Epithelial-to-mesenchymal transition is not required for lung metastasis but contributes to chemoresistance

Nature

Volumn 527, Issue 7579, 2015, Pages 472-476

  Fischer, Kari R ^a,b   Durrans, Anna ^a   Lee, Sharrell ^a   Sheng, Jianting ^c   Li, Fuhai ^c   Wong, Stephen T C ^c   Choi, Hyejin ^a,b   El Rayes, Tina ^a,b   Ryu, Seongho ^a,d   Troeger, Juliane ^e,f   Schwabe, Robert F ^e,f   Vahdat, Linda T ^a   Altorki, Nasser K ^a   Mittal, Vivek ^a   Gao, Dingcheng ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b Weill Cornell Graduate School of Biomedical Sciences   (United States)

^c HOUSTON METHODIST HOSPITAL   (United States)

^d Soonchunhyang University   (South Korea)

^e Columbia University ^*  (United States)

^f Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLOPHOSPHAMIDE; MICRORNA 200; ALKYLATING AGENT; MICRORNA; MIRN200 MICRORNA, MOUSE;

CANCER; CHEMOTHERAPY; GENE EXPRESSION; HOMEOSTASIS; PHENOTYPE; TOLERANCE; TUMOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER RECURRENCE; CANCER RESISTANCE; CELL LINEAGE; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; LUNG METASTASIS; MOUSE; NONHUMAN; PHENOTYPE; PRIMARY TUMOR; PRIORITY JOURNAL; TRANSGENIC MOUSE; ANIMAL; APOPTOSIS; CELL PROLIFERATION; CELL TRACKING; DISEASE COURSE; DISEASE MODEL; DRUG EFFECTS; DRUG RESISTANCE; GENETICS; LUNG NEOPLASMS; MALE; MAMMARY NEOPLASMS, EXPERIMENTAL; NEOPLASM METASTASIS; PATHOLOGY; REPRODUCIBILITY; SECONDARY;

MUS;

ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; APOPTOSIS; CELL LINEAGE; CELL PROLIFERATION; CELL TRACKING; CYCLOPHOSPHAMIDE; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; LUNG NEOPLASMS; MALE; MAMMARY NEOPLASMS, EXPERIMENTAL; MICE; MICRORNAS; NEOPLASM METASTASIS; REPRODUCIBILITY OF RESULTS;

EID: 84948429460     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature15748     Document Type: Article

References (35)

1. Bastid, J. EMT in carcinoma progression and dissemination: facts, unanswered questions, and clinical considerations. Cancer Metastasis Rev. 31, 277-283 (2012).
2. Kalluri, R. & Weinberg, R. A. The basics of epithelial-mesenchymal transition. J. Clin. Invest. 119, 1420-1428 (2009).
3. Scheel, C. & Weinberg, R. A. Phenotypic plasticity and epithelial-mesenchymal transitions in cancer and normal stem cells? Int. J. Cancer 129, 2310-2314 (2011).
4. Mani, S. A. et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133, 704-715 (2008).
5. Gal, A. et al. Sustained TGF beta exposure suppresses Smad and non-Smad signalling in mammary epithelial cells, leading to EMT and inhibition of growth arrest and apoptosis. Oncogene 27, 1218-1230 (2008).
6. Hennessy, B. T. et al. Characterization of a naturally occurring breast cancer subset enriched in epithelial-to-mesenchymal transition and stem cell characteristics. Cancer Res. 69, 4116-4124 (2009).
7. Gao, D. et al. Myeloid progenitor cells in the premetastatic lung promote metastases by inducing mesenchymal to epithelial transition. Cancer Res. 72, 1384-1394 (2012).
8. Lin, E. Y. et al. Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases. Am. J. Pathol. 163, 2113-2126 (2003).
9. Guy, C. T., Cardiff, R. D. & Muller, W. J. Induction of mammary tumors by expression of polyomavirus middle T oncogene: A transgenic mouse model for metastatic disease. Mol. Cell. Biol. 12, 954-961 (1992).
10. Bhowmick, N. A. et al. TGF-signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 303, 848-851 (2004).
11. Muzumdar, M. D., Tasic, B., Miyamichi, K., Li, L. & Luo, L. A global doublefluorescent Cre reporter mouse. Genesis 45, 593-605 (2007).
12. Xue, C., Plieth, D., Venkov, C., Xu, C. & Neilson, E. G. The gatekeeper effect of epithelial-mesenchymal transition regulates the frequency of breast cancer metastasis. Cancer Res. 63, 3386-3394 (2003).
13. Okada, H., Danoff, T. M., Kalluri, R. & Neilson, E. G. Early role of Fsp1 in epithelial-mesenchymal transformation. Am. J. Physiol. 273, F563-F574 (1997).
14. Gunasinghe, N. P., Wells, A., Thompson, E. W. & Hugo, H. J. Mesenchymal-epithelial transition (MET) as a mechanism for metastatic colonisation in breast cancer. Cancer Metastasis Rev. 31, 469-478 (2012).
15. Cabeon, T. et al. Expression of S100A4 by a variety of cell types present in the tumor microenvironment of human breast cancer. Int. J. Cancer 121, 1433-1444 (2007).
16. Guy, C. T. et al. Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease. Proc. Natl Acad. Sci. USA 89, 10578-10582 (1992).
17. Troeger, J. S. et al. Deactivation of hepatic stellate cells during liver fibrosis resolution in mice. Gastroenterology 143, 1073-1083 (2012).
18. Dumont, N. et al. Sustained induction of epithelial to mesenchymal transition activates DNA methylation of genes silenced in basal-like breast cancers. Proc. Natl Acad. Sci. USA 105, 14867-14872 (2008).
19. Park, S. M., Gaur, A. B., Lengyel, E. & Peter, M. E. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev. 22, 894-907 (2008).
20. Gregory, P. A. et al. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nature Cell Biol. 10, 593-601 (2008).
21. Singh, A. & Settleman, J. EMT, cancer stem cells and drug resistance: An emerging axis of evil in the war on cancer. Oncogene 29, 4741-4751 (2010).
22. Zhang, Y., Toy, K. A. & Kleer, C. G. Metaplastic breast carcinomas are enriched in markers of tumor-initiating cells and epithelial to mesenchymal transition. Mod. Pathol. 25, 178-184 (2012).
23. Creighton, C. J. et al. Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc. Natl Acad. Sci. USA 106, 13820-13825 (2009).
24. von Minckwitz, G. Docetaxel/anthracycline combinations for breast cancer treatment. Expert Opin. Pharmacother. 8, 485-495 (2007).
25. Lau, C. K. et al. An Akt/hypoxia-inducible factor-1? /platelet-derived growth factor-BB autocrine loop mediates hypoxia-induced chemoresistance in liver cancer cells and tumorigenic hepatic progenitor cells. Clin. Cancer Res. 15, 3462-3471 (2009).
26. Xiao, Z. M., Wang, X. Y. & Wang, A. M. Periostin induces chemoresistance in colon cancer cells through activation of the PI3K/Akt/survivin pathway. Biotechnol. Appl. Biochem. 62, 401-406 (2015).
27. Yamada, D. et al. Role of crosstalk between interleukin-6 and transforming growth factor-beta 1 in epithelial-mesenchymal transition and chemoresistance in biliary tract cancer. Eur. J. Cancer 49, 1725-1740 (2013).
28. Yao, Z. et al. TGF-IL-6 axis mediates selective and adaptive mechanisms of resistance to molecular targeted therapy in lung cancer. Proc. Natl Acad. Sci. USA 107, 15535-15540 (2010).
29. Russo, J. E. & Hilton, J. Characterization of cytosolic aldehyde dehydrogenase from cyclophosphamide resistant L1210 cells. Cancer Res. 48, 2963-2968 (1988).
30. Tam, W. L. & Weinberg, R. A. The epigenetics of epithelial-mesenchymal plasticity in cancer. Nature Med. 19, 1438-1449 (2013).
31. Trimboli, A. J. et al. Direct evidence for epithelial-mesenchymal transitions in breast cancer. Cancer Res. 68, 937-945 (2008).
32. Yu, M. et al. Circulating breast tumor cells exhibit dynamic changes in epithelial and mesenchymal composition. Science 339, 580-584 (2013).
33. Korpal, M. et al. Direct targeting of Sec23a by miR-200s influences cancer cell secretome and promotes metastatic colonization. Nature Med. 17, 1101-1108 (2011).
34. Gupta, P. B. et al. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138, 645-659 (2009).
35. Diessner, J. et al. Targeting of preexisting and induced breast cancer stem cells with trastuzumab and trastuzumab emtansine (T-DM1). Cell Death Dis. 5, e1149 (2014).