Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor

The role of low affinity, heparin-like binding sites for basic fibroblast growth factor (bFGF) was investigated in CHO cells mutant in their metabolism of glycosaminoglycans. Heparan sulfate-deficient mutants transfected to express a cloned mouse FGF receptor cDNA are not able to bind bFGF. It is demonstrated that free heparin and heparan sulfate can reconstitute a low affinity receptor that is, in turn, required for the high affinity binding of bFGF. These studies suggest that the low affinity receptor is an accessory molecule required for binding of bFGF to the high affinity site. Such an obligatory interaction of low and high affinity FGF receptors suggests a physiological role for heparin-like, low affinity receptors and constitutes a novel mechanism for the regulation of growth factor-receptor interactions.

[1]  O. Bernard,et al.  Two forms of the basic fibroblast growth factor receptor-like mRNA are expressed in the developing mouse brain. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[2]  H. Hanafusa,et al.  Novel tyrosine kinase identified by phosphotyrosine antibody screening of cDNA libraries , 1988, Molecular and cellular biology.

[3]  J. Folkman,et al.  Importance of size, sulfation, and anticoagulant activity in the potentiation of acidic fibroblast growth factor by heparin. , 1989, The Journal of biological chemistry.

[4]  L. Culp,et al.  Glycosaminoglycans that bind cold-insoluble globulin in cell-substratum adhesion sites of murine fibroblasts. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[5]  J. Esko,et al.  Undersulfated heparan sulfate in a Chinese hamster ovary cell mutant defective in heparan sulfate N-sulfotransferase. , 1989, The Journal of biological chemistry.

[6]  J. Folkman,et al.  Endothelial cell-derived basic fibroblast growth factor: synthesis and deposition into subendothelial extracellular matrix. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[7]  M. Klagsbrun,et al.  Heparin affinity of anionic and cationic capillary endothelial cell growth factors: analysis of hypothalamus-derived growth factors and fibroblast growth factors. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[8]  D. Rifkin,et al.  Recent developments in the cell biology of basic fibroblast growth factor , 1989, The Journal of cell biology.

[9]  R. Kaner,et al.  Fibroblast growth factor receptor is a portal of cellular entry for herpes simplex virus type 1. , 1990, Science.

[10]  D. Moscatelli,et al.  A murine fibroblast growth factor (FGF) receptor expressed in CHO cells is activated by basic FGF and Kaposi FGF. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[11]  M. Rusnati,et al.  Modulation of plasminogen activator activity in human endometrial adenocarcinoma cells by basic fibroblast growth factor and transforming growth factor beta. , 1988, Cancer research.

[12]  H. Nader,et al.  Heparin sequences in the heparan sulfate chains of an endothelial cell proteoglycan. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[13]  M. Höök,et al.  Glycosaminoglycans and their binding to biological macromolecules. , 1978, Annual review of biochemistry.

[14]  J. Folkman,et al.  Heparin affinity: purification of a tumor-derived capillary endothelial cell growth factor. , 1984, Science.

[15]  D. Rifkin,et al.  Endothelial cell-derived heparan sulfate binds basic fibroblast growth factor and protects it from proteolytic degradation , 1988, The Journal of cell biology.

[16]  M. Klagsbrun.  The fibroblast growth factor family: structural and biological properties. , 1989, Progress in growth factor research.

[17]  R. Sanderson,et al.  Syndecan, a developmentally regulated cell surface proteoglycan that binds extracellular matrix and growth factors. , 1990, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[18]  J. Esko,et al.  Altered metabolism of thrombospondin by Chinese hamster ovary cells defective in glycosaminoglycan synthesis. , 1988, The Journal of biological chemistry.

[19]  D. Moscatelli,et al.  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 , 1987, Journal of cellular physiology.

[20]  D. Ingber,et al.  A heparin-binding angiogenic protein--basic fibroblast growth factor--is stored within basement membrane. , 1988, The American journal of pathology.

[21]  Y. Yarden,et al.  The murine flg gene encodes a receptor for fibroblast growth factor. , 1990, Oncogene.

[22]  J. Folkman,et al.  Protamine is an inhibitor of angiogenesis , 1982, Nature.

[23]  V. Fried,et al.  Purification and complementary DNA cloning of a receptor for basic fibroblast growth factor. , 1989, Science.

[24]  M. Klagsbrun,et al.  Autocrine transformation by chimeric signal peptide-basic fibroblast growth factor: reversal by suramin. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[25]  J. Folkman,et al.  Basic fibroblast growth factor binds to subendothelial extracellular matrix and is released by heparitinase and heparin-like molecules. , 1989, Biochemistry.

[26]  D. Moscatelli.  Metabolism of receptor-bound and matrix-bound basic fibroblast growth factor by bovine capillary endothelial cells , 1988, The Journal of cell biology.

[27]  D. Rifkin,et al.  Role of extracellular matrix in the action of basic fibroblast growth factor: Matrix as a source of growth factor for long‐term stimulation of plasminogen activator production and DNA synthesis , 1989, Journal of cellular physiology.

[28]  T. Imamura,et al.  Heparan sulfate and heparin as a potentiator or a suppressor of growth of normal and transformed vascular endothelial cells. , 1987, Experimental cell research.

[29]  S. Singer,et al.  Identification of a developmentally regulated protein-tyrosine kinase by using anti-phosphotyrosine antibodies to screen a cDNA expression library. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[30]  D. Gospodarowicz,et al.  Heparin protects basic and acidic FGF from inactivation , 1986, Journal of cellular physiology.

[31]  H. Saiga,et al.  The role of proteoglycan in the development of sea urchins. I. Abnormal development of sea urchin embryos caused by the disturbance of proteoglycan synthesis. , 1979, Experimental cell research.

[32]  P. Barr,et al.  Ligand-affinity cloning and structure of a cell surface heparan sulfate proteoglycan that binds basic fibroblast growth factor. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[33]  B. Seed.  An LFA-3 cDNA encodes a phospholipid-linked membrane protein homologous to its receptor CD2 , 1987, Nature.

[34]  D. Gospodarowicz,et al.  Basic and acidic fibroblast growth factors interact with the same cell surface receptors. , 1986, The Journal of biological chemistry.

[35]  S. Jeronimo,et al.  Isolation and structural studies of heparan sulfates and chondroitin sulfates from three species of molluscs. , 1984, The Journal of biological chemistry.

[36]  K. Thomas,et al.  Stabilization by heparin of acidic fibroblast growth factor mitogenicity for human endothelial cells in vitro , 1989, Journal of cellular physiology.

[37]  R. Lerner,et al.  Nucleotide sequence of Moloney murine leukaemia virus , 1981, Nature.

[38]  J. Esko,et al.  Tumor formation dependent on proteoglycan biosynthesis. , 1988, Science.

[39]  H. Nader,et al.  Structural differences of heparan sulfates according to the tissue and species of origin. , 1983, Biochemical and biophysical research communications.

[40]  P. Spear,et al.  Initial interaction of herpes simplex virus with cells is binding to heparan sulfate , 1989, Journal of virology.

[41]  E. Levine,et al.  Human endothelial cells: use of heparin in cloning and long-term serial cultivation. , 1983, Science.

[42]  P. Barr,et al.  Acidic and basic fibroblast growth factors stimulate tyrosine kinase activity in vivo. , 1988, The Journal of biological chemistry.

[43]  J. Esko,et al.  Binding of heparan sulfate to type V collagen. A mechanism of cell-substrate adhesion. , 1989, The Journal of biological chemistry.