Slug is required for cell survival during partial epithelial-mesenchymal transition of HGF-induced tubulogenesis

Molecular Biology of the Cell

Volumn 18, Issue 5, 2007, Pages 1943-1952

  Leroy, Pascale ^a   Mostov, Keith E ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SCATTER FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SNAIL; UVOMORULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CELL KINETICS; CELL MATURATION; CELL STRUCTURE; CELL SURVIVAL; CONTROLLED STUDY; EPITHELIUM CELL; KIDNEY TUBULE CELL; MESENCHYME CELL; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; THREE DIMENSIONAL IMAGING;

ANIMALS; BASE SEQUENCE; CADHERINS; CELL LINE; CELL NUCLEUS; CELL SURVIVAL; DNA PRIMERS; DOGS; EPITHELIUM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEPATOCYTE GROWTH FACTOR; KIDNEY TUBULES; MESODERM; RNA, MESSENGER; TRANSCRIPTION FACTORS; TRANSFECTION; UP-REGULATION;

GASTROPODA;

EID: 34248209601     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E06-09-0823     Document Type: Article

References (46)

1. Barrallo-Gimeno, A., and Nieto, M. A. (2005). The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development 132, 3151-3161.
2. 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.
3. Birchmeier, C., Birchmeier, W., and Brand-Saberi, B. (1996). Epithelial-mesenchymal transitions in cancer progression. Acta Anat. (Basel) 156, 217-226.
4. Birchmeier, C., Birchmeier, W., Gherardi, E., and Vande Woude, G. F. (2003). Met, metastasis, motility and more. Nat. Rev. Mol. Cell Biol. 4, 915-925.
5. Bissell, M. J., Radisky, D. C., Rizki, A., Weaver, V. M., and Petersen, O. W. (2002). The organizing principle: microenvironmental influences in the normal and malignant breast. Differentiation 70, 537-546.
6. Blanco, M. J., Moreno-Bueno, G., Sarrio, D., Locascio, A., Cano, A., Palacios, J., and Nieto, M. A. (2002). Correlation of Snail expression with histological grade and lymph node status in breast carcinomas. Oncogene 21, 3241-3246.
7. Bolos, V., Peinado, H., Perez-Moreno, M. A., Fraga, M. F., Esteller, M., and Cano, A. (2003). The transcription factor Slug represses E-cadherin expression and induces epithelial to mesenchymal transitions: a comparison with Snail and E47 repressors. J. Cell Sci. 116, 499-511.
8. Boudreau, N., and Bissell, M. J. (1998). Extracellular matrix signaling: integration of form and function in normal and malignant cells. Curr. Opin. Cell Biol. 10, 640-646.
9. Boudreau, N. J., and Varner, J. A. (2004). The homeobox transcription factor Hox D3 promotes integrin alpha5beta1 expression and function during angiogenesis. J. Biol. Chem. 279, 4862-4868.
10. 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.
11. Cheung, M., Chaboissier, M. C., Mynett, A., Hirst, E., Schedl, A., and J. Briscoe. (2005). The transcriptional control of trunk neural crest induction, survival, and delamination. Dev. Cell 8, 179-192.
12. Conacci-Sorrell, M., Simcha, I., Ben-Yedidia, T., Blechman, J., Savagner, P., and Ben-Ze'ev, A. (2003). Autoregulation of E-cadherin expression by cadherin-cadherin interactions: the roles of beta-catenin signaling, Slug, and MAPK. J. Cell Biol. 163, 847-857.
13. Debnath, J., and Brugge, J. S. (2005). Modelling glandular epithelial cancers in three-dimensional cultures. Nat. Rev. Cancer 5, 675-688.
14. Grunert, S., Jechlinger, M., and Beug, H. (2003). Diverse cellular and molecular mechanisms contribute to epithelial plasticity and metastasis. Nat. Rev. Mol. Cell Biol. 4, 657-665.
15. Hay, E. D. (1995). An overview of epithelio-mesenchymal transformation. Acta Anat. (Basel) 154, 8-20.
16. Huber, M. A., Kraut, N., and Beug, H. (2005). Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr. Opin. Cell Biol. 17, 548-558.
17. Ikenouchi, J., Furuse, M., Furuse, K., Sasaki, H., Tsukita, S., and Tsukita, S. (2005). Tricellulin constitutes a novel barrier at tricellular contacts of epithelial cells. J. Cell Biol. 171, 939-945.
18. Ikenouchi, J., Matsuda, M., Furuse, M., and Tsukita, S. (2003). Regulation of tight junctions during the epithelium-mesenchyme transition: direct repression of the gene expression of claudins/occludin by Snail. J. Cell Sci. 116, 1959-1967.
19. Inoue, A. et al. (2002). Slug, a highly conserved zinc finger transcriptional repressor, protects hematopoietic progenitor cells from radiation-induced apoptosis in vivo. Cancer Cell 2, 279-288.
20. Kajita, M., McClinic, K. N., and Wade, P. A. (2004). Aberrant expression of the transcription factors Snail and Slug alters the response to genotoxic stress. Mol. Cell. Biol. 24, 7559-7566.
21. Kalluri, R., and Neilson, E. G. (2003). Epithelial-mesenchymal transition and its implications for fibrosis. J. Clin. Invest. 112, 1776-1784.
22. Kuphal, S., Palm, H. G., Poser, I., and Bosserhoff, A. K. (2005). Snail-regulated genes in malignant melanoma. Melanoma Res. 15, 305-313.
23. Lai, J. F., Juang, S. H., Hung, Y. M., Cheng, H. Y., Cheng, T. L., Mostov, K. E., and Jou, T. S. (2003). An ecdysone and tetracycline dual regulatory expression system for studies on Rac1 small GTPase-mediated signaling. Am. J. Physiol. Cell Physiol. 285, C711-C719.
24. Leroy, P., Berto, F., Bourget, I., and Rossi, B. (2004). Down-regulation of Hox A7 is required for cell adhesion and migration on fibronectin during early HL-60 monocytic differentiation. J. Leukoc. Biol. 75, 680-688.
25. Montesano, R., Schaller, G., and Orci, L. (1991). Induction of epithelial tubular morphogenesis in vitro by fibroblast-derived soluble factors. Cell 66, 697-711.
26. Nelson, C. M., and Bissell, M. J. (2005). Modeling dynamic reciprocity: engineering three-dimensional culture models of breast architecture, function, and neoplastic transformation. Semin. Cancer Biol. 15, 342-352.
27. Nieto, M. A. (2002). The snail superfamily of zinc-finger transcription factors. Nat. Rev. Mol. Cell Biol. 3, 155-166.
28. Nieto, M. A., Sargent, M. G., Wilkinson, D. G., and Cooke, J. (1994). Control of cell behavior during vertebrate development by Slug, a zinc finger gene. Science 264, 835-839.
29. O'Brien, L. E., Jou, T. S., Pollack, A. L., Zhang, Q., Hansen, S. H., Yurchenco, P., and Mostov, K. E. (2001). Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly. Nat. Cell Biol. 3, 831-838.
30. O'Brien, L. E., Tang, K., Kats, E. S., Schutz-Geschwender, A., Lipschutz, J. H., and Mostov, K. E. (2004). ERK and MMPs sequentially regulate distinct stages of epithelial tubule development. Dev. Cell 7, 21-32.
31. O'Brien, L. E., Zegers, M. M., and Mostov, K. E. (2002). Opinion: building epithelial architecture: insights from three-dimensional culture models. Nat. Rev. Mol. Cell Biol. 3, 531-537.
32. Peinado, H., Quintanilla, M., and Cano, A. (2003). Transforming growth factor beta-1 induces snail transcription factor in epithelial cell lines: mechanisms for epithelial mesenchymal transitions. J. Biol. Chem. 278, 21113-21123.
33. Pollack, A. L., Runyan, R. B., and Mostov, K. E. (1998). Morphogenetic mechanisms of epithelial tubulogenesis: MDCK cell polarity is transiently rearranged without loss of cell-cell contact during scatter factor/hepatocyte growth factor-induced tubulogenesis. Dev. Biol. 204, 64-79.
34. Robson, E. J., Khaled, W. T., Abell, K., and Watson, C. J. (2006). Epithelial-to-mesenchymal transition confers resistance to apoptosis in three murine mammary epithelial cell lines. Differentiation 74, 254-264.
35. Romano, L. A., and Runyan, R. B. (2000). Slug is an essential target of TGFbeta2 signaling in the developing chicken heart. Dev. Biol. 223, 91-102.
36. Savagner, P. (2001). Leaving the neighborhood: molecular mechanisms involved during epithelial-mesenchymal transition. Bioessays 23, 912-923.
37. Savagner, P., Kusewitt, D. F., Carver, E. A., Magnino, F., Choi, C., Gridley, T., and Hudson, L. G. (2005). Developmental transcription factor slug is required for effective re-epithelialization by adult keratinocytes. J. Cell. Physiol. 202, 858-866.
38. Savagner, P., Yamada, K. M., and Thiery, J. P. (1997). The zinc-finger protein slug causes desmosome dissociation, an initial and necessary step for growth factor-induced epithelial-mesenchymal transition. J. Cell Biol. 137, 1403-1419.
39. Sefton, M., Sanchez, S., and Nieto, M. A. (1998). Conserved and divergent roles for members of the Snail family of transcription factors in the chick and mouse embryo. Development 125, 3111-3121.
40. Shih, J. Y. et al. (2005). Transcription repressor slug promotes carcinoma invasion and predicts outcome of patients with lung adenocarcinoma. Clin. Cancer Res. 11, 8070-8078.
41. Thiery, J. P. (2002). Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. Cancer 2, 442-454.
42. Uchikado, Y., Natsugoe, S., Okumura, H., Setoyama, T., Matsumoto, M., Ishigami, S., and Aikou, T. (2005). Slug Expression in the E-cadherin preserved tumors is related to prognosis in patients with esophageal squamous cell carcinoma. Clin. Cancer Res. 11, 1174-1180.
43. Valdes, F., Alvarez, A. M., Locascio, A., Vega, S., Herrera, B., Fernandez, M., Benito, M., Nieto, M. A., and Fabregat, I. (2002). The epithelial mesenchymal transition confers resistance to the apoptotic effects of transforming growth factor Beta in fetal rat hepatocytes. Mol. Cancer Res. 1, 68-78.
44. Vega, S., Morales, A. V., Ocana, O. H., Valdes, F., Fabregat, I., and Nieto, M. A. (2004). Snail blocks the cell cycle and confers resistance to cell death. Genes Dev. 18, 1131-1143.
45. Verrecchia, F., Rossert, J., and Mauviel, A. (2001). Blocking sp1 transcription factor broadly inhibits extracellular matrix gene expression in vitro and in vivo: implications for the treatment of tissue fibrosis. J. Invest. Dermatol. 116, 755-763.
46. Wu, W. S., Heinrichs, S., Xu, D., Garrison, S. P., Zambetti, G. P., Adams, J. M., and Look, A. T. (2005). Slug antagonizes p53-mediated apoptosis of hematopoietic progenitors by repressing puma. Cell 123, 641-653.