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PMID: 8609172 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

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

The Journal of cell biology ·Vol. 133 ·No. 2 ·1996-04-00 ·Pages 405-16

Steinfeld R, Van Den Berghe H, David G

Abstract

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.

MeSH Terms
Base Sequence Cell Differentiation Cross-Linking Reagents Fibroblast Growth Factor 2/genetics,metabolism,pharmacology Glycophorins/analysis Glycosaminoglycans/analysis Hematopoietic Stem Cells/cytology Heparan Sulfate Proteoglycans Heparin/pharmacology Heparitin Sulfate/analysis,genetics,metabolism,physiology Humans Lipopolysaccharide Receptors/analysis Membrane Glycoproteins/genetics,metabolism,physiology Molecular Sequence Data Protein Binding Proteoglycans/genetics,metabolism,physiology Receptor Protein-Tyrosine Kinases Receptor, Fibroblast Growth Factor, Type 1 Receptors, Fibroblast Growth Factor/genetics,metabolism Recombinant Fusion Proteins/isolation & purification,metabolism Signal Transduction/physiology Transfection Tumor Cells, Cultured
Chemicals
Cross-Linking Reagents Glycophorins Glycosaminoglycans Heparan Sulfate Proteoglycans Lipopolysaccharide Receptors Membrane Glycoproteins Proteoglycans Receptors, Fibroblast Growth Factor Recombinant Fusion Proteins Fibroblast Growth Factor 2 Heparin Heparitin Sulfate FGFR1 protein, human Receptor Protein-Tyrosine Kinases Receptor, Fibroblast Growth Factor, Type 1
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Steinfeld R
Center for Human Genetics, University of Leuven, Belgium.
Van Den Berghe H
David G
References (47)
47 references, click to expand
  1. Isolation of an additional member of the fibroblast growth factor receptor family, FGFR-3.
    Proc Natl Acad Sci U S A. 1991 Feb 15;88(4):1095-9 PMID: 1847508
  2. Specific heparan sulfate saccharides mediate the activity of basic fibroblast growth factor.
    J Biol Chem. 1994 Jan 14;269(2):931-5 PMID: 8288646
  3. FGFR-4, a novel acidic fibroblast growth factor receptor with a distinct expression pattern.
    EMBO J. 1991 Jun;10(6):1347-54 PMID: 1709094
  4. Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation.
    Science. 1991 Jun 21;252(5013):1705-8 PMID: 1646484
  5. The human fibroblast growth factor receptor genes: a common structural arrangement underlies the mechanisms for generating receptor forms that differ in their third immunoglobulin domain.
    Mol Cell Biol. 1991 Sep;11(9):4627-34 PMID: 1652059
  6. Heparin is required for cell-free binding of basic fibroblast growth factor to a soluble receptor and for mitogenesis in whole cells.
    Mol Cell Biol. 1992 Jan;12(1):240-7 PMID: 1309590
  7. Differential splicing in the extracellular region of fibroblast growth factor receptor 1 generates receptor variants with different ligand-binding specificities.
    Mol Cell Biol. 1992 Jan;12(1):82-8 PMID: 1309595
  8. Determination of ligand-binding specificity by alternative splicing: two distinct growth factor receptors encoded by a single gene.
    Proc Natl Acad Sci U S A. 1992 Jan 1;89(1):246-50 PMID: 1309608
  9. cDNA cloning and expression of a human FGF receptor which binds acidic and basic FGF.
    Growth Factors. 1991;4(3):197-208 PMID: 1722683
  10. Molecular cloning of a human basic fibroblast growth factor receptor cDNA and expression of a biologically active extracellular domain in a baculovirus system.
    Growth Factors. 1991;5(2):115-27 PMID: 1662973
  11. Expression of fibroblast growth factor receptors in human leukemia cells.
    Cancer Res. 1992 Apr 1;52(7):2004-7 PMID: 1372535
  12. A confined variable region confers ligand specificity on fibroblast growth factor receptors: implications for the origin of the immunoglobulin fold.
    EMBO J. 1992 May;11(5):1885-90 PMID: 1316275
  13. Identification of the basic fibroblast growth factor binding sequence in fibroblast heparan sulfate.
    J Biol Chem. 1992 May 25;267(15):10337-41 PMID: 1587820
  14. Heparin increases the affinity of basic fibroblast growth factor for its receptor but is not required for binding.
    J Biol Chem. 1994 Feb 11;269(6):3976-84 PMID: 8307953
  15. Formation of anhydrosugars in the chemical depolymerization of heparin.
    Biochemistry. 1976 Sep 7;15(18):3932-42 PMID: 9127
  16. Human erythroleukemia cell line (HEL) undergoes a drastic macrophage-like shift with TPA.
    Blood. 1983 Oct;62(4):832-45 PMID: 6309287
  17. Heparan sulfate proteoglycans of human lung fibroblasts. Structural heterogeneity of the core proteins of the hydrophobic cell-associated forms.
    J Biol Chem. 1987 Jan 15;262(2):854-9 PMID: 2948951
  18. High and low affinity binding sites for basic fibroblast growth factor on cultured cells: absence of a role for low affinity binding in the stimulation of plasminogen activator production by bovine capillary endothelial cells.
    J Cell Physiol. 1987 Apr;131(1):123-30 PMID: 3032990
  19. Reduction in protein tyrosine phosphorylation during differentiation of human leukemia cell line K-562.
    Cancer Res. 1987 Aug 1;47(15):4066-70 PMID: 2440557
  20. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase.
    Science. 1988 Jan 29;239(4839):487-91 PMID: 2448875
  21. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa.
    Anal Biochem. 1987 Nov 1;166(2):368-79 PMID: 2449095
  22. Induction of erythroid differentiation of K562 human leukemic cells by herbimycin A, an inhibitor of tyrosine kinase activity.
    Cancer Res. 1989 Jan 15;49(2):331-4 PMID: 2910452
  23. Multiple distinct membrane heparan sulfate proteoglycans in human lung fibroblasts.
    J Biol Chem. 1989 Apr 25;264(12):7009-16 PMID: 2523387
  24. Partial primary structure of the 48- and 90-kilodalton core proteins of cell surface-associated heparan sulfate proteoglycans of lung fibroblasts. Prediction of an integral membrane domain and evidence for multiple distinct core proteins at the cell surface of human lung fibroblasts.
    J Biol Chem. 1989 Apr 25;264(12):7017-24 PMID: 2523388
  25. Carboxyl-terminal structure of basic fibroblast growth factor significantly contributes to its affinity for heparin.
    Eur J Biochem. 1990 Mar 10;188(2):239-45 PMID: 2180699
  26. Sequence of human syndecan indicates a novel gene family of integral membrane proteoglycans.
    J Biol Chem. 1990 Apr 25;265(12):6884-9 PMID: 2324102
  27. Cloning and expression of two distinct high-affinity receptors cross-reacting with acidic and basic fibroblast growth factors.
    EMBO J. 1990 Sep;9(9):2685-92 PMID: 1697263
  28. Release of GPI-anchored membrane proteins by a cell-associated GPI-specific phospholipase D.
    EMBO J. 1994 Apr 1;13(7):1741-51 PMID: 7512501
  29. Fibroblast growth factor receptor (FGFR) 3. Alternative splicing in immunoglobulin-like domain III creates a receptor highly specific for acidic FGF/FGF-1.
    J Biol Chem. 1994 Apr 15;269(15):11620-7 PMID: 7512569
  30. Cell surface syndecan-1 on distinct cell types differs in fine structure and ligand binding of its heparan sulfate chains.
    J Biol Chem. 1994 Jul 22;269(29):18881-90 PMID: 8034644
  31. Multivalent ligand-receptor binding interactions in the fibroblast growth factor system produce a cooperative growth factor and heparin mechanism for receptor dimerization.
    Biochemistry. 1994 Aug 30;33(34):10229-48 PMID: 7520751
  32. The ins and outs of fibroblast growth factors.
    Cell. 1994 Aug 26;78(4):547-52 PMID: 8069907
  33. Pathway-specific regulation of the synthesis of anticoagulantly active heparan sulfate.
    J Biol Chem. 1994 Oct 7;269(40):24941-52 PMID: 7929177
  34. Perlecan, basal lamina proteoglycan, promotes basic fibroblast growth factor-receptor binding, mitogenesis, and angiogenesis.
    Cell. 1994 Dec 16;79(6):1005-13 PMID: 7528102
  35. Heparin-induced oligomerization of FGF molecules is responsible for FGF receptor dimerization, activation, and cell proliferation.
    Cell. 1994 Dec 16;79(6):1015-24 PMID: 7528103
  36. Structure of a heparan sulphate oligosaccharide that binds to basic fibroblast growth factor.
    Biochem J. 1992 Aug 1;285 ( Pt 3):805-13 PMID: 1497618
  37. Kinetics of basic fibroblast growth factor binding to its receptor and heparan sulfate proteoglycan: a mechanism for cooperactivity.
    Biochemistry. 1992 Sep 22;31(37):8876-83 PMID: 1390674
  38. Characterization of a biologically active extracellular domain of fibroblast growth factor receptor 1 expressed in Escherichia coli.
    Eur J Biochem. 1992 Dec 15;210(3):823-29 PMID: 1336458
  39. Preparation of affinity-fractionated, heparin-derived oligosaccharides and their effects on selected biological activities mediated by basic fibroblast growth factor.
    J Biol Chem. 1993 Mar 5;268(7):4675-83 PMID: 8444841
  40. Structure and biological activities of a heparin-derived hexasaccharide with high affinity for basic fibroblast growth factor.
    J Biol Chem. 1993 Mar 5;268(7):4684-9 PMID: 8444842
  41. An essential heparin-binding domain in the fibroblast growth factor receptor kinase.
    Science. 1993 Mar 26;259(5103):1918-21 PMID: 8456318
  42. Developmental regulation of neural response to FGF-1 and FGF-2 by heparan sulfate proteoglycan.
    Science. 1993 Apr 2;260(5104):103-6 PMID: 7682010
  43. Minimal sequence in heparin/heparan sulfate required for binding of basic fibroblast growth factor.
    J Biol Chem. 1993 Nov 15;268(32):23898-905 PMID: 8226930
  44. Activating and inhibitory heparin sequences for FGF-2 (basic FGF). Distinct requirements for FGF-1, FGF-2, and FGF-4.
    J Biol Chem. 1993 Nov 15;268(32):23906-14 PMID: 7693696
  45. Inhibition of basic fibroblast growth factor-induced growth promotion by overexpression of syndecan-1.
    J Biol Chem. 1993 Nov 15;268(32):24215-22 PMID: 8226969
  46. Differential structural requirements of heparin and heparan sulfate proteoglycans that promote binding of basic fibroblast growth factor to its receptor.
    J Biol Chem. 1994 Jan 7;269(1):114-21 PMID: 8276782
  47. Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor.
    Cell. 1991 Feb 22;64(4):841-8 PMID: 1847668
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1996-04-00
Pages
405-16
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2120790
Subset
IM
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