Acquisition of epithelial-mesenchymal transition phenotype in the tamoxifen-resistant breast cancer cell: A new role for G protein-coupled estrogen receptor in mediating tamoxifen resistance through cancer-associated fibroblast-derived fibronectin and β1-integrin signaling pathway in tumor cells

Breast Cancer Research

Volumn 17, Issue 1, 2015, Pages

  Yuan, Jie ^a   Liu, Manran ^b   Yang, Li ^b   Tu, Gang ^a   Zhu, Qing ^a   Chen, Maoshan ^a   Cheng, Hong ^a   Luo, Haojun ^a   Fu, Weijie ^a   Li, Zhenhua ^a   Yang, Guanglun ^a  

^a THE FIRST AFFILIATED HOSPITAL OF CHONGQING MEDICAL UNIVERSITY   (China)

^b CHONGQING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTEGRIN; FIBRONECTIN; FOCAL ADHESION KINASE; G PROTEIN COUPLED RECEPTOR 30; PROTEIN KINASE B; PROTEIN TYROSINE KINASE; TAMOXIFEN; VIMENTIN; ANTINEOPLASTIC HORMONE AGONISTS AND ANTAGONISTS; BIOLOGICAL MARKER; EPIDERMAL GROWTH FACTOR RECEPTOR; ESTROGEN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; SELECTIVE ESTROGEN RECEPTOR MODULATOR;

ARTICLE; BREAST CANCER CELL LINE; CANCER ASSOCIATED FIBROBLAST; CANCER RESISTANCE; CELL MIGRATION; CONTROLLED STUDY; DISTANT METASTASIS; EPIDERMAL GROWTH FACTOR RECEPTOR EXTRACELLULAR REGULATED PROTEIN KINASE SIGNALING PATHWAY; EPITHELIAL MESENCHYMAL TRANSITION; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MCF 7 CELL LINE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UPREGULATION; WESTERN BLOTTING; BREAST NEOPLASMS; DRUG EFFECTS; DRUG RESISTANCE; FEMALE; GENETICS; MCF-7 CELL LINE; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ANTIGENS, CD29; ANTINEOPLASTIC AGENTS, HORMONAL; BIOMARKERS; BREAST NEOPLASMS; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; FIBROBLASTS; FIBRONECTINS; FOCAL ADHESION PROTEIN-TYROSINE KINASES; HUMANS; IMMUNOHISTOCHEMISTRY; MCF-7 CELLS; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, ESTROGEN; SELECTIVE ESTROGEN RECEPTOR MODULATORS; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TAMOXIFEN;

EID: 84930662180     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/s13058-015-0579-y     Document Type: Article

References (49)

1. Briest S, Stearns V. Tamoxifen metabolism and its effect on endocrine treatment of breast cancer. Clin Adv Hematol Oncol. 2009;7:185-92.
2. Cui J, Germer K, Wu T, Wang J, Luo J, Wang SC, et al. Cross-talk between HER2 and MED1 regulates tamoxifen resistance of human breast cancer cells. Cancer Res. 2012;72:5625-34.
3. Fagan DH, Uselman RR, Sachdev D, Yee D. Acquired resistance to tamoxifen is associated with loss of the type I insulin-like growth factor receptor: implications for breast cancer treatment. Cancer Res. 2012;72:3372-80.
4. Yi EH, Lee CS, Lee JK, Lee YJ, Shin MK, Cho CH, et al. STAT3-RANTES autocrine signaling is essential for tamoxifen resistance in human breast cancer cells. Mol Cancer Res. 2013;11:31-42.
5. Shah N, Jin K, Cruz LA, Park S, Sadik H, Cho S, et al. HOXB13 mediates tamoxifen resistance and invasiveness in human breast cancer by suppressing ERalpha and inducing IL-6 expression. Cancer Res. 2013;73:5449-58.
6. Desgrosellier JS, Cheresh DA. Integrins in cancer: biological implications and therapeutic opportunities. Nat Rev Cancer. 2010;10:9-22.
7. Goetz JG, Minguet S, Navarro-Lerida I, Lazcano JJ, Samaniego R, Calvo E, et al. Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell. 2011;146:148-63.
8. Zhang X, Liu G, Kang Y, Dong Z, Qian Q, Ma X. N-cadherin expression is associated with acquisition of EMT phenotype and with enhanced invasion in erlotinib-resistant lung cancer cell lines. PLoS One. 2013;8:e57692.
9. Neel DS, Bivona TG. Secrets of drug resistance in NSCLC exposed by new molecular definition of EMT. Clin Cancer Res. 2013;19:3-5.
10. Thiery JP, Acloque H, Huang RY, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell. 2009;139:871-90.
11. Fantozzi A, Gruber DC, Pisarsky L, Heck C, Kunita A, Yilmaz M, et al. VEGF-mediated angiogenesis links EMT-induced cancer stemness to tumor initiation. Cancer Res. 2014;74:1566-75.
12. Hiscox S, Jiang WG, Obermeier K, Taylor K, Morgan L, Burmi R, et al. Tamoxifen resistance in MCF7 cells promotes EMT-like behaviour and involves modulation of beta-catenin phosphorylation. Int J Cancer. 2006;118:290-301.
13. Ward A, Balwierz A, Zhang JD, Kublbeck M, Pawitan Y, Hielscher T, et al. Re-expression of microRNA-375 reverses both tamoxifen resistance and accompanying EMT-like properties in breast cancer. Oncogene. 2013;32:1173-82.
14. Oliveras-Ferraros C, Corominas-Faja B, Cufi S, Vazquez-Martin A, Martin-Castillo B, Iglesias JM, et al. Epithelial-to-mesenchymal transition (EMT) confers primary resistance to trastuzumab (Herceptin). Cell Cycle. 2012;11:4020-32.
15. Ignatov A, Ignatov T, Roessner A, Costa SD, Kalinski T. Role of GPR30 in the mechanisms of tamoxifen resistance in breast cancer MCF-7 cells. Breast Cancer Res Treat. 2010;123:87-96.
16. Ignatov A, Ignatov T, Weissenborn C, Eggemann H, Bischoff J, Semczuk A, et al. G-protein-coupled estrogen receptor GPR30 and tamoxifen resistance in breast cancer. Breast Cancer Res Treat. 2011;128:457-66.
17. Mo Z, Liu M, Yang F, Luo H, Li Z, Tu G, et al. GPR30 as an initiator of tamoxifen resistance in hormone-dependent breast cancer. Breast Cancer Res. 2013;15:R114.
18. Chen HM, Lin YH, Cheng YM, Wing LY, Tsai SJ. Overexpression of integrin-beta1 in leiomyoma promotes cell spreading and proliferation. J Clin Endocrinol Metab. 2013;98:E837-46.
19. Kocaturk B, Van den Berg YW, Tieken C, Mieog JS, de Kruijf EM, Engels CC, et al. Alternatively spliced tissue factor promotes breast cancer growth in a beta1 integrin-dependent manner. Proc Natl Acad Sci U S A. 2013;110:11517-22.
20. Hassan H, Greve B, Pavao MS, Kiesel L, Ibrahim SA, Gotte M. Syndecan-1 modulates beta-integrin-dependent and interleukin-6-dependent functions in breast cancer cell adhesion, migration, and resistance to irradiation. FEBS J. 2013;280:2216-27.
21. Huang C, Park CC, Hilsenbeck SG, Ward R, Rimawi MF, Wang YC, et al. beta1 integrin mediates an alternative survival pathway in breast cancer cells resistant to lapatinib. Breast Cancer Res. 2011;13:R84.
22. Pontiggia O, Sampayo R, Raffo D, Motter A, Xu R, Bissell MJ, et al. The tumor microenvironment modulates tamoxifen resistance in breast cancer: a role for soluble stromal factors and fibronectin through beta1 integrin. Breast Cancer Res Treat. 2012;133:459-71.
23. Coser KR, Wittner BS, Rosenthal NF, Collins SC, Melas A, Smith SL, et al. Antiestrogen-resistant subclones of MCF-7 human breast cancer cells are derived from a common monoclonal drug-resistant progenitor. Proc Natl Acad Sci U S A. 2009;106:14536-41.
24. Yu T, Liu M, Luo H, Wu C, Tang X, Tang S, et al. GPER mediates enhanced cell viability and motility via non-genomic signaling induced by 17beta-estradiol in triple-negative breast cancer cells. J Steroid Biochem Mol Biol. 2014;143:392-403.
25. Peng Q, Zhao L, Hou Y, Sun Y, Wang L, Luo H, et al. Biological characteristics and genetic heterogeneity between carcinoma-associated fibroblasts and their paired normal fibroblasts in human breast cancer. PLoS One. 2013;8:e60321.
26. Yao ES, Zhang H, Chen YY, Lee B, Chew K, Moore D, et al. Increased beta1 integrin is associated with decreased survival in invasive breast cancer. Cancer Res. 2007;67:659-64.
27. Mima K, Okabe H, Ishimoto T, Hayashi H, Nakagawa S, Kuroki H, et al. CD44s regulates the TGF-beta-mediated mesenchymal phenotype and is associated with poor prognosis in patients with hepatocellular carcinoma. Cancer Res. 2012;72:3414-23.
28. Sengupta S, Jordan VC. Selective estrogen modulators as an anticancer tool: mechanisms of efficiency and resistance. Adv Exp Med Biol. 2008;630:206-19.
29. Hutcheson IR, Knowlden JM, Madden TA, Barrow D, Gee JM, Wakeling AE, et al. Oestrogen receptor-mediated modulation of the EGFR/MAPK pathway in tamoxifen-resistant MCF-7 cells. Breast Cancer Res Treat. 2003;81:81-93.
30. Quinn JA, Graeber CT, Frackelton AJ, Kim M, Schwarzbauer JE, Filardo EJ. Coordinate regulation of estrogen-mediated fibronectin matrix assembly and epidermal growth factor receptor transactivation by the G protein-coupled receptor, GPR30. Mol Endocrinol. 2009;23:1052-64.
31. Goodman SL, Picard M. Integrins as therapeutic targets. Trends Pharmacol Sci. 2012;33:405-12.
32. Bergamaschi A, Tagliabue E, Sorlie T, Naume B, Triulzi T, Orlandi R, et al. Extracellular matrix signature identifies breast cancer subgroups with different clinical outcome. J Pathol. 2008;214:357-67.
33. Finak G, Bertos N, Pepin F, Sadekova S, Souleimanova M, Zhao H, et al. Stromal gene expression predicts clinical outcome in breast cancer. Nat Med. 2008;14:518-27.
34. Lebret SC, Newgreen DF, Thompson EW, Ackland ML. Induction of epithelial to mesenchymal transition in PMC42-LA human breast carcinoma cells by carcinoma-associated fibroblast secreted factors. Breast Cancer Res. 2007;9:R19.
35. Orimo A, Gupta PB, Sgroi DC, Arenzana-Seisdedos F, Delaunay T, Naeem R, et al. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell. 2005;121:335-48.
36. Radisky DC, Levy DD, Littlepage LE, Liu H, Nelson CM, Fata JE, et al. Rac1b and reactive oxygen species mediate MMP-3-induced EMT and genomic instability. Nature. 2005;436:123-7.
37. Thewes V, Simon R, Schroeter P, Schlotter M, Anzeneder T, Buttner R, et al. Reprogramming of the ERRalpha and ERalpha target gene landscape triggers tamoxifen resistance in breast cancer. Cancer Res. 2015;75:720-31.
38. Prossnitz ER, Maggiolini M. Mechanisms of estrogen signaling and gene expression via GPR30. Mol Cell Endocrinol. 2009;308:32-8.
39. Ahmed KM, Zhang H, Park CC. NF-kappaB regulates radioresistance mediated by beta1-integrin in three-dimensional culture of breast cancer cells. Cancer Res. 2013;73:3737-48.
40. Eke I, Deuse Y, Hehlgans S, Gurtner K, Krause M, Baumann M, et al. beta(1)Integrin/FAK/cortactin signaling is essential for human head and neck cancer resistance to radiotherapy. J Clin Invest. 2012;122:1529-40.
41. Zhou C, Zhong Q, Rhodes LV, Townley I, Bratton MR, Zhang Q, et al. Proteomic analysis of acquired tamoxifen resistance in MCF-7 cells reveals expression signatures associated with enhanced migration. Breast Cancer Res. 2012;14:R45.
42. Hiscox S, Barnfather P, Hayes E, Bramble P, Christensen J, Nicholson RI, et al. Inhibition of focal adhesion kinase suppresses the adverse phenotype of endocrine-resistant breast cancer cells and improves endocrine response in endocrine-sensitive cells. Breast Cancer Res Treat. 2011;125:659-69.
43. Hiscox S, Morgan L, Green TP, Barrow D, Gee J, Nicholson RI. Elevated Src activity promotes cellular invasion and motility in tamoxifen resistant breast cancer cells. Breast Cancer Res Treat. 2006;97:263-74.
44. Palacios F, Tushir JS, Fujita Y, D'Souza-Schorey C. Lysosomal targeting of E-cadherin: a unique mechanism for the down-regulation of cell-cell adhesion during epithelial to mesenchymal transitions. Mol Cell Biol. 2005;25:389-402.
45. Kato H, Liao Z, Mitsios JV, Wang HY, Deryugina EI, Varner JA, et al. The primacy of beta1 integrin activation in the metastatic cascade. PLoS One. 2012;7:e46576.
46. Nam JM, Ahmed KM, Costes S, Zhang H, Onodera Y, Olshen AB, et al. beta1-Integrin via NF-kappaB signaling is essential for acquisition of invasiveness in a model of radiation treated in situ breast cancer. Breast Cancer Res. 2013;15:R60.
47. Kakkad SM, Solaiyappan M, O'Rourke B, Stasinopoulos I, Ackerstaff E, Raman V, et al. Hypoxic tumor microenvironments reduce collagen I fiber density. Neoplasia. 2010;12:608-17.
48. Gao Y, Xiao Q, Ma H, Li L, Liu J, Feng Y, et al. LKB1 inhibits lung cancer progression through lysyl oxidase and extracellular matrix remodeling. Proc Natl Acad Sci U S A. 2010;107:18892-7.
49. Fata JE, Werb Z, Bissell MJ. Regulation of mammary gland branching morphogenesis by the extracellular matrix and its remodeling enzymes. Breast Cancer Res. 2004;6:1-11.