Bone morphogenetic protein receptor complexes on the surface of live cells: A new oligomerization mode for serine/threonine kinase receptors

Molecular Biology of the Cell

Volumn 11, Issue 3, 2000, Pages 1023-1035

  Gilboa, Lilach ^b   Nohe, Anja ^a   Geissendörfer, Tanja ^a   Sebald, Walter ^a   Henis, Yoav I ^b   Knaus, Petra ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN RECEPTOR; CELL SURFACE RECEPTOR; PROTEIN SERINE THREONINE KINASE; RECEPTOR SUBTYPE; TRANSFORMING GROWTH FACTOR BETA RECEPTOR;

ANIMAL CELL; ARTICLE; CELL SURFACE; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; PROTEIN POLYMERIZATION; RECEPTOR BINDING; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0034021776     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.11.3.1023     Document Type: Article

References (57)

1. Ahrens, M., Ankenbauer, T., Schroder, D., Hollnagel, A., Mayor, H., and Gross, G. (1993). Expression of human bone morphogenetic proteins-2 or -4 in murine mesenchymal progenitor C3H10T1/2 cells induces differentiation into distinct mesenchymal cell lineages. DNA Cell Biol. 12, 871-880.
2. Anders, R.A., and Leof, E.B. (1996). Chimeric granulocyte/macrophage colony-stimulating factor/transforming growth factor-beta (TCP-beta) receptors define a model system for investigating the role of homomeric and heteromeric receptors in TGF-beta signaling. J. Biol. Chem. 277, 21758-21766.
3. Asahina, I., Sampath, T.K., and Hauschka, P.V. (1996). Human osteogenic protein-1 induces chondroblastic, osteoblastic, and/or adipocytic differentiation of clonal murine target cells. Exp. Cell Res. 222, 38-47.
4. Cheifetz, S., Bassols, A., Stanley, K., Ohta, M., Greenberger, J., and Massague, J. (1988). Heterodimeric transforming growth factor beta. Biological properties and interaction with three types of cell surface receptors. J. Biol. Chem. 263, 10783-10789.
5. Chen, D., Ji, X., Harris, M.A., Feng, J.Q., Karsenty, G., Celeste, A.J., Rosen, V., Mundy, G.R., and Harris, S.E. (1998). Differential roles for bone morphogenetic protein (BMP) receptor type IB and IA in differentiation and specification of mesenchymal precursor cells to osteoblast and adipocyte lineages. J. Cell Biol. 142, 295-305.
6. Chen, R.-H., and Derynck, R. (1994). Homomeric interactions between type II transforming growth factor-b receptors. J. Biol Chem. 269, 22868-22874.
7. Chen, Y.G., Liu, F., and Massague, J. (1997). Mechanism of TGFb receptor inhibition by FKBP12. EMBO J. 16, 3866-3876.
8. Dewulf, N., Verschueren, K., Lonnoy, O., Moren, A., Grimsby, S., Vande Spiegle, K., Miyazono, K., Huylebroeck, D., and ten Dijke, P. (1995). Distinct spatial and temporal expression patterns of two type I receptors for bone morphogenetic proteins during mouse embryogenesis. Endocrinology 136, 2652-2663.
9. Dunn, N.R., Winnier, G.E., Hargett, L.K., Schrick, J.J., Fogo, A.B., and Hogan, B.L. (1997). Haploin sufficient phenotypes in Bmp4 heterozygous null mice and modification by mutations in Gli3 and Alx4. Dev. Biol. 188, 235-247.
10. Evan, G.I., Lewis, G.K., Ramsay, G., and Bishop, J.M. (1985). Isolation of monoclonal antibodies specific for human c-myc protooncogene product. Mol. Cell. Biol. 5, 3610-3616.
11. Gadella, T.W., Jr., and Jovin, T.M. (1995). Oligomerization of epidermal growth factor receptors on A431 cells studied by time-resolved fluorescence imaging microscopy. A stereochemical model for tyrosine kinase receptor activation. J. Cell Biol. 129, 1543-1558.
12. Gilboa, L., Wells, R.G., Lodish, H.F., and Henis, Y.I. (1998). Oligomeric structure of type I and type II transforming growth factor beta receptors: homodimers form in the ER and persist at the plasma membrane. J. Cell Biol. 140, 767-777.
13. Harlow, E., and Lane, D. (1988). Antibodies: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Press.
14. Henis, Y.I., Moustakas, A., Lin, H.Y., and Lodish, H.F. (1994). The types II and III transforming growth factor-beta receptors form homo-oligomers. J. Cell Biol. 126, 139-154.
15. Hogan, B.L. (1996). Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 10, 1580-1594.
16. Hoodless, P.A., Haerry, T., Abdollah, S., Stapleton, M., O'Connor, M.B., Attisano, L., and Wrana, J.L. (1996). MADR1, a MAD-related protein that functions in BMP2 signaling pathways. Cell 85, 489-500.
17. Huse, M., Chen, Y.-G., Massague, J., and Kuriyan, J. (1999). Crystal structure of the cytoplasmic domain of the type I TGFb receptor in complex with FKBP12. Cell 96, 425-436.
18. Jonk, L.J., Itoh, S., Heldin, C.H., ten Dijke, P., and Kruijer, W. (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.
19. Katagiri, T., Yamaguchi, A., Komaki, M., Abe, E., Takahashi, N., Ikeda, T., Rosen, V., Wozney, J.M., Fujisawa-Sehara, A., and Suda, T. (1994). Bone morphogenetic protein-2 converts the differentiation pathway of C2C12 myoblasts into the osteoblast lineage. J. Cell Biol. 127, 1755-1766.
20. Kawabata, M., Chytil, A., and Moses, H.L. (1995). Cloning of a novel type II serine/threonine kinase receptor through interaction with the type I transforming growth factor-beta receptor. J. Biol. Chem. 270, 5625-5630.
21. Kretzschmar, M., Liu, F., Hata, A., Doody, J., and Massague, J. (1997). The TGF-beta family mediator Smad1 is phosphorylated directly and activated functionally by the BMP receptor kinase. Genes Dev. 11, 984-995.
22. Kurozumi, K., Nishita, M., Yamaguchi, K., Fujita, T., Ueno, N., and Shibuya, H. (1998). BRAM1, a BMP receptor-associated molecule involved in BMP signaling. Genes Cells 3, 257-264.
23. Lin, H.Y., Moustakas, A., Knaus, P., Wells, R.G., Henis, Y.I., and Lodish, H.F. (1995). The soluble exoplasmic domain of the type II transforming growth factor (TGF)-beta receptor. A heterogeneously glycosylated protein with high affinity and selectivity for TGF-beta ligands. J. Biol. Chem. 270, 2747-2754.
24. Liu, F., Ventura, F., Doody, J., and Massague, J. (1995). Human type II receptor for bone morphogenic proteins (BMPs): extension of the two-kinase receptor model to the BMPs. Mol. Cell. Biol. 15, 3479-3486.
25. Livnah, O., Stura, E.A., Middleton, S.A., Johnson, D.L., Jolliffe, L.K., and Wilson, I.A. (1999). Crystallographic evidence for preformed dimers of erythropoietin receptor before ligand activation. Science 283, 987-990.
26. Luo, K., and Lodish, H.F. (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.
27. Luo, K., and Lodish, H.F. (1997). Positive and negative regulation of type II TGF-beta receptor signal transduction by autophosphorylation on multiple serine residues. EMBO J. 16, 1970-1981.
28. Massague, J. (1998). TGF-beta signal transduction. Annu. Rev. Biochem. 67, 753-791.
29. Moustakas, A., Lin, H.Y., Henis, Y.I., Plamondon, J., O'Connor, M.M., and Lodish, H.F. (1993). The transforming growth factor beta receptors types I, II, and III form hetero-oligomeric complexes in the presence of ligand. J. Biol. Chem. 268, 22215-22218.
30. Muramatsu, M., Yan, J., Eto, K., Tomoda, T., Yamada, R., and Arai, K. (1997). A chimeric serine/threonine kinase receptor system reveals the potential of multiple type II receptors to cooperate with transforming growth factor-beta type I receptor. Mol. Biol. Cell 8, 469-480.
31. Neul, J.L., and Ferguson, E.L. (1998). Spatially restricted activation of the SAX receptor by SCW modulates DPP/TKV signaling in Drosophila dorsal-ventral patterning. Cell 95, 483-494.
32. Nguyen, M., Park, S., Marques, G., and Arora, K. (1998). Interpretation of a BMP activity gradient in Drosophila embryos depends on synergistic signaling by two type I receptors, SAX and TKV. Cell 95, 495-506.
33. Nishitoh, H., Ichijo, H., Kimura, M., Matsumoto, T., Makishima, F., Yamaguchi, A., Yamashita, H., Enomoto, S., and Miyazono, K. (1996). Identification of type I and type II serine/threonine kinase receptors for growth/differentiation factor-5. J. Biol. Chem. 271, 21345-21352.
34. Nohno, T., Ishikawa, T., Saito, T., Hosokawa, K., Noji, S., Wolsing, D.H., and Rosenbaum, J.S. (1995). Identification of a human type II receptor for bone morphogenetic protein-4 that forms differential heteromeric complexes with bone morphogenetic protein type I receptors. J. Biol. Chem. 270, 22522-22526.
35. 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-beta type I and type II receptors in signal transduction. J. Biol. Chem. 269, 30753-30756.
36. Reddi, H. (1995). Bone morphogenetic proteins. Adv. Dent. Res. 9(Suppl 3), 13.
37. Remy, I., Wilson, I.A., and Michnick, S.W. (1999). Erythropoietin receptor activation by a ligand-induced conformation change. Science 283, 990-993.
38. Rodriguez, C., Chen, F., Weinberg, R.A., and Lodish, H.F. (1995). Cooperative binding of transforming growth factor (TGF)-beta 2 to the types I and II TCP-beta receptors. J. Biol. Chem. 270, 15919-15922.
39. Rosen, V., Thies, R.S., and Lyons, K. (1996). Signaling pathways in skeletal formation: a role for BMP receptors. Ann. NY Acad. Sci. 785, 59-69.
40. Rosenzweig, B.L., Imamura, T., Okadome, T., Cox, G.N., Yamashita, H., ten Dijke, P., Heldin, C.H., and Miyazono, K. (1995). Cloning and characterization of a human type II receptor for bone morphogenetic proteins. Proc. Natl. Acad. Sci. USA 92, 7632-7636.
41. Ruppert, R., Hoffmann, E., and Sebald, W. (1996). Human bone morphogenetic protein 2 contains a heparin-binding site which modifies its biological activity. Eur. J. Biochem. 237, 295-302.
42. Seed, B., and Aruffo, A. (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.
43. Storm, E.E., Huynh, T.V., Copeland, N.G., Jenkins, N.A., Kingsley, D.M., and Lee, S.J. (1994). Limb alterations in brachypodism mice due to mutations in a new member of the TGF beta-superfamily. Nature 368, 639-643.
44. Storm, E.E., and Kingsley, D.M. (1996). Joint patterning defects caused by single and double mutations in members of the bone morphogenetic protein (BMP) family. Development 122, 3969-3979.
45. Vivien, D., Attisano, L., Wrana, J.L., and Massague, J. (1995). Signaling activity of homologous and heterologous transforming growth factor-beta receptor kinase complexes. J. Biol. Chem. 270, 7134-7141.
46. Wang, E.A., Israel, D.I., Kelly, S., and Luxenberg, D.P. (1993). Bone morphogenetic protein-2 causes commitment and differentiation in C3H10T1/2 and 3T3 cells. Growth Factors 9, 57-71.
47. Wang, T., Li, B.Y., Danielson, P.D., Shah, P.C., Rockwell, S., Lechleider, R.J., Martin, J., Manganaro, T., and Donahoe, P.K. (1996). The immunophilin FKBP12 functions as a common inhibitor of the TGF beta family type I receptors. Cell 86, 435-444.
48. Weis-Garcia, F., and Massague, J. (1996). Complementation between kinase-defective and activation-defective TGF-beta receptors reveals a novel form of receptor cooperatively essential for signaling. EMBO J. 15, 276-284.
49. Wells, R.G., Gilboa, L., Sun, Y., Liu, X., Henis, Y.I., and Lodish, H.F. (1994). Transforming growth factor-β induces formation of a dithiothreitol-resistant type I/type II receptor complex in live cells. J. Biol. Chem. 274, 5716-5722.
50. Wilson, I.A., Niman, H.L., Houghten, R.A., Cherenson, A.R., Connolly, M.L., and Lerner, R.A. (1984). The structure of an antigenic determinant in a protein. Cell 37, 767-778.
51. Winnier, C., Blessing, M., Labosky, P.A., and Hogan, B.L (1995). Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 9, 2105-2116.
52. Wrana, J.L., Attisano, L., Carcamo, J., Zentella, A., Doody, J., Laiho, M., Wang, X.F., and Massague, J. (1992). TGF-α signals through a heteromeric protein kinase receptor complex. Cell 71, 1003-1014.
53. 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.
54. Yamaguchi, K., Nagai, S., Ninomiya-Tsuji, J., Nishita, M., Tamai, K., Irie, K., Ueno, N., Nishida, E., Shibuya, H., and Matsumoto, K. (1999). XIAP, a cellular member of the inhibitor of apoptosis protein family, links the receptors to TAB1-TAK1 in the BMP signaling pathway. EMBO J. 18, 179-187
55. Zhang, H., and Bradley, A. (1996). Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development 122, 2977-2986.
56. Zou, H., and Niswander, L. (1996). Requirement for BMP signaling in interdigital apoptosis and scale formation. Science 272, 738-741.
57. Zou, H., Wieser, R., Massague, J., and Niswander, L. (1997). Distinct roles of type I bone morphogenetic protein receptors in the formation and differentiation of cartilage. Genes Dev. 11, 2191-2203.