A kinase subdomain of transforming growth factor-β (TGF-β) type I receptor determines the TGF-β intracellular signaling specificity

EMBO Journal

Volumn 16, Issue 13, 1997, Pages 3912-3923

  Feng, Xin Hua ^a   Derynck, Rik ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Kinase; Signaling; Specificity; TGF ; Type I receptor

Indexed keywords

TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANIMAL CELL; ARTICLE; CELL COMMUNICATION; CELL GROWTH; CRYSTAL STRUCTURE; EPITHELIUM CELL; GENETIC TRANSFECTION; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION;

ACTIVIN RECEPTORS, TYPE I; AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CELL MEMBRANE; COS CELLS; CYTOPLASM; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; PROTEIN-SERINE-THREONINE KINASES; RABBITS; RECEPTORS, GROWTH FACTOR; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA; RECOMBINANT FUSION PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSFORMING GROWTH FACTOR BETA;

EID: 0030926005     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.13.3912     Document Type: Article

References (55)

1. Attisano, L., Carcamo, J., Ventura, F., Weis, F.M., Massagué, J. and Wrana, J.L. (1993) Identification of human activin and TGFβ type I receptors that form heteromeric kinase complexes with type II receptors. Cell, 75, 671-680.
2. Bassing, C.H., Howe, D.J., Segarini, P.R., Donahoe, P.K. and Wang, X.-F. (1994a) A single heteromeric receptor complex is sufficient to mediate biological effects of transforming growth factor-β ligands. J. Biol. Chem., 269, 14861-14864.
3. Bassing, C.H., Yingling, J.M., Howe, D.J., Wang, T., He, W.W., Gustafson, M.L., Shah, P., Donahoe, P.K. and Wang, X.-F. (1994b) A transforming growth factor β type I receptor that signals to activate gene expression. Science, 263, 87-89.
4. Brand, T. and Schneider, M. (1995) Inactive type-II and type I receptors for TGF-β are dominant inhibitors of TGF-β-dependent transcription. J. Biol. Chem., 270, 8274-8284.
5. Cárcamo, J., Weis, F.M., Ventura, F., Wieser, R., Wrana, J.L., Attisano, L. and Massagué, J. (1994) Type I receptors specify growth-inhibitory and transcriptional responses to transforming growth factor β and activin. Mol. Cell. Biol., 14, 3810-3821.
6. Charng, M.-J., Kinnunen, P., Hawker, J., Brand, T. and Schneider, M. (1996) FKBP-12 recognition is dispensable for signal generation by type I transforming growth factor-β receptors. J. Biol. Chem., 271, 22941-22944.
7. Chen, F. and Weinberg, R.A. (1995) Biochemical evidence for the autophosphorylation and transphosphorylation of transforming growth factor β receptor kinases. Proc. Natl Acad. Sci. USA, 92, 1565-1569.
8. Chen, R.-H. and Derynck, R. (1994) Homomeric interactions between the type II TGF-β receptors. J. Biol. Chem., 269, 22868-22874.
9. Chen, R.-H., Moses, H.L., Maruoka, E.M., Derynck, R. and Kawabata, M. (1995) Phosphorylation-dependent interaction of the cytoplasmic domains of the type I and type II TGF-β receptors. J. Biol. Chem., 270, 12235-12241.
10. Cox, S. and Taylor, S.S. (1994) Holoenzyme interaction sites in the cAMP-dependent protein kinase. Histidine 87 in the catalytic subunit complements serine 99 in the type I regulatory subunit. J. Biol. Chem., 269, 22614-22622.
11. De Bondt, H., Rosenblatt, J., Jancarik, J., Jones, H., Morgan, D. and Kim, S.-H. (1993) Crystal structure of cyclin-dependent kinase 2. Nature, 363, 595-602.
12. Derynck, R. (1994a) Transforming growth factor-β. In Thomson, A.W. (ed.), The Cytokine Handbook. Academic Press, San Diego, CA, pp. 319-342.
13. Derynck, R. (1994b) TGF-β receptor-mediated signaling. Trends Biochem. Sci., 19, 548-553.
14. Derynck, R. and Zhang, Y. (1996) The Mad way to do it. Curr. Biol., 6, 1226-1229.
15. Ducommun, B., Brambilla, P., Félix, M.-A., Franza, J., Karsenti, E. and Draetta, G. (1991) cdc2 phosphorylation is required for its interaction with cyclin. EMBO J., 10, 3311-3319.
16. Ebner, R., Chen, R.-H., Lawler, S., Zioncheck, T. and Derynck, R. (1993a) Determination of type I receptor specificity by the type II receptors for TGF-β or activin. Science, 262, 900-902.
17. Ebner, R., Chen, R.-H., Shum, L., Lawler, S., Zioncheck, T.F., Lee, A., Lopez, A.R. and Derynck, R. (1993b) Cloning of a type I TGF-β receptor and its effect on TGF-β binding to the type II receptor. Science, 260, 1344-1348.
18. Feng, X.-H. and Derynck, R. (1996) Ligand-independent activation of transforming growth factor (TGF)-β signaling pathways by heteromeric cytoplasmic domains of TGF-β receptors. J. Biol. Chem., 271, 13123-13129.
19. Feng, X.-H., Filvaroff, E.H. and Derynck, R. (1995) Transforming growth factor-β (TGF-β)-induced down-regulation of cyclin A expression requires a functional TGF-β receptor complex. Characterization of chimeric and truncated type I and type II receptors. J. Biol. Chem., 270, 24237-24245.
20. Franzén, P., ten Dijke, P. Ichijo, H., Yamashita, H., Schulz, P., Heldin, C.-H. and Miyazono, K. (1993) Cloning of a TGFβ type I receptor that forms a heteromeric complex with the TGFβ type II receptor. Cell, 75, 681-692.
21. Gazit, D., Ebner, R., Kahn, A. and Derynck, R. (1993) Modulation of expression and cell surface binding of members of the transforming growth factor-β superfamily during retinoic acid-induced osteoblastic differentiation of multipotential messenchymal cells. Mol. Endocrinol., 7, 189-198.
22. Hanks, S. and Hunter, T. (1995) The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J., 9, 576-596.
23. Hanks, S., Quinn, A.M. and Hunter, T. (1988) The protein kinase family: conserved features and deduced phylogeny of the catalytic domains. Science, 241, 42-52.
24. Henis, Y.I., Moustakas, A., Lin, H.Y. and Lodish, H.F. (1994) The type II and III transforming growth factor-β receptors form homo-oligomers. J. Cell Biol., 126, 139-154.
25. Hubbard, S., Wei, L., Ellis, L. and Hendrickson, W. (1994) Crystal structure of the tyrosine kinase domain of the human insulin receptor. Nature, 372, 746-754.
26. Keeton, M.R., Curriden, S.A., van Zonneveld, A. and Loskutoff, D.J. (1991) Identification of regulatory sequences in the type I plasminogen activator inhibitor gene responsive to transforming growth factor beta. J. Biol. Chem., 266, 23048-23052.
27. Kingsley, D.M. (1994) The TGF-β superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev., 8, 133-146.
28. Knighton, D., Zheng, J., ten Eyck, L., Ashford, V., Xuong, N.-H., Taylor, S. and Sowadski, J. (1991) Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science, 253, 407-414.
29. Lagna, G., Hata, A., Hemmati-Brivanlou, A. and Massagué, J. (1996) Partnership between DPC4 and SMAD proteins in TGF-β signalling pathways. Nature, 383, 832-836.
30. Laiho, M., Weis, F.M. and Massagué, J. (1990) Concomitant loss of transforming growth factor (TGF)-β receptor types I and II in TGF-β-resistant cell mutants implicates both receptor types in signal transduction. J. Biol. Chem., 265, 18518-18524.
31. Laiho, M., Weis, F.M., Boyd, F.T., Ignotz, R.A. and Massagué, J. (1991) Responsiveness to transforming growth factor-β (TGF-β) restored by genetic complementation between cells defective in TGF-β receptors I and II. J. Biol. Chem., 266, 9108-9112.
32. Liu, F., Hata, A., Baker, J.C., Doody, J. Cárcamo, J., Harland, R.M. and Massagué, J. (1996) A human Mad protein acting as a BMP-regulated transcriptional activator. Nature, 381, 620-623.
33. Luo, K. and Lodish, H.F. (1996) Signaling by chimeric erythropoietin-TGF-β receptors: homodimerization of the cytoplasmic domain of the type I TGF-β receptor and heterodimerization with the type II receptor are both required for intracellular signal transduction. EMBO J., 15, 4485-4496.
34. Macias-Silva, M., Abdollah, S., Hoodless, P., Pirone, R., Attisano, L. and Wrana, J.L. (1996) MADR-2 is a substrate of the TGF-β receptor and its phosphorylation is required for nuclear accumulation and signaling. Cell, 87, 1215-1224.
35. Massagué, J. (1996) TGFβ signaling: receptors, transducers, and Mad proteins. Cell, 85, 947-950.
36. 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.
37. Okadome, T., Yamashita, H., Franzen, P., Moren, A., Heldin, C.-H. and Miyazono, K. (1994) Distinct roles of the intracellular domains of transforming growth factor-β type I and type II receptors in signal transduction. J. Biol. Chem., 269, 30753-30756.
38. Okadome, T., Oeda, E., Saitoh, M., Ichijo, H., Moses, H.L., Miyazono, K. and Kawabata, M. (1996) Characterization of the interaction of FKBP12 with the transforming growth factor-β type I receptor in vivo. J. Biol. Chem., 271, 21687-21690.
39. Rodriguez, C., Chen, F., Weinberg, R.A. and Lodish, H.F. (1995) Cooperative binding of transforming growth factor (TGF)-β2 to the types I and II TGF-β receptors. J. Biol. Chem., 270, 15919-15922.
40. Saitoh, M., Nishitoh, H., Amagasa, T., Miyazono, K., Takagi, M. and Ichijo, H. (1996) Identification of important regions in the cytoplasmic juxtamembrane domain of type I receptor that separate signaling pathways of transforming growth factor-β. J. Biol. Chem., 271, 2769-2775.
41. Schlessinger, J. and Ullrich, A. (1992) Growth factor signaling by receptor tyrosine kinases. Neuron, 9, 383-391.
42. Sekelsky, J., Newfeld, S., Raftery, L., Chartoff, E. and Gelbart, W.M. (1995) Genetic characterization and cloning of mothers against dpp, a gene required for decapentaplegic function in Drosophila melanogaster. Genetics, 139, 1347-1358
43. Souchelnytskyi, S., ten Dijke, P. Miyazono, K. and Heldin, C.-H. (1996) Phosphorylation of Ser165 in TGF-β type I receptor modulates TGF-β1-induced cellular responses. EMBO J., 15, 6231-6240.
44. ten Dijke, P., Yamashita, H., Ichijo, H., Franzén, P., Laiho, M., Miyazono, K. and Heldin, C.-H. (1994a) Characterization of type I receptors for transforming growth factor-β and activin. Science, 264, 101-104.
45. ten Dijke, P., Yamashita, H., Sammpath, T.K., Reddi, A.H., Estevez, M., Riddle, D.L., Ichojo, H., Heldin, C.-H. and Miyazono, K. (1994b) Identification of type I receptors for osteogenic protein-1 and bone morphogenetic protein-4. J. Biol. Chem., 269, 16985-16988.
46. Ventura, F., Doody, J., Liu, F., Wrana, J.L. and Massagué, J. (1994) Reconstitution and transphosphorylation of TGF-β receptor complexes. EMBO J., 13, 5581-5589.
47. Wang, T., Li, B.-Y., Danielson, P., Shah, P., Rockwell, S., Lechleider, R., Martin, J., Manganaro, T. and Donahoe, P. (1996) The immunophilin FKBP12 functions as a common inhibitor of the TGF-β family type I receptors. Cell, 86, 435-444.
48. Weis-Garcia, F. and Massagué, J. (1996) Complementation between kinase-defective and activation-defective TGF-β receptors reveals a novel form of receptor cpoperativity essential for signaling. EMBO J., 15, 276-289.
49. Wieser, R., Wrana, J.L. and Massagué, J. (1995) GS domain mutations that constitutively activate TβRI, the downstream signaling component in the TGF-β receptor complex. EMBO J., 14, 2199-2208.
50. Wrana, J.L., Attisano, L., Cárcamo, J., Zentella, A., Doody, J., Laiho, M., Wang, X.F. and Massagué, J. (1992) TGF β signals through a heteromeric protein kinase receptor complex. Cell, 71, 1003-1014.
51. Wrana, J.L., Attisano, L., Wieser, R., Ventura, F. and Massagué, J. (1994) Mechanism of activation of the TGF-β receptor. Nature, 370, 341-347.
52. Wu, R.Y., Zhang, Y., Feng, X.-H. and Derynck, R. (1997) Homomeric and heteromeric interactions are required for signaling activity and functional cooperativity of Smad3 and 4. Mol. Cell. Biol., 17, 2521-2528.
53. Yamashita, H., ten Dijke, P., Franzen, P., Miyazono, K. and Heldin, C.-H. (1994) Formation of hetero-oligomeric complexes of type I and type II receptors for transforming growth factor-β. J. Biol. Chem., 269, 20172-20178.
54. Zhang, Y., Feng, X.-H., Wu, R.-Y. and Derynck, R. (1996) Receptor-associated Mad homologues synergize as effectors of the TGF-β response. Nature, 383, 168-172.
55. Zhang, Y., Musci, T. and Derynck, R. (1997) The tumor suppressor Smad4/ DPC4 as a central mediator of Smad function. Curr. Biol., 7, 270-276.