Transcription Factor Ets1 Cooperates with Estrogen Receptor α to Stimulate Estradiol-Dependent Growth in Breast Cancer Cells and Tumors

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Kalet, Brian T ^a   Anglin, Sara R ^a   Handschy, Anne ^a   O'Donoghue, Liza E ^a   Halsey, Charles ^a   Chubb, Laura ^a   Korch, Christopher ^b,c   Duval, Dawn L ^a,c  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF COLORADO CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; KI 67 ANTIGEN; NUCLEAR RECEPTOR COACTIVATOR; PROTEIN P160; TRANSCRIPTION FACTOR ETS 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BINDING AFFINITY; BREAST CANCER; CANCER CELL; CANCER GROWTH; CANCER INHIBITION; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; COLONY FORMATION; CONTROLLED STUDY; FEMALE; GENE TARGETING; HORMONE BINDING; HORMONE RESPONSE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSCRIPTION INITIATION; TUMOR GROWTH; TUMOR VOLUME;

ANIMALS; ANTIGENS, CD31; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION; HUMANS; KI-67 ANTIGEN; MCF-7 CELLS; MICE; MULTIPROTEIN COMPLEXES; PROTEIN BINDING; PROTO-ONCOGENE PROTEIN C-ETS-1; RESPONSE ELEMENTS; TUMOR BURDEN; TUMOR STEM CELL ASSAY;

LOTUS; MUS MUSCULUS;

EID: 84879909340     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068815     Document Type: Article

References (60)

1. Kim HJ, Cui X, Hilsenbeck SG, Lee AV, (2006) Progesterone receptor loss correlates with human epidermal growth factor receptor 2 overexpression in estrogen receptor-positive breast cancer. Clin Cancer Res 12: 1013s-1018s.
2. Rau KM, Kang HY, Cha TL, Miller SA, Hung MC, (2005) The mechanisms and managements of hormone-therapy resistance in breast and prostate cancers. Endocr Relat Cancer 12: 511-532.
3. Zhou Y, Eppenberger-Castori S, Eppenberger U, Benz CC, (2005) The NFkappaB pathway and endocrine-resistant breast cancer. Endocr Relat Cancer 12Suppl 1: S37-46.
4. Prescott JD, Koto KS, Singh M, Gutierrez-Hartmann A, (2004) The ETS transcription factor ESE-1 transforms MCF-12A human mammary epithelial cells via a novel cytoplasmic mechanism. Mol Cell Biol 24: 5548-5564.
5. Myers E, Hill AD, Kelly G, McDermott EW, O'Higgins NJ, et al. (2005) Associations and interactions between Ets-1 and Ets-2 and coregulatory proteins, SRC-1, AIB1, and NCoR in breast cancer. Clin Cancer Res 11: 2111-2122.
6. Mitas M, Mikhitarian K, Hoover L, Lockett MA, Kelley L, et al. (2002) Prostate-Specific Ets (PSE) factor: a novel marker for detection of metastatic breast cancer in axillary lymph nodes. Br J Cancer 86: 899-904.
7. Hsu T, Trojanowska M, Watson DK, (2004) Ets proteins in biological control and cancer. J Cell Biochem 91: 896-903.
8. Seth A, Watson DK, (2005) ETS transcription factors and their emerging roles in human cancer. European Journal of Cancer 41: 2462-2478.
9. Span PN, Manders P, Heuvel JJ, Thomas CMG, Bosch RR, et al. (2002) Expression of the transcription factor Ets-1 is an independent prognostic marker for relapse-free survival in breast cancer. Oncogene 21: 8506-8509.
10. Barrett JM, Puglia MA, Singh G, Tozer RG, (2002) Expression of Ets-related transcription factors and matrix metalloproteinase genes in human breast cancer cells. Breast Cancer Res Treat 72: 227-232.
11. Zhang Y, Yan LX, Wu QN, Du ZM, Chen J, et al. (2011) miR-125b is methylated and functions as a tumor suppressor by regulating the ETS1 proto-oncogene in human invasive breast cancer. Cancer Res 71: 3552-3562.
12. Neznanov N, Man AK, Yamamoto H, Hauser CA, Cardiff RD, et al. (1999) A single targeted Ets2 allele restricts development of mammary tumors in transgenic mice. Cancer Res 59: 4242-4246.
13. Schedin PJ, Eckel-Mahan KL, McDaniel SM, Prescott JD, Brodsky KS, et al. (2004) ESX induces transformation and functional epithelial to mesenchymal transition in MCF-12A mammary epithelial cells. Oncogene 23: 1766-1779.
14. Sun Z, Asmann YW, Kalari KR, Bot B, Eckel-Passow JE, et al. (2011) Integrated analysis of gene expression, CpG island methylation, and gene copy number in breast cancer cells by deep sequencing. PLoS One 6: e17490.
15. He J, Pan Y, Hu J, Albarracin C, Wu Y, et al. (2007) Profile of Ets gene expression in human breast carcinoma. Cancer Biol Ther 6: 76-82.
16. Ronneberg JA, Fleischer T, Solvang HK, Nordgard SH, Edvardsen H, et al. (2011) Methylation profiling with a panel of cancer related genes: association with estrogen receptor, TP53 mutation status and expression subtypes in sporadic breast cancer. Mol Oncol 5: 61-76.
17. Donaldson LW, Petersen JM, Graves BJ, McIntosh LP, (1994) Secondary structure of the ETS domain places murine Ets-1 in the superfamily of winged helix-turn-helix DNA-binding proteins. Biochemistry 33: 13509-13516.
18. Donaldson LW, Petersen JM, Graves BJ, McIntosh LP, (1996) Solution structure of the ETS domoain from mruine Ets-1: A winged helix-turn-helix DNA-binding motif. EMBO J 15: 125-134.
19. Xie M, Zhang D, Dyck JR, Li Y, Zhang H, et al. (2006) A pivotal role for endogenous TGF-beta-activated kinase-1 in the LKB1/AMP-activated protein kinase energy-sensor pathway. Proc Natl Acad Sci U S A 103: 17378-17383.
20. Foulds CE, Nelson ML, Blaszczak AG, Graves BJ, (2004) Ras/mitogen-activated protein kinase signaling activates Ets-1 and Ets-2 by CBP/p300 recruitment. Mol Cell Biol 24: 10954-10964.
21. Long W, Foulds CE, Qin J, Liu J, Ding C, et al. (2012) ERK3 signals through SRC-3 coactivator to promote human lung cancer cell invasion. J Clin Invest 122: 1869-1880.
22. Goel A, Janknecht R, (2004) Concerted activation of ETS protein ER81 by p160 coactivators, the acetyltransferase p300 and the receptor tyrosine kinase HER2/Neu. J Biol Chem 279: 14909-14916.
23. Xu J, Li Q, (2003) Review of the in vivo functions of the p160 steroid receptor coactivator family. Mol Endocrinol 17: 1681-1692.
24. Xu J, Wu RC, O'Malley BW, (2009) Normal and cancer-related functions of the p160 steroid receptor co-activator (SRC) family. Nat Rev Cancer 9: 615-630.
25. Giraud S, Bienvenu F, Avril S, Gascan H, Heery DM, et al. (2002) Functional interaction of STAT3 transcription factor with the coactivator NcoA/SRC1a. J Biol Chem 277: 8004-8011.
26. Tolon RM, Castillo AI, Jimenez-Lara AM, Aranda A, (2000) Association with Ets-1 causes ligand- and AF2-independent activation of nuclear receptors. Mol Cell Biol 20: 8793-8802.
27. Massie CE, Adryan B, Barbosa-Morais NL, Lynch AG, Tran MG, et al. (2007) New androgen receptor genomic targets show an interaction with the ETS1 transcription factor. Embo Reports 8: 871-878.
28. Ritter HD, Antonova L, Mueller CR, (2012) The unliganded glucocorticoid receptor positively regulates the tumor suppressor gene BRCA1 through GABP beta. Mol Cancer Res 10: 558-569.
29. Young RK, Cailleau RM, Mackay B, Reeves WJ, (1974) Establishment of epithelial cell line MDA-MB-157 from metastatic pleural effusion of human breast carcinoma. In Vitro 9: 239-245.
30. Horwitz KB, Costlow ME, McGuire WL, (1975) MCF-7; a human breast cancer cell line with estrogen, androgen, progesterone, and glucocorticoid receptors. Steroids 26: 785-795.
31. Lasfargues EY, Coutinho WG, Redfield ES, (1978) Isolation of two human tumor epithelial cell lines from solid breast carcinomas. J Natl Cancer Inst 61: 967-978.
32. Cailleau R, Olive M, Cruciger QV, (1978) Long-term human breast carcinoma cell lines of metastatic origin: preliminary characterization. In Vitro 14: 911-915.
33. Engel LW, Young NA, Tralka TS, Lippman ME, O'Brien SJ, et al. (1978) Establishment and characterization of three new continuous cell lines derived from human breast carcinomas. Cancer Res 38: 3352-3364.
34. Lamp SJ, Findlay DM, Moseley JM, Martin TJ, (1981) Calcitonin induction of a persistent activated state of adenylate cyclase in human breast cancer cells (T 47D). J Biol Chem 256: 12269-12274.
35. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
36. Wasylyk C, Kerckaert JP, Wasylyk B, (1992) A novel modulator domain of Ets transcription factors. Genes Dev 6: 965-974.
37. Ahmed SA, Gogal RM Jr, Walsh JE, (1994) A new rapid and simple non-radioactive assay to monitor and determine the proliferation of lymphocytes: an alternative to [3H]thymidine incorporation assay. J Immunol Methods 170: 211-224.
38. Sartorius CA, Shen T, Horwitz KB, (2003) Progesterone receptors A and B differentially affect the growth of estrogen-dependent human breast tumor xenografts. Breast Cancer Res Treat 79: 287-299.
39. Kalet BT, McBryde MB, Espinosa JM, Koch TH, (2007) Doxazolidine induction of apoptosis by a topoisomerase II independent mechanism. J Med Chem 50: 4493-4500.
40. Duval DL, Jean A, Gutierrez-Hartmann A, (2003) Ras signaling and transcriptional synergy at a flexible Ets-1/Pit-1 composite DNA element is defined by the assembly of selective activation domains. Journal of Biological Chemistry 278: 39684-39696.
41. Lacroix M, Leclercq G, (2004) Relevance of breast cancer cell lines as models for breast tumours: an update. Breast Cancer Research and Treatment 83: 249-289.
42. Dittmer J, (2006) Does a truncated form of the transcription factor Ets1 exist in breast cancer cells? Br J Cancer 94: 176-177.
43. Dittmer J, (2003) The biology of the Ets1 proto-oncogene. Mol Cancer 2: 29.
44. Sartorius (2003) Progesterone receptors A and B differentially affect the growth of estrogen-dependent human breast tumor xenografts. Breast Cancer Research and Treatment 79: 287-299.
45. Soule HD, McGrath CM, (1980) Estrogen responsive proliferation of clonal human breast carcinoma cells in athymic mice. Cancer Lett 10: 177-189.
46. Lin CY, Strom A, Vega VB, Kong SL, Yeo AL, et al. (2004) Discovery of estrogen receptor alpha target genes and response elements in breast tumor cells. Genome Biol 5: R66.
47. Kyprianou N, English HF, Davidson NE, Isaacs JT, (1991) Programmed cell death during regression of the MCF-7 human breast cancer following estrogen ablation. Cancer Res 51: 162-166.
48. Mullen P, Ritchie A, Langdon SP, Miller WR, (1996) Effect of Matrigel on the tumorigenicity of human breast and ovarian carcinoma cell lines. Int J Cancer 67: 816-820.
49. Yue W, Brodie A, (1993) MCF-7 human breast carcinomas in nude mice as a model for evaluating aromatase inhibitors. J Steroid Biochem Mol Biol 44: 671-673.
50. Scholzen T, Gerdes J, (2000) The Ki-67 protein: from the known and the unknown. J Cell Physiol 182: 311-322.
51. Gong P, Wang Y, Liu G, Zhang J, Wang Z, (2013) New insight into ki67 expression at the invasive front in breast cancer. PLoS One 8: e54912.
52. Mastronardi L, Guiducci A, Puzzilli F, (2001) Lack of correlation between Ki-67 labelling index and tumor size of anterior pituitary adenomas. BMC Cancer 1: 12.
53. McIntyre A, Patiar S, Wigfield S, Li JL, Ledaki I, et al. (2012) Carbonic anhydrase IX promotes tumor growth and necrosis in vivo and inhibition enhances anti-VEGF therapy. Clin Cancer Res 18: 3100-3111.
54. Salnikow K, Aprelikova O, Ivanov S, Tackett S, Kaczmarek M, et al. (2008) Regulation of hypoxia-inducible genes by ETS1 transcription factor. Carcinogenesis 29: 1493-1499.
55. Wernert N, Raes MB, Lassalle P, Dehouck MP, Gosselin B, et al. (1992) c-ets1 proto-oncogene is a transcription factor expressed in endothelial cells during tumor vascularization and other forms of angiogenesis in humans. Am J Pathol 140: 119-127.
56. Karmakar S, Foster EA, Smith CL, (2009) Unique roles of p160 coactivators for regulation of breast cancer cell proliferation and estrogen receptor-alpha transcriptional activity. Endocrinology 150: 1588-1596.
57. Eckel KL, Tentler JJ, Cappetta GJ, Diamond SE, Gutierrez-Hartmann A, (2003) The epithelial-specific ETS transcription factor ESX/ESE-1/Elf-3 modulates breast cancer-associated gene expression. DNA Cell Biol 22: 79-94.
58. Osborne CK, Shou J, Massarweh S, Schiff R, (2005) Crosstalk between estrogen receptor and growth factor receptor pathways as a cause for endocrine therapy resistance in breast cancer. Clinical Cancer Research 11: 865s-870s.
59. Arpino G, Wiechmann L, Osborne CK, Schiff R, (2008) Crosstalk between the estrogen receptor and the HER tyrosine kinase receptor family: molecular mechanism and clinical implications for endocrine therapy resistance. Endocr Rev 29: 217-233.
60. Duplessis TT, Williams CC, Hill SM, Rowan BG, (2011) Phosphorylation of Estrogen Receptor alpha at serine 118 directs recruitment of promoter complexes and gene-specific transcription. Endocrinology 152: 2517-2526.