ZEB1 enhances transendothelial migration and represses the epithelial phenotype of prostate cancer cells

Molecular Biology of the Cell

Volumn 20, Issue 8, 2009, Pages 2207-2217

  Drake, Justin M ^a   Strohbehn, Garth ^a   Bair, Thomas B ^a   Moreland, Jessica G ^a   Henry, Michael D ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; MOLECULAR MARKER; UNCLASSIFIED DRUG; UVOMORULIN; ZEB1 PROTEIN;

ARTICLE; CANCER CELL; CELL ADHESION; CELL MIGRATION; CELL SUBPOPULATION; CONTROLLED STUDY; DOWN REGULATION; ENDOTHELIUM CELL; EPITHELIUM CELL; FLUORESCENCE ACTIVATED CELL SORTING; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; MESENCHYME CELL; METASTASIS; MICROARRAY ANALYSIS; MICROVASCULATURE; PHENOTYPE; PRIORITY JOURNAL; PROSTATE CANCER; PROSTATE EPITHELIUM; PROTEIN EXPRESSION; UPREGULATION;

ANIMALS; CADHERINS; CELL LINE, TUMOR; CELL MOVEMENT; ENDOTHELIAL CELLS; EPITHELIAL CELLS; EPITHELIUM; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEODOMAIN PROTEINS; HUMANS; MALE; MESODERM; MICE; NEOPLASM METASTASIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; PROSTATIC NEOPLASMS; TRANSCRIPTION FACTORS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

MURINAE;

EID: 65249101685     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E08-10-1076     Document Type: Article

References (45)

1. Aigner, K., et al. (2007). The transcription factor ZEB1 (deltaEFl) promotes tumour cell dedifferentiation by repressing master regulators of epithelial polarity. Oncogene 26, 6979-6988.
2. Albini, A., Iwamoto, Y., Kleinman, H. K., Martin, G. R., Aaronson, S. A., Kozlowski, J. M., and McEwan, R. N. (1987). A rapid in vitro assay for quantitating the invasive potential of tumor cells. Cancer Res. 47, 3239-3245.
3. Batlle, E., Sancho, E., Franci, C., Dominguez, D., Monfar, M., Baulida, J., and Garcia De Herreros, A. (2000). The transcription factor snail is a repressor of E-cadherin gene expression in epithelial tumour cells. Nat. Cell Biol. 2, 84-89.
4. Bauer, K., Mierke, C., and Behrens, J. (2007). Expression profiling reveals genes associated with transendothelial migration of tumor cells: a functional role for alphavbeta3 integrin. Int. J. Cancer 121, 1910-1918.
5. Berx, G., Raspe, E., Christofori, G., Thiery, J. P., and Sleeman, J. P. (2007). Pre-EMTing metastasis? Recapitulation of morphogenetic processes in cancer. Clin. Exp. Metastasis 24, 587-597.
6. Bracken, C. P., Gregory, P. A., Kolesnikoff, N., Bert, A. G., Wang, J., Shannon, M. F., and Goodall, G. J. (2008). A double-negative feedback loop between ZEB1-SIP1 and the microRNA-200 family regulates epithelial-mesenchymal transition. Cancer Res. 68, 7846-7854.
7. Burk, U., Schubert, J., Wellner, U., Schmalhofer, O., Vincan, E., Spaderna, S., and Brabletz, T. (2008). A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep. 9, 582-589.
8. Cano, A., Perez-Moreno, M. A., Rodrigo, I., Locascio, A., Blanco, M. J., del Barrio, M. G., Portillo, F., and Nieto, M. A. (2000). The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2, 76-83.
9. Costantino, M. E., Stearman, R. P., Smith, G. E., and Darling, D. S. (2002). Cell-specific phosphorylation of Zfhep transcription factor. Biochem. Biophys. Res. Commun. 296, 368-373.
10. Crissman, J. D., Hatfield, J., Schaldenbrand, M., Sloane, B. F., and Honn, K. V. (1985). Arrest and extravasation of B16 amelanotic melanoma in murine lungs. A light and electron microscopic study. Lab. Invest. 53, 470-478.
11. Darling, D. S., Stearman, R. P., Qi, Y., Qiu, M. S., and Feller, J. P. (2003). Expression of Zfhep/deltaEF1 protein in palate, neural progenitors, and differentiated neurons. Gene Expr. Patterns 3, 709-717.
12. Drake, J. M., Gabriel, C. L., and Henry, M. D. (2005). Assessing tumor growth and distribution in a model of prostate cancer metastasis using biolumines-cence imaging. Clin. Exp. Metastasis 22, 674-684.
13. Friedl, P., and Wolf, K. (2003). Tumour-cell invasion and migration: diversity and escape mechanisms. Nat. Rev. Cancer 3, 362-374.
14. Giavazzi, R., Foppolo, M., Dossi, R., and Remuzzi, A. (1993). Rolling and adhesion of human tumor cells on vascular endothelium under physiological flow conditions. J. Clin. Invest. 92, 3038-3044.
15. Graham, T. R., Zhau, H. E., Odero-Marah, V. A., Osunkoya, A. O., Kimbro, K. S., Tighiouart, M., Liu, T., Simons, J. W., and O'Regan, R. M. (2008). Insulin-like growth factor-I-dependent up-regulation of ZEB1 drives epithe-lial-to-mesenchymal transition in human prostate cancer cells. Cancer Res. 68, 2479-2488.
16. Gregory, P. A., Bert, A. G., Paterson, E. L., Barry, S. C., Tsykin, A., Farshid, G., Vadas, M. A., Khew-Goodall, Y., and Goodall,G. J. (2008). The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol. 10, 593-601.
17. Hurteau, G. J., Carlson, J. A., Spivack, S. D., and Brock, G. J. (2007). Overex-pression of the microRNA hsa-miR-200c leads to reduced expression of transcription factor 8 and increased expression of E-cadherin. Cancer Res. 67, 7972-7976.
18. Jemal, A., Siegel, R., Ward, E., Hao, Y., Xu, J., Murray, T., and Thun, M. J. (2008). Cancer statistics, 2008. CA Cancer J Clin. 58, 71-96.
19. Korpal, M., Lee, E. S., Hu, G., and Kang, Y. (2008). The miR-200 familyinhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J. Biol. Chem. 283, 14910-14914.
20. Kramer, R. H., and Nicolson, G. L. (1979). Interactions of tumor cells with vascular endothelial cell monolayers: a model for metastatic invasion. Proc. Natl. Acad. Sci. USA 76, 5704-5708.
21. Lapis, K., Paku, S., and Liotta, L. A. (1988). Endothelialization of embolized tumor cells during metastasis formation. Clin. Exp. Metastasis 6, 73-89.
22. Lee, T. H., Avraham, H. K., Jiang, S., and Avraham, S. (2003). Vascular endothelial growth factor modulates the transendothelial migration of MDA-MB-231 breast cancer cells through regulation of brain microvascular endo-thelial cell permeability. J. Biol. Chem. 278, 5277-5284.
23. Luzzi, K. J., MacDonald, I. C., Schmidt, E. E., Kerkvliet, N., Morris, V. L., Chambers, A. F., and Groom, A. C. (1998). Multistep nature of metastatic inefficiency: dormancy of solitary cells after successful extravasation and limited survival of early micrometastases. Am. J. Pathol. 153, 865-873.
24. Miles, F. L., Pruitt, F. L., van Golen, K. L., and Cooper, C. R. (2008). Stepping out of the flow: capillary extravasation in cancer metastasis. Clin. Exp. Metastasis 25, 305-324.
25. Moreland, J. G., and Bailey, G. (2006). Neutrophil transendothelial migration in vitro to Streptococcus pneumoniae is pneumolysin dependent. Am. J. Physiol. Lung Cell Mol. Physiol. 290, L833-L840.
26. Muller, A., et al. (2001). Involvement of chemokine receptors in breast cancer metastasis. Nature 410, 50-56.
27. Okada, T., Okuno, H., and Mitsui, Y. (1994). A novel in vitro assay system for transendothelial tumor cell invasion: significance of E-selectin and alpha 3 integrin in the transendothelial invasion by HT1080 fibrosarcoma cells. Clin. Exp. Metastasis 12, 305-314.
28. Onder, T. T., Gupta, P. B., Mani, S. A., Yang, J., Lander, E. S., and Weinberg, R. A. (2008). Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res. 68, 3645-3654.
29. Padua, D., Zhang, X. H., Wang, Q., Nadal, C., Gerald, W. L., Gomis, R. R., and Massague, J. (2008). TGFbeta primes breast tumors for lung metastasis seeding through angiopoietin-like 4. Cell 133, 66-77.
30. Park, S. M., Gaur, A. B., Lengyel, E., and Peter, M. E. (2008). 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.
31. Pettaway, C. A., Pathak, S., Greene, G., Ramirez, E., Wilson, M. R., Killion, J. J., and Fidler, I. J. (1996). Selection of highly metastatic variants of different human prostatic carcinomas using orthotopic implantation in nude mice. Clin. Cancer Res. 2, 1627-1636.
32. Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45
33. Qi, J., Chen, N., Wang, J., and Siu, C. H. (2005). Transendothelial migration of melanoma cells involves N-cadherin-mediated adhesion and activation of the beta-catenin signaling pathway. Mol. Biol. Cell 16, 4386-4397.
34. Qi, J., Wang, J., Romanyuk, O., and Siu, C. H. (2006). Involvement of Src family kinases in N-cadherin phosphorylation and beta-catenin dissociation during transendothelial migration of melanoma cells. Mol. Biol. Cell 17, 1261-1272.
35. Rokhlin, O. W., and Cohen, M. B. (1995). Expression of cellular adhesion molecules on human prostate tumor cell lines. Prostate 26, 205-212.
36. Romanov, V. I., and Goligorsky, M. S. (1999). RGD-recognizing integrins mediate interactions of human prostate carcinoma cells with endothelial cells in vitro. Prostate 39, 108-118.
37. Spaderna, S., et al. (2008). The transcriptional repressor ZEB1 promotes metastasis and loss of cell polarity in cancer. Cancer Res. 68, 537-544.
38. Svensson, R. U., Barnes, J. M., Rokhlin, O. W., Cohen, M. B., and Henry, M. D. (2007). Chemotherapeutic agents up-regulate the cytomegalovirus promoter: implications for bioluminescence imaging of tumor response to therapy. Cancer Res. 67, 10445-10454.
39. Tomita, K., van Bokhoven, A., van Leenders, G. J., Ruijter, E. T., Jansen, C. F., Bussemakers, M. J., and Schalken, J. A. (2000). Cadherin switching in human prostate cancer progression. Cancer Res. 60, 3650-3654.
40. Voura, E. B., Ramjeesingh, R. A., Montgomery, A. M., and Siu, C. H. (2001). Involvement of integrin alpha(v)beta(3) and cell adhesion molecule L1 in transendothelial migration of melanoma cells. Mol. Biol. Cell 12, 2699-2710.
41. Wang, X., Ferreira, A. M., Shao, Q., Laird, D. W., and Sandig, M. (2005). Beta3 integrins facilitate matrix interactions during transendothelial migration of PC3 prostate tumor cells. Prostate 63, 65-80.
42. Warren, B. A., and Vales, O. (1972). The adhesion of thromboplastic tumour emboli to vessel walls in vivo. Br. J. Exp. Pathol. 53, 301-313.
43. Wood, S., Jr. (1958). Pathogenesis of metastasis formation observed in vivo in the rabbit ear chamber. AMA Arch. Pathol. 66, 550-568.
44. Yang, J., Mani, S. A., Donaher, J. L., Ramaswamy, S., Itzykson, R. A., Come, C., Savagner, P., Gitelman, I., Richardson, A., and Weinberg, R. A. (2004). Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117, 927-939.
45. Zeeberg, B. R., et al. (2003). GoMiner: a resource for biological interpretation of genomic and proteomic data. Genome Biol. 4, R28.