The Journal of Cell Biology, Vol 133, 405-416, Copyright © 1996 by The Rockefeller University Press

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Stimulation of fibroblast growth factor receptor-1 occupancy and signaling by cell surface-associated syndecans and glypican

R Steinfeld, H Van Den Berghe and G David
Center for Human Genetics, University of Leuven, Belgium.

The formation of distinctive basic FGF-heparan sulfate complexes is essential for the binding of bFGF to its cognate receptor. In previous experiments, cell-surface heparan sulfate proteoglycans extracted from human lung fibroblasts could not be shown to promote high affinity binding of bFGF when added to heparan sulfate-deficient cells that express FGF receptor-1 (FGFR1) (Aviezer, D., D. Hecht, M. Safran, M. Eisinger, G. David, and A. Yayon. 1994. Cell 79:1005-1013). In alternative tests to establish whether cell-surface proteoglycans can support the formation of the required complexes, K562 cells were first transfected with the IIIc splice variant of FGFR1 and then transfected with constructs coding for either syndecan-1, syndecan-2, syndecan-4 or glypican, or with an antisense syndecan-4 construct. Cells cotransfected with receptor and proteoglycan showed a two- to three- fold increase in neutral salt-resistant specific 125I-bFGF binding in comparison to cells transfected with only receptor or cells cotransfected with receptor and anti-syndecan-4. Exogenous heparin enhanced the specific binding and affinity cross-linking of 125I-bFGF to FGFR1 in receptor transfectants that were not cotransfected with proteoglycan, but had no effect on this binding and decreased the yield of bFGFR cross-links in cells that were cotransfected with proteoglycan. Receptor-transfectant cells showed a decrease in glycophorin A expression when exposed to bFGF. This suppression was dose-dependent and obtained at significantly lower concentrations of bFGF in proteoglycan-cotransfected cells. Finally, complementary cell- free binding assays indicated that the affinity of 125I-bFGF for an immobilized FGFR1 ectodomain was increased threefold when the syndecan- 4 ectodomain was coimmobilized with receptor. Equimolar amounts of soluble syndecan-4 ectodomain, in contrast, had no effect on this binding. We conclude that, at least in K562 cells, syndecans and glypican can support bFGF-FGFR1 interactions and signaling, and that cell-surface association may augment their effectiveness.
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• Penc, S. F., Pomahac, B., Winkler, T., Dorschner, R. A., Eriksson, E., Herndon, M., Gallo, R. L. (1998). Dermatan Sulfate Released after Injury Is a Potent Promoter of Fibroblast Growth Factor-2 Function. J. Biol. Chem. 273: 28116-28121 [Abstract] [Full Text]  
• Zhang, Z., Galileo, D. S. (1998). Retroviral Transfer of Antisense Integrin alpha 6 or alpha 8 Sequences Results in Laminar Redistribution or Clonal Cell Death in Developing Brain. J. Neurosci. 18: 6928-6938 [Abstract] [Full Text]  
• Liu, W., Litwack, E. D., Stanley, M. J., Langford, J. K., Lander, A. D., Sanderson, R. D. (1998). Heparan Sulfate Proteoglycans as Adhesive and Anti-invasive Molecules. SYNDECANS AND GLYPICAN HAVE DISTINCT FUNCTIONS. J. Biol. Chem. 273: 22825-22832 [Abstract] [Full Text]  
• Gonzalez, A. D., Kaya, M., Shi, W., Song, H., Testa, J. R., Penn, L. Z., Filmus, J. (1998). OCI-5/GPC3, a Glypican Encoded by a Gene That Is Mutated in the Simpson-Golabi-Behmel Overgrowth Syndrome, Induces Apoptosis in a Cell Line-specific Manner. JCB 141: 1407-1414 [Abstract] [Full Text]  
• Kainulainen, V., Wang, H., Schick, C., Bernfield, M. (1998). Syndecans, Heparan Sulfate Proteoglycans, Maintain the Proteolytic Balance of Acute Wound Fluids. J. Biol. Chem. 273: 11563-11569 [Abstract] [Full Text]  
• Perollet, C., Han, Z. C., Savona, C., Caen, J. P., Bikfalvi, A. (1998). Platelet Factor 4 Modulates Fibroblast Growth Factor 2 (FGF-2) Activity and Inhibits FGF-2 Dimerization. Blood 91: 3289-3299 [Abstract] [Full Text]  
• Sherman, L., Wainwright, D., Ponta, H., Herrlich, P. (1998). A splice variant of CD44 expressed in the apical ectodermal ridge presents fibroblast growth factors to limb mesenchyme and is required for limb outgrowth. Genes Dev. 12: 1058-1071 [Abstract] [Full Text]  
• Grootjans, J. J., Zimmermann, P., Reekmans, G., Smets, A., Degeest, G., Durr, J., David, G. (1997). Syntenin, a PDZ protein that binds syndecan cytoplasmic domains. Proc. Natl. Acad. Sci. USA 94: 13683-13688 [Abstract] [Full Text]  
• Larrain, J., Cizmeci-Smith, G., Troncoso, V., Stahl, R. C., Carey, D. J., Brandan, E. (1997). Syndecan-1 Expression Is Down-regulated during Myoblast Terminal Differentiation. MODULATION BY GROWTH FACTORS AND RETINOIC ACID. J. Biol. Chem. 272: 18418-18424 [Abstract] [Full Text]  
• Subramanian, S. V., Fitzgerald, M. L., Bernfield, M. (1997). Regulated Shedding of Syndecan-1 and -4 Ectodomains by Thrombin and Growth Factor Receptor Activation. J. Biol. Chem. 272: 14713-14720 [Abstract] [Full Text]  
• McFall, A. J., Rapraeger, A. C. (1997). Identification of an Adhesion Site within the Syndecan-4 Extracellular Protein Domain. J. Biol. Chem. 272: 12901-12904 [Abstract] [Full Text]  
• Bonneh-Barkay, D., Shlissel, M., Berman, B., Shaoul, E., Admon, A., Vlodavsky, I., Carey, D. J., Asundi, V. K., Reich-Slotky, R., Ron, D. (1997). Identification of Glypican as a Dual Modulator of the Biological Activity of Fibroblast Growth Factors. J. Biol. Chem. 272: 12415-12421 [Abstract] [Full Text]  
• Song, H. H., Shi, W., Filmus, J. (1997). OCI-5/Rat Glypican-3 Binds to Fibroblast Growth Factor-2 but Not to Insulin-like Growth Factor-2. J. Biol. Chem. 272: 7574-7577 [Abstract] [Full Text]  
• Jackson, S., Nakato, H, Sugiura, M, Jannuzi, A, Oakes, R, Kaluza, V, Golden, C, Selleck, S. (1997). dally, a Drosophila glypican, controls cellular responses to the TGF-beta-related morphogen, Dpp. Development 124: 4113-4120 [Abstract]  
• Haerry, T., Heslip, T., Marsh, J., O'Connor, M. (1997). Defects in glucuronate biosynthesis disrupt Wingless signaling in Drosophila. Development 124: 3055-3064 [Abstract]  
• Walz, A, McFarlane, S, Brickman, Y., Nurcombe, V, Bartlett, P., Holt, C. (1997). Essential role of heparan sulfates in axon navigation and targeting in the developing visual system. Development 124: 2421-2430 [Abstract]  
• Rodriguez-Manzaneque, J. C., Milchanowski, A. B., Dufour, E. K., Leduc, R., Iruela-Arispe, M. L. (2000). Characterization of METH-1/ADAMTS1 Processing Reveals Two Distinct Active Forms. J. Biol. Chem. 275: 33471-33479 [Abstract] [Full Text]  
• Park, P. W., Reizes, O., Bernfield, M. (2000). Cell Surface Heparan Sulfate Proteoglycans: Selective Regulators of Ligand-Receptor Encounters. J. Biol. Chem. 275: 29923-29926 [Full Text]  

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