Differential regulation of epithelial and mesenchymal markers by δEF1 proteins in epithelial-mesenchymal transition induced by TGF-β

Molecular Biology of the Cell

Volumn 18, Issue 9, 2007, Pages 3533-3544

  Shirakihara, Takuya ^a   Saitoh, Masao ^a   Miyazono, Kohei ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL MARKER; FIBRONECTIN; INHIBITOR OF DIFFERENTIATION PROTEIN; NERVE CELL ADHESION MOLECULE; PROTEIN DELTA EF1; PROTEIN SIP1; PROTEIN ZEB1; TRANSCRIPTION FACTOR ETS 1; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN; ZINC FINGER PROTEIN;

ANIMAL CELL; ARTICLE; CANCER GROWTH; CELL INTERACTION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO DEVELOPMENT; EPITHELIUM CELL; GENE EXPRESSION PROFILING; GENE SILENCING; MESENCHYME CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FAMILY; REGULATORY MECHANISM; UPREGULATION;

ANIMALS; BIOLOGICAL MARKERS; CADHERINS; CELL MOVEMENT; DOGS; E-BOX ELEMENTS; EPITHELIAL CELLS; HOMEODOMAIN PROTEINS; HUMANS; MESODERM; MICE; NERVE TISSUE PROTEINS; PROTEIN BIOSYNTHESIS; PROTO-ONCOGENE PROTEIN C-ETS-1; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; SMAD PROTEINS; TRANSCRIPTION FACTORS; TRANSFORMING GROWTH FACTOR BETA; UP-REGULATION;

EID: 34548496683     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-03-0249     Document Type: Article

References (52)

1. Akhurst, R. J., and Derynck, R. (2001). TGF-β signaling in cancer - a double-edged sword. Trends Cell Biol. 11, S44-S51.
2. Akiyoshi, S., Ishii, M., Nemoto, N., Kawabata, M., Aburatani, H., and Miyazono, K. (2001). Targets of transcriptional regulation by transforming growth factor-β: expression profile analysis using oligonucleotide arrays. Jpn. J. Cancer Res. 92, 257-268.
3. Azuma, H. et al. (2005). Effect of Smad7 expression on metastasis of mouse mammary carcinoma JygMC(A) cells. J. Natl. Cancer Inst. 97, 1734-1746.
4. 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.
5. Bhowmick, N. A., Ghiassi, M., Bakin, A., Aakre, M., Lundquist, C. A., Engel, M. E., Arteaga, C. L., and Moses, H. L. (2001). Transforming growth factor-β 1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Mol. Biol. Cell 12, 27-36.
6. Bierie, B., and Moses, H. L. (2006). TGF-β and cancer. Cytokine Growth Factor Rev. 17, 29-40.
7. Caulin, C., Scholl, F. G., Frontelo, P., Gamallo, C., and Quintanilla, M. (1995). Chronic exposure of cultured transformed mouse epidermal cells to transforming growth factor-β 1 induces an epifhelial-mesenchymal transdifferentiation and a spindle tumoral phenotype. Cell Growth Differ. 6, 1027-1035.
8. Comijn, J., Berx, G., Vermassen, P., Verschueren, K., van Grunsven, L., Bruyneel, E., Mareel, M., Huylebroeck, D., and van Roy, F. (2001). The two-handed E box binding zinc finger protein SIP1 downregulates E-cadherin and induces invasion. Mol. Cell 7, 1267-1278.
9. Dang, W., Sun, X. H., and Sen, R. (1998). ETS-mediated cooperation between basic helix-loop-helix motifs of the immunoglobulin mu heavy-chain gene enhancer. Mol. Cell. Biol. 18, 1477-1488.
10. del Valle-Perez, B., Martinez-Estrada, O. M., Vilaro, S., Ventura, F., and Vinals, F. (2004). cAMP inhibits TGF-β 1-induced in vitro angiogenesis. FEBS Lett. 569, 105-111.
11. Derynck, R., Akhurst, R. J., and Balmain, A. (2001). TGF-β signaling in tumor suppression and cancer progression. Nat. Genet. 29, 117-129.
12. Gorska, A. E., Jensen, R. A., Shyr, Y., Aakre, M. E., Bhowmick, N. A., and Moses, H. L. (2003). Transgenic mice expressing a dominant-negative mutant type II transforming growth factor-β receptor exhibit impaired mammary development and enhanced mammary tumor formation. Am. J. Pathol. 163, 1539-1549.
13. Gotzmann, J., Huber, H., Thallinger, C., Wolschek, M., Jansen, B., Schulte-Hermann, R., Beug, H., and Mikulits, W. (2002). Hepatocytes convert to a fibroblastoid phenotype through the cooperation of TGF-β 1 and Ha-Ras: steps towards invasiveness. J. Cell Sci. 115, 1189-1202.
14. Heldin, C. H., Miyazono, K., and ten Dijke, P. (1997). TGF-β signalling from cell membrane to nucleus through SMAD proteins. Nature 390, 465-471.
15. Hocevar, B. A., Brown, T. L., and Howe, P. H. (1999). TGF-β induces fibronectin synthesis through a c-Jun N-terminal kinase-dependent, Smad4-independent pathway. EMBO J. 18, 1345-1356.
16. Kim, Y. H., Lee, H. S., Lee, H. J., Hur, K., Kim, W. H., Bang, Y. J., Kim, S. J., Lee, K. U., Choe, K. J., and Yang, H. K. (2004). Prognostic significance of the expression of Smad4 and Smad7 in human gastric carcinomas. Ann. Oncol. 15, 574-580.
17. Kleeff, J., Ishiwata, T., Maruyama, H., Friess, H., Truong, P., Buchler, M. W., Falb, D., and Korc, M. (1999). The TGF-β signaling inhibitor Smad7 enhances tumorigenicity in pancreatic cancer. Oncogene 18, 5363-5372.
18. Kobayashi, N., Goto, K., Horiguchi, K., Nagata, M., Kawata, M., Miyazawa, K., Saitoh, M., and Miyazono, K. (2007). c-Ski activates MyoD in the nucleus of myoblastic cells through suppression of histone deacetylases. Genes Cells 12, 375-385.
19. Kondo, M., Cubillo, E., Tobiume, K., Shirakihara, T., Fukuda, N., Suzuki, H., Shimizu, K., Takehara, K., Cano, A., Saitoh, M., and Miyazono, K. (2004). A role for Id in the regulation of TGF-β-induced epithelial-mesenchymal transdifferentiation. Cell Death Differ. 11, 1092-1101.
20. Kowanetz, M., Valcourt, U., Bergstrom, R., Heldin, C. H., and Moustakas, A. (2004). Id2 and Id3 define the potency of cell proliferation and differentiation responses to transforming growth factor β and bone morphogenetic protein. Mol. Cell. Biol. 24, 4241-4254.
21. Lee, J. M., Dedhar, S., Kalluri, R., and Thompson, E. W. (2006). The epithelial-mesenchymal transition: new insights in signaling, development, and disease. J. Cell Biol. 172, 973-981.
22. Lu, S. L. et al. (2006). Loss of transforming growth factor-β type II receptor promotes metastatic head-and-neck squamous cell carcinoma. Genes Dev. 20, 1331-1342.
23. Miettinen, P. J., Ebner, R., Lopez, A. R., and Derynck, R. (1994). TGF-β induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. J. Cell Biol. 127, 2021-2036.
24. Miyazawa, K., Shinozaki, M., Hara, T., Furuya, T., and Miyazono, K. (2002). Two major Smad pathways in TGF-β superfamily signalling. Genes Cells 7, 1191-1204.
25. Miyazono, K., Suzuki, H., and Imamura, T. (2003). Regulation of TGF-β signaling and its roles in progression of tumors. Cancer Sci. 94, 230-234.
26. Moreno-Bueno, G. et al. (2006). Genetic profiling of epithelial cells expressing E-cadherin repressors reveals a distinct role for snail, slug, and E47 factors in epithelial-mesenchymal transition. Cancer Res. 66, 9543-9556.
27. Muraoka, R. S. et al. (2002). Blockade of TGF-β inhibits mammary tumor cell viability, migration, and metastases. J. Clin. Invest. 109, 1551-1559.
28. Nagata, M., Goto, K., Ehata, S., Kobayashi, N., Saitoh, M., Miyoshi, H., Imamura, T., Miyazawa, K., and Miyazono, K. (2006). Nuclear and cytoplasmic c-Ski differently modulate cellular functions. Genes Cells 11, 1267-1280.
29. Oft, M., Akhurst, R. J., and Balmain, A. (2002). Metastasis is driven by sequential elevation of H-ras and Smad2 levels. Nat. Cell Biol. 4, 487-494.
30. Ozdamar, B., Bose, R., Barrios-Rodiles, M., Wang, H. R., Zhang, Y., and Wrana, J. L. (2005). Regulation of the polarity protein Par6 by TGF-β receptors controls epithelial cell plasticity. Science 307, 1603-1609.
31. Park, K., Kim, S. J., Bang, Y. J., Park, J. G., Kim, N. K., Roberts, A. B., and Sporn, M. B. (1994). Genetic changes in the transforming growth factor β (TGF-β) type II receptor gene in human gastric cancer cells: correlation with sensitivity to growth inhibition by TGF-β. Proc. Natl. Acad. Sci. USA 91, 8772-8776.
32. Peinado, H., Del Carmen Iglesias-de la Cruz, M., Olmeda, D., Csiszar, K., Fong, K. S., Vega, S., Nieto, M. A., Cano, A., and Portillo, F. (2005). A molecular role for lysyl oxidase-like 2 enzyme in snail regulation and tumor progression. EMBO J. 24, 3446-3458.
33. Peinado, H., Portillo, F., and Cano, A. (2004). Transcriptional regulation of cadherins during development and carcinogenesis. Int. J. Dev. Biol. 48, 365-375.
34. Peinado, H., Quintanilla, M., and Cano, A. (2003). Transforming growth factor β-1 induces snail transcription factor in epithelial cell lines: mechanisms for epithelial mesenchymal transitions. J. Biol. Chem. 278, 21113-21123.
35. Piek, E., Moustakas, A., Kurisaki, A., Heldin, C. H., and ten Dijke, P. (1999). TGF-β type I receptor/ALK-5 and Smad proteins mediate epithelial to mesenchymal transdifferentiation in NMuMG breast epithelial cells. J. Cell Sci. 112(Pt 24), 4557-4568.
36. Portella, G., Cumming, S. A., Liddell, J., Cui, W., Ireland, H., Akhurst, R. J., and Balmain, A. (1998). Transforming growth factor β is essential for spindle cell conversion of mouse skin carcinoma in vivo: implications for tumor invasion. Cell Growth Differ. 9, 393-404.
37. Postigo, A. A. (2003). Opposing functions of ZEB proteins in the regulation of the TGFbeta/BMP signaling pathway. EMBO J. 22, 2443-2452.
38. Postigo, A. A., Depp, J. L., Taylor, J. J., and Kroll, K. L. (2003). Regulation of Smad signaling through a differential recruitment of coactivators and compressors by ZEB proteins. EMBO J. 22, 2453-2462.
39. Sapkota, G., Alarcon, C., Spagnoli, F. M., Brivanlou, A. H., and Massague, J. (2007). Balancing BMP signaling through integrated inputs into the Smad1 linker. Mol. Cell 25, 441-454.
40. Shi, Y., and Massague, J. (2003). Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 113, 685-700.
41. Thiery, J. P., and Sleeman, J. P. (2006). Complex networks orchestrate epithelial-mesenchymal transitions. Nat. Rev. Mol. Cell Biol. 7, 131-142.
42. Thuault, S., Valcourt, U., Petersen, M., Manfioletti, G., Heldin, C. H., and Moustakas, A. (2006). Transforming growth factor-β employs HMGA2 to elicit epithelial-mesenchymal transition. J. Cell Biol. 174, 175-183.
43. Tootle, T. L., and Rebay, I. (2005). Post-translational modifications influence transcription factor activity: a view from the ETS superfamily. Bioessays 27, 285-298.
44. van Grunsven, L. A., Michiels, C., Van de Putte, T., Nelles, L., Wuytens, G., Verschueren, K., and Huylebroeck, D. (2003), Interaction between Smad-interacting protein-1 and the corepressor C-terminal binding protein is dispensable for transcriptional repression of E-cadherin. J. Biol. Chem. 278, 26135-26145.
45. Verschueren, K. et al. (1999). SIP1, a novel zinc finger/homeodomain repressor, interacts with Smad proteins and binds to 5′-CACCT sequences in candidate target genes. J. Biol. Chem. 274, 20489-20498.
46. Xie, L., Law, B. K., Aakre, M. E., Edgerton, M., Shyr, Y., Bhowmick, N. A., and Moses, H. L. (2003). Transforming growth factor β-regulated gene expression in a mouse mammary gland epithelial cell line. Breast Cancer Res. 5, R187-198.
47. Yamagata, H. et al. (2005). Acceleration of Smad2 and Smad3 phosphorylation via c-Jun NH(2)-terminal kinase during human colorectal carcinogenesis. Cancer Res. 65, 157-165.
48. Yamashita, S., Miyagi, C., Fukada, T., Kagara, N., Che, Y. S., and Hirano, T. (2004). Zinc transporter LIVI controls epithelial-mesenchymal transition in zebrafish gastrula organizer. Nature 429, 298-302.
49. 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.
50. Yates, P. R., Atherton, G. T., Deed, R. W., Norton, J. D., and Sharrocks, A. D. (1999). Id helix-loop-helix proteins inhibit nucleoprotein complex formation by the TCF ETS-domain transcription factors. EMBO J. 18, 968-976.
51. Zavadil, J., and Bottinger, E. P. (2005). TGF-β and epithelial-to-mesenchymal transitions. Oncogene 24, 5764-5774.
52. 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-3β-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat. Cell Biol. 6, 931-940.