Overexpression of Snail induces epithelial-mesenchymal transition and a cancer stem cell-like phenotype in human colorectal cancer cells

Cancer Medicine

Volumn 1, Issue 1, 2012, Pages 5-16

  Fan, Fan ^a   Samuel, Shaija ^a   Evans, Kurt W ^a   Lu, Jia ^a   Xia, Ling ^a   Zhou, Yunfei ^a   Sceusi, Eric ^a   Tozzi, Federico ^a   Ye, Xiang Cang ^a   Mani, Sendurai A ^a,b   Ellis, Lee M ^a,b  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

Cancer stem cells; Colorectal cancer; EMT; Migration; Snail

Indexed keywords

CELL MARKER; OXALIPLATIN; TRANSCRIPTION FACTOR SNAIL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CANCER RESISTANCE; CANCER STEM CELL; CELL FUNCTION; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CHEMOSENSITIVITY; COLORECTAL CANCER; CONTROLLED STUDY; DRUG TARGETING; EPITHELIAL MESENCHYMAL TRANSITION; GENETIC TRANSDUCTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; METASTASIS POTENTIAL; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RETROVIRUS INFECTION;

EID: 84878583653     PISSN: None     EISSN: 20457634     Source Type: Journal    
DOI: 10.1002/cam4.4     Document Type: Article

References (41)

1. Thiery, J. P., and J. P. Sleeman. 2006. Complex networks orchestrate epithelial-mesenchymal transitions. Nat. Rev. Mol. Cell Biol. 7:131-142.
2. Nieto, M. A. 2002. The snail superfamily of zinc-finger transcription factors. Nat. Rev. Mol. Cell Biol. 3:155-166.
3. Yang, J., S. A. Mani, J. L. Donaher, S. Ramaswamy, R. A. Itzykson, C. Come, et al. 2004. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117:927-939.
4. Hartwell, K. A., B. Muir, F. Reinhardt, A. E. Carpenter, D. C. Sgroi, and R. A. Weinberg. 2006. The Spemann organizer gene, Goosecoid, promotes tumor metastasis. Proc. Natl Acad. Sci. USA 103:18969-18974.
5. Peinado, H., D. Olmeda, and A. Cano. 2007. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype? Nat. Rev. Cancer 7:415-428.
6. Moody, S. E., D. Perez, T. C. Pan, C. J. Sarkisian, C. P. Portocarrero, C. J. Sterner, et al. 2005. The transcriptional repressor Snail promotes mammary tumor recurrence. Cancer Cell 8:197-209.
7. Miyoshi, A., Y. Kitajima, S. Kido, T. Shimonishi, S. Matsuyama, K. Kitahara, et al. 2005. Snail accelerates cancer invasion by upregulating MMP expression and is associated with poor prognosis of hepatocellular carcinoma. Br. J. Cancer 92:252-258.
8. Come, C., F. Magnino, F. Bibeau, P. De Santa Barbara, K. F. Becker, C. Theillet, et al. 2006. Snail and slug play distinct roles during breast carcinoma progression. Clin. Cancer Res. 12:5395-5402.
9. Roy, H. K., T. C. Smyrk, J. Koetsier, T. A. Victor, and R. K. Wali. 2005. The transcriptional repressor SNAIL is overexpressed in human colon cancer. Dig. Dis. Sci. 50:42-46.
10. Elloul, S., M. B. Elstrand, J. M. Nesland, C. G. Trope, G. Kvalheim, I. Goldberg, et al. 2005. Snail, Slug, and Smad-interacting protein 1 as novel parameters of disease aggressiveness in metastatic ovarian and breast carcinoma. Cancer 103:1631-1643.
11. Mani, S. A., W. Guo, M. J. Liao, E. N. Eaton, A. Ayyanan, A. Y. Zhou, et al. 2008. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133:704-715.
12. Chen, Y. C., Y. W. Chen, H. S. Hsu, L. M. Tseng, P. I. Huang, K. H. Lu, et al. 2009. Aldehyde dehydrogenase 1 is a putative marker for cancer stem cells in head and neck squamous cancer. Biochem. Biophys. Res. Commun. 385:307-313.
13. Kurrey, N. K., S. P. Jalgaonkar, A. V. Joglekar, A. D. Ghanate, P. D. Chaskar, R. Y. Doiphode, et al. 2009. Snail and slug mediate radioresistance and chemoresistance by antagonizing p53-mediated apoptosis and acquiring a stem-like phenotype in ovarian cancer cells. Stem Cells 27:2059-2068.
14. Efstathiou, J. A., D. Liu, J. M. Wheeler, H. C. Kim, N. E. Beck, M. Ilyas, et al. 1999. Mutated epithelial cadherin is associated with increased tumorigenicity and loss of adhesion and of responsiveness to the motogenic trefoil factor 2 in colon carcinoma cells. Proc. Natl Acad. Sci. USA 96:2316-2321.
15. Wheeler, J. M., H. C. Kim, J. A. Efstathiou, M. Ilyas, N. J. Mortensen, and W. F. Bodmer. 2001. Hypermethylation of the promoter region of the E-cadherin gene (CDH1) in sporadic and ulcerative colitis associated colorectal cancer. Gut 48:367-371.
16. Fan, F., S. Samuel, P. Gaur, J. Lu, N. A. Dallas, L. Xia, et al. 2011. Chronic exposure of colorectal cancer cells to bevacizumab promotes compensatory pathways that mediate tumour cell migration. Br. J. Cancer 104:1270-1277.
17. Reynolds, B. A., W. Tetzlaff, and S. Weiss. 1992. A multipotent EGF-responsive striatal embryonic progenitor cell produces neurons and astrocytes. J. Neurosci. 12:4565-4574.
18. Dallas, N. A., M. J. Gray, L. Xia, F. Fan, G. van Buren II, P. Gaur, et al. 2008. Neuropilin-2-mediated tumor growth and angiogenesis in pancreatic adenocarcinoma. Clin. Cancer Res. 14:8052-8060.
19. Pena, C., J. M. Garcia, M. J. Larriba, R. Barderas, I. Gomez, M. Herrera, et al. 2009. SNAI1 expression in colon cancer related with CDH1 and VDR downregulation in normal adjacent tissue. Oncogene 28:4375-4385.
20. Morel, A. P., M. Lievre, C. Thomas, G. Hinkal, S. Ansieau, and A. Puisieux. 2008. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS ONE 3:e2888.
21. McCoy, E. L., R. Iwanaga, P. Jedlicka, N. S. Abbey, L. A. Chodosh, K. A. Heichman, et al. 2009. Six1 expands the mouse mammary epithelial stem/progenitor cell pool and induces mammary tumors that undergo epithelial-mesenchymal transition. J. Clin. Invest. 119:2663-2677.
22. Gupta, P. B., T. T. Onder, G. Jiang, K. Tao, C. Kuperwasser, R. A. Weinberg, et al. 2009. Identification of selective inhibitors of cancer stem cells by high-throughput screening. Cell 138:645-659.
23. Batlle, E., E. Sancho, C. Franci, D. Dominguez, M. Monfar, J. Baulida, et al. 2000. The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat. Cell Biol. 2:84-89.
24. Zhou, B. P., J. Deng, W. Xia, J. Xu, Y. M. Li, M. Gunduz, et al. 2004. Dual regulation of Snail by GSK-3beta-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat. Cell Biol. 6:931-940.
25. Thiery, J. P., H. Acloque, R. Y. Huang, and M. A. Nieto. 2009. Epithelial-mesenchymal transitions in development and disease. Cell 139:871-890.
26. Rosivatz, E., I. Becker, K. Specht, E. Fricke, B. Luber, R. Busch, et al. 2002. Differential expression of the epithelial-mesenchymal transition regulators snail, SIP1, and twist in gastric cancer. Am. J. Pathol. 161:1881-1891.
27. Chen, W. C., and B. Obrink. 1991. Cell-cell contacts mediated by E-cadherin (uvomorulin) restrict invasive behavior of L-cells. J. Cell Biol. 114:319-327.
28. Kalluri, R., and R. A. Weinberg. 2009. The basics of epithelial-mesenchymal transition. J. Clin. Invest. 119:1420-1428.
29. Hwang, W. L., M. H. Yang, M. L. Tsai, H. Y. Lan, S. H. Su, S. C. Chang, et al. 2011. SNAIL regulates interleukin-8 expression, stem cell-like activity, and tumorigenicity of human colorectal carcinoma cells. Gastroenterology 141:279-291.
30. Yang, A. D., F. Fan, E. R. Camp, G. van Buren, W. Liu, R. Somcio, et al. 2006. Chronic oxaliplatin resistance induces epithelial-to-mesenchymal transition in colorectal cancer cell lines. Clin. Cancer Res. 12:4147-4153.
31. Cheng, G. Z., J. Chan, Q. Wang, W. Zhang, C. D. Sun, and L. H. Wang. 2007. Twist transcriptionally up-regulates AKT2 in breast cancer cells leading to increased migration, invasion, and resistance to paclitaxel. Cancer Res. 67:1979-1987.
32. Kajiyama, H., K. Shibata, M. Terauchi, M. Yamashita, K. Ino, A. Nawa, et al. 2007. Chemoresistance to paclitaxel induces epithelial-mesenchymal transition and enhances metastatic potential for epithelial ovarian carcinoma cells. Int. J. Oncol. 31:277-283.
33. de Grouw, E. P., M. H. Raaijmakers, J. B. Boezeman, B. A. van der Reijden, L. T. van de Locht, T. J. de Witte, et al. 2006. Preferential expression of a high number of ATP binding cassette transporters in both normal and leukemic CD34+ CD38- cells. Leukemia 20:750-754.
34. Lugli, A., G. Iezzi, I. Hostettler, M. G. Muraro, V. Mele, L. Tornillo, et al. 2010. Prognostic impact of the expression of putative cancer stem cell markers CD133, CD166, CD44s, EpCAM, and ALDH1 in colorectal cancer. Br. J. Cancer 103:382-390.
35. Neumeister, V., J. Agarwal, R. L. Bordeaux, and D. L. Rimm. 2010. In situ identification of putative cancer stem cells by multiplexing ALDH1, CD44, and cytokeratin identifies breast cancer patients with poor prognosis. Am. J. Pathol. 176:2131-2138.
36. Bao, S., Q. Wu, R. E. McLendon, Y. Hao, Q. Shi, A. B. Hjelmeland, et al. 2006. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:756-760.
37. Ma, S., T. K. Lee, B. J. Zheng, K. W. Chan, and X. Y. Guan. 2008. CD133+ HCC cancer stem cells confer chemoresistance by preferential expression of the Akt/PKB survival pathway. Oncogene 27:1749-1758.
38. Dean, M., T. Fojo, and S. Bates. 2005. Tumour stem cells and drug resistance. Nat. Rev. Cancer 5:275-284.
39. Diehn, M., and M. F. Clarke. 2006. Cancer stem cells and radiotherapy: new insights into tumor radioresistance. J. Natl Cancer Inst. 98:1755-1757.
40. Todaro, M., M. P. Alea, A. B. Di Stefano, P. Cammareri, L. Vermeulen, F. Iovino, et al. 2007. Colon cancer stem cells dictate tumor growth and resist cell death by production of interleukin-4. Cell Stem Cell 1:389-402.
41. Cammareri, P., A. Scopelliti, M. Todaro, V. Eterno, F. Francescangeli, M. P. Moyer, et al. 2010. Aurora-A is essential for the tumorigenic capacity and chemoresistance of colorectal cancer stem cells. Cancer Res. 70:4655-4665.