Interaction of the Ski oncoprotein with Smad3 regulates TGF-β signaling

Molecular Cell

Volumn 4, Issue 4, 1999, Pages 499-509

  Sun, Yin ^a   Liu, Xuedong ^a   Eaton, Elinor Ng ^a   Lane, William S ^c   Lodish, Harvey F ^a,b   Weinberg, Robert A ^a,b  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c HARVARD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; ONCOPROTEIN; PROTEIN DERIVATIVE; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; GROWTH INHIBITION; MINK; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; PROTO ONCOGENE; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANIMALIA; MUSTELA VISON;

EID: 0033213606     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1097-2765(00)80201-4     Document Type: Article

References (50)

1. Alexandrow, M.G., Kawabata, M., Aakre, M., and Moses, H.L. (1995). Overexpression of the c-Myc oncoprotein blocks the growth-inhibitory response but is required for the mitogenic effects of transforming growth factor beta 1. Proc. Natl. Acad. Sci. USA 92, 3239-3243.
2. Boyer, P.L., Colmenares, C., Stavnezer, E., and Hughes, S.H. (1993). Sequence and biological activity of chicken snoN cDna clones. Oncogene 8, 457-466.
3. Carcamo, J., Zentella, A., and Massague, J. (1995). Disruption of transforming growth factor beta signaling by a mutation. Mol. Cell. Biol. 15, 1573-1581.
4. Chittum, H.S., Lane, W.S., Carlson, B.A., Roller, P.P., Lung, F.D., Lee, B.J., and Hatfield, D.L. (1998). Rabbit beta-globin is extended beyond its UGA stop codon by multiple suppressions and translational reading gaps. Biochemistry 37, 10866-10870.
5. Colmenares, C., and Stavnezer, E. (1989). The ski oncogene induces muscle differentiation in quail embryo cells. Cell 59, 293-303.
6. Datto, M.B., Frederick, J.P., Pan, L., Borton, A.J., Zhuang, Y., and Wang, X.F. (1999). Targeted disruption of smad3 reveals an essential role in transforming growth factor beta-mediated signal transduction. Mol. Cell. Biol. 19, 2495-2504.
7. Eng, J.K., McCormick, A.L., and Yates, J.R., III (1994). An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom. 5, 976-989.
8. Engert, J.C., Servaes, S., Sutrave, P., Hughes, S.H., and Rosenthal, N. (1995). Activation of a muscle-specific enhancer by the ski proto-oncogene. Nucleic Acids Res. 23, 2988-2994.
9. Eppert, K., Scherer, S.W., Ozcelik, H., Pirone, R., Hoodless, P., Kim, H., Tsui, L.C., Bapat, B., Gallinger, S., Andrulis, I.L., et al. (1996). MADR2 maps to 18q21 and encodes a TGFβ-regulated MAD-related protein that is functionally mutated in colorectal carcinoma. Cell 86, 543-552.
10. Franzen, P., ten Dijke, P., Ichijo, H., Yamashita, H., Schulz, P., Heldin, C.H., and Miyazono, K. (1993). Cloning of a TGF beta type I receptor that forms a heteromeric complex. Cell 75, 681-692.
11. Guan, K.L., and Dixon, J.E. (1991). Eukaryotic proteins expressed in Escherichia coli: An improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal. Biochem. 192, 262-267.
12. Hahn, S.A., Schutte, M., Hoque, A.T., Moskaluk, C.A., da Costa, L.T., Rozenblum, E., Weinstein, C.L., Fischer, A., Yeo, C.J., Hruban, R.H., and Kern, S.E. (1996). DPC4, a candidate tumor suppressor gene at human chromosome 18q21.1. Science 271, 350-353.
13. Hannon, G.J., and Beach, D. (1994). P15INK4B is a potential effector of TGF-beta-induced cell cycle arrest. Nature 371, 257-261.
14. Heldin, C.H., Miyazono, K., and ten Dijke, P. (1997). TGF-beta signaling from cell membrane to nucleus through SMAD proteins. Nature 390, 465-471
15. Hua, X., Liu, X., Ansari, D.O., and Lodish, H.F. (1998). Synergistic cooperation of TFE3 and smad proteins in TGF-beta-induced transcription of the plasminogen activator inhibitor-1 gene. Genes Dev. 12, 3084-3095.
16. Keeton, M.R., Curriden, S.A., van Zonneveld, A.J., and Loskutoff, D.J. (1991). Identification of regulatory sequences in the type 1 plasminogen activator inhibitor gene responsive to transforming growth factor beta. J. Biol. Chem. 266, 23048-23052.
17. Kimchi, A., Wang, X.F., Weinberg, R.A., Cheifetz, S., and Massague, J. (1988). Absence of TGF-beta receptors and growth inhibitory responses in retinoblastoma cells. Science 240, 196-199.
18. Kurokawa, M., Mitani, K., Irie, K., Matsuyama, T., Takahashi, T., Chiba, S., Yazaki, Y., Matsumoto, K., and Hirai, H. (1998). The oncoprotein Evi-1 represses TGF-beta signaling by inhibiting smad3. Nature 394, 92-96.
19. Lagna, G., Hata, A., Hemmati-Brivanlou, A., and Massague, J. (1996). Partnership between DPC4 and SMAD proteins in TGF-beta signaling pathways. Nature 383, 832-836.
20. Laiho, M., Weis, F.M., Boyd, F.T., Ignotz, R.A., and Massague, J. (1991). Responsiveness to transforming growth factor-beta (TGF-beta) restored by genetic complementation between cells defective in TGF-beta receptors I and II. J. Biol. Chem. 266, 9108-9112.
21. Lin, H.Y., Wang, X.F., Ng-Eaton, E., Weinberg, R.A., and Lodish, H.F. (1992). Expression cloning of the TGF-beta type II receptor, a functional transmembrane serine/threonine kinase. Cell 68, 775-785.
22. Liu, X., Sun, Y., Constantinescu, S.N., Karam, E., Weinberg, R.A., and Lodish, H.F. (1997). Transforming growth factor beta-induced phosphorylation of smad3 is required for growth inhibition and transcriptional induction in epithelial cells. Proc. Natl. Acad. Sci. USA 94, 10669-10674.
23. Macias-Silva, M., Abdollah, S., Hoodless, P.A., Pirone, R., Attisano, L., and Wrana, J.L. (1996). MADR2 is a substrate of the TGFbeta receptor and its phosphorylation is required for nuclear accumulation and signaling. Cell 87, 1215-1224.
24. Markowitz, S., Wang, J., Myeroff, L., Parsons, R., Sun, L., Lutterbaugh, J., Fan, R.S., Zborowska, E., Kinzler, K.W., Vogelstein, B., et al. (1995). Inactivation of the type II TGF-beta receptor in colon cancer cells with microsatellite instability. Science 268, 1336-1338.
25. Massague, J. (1998). TGF-beta signal transduction. Annu. Rev. BioChem. 67, 753-791.
26. Massague, J., and Weis-Garcia, F. (1996). Serine/threonine kinase receptors: Mediators of transforming growth factor beta family signals. Cancer Surv. 27, 41-64.
27. Morgenstern, J.P., and Land, H. (1990). Advanced mammalian gene transfer: High titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18, 3587-3596.
28. Nagase, T., Mizuguchi, G., Nomura, N., Ishizaki, R., Ueno, Y., and Ishii, S. (1990). Requirement of protein co-factor for the DNA-binding function of the human ski proto-oncogene product. Nucleic Acids Res. 18, 337-343.
29. Nakao, A., Imamura, T., Souchelnytskyi, S., Kawabata, M., Ishisaki, A., Oeda, E., Tamaki, K., Hanai, J., Heldin, C.H., Miyazono, K., and ten Dijke, P. (1997). TGF-beta receptor-mediated signaling through smad2, smad3 and smad4. EMBO J. 16, 5353-5362.
30. Nicol, R., and Stavnezer, E. (1998). Transcriptional repression by v-ski and c-ski mediated by a specific DNA binding site. J. Biol. Chem. 273, 3588-3597.
31. 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 Acids Res. 17, 5489-5500.
32. 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.
33. Pear, W.S., Nolan, G.P., Scott, M.L., and Baltimore, D. (1993). Production of high-titer helper-free retroviruses by transient transfection. Proc. Natl. Acad. Sci. USA 90, 8392-8396.
34. Pietenpol, J.A., Stein, R.W., Moran, E., Yaciuk, P., Schlegel, R., Lyons, R.M., Pittelkow, M.R., Munger, K., Howley, P.M., and Moses, H.L. (1990). TGF-beta 1 inhibition of c-myc transcription and growth in keratinocytes is abrogated by viral transforming proteins with pRB binding domains. Cell 61, 777-785.
35. Reynisdottir, I., Polyak, K., Iavarone, A., and Massague, J. (1995). Kip/Cip and Ink4 Cdk inhibitors cooperate to induce cell cycle arrest in response to TGF-beta. Genes Dev. 9, 1831-1845.
36. Sambrook, J., Fritsch, E., and Maniatis, T. (1989). Molecular Cloning (Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press).
37. Stavnezer, E., Gerhard, D.S., Binari, R.C., and Balazs, I. (1981). Generation of transforming viruses in cultures of chicken fibroblasts infected with an avian leukosis virus. J. Virol. 39, 920-934.
38. Tarapore, P., Richmond, C., Zheng, G., Cohen, S.B., Kelder, B., Kopchick, J., Kruse, U., Sippel, A.E., Colmenares, C., and Stavnezer, E. (1997). DNA binding and transcriptional activation by the ski oncoprotein mediated by interaction with NFI. Nucleic Acids Res. 25, 3895-3903.
39. Tokitou, F., Nomura, T., Khan, M.M., Kaul, S.C., Wadhwa, R., Yasukawa, T., Kohno, I., and Ishii, S. (1999). Viral ski inhibits retinoblastoma protein (Rb)-mediated transcriptional repression in a dominant negative fashion. J. Biol. Chem. 274, 4485-4488.
40. Westerhausen, D.R., Jr., Hopkins, W.E., and Billadello, J.J. (1991). Multiple transforming growth factor-beta-inducible elements regulate expression of the plasminogen activator inhibitor type-1 gene in Hep G2 cells. J. Biol. Chem. 266, 1092-1100.
41. Wieser, R., Wrana, J.L., and Massague, J. (1995). GS domain mutations that constitutively activate T beta R-I, the downstream signaling component in the TGF-beta receptor complex. EMBO J. 14, 2199-2208.
42. Wotton, D., Lo, R.S., Lee, S., and Massague, J. (1999). A smad transcriptional corepressor. Cell 97, 29-39.
43. Wrana, J.L., Attisano, L., Carcamo, J., Zentella, A., Doody, J., Laiho, M., Wang, X.F., and Massague, J. (1992). TGF beta signals through a heteromeric protein kinase receptor complex. Cell 71, 1003-1014.
44. Wrana, J.L., Attisano, L., Wieser, R., Ventura, F., and Massague, J. (1994). Mechanism of activation of the TGF-beta receptor. Nature 370, 341-347.
45. Yamaguchi, A. (1995). Regulation of differentiation pathway of skeletal mesenchymal cells in cell lines by transforming growth factor-beta superfamily. Semin. Cell Biol. 6, 165-173.
46. Yamaguchi, K., Shirakabe, K., Shibuya, H., Irie, K., Oishi, I., Ueno, N., Taniguchi, T., Nishida, E., and Matsumoto, K. (1995). Identification of a member of the MAPKKK family as a potential mediator of TGF-beta signal transduction. Science 270, 2008-2011.
47. Yingling, J.M., Datto, M.B., Wong, C., Frederick, J.P., Liberati, N.T., and Wang, X.F. (1997). Tumor suppressor smad4 is a transforming growth factor beta-inducible DNA binding protein. Mol. Cell. Biol. 17, 7019-7028.
48. Zawel, L., Dai, J.L., Buckhaults, P., Zhou, S., Kinzler, K.W., Vogelstein, B., and Kern, S.E. (1998). Human smad3 and smad4 are sequence-specific transcription activators. Mol. Cell 1, 611-617.
49. Zhu, Y., Richardson, J.A., Parada, L.F., and Graff, J.M. (1998). Smad3 mutant mice develop metastatic colorectal cancer. Cell 94, 703-714.
50. Zhang, Y., and Derynck, R. (1999). Regulation of smad signaling by protein associations and signaling crosstalk. Trends Cell. Biol. 9, 274-279.