The Ski oncoprotein interacts with the Smad proteins to repress TGF̄ signaling

Genes and Development

Volumn 13, Issue 17, 1999, Pages 2196-2206

  Luo, Kunxin ^a,b   Stroschein, Shannon L ^a,b   Wang, Wei ^a,c   Chen, Dan ^b   Martens, Eric ^b   Zhou, Sharleen ^b   Zhou, Qiang ^b  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

Author keywords

Growth inhibition; Signal transduction; Ski; Smad proteins; TGF ; Transcriptional activation

Indexed keywords

DNA; OLIGOMER; ONCOPROTEIN; PROTEIN; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DNA BINDING; GENE; GENETIC TRANSCRIPTION; GROWTH INHIBITION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

CELL LINE; DNA-BINDING PROTEINS; GENES, TUMOR SUPPRESSOR; HUMANS; LYMPHOTOXIN-ALPHA; PROTO-ONCOGENE PROTEINS; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RECOMBINANT PROTEINS; RETROVIRIDAE; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; SMAD3 PROTEIN; SMAD4 PROTEIN; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 0033200361     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.13.17.2196     Document Type: Article

References (60)

1. Alland, L., R. Muhle, H. Hou, Jr., J. Potes, L. Chin, N. Schreiber-Agus, and R.A. DePinho. 1997. Role for N-CoR and histone deacetylase in Sin3-mediated transcriptional repression. Nature 387: 49-55.
2. Amaravadi, L.S., A.W. Neff, J.P. Sleeman, and R.C. Smith. 1997. Autonomous neural axis formation by ecotopic expression of the protooncogene c-ski. Dev. Biol. 192: 392-404.
3. Berk, M., S.Y. Desai, H.C. Heyman, and C. Colmenares. 1997. Mice lacking the ski proto-oncogene have defects in neurulation, craniofacial, patterning, and skeletal muscle development. Genes & Dev. 11: 2029-2039.
4. Chen, X., M.J. Rubock, and M. Whitman. 1996. A transcriptional partner for MAD proteins in TGF-beta signalling. Nature 383: 691-696.
5. Chen, X., E. Weisberg, V. Fridmacher, M. Watanabe, G. Naco, and M. Whitman. 1997. Smad4 and FAST-1 in the assembly of activin-responsive factor. Nature 389: 85-89.
6. Colmenares, C. and E. Stavnezer. 1989. The ski oncogene induces muscle differentiation in quail embryo cells. Cell 59: 293-303.
7. Colmenares, C., P. Sutrave, S.H. Hughes, and E. Stavnezer. 1991. Activation of the c-ski oncogene by overexpression. J. Virol. 65: 4929-4935.
8. Dahl, R., M. Kieslinger, H. Beug, and M.J. Hayman. 1998. Transformation of hematopoietic cells by the Ski oncoprotein involves repression of retinoic acid receptor signaling. Proc. Natl. Acad. Sci. 95: 11187-11192.
9. Dennler, S., S. Itoh, D. Vivien, P. ten Dijke, S. Huet, and J.M. Gauthier. 1998. Direct binding of Smad3 and Smad4 to critical TGF beta-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J. 17: 3091-3100.
10. Engert, J. C., S. Servaes, P. Sutrave, S.H. Hughes, and N. Rosenthal. 1995. Activation of a muscle-specific enhancer by the Ski proto-oncogene. Nucleic Acids Res. 23: 2988-2994.
11. Feng, X.-H., Y, Zhang, R.-Y. Wu, and R. Derynck. 1998. The tumor suppressor Smad4/DPC4 and transcriptional adaptor CBP/p300 are coactivators for Smad3 in TGF-β-induced transcriptional activation. Genes & Dev. 12: 2153-2163.
12. Fumagalli, S., L. Doneda, N. Nomura, and L. Larizza. 1993. Expression of the c-ski proto-oncogene in human melanoma cell lines. Melanoma Res. 3: 23-27.
13. Hata, A., R.S. Lo, D. Wotton, G. Lagna, and J. Massagué. 1997. Mutations increasing autoinhibition inactivate tumour suppressors Smad2 and Smad4. Nature 388: 82-87.
14. Heinzel, T., R.M. Lavinsky, T.M. Mullen, M. Soderstrom, C.D. Laherty, J. Torchia, W.M. Yang, G. Brard, S.D. Ngo, J.R. Davie, E. Seto, R.N. Eisenman, D.W. Rose, C.K. Glass, and M.G. Rosenfeld. 1997. A complex containing N-CoR, mSin3 and histone deacetylase mediates transcriptional repression. Nature 387: 43-48.
15. Heldin, C-H., K. Miyazono, and P. ten Dijke. 1997. TGF-β signaling from cell membrane to nucleus through SMAD proteins. Nature 390: 465-471.
16. Horlein, A.J., A.M. Naar, T. Heinzel, J. Torchia, B. Gloss, R. Kurokawa, A. Ryan, Y. Kamei, M. Soderstrom, C.K. Glass, et al. 1995. Ligand-independent repression by the thyroid hormone receptor mediated by a nuclear receptor co-repressor. Nature 377: 397-404.
17. Hua, X., X. Liu, D.O. Ansari, and H.F, Lodish. 1998. Synergistic cooperation of TFE3 and Smad proteins in TGFβ-induced transcription of the plasminogen activator inhibitor-1 gene. Genes & Dev. 12: 084-3095.
18. Janknecht, R., N.J. Wells, and T. Hunter. 1998. TGF-β-stimulated cooperation of Smad proteins with the coactivators CBP/p300. Genes & Dev. 12: 2114-2119.
19. Jonk, L.J., S. Itoh, C.H. Heldin, P. ten Dijke, and W. Kruijer. 1998. Identification and functional characterization of a Smad binding element (SBE) in the JunB promoter that acts as a transforming growth factor-beta, activin, and bone morphogenetic protein-inducible enhancer. J. Biol. Chem. 273: 21145-21152.
20. Kon, A., L. Vindevoghel, D.J. Kouba, Y. Fujimura, J. Uitto, and A. Mauviel. 1999. Cooperation between SMAD and NF-kappaB in growth factor regulated type VII collagen gene expression. Oncogene 18: 1837-1844.
21. Kretzschmar, M., J. Doody, and J. Massagué. 1997. Opposing BMP and EGF signalling pathways converge on the TGF-beta family mediator Smad1. Nature 389: 618-622.
22. Kretzschmar, M., J. Doody, I. Timokhina, and J. Massagué. 1999. A mechanism of repression of TGFβ/Smad signaling by oncogenic Ras. Genes & Dev. 13: 804-816.
23. Kurokawa, M., K. Mitani, K.M. Irie, T. Takahashi, S. Chiba, Y. Yazaki, K. Matsumoto, and H. Hirai. 1998. The oncoprotein Evi-1 represses TGFβ signaling by inhibiting Smad3. Nature 394: 92-96.
24. Labbe, E., C. Silvestri, P.A. Hoodless, J.L. Wrana, and L. Attisano. 1998. Smad2 and Smad3 positively and negatively regulate TGF beta-dependent transcription through the forkhead DNA-binding protein FAST2. Mol. Cell 2: 109-120.
25. Lee, K.A.W., A. Bindereif, and M.R. Green. 1987. A small-scale procedure for preparation of nuclear extracts that support efficient transcription and pre-mRNA splicing. Genet. Anal. Technol. 5: 22-31.
26. Leferovich, J.M., D.P. Lana, P. Sutrave, S.H. Hughes, and A.M. Kelly. 1995. Regulation of c-ski transgene expression in developing and mature mice. J. Neurosci. 15: 596-603.
27. Li, Y., C.M. Turck, J.K. Teumer, and E. Stavnezer. 1986. Unique sequence, ski, in Sloan-Kettering avian retroviruses with properties of a new cell-derived oncogene. J. Virol. 57: 1065-1072.
28. Liu, F., A. Hata, J.C. Baker, J. Doody, J. Carcamo, R.M. Harland, and J. Massagué. 1996. A human Mad protein acting as a BMP-regulated transcriptional activator. Nature 381: 620-623.
29. Luo, K. and H.F. Lodish. 1996. Signaling by chimeric erythropoietin-TGF-beta receptors: Homodimerization of the cytoplasmic domain of the type I TGF-beta receptor and heterodimerization with the type II receptor are both required for intracellular signal transduction. EMBO J. 15: 4485-4496.
30. Massagué, J. 1998. TGF-beta signal transduction. Annu. Rev. Biochem. 67: 753-791.
31. Moustakas, A. and D. Kardassis. 1998. Regulation of the human p21/WAF1/Cip1 promoter in hepatic cells by functional interactions between Sp1 and Smad family members. Proc. Natl. Acad. Sci 95: 6733-6738.
32. Nagase, T., G. Mizuguchi, N. Nomura, R. Ishizaki, Y. Ueno, and S. Ishii. 1990. Requirement of protein co-factor for the DNA-binding function of the human ski proto-oncogene product. Nucleic Acids Res. 18: 337-343.
33. Namciu, S., M.A. Lieberman, and E. Stavnezer. 1994. Induction of the c-ski proto-oncogene by phorbol ester correlates with induction of megakaryocyte differentiation. Oncogene 9: 1407-1416.
34. Nicol, R. and E. Stavnezer. 1998. Transcriptional repression by v-Ski and c-Ski mediated by a specific DNA binding site. J. Biol. Chem. 273: 3588-3597.
35. Nomura, N., S. Sasamoto, S. Ishii, T. Date, M. Matsui, and R. Ishizaki. 1989. Isolation of human cDNA clones of ski and the ski-related gene, sno. Nucleic Acids Res. 17: 5489-5500.
36. Nomura, T., M.M. Khan, S.C. Kaul, H.-D. Dona, R. Wadhwa, C. Colmenares, I. Kohno, and S. Ishii. 1999. Ski is a component of the histone deacetylase complex required for transcriptional repression by Mad and thyroid horomone receptor. Genes & Dev. 13: 412-423.
37. Pearson-White, S. 1993. Snol, a novel alternatively spliced isoform of the ski protooncogene homolog, sno. Nucleic Acids Res. 21:4632-4638.
38. Pouponnot, C., L. Jayaraman, and J. Massagué. 1998. Physical and functional interaction of SMADs and p300/CBP. J. Biol. Chem. 273: 22865-22868.
39. Roberts, A.B. and M.B. Sporn. 1990. The transforming growth factor-βs. In Peptide growth factors and their receptors (ed. A.B. Roberts and M.B. Sporn), pp. 421-472. Springer-Verlag, Heidelberg, Germany.
40. Shen, X., P.P. Hu, N.T. Liberati, M.B. Datto, J.P. Frederick, and X.F. Wang. 1998. TGF-beta-induced phosphorylation of Smad3 regulates its interaction with coactivator p300/ CREB-binding protein. Mol. Biol. Cell. 9: 3309-3319.
41. Shi, Y, A. Hata, R.S. Lo, J. Massagué, and N.P. Pavletich. 1997. A structural basis for mutational inactivation of the tumour suppressor Smad4. Nature 388: 87-93.
42. Shi, Y., Y.-F. Wang, L. Jayaraman, H. Yang, J. Massagué, and N.P. Pavletich. 1998. Crystal structure of a Smad MH1 domain bound to DNA: Insights on DNA binding in TGF-β signaling. Cell 94: 585-594.
43. Song, C.-Z., T.E. Siok, and T.D. Gelehrter. 1998. Smad4/DPC4 and Smad3 mediate transforming growth factor-β (TGF-β) signaling through direct binding to a novel TGF-responsive element in the human plasminogen activator inhibitor-1 promoter. J. Biol. Chem. 273: 29287-29290.
44. Stavnezer, E., D. Brodeur, and L.A. Brennan. 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.
45. Stroschein, S.L., W. Wang, and K. Luo. 1999. Cooperative binding of Smad proteins to two adjacent DNA elements in the plasminogen activator inhibitor-1 promoter mediates transforming growth factor β-induced Smad-dependent transcriptional activation. J. Biol. Chem. 274: 9431-9441.
46. Sutrave, P. and S.H. Hughes. 1989. Isolation and characterization of three distinct cDNAs for the chicken c-ski gene. Mol. Cell. Biol. 9: 4046-4051.
47. Sutrave, P., T.D. Copeland, S.D. Showalter, and S.H. Hughes. 1990a. Characterization of chicken c-ski oncogene products expressed by retrovirus vectors. Mol. Cell. Biol. 10:3137-3144.
48. Sutrave, P., A.M. Kelly, and S.H. Hughes. 1990b. ski can cause selective growth of skeletal muscle in transgenic mice. Genes & Dev. 4: 1462-1472.
49. Tarapore, P., C. Richmond, G. Zheng, S.B. Cohen, B. Kelder, J. Kopchick, U. Kruse, A.E. Sippel, C. Colmenares, and E. Stavnezer. 1997. DNA binding and transcriptional activation by the Ski oncoprotein mediated by interaction with NFI. Nucleic Acids Res. 25: 3895-3903.
50. Tokitou, F., T. Nomura, M.M. Khan, S.C. Kaul, R. Wadhwa, T. Yasukawa, I. Kohno, and S. Ishii. 1999. Viral ski inhibits retinoblastoma protein (Rb)-mediated transcriptional repression in a dominant negative fashion. J. Biol. Chem. 274: 4485-4488.
51. Topper, J.N., M.R. DiChiara, J.D. Brown, A.J. Williams, D. Falb, T. Collins, and M.A.J. Gimbrone. 1998. CREB binding protein is a required coactivator for smad-dependent, transforming growth factor beta transcriptional responses in endothelial cells. Proc. Natl. Acad. Sci. 95: 9506-9511.
52. Tsukazaki, T., T.A. Chiang, A.F. Davison, L. Attisano, and J.L. Wrana. 1998. SARA, a FYVE domain protein that recruits Smad2 to the TGFbeta receptor. Cell 95: 779-791.
53. Wong, C., E.M. Rougier-Chapman, J.P. Frederick, M.B. Datto, N.T. Liberati, J.M. Li, and X.F. Wang. 1999. Smad3-Smad4 and AP-1 complexes synergize in transcriptional activation of the c-Jun promoter by transforming growth factor beta. Mol. Cell. Biol. 19: 1821-1830.
54. Wotton, D., R.S. Lo, S. Lee, and J. Massagué. 1999. A Smad transcriptional corepressor. Cell 97: 29-39.
55. Yingling, J.M., M.B. Datto, C. Wong, J.P. Frederick, N.T. Liberati, and X.F. Wang. 1997. Tumor suppressor Smad4 is a transforming growth factor beta-inducible DNA binding protein. Mol. Cell Biol. 17: 7019-7028.
56. Zawel, L., J.L. Dai, P. Buckhaults, S. Zhou, K.W. Kinzler, B. Vogelstein, and S.E. Kern. 1998. Human Smad3 and Smad4 are sequence-specific transcription activators. Mol. Cell 1: 611-617.
57. Zhang, Y., X.-H. Feng, and R. Derynck. 1998. Smad3 and Smad4 cooperate with c-Jun/c-Fos to mediate TGF-β-induced transcription. Nature 394: 909-913.
58. Zheng, G., J. Teumer, C. Colmenares, C. Richmond, and E. Stavnezer. 1997. Identification of a core functional and structural domain of the v-Ski oncoprotein responsible for both transformation and myogenesis. Oncogene 15: 459-471.
59. Zhou, Q., D. Chen, E. Pierstorff, and K. Luo. 1998a. Transcription elongation factor P-TEFb mediates Tat activation of HIV-1 transcription at multiple stages. EMBO J. 17: 3681-3691.
60. Zhou, S., L. Zawel, C. Lengauer, K.W. Kinzler, and B. Vogelstein. 1998b. Characterization of human FAST-1, a TGF beta and activin signal transducer. Mol. Cell. 2: 121-127.