Oligomeric structure of type I and type II transforming growth factor β receptors: Homodimers form in the ER and persist at the plasma membrane

Journal of Cell Biology

Volumn 140, Issue 4, 1998, Pages 767-777

  Gilboa, Lilach ^a,b   Wells, Rebecca G ^b,c   Lodish, Harvey F ^b,d   Henis, Yoav I ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OLIGOMER; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; DIMERIZATION; ENDOPLASMIC RETICULUM; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE;

ACTIVIN RECEPTORS, TYPE I; ANIMALS; BINDING SITES; CELL LINE; CELL MEMBRANE; COS CELLS; DIMERIZATION; DITHIOTHREITOL; DNA, RECOMBINANT; ENDOPLASMIC RETICULUM; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOHISTOCHEMISTRY; LIGANDS; PRECIPITIN TESTS; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, CELL SURFACE; RECEPTORS, TRANSFORMING GROWTH FACTOR BETA;

ANIMALIA;

EID: 0032559594     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.140.4.767     Document Type: Article

References (45)

1. Attisano, L., and J.L. Wrana. 1996. Signal transduction by members of the transforming growth factor-β superfamily. Cytokine Growth Factor Rev. 7:327-339.
2. Attisano, L., J.L. Wrana, F. Lopez-Casillas, and J. Massague. 1994. TGF-β receptors and actions. Biochim. Biophys. Acta. 1222:71-80.
3. Bassing, C.H., J.M. Yingling, D.J. Howe, T. Wang, W.W. He, M.L. Gustafson, P. Shah, P.K. Donahoe, and X.-F. Wang. 1994. A transforming growth factor β type I receptor that signals to activate gene expression. Science. 263:87-89.
4. Cheifetz, S., and J. Massague. 1991. Isoform-specific transforming growth factor-β binding proteins with membrane attachments sensitive to phosphatidylinositol-specific phospholipase C. J. Biol. Chem. 266:20767-20772.
5. Chen, H., D.D. Hughes, T.A. Chan, J.W. Sedat, and D.A. Agard. 1996. IVE (Image Visualization Environment): a software platform for all three-dimensional microscopy applications. J. Struct. Biol. 116:56-60.
6. Chen, R.-H., and R. Derynck. 1994. Homomeric interactions between type II transforming growth factor-β receptors. J. Biol. Chem. 269:22868-22874.
7. Chen, R.-H., H.L. Moses, E.M. Maruoka, R. Derynck, and M. Kawabata. 1995. Phosphorylation-dependent interaction of the cytoplasmic domains of the type I and type II transforming growth factor-β receptors. J. Biol. Chem. 270:12235-12241.
8. Evan, G.I., G.K. Lewis, G. Ramsay, and J.M. Bishop. 1985. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5:3610-3616.
9. Franzen, P., P. ten Dijke, H. Ichijo, H. Yamashita, P. Schulz, C.H. Heldin, and K. Miyazono. 1993. Cloning of a TGFβ type I receptor that forms a heteromeric complex with the TGFβ type II receptor. Cell. 75:681-692.
10. Harlow, E., and D. Lane. 1988. Antibodies: A Laboratory Manual. Cold Spring Harbor Press, Cold Spring Harbor, NY, 726 pp.
11. Henis, Y.I., O. Gutman, and A. Loyter. 1985. Sendai virus envelope glycoproteins become laterally mobile on the surface of human erythrocytes following fusion. Exp. Cell Res. 160:514-526.
12. Henis, Y.I., A. Moustakas, H.Y. Lin, and H.F. Lodish. 1994. The types II and III transforming growth factor-β receptors form homo-oligomers. J. Cell Biol. 126:139-154.
13. Inagaki, M., A. Moustakas, H.Y. Lin, H.F. Lodish, and B.I. Carr. 1993. Growth inhibition by transforming growth factor β (TGF-β) receptor type I is restored in TGF-β-resistant cells after expression of TGF-β receptor type II cDNA. Proc. Natl. Acad Sci. USA. 90:5359-5363.
14. Kam, Z., H. Chen, J.W. Sedat, and D.A. Agard. 1992. Analysis of three-dimensional image data: display and feature tracking. In Electron Tomography: Three-dimensional Imaging with the Transmission Electron Microscope. J. Frank, editor. Plenum Press, New York. 237-256.
15. Kam, Z., M.O. Jones, H. Chen, D.A. Agard, and J.W. Sedat. 1993. Design and construction of an optimal illumination system for quantitative wide-field multi-dimensional microscopy. Bioimaging. 1:71-81.
16. Kolodziej, P.A., and R.A. Young. 1991. Epitope tagging and protein surveillance. Methods Enzymol. 194:508-519.
17. Kunkel, T.A., J.D. Roberts, and R.A. Zakour. 1987. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 154:367-382.
18. 2 fragments from monoclonal mouse IgG1 suitable for use in radioimaging. J. Immunol. Methods. 110:229-236.
19. Laiho, M., P.M. Weis, F.T. Boyd, R.A. Ignotz, and J. Massague. 1991. Responsiveness to transforming growth factor-β restored by complementation between cells defective in TGF-β receptors I and II. J. Biol. Chem. 266:9108-9112.
20. Letourneur, O., J.F. Goetschy, M. Horisberger, and M.G. Grutier. 1996. Ligand-induced dimerization of the extracellular domain of the TGF-β receptor type II. Biochem. Biophys. Res. Commun. 224:709-716.
21. Lin, H.Y., and H.F. Lodish. 1993. Receptors for the TGF-β superfamily: multiple polypeptides and serine/threonine kinases. Trends Cell Biol. 3:14-19.
22. Lin, H.Y., and A. Moustakas. 1994. TGF-β receptors: structure and function. Cell. Mol. Biol. 40:337-349.
23. Lin, H.Y., X.-F. Wang, E. Ng-Eaton, R.A. Weinberg, and H.F. Lodish. 1992. Expression cloning of the TGF-β type II receptor, a functional transmembrane serine/threonine kinase. Cell. 68:775-785.
24. Lin, H.Y., A. Moustakas, P. Knaus, R.G. Wells, Y.I. Henis, and H.F. Lodish. 1995. The soluble exoplasmic domain of the type II transforming growth factor (TGF)-β receptor. A heterogeneously glycosylated protein with high affinity and selectivity for TGF-β ligands. J. Biol. Chem. 270: 2747-2754.
25. Lopez-Casillas, F., S. Cheifetz, J. Doodey, J.L. Andres, W.S. Lane, and J. Massague. 1991. Structure and expression of the membrane proteoglycan betaglycan, a component of the TGF-β receptor system. Cell. 67:785-795.
26. Lopez-Casillas, F., J.L. Wrana, and J. Massague. 1993. Betaglycan presents ligand to the TGF-β signaling receptor. Cell. 73:1435-1444.
27. Luo, K., and H.F. Lodish. 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 (Eur. Mol. Biol. Organ.) J. 15:4485-4496.
28. Luo, K., and H.F. Lodish. 1997. Positive and negative regulation of type II TGF-β receptor signal transduction by autophosphorylation on multiple serine residues. EMBO (Eur. Mol. Biol. Organ.) J. 16:1970-1981.
29. Massague, J. 1990. The transforming growth factor-β family. Annu. Rev. Cell Biol. 6:597-641.
30. Massague, J. 1992. Receptors for the TGF-β family. Cell. 69:1067-1070.
31. Massague, J. 1996. TGFβ signaling: receptors, transducers, and Mad proteins. Cell. 85:947-950.
32. Massague, J., and F. Weis-Garcia. 1996. Serine/threonine kinase receptors: mediators of transforming growth factor β family signals. Cancer Surv. 27:41-64.
33. Massague, J., L. Attisano, and J.L. Wrana. 1994. The TGF-β family and its composite receptors. Trends Cell Biol. 4:172-178.
34. Mitchell, E.J., K. Lee, and M.D. O'Connor-McCourt. 1992. Characterization of transforming growth factor-β (TGF-β) receptors on BeWo choriocarcinoma cells including the identification of a novel 38-kDa TGF-β binding glycoprotein. Mol. Biol. Cell. 3:1295-1307.
35. Moses, H.L., E.Y. Yang, and J.A. Pietenpol. 1990. TGF-β stimulation and inhibition of cell proliferation: new mechanistic insights. Cell. 63:245-247.
36. Moustakas, A., H.Y. Lin, Y.I. Henis, J. Plamondon, M.D. O'Connor McCourt, and H.F. Lodish. 1993. The transforming growth factor β receptors types I, II, and III form hetero-oligomeric complexes in the presence of ligand. J. Biol. Chem. 268:22215-22218.
37. Roberts, A.B., and M.B. Sporn. 1990. The transforming growth factor-betas. In Peptide Growth Factors and Their Receptors. M.B. Sporn and A.B. Roberts, editors. Springer-Verlag, Heidelberg. 419-472.
38. Seed, B., and A. Aruffo. 1987. Molecular cloning of the CD2 antigen, the T-cell erythrocyte receptor, by a rapid immunoselection procedure. Proc. Natl. Acad. Sci. USA. 84:3365-3369.
39. Wang, X.-F., H.Y. Lin, E. Ng-Eaton, J. Downward, H.F. Lodish, and R.A. Weinberg. 1991. Expression cloning and characterization of the TGF-β type III receptor. Cell. 67:797-805.
40. Weis-Garcia, F., and J. Massague. 1996. Complementation between kinase-defective and activation-defective TGF-β receptors reveals a novel form of receptor cooperativity essential for signaling. EMBO (Eur. Mol. Biol. Organ.) J. 15:276-289.
41. Wells, R.G., H. Yankelev, H.Y. Lin, and H.F. Lodish. 1997. Biosynthesis of the type I and type II TGF-β receptors. Implications for complex formation. J. Biol. Chem. 272:11444-11451.
42. Wilson, I.A., H.L. Niman, R.A. Houghten, A.R. Cherenson, M.L. Connolly, and R.A. Lerner. 1984. The structure of an antigenic determinant in a protein. Cell. 37:767-778.
43. Wrana, J.L., L. Attisano, J. Carcamo, A. Zentella, J. Doodey, M. Laiho, X.-F. Wang, and J. Massague. 1992. TGFβ signals through a heteromeric protein kinase receptor complex. Cell. 71:1003-1014.
44. Wrana, J.L., L. Attisano, R. Wieser, F. Ventura, and J. Massague. 1994. Mechanism of activation of the TGF-β receptor. Nature. 370:341-347.
45. Zhang, Y., X. Feng, R. We, and R. Derynck. 1996. Receptor-associated Mad homologues synergize as effectors of the TGF-β response. Nature. 383:168-172.