Monomeric and dimeric GDF-5 show equal type I receptor binding and oligomerization capability and have the same biological activity

References

Amatayakul-Chantler, S., Qian, S.W., Gakenheimer, K., Bottinger, E.P., Roberts, A.B., and Sporn, M.B. (1994). [Ser77] transforming growth factor-β 1. Selective biological activity and receptor binding in mink lung epithelial cells. J. Biol. Chem.269, 27687–27691.Search in Google Scholar

Canalis, E., Economides, A.N., and Gazzerro, E. (2003). Bone morphogenetic proteins, their antagonists, and the skeleton. Endocr. Rev.24, 218–235.10.1210/er.2002-0023Search in Google Scholar

Cheifetz, S., Weatherbee, J.A., Tsang, M.L., Anderson, J.K., Mole, J.E., Lucas, R., and Massague, J. (1987). The transforming growth factor-b system, a complex pattern of cross-reactive ligands and receptors. Cell48, 409–415.10.1016/0092-8674(87)90192-9Search in Google Scholar

Daopin, S., Piez, K.A., Ogawa, Y., and Davies, D.R. (1992). Crystal structure of transforming growth factor-β2: an unusual fold for the superfamily. Science257, 369–373.10.1126/science.1631557Search in Google Scholar

De Crescenzo, G., Pham, P.L., Durocher, Y., and O'Connor-McCourt, M.D. (2003). Transforming growth factor-β (TGF-β) binding to the extracellular domain of the type II TGF-β receptor: receptor capture on a biosensor surface using a new coiled-coil capture system demonstrates that avidity contributes significantly to high affinity binding. J. Mol. Biol.328, 1173–1183.10.1016/S0022-2836(03)00360-7Search in Google Scholar

Evan, G.I., Lewis, G.K., Ramsay, G., and Bishop, J.M. (1985). Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol.5, 3610–3616.Search in Google Scholar

Gilboa, L., Wells, R.G., Lodish, H.F., and Henis, Y.I. (1998). Oligomeric structure of type I and type II transforming growth factor β receptors: homodimers form in the ER and persist at the plasma membrane. J. Cell Biol.140, 767–777.10.1083/jcb.140.4.767Search in Google Scholar

Gilboa, L., Nohe, A., Geissendorfer, T., Sebald, W., Henis, Y.I., and Knaus, P. (2000). Bone morphogenetic protein receptor complexes on the surface of live cells: a new oligomerization mode for serine/threonine kinase receptors. Mol. Biol. Cell11, 1023–1035.10.1091/mbc.11.3.1023Search in Google Scholar

Greenwald, J., Groppe, J., Gray, P., Wiater, E., Kwiatkowski, W., Vale, W., and Choe, S. (2003). The BMP7/ActRII extracellular domain complex provides new insights into the cooperative nature of receptor assembly. Mol. Cell11, 605–617.10.1016/S1097-2765(03)00094-7Search in Google Scholar

Hart, P.J., Deep, S., Taylor, A.B., Shu, Z., Hinck, C.S., and Hinck, A.P. (2002). Crystal structure of the human TbR2 ectodomain-TGF-β3 complex. Nat. Struct. Biol.9, 203–208.Search in Google Scholar

Henis, Y.I., Moustakas, A., Lin, H.Y., and Lodish, H.F. (1994). The types II and III transforming growth factor-β receptors form homo-oligomers. J. Cell Biol.126, 139–154.10.1083/jcb.126.1.139Search in Google Scholar

Honda, J., Andou, H., Mannen, T., and Sugimoto, S. (2000). Direct refolding of recombinant human growth differentiation factor 5 for large-scale production process. J. Biosci. Bioeng.89, 582–589.10.1016/S1389-1723(00)80061-4Search in Google Scholar

Hotten, G.C., Matsumoto, T., Kimura, M., Bechtold, R.F., Kron, R., Ohara, T., Tanaka, H., Satoh, Y., Okazaki, M., Shirai, T., et al. (1996). Recombinant human growth/differentiation factor 5 stimulates mesenchyme aggregation and chondrogenesis responsible for the skeletal development of limbs. Growth Factors13, 65–74.10.3109/08977199609034567Search in Google Scholar PubMed

Husken-Hindi, P., Tsuchida, K., Park, M., Corrigan, A.Z., Vaughan, J.M., Vale, W.W., and Fischer, W.H. (1994). Monomeric activin A retains high receptor binding affinity but exhibits low biological activity. J. Biol. Chem.269, 19380–19384.10.1016/S0021-9258(17)32179-8Search in Google Scholar

Israel, D.I., Nove, J., Kerns, K.M., Kaufman, R.J., Rosen, V., Cox, K.A., and Wozney, J.M. (1996). Heterodimeric bone morphogenetic proteins show enhanced activity in vitro and in vivo. Growth Factors13, 291–300.10.3109/08977199609003229Search in Google Scholar

Jen, A., Madorin, K., Vosbeck, K., Arvinte, T., and Merkle, H.P. (2002). Transforming growth factor β-3 crystals as reservoirs for slow release of active TGF-β3. J. Control Release78, 25–34.10.1016/S0168-3659(01)00490-4Search in Google Scholar

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-β, activin, and bone morphogenetic protein-inducible enhancer. J. Biol. Chem.273, 21145–21152.10.1074/jbc.273.33.21145Search in Google Scholar

Kingsley, D.M. (1994). The TGF-β superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev.8, 133–146.10.1101/gad.8.2.133Search in Google Scholar

Kirsch, T., Sebald, W., and Dreyer, M.K. (2000). Crystal structure of the BMP-2-BRIA ectodomain complex. Nat. Struct. Biol.7, 492–496.10.1038/75903Search in Google Scholar

Knaus, P. and Sebald, W. (2001). Cooperativity of binding epitopes and receptor chains in the BMP/TGFβ superfamily. Biol. Chem.382, 1189–1195.10.1515/BC.2001.149Search in Google Scholar

Lachmanovich, E., Shvartsman, D.E., Malka, Y., Botvin, C., Henis, Y.I., and Weiss, A.M. (2003). Co-localization analysis of complex formation among membrane proteins by computerized fluorescence microscopy: application to immunofluorescence co-patching studies. J. Microsc.212, 122–131.10.1046/j.1365-2818.2003.01239.xSearch in Google Scholar

Massague, J. (2000). How cells read TGF-β signals. Nat. Rev. Mol. Cell. Biol.1, 169–178.10.1038/35043051Search in Google Scholar

McPherron, A.C. and Lee, S.J. (1993). GDF-3 and GDF-9: two new members of the transforming growth factor-β superfamily containing a novel pattern of cysteines. J. Biol. Chem.268, 3444–3449.10.1016/S0021-9258(18)53714-5Search in Google Scholar

Nakamura, K., Shirai, T., Morishita, S., Uchida, S., Saeki-Miura, K., and Makishima, F. (1999). p38 mitogen-activated protein kinase functionally contributes to chondrogenesis induced by growth/differentiation factor-5 in ATDC5 cells. Exp. Cell. Res.250, 351–363.10.1006/excr.1999.4535Search in Google Scholar PubMed

Nickel, J., Kotzsch, A., Sebald, W., and Mueller, T.D. (2005). A single residue of GDF-5 defines binding specificity to BMP receptor IB. J. Mol. Biol.349, 933–947.10.1016/j.jmb.2005.04.015Search in Google Scholar PubMed

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, 21345–21352.10.1074/jbc.271.35.21345Search in Google Scholar PubMed

Nohe, A., Hassel, S., Ehrlich, M., Neubauer, F., Sebald, W., Henis, Y.I., and Knaus, P. (2002). The mode of bone morphogenetic protein (BMP) receptor oligomerization determines different BMP-2 signaling pathways. J. Biol. Chem.277, 5330–5338.10.1074/jbc.M102750200Search in Google Scholar PubMed

Ogawa, Y., Schmidt, D.K., Dasch, J.R., Chang, R.J., and Glaser, C.B. (1992). Purification and characterization of transforming growth factor-β 2.3 and -β 1.2 heterodimers from bovine bone. J. Biol. Chem.267, 2325–2328.Search in Google Scholar

O'Keeffe, G.W., Hanke, M., Pohl, J., and Sullivan, A.M. (2004). Expression of growth differentiation factor-5 in the developing and adult rat brain. Brain Res. Dev. Brain Res.151, 199–202.10.1016/j.devbrainres.2004.04.004Search in Google Scholar PubMed

Piek, E., Heldin, C.H., and Ten Dijke, P. (1999). Specificity, diversity, and regulation in TGF-β superfamily signaling. FASEB J.13, 2105–2124.10.1096/fasebj.13.15.2105Search in Google Scholar

Sammar, M., Stricker, S., Schwabe, G.C., Sieber, C., Hartung, A., Hanke, M., Oishi, I., Pohl, J., Minami, Y., Sebald, W., et al. (2004). Modulation of GDF5/BRI-b signalling through interaction with the tyrosine kinase receptor Ror2. Genes Cells9, 1227–1238.10.1111/j.1365-2443.2004.00799.xSearch in Google Scholar PubMed

Schlunegger, M.P. and Grutter, M.G. (1992). An unusual feature revealed by the crystal structure at 2.2 Å resolution of human transforming growth factor-β 2. Nature358, 430–434.Search in Google Scholar

Schreuder, H., Liesum, A., Pohl, J., Kruse, M., and Koyama, M. (2005). Crystal structure of recombinant human growth and differentiation factor 5: evidence for interaction of the type I and type II receptor-binding sites. Biochem. Biophys. Res. Commun.329, 1076–1086.10.1016/j.bbrc.2005.02.078Search in Google Scholar PubMed

Sebald, W., Nickel, J., Zhang, J.L., and Mueller, T.D. (2004). Molecular recognition in bone morphogenetic protein (BMP)/receptor interaction. Biol. Chem.385, 697–710.10.1515/BC.2004.086Search in Google Scholar PubMed

Seemann, P., Schwappacher, R., Kjaer, K.W., Krakow, D., Lehmann, K., Dawson, K., Stricker, S., Pohl, J., Ploger, F., Staub, E., et al. (2005). Activating and deactivating mutations in the receptor interaction site of GDF5 cause symphalangism or brachydactyly type A2. J. Clin. Invest.115, 2373–2381.10.1172/JCI25118Search in Google Scholar PubMed PubMed Central

Shi, Y. and Massague, J. (2003). Mechanisms of TGF-β signaling from cell membrane to the nucleus. Cell113, 685–700.10.1016/S0092-8674(03)00432-XSearch in Google Scholar

Shimmi, O., Umulis, D., Othmer, H., and O'Connor, M.B. (2005). Facilitated transport of a Dpp/Scw heterodimer by Sog/Tsg leads to robust patterning of the Drosophila blastoderm embryo. Cell120, 873–886.10.1016/j.cell.2005.02.009Search in Google Scholar PubMed PubMed Central

Vitt, U.A., Mazerbourg, S., Klein, C., and Hsueh, A.J. (2002). Bone morphogenetic protein receptor type II is a receptor for growth differentiation factor-9. Biol. Reprod.67, 473–480.10.1095/biolreprod67.2.473Search in Google Scholar PubMed