinology. 2005;19(11):2696-2712.
Teyssier C, Belguise K, Galtier F, Chalbos D. Characterization of the physical interaction between estrogen receptor alpha and JUN proteins. The Journal of biological chemistry. 2001;276(39):36361-36369.
Berry NB, Fan M, Nephew KP. Estrogen receptor-alpha hinge-region lysines 302 and 303 regulate receptor degradation by the proteasome. Molecular endocrinology. 2008;22(7):1535-1551.
Tamrazi A, Carlson KE, Daniels JR, Hurth KM, Katzenellenbogen JA. Estrogen receptor dimerization: ligand binding regulates dimer affinity and dimer dissociation rate. Molecular endocrinology. 2002;16(12):2706-2719.
Vajdos FF, Hoth LR, Geoghegan KF, et al. The 2.0 A crystal structure of the ERalpha ligand-binding domain complexed with lasofoxifene. Protein Sci. 2007;16(5):897-905.
Brzozowski AM, Pike AC, Dauter Z, et al. Molecular basis of agonism and antagonism in the oestrogen receptor. Nature. 1997;389(6652):753-758.
Pike AC, Brzozowski AM, Hubbard RE. A structural biologist's view of the oestrogen receptor. J Steroid Biochem Mol Biol. 2000;74(5):261-268.
Shiau AK, Barstad D, Loria PM, et al. The structural basis of estrogen receptor/coactivator recognition and the antagonism of this interaction by tamoxifen. Cell. 1998;95(7):927-937.
Emmen JM, Korach KS. Estrogen receptor knockout mice: phenotypes in the female reproductive tract. Gynecol Endocrinol. 2003;17(2):169-176.
Hwang CJ, Yun HM, Park KR, et al. Memory Impairment in Estrogen Receptor alpha Knockout Mice Through Accumulation of Amyloid-beta Peptides. Mol Neurobiol. 2015;52(1):176-186.
Cheng CK, Chow BK, Leung PC. An activator protein 1-like motif mediates 17beta-estradiol repression of gonadotropin-releasing hormone receptor promoter via an estrogen receptor alpha-dependent mechanism in ovarian and breast cancer cells. Mol Endocrinol. 2003;17(12):2613-2629.
Jones LP, Tilli MT, Assefnia S, et al. Activation of estrogen signaling pathways collaborates with loss of Brca1 to promote development of ERalpha-negative and ERalpha-positive mammary preneoplasia and cancer. Oncogene. 2008;27(6):794-802.
Yang M, Wang J, Wang L, et al. Estrogen induces androgen-repressed SOX4 expression to promote progression of prostate cancer cells. Prostate. 2015;75(13):1363-1375.
Yager JD, Davidson NE. Estrogen carcinogenesis in breast cancer. N Engl J Med. 2006;354(3):270-282.
Yue W, Wang JP, Li Y, et al. Effects of estrogen on breast cancer development: Role of estrogen receptor independent mechanisms. Int J Cancer. 2010;127(8):1748-1757.
Zhu J, Zhao C, Kharman-Biz A, et al. The atypical ubiquitin ligase RNF31 stabilizes estrogen receptor alpha and modulates estrogen-stimulated breast cancer cell proliferation. Oncogene. 2014;33(34):4340-4351.
Zhuang T, Yu S, Zhang L, et al. SHARPIN stabilizes estrogen receptor alpha and promotes breast cancer cell proliferation. Oncotarget. 2017;8(44):77137-77151.
Tecalco-Cruz AC, Ramirez-Jarquin JO. Mechanisms that Increase Stability of Estrogen Receptor Alpha in Breast Cancer. Clin Breast Cancer. 2017;17(1):1-10.
Williams CC, Basu A, El-Gharbawy A, Carrier LM, Smith CL, Rowan BG. Identification of four novel phosphorylation sites in estrogen receptor alpha: impact on receptor-dependent gene expression and phosphorylation by protein kinase CK2. BMC Biochem. 2009;10:36.
Murphy LC, Seekallu SV, Watson PH. Clinical significance of estrogen receptor phosphorylation. Endocr Relat Cancer. 2011;18(1):R1-14.
He X, Zheng Z, Song T, et al. c-Abl regulates estrogen receptor alpha transcription activity through its stabilization by phosphorylation. Oncogene. 2010;29(15):2238-2251.
Giamas G, Filipovic A, Jacob J, et al. Kinome screening for regulators of the estrogen receptor identifies LMTK3 as a new therapeutic target in breast cancer. Nat Med. 2011;17(6):715-719.
Tecalco-Cruz AC, Ramirez-Jarquin JO. Mechanisms that Increase Stability of Estrogen Receptor Alpha in Breast Cancer. Clin Breast Cancer. 2017;17(1):1-10.
Grisouard J, Medunjanin S, Hermani A, Shukla A, Mayer D. Glycogen synthase kinase-3 protects estrogen receptor alpha from proteasomal degradation and is required for full transcriptional activity of the receptor. Molecular endocrinology. 2007;21(10):2427-2439.
Zhao G, Guo J, Li D, et al. MicroRNA-34a suppresses cell proliferation by targeting LMTK3 in human breast cancer mcf-7 cell line. DNA Cell Biol. 2013;32(12):699-707.
Wei X, Xu H, Kufe D. MUC1 oncoprotein stabilizes and activates estrogen receptor alpha. Mol Cell. 2006;21(2):295-305.
Rajbhandari P, Schalper KA, Solodin NM, et al. Pin1 modulates ERalpha levels in breast cancer through inhibition of phosphorylation-dependent ubiquitination and degradation. Oncogene. 2014;33(11):1438-1447.
Xue M, Zhang K, Mu K, et al. Regulation of estrogen signaling and breast cancer proliferation by an ubiquitin ligase TRIM56. Oncogenesis. 2019;8(5):30.
Caligiuri I, Toffoli G, Giordano A, Rizzolio F. pRb controls estrogen receptor alpha protein stability and activity. Oncotarget. 2013;4(6):875-883.
Lannigan DA. Estrogen receptor phosphorylation. Steroids. 2003;68(1):1-9.
Likhite VS, Stossi F, Kim K, Katzenellenbogen BS, Katzenellenbogen JA. Kinase-specific phosphorylation of the estrogen receptor changes receptor interactions with ligand, deoxyribonucleic acid, and coregulators associated with alterations in estrogen and tamoxifen activity. Mol Endocrinol. 2006;20(12):3120-3132.
de Leeuw R, Neefjes J, Michalides R. A role for estrogen receptor phosphorylation in the resistance to tamoxifen. Int J Breast Cancer. 2011;2011:232435.
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. 2002;21(32):4921-4931.
Sarwar N, Kim JS, Jiang J, et al. Phosphorylation of ERalpha at serine 118 in primary breast cancer and in tamoxifen-resistant tumours is indicative of a complex role for ERalpha phosphorylation in breast cancer progression. Endocr Relat Cancer. 2006;13(3):851-861.
Yamashita H, Nishio M, Toyama T, et al. Low phosphorylation of estrogen receptor alpha (ERalpha) serine 118 and high phosphorylation of ERalpha serine 167 improve survival in ER-positive breast cancer. Endocr Relat Cancer. 2008;15(3):755-763.
Gee JM, Robertson JF, Ellis IO, Nicholson RI. 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. 2001;95(4):247-254.
Liu H, Qiu J, Li N, Chen T, Cao X. Human phosphatidylethanolamine-binding protein 4 promotes transactivation of estrogen receptor alpha (ERalpha) in human cancer cells by inhibiting proteasome-dependent ERalpha degradation via association with Src. J Biol Chem. 2010;285(29):21934-21942.
Cui Y, Zhang M, Pestell R, Curran EM, Welshons WV, Fuqua SA. Phosphorylation of estrogen receptor alpha blocks its acetylation and regulates estrogen sensitivity. Cancer Res. 2004;64(24):9199-9208.
La Rosa P, Pesiri V, Leclercq G, Marino M, Acconcia F. Palmitoylation regulates 17beta-estradiol-induced estrogen receptor-alpha degradation and transcriptional activity. Mol Endocrinol. 2012;26(5):762-774.
Cheng X, Cole RN, Zaia J, Hart GW. Alternative O-glycosylation/O-phosphorylation of the murine estrogen receptor beta. Biochemistry. 2000;39(38):11609-11620.
Cheng X, Hart GW. Glycosylation of the murine estrogen receptor-alpha. J Steroid Biochem Mol Biol. 2000;75(2-3):147-158.
Jiang MS, Hart GW. A subpopulation of estrogen receptors are modified by O-linked N-acetylglucosamine. J Biol Chem. 1997;272(4):2421-2428.
Deng B, Tarhan YE, Ueda K, et al. Critical Role of Estrogen Receptor Alpha O-Glycosylation by N-Acetylgalactosaminyltransferase 6 (GALNT6) in Its Nuclear Localization in Breast Cancer Cells. Neoplasia. 2018;20(10):1038-1044.
Mohammed H, D'Santos C, Serandour AA, et al. Endogenous purification reveals GREB1 as a key estrogen receptor regulatory factor. Cell Rep. 2013;3(2):342-349.
Iyer LM, Zhang D, Burroughs AM, Aravind L. Computational identification of novel biochemical systems involved in oxidation, glycosylation and other complex modifications of bases in DNA. Nucleic Acids Res. 2013;41(16):7635-7655.
Haines CN, Braunreiter KM, Mo XM, Burd CJ. GREB1 isoforms regulate proliferation independent of ERalpha co-regulator activities in breast cancer. Endocr Relat Cancer. 2018;25(7):735-746.
Toy W, Shen Y, Won H, et al. ESR1 ligand-binding domain mutations in hormone-resistant breast cancer. Nat Genet. 2013;45(12):1439-1445.
Merenbakh-Lamin K, Ben-Baruch N, Yeheskel A, et al. D538G mutation in estrogen receptor-alpha: A novel mechanism for acquired endocrine resistance in breast cancer. Cancer research. 2013;73(23):6856-6864.
Li S, Shen D, Shao J, et al. Endocrine-therapy-resistant ESR1 variants revealed by genomic characterization of breast-cancer-derived xenografts. Cell reports. 2013;4(6):1116-1130.
Jeselsohn R, Yelensky R, Buchwalter G, et al. Emergence of constitutively active estrogen receptor-alpha mutations in pretreated advanced estrogen receptor-positive breast cancer. Clin Cancer Res. 2014;20(7):1757-1767.
Giuliano M, Trivedi MV, Schiff R. Bidirectional Crosstalk between the Estrogen Receptor and Human Epidermal Growth Factor Receptor 2 Signaling Pathways in Breast Cancer: Molecular Basis and Clinical Implications. Breast Care (Basel). 2013;8(4):256-262.
Trevino LS, Weigel NL. Phosphorylation: a fundamental regulator of steroid receptor action. Trends Endocrinol Metab. 2013;24(10):515-524.
Zhou W, Slingerland JM. Links between oestrogen receptor activation and proteolysis: relevance to hormone-regulated cancer therapy. Nat Rev Cancer. 2014;14(1):26-38.
Yang X, Yan L, Davidson NE. DNA methylation in breast cancer. Endocr Relat Cancer. 2001;8(2):115-127.
Sabbah M, Courilleau D, Mester J, Redeuilh G. Estrogen induction of the cyclin D1 promoter: involvement of a cAMP response-like element. Proc Natl Acad Sci U S A. 1999;96(20):11217-11222.
Herber B, Truss M, Beato M, Muller R. Inducible regulatory elements in the human cyclin D1 promoter. Oncogene. 1994;9(4):1295-1304.
Conzen SD. Minireview: nuclear receptors and breast cancer. Mol Endocrinol. 2008;22(10):2215-2228.
Kim R, Kaneko M, Arihiro K, et al. Extranuclear expression of hormone receptors in primary breast cancer. Ann Oncol. 2006;17(8):1213-1220.
Chen H, Lin RJ, Schiltz RL, et al. Nuclear receptor coactivator ACTR is a novel histone acetyltransferase and forms a multimeric activation complex with P/CAF and CBP/p300. Cell. 1997;90(3):569-580.
Shao W, Keeton EK, McDonnell DP, Brown M. Coactivator AIB1 links estrogen receptor transcriptional activity and stability. Proc Natl Acad Sci U S A. 2004;101(32):11599-11604.
Rae JM, Johnson MD, Scheys JO, Cordero KE, Larios JM, Lippman ME. GREB 1 is a critical regulator of hormone dependent breast cancer growth. Breast Cancer Res Treat. 2005;92(2):141-149.
Rae JM, Johnson MD, Cordero KE, et al. GREB1 is a novel androgen-regulated gene required for prostate cancer growth. Prostate. 2006;66(8):886-894.
Laviolette LA, Hodgkinson KM, Minhas N, Perez-Iratxeta C, Vanderhyden BC. 17beta-estradiol upregulates GREB1 and accelerates ovarian tumor progression in vivo. International journal of cancer. 2014;135(5):1072-1084.
Wei X, Xu H, Kufe D. MUC1 oncoprotein stabilizes and activates estrogen receptor alpha. Mol Cell. 2006;21(2):295-305.
Dobrzycka KM, Townson SM, Jiang S, Oesterreich S. Estrogen receptor corepressors -- a role in human breast cancer? Endocr Relat Cancer. 2003;10(4):517-536.
Mazumdar A, Wang RA, Mishra SK, et al. Transcriptional repression of oestrogen receptor by metastasis-associated protein 1 corepressor. Nat Cell Biol. 2001;3(1):30-37.
Girault I, Lerebours F, Amarir S, et al. Expression analysis of estrogen receptor alpha coregulators in breast carcinoma: evidence that NCOR1 expression is predictive of the response to tamoxifen. Clin Cancer Res. 2003;9(4):1259-1266.
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