Transient SNAIL1 expression is necessary for metastatic competence in breast cancer

Cancer Research

Volumn 74, Issue 21, 2014, Pages 6330-6340

  Tran, Hung D ^a   Luitel, Krishna ^a   Kim, Michael ^a   Zhang, Kun ^a   Longmore, Gregory D ^a   Tran, David D ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR SNAIL1; UNCLASSIFIED DRUG; SNAIL FAMILY TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; GENE DELETION; GENETIC MODEL; LUNG METASTASIS; METASTASIS; MOUSE; MOUSE MODEL; NONHUMAN; PRECANCER; PRIMARY TUMOR; TRANSIENT EXPRESSION; BIOSYNTHESIS; BREAST TUMOR; CELL PROLIFERATION; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

BREAST NEOPLASMS; CELL PROLIFERATION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASM METASTASIS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TUMOR MICROENVIRONMENT;

EID: 84909606776     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-0923     Document Type: Article

References (41)

1. Thiery JP, Acloque H, Huang RYJ, Nieto MA. Epithelial-mesenchymal transitions in development and disease. Cell 2009;139:871-90.
2. Kudo-Saito C, Shirako H, Takeuchi T, Kawakami Y. Cancer metastasis is accelerated through immunosuppression during Snail-induced EMT of cancer cells. Cancer Cell 2009;15:195-206.
3. Moody SE, Perez D, Pan TC, Sarkisian CJ, Portocarrero CP, Sterner CJ, et al. The transcriptional repressor Snail promotesmammary tumor recurrence. Cancer Cell 2005;8:197-209.
4. Tran DD, Corsa CAS, Biswas H, Aft RL, Longmore GD. Temporal and spatial cooperation of Snail1 and Twist1 during epithelialmesenchymal transition predicts for human breast cancer recurrence. Mol Cancer Res 2011;9:1644-57.
5. Tarin D, Thompson EW, Newgreen DF. The fallacy of epithelial mesenchymal transition in neoplasia. Cancer Res 2005;65:5996-6000.
6. Garber K. Epithelial-to-mesenchymal transition is important to metastasis, but questions remain. J Natl Cancer Ins 2008;100: 232-39.
7. Giampieri S, Manning C, Hooper S, Jones L, Hill CS, Sahai E. Localized and reversible TGFbeta signalling switches breast cancer cells from cohesive to single cell motility. Nat Cell Biol 2009;11:1287-96.
8. Christiansen JJ, Rajasekaran AK. Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis. Cancer Res 2006;66:8319-26.
9. Tsai JH, Donaher JL, Murphy DA, Chau S, Yang J. Spatiotemporal regulation of epithelial-mesenchymal transition is essential for squamous cell carcinoma metastasis. Cancer Cell 2012;22:725-36.
10. Ocana OH, Corcoles R, Fabra A,Moreno-Bueno G, Acloque H, Vega S, et al. Metastatic colonization requires the repression of the epithelial-mesenchymal transition inducer Prrx1. Cancer Cell 2012; 22:709-24.
11. Ansieau S, Bastid J, Doreau A, Morel AP, Bouchet BP, Thomas C, et al. Induction of EMT by twist proteins as a collateral effect of tumorpromoting inactivation of premature senescence. Cancer Cell 2008; 14:79-89.
12. Mani SA, Guo W, Liao M-J, Eaton EN, Ayyanan A, Zhou AY, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008;133:704-15.
13. Rowe RG, Li X-Y, Hu Y, Saunders TL, Virtanen I, de Herreros AG, et al. Mesenchymal cells reactivate Snail1 expression to drive three-dimensional invasion programs. J Cell Biol 2009;184:399-408.
14. Poueymirou WT, Auerbach W, Frendewey D, Hickey JF, Escaravage JM, Esau L, et al. F0 generation mice fully derived from gene-targeted embryonic stem cells allowing immediate phenotypic analyses. Nat Biotechnol 2007;25:91-9.
15. Bagheri-Yarmand R, Talukder AH, Wang RA, Vadlamudi RK, Kumar R. Metastasis-associated protein 1 deregulation causes inappropriate mammary gland development and tumorigenesis. Development 2004; 131:3469-79.
16. Fujii T, Fuchs BC, Yamada S, Lauwers GY, Kulu Y, Goodwin JM, et al. Mouse model of carbon tetrachloride induced liver fibrosis: Histopathological changes and expression of CD133 and epidermal growth factor. BMC Gastroenterol 2010;10:79.
17. Miretti S, Roato I, Taulli R, Ponzetto C, Cilli M, Olivero M, et al. A mouse model of pulmonary metastasis from spontaneous osteosarcoma monitored in vivo by Luciferase imaging. PLoS ONE 2008;3:e1828.
18. Zhang K, Corsa CA, Ponik SM, Prior JL, Piwnica-Worms D, EliceiriKW, et al. The collagen receptor discoidin domain receptor 2 stabilizes SNAIL1 to facilitate breast cancer metastasis. Nat Cell Biol 2013;15: 677-87.
19. Zhang K, Rodriguez-Aznar E, Yabuta N, Owen RJ, Mingot JM, Nojima H, et al. Lats2 kinase potentiates Snail1 activity by promoting nuclear retention upon phosphorylation. EMBO J 2012;31:29-43.
20. Gill JG, Langer EM, Lindsley RC, Cai M, Murphy TL, Kyba M, et al. Snail and the microRNA-200 family act in opposition to regulate epithelialto-mesenchymal transition and germ layer fate restriction in differentiating ESCs. Stem Cells 2011;29:764-76.
21. Kokudo T, Suzuki Y, Yoshimatsu Y, Yamazaki T, Watabe T, Miyazono K. Snail is required for TGFbeta-induced endothelial-mesenchymal transition of embryonic stem cell-derived endothelial cells. J Cell Sci 2008;121:3317-24.
22. Fedorova L, Gatto-Weis C, Smaili S, Khurshid N, Shapiro J, Malhotra D, et al. Down-regulation of the transcription factor snail in the placentas of patients with preeclampsia and in a rat model of preeclampsia. Reprod Biol Endocrinol 2012;10:1-11.
23. Nakayama H, Scott IC, Cross JC. The transition to endoreduplication in trophoblast giant cells is regulated by the mSNA zinc finger transcription factor. Dev Biol 1998;199:150-63.
24. Senner CE, Hemberger M. Regulation of early trophoblast differentiation lessons from the mouse. Placenta 2010;31:944-50.
25. Nieto MA, Bennett MF, Sargent MG, Wilkinson DG. Cloning and developmental expression of Sna, a murine homologue of the Drosophila snail gene. Development 1992;116:227-37.
26. Rowe RG, Lin Y, Shimizu-Hirota R, Hanada S, Neilson EG, Greenson JK, et al. Hepatocyte-derived Snail1 propagates liver fibrosis progression. Mol Cell Biol 2011;31:2392-403.
27. Come C, Arnoux V, Bibeau F, Savagner P. Roles of the transcription factors snail and slug during mammary morphogenesis and breast carcinoma progression. J Mammary Gland Biol Neoplasia 2004;9: 183-93.
28. Chakrabarti R, Hwang J, Andres Blanco M, Wei Y, Lukacisin M, Romano R-A, et al. Elf5 inhibits the epithelial mesenchymal transition in mammary gland development and breast cancer metastasis by transcriptionally repressing Snail2. Nat Cell Biol 2012;14: 1212-22.
29. Wagner KU, McAllister K, Ward T, Davis B, Wiseman R, Hennighausen L. Spatial and temporal expression of the Cre gene under the control of the MMTV-LTR in different lines of transgenic mice. Transgenic Res 2001;10:545-53.
30. Fantozzi A, Christofori G. Mouse models of breast cancer metastasis. Breast Cancer Res 2006;8:212.
31. Muller WJ, Sinn E, Pattengale PK, Wallace R, Leder P. Single-step induction of mammary adenocarcinoma in transgenic mice bearing the activated c-neu oncogene. Cell 1988;54:105-15.
32. Vincent-Salomon A, Thiery JP. Host microenvironment in breast cancer development: epithelial-mesenchymal transition in breast cancer development. Breast Cancer Res 2003;5:101-6.
33. Husemann Y, Geigl JB, Schubert F, Musiani P, Meyer M, Burghart E, et al. Systemic spread is an early step in breast cancer. Cancer cell 2008;13:58-68.
34. Moody SE, Sarkisian CJ, Hahn KT, Gunther EJ, Pickup S, Dugan KD, et al. Conditional activation of Neu in the mammary epithelium of transgenic mice results in reversible pulmonary metastasis. Cancer Cell 2002;2:451-61.
35. Guy CT, Cardiff RD, Muller WJ. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol Cell Biol 1992;12:954-61.
36. Franken B, de Groot M, Mastboom W, Vermes I, van der Palen J, Tibbe A, et al. Circulating tumor cells, disease recurrence and survival in newly diagnosed breast cancer. Breast Cancer Res 2012;14:R133.
37. Roses RE, Arun BK, Lari SA, Mittendorf EA, Lucci A, Hunt KK, et al. Ductal carcinoma-in-situ of the breast with subsequent distant metastasis and death. Ann Surg Oncol 2011;18:2873-8.
38. Weng D, Penzner J, Song B, Koido S, Calderwood S, Gong J. Metastasis is an early event in mouse mammary carcinomas and is associated with cells bearing stem cell markers. Breast Cancer Res 2012;14:R18.
39. Madisen L, Zwingman TA, Sunkin SM, OhSW, Zariwala HA, Gu H, et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 2010;13:133-40.
40. Peinado H, Olmeda D, Cano A. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat Reviews Cancer 2007;7:415-28.
41. Celia-Terrassa T, Meca-Cortes O, Mateo F, de Paz AM, Rubio N, Arnal-Estape A, et al. Epithelial-mesenchymal transition can suppress major attributes of human epithelial tumor-initiating cells. J Clin Invest 2012;122:1849-68.