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Genes & Dev. 13 (17): 2196-2206

Copyright © 1999 by Cold Spring Harbor Laboratory Press.

Vol. 13, No. 17, pp. 2196-2206, September 1, 1999

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

Kunxin Luo,1,2,4 Shannon L. Stroschein,1,2 Wei Wang,1,3 Dan Chen,2 Eric Martens,2 Sharleen Zhou,2 and Qiang Zhou2

1 Life Sciences Division, Lawrence Berkeley National Laboratory (LBNL), and 2  Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, California 94720 USA; 3 Department of Biology, University of Science and Technology of China, Hefei, Anhui, China

Smad proteins are critical signal transducers downstream of the receptors of the transforming growth factor-beta (TGFbeta ) superfamily. On phosphorylation and activation by the active TGFbeta receptor complex, Smad2 and Smad3 form hetero-oligomers with Smad4 and translocate into the nucleus, where they interact with different cellular partners, bind to DNA, regulate transcription of various downstream response genes, and cross-talk with other signaling pathways. Here we show that a nuclear oncoprotein, Ski, can interact directly with Smad2, Smad3, and Smad4 on a TGFbeta -responsive promoter element and repress their abilities to activate transcription through recruitment of the nuclear transcriptional corepressor N-CoR and possibly its associated histone deacetylase complex. Overexpression of Ski in a TGFbeta -responsive cell line renders it resistant to TGFbeta -induced growth inhibition and defective in activation of JunB expression. This ability to overcome TGFbeta -induced growth arrest may be responsible for the transforming activity of Ski in human and avian cancer cells. Our studies suggest a new paradigm for inactivation of the Smad proteins by an oncoprotein through transcriptional repression.

[Key Words: Ski; TGFbeta ; Smad proteins; growth inhibition; signal transduction; transcriptional activation]

GENES & DEVELOPMENT 13:2196-2206 © 1999 by Cold Spring Harbor Laboratory Press  ISSN 0890-9369/99 $5.00

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J. Biol. Chem. 279, 2666-2672
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CHIP Mediates Degradation of Smad Proteins and Potentially Regulates Smad-Induced Transcription.
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J. Biol. Chem. 278, 51673-51684
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Signal-dependent N-CoR Requirement for Repression by the Ski Oncoprotein.
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J. Biol. Chem. 278, 24858-24864
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The Ski-binding Protein C184M Negatively Regulates Tumor Growth Factor-{beta} Signaling by Sequestering the Smad Proteins in the Cytoplasm.
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Aging-related satellite cell differentiation defect occurs prematurely after Ski-induced muscle hypertrophy.
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Am J Physiol Cell Physiol 283, C1228-C1241
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J. Biol. Chem. 277, 28483-28490
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c-Jun Associates with the Oncoprotein Ski and Suppresses Smad2 Transcriptional Activity.
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J. Biol. Chem. 277, 29094-29100
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Phosphatase Inhibition Leads to Histone Deacetylases 1 and 2 Phosphorylation and Disruption of Corepressor Interactions.
S. C. Galasinski, K. A. Resing, J. A. Goodrich, and N. G. Ahn (2002)
J. Biol. Chem. 277, 19618-19626
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Three habits of highly effective signaling pathways: principles of transcriptional control by developmental cell signaling.
S. Barolo and J. W. Posakony (2002)
Genes & Dev. 16, 1167-1181
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Transforming growth factor {beta} signal transduction.
S. Dennler, M.-J. Goumans, and P. ten Dijke (2002)
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Factors Involved in the Regulation of Type I Collagen Gene Expression: Implication in Fibrosis.
A. K. Ghosh (2002)
Experimental Biology and Medicine 227, 301-314
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K. Jepsen and M. G. Rosenfeld (2002)
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   Abstract »    Full Text »    PDF »
SNIP1 Inhibits NF-kappa B Signaling by Competing for Its Binding to the C/H1 Domain of CBP/p300 Transcriptional Co-activators.
R. H. Kim, K. C. Flanders, S. B. Reffey, L. A. Anderson, C. S. Duckett, N. D. Perkins, and A. B. Roberts (2001)
J. Biol. Chem. 276, 46297-46304
   Abstract »    Full Text »    PDF »
TGF-beta inhibits muscle differentiation through functional repression of myogenic transcription factors by Smad3.
D. Liu, B. L. Black, and R. Derynck (2001)
Genes & Dev. 15, 2950-2966
   Abstract »    Full Text »    PDF »
Cytoplasmic Localization of the Oncogenic Protein Ski in Human Cutaneous Melanomas in Vivo: Functional Implications for Transforming Growth Factor {beta} Signaling.
J. A. Reed, E. Bales, W. Xu, N. A. Okan, D. Bandyopadhyay, and E. E. Medrano (2001)
Cancer Res. 61, 8074-8078
   Abstract »    Full Text »    PDF »
Smad3 recruits the anaphase-promoting complex for ubiquitination and degradation of SnoN.
S. L. Stroschein, S. Bonni, J. L. Wrana, and K. Luo (2001)
Genes & Dev. 15, 2822-2836
   Abstract »    Full Text »    PDF »
Synergistic Cooperation between Hypoxia and Transforming Growth Factor-{beta} Pathways on Human Vascular Endothelial Growth Factor Gene Expression.
T. Sanchez-Elsner, L. M. Botella, B. Velasco, A. Corbi, L. Attisano, and C. Bernabeu (2001)
J. Biol. Chem. 276, 38527-38535
   Abstract »    Full Text »    PDF »
The Smad Transcriptional Corepressor TGIF Recruits mSin3.
D. Wotton, P. S. Knoepfler, C. D. Laherty, R. N. Eisenman, and J. Massague (2001)
Cell Growth Differ. 12, 457-463
   Abstract »    Full Text »    PDF »
Regulation of myostatin activity and muscle growth.
S.-J. Lee and A. C. McPherron (2001)
PNAS 98, 9306-9311
   Abstract »    Full Text »    PDF »
The Smad3 Protein Is Involved in TGF-{beta} Inhibition of Class II Transactivator and Class II MHC Expression.
Y. Dong, L. Tang, J. J. Letterio, and E. N. Benveniste (2001)
J. Immunol. 167, 311-319
   Abstract »    Full Text »    PDF »
TGF-{beta}-induced repression of CBFA1 by Smad3 decreases cbfa1 and osteocalcin expression and inhibits osteoblast differentiation.
T. Alliston, L. Choy, P. Ducy, G. Karsenty, and R. Derynck (2001)
EMBO J. 20, 2254-2272
   Abstract »    Full Text »    PDF »
Human T-cell leukemia virus type I oncoprotein Tax represses Smad-dependent transforming growth factor {beta} signaling through interaction with CREB-binding protein/p300.
N. Mori, M. Morishita, T. Tsukazaki, C.-Z. Giam, A. Kumatori, Y. Tanaka, and N. Yamamoto (2001)
Blood 97, 2137-2144
   Abstract »    Full Text »    PDF »
Inactivation of menin, a Smad3-interacting protein, blocks transforming growth factor type {beta} signaling.
H. Kaji, L. Canaff, J.-J. Lebrun, D. Goltzman, and G. N. Hendy (2001)
PNAS 98, 3837-3842
   Abstract »    Full Text »    PDF »
Caveolin-1 Regulates Transforming Growth Factor (TGF)-beta /SMAD Signaling through an Interaction with the TGF-beta Type I Receptor.
B. Razani, X. L. Zhang, M. Bitzer, G. von Gersdorff, E. P. Bottinger, and M. P. Lisanti (2001)
J. Biol. Chem. 276, 6727-6738
   Abstract »    Full Text »    PDF »

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