Interaction with Smad4 is Indispensable for Suppression of BMP Signaling by c-Ski

Molecular Biology of the Cell

Volumn 15, Issue 3, 2004, Pages 963-972

  Takeda, Masafumi ^a   Mizuide, Masafumi ^b   Oka, Masako ^a   Watabe, Tetsuro ^a   Inoue, Hirofumi ^b   Suzuki, Hiroyuki ^a   Fujita, Toshiro ^a   Imamura, Takeshi ^b   Miyazono, Kohei ^a,b   Miyazawa, Keiji ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b CANCER INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVIN; BONE MORPHOGENETIC PROTEIN; HISTONE DEACETYLASE; HISTONE DEACETYLASE 1; LUCIFERASE; MUTANT PROTEIN; PROTEIN C SKI; REPRESSOR PROTEIN; SMAD1 PROTEIN; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD4 PROTEIN; SMAD5 PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL DIFFERENTIATION; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; EPITHELIUM CELL; HUMAN; HUMAN CELL; MAMMAL CELL; MESENCHYME CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; XENOPUS;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL DIFFERENTIATION; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; DNA-BINDING PROTEINS; EMBRYO, NONMAMMALIAN; HISTONE DEACETYLASES; HUMANS; MUTATION; OSTEOBLASTS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; SMAD PROTEINS; SMAD1 PROTEIN; SMAD4 PROTEIN; TRANS-ACTIVATORS; TRANSFORMING GROWTH FACTOR BETA; XENOPUS; XENOPUS PROTEINS;

ANIMALIA; MAMMALIA;

EID: 12144291415     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E03-07-0478     Document Type: Article

References (48)

1. Akhurst, R.J. (2002). TGF-β antagonists: why suppress a tumor suppressor? J. Clin. Invest. 109, 1533-1536.
2. Akiyoshi, S., Inoue, H., Hanai, J., Kusanagi, K., Nemoto, N., Miyazono, K., and Kawabata, M. (1999). c-Ski acts as a transcriptional co-repressor in transforming growth factor-β signaling through interaction with Smads. J. Biol. Chem. 274, 35269-35277.
3. Amaravadi, L.S., Neff, A.W., Sleeman, J.P., and Smith, R.C. (1997). Autonomous neural axis formation by ectopic expression of the protooncogene c-ski. Dev. Biol. 192, 392-404.
4. Asahina, I., Sampath, T.K., Nishimura, I., and Hauschka, P.V. (1993). Human osteogenic protein-1 induces both chondroblastic and osteoblastic differentiation of osteoprogenitor cells derived from newborn rat calvaria. J. Cell Biol. 123, 921-933.
5. Attisano, L., and Wrana, J.L. (2000). Smads as transcriptional co-modulators. Curr. Opin. Cell Biol. 12, 235-243.
6. Bakin, A., Tomlinson, A.K., Bhowmick, N.A., Moses, H.L., and Artega, C.L. (2000). Phosphatidylinositol 3-kinase function is required for transforming growth factor β-mediated epithelial to mesenchymal transition and cell migration. J. Biol. Chem. 275, 36803-36810.
7. 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-β1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Mol. Biol. Cell 12, 27-36.
8. Cho, K.W., Blumberg, B., Steinbeisser, H., and De Robertis, E.M. (1991). Molecular nature of Spemann's organizer: the role of the Xenopus homeobox gene gooscoid. Cell 67, 1111-1120.
9. Colmenares, C., and Stavnezer, E. (1989). The ski oncogene induces muscle differentiation in quail embryo cells. Cell 59, 293-303.
10. Colmenares, C., Teumer, J.K., and Stavnezer, E. (1991). Translation-defective v-ski induces MyoD and myogenin expression but not myotube formation. Mol. Cell. Biol. 11, 1167-1170.
11. Correia, J., Chacko, B.B., Lam, S.S., and Lin, K. (2001). Sedimentation studies reveal a direct role of phosphorylation in Smad3:Smad4 homo- and heterotrimerization. Biochemistry 40, 1473-1482.
12. Dennler, S., Itoh, S., Vivien, D., ten Dijke, P., Huet, S., and Gauthier, J.-M. (1998). Direct binding of Smad3 and Smad4 to critical TGFβ-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J. 17, 3091-3100.
13. Derynck, R., Zhang, Y., and Feng, X.H. (1998). Smads: transcriptional activators of TGF-β responses. Cell 95, 737-740.
14. Fujii, M. et al. (1999). Roles of bone morphogenetic protein type I receptors and Smad proteins in osteoblast and chondroblast differentiation. Mol. Biol. Cell 10, 3801-3813.
15. Fumagalli, S., Doneda, L., Nomura, N., and Larizza, L. (1993). Expression of the c-ski proto-oncogene in human melanoma cell lines. Melanoma Res. 3, 23-37.
16. Goldman, L.A., Cutrone, E.C., Kotenko, S.V., Krause, C.D., and Langer, J.A. (1996). Modifications of vectors pEF-BOS, pcDNA1 and pcDNA3 result in improved convenience and expression. Biotechniques 21, 1013-1015.
17. He, J., Tegen, A.B., Krawitz, A.R., Martin, G.S., and Luo, K. (2003). The transforming activity of Ski and SnoN is dependent on their ability to repress the activity of Smad proteins. J. Biol. Chem. 278, 30540-30547.
18. Inman, G.J., Nicolas, F.J., Callahan, J.F., Harling, J.D., Gaster, L.M., Reith, A.D., Laping, N.J., and Hill, C.S. (2002). SB-431542 is a potent and specific inhibitor of transforming growth factor-β superfamily type I activin receptor-like kinase (ALK) receptors ALK4, ALK5, and ALK7. Mol. Pharmacol, 63, 65-74.
19. Ishida, W., Hamamoto, T., Kusanagi, K., Yagi, K., Kawabata, M., Takehara, K., Sampath, T.K., Kato, M., and Miyazono, K. (2000), Smad6 is a Smad1/5-induced Smad inhibitor: characterization of bone morphogeneic protein-responsive element in the mouse Smad6 promoter. J. Biol. Chem. 275, 6075-6079.
20. Katagiri, T. et al. (1994). Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage. J. Cell Biol. 127, 1755-1766.
21. Kawabata, M., Inoue, H., Hanyu, A., Imamura, T., and Miyazono, K. (1998). Smad proteins exist as monomers in vivo and undergo homo- and heterooligomerization upon activation by serine/threonine kinase receptors. EMBO J. 17, 4056-4065.
22. Li, Y., Turck, C.M., Teumer, J.K., and Stavnezer, E. (1986). Unique sequence, ski, in Sloan-Kettering avian retroviruses with properties of a new cell-derived oncogene. J. Virol. 57, 1065-1072.
23. Liu, X., Sun, Y., Weinberg, R.A., and Lodish, H.F. (2001). Ski/Sno and TGF-β signaling. Cytokine Growth Factor Rev. 12, 1-8.
24. Luo, K., Stroschein, S.L., Wang, W., Chen, D., Martens, E., Zhou, S., and Zhou, Q. (1999). The Ski oncoprotein interacts with the Smad proteins to repress TGFβ signaling. Genes Dev. 13, 2196-2206.
25. Massagué, J., and Chen, Y.-G. (2000). Controlling TGF-β signaling. Genes Dev. 14, 637-644.
26. 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.
27. 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.
28. Miyazono, K., Kusanagi, K., and Inoue, H. (2001). Divergence and convergence of TGF-β/BMP signaling. J. Cell. Physiol. 187, 265-276.
29. Mizuide, M. et al. (2003). Two short segments of Smad3 are important for specific interaction of Smad3 with c-Ski and SnoN. J. Biol. Chem. 278, 531-536.
30. Muraoka, R.S. et al. (2002). Blockade of TGF-β inhibits mammary tumor cell viability, migration, and metastases. J. Clin. Invest. 109, 1551-1559.
31. Nakao, A., Fujii, M., Matsumura, R., Kumano, K., Saito, Y., Miyazono, K., and Iwamoto, I. (1999). Transient gene transfer and expression of Smad7 prevents bleomycin-induced lung fibrosis in mice. J. Clin. Invest. 104, 5-11.
32. Nakayama, T., Snyder, M.A., Grewal, S.S., Tsuneizumi, K., Tabata, T., and Christian, J.L. (1998). Xenopus Smad8 acts downstream of BMP-4 to modulate its activity during vertebrate embryonic patterning. Development 125, 857-867.
33. Nomura, N., Sasamoto, S., Ishii, S., Date, T., Matsui, M., and Ishizaki, R. (1989). Isolation of human cDNA clones of ski and the ski-related gene, sno. Nucleic Acid Res. 17, 5489-5550.
34. Nomura, T., Khan, M.M., Kaul, S.C., Dong, H.D., Wadhwa, R., Colmenares, C., Kohno, I., and Ishii, S. (1999). Ski is a component of the histone deacetylase complex required for transcriptional repression by Mad and thyroid hormone receptor. Genes Dev. 13, 412-423.
35. Oft, M., Akhurst, R.J., and Balmain, A. (2002). Metastasis is driven by sequential elevation of H-ras and Smad2 level. Nat. Cell Biol. 4, 487-494.
36. Ota, T., Fujii, M., Sugizaki, T., Ishii, M., Miyazawa, K., Aburatani, H., and Miyazono, K. (2002). Targets of transcriptional regulation by two distinct type I receptors for transforming growth factor-β in human umbilical vein endothelial cells. J. Cell. Physiol. 193, 299-318.
37. Piek, E., and Roberts, A.B. (2001). Suppressor and oncogenic roles of transforming growth factor-β and its signaling pathways in tumorigenesis. Adv. Cancer Res. 83, 1-54.
38. 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, 4557-4568.
39. Prunier, C., Pessah, M., Ferrand, N., Seo, S. R., Howe, P., and Atfi, A. (2003). The oncoprotein Ski acts as an antagonist of TGF-β signaling by suppressing Smad2 phosphorylation. J. Biol. Chem. 278, 26249-26257.
40. Qin, B.Y., Lam, S.S., Correia, J.J., and Lin, K. (2002). Smad3 allostery links TGF-β receptor kinase activation to transcriptional control. Genes Dev. 16, 1950-1963.
41. Reed, J.A., Bales, E., Xu, W., Okan, N.A., Bandyopadhyay, D., and Medrano, E.E. (2001). Cytoplasmic localization of the oncogenic protein Ski in human cutaneous melanomas in vivo: functional implications for transforming growth factor β signaling. Cancer Res. 61, 8074-8078.
42. Shi, Y., and Massagué, J. (2003). Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell 113, 685-700.
43. Stavnezer, E., Brodeur, D., and Brennan, L. (1989). The v-ski oncogene encodes a truncated set of c-ski coding exons with limited sequence and structural relatedness to v-myc. Mol. Cell. Biol. 9, 4038-4045.
44. Sun, Y., Liu, X., Eaton, E.N., Lane, W.S., Lodish, H.F., and Weinberg, R.A. (1999). Interaction of the Ski oncoprotein with Smad3 regulates TGF-β signaling. Mol. Cell 4, 499-509.
45. Wang, W., Mariani, F.V., Harland, R.M., and Luo, K. (2000). Ski represses bone morphogenic protein signaling in Xenopus and mammalian cells. Proc. Natl. Acad. Sci. USA 97, 14394-14399.
46. Wu, J.W., Krawitz, A.R., Chai, J., Li, W., Zhang, F., Luo, K., and Shi, Y. (2002). Structural mechanism of Smad4 recognition by the nuclear oncoprotein Ski. Insights on Ski-mediated repression of TGF-β signaling. Cell 111, 357-367.
47. Xu, W., Angelis, K., Danielpour, D., Haddad, M.M., Bischof, O., Campisi, J., Stavnezer, E., and Medrano, E.E. (2000). Ski acts as a co-repressor with Smad2 and Smad3 to regulate the response to type β transforming growth factor. Proc. Natl. Acad. Sci. USA 97, 5924-5929.
48. Yang, Y. et al. (2002). Lifetime exposure to soluble TGF-β antagonist protects mice against metastasis without adverse side effects. J. Clin. Invest. 109, 1607-1615.