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Discover Oncology

Erschienen in:

26.06.2020 | Review

Intrinsic and Extrinsic Factors Governing the Transcriptional Regulation of ESR1

verfasst von: David K. Lung, Rebecca M. Reese, Elaine T. Alarid

Erschienen in: Discover Oncology | Ausgabe 3-4/2020

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Abstract

Transcriptional regulation of ESR1, the gene that encodes for estrogen receptor α (ER), is critical for regulating the downstream effects of the estrogen signaling pathway in breast cancer such as cell growth. ESR1 is a large and complex gene that is regulated by multiple regulatory elements, which has complicated our understanding of how ESR1 expression is controlled in the context of breast cancer. Early studies characterized the genomic structure of ESR1 with subsequent studies focused on identifying intrinsic (chromatin environment, transcription factors, signaling pathways) and extrinsic (tumor microenvironment, secreted factors) mechanisms that impact ESR1 gene expression. Currently, the introduction of genomic sequencing platforms and additional genome-wide technologies has provided additional insight on how chromatin structures may coordinate with these intrinsic and extrinsic mechanisms to regulate ESR1 expression. Understanding these interactions will allow us to have a clearer understanding of how ESR1 expression is regulated and eventually provide clues on how to influence its regulation with potential treatments. In this review, we highlight key studies concerning the genomic structure of ESR1, mechanisms that affect the dynamics of ESR1 expression, and considerations towards affecting ESR1 expression and hormone responsiveness in breast cancer.

Harvey JM, Clark GM, Osborne CK, Allred DC (1999) Estrogen receptor status by immunohistochemistry is superior to the ligand-binding assay for predicting response to adjuvant endocrine therapy in breast cancer. J Clin Oncol 17:1474–1481PubMed

Stierer M, Rosen H, Weber R, Hanak H, Spona J, Tuchler H (1993) Immunohistochemical and biochemical measurement of estrogen and progesterone receptors in primary breast cancer. Correlation of histopathology and prognostic factors. Ann Surg 218:13–21PubMedPubMedCentral

Allegra JC, Lippman ME, Thompson EB, Simon R, Barlock A, Green L, Huff KK, Do HM, Aitken SC, Warren R (1980) Estrogen receptor status: an important variable in predicting response to endocrine therapy in metastatic breast cancer. Eur J Cancer 16:323–331PubMed

Cook KL, Clarke PA, Parmar J, Hu R, Schwartz-Roberts JL, Abu-Asab M, Warri A, Baumann WT, Clarke R (2014) Knockdown of estrogen receptor-alpha induces autophagy and inhibits antiestrogen-mediated unfolded protein response activation, promoting ROS-induced breast cancer cell death. FASEB Journal : official publication of the Federation of American Societies for Experimental Biology 28:3891–3905

Rosenberg PS, KA Barker, WF Anderson. 2015. Estrogen receptor status and the future burden of invasive and in situ breast cancers in the United States. J Natl Cancer Inst 107

Hammond ME, Hayes DF, Dowsett M, Allred DC, Hagerty KL, Badve S, Fitzgibbons PL, Francis G, Goldstein NS, Hayes M, Hicks DG, Lester S, Love R, Mangu PB, McShane L, Miller K, Osborne CK, Paik S, Perlmutter J, Rhodes A, Sasano H, Schwartz JN, Sweep FC, Taube S, Torlakovic EE, Valenstein P, Viale G, Visscher D, Wheeler T, Williams RB, Wittliff JL, Wolff AC (2010) Oncology American Society of Clinical, Pathologists College of American.. American Society of Clinical Oncology/College of American Pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer (unabridged version). Arch Pathol Lab Med 134:e48–e72PubMed

Allred DC, Brown P, Medina D (2004) The origins of estrogen receptor alpha-positive and estrogen receptor alpha-negative human breast cancer. Breast Cancer Research : BCR 6:240–245PubMedPubMedCentral

Russo J, Ao X, Grill C, Russo IH (1999) Pattern of distribution of cells positive for estrogen receptor alpha and progesterone receptor in relation to proliferating cells in the mammary gland. Breast Cancer Res Treat 53:217–227PubMed

Rosen JM (2003) Hormone receptor patterning plays a critical role in normal lobuloalveolar development and breast cancer progression. Breast Dis 18:3–9PubMed

10.

Walker KJ, McClelland RA, Candlish W, Blamey RW, Nicholson RI (1992) Heterogeneity of oestrogen receptor expression in normal and malignant breast tissue. Eur J Cancer 28:34–37PubMed

11.

Welsh AW, Moeder CB, Kumar S, Gershkovich P, Alarid ET, Harigopal M, Haffty BG, Rimm DL (2011) Standardization of estrogen receptor measurement in breast cancer suggests false-negative results are a function of threshold intensity rather than percentage of positive cells. J Clin Oncol 29:2978–2984PubMedPubMedCentral

12.

Chung W, Eum HH, Lee HO, Lee KM, Lee HB, Kim KT, Ryu HS, Kim S, Lee JE, Park YH, Kan Z, Han W, Park WY (2017) Single-cell RNA-Seq enables comprehensive tumour and immune cell profiling in primary breast cancer. Nat Commun 8:15081PubMedPubMedCentral

13.

Hong SP, Chan TE, Lombardo Y, Corleone G, Rotmensz N, Bravaccini S, Rocca A, Pruneri G, McEwen KR, Charles Coombes R, Barozzi I, Magnani L (2019) Single-cell transcriptomics reveals multi-step adaptations to endocrine therapy. Nat Commun 10

14.

Nguyen QH, Pervolarakis N, Blake K, Ma D, Davis RT, James N, Phung AT, Willey E, Kumar R, Jabart E, Driver I, Rock J, Goga A, Khan SA, Lawson DA, Werb Z, Kessenbrock K (2018) Profiling human breast epithelial cells using single cell RNA sequencing identifies cell diversity. Nat Commun 9:2028PubMedPubMedCentral

15.

Petersen OW, Hoyer PE, van Deurs B (1987) Frequency and distribution of estrogen receptor-positive cells in normal, nonlactating human breast tissue. Cancer Res 47:5748–5751PubMed

16.

Ricketts D, Turnbull L, Ryall G, Bakhshi R, Rawson NS, Gazet JC, Nolan C, Coombes RC (1991) Estrogen and progesterone receptors in the normal female breast. Cancer Res 51:1817–1822PubMed

17.

EBCTCG (2005) Effects of chemotherapy and hormonal therapy for early breast cancer on recurrence and 15-year survival: an overview of the randomised trials. Lancet 365:1687–1717

18.

Campbell FC, Blamey RW, Elston CW, Morris AH, Nicholson RI, Griffiths K, Haybittle JL (1981) Quantitative oestradiol receptor values in primary breast cancer and response of metastases to endocrine therapy. Lancet 2:1317–1319PubMed

19.

Gyorffy B, Lanczky A, Eklund AC, Denkert C, Budczies J, Li Q, Szallasi Z (2010) An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients. Breast Cancer Res Treat 123:725–731PubMed

20.

Cejalvo JM, Martinez de Duenas E, Galvan P, Garcia-Recio S, Burgues Gasion O, Pare L, Antolin S, Martinello R, Blancas I, Adamo B, Guerrero-Zotano A, Munoz M, Nuciforo P, Vidal M, Perez RM, Chacon Lopez-Muniz JI, Caballero R, Peg V, Carrasco E, Rojo F, Perou CM, Cortes J, Adamo V, Albanell J, Gomis RR, Lluch A, Prat A (2017) Intrinsic subtypes and gene expression profiles in primary and metastatic breast cancer. Cancer Res 77:2213–2221PubMedPubMedCentral

21.

Dieci MV, Piacentini F, Dominici M, Omarini C, Goubar A, Ficarra G, Conte P, Guarneri V (2014) Quantitative expression of estrogen receptor on relapse biopsy for ER-positive breast cancer: prognostic impact. Anticancer Res 34:3657–3662PubMed

22.

Webb P, Lopez GN, Greene GL, Baxter JD, Kushner PJ (1992) The limits of the cellular capacity to mediate an estrogen response. Mol Endocrinol 6:157–167PubMed

23.

Saez RA, McGuire WL, Clark GM (1989) Prognostic factors in breast cancer. Semin Surg Oncol 5:102–110PubMed

24.

Knight KA, Livingston RB, Gregory EJ, McGuire WL (1977) Estrogen receptor as an independent prognostic factor for early recurrence in breast cancer. Cancer Res 37:4969–4671

25.

Cheang MC, Martin M, Nielsen TO, Prat A, Voduc D, Rodriguez-Lescure A, Ruiz A, Chia S, Shepherd L, Ruiz-Borrego M, Calvo L, Alba E, Carrasco E, Caballero R, Tu D, Pritchard KI, Levine MN, Bramwell VH, Parker J, Bernard PS, Ellis MJ, Perou CM, Di Leo A, Carey LA (2015) Defining breast cancer intrinsic subtypes by quantitative receptor expression. Oncologist 20:474–482PubMedPubMedCentral

26.

Ellison-Zelski SJ, Solodin NM, Alarid ET (2009) Repression of ESR1 through actions of estrogen receptor alpha and Sin3A at the proximal promoter. Mol Cell Biol 29:4949–4958PubMedPubMedCentral

27.

Alarid ET, Bakopoulos N, Solodin N (1999) Proteasome-mediated proteolysis of estrogen receptor: a novel component in autologous down-regulation. Mol Endocrinol 13:1522–1534PubMed

28.

Preisler-Mashek MT, Solodin N, Stark BL, Tyriver MK, Alarid ET (2002) Ligand-specific regulation of proteasome-mediated proteolysis of estrogen receptor-alpha. Am J Physiol Endocrinol Metab 282:E891–E898PubMed

29.

Nawaz Z, Lonard DM, Dennis AP, Smith CL, O'Malley BW (1999) Proteasome-dependent degradation of the human estrogen receptor. Proc Natl Acad Sci U S A 96:1858–1862PubMedPubMedCentral

30.

Castellano L, Giamas G, Jacob J, Coombes RC, Lucchesi W, Thiruchelvam P, Barton G, Jiao LR, Wait R, Waxman J, Hannon GJ, Stebbing J (2009) The estrogen receptor-alpha-induced microRNA signature regulates itself and its transcriptional response. Proc Natl Acad Sci U S A 106:15732–15737PubMedPubMedCentral

31.

Pandey DP, Picard D (2009) miR-22 inhibits estrogen signaling by directly targeting the estrogen receptor alpha mRNA. Mol Cell Biol 29:3783–3790PubMedPubMedCentral

32.

Di Leva G, Gasparini P, Piovan C, Ngankeu A, Garofalo M, Taccioli C, Iorio MV, Li M, Volinia S, Alder H, Nakamura T, Nuovo G, Liu Y, Nephew KP, Croce CM (2010) MicroRNA cluster 221-222 and estrogen receptor alpha interactions in breast cancer. J Natl Cancer Inst 102:706–721PubMedPubMedCentral

33.

Adams BD, Furneaux H, White BA (2007) The micro-ribonucleic acid (miRNA) miR-206 targets the human estrogen receptor-alpha (ERalpha) and represses ERalpha messenger RNA and protein expression in breast cancer cell lines. Mol Endocrinol 21:1132–1147PubMed

34.

Saceda M, Lindsey RK, Solomon H, Angeloni SV, Martin MB (1998) Estradiol regulates estrogen receptor mRNA stability. J Steroid Biochem Mol Biol 66:113–120PubMed

35.

Saceda M, Lippman ME, Chambon P, Lindsey RL, Ponglikitmongkol M, Puente M, Martin MB (1988) Regulation of the estrogen receptor in MCF-7 cells by estradiol. Mol Endocrinol 2:1157–1162PubMed

36.

Tian D, Solodin NM, Rajbhandari P, Bjorklund K, Alarid ET, Kreeger PK (2015) A kinetic model identifies phosphorylated estrogen receptor-alpha (ERalpha) as a critical regulator of ERalpha dynamics in breast cancer. FASEB Journal : official publication of the Federation of American Societies for Experimental Biology 29:2022–2031

37.

Itoh M, Iwamoto T, Matsuoka J, Nogami T, Motoki T, Shien T, Taira N, Niikura N, Hayashi N, Ohtani S, Higaki K, Fujiwara T, Doihara H, Symmans WF, Pusztai L (2014) Estrogen receptor (ER) mRNA expression and molecular subtype distribution in ER-negative/progesterone receptor-positive breast cancers. Breast Cancer Res Treat 143:403–409PubMed

38.

Iwamoto T, Booser D, Valero V, Murray JL, Koenig K, Esteva FJ, Ueno NT, Zhang J, Shi W, Qi Y, Matsuoka J, Yang EJ, Hortobagyi GN, Hatzis C, Symmans WF, Pusztai L (2012) Estrogen receptor (ER) mRNA and ER-related gene expression in breast cancers that are 1% to 10% ER-positive by immunohistochemistry. J Clin Oncol 30:729–734PubMed

39.

Prat A, Adamo B, Cheang MC, Anders CK, Carey LA, Perou CM (2013) Molecular characterization of basal-like and non-basal-like triple-negative breast cancer. Oncologist 18:123–133PubMedPubMedCentral

40.

Walter P, Green S, Greene G, Krust A, Bornert JM, Jeltsch JM, Staub A, Jensen E, Scrace G, Waterfield M et al (1985) Cloning of the human estrogen receptor cDNA. Proc Natl Acad Sci U S A 82:7889–7893PubMedPubMedCentral

41.

Green S, Walter P, Kumar V, Krust A, Bornert JM, Argos P, Chambon P (1986) Human oestrogen receptor cDNA: sequence, expression and homology to v-erb-A. Nature 320:134–139PubMed

42.

Ponglikitmongkol M, Green S, Chambon P (1988) Genomic organization of the human oestrogen receptor gene. EMBO J 7:3385–3388PubMedPubMedCentral

43.

Keaveney M, Klug J, Dawson MT, Nestor PV, Neilan JG, Forde RC, Gannon F (1991) Evidence for a previously unidentified upstream exon in the human oestrogen receptor gene. J Mol Endocrinol 6:111–115PubMed

44.

Grandien K (1996) Determination of transcription start sites in the human estrogen receptor gene and identification of a novel, tissue-specific, estrogen receptor-mRNA isoform. Mol Cell Endocrinol 116:207–212PubMed

45.

Grandien KF, Berkenstam A, Nilsson S, Gustafsson JA (1993) Localization of DNase I hypersensitive sites in the human oestrogen receptor gene correlates with the transcriptional activity of two differentially used promoters. J Mol Endocrinol 10:269–277PubMed

46.

Piva R, Bianchi N, Aguiari GL, Gambari R, del Senno L (1993) Sequencing of an RNA transcript of the human estrogen receptor gene: evidence for a new transcriptional event. J Steroid Biochem Mol Biol 46:531–538PubMed

47.

Tang Z, Treilleux I, Brown M (1997) A transcriptional enhancer required for the differential expression of the human estrogen receptor in breast cancers. Mol Cell Biol 17:1274–1280PubMedPubMedCentral

48.

Flouriot G, Griffin C, Kenealy M, Sonntag-Buck V, Gannon F (1998) Differentially expressed messenger RNA isoforms of the human estrogen receptor-alpha gene are generated by alternative splicing and promoter usage. Mol Endocrinol 12:1939–1954PubMed

49.

Kos M, Reid G, Denger S, Gannon F (2001) Minireview: genomic organization of the human ERalpha gene promoter region. Mol Endocrinol 15:2057–2063PubMed

50.

Brand H, Kos M, Denger S, Flouriot G, Gromoll J, Gannon F, Reid G (2002) A novel promoter is involved in the expression of estrogen receptor alpha in human testis and epididymis. Endocrinology 143:3397–3404PubMed

51.

Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D (2002) The human genome browser at UCSC. Genome Res 12:996–1006PubMedPubMedCentral

52.

Reid G, Denger S, Kos M, Gannon F (2002) Human estrogen receptor-a: regulation by synthesis, modification and degradation. Cell Mol Life Sci 59:821–831PubMed

53.

Inoue A, Hayashi S-i, Aoyagi K, Nishigaki M, Sasaki H, Kiyama R (2002) A reporter gene assay for evaluation of tissue-specific responses to estrogens based on the differential use of promoters A to F of the human estrogen receptor α gene. J Pharmacol Toxicol Methods 47:129–135PubMed

54.

Higuchi T, Gohno T, Nagatomo T, Tokiniwa H, Niwa T, Horiguchi J, Oyama T, Takeyoshi I, Hayashi S (2014) Variation in use of estrogen receptor-alpha gene promoters in breast cancer compared by quantification of promoter-specific messenger RNA. Clin Breast Cancer 14:249–257PubMed

55.

Eeckhoute J, Keeton EK, Lupien M, Krum SA, Carroll JS, Brown M (2007) Positive cross-regulatory loop ties GATA-3 to estrogen receptor alpha expression in breast cancer. Cancer Res 67:6477–6483PubMed

56.

Asselin-Labat ML, Sutherland KD, Barker H, Thomas R, Shackleton M, Forrest NC, Hartley L, Robb L, Grosveld FG, van der Wees J, Lindeman GJ, Visvader JE (2007) Gata-3 is an essential regulator of mammary-gland morphogenesis and luminal-cell differentiation. Nat Cell Biol 9:201–209PubMed

57.

Kouros-Mehr H, Slorach EM, Sternlicht MD, Werb Z (2006) GATA-3 maintains the differentiation of the luminal cell fate in the mammary gland. Cell 127:1041–1055PubMedPubMedCentral

58.

Powers GL, Ellison-Zelski SJ, Casa AJ, Lee AV, Alarid ET (2010) Proteasome inhibition represses ERalpha gene expression in ER+ cells: a new link between proteasome activity and estrogen signaling in breast cancer. Oncogene 29:1509–1518PubMed

59.

Powers GL, Rajbhandari P, Solodin NM, Bickford B, Alarid ET (2013) The proteasome inhibitor bortezomib induces an inhibitory chromatin environment at a distal enhancer of the estrogen receptor-alpha gene. PLoS One 8:e81110PubMedPubMedCentral

60.

Bailey SD, Desai K, Kron KJ, Mazrooei P, Sinnott-Armstrong NA, Treloar AE, Dowar M, Thu KL, Cescon DW, Silvester J, Yang SY, Wu X, Pezo RC, Haibe-Kains B, Mak TW, Bedard PL, Pugh TJ, Sallari RC, Lupien M (2016) Noncoding somatic and inherited single-nucleotide variants converge to promote ESR1 expression in breast cancer. Nat Genet 48:1260–1266PubMedPubMedCentral

61.

deGraffenried LA, Hilsenbeck SG, Fuqua SAW (2002) Sp1 is essential for estrogen receptor alpha gene transcription. J Steroid Biochem 82:7–18

62.

Cowper-Sal lari R, Zhang X, Wright JB, Bailey SD, Cole MD, Eeckhoute J, Moore JH, Lupien M (2012) Breast cancer risk-associated SNPs modulate the affinity of chromatin for FOXA1 and alter gene expression. Nat Genet 44:1191–1198PubMedPubMedCentral

63.

deConinck EC, McPherson LA, Weigel RJ (1995) Transcriptional regulation of estrogen receptor in breast carcinomas. Mol Cell Biol 15:2191–2196PubMedPubMedCentral

64.

deGraffenried LA, Friedrichs WE, Russell DH, Donzis EJ, Middleton AK, Silva JM, Roth RA, Hidalgo M (2004) Inhibition of mTOR activity restores tamoxifen response in breast cancer cells with aberrant Akt activity. Clin Cancer Res 10:8059–8067PubMed

65.

Li L, He S, Sun JM, Davie JR (2004) Gene regulation by Sp1 and Sp3. Biochem Cell Biol 82:460–471PubMed

66.

Jiang Q, Zhang H, Zhang P (2011) ShRNA-mediated gene silencing of MTA1 influenced on protein expression of ER alpha, MMP-9, CyclinD1 and invasiveness, proliferation in breast cancer cell lines MDA-MB-231 and MCF-7 in vitro. J Exp Clin Cancer Res 30:60PubMedPubMedCentral

67.

Kang HJ, Lee MH, Kang HL, Kim SH, Ahn JR, Na H, Na TY, Kim YN, Seong JK, Lee MO (2014) Differential regulation of estrogen receptor alpha expression in breast cancer cells by metastasis-associated protein 1. Cancer Res 74:1484–1494PubMed

68.

Guo S, Sonenshein GE (2004) Forkhead box transcription factor FOXO3a regulates estrogen receptor alpha expression and is repressed by the Her-2/neu/phosphatidylinositol 3-kinase/Akt signaling pathway. Mol Cell Biol 24:8681–8690PubMedPubMedCentral

69.

Shirley SH, Rundhaug JE, Tian J, Cullinan-Ammann N, Lambertz I, Conti CJ, Fuchs-Young R (2009) Transcriptional regulation of estrogen receptor-alpha by p53 in human breast cancer cells. Cancer Res 69:3405–3414PubMedPubMedCentral

70.

Fullwood MJ, Liu MH, Pan YF, Liu J, Xu H, Mohamed YB, Orlov YL, Velkov S, Ho A, Mei PH, Chew EG, Huang PY, Welboren WJ, Han Y, Ooi HS, Ariyaratne PN, Vega VB, Luo Y, Tan PY, Choy PY, Wansa KD, Zhao B, Lim KS, Leow SC, Yow JS, Joseph R, Li H, Desai KV, Thomsen JS, Lee YK, Karuturi RK, Herve T, Bourque G, Stunnenberg HG, Ruan X, Cacheux-Rataboul V, Sung WK, Liu ET, Wei CL, Cheung E, Ruan Y (2009) An oestrogen-receptor-alpha-bound human chromatin interactome. Nature 462:58–64PubMedPubMedCentral

71.

Dunbier AK, H Anderson, Z Ghazoui, E Lopez-Knowles, S Pancholi, R Ribas, S Drury, K Sidhu, A Leary, LA Martin, M Dowsett. 2011. ESR1 is co-expressed with closely adjacent uncharacterised genes spanning a breast cancer susceptibility locus at 6q25.1. PLoS Genet 7:e1001382

72.

Zurück zum Zitat Dunning AM, K Michailidou, KB Kuchenbaecker, D Thompson, JD French, J Beesley, CS Healey, S Kar, KA Pooley, E Lopez-Knowles, E Dicks, D Barrowdale, NA Sinnott-Armstrong, RC Sallari, KM Hillman, S Kaufmann, H Sivakumaran, M Moradi Marjaneh, JS Lee, M Hills, M Jarosz, S Drury, S Canisius, MK Bolla, J Dennis, Q Wang, JL Hopper, MC Southey, A Broeks, MK Schmidt, A Lophatananon, K Muir, MW Beckmann, PA Fasching, I Dos-Santos-Silva, J Peto, EJ Sawyer, I Tomlinson, B Burwinkel, F Marme, P Guenel, T Truong, SE Bojesen, H Flyger, A Gonzalez-Neira, JI Perez, H Anton-Culver, L Eunjung, V Arndt, H Brenner, A Meindl, RK Schmutzler, H Brauch, U Hamann, K Aittomaki, C Blomqvist, H Ito, K Matsuo, N Bogdanova, T Dork, A Lindblom, S Margolin, VM Kosma, A Mannermaa, CC Tseng, AH Wu, D Lambrechts, H Wildiers, J Chang-Claude, A Rudolph, P Peterlongo, P Radice, JE Olson, GG Giles, RL Milne, CA Haiman, BE Henderson, MS Goldberg, SH Teo, CH Yip, S Nord, AL Borresen-Dale, V Kristensen, J Long, W Zheng, K Pylkas, R Winqvist, IL Andrulis, JA Knight, P Devilee, C Seynaeve, J Figueroa, ME Sherman, K Czene, H Darabi, A Hollestelle, AM van den Ouweland, K Humphreys, YT Gao, XO Shu, A Cox, SS Cross, W Blot, Q Cai, M Ghoussaini, BJ Perkins, M Shah, JY Choi, D Kang, SC Lee, M Hartman, M Kabisch, D Torres, A Jakubowska, J Lubinski, P Brennan, S Sangrajrang, CB Ambrosone, AE Toland, CY Shen, PE Wu, N Orr, A Swerdlow, L McGuffog, S Healey, A Lee, M Kapuscinski, EM John, MB Terry, MB Daly, DE Goldgar, SS Buys, R Janavicius, L Tihomirova, N Tung, CM Dorfling, EJ van Rensburg, SL Neuhausen, B Ejlertsen, TV Hansen, A Osorio, J Benitez, R Rando, JN Weitzel, B Bonanni, B Peissel, S Manoukian, L Papi, L Ottini, I Konstantopoulou, P Apostolou, J Garber, MU Rashid, D Frost, Embrace L Izatt S Ellis A K Godwin, N Arnold, D Niederacher, K Rhiem, N Bogdanova-Markov, C Sagne, D Stoppa-Lyonnet, F Damiola, Gemo Study Collaborators, O M Sinilnikova, S Mazoyer, C Isaacs, KB Claes, K De Leeneer, M de la Hoya, T Caldes, H Nevanlinna, S Khan, AR Mensenkamp, Hebon M J Hooning, MA Rookus, A Kwong, E Olah, O Diez, J Brunet, MA Pujana, J Gronwald, T Huzarski, RB Barkardottir, R Laframboise, P Soucy, M Montagna, S Agata, MR Teixeira, Investigators kConFab, SK Park, N Lindor, FJ Couch, M Tischkowitz, L Foretova, J Vijai, K Offit, CF Singer, C Rappaport, CM Phelan, MH Greene, PL Mai, G Rennert, EN Imyanitov, PJ Hulick, KA Phillips, M Piedmonte, AM Mulligan, G Glendon, A Bojesen, M Thomassen, MA Caligo, SY Yoon, E Friedman, Y Laitman, A Borg, A von Wachenfeldt, H Ehrencrona, J Rantala, OI Olopade, PA Ganz, RL Nussbaum, SA Gayther, KL Nathanson, SM Domchek, BK Arun, G Mitchell, BY Karlan, J Lester, G Maskarinec, C Woolcott, C Scott, J Stone, C Apicella, R Tamimi, R Luben, KT Khaw, A Helland, V Haakensen, M Dowsett, PD Pharoah, J Simard, P Hall, M Garcia-Closas, C Vachon, G Chenevix-Trench, AC Antoniou, DF Easton, SL Edwards. 2016. Breast cancer risk variants at 6q25 display different phenotype associations and regulate ESR1, RMND1 and CCDC170. Nat Genet 48:374–386 Dunning AM, K Michailidou, KB Kuchenbaecker, D Thompson, JD French, J Beesley, CS Healey, S Kar, KA Pooley, E Lopez-Knowles, E Dicks, D Barrowdale, NA Sinnott-Armstrong, RC Sallari, KM Hillman, S Kaufmann, H Sivakumaran, M Moradi Marjaneh, JS Lee, M Hills, M Jarosz, S Drury, S Canisius, MK Bolla, J Dennis, Q Wang, JL Hopper, MC Southey, A Broeks, MK Schmidt, A Lophatananon, K Muir, MW Beckmann, PA Fasching, I Dos-Santos-Silva, J Peto, EJ Sawyer, I Tomlinson, B Burwinkel, F Marme, P Guenel, T Truong, SE Bojesen, H Flyger, A Gonzalez-Neira, JI Perez, H Anton-Culver, L Eunjung, V Arndt, H Brenner, A Meindl, RK Schmutzler, H Brauch, U Hamann, K Aittomaki, C Blomqvist, H Ito, K Matsuo, N Bogdanova, T Dork, A Lindblom, S Margolin, VM Kosma, A Mannermaa, CC Tseng, AH Wu, D Lambrechts, H Wildiers, J Chang-Claude, A Rudolph, P Peterlongo, P Radice, JE Olson, GG Giles, RL Milne, CA Haiman, BE Henderson, MS Goldberg, SH Teo, CH Yip, S Nord, AL Borresen-Dale, V Kristensen, J Long, W Zheng, K Pylkas, R Winqvist, IL Andrulis, JA Knight, P Devilee, C Seynaeve, J Figueroa, ME Sherman, K Czene, H Darabi, A Hollestelle, AM van den Ouweland, K Humphreys, YT Gao, XO Shu, A Cox, SS Cross, W Blot, Q Cai, M Ghoussaini, BJ Perkins, M Shah, JY Choi, D Kang, SC Lee, M Hartman, M Kabisch, D Torres, A Jakubowska, J Lubinski, P Brennan, S Sangrajrang, CB Ambrosone, AE Toland, CY Shen, PE Wu, N Orr, A Swerdlow, L McGuffog, S Healey, A Lee, M Kapuscinski, EM John, MB Terry, MB Daly, DE Goldgar, SS Buys, R Janavicius, L Tihomirova, N Tung, CM Dorfling, EJ van Rensburg, SL Neuhausen, B Ejlertsen, TV Hansen, A Osorio, J Benitez, R Rando, JN Weitzel, B Bonanni, B Peissel, S Manoukian, L Papi, L Ottini, I Konstantopoulou, P Apostolou, J Garber, MU Rashid, D Frost, Embrace L Izatt S Ellis A K Godwin, N Arnold, D Niederacher, K Rhiem, N Bogdanova-Markov, C Sagne, D Stoppa-Lyonnet, F Damiola, Gemo Study Collaborators, O M Sinilnikova, S Mazoyer, C Isaacs, KB Claes, K De Leeneer, M de la Hoya, T Caldes, H Nevanlinna, S Khan, AR Mensenkamp, Hebon M J Hooning, MA Rookus, A Kwong, E Olah, O Diez, J Brunet, MA Pujana, J Gronwald, T Huzarski, RB Barkardottir, R Laframboise, P Soucy, M Montagna, S Agata, MR Teixeira, Investigators kConFab, SK Park, N Lindor, FJ Couch, M Tischkowitz, L Foretova, J Vijai, K Offit, CF Singer, C Rappaport, CM Phelan, MH Greene, PL Mai, G Rennert, EN Imyanitov, PJ Hulick, KA Phillips, M Piedmonte, AM Mulligan, G Glendon, A Bojesen, M Thomassen, MA Caligo, SY Yoon, E Friedman, Y Laitman, A Borg, A von Wachenfeldt, H Ehrencrona, J Rantala, OI Olopade, PA Ganz, RL Nussbaum, SA Gayther, KL Nathanson, SM Domchek, BK Arun, G Mitchell, BY Karlan, J Lester, G Maskarinec, C Woolcott, C Scott, J Stone, C Apicella, R Tamimi, R Luben, KT Khaw, A Helland, V Haakensen, M Dowsett, PD Pharoah, J Simard, P Hall, M Garcia-Closas, C Vachon, G Chenevix-Trench, AC Antoniou, DF Easton, SL Edwards. 2016. Breast cancer risk variants at 6q25 display different phenotype associations and regulate ESR1, RMND1 and CCDC170. Nat Genet 48:374–386

73.

Jiang P, Li Y, Poleshko A, Medvedeva V, Baulina N, Zhang Y, Zhou Y, Slater CM, Pellegrin T, Wasserman J, Lindy M, Efimov A, Daly M, Katz RA, Chen X (2017) The protein encoded by the CCDC170 breast cancer gene functions to organize the Golgi-microtubule network. EBioMedicine 22:28–43PubMedPubMedCentral

74.

Perry JJ, Ballard GD, Albert AE, Dobrolecki LE, Malkas LH, Hoelz DJ (2015) Human C6orf211 encodes Armt1, a protein carboxyl methyltransferase that targets PCNA and is linked to the DNA damage response. Cell Rep 10:1288–1296PubMedPubMedCentral

75.

Janer A, Antonicka H, Lalonde E, Nishimura T, Sasarman F, Brown GK, Brown RM, Majewski J, Shoubridge EA (2012) An RMND1 mutation causes encephalopathy associated with multiple oxidative phosphorylation complex deficiencies and a mitochondrial translation defect. Am J Hum Genet 91:737–743PubMedPubMedCentral

76.

Yamamoto-Ibusuki M, Yamamoto Y, Fujiwara S, Sueta A, Yamamoto S, Hayashi M, Tomiguchi M, Takeshita T, Iwase H (2015) C6ORF97-ESR1 breast cancer susceptibility locus: influence on progression and survival in breast cancer patients. Eur J Hum Genet 23:949–956PubMed

77.

Sofueva S, Yaffe E, Chan WC, Georgopoulou D, Vietri Rudan M, Mira-Bontenbal H, Pollard SM, Schroth GP, Tanay A, Hadjur S (2013) Cohesin-mediated interactions organize chromosomal domain architecture. EMBO J 32:3119–3129PubMedPubMedCentral

78.

Prenzel T, F Kramer, U Bedi, S Nagarajan, T Beissbarth, SA Johnsen. 2012. Cohesin is required for expression of the estrogen receptor-alpha (ESR1) gene. Epigenet Chromatin 5

79.

Achinger-Kawecka J, Valdes-Mora F, Luu PL, Giles KA, Caldon CE, Qu W, Nair S, Soto S, Locke WJ, Yeo-Teh NS, Gould CM, Du Q, Smith GC, Ramos IR, Fernandez KF, Hoon DS, Gee JMW, Stirzaker C, Clark SJ (2020) Epigenetic reprogramming at estrogen-receptor binding sites alters 3D chromatin landscape in endocrine-resistant breast cancer. Nat Commun 11:320PubMedPubMedCentral

80.

Korkmaz G, Manber Z, Lopes R, Prekovic S, Schuurman K, Kim Y, Teunissen H, Flach K, Wit E, Galli GG, Zwart W, Elkon R, Agami R (2019) A CRISPR-Cas9 screen identifies essential CTCF anchor sites for estrogen receptor-driven breast cancer cell proliferation. Nucleic Acids Res 47:9557–9572PubMedPubMedCentral

81.

Harrell JC, Dye WW, Harvell DM, Pinto M, Jedlicka P, Sartorius CA, Horwitz KB (2007) Estrogen insensitivity in a model of estrogen receptor positive breast cancer lymph node metastasis. Cancer Res 67:10582–10591PubMed

82.

Khan SA, Sachdeva A, Naim S, Meguid MM, Marx W, Simon H, Halverson JD, Numann PJ (1999) The normal breast epithelium of women with breast cancer displays an aberrant response to estradiol. Cancer epidemiology, Biomarkers & Prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology 8:867–872

83.

Frech MS, Halama ED, Tilli MT, Singh B, Gunther EJ, Chodosh LA, Flaws JA, Furth PA (2005) Deregulated estrogen receptor alpha expression in mammary epithelial cells of transgenic mice results in the development of ductal carcinoma in situ. Cancer Res 65:681–685PubMedPubMedCentral

84.

Barr FE, Degnim AC, Hartmann LC, Radisky DC, Boughey JC, Anderson SS, Vierkant RA, Frost MH, Visscher DW, Reynolds C (2011) Estrogen receptor expression in atypical hyperplasia: lack of association with breast cancer. Cancer Prev Res 4:435–444

85.

Fowler AM, Solodin NM, Valley CC, Alarid ET (2006) Altered target gene regulation controlled by estrogen receptor-alpha concentration. Mol Endocrinol 20:291–301PubMed

86.

Tolhurst RS, Thomas RS, Kyle FJ, Patel H, Periyasamy M, Photiou A, Thiruchelvam PT, Lai CF, Al-Sabbagh M, Fisher RA, Barry S, Crnogorac-Jurcevic T, Martin LA, Dowsett M, Charles Coombes R, Kamalati T, Ali S, Buluwela L (2011) Transient over-expression of estrogen receptor-alpha in breast cancer cells promotes cell survival and estrogen-independent growth. Breast Cancer Res Treat 128:357–368PubMed

87.

Tomita S, Zhang Z, Nakano M, Ibusuki M, Kawazoe T, Yamamoto Y, Iwase H (2009) Estrogen receptor alpha gene ESR1 amplification may predict endocrine therapy responsiveness in breast cancer patients. Cancer Sci 100:1012–1017PubMed

88.

Holst F, Stahl PR, Ruiz C, Hellwinkel O, Jehan Z, Wendland M, Lebeau A, Terracciano L, Al-Kuraya K, Janicke F, Sauter G, Simon R (2007) Estrogen receptor alpha (ESR1) gene amplification is frequent in breast cancer. Nat Genet 39:655–660PubMed

89.

Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, Jacobsen A, Byrne CJ, Heuer ML, Larsson E, Antipin Y, Reva B, Goldberg AP, Sander C, Schultz N (2012) The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov 2:401–404PubMed

90.

Gao MQ, Kim BG, Kang S, Choi YP, Park H, Kang KS, Cho NH (2010) Stromal fibroblasts from the interface zone of human breast carcinomas induce an epithelial-mesenchymal transition-like state in breast cancer cells in vitro. J Cell Sci 123:3507–3514PubMed

91.

Read LD, Greene GL, Katzenellenbogen BS (1989) Regulation of estrogen-receptor messenger ribonucleic-acid and protein-levels in human-breast cancer cell-lines by sex steroid-hormones, their antagonists, and growth-factors. Mol Endocrinol 3:295–304PubMed

92.

Berkenstam A, Glaumann H, Martin M, Gustafsson JA, Norstedt G (1989) Hormonal regulation of estrogen receptor messenger ribonucleic acid in T47Dco and MCF-7 breast cancer cells. Mol Endocrinol 3:22–28PubMed

93.

Saceda M, Lippman ME, Lindsey RK, Puente M, Martin MB (1989) Role of an estrogen receptor-dependent mechanism in the regulation of estrogen receptor mRNA in MCF-7 cells. Mol Endocrinol 3:1782–1787PubMed

94.

Hassig CA, Fleischer TC, Billin AN, Schreiber SL, Ayer DE (1997) Histone deacetylase activity is required for full transcriptional repression by mSin3A. Cell 89:341–347PubMed

95.

Zhang Y, Iratni R, Erdjument-Bromage H, Tempst P, Reinberg D (1997) Histone deacetylases and SAP18, a novel polypeptide, are components of a human Sin3 complex. Cell 89:357–364PubMed

96.

Yao ZX, Lu LJ, Wang RJ, Jin LB, Liu SC, Li HY, Ren GS, Wu KN, Wang DL, Kong LQ (2014) Discordance and clinical significance of ER, PR, and HER2 status between primary breast cancer and synchronous axillary lymph node metastasis. Med Oncol 31:798PubMed

97.

Amir E, Clemons M, Purdie CA, Miller N, Quinlan P, Geddie W, Coleman RE, Freedman OC, Jordan LB, Thompson AM (2012) Tissue confirmation of disease recurrence in breast cancer patients: pooled analysis of multi-centre, multi-disciplinary prospective studies. Cancer Treat Rev 38:708–714PubMed

98.

Amir E, Miller N, Geddie W, Freedman O, Kassam F, Simmons C, Oldfield M, Dranitsaris G, Tomlinson G, Laupacis A, Tannock IF, Clemons M (2012) Prospective study evaluating the impact of tissue confirmation of metastatic disease in patients with breast cancer. J Clin Oncol 30:587–592PubMed

99.

Amir E, Ooi WS, Simmons C, Kahn H, Christakis M, Popovic S, Kalina M, Chesney A, Singh G, Clemons M (2008) Discordance between receptor status in primary and metastatic breast cancer: an exploratory study of bone and bone marrow biopsies. Clin Oncol (R Coll Radiol) 20:763–768

100.

Broom RJ, Tang PA, Simmons C, Bordeleau L, Mulligan AM, O'Malley FP, Miller N, Andrulis IL, Brenner DM, Clemons MJ (2009) Changes in estrogen receptor, progesterone receptor and Her-2/neu status with time: discordance rates between primary and metastatic breast cancer. Anticancer Res 29:1557–1562PubMed

101.

Curtit E, Nerich V, Mansi L, Chaigneau L, Cals L, Villanueva C, Bazan F, Montcuquet P, Meneveau N, Perrin S, Algros MP, Pivot X (2013) Discordances in estrogen receptor status, progesterone receptor status, and HER2 status between primary breast cancer and metastasis. Oncologist 18:667–674PubMedPubMedCentral

102.

Aitken SJ, Thomas JS, Langdon SP, Harrison DJ, Faratian D (2010) Quantitative analysis of changes in ER, PR and HER2 expression in primary breast cancer and paired nodal metastases. Ann Oncol 21:1254–1261PubMed

103.

Li BDL, Byskosh A, Molteni A, Duda RB (1994) Estrogen and progesterone-receptor concordance between primary and recurrent breast-cancer. J Surg Oncol 57:71–77PubMed

104.

Iwase H, Omoto Y, Iwata H, Toyama T, Hara Y, Ando Y, Ito Y, Fujii Y, Kobayashi S (1999) DNA methylation analysis at distal and proximal promoter regions of the oestrogen receptor gene in breast cancers. Brit J Cancer 80:1982–1986PubMedPubMedCentral

105.

Nass SJ, Herman JG, Gabrielson E, Iversen PW, Parl FF, Davidson NE, Graff JR (2000) Aberrant methylation of the estrogen receptor and E-cadherin 5′ CpG islands increases with malignant progression in human breast cancer. Cancer Res 60:4346–4348PubMed

106.

Ottaviano YL, Issa JP, Parl FF, Smith HS, Baylin SB, Davidson NE (1994) Methylation of the estrogen receptor gene CpG island marks loss of estrogen receptor expression in human breast cancer cells. Cancer Res 54:2552–2555PubMed

107.

Yan L, Nass SJ, Smith D, Nelson WG, Herman JG, Davidson NE (2003) Specific inhibition of DNMT1 by antisense oligonucleotides induces re-expression of estrogen receptor-alpha (ER) in ER-negative human breast cancer cell lines. Cancer Biology & Therapy 2:552–556

108.

Sharma D, Blum J, Yang X, Beaulieu N, Macleod AR, Davidson NE (2005) 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 19:1740–1751PubMed

109.

Sharma D, Saxena NK, Davidson NE, Vertino PM (2006) Restoration of tamoxifen sensitivity in estrogen receptor-negative breast cancer cells: tamoxifen-bound reactivated ER recruits distinctive corepressor complexes. Cancer Res 66:6370–6378PubMedPubMedCentral

110.

Nakshatri H, Bhat-Nakshatri P, Martin DA, Goulet RJ Jr, Sledge GW Jr (1997) Constitutive activation of NF-kappaB during progression of breast cancer to hormone-independent growth. Mol Cell Biol 17:3629–3639PubMedPubMedCentral

111.

Wang X, Belguise K, O'Neill CF, Sanchez-Morgan N, Romagnoli M, Eddy SF, Mineva ND, Yu Z, Min C, Trinkaus-Randall V, Chalbos D, Sonenshein GE (2009) RelB NF-kappaB represses estrogen receptor alpha expression via induction of the zinc finger protein Blimp1. Mol Cell Biol 29:3832–3844PubMedPubMedCentral

112.

Gyory I, Wu J, Fejer G, Seto E, Wright KL (2004) PRDI-BF1 recruits the histone H3 methyltransferase G9a in transcriptional silencing. Nat Immunol 5:299–308PubMed

113.

Ren B, Chee KJ, Kim TH, Maniatis T (1998) PRDI-BF1/Blimp-1 repression is mediated by corepressors of the Groucho family of proteins. Genes Dev 13:125–137

114.

Yu J, Angelin-Duclos C, Greenwood J, Liao J, Calame K (2000) Transcriptional repression by blimp-1 (PRDI-BF1) involves recruitment of histone deacetylase. Mol Cell Biol 20:2592–2603PubMedPubMedCentral

115.

Sainsbury JR, Farndon JR, Sherbet GV, Harris AL (1985) Epidermal-growth-factor receptors and oestrogen receptors in human breast cancer. Lancet 1:364–366PubMed

116.

Papa V, Gliozzo B, Clark GM, McGuire WL, Moore D, Fujita-Yamaguchi Y, Vigneri R, Goldfine ID, Pezzino V (1993) Insulin-like growth factor-I receptors are overexpressed and predict a low risk in human breast cancer. Cancer Res 53:3736–3740PubMed

117.

Sharma AK, Horgan K, Douglas-Jones A, McClelland R, Gee J, Nicholson R (1994) Dual immunocytochemical analysis of oestrogen and epidermal growth factor receptors in human breast cancer. Br J Cancer 69:1032–1037PubMedPubMedCentral

118.

van Agthoven T, Timmermans M, Foekens JA, Dorssers LC, Henzen-Logmans SC (1994) Differential expression of estrogen, progesterone, and epidermal growth factor receptors in normal, benign, and malignant human breast tissues using dual staining immunohistochemistry. Am J Pathol 144:1238–1246PubMedPubMedCentral

119.

Rosenbluth JM, Schackmann RCJ, Gray GK, Selfors LM, Li CM, Boedicker M, Kuiken HJ, Richardson A, Brock J, Garber J, Dillon D, Sachs N, Clevers H, Brugge JS (2020) Organoid cultures from normal and cancer-prone human breast tissues preserve complex epithelial lineages. Nat Commun 11:1711PubMedPubMedCentral

120.

Oh AS, Lorant LA, Holloway JN, Miller DL, Kern FG, El-Ashry D (2001) Hyperactivation of MAPK induces loss of ER alpha expression in breast cancer cells. Mol Endocrinol 15:1344–1359PubMed

121.

Plotkin A, Volmar CH, Wahlestedt C, Ayad N, El-Ashry D (2014) Transcriptional repression of ER through hMAPK dependent histone deacetylation by class I HDACs. Breast Cancer Res Treat 147:249–263PubMed

122.

Citro S, Miccolo C, Meloni L, Chiocca S (2015) PI3K/mTOR mediate mitogen-dependent HDAC1 phosphorylation in breast cancer: a novel regulation of estrogen receptor expression. J Mol Cell Biol 7:132–142PubMed

123.

Cai FF, Kohler C, Zhang B, Wang MH, Chen WJ, Zhong XY (2011) Epigenetic therapy for breast cancer. Int J Mol Sci 12:4465–4487PubMedPubMedCentral

124.

Connolly RM, Li H, Jankowitz RC, Zhang Z, Rudek MA, Jeter SC, Slater SA, Powers P, Wolff AC, Fetting JH, Brufsky A, Piekarz R, Ahuja N, Laird PW, Shen H, Weisenberger DJ, Cope L, Herman JG, Somlo G, Garcia AA, Jones PA, Baylin SB, Davidson NE, Zahnow CA, Stearns V (2017) Combination epigenetic therapy in advanced breast cancer with 5-azacitidine and entinostat: a phase II National Cancer Institute/Stand Up to Cancer Study. Clin Cancer Res 23:2691–2701PubMed

125.

Pryzbylkowski P, Obajimi O, Keen JC (2008) Trichostatin A and 5 Aza-2′ deoxycytidine decrease estrogen receptor mRNA stability in ER positive MCF7 cells through modulation of HuR. Breast Cancer Res Treat 111:15–25PubMed

126.

Moody SE, Perez D, Pan TC, Sarkisian CJ, Portocarrero CP, Sterner CJ, Notorfrancesco KL, Cardiff RD, Chodosh LA (2005) The transcriptional repressor Snail promotes mammary tumor recurrence. Cancer Cell 8:197–209PubMed

127.

Mironchik Y, Winnard PT Jr, Vesuna F, Kato Y, Wildes F, Pathak AP, Kominsky S, Artemov D, Bhujwalla Z, Van Diest P, Burger H, Glackin C, Raman V (2005) Twist overexpression induces in vivo angiogenesis and correlates with chromosomal instability in breast cancer. Cancer Res 65:10801–10809PubMedPubMedCentral

128.

Martin TA, Goyal A, Watkins G, Jiang WG (2005) Expression of the transcription factors snail, slug, and twist and their clinical significance in human breast cancer. Ann Surg Oncol 12:488–496PubMed

129.

Dhasarathy A, Kajita M, Wade PA (2007) The transcription factor snail mediates epithelial to mesenchymal transitions by repression of estrogen receptor-alpha. Mol Endocrinol 21:2907–2918PubMed

130.

Peinado H, Ballestar E, Esteller M, Cano A (2004) Snail mediates E-cadherin repression by the recruitment of the Sin3A/histone deacetylase 1 (HDAC1)/HDAC2 complex. Mol Cell Biol 24:306–319PubMedPubMedCentral

131.

Vesuna F, Lisok A, Kimble B, Domek J, Kato Y, van der Groep P, Artemov D, Kowalski J, Carraway H, van Diest P, Raman V (2011) Twist contributes to hormone resistance in breast cancer by downregulating estrogen receptor-α. Oncogene 31:3223–3234PubMedPubMedCentral

132.

Fu J, Zhang L, He T, Xiao X, Liu X, Wang L, Yang L, Yang M, Zhang T, Chen R, Xu J (2012) TWIST represses estrogen receptor-alpha expression by recruiting the NuRD protein complex in breast cancer cells. Int J Biol Sci 8:522–532PubMedPubMedCentral

133.

Bai JW, Chen MN, Wei XL, Li YC, Lin HY, Chen M, Li JW, Du CW, Man K, Zhang GJ (2017) The zinc-finger transcriptional factor Slug transcriptionally downregulates ERalpha by recruiting lysine-specific demethylase 1 in human breast cancer. Oncogenesis 6:e330PubMedPubMedCentral

134.

Theodorou V, Stark R, Menon S, Carroll JS (2013) GATA3 acts upstream of FOXA1 in mediating ESR1 binding by shaping enhancer accessibility. Genome Res 23:12–22PubMedPubMedCentral

135.

Cheng AS, Jin VX, Fan M, Smith LT, Liyanarachchi S, Yan PS, Leu YW, Chan MW, Plass C, Nephew KP, Davuluri RV, Huang TH (2006) Combinatorial analysis of transcription factor partners reveals recruitment of c-MYC to estrogen receptor-alpha responsive promoters. Mol Cell 21:393–404PubMed

136.

Nguyen NT, Vendrell JA, Poulard C, Gyorffy B, Goddard-Leon S, Bieche I, Corbo L, Le Romancer M, Bachelot T, Treilleux I, Cohen PA (2014) A functional interplay between ZNF217 and estrogen receptor alpha exists in luminal breast cancers. Mol Oncol 8:1441–1457PubMedPubMedCentral

137.

Cahill MA, Ernst WH, Janknecht R, Nordheim A (1994) Regulatory squelching. FEBS Lett 344:105–108PubMed

138.

Gill G, Ptashne M (1988) Negative effect of the transcriptional activator GAL4. Nature 334:721–724PubMed

139.

Meyer ME, Gronemeyer H, Turcotte B, Bocquel MT, Tasset D, Chambon P (1989) Steroid-hormone receptors compete for factors that mediate their enhancer function. Cell 57:433–442PubMed

140.

He HH, Meyer CA, Chen MW, Jordan VC, Brown M, Liu XS (2012) Differential DNase I hypersensitivity reveals factor-dependent chromatin dynamics. Genome Res 22:1015–1025PubMedPubMedCentral

141.

Guertin MJ, Zhang X, Coonrod SA, Hager GL (2014) Transient estrogen receptor binding and p300 redistribution support a squelching mechanism for estradiol-repressed genes. Mol Endocrinol 28:1522–1533PubMedPubMedCentral

142.

Priedigkeit N, Watters RJ, Lucas PC, Basudan A, Bhargava R, Horne W, Kolls JK, Fang Z, Rosenzweig MQ, Brufsky AM, Weiss KR, Oesterreich S, Lee AV (2017) Exome-capture RNA sequencing of decade-old breast cancers and matched decalcified bone metastases. JCI Insight 2:e95703PubMedCentral

143.

Ignar-Trowbridge DM, Teng CT, Ross KA, Parker MG, Korach KS, McLachlan JA (1993) Peptide growth factors elicit estrogen receptor-dependent transcriptional activation of an estrogen-responsive element. Mol Endocrinol 7:992–998PubMed

144.

Bunone G, Briand PA, Miksicek RJ, Picard D (1996) Activation of the unliganded estrogen receptor by EGF involves the MAP kinase pathway and direct phosphorylation. EMBO J 15:2174–2183PubMedPubMedCentral

145.

Cavailles V, Garcia M, Rochefort H (1989) Regulation of cathepsin-D and pS2 gene expression by growth factors in MCF7 human breast cancer cells. Mol Endocrinol 3:552–558PubMed

146.

Nunez AM, Berry M, Imler JL, Chambon P (1989) The 5′ flanking region of the pS2 gene contains a complex enhancer region responsive to oestrogens, epidermal growth factor, a tumour promoter (TPA), the c-Ha-ras oncoprotein and the c-jun protein. EMBO J 8:823–829PubMedPubMedCentral

147.

Kato S, Endoh H, Masuhiro Y, Kitamoto T, Uchiyama S, Sasaki H, Masushige S, Gotoh Y, Nishida E, Kawashima H, Metzger D, Chambon P (1995) Activation of the estrogen-receptor through phosphorylation by mitogen-activated protein-kinase. Science 270:1491–1494PubMed

148.

Divekar SD, Storchan GB, Sperle K, Veselik DJ, Johnson E, Dakshanamurthy S, Lajiminmuhip YN, Nakles RE, Huang L, Martin MB (2011) The role of calcium in the activation of estrogen receptor-alpha. Cancer Res 71:1658–1668PubMedPubMedCentral

149.

Becker MA, Ibrahim YH, Cui X, Lee AV, Yee D (2011) The IGF pathway regulates ERalpha through a S6K1-dependent mechanism in breast cancer cells. Mol Endocrinol 25:516–528PubMedPubMedCentral

150.

Campbell RA, Bhat-Nakshatri P, Patel NM, Constantinidou D, Ali S, Nakshatri H (2001) Phosphatidylinositol 3-kinase/AKT-mediated activation of estrogen receptor alpha: a new model for anti-estrogen resistance. J Biol Chem 276:9817–9824PubMed

151.

Lee AV, Weng CN, Jackson JG, Yee D (1997) Activation of estrogen receptor-mediated gene transcription by IGF-I in human breast cancer cells. J Endocrinol 152:39–47PubMed

152.

Stoica A, Saceda M, Doraiswamy VL, Coleman C, Martin MB (2000) Regulation of estrogen receptor-alpha gene expression by epidermal growth factor. J Endocrinol 165:371–378PubMed

153.

Stoica A, Saceda M, Fakhro A, Harrison BS, Fenster BD, Martin MB (1997) The role of transforming growth factor-beta in the regulation of estrogen receptor expression in the MCF-7 breast cancer cell line. Endocrinology 138:1498–1505PubMed

154.

Stoica A, Saceda M, Fakhro A, Joyner M, Martin MB (2000) Role of insulin-like growth factor-1 in regulating estrogen receptor-alpha gene expression. J Cell Biochem 76:605–614PubMed

155.

Lang JD, Berry SM, Powers GL, Beebe DJ, Alarid ET (2013) Hormonally responsive breast cancer cells in a microfluidic co-culture model as a sensor of microenvironmental activity. Integrative Biology : Quantitative Biosciences from Nano to Macro 5:807–816

156.

Stossi F, Madak-Erdogan Z, Katzenellenbogen BS (2012) Macrophage-elicited loss of estrogen receptor-alpha in breast cancer cells via involvement of MAPK and c-Jun at the ESR1 genomic locus. Oncogene 31:1825–1834PubMed

157.

Yao-Borengasser A, Monzavi-Karbassi B, Hedges RA, Rogers LJ, Kadlubar SA, Kieber-Emmons T (2015) Adipocyte hypoxia promotes epithelial-mesenchymal transition-related gene expression and estrogen receptor-negative phenotype in breast cancer cells. Oncol Rep 33:2689–2694PubMedPubMedCentral

158.

Ryu K, Park C, Lee Y (2011) Hypoxia-inducible factor 1 alpha represses the transcription of the estrogen receptor alpha gene in human breast cancer cells. Biochem Biophys Res Commun 407:831–836PubMed

159.

Lloyd MC, Alfarouk KO, Verduzco D, Bui MM, Gillies RJ, Ibrahim ME, Brown JS, Gatenby RA (2014) Vascular measurements correlate with estrogen receptor status. BMC Cancer 14:279PubMedPubMedCentral

160.

Coleman RE, Rubens RD (1987) The clinical course of bone metastases from breast cancer. Br J Cancer 55:61–66PubMedPubMedCentral

161.

Huang J, Woods P, Normolle D, Goff JP, Benos PV, Stehle CJ, Steinman RA (2016) Downregulation of estrogen receptor and modulation of growth of breast cancer cell lines mediated by paracrine stromal cell signals. Breast Cancer Res Treat 161:229–243PubMedPubMedCentral

162.

Brechbuhl HM, Finlay-Schultz J, Yamamoto TM, Gillen AE, Cittelly DM, Tan AC, Sams SB, Pillai MM, Elias AD, Robinson WA, Sartorius CA, Kabos P (2017) Fibroblast subtypes regulate responsiveness of luminal breast cancer to estrogen. Clin Cancer Res 23:1710–1721PubMed

163.

Lung DK, Warrick JW, Hematti P, Callander NS, Mark CJ, Miyamoto S, Alarid ET (2019) Bone marrow stromal cells transcriptionally repress ESR1 but cannot overcome constitutive ESR1 mutant activity. Endocrinology 160:2427–2440PubMedPubMedCentral

164.

Hoadley KA, Yau C, Hinoue T, Wolf DM, Lazar AJ, Drill E, Shen R, Taylor AM, Cherniack AD, Thorsson V, Akbani R, Bowlby R, Wong CK, Wiznerowicz M, Sanchez-Vega F, Robertson AG, Schneider BG, Lawrence MS, Noushmehr H, Malta TM, Network Cancer Genome Atlas, Stuart JM, Benz CC, Laird PW (2018) Cell-of-origin patterns dominate the molecular classification of 10,000 tumors from 33 types of cancer. Cell 173(291–304):e296

165.

Pereira B, Chin SF, Rueda OM, Vollan HK, Provenzano E, Bardwell HA, Pugh M, Jones L, Russell R, Sammut SJ, Tsui DW, Liu B, Dawson SJ, Abraham J, Northen H, Peden JF, Mukherjee A, Turashvili G, Green AR, McKinney S, Oloumi A, Shah S, Rosenfeld N, Murphy L, Bentley DR, Ellis IO, Purushotham A, Pinder SE, Borresen-Dale AL, Earl HM, Pharoah PD, Ross MT, Aparicio S, Caldas C (2016) The somatic mutation profiles of 2,433 breast cancers refines their genomic and transcriptomic landscapes. Nat Commun 7:11479PubMedPubMedCentral

166.

Cohn CS, Sullivan JA, Kiefer T, Hill SM (1999) Identification of an enhancer element in the estrogen receptor upstream region: implications for regulation of ER transcription in breast cancer. Mol Cell Endocrinol 158:25–36PubMed

167.

Macaluso M, Cinti C, Russo G, Russo A, Giordano A (2003) pRb2/p130-E2F4/5-HDAC1-SUV39H1-p300 and pRb2/p130-E2F4/5-HDAC1-SUV39H1-DNMT1 multimolecular complexes mediate the transcription of estrogen receptor-alpha in breast cancer. Oncogene 22:3511–3517PubMed

168.

Gertz J, Reddy TE, Varley KE, Garabedian MJ, Myers RM (2012) Genistein and bisphenol A exposure cause estrogen receptor 1 to bind thousands of sites in a cell type-specific manner. Genome Res 22:2153–2162PubMedPubMedCentral

169.

Snyder M, M Gerstein, S Weissman, PJ Farnham, K Struhl: ENCODE Transcription Factor Binding Sites by ChIP-seq from Stanford/Yale/USC/Harvard (GSE31477). http://www.encodeproject.org/, 2011,

170.

deGraffenried LA, Hopp TA, Valente AJ, Clark RA, Fuqua SA (2004) Regulation of the estrogen receptor alpha minimal promoter by Sp1, USF-1 and ERalpha. Breast Cancer Res Treat 85:111–120PubMed

171.

Angeloni SV, Martin MB, Garcia-Morales P, Castro-Galache MD, Ferragut JA, Saceda M (2004) Regulation of estrogen receptor-alpha expression by the tumor suppressor gene p53 in MCF-7 cells. J Endocrinol 180:497–504PubMed

172.

Tomita S, Abdalla MO, Fujiwara S, Matsumori H, Maehara K, Ohkawa Y, Iwase H, Saitoh N, Nakao M (2015) A cluster of noncoding RNAs activates the ESR1 locus during breast cancer adaptation. Nat Commun 6:6966PubMed

173.

McPherson LA, Weigel RJ (1999) AP2alpha and AP2gamma: a comparison of binding site specificity and trans-activation of the estrogen receptor promoter and single site promoter constructs. Nucleic Acids Res 27:4040–4049PubMedPubMedCentral

174.

Hosey AM, Gorski JJ, Murray MM, Quinn JE, Chung WY, Stewart GE, James CR, Farragher SM, Mulligan JM, Scott AN, Dervan PA, Johnston PG, Couch FJ, Daly PA, Kay E, McCann A, Mullan PB, Harkin DP (2007) Molecular basis for estrogen receptor alpha deficiency in BRCA1-linked breast cancer. J Natl Cancer Inst 99:1683–1694PubMed

175.

Chiang HC, Zhang X, Li J, Zhao X, Chen J, Wang HT, Jatoi I, Brenner A, Hu Y, Li R (2019) BRCA1-associated R-loop affects transcription and differentiation in breast luminal epithelial cells. Nucleic Acids Res 47:5086–5099PubMedPubMedCentral

176.

Madureira PA, Varshochi R, Constantinidou D, Francis RE, Coombes RC, Yao KM, Lam EW (2006) The Forkhead box M1 protein regulates the transcription of the estrogen receptor alpha in breast cancer cells. J Biol Chem 281:25167–25176PubMed

177.

Furey TS, Z Zhang, L Song, G Crawford, P Giresi, J Lieb, Z Liu, R McDaniell, B Lee, VR Iyer, P Flicek, D Keefe, E Birney, S Graf: Open Chromatin TFBS by ChIP-seq from ENCODE/Open Chrom(UT Austin) (GSE33213). http://www.encodeproject.org, 2011,

178.

Bernardo GM, Lozada KL, Miedler JD, Harburg G, Hewitt SC, Mosley JD, Godwin AK, Korach KS, Visvader JE, Kaestner KH, Abdul-Karim FW, Montano MM, Keri RA (2010) FOXA1 is an essential determinant of ERalpha expression and mammary ductal morphogenesis. Development 137:2045–2054PubMedPubMedCentral

179.

Han Y, Yang L, Suarez-Saiz F, San-Marina S, Cui J, Minden MD (2008) Wilms’ tumor 1 suppressor gene mediates antiestrogen resistance via down-regulation of estrogen receptor-alpha expression in breast cancer cells. Mol Cancer Res 6:1347–1355PubMed

180.

De Amicis F, Zupo S, Panno ML, Malivindi R, Giordano F, Barone I, Mauro L, Fuqua SA, Ando S (2009) Progesterone receptor B recruits a repressor complex to a half-PRE site of the estrogen receptor alpha gene promoter. Mol Endocrinol 23:454–465PubMedPubMedCentral

181.

Stevens TA, Meech R (2006) BARX2 and estrogen receptor-alpha (ESR1) coordinately regulate the production of alternatively spliced ESR1 isoforms and control breast cancer cell growth and invasion. Oncogene 25:5426–5435PubMed

182.

Molloy ME, Lewinska M, Williamson AK, Nguyen TT, Kuser-Abali G, Gong L, Yan J, Little JB, Pandolfi PP, Yuan ZM (2018) ZBTB7A governs estrogen receptor alpha expression in breast cancer. J Mol Cell Biol 10:273–284PubMedPubMedCentral

183.

Hata T, Rajabi H, Takahashi H, Yasumizu Y, Li W, Jin C, Long MD, Hu Q, Liu S, Fushimi A, Yamashita N, Kui L, Hong D, Yamamoto M, Miyo M, Hiraki M, Maeda T, Suzuki Y, Samur MK, Kufe D (2019) MUC1-C activates the NuRD complex to drive dedifferentiation of triple-negative breast cancer cells. Cancer Res 79:5711–5722PubMedPubMedCentral

184.

Zhang Q, Liu XY, Li S, Zhao Z, Li J, Cui MK, Wang EH (2017) Repression of ESR1 transcription by MYOD potentiates letrozole-resistance in ERalpha-positive breast cancer cells. Biochem Biophys Res Commun 492:425–433PubMed

185.

Ye L, Lin C, Wang X, Li Q, Li Y, Wang M, Zhao Z, Wu X, Shi D, Xiao Y, Ren L, Jian Y, Yang M, Ou R, Deng G, Ouyang Y, Chen X, Li J, Song L (2019) Epigenetic silencing of SALL2 confers tamoxifen resistance in breast cancer. EMBO Mol Med 11:e10638PubMedPubMedCentral

186.

Kim SS, Lee MH, Lee MO (2020) Histone methyltransferases regulate the transcriptional expression of ERalpha and the proliferation of tamoxifen-resistant breast cancer cells. Breast Cancer Res Treat

187.

El Khissiin A, Leclercq G (1999) Implication of proteasome in estrogen receptor degradation. FEBS Lett 448:160–166PubMed

188.

Adams BD, Cowee DM, White BA (2009) The role of miR-206 in the epidermal growth factor (EGF) induced repression of estrogen receptor-alpha (ERalpha) signaling and a luminal phenotype in MCF-7 breast cancer cells. Mol Endocrinol 23:1215–1230PubMedPubMedCentral

189.

Bhat-Nakshatri P, Campbell RA, Patel NM, Newton TR, King AJ, Marshall MS, Ali S, Nakshatri H (2004) Tumour necrosis factor and PI3-kinase control oestrogen receptor alpha protein level and its transrepression function. Br J Cancer 90:853–859PubMedPubMedCentral

190.

DuSell CD, Umetani M, Shaul PW, Mangelsdorf DJ, McDonnell DP (2008) 27-Hydroxycholesterol is an endogenous selective estrogen receptor modulator. Mol Endocrinol 22:65–77PubMed

191.

West NR, Murphy LC, Watson PH (2012) Oncostatin M suppresses oestrogen receptor-alpha expression and is associated with poor outcome in human breast cancer. Endocr Relat Cancer 19:181–195PubMed

192.

Gutzman JH, Miller KK, Schuler LA (2004) Endogenous human prolactin and not exogenous human prolactin induces estrogen receptor alpha and prolactin receptor expression and increases estrogen responsiveness in breast cancer cells. J Steroid Biochem Mol Biol 88:69–77PubMed

193.

Weitsman GE, Weebadda W, Ung K, Murphy LC (2009) Reactive oxygen species induce phosphorylation of serine 118 and 167 on estrogen receptor alpha. Breast Cancer Res Treat 118:269–279PubMed

194.

Martin MB, Reiter R, Pham T, Avellanet YR, Camara J, Lahm M, Pentecost E, Pratap K, Gilmore BA, Divekar S, Dagata RS, Bull JL, Stoica A (2003) Estrogen-like activity of metals in MCF-7 breast cancer cells. Endocrinology 144:2425–2436PubMed

195.

Garcia-Morales P, Saceda M, Kenney N, Kim N, Salomon DS, Gottardis MM, Solomon HB, Sholler PF, Jordan VC, Martin MB (1994) Effect of cadmium on estrogen receptor levels and estrogen-induced responses in human breast cancer cells. J Biol Chem 269:16896–16901PubMed

196.

Creighton CJ, Hilger AM, Murthy S, Rae JM, Chinnaiyan AM, El-Ashry D (2006) Activation of mitogen-activated protein kinase in estrogen receptor alpha-positive breast cancer cells in vitro induces an in vivo molecular phenotype of estrogen receptor alpha-negative human breast tumors. Cancer Res 66:3903–3911PubMed

197.

Bhatt S, Xiao Z, Meng Z, Katzenellenbogen BS (2012) Phosphorylation by p38 mitogen-activated protein kinase promotes estrogen receptor alpha turnover and functional activity via the SCF(Skp2) proteasomal complex. Mol Cell Biol 32:1928–1943PubMedPubMedCentral

198.

Stoner M, Saville B, Wormke M, Dean D, Burghardt R, Safe S (2002) Hypoxia induces proteasome-dependent degradation of estrogen receptor alpha in ZR-75 breast cancer cells. Mol Endocrinol 16:2231–2242PubMed

199.

Jimenez-Garduno AM, Mendoza-Rodriguez MG, Urrutia-Cabrera D, Dominguez-Robles MC, Perez-Yepez EA, Ayala-Sumuano JT, Meza I (2017) IL-1beta induced methylation of the estrogen receptor ERalpha gene correlates with EMT and chemoresistance in breast cancer cells. Biochem Biophys Res Commun 490:780–785PubMed

200.

Holton SE, Bergamaschi A, Katzenellenbogen BS, Bhargava R (2014) Integration of molecular profiling and chemical imaging to elucidate fibroblast-microenvironment impact on cancer cell phenotype and endocrine resistance in breast cancer. PLoS One 9:e96878PubMedPubMedCentral

201.

Bliss SA, Sinha G, Sandiford OA, Williams LM, Engelberth DJ, Guiro K, Isenalumhe LL, Greco SJ, Ayer S, Bryan M, Kumar R, Ponzio NM, Rameshwar P (2016) Mesenchymal stem cell-derived exosomes stimulate cycling quiescence and early breast cancer dormancy in bone marrow. Cancer Res 76:5832–5844PubMed

202.

Morgan MM, Livingston MK, Warrick JW, Stanek EM, Alarid ET, Beebe DJ, Johnson BP (2018) Mammary fibroblasts reduce apoptosis and speed estrogen-induced hyperplasia in an organotypic MCF7-derived duct model. Sci Rep 8:7139PubMedPubMedCentral

203.

Shah SH, Miller P, Garcia-Contreras M, Ao Z, Machlin L, Issa E, El-Ashry D (2015) Hierarchical paracrine interaction of breast cancer associated fibroblasts with cancer cells via hMAPK-microRNAs to drive ER-negative breast cancer phenotype. Cancer Biology & Therapy 16:1671–1681

204.

Lim PK, Bliss SA, Patel SA, Taborga M, Dave MA, Gregory LA, Greco SJ, Bryan M, Patel PS, Rameshwar P (2011) Gap junction-mediated import of microRNA from bone marrow stromal cells can elicit cell cycle quiescence in breast cancer cells. Cancer Res 71:1550–1560PubMed

Titel: Intrinsic and Extrinsic Factors Governing the Transcriptional Regulation of ESR1
verfasst von: David K. Lung
Rebecca M. Reese
Elaine T. Alarid
Publikationsdatum: 26.06.2020
Verlag: Springer US
Erschienen in: Discover Oncology / Ausgabe 3-4/2020
Print ISSN: 1868-8497
Elektronische ISSN: 2730-6011
DOI: https://doi.org/10.1007/s12672-020-00388-0

Springer Medizin

Intrinsic and Extrinsic Factors Governing the Transcriptional Regulation of ESR1

Abstract

Neu im Fachgebiet Onkologie

Adjuvante Immuntherapie verlängert Leben bei RCC

Alectinib verbessert krankheitsfreies Überleben bei ALK-positivem NSCLC

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ICI-Therapie in der Schwangerschaft wird gut toleriert

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Springer Medizin

Abstract

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