Transforming growth factor-β2 promotes Snail-mediated endothelial - Mesenchymal transition through convergence of Smad-dependent and Smad-independent signalling

Biochemical Journal

Volumn 437, Issue 3, 2011, Pages 515-520

  Medici, Damian ^a   Potenta, Scott ^a   Kalluri, Raghu ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD MIT DIVISION OF HEALTH SCIENCES AND TECHNOLOGY   (United States)

Author keywords

Endothelial Mesenchymal transition (EMT); GSK 3 (glycogen synthase kinase 3 ); Smad; Snail; Transforming growth factor (TGF )

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3BETA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; SMAD PROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR SNAIL; TRANSFORMING GROWTH FACTOR BETA2;

ARTICLE; CELL TRANSFORMATION; ENDOTHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION;

CELLS, CULTURED; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; MESENCHYMAL STEM CELLS; RNA INTERFERENCE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SMAD PROTEINS; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA2;

GASTROPODA;

EID: 79960217559     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20101500     Document Type: Article

References (36)

1. Boyer, A. S., Ayerinskas, I. I., Vincent, E. B., McKinney, L. A., Weeks, D. L. and Runyan, R. B. (1999) TGFβ2 and TGFbeta3 have separate and sequential activities during epithelial - mesenchymal cell transformation in the embryonic heart. Dev. Biol. 208, 530-545
2. Camenisch, T D., Molin, D. G., Person, A., Runyan, R. B., Gittenberger-de Groot, A. C., McDonald, J. A. and Klewer, S. E. (2002) Temporal and distinct TGFβ ligand requirements during mouse and avian endocardial cushion morphogenesis. Dev. Biol. 248, 170-181
3. Azhar, M., Runyan, R. B., Gard, C., Sanford, L. P., Miller, M. L., Andringa, A., Pawlowski, S., Rajan, S. and Doetschman, T. (2009) Ligand-specific function of transforming growth factor β in epithelial - mesenchymal transition in heart development. Dev. Dyn. 238, 431-442
4. Zeisberg, E. M., Tarnavski, O., Zeisberg, M., Dorfman, A. L., McMullen, J. R., Gustafsson, E., Chandraker, A., Yuan, X., Pu, W. T., Roberts, A. B. et al. (2007) Endothelial-tomesenchymal transition contributes to cardiac fibrosis. Nat. Med. 13, 952-961
5. Zeisberg, E. M., Potenta, S., Xie, L., Zeisberg, M. and Kalluri, R. (2007) Discovery of endothelial to mesenchymal transition as a source for carcinoma-associated fibroblasts. Cancer Res. 67, 10123-10128 (Pubitemid 350070783)
6. Zeisberg, E. M., Potenta, S. E., Sugimoto, H., Zeisberg, M. and Kalluri, R. (2008) Fibroblasts in kidney fibrosis emerge via endothelial-to-mesenchymal transition. J. Am. Soc. Nephrol. 19, 2282-2287
7. Mironov, V., Hill, C., Starcher, B., Shih, J., Hoffman, S. and Markwald, R. (1995) Endothelial - mesenchymal transformation in atherosclerosis: a recapitulation of embryonic heart tissue morphogenesis. Ann. Biomed. Eng. 23, S29A
8. Arciniegas, E., Frid, M. G., Douglas, I. S. and Stenmark, K. R. (2007) Perspectives on endothelial-to-mesenchymal transition: potential contribution to vascular remodeling in chronic pulmonary hypertension. Am. J. Physiol. Lung Cell Mol. Physiol. 293, L1-L8
9. Kizu, A., Medici, D. and Kalluri, R. (2009) Endothelial - mesenchymal transition as a novel mechanism for generating myofibroblasts during diabetic nephropathy. Am. J. Pathol. 175, 1371-1373
10. Lee, J. G. and Kay, E. P. (2006) FGF-2-mediated signal transduction during endothelial mesenchymal transformation in corneal endothelial cells. Exp. Eye Res. 83, 1309-1316
11. Potenta, S., Zeisberg, E. and Kalluri, R. (2008) The role of endothelial-to-mesenchymal transition in cancer progression. Br. J. Cancer 99, 1375-1379
12. Liebner, S., Cattelino, A., Gallini, R., Rudini, N., Iurlaro, M., Piccolo, S. and Dejana, E (2004) β-Catenin is required for endothelial - mesenchymal transformation during heart cushion development in the mouse. J. Cell Biol. 166, 359-367 (Pubitemid 39031239)
13. Peinado, H., Portillo, F. and Cano, A. (2004) Transcriptional regulation of cadherins during development and carcinogenesis. Int. J. Dev. Biol. 48, 365-375
14. 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
15. Nawhsad, A., Medici, D., Liu, C. C. and Hay, E. D. (2007) TGFβ3 inhibits E-cadherin gene expression in palate medial-edge epithelial cells through a Smad2-Smad4-LEF-1 transcription complex. J. Cell Sci. 120, 1646-1653
16. Medici, D., Hay, E. D. and Goodenough, D. A. (2006) Cooperation between snail and LEF-1 transcription factors is essential for TGF-β1-induced epithelial - mesenchymal transition. Mol. Biol. Cell 17, 1871-1879
17. Kokudo, T., Suzuki, Y., Yoshimatsu, Y., Yamazaki, T., Watabe, T. and Miyazono, K. (2008) Snail is required for TGFβ-induced endothelial- mesenchymal transition of embryonic stem cell-derived endothelial cells. J. Cell Sci. 121, 3317-3324
18. Medici, D., Hay, E. D. and Olsen, B. R. (2008) Snail and Slug promote epithelial - mesenchymal transition through β-catenin-TCF-4-dependent expression of TGF-β3. Mol. Biol. Cell 19, 4875-4887
19. Akhurst, R. J. and Derynck, R. (2001) TGF-β signaling in cancer: a double-edged sword. Trends Cell Biol. 11, S44-S51
20. Thiery, J. P. (2003) Epithelial-mesenchymal transitions in development and pathologies. Curr. Opin. Cell Biol. 15, 740-746
21. Romano, L. A. and Runyan, R. B. (2000) Slug is an essential target of TGFβ2 signaling in the developing chicken heart. Dev. Biol. 223, 91-102
22. Deissler, H., Deissler, H., Lang, G. K. and Lang, G. E (2006) TGFβ induces transdifferentiation of iBREC to alphaSMA-expressing cells. Int. J. Mol. Med. 18, 577-582
23. Tavares, A. L., Mercado-Pimentel, M. E., Runyan, R. B. and Kitten, G. T (2006) TGFβ-mediated RhoA expression is necessary for epithelial - mesenchymal transition in the embryonic chick heart. Dev. Dyn. 235, 1589-1598
24. Mercado-Pimentel, M. E. and Runyan, R. B. (2007) Multiple transforming growth factor-β isoforms and receptors function during epithelial- mesenchymal cell transformation in the embryonic heart. Cells Tissues Organs 185, 146-156
25. Medici, D., Shore, E. M., Lounev, V. Y., Kaplan, F. S., Kalluri, R. and Olsen, B. R. (2010) Conversion of vascular endothelial cells into multipotent stem-like cells. Nat. Med. 16, 1400-1406
26. Boye, E., Yu, Y., Paranya, G., Mulliken, J. B., Olsen, B. R. and Bischoff, J. (2001) Clonality and altered behavior of endothelial cells from hemangiomas. J. Clin. Invest. 107, 745-752
27. Jinnin, M., Medici, D., Park, L., Limaye, N., Liu, Y., Boscolo, E., Bischoff, J., Vikkula, M., Boye, E. and Olsen, B. R. (2008) Suppressed NFAT-dependent VEGFR1 expression and constitutive VEGFR2 signaling in infantile hemangioma. Nat. Med. 14, 1236-1246
28. Zhang, L., Graziano, K., Pham, T., Logsdon, C. D. and Simeone, D. M. (2001) Adenovirus mediated gene transfer of dominant negative Smad4 blocks TGF-β signaling in pancreatic acinar cells. Am. J. Physiol. Gastrointest. Liver Physiol. 280, G1247-G1253
29. Zhou, B. P., Deng, J., Xia, W., Xu, J., Li, Y. M., Gunduz, M. and Hung, M. C. (2004) Dual regulation of Snail by GSK-3beta-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat. Cell Biol. 6, 931-940
30. Cantley, L. C. (2002) The phosphoinositide 3-kinase pathway. Science 296, 1655-1657
31. Jamora, C., Lee, P., Kocieniewski, P., Azhar, M., Hosokawa, R., Chai, Y. and Fuchs, E. (2005) A signaling pathway involving TGF-β2 and Snail in hair follicle morphogenesis. PLoS Biol. 3, 131-142
32. Hoot, K. E., Lighthall, J., Han, G., Lu, S. L., Li, A., Ju, W., Kulesz-Martin, M., Bottinger, E. and Wang, X. J. (2008) Keratinocyte-specific Smad2 ablation results in increased epithelial - mesenchymal transition during skin cancer formation and progression. J. Clin. Invest. 118, 2722-2732
33. Smith, A. P., Verrecchia, A., Faga, G., Doni, M., Perna, D., Martinato, F., Guccione, E. and Amati, B. (2009) A positive role for Myc in TGFβ-induced Snail transcription and epithelial-to-mesenchymal transition. Oncogene 28, 422-430
34. Brandl, M., Seidler, B., Haller, F., Adamski, J., Schmid, R. M., Saur, D. and Schneider, G. (2010) IKKα controls canonical TGFβ-SMAD signaling to regulate genes expressing SNAIL and SLUG during EMT in Panc1 cells. J. Cell Sci. 123, 4231-4239
35. Cano, A., Perez-Moreno, M. A., Rodrigo, I., Locascio, A., Bianco, 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
36. Vetter, G., Saumet, A., Moes, M., Vallar, L., Le Bechec, A., Laurini, C., Sabbah, M., Arar, K., Theillet, C., Lecellier, C. H. and Friederich, E. (2010) miR-661 expression in SNAI1-induced epithelial to mesenchymal transition contributes to breast cancer cell invasion by targeting Nectin-1 and StarD10 messengers. Oncogene 29, 4436-4448