Modulation of fibroblast growth factor-2 receptor binding, dimerization, signaling, and angiogenic activity by a synthetic heparin-mimicking polyanionic compound

Journal of Clinical Investigation

Volumn 99, Issue 7, 1997, Pages 1565-1575

  Miao, Hua Quan ^a   Ornitz, David M ^b   Aingorn, Elena ^a   Ben Sasson, Shmuel A ^c   Vlodavsky, Israel ^a  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c HEBREW UNIVERSITY   (Israel)

Author keywords

angiogenesis; antiproliferative activity; heparan sulfate; heparin mimetics; vascular endothelial cells

Indexed keywords

4 HYDROXYPHENOXYACETIC ACID; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR; HEPARAN SULFATE; HEPARIN; HEPARIN LYASE; POLYANION; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CATTLE; CELL ADHESION; CELL PROLIFERATION; CONTROLLED STUDY; DIMERIZATION; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BINDING; VASCULAR ENDOTHELIUM;

EID: 0030985599     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI119319     Document Type: Article

References (53)

1. Burgess, W.H., and T. Maciag. 1989. The heparin-binding (fibroblast) growth factor family of proteins. Annu. Rev. Biochem. 58:575-606.
2. Johnson, O.E., and L.T. Williams. 1993. Structural and functional diversity in the FGF receptor multigene family. Adv. Cancer Res. 60:1-41.
3. Rapraeger, A.C. 1995. In the clutches of proteoglycans: how does heparan sulfate regulate FGF binding. Chem. Biol. 2:645-649.
4. Klagsbrun, M., and A. Baird. 1991. A dual receptor system is required for basic fibroblast growth factor activity. Cell. 67:229-231.
5. Schlessinger, J., I. Lax, and M. Lemmon. 1995. Regulation of growth factor activation by proteoglycans: what is the role of the low affinity receptors? Cell. 83:357-360.
6. Saksela, O., D. Moscatelli, A. Sommer, and D.E. Rifkin. 1988. Endothelial cell-derived heparan sulfate binds basic fibroblast growth factor and protects it from proteolytic degradation. J. Cell Biol. 107:743-751.
7. Kan, M., F. Wang, J. Xu, J.W. Crabb, J. Hon, and W.L. McKeehan. 1993. An essential heparin-binding domain in the fibroblast growth factor receptor kinase. Science (Wash. DC). 259:1918-1921.
8. Moscatelli, D., and N. Quarto. 1989. Transformation of NIH 3T3 cells with basic fibroblast growth factor or the hst/K-FGF oncogene causes down regulation of the fibroblast growth factor receptor: reversal of morphological transformation and restoration of receptor number by suramin. J. Cell Biol. 109:2519-2527.
9. Yayon, A., and M. Klagsbrun. 1990. Autocrine transformation by chimeric signal peptide-basic fibroblast growth factor: reversal by suramin. Proc. Natl. Acad. Sci. USA. 87:5346-5350.
10. Gagliardi, A., H. Hadd, and D.C. Collins. 1992. Inhibition of angiogenesis by suramin. Cancer Res. 52:5073-5075.
11. Zugmaier, G., M.E. Lippman, and A. Wellstein. 1992. Inhibition by pentosan polysulfate (PPS) of heparin-binding growth factors released from tumor cells and blockage by PPS of tumor growth in animals. J. Natl. Cancer Inst. 84: 1716-1724.
12. Miao, H.-Q., R. Ishai-Michaeli, T. Peretz, and I. Vlodavsky. 1995. Laminarin sulfate mimics the effects of heparin on smooth muscle cell proliferation and basic fibroblast growth factor-receptor binding and mitogenic activity. J. Cell. Physiol. 164:482-490.
13. Szabo, S., P. Vattay, E. Scarbrough, and J. Folkman. 1991. Role of vascular factors, including angiogenesis, in the mechanisms of action of sucralfate. Am. J. Med. 91:158S-160S.
14. Spivak-Kroizman, T., M.A. Lemmon, I. Dikic, J.E. Ladbury, D. Pinchasi, J. Huang, M. Jaye, G. Crumley, J. Schlessinger, and I. Lax. 1994. Heparin-induced oligomerization of FGF molecules is responsible for FGF receptor dimerization, activation, and cell proliferation. Cell. 79:1015-1024.
15. Gagliardi, A.R., and D.C. Collins. 1994. Inhibition of angiogenesis by aurintricarboxylic acid. Anticancer Res. 14:475-479.
16. Folkman, J. 1995. Angiogenesis in cancer, vascular, rheumatoid and other diseases. Nat. Med. 1:27-31.
17. Regan, J., S.A. Ben-Sasson, R. Sabatino, D. Eilat, J.G. Bruno, R. D'Alisa, and M.N. Chang. 1993. Mimicry of biological macromolecules by polyaromatic anionic compounds. J. Bioact. Compat. Polym. 8:317-337.
18. Benezra, M., I. Vlodavsky, A. Yayon, R. Bar-Shavit, J. Regan, M. Chang, and S.A. Ben-Sasson. 1992. Reversal of basic fibroblast growth factor-mediated autocrine cell transformation by aromatic anionic compounds. Cancer Res. 52:5656-5662.
19. Benezra, M., S.A. Ben-Sasson, J. Regan, M. Chang, R. Bar-Shavit, and I. Vlodavsky. 1994. Antiproliferative activity to vascular smooth muscle cells and receptor binding of heparin-mimicking polyaromatic anionic compounds. Arterioscler. Thromb. 14:1992-1999.
20. Gospodarowicz, D., J. Moran, D. Braun, and C.R. Birdwell. 1976. Clonal growth of bovine vascular endothelial cells in tissue culture: fibroblast growth factor as a survival agent. Proc. Natl. Acad. Sci. USA. 73:4120-4124.
21. Vlodavsky, I., J. Folkman, R. Sullivan, R. Fridman, R. Ishai-Michaeli, J. Sasse, and M. Klagsbrun. 1987. Endothelial cell-derived basic fibroblast growth factor: synthesis and deposition into subendothelial extracellular matrix. Proc. Natl. Acad. Sci. USA. 84:2292-2296.
22. Esko, J.D. 1991. Genetic analysis of proteoglycan structure, function and metabolism. Curr. Opin. Cell Biol. 3:805-816.
23. Yayon, A., M. Klagsbrun, J.D. Esko, P. Leder, and D.M. Ornitz. 1991. Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell. 64:841-848.
24. Miao, H.-Q., T.A. Fritz, J.D. Esko, J. Zimmermann, A. Yayon, and I. Vlodavsky. 1995. Heparan sulfate primed on beta-D-xylosides restores binding of basic fibroblast growth factor. J. Cell. Biochem. 57:173-184.
25. Ornitz, D.M., A. Yayon, J.G. Flanagan, C.M. Svahn, E. Levi, and P. Leder. 1992. 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. 12:240-247.
26. Glabe, C.G., P.K. Harty, and S.D. Rosen. 1983. Preparation and properties of fluorescent polysaccharides. Anal. Biochem. 130:287-294.
27. Ornitz, D.M., A.B. Herr, M. Nilsson, J. Westman, C.-M. Svahn, and G. Waksman. 1995. FGF binding and FGF receptor activation by synthetic heparan-derived di- and trisaccharides. Science (Wash. DC). 268:432-436.
28. Chellaiah, A.T., D.G. McEwen, S. Werner, J. Xu, and D.M. Ornitz. 1994. 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. 269:11620-11627.
29. Moscatelli, D. 1987. 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. 13:123-130.
30. Moscatelli, D. 1988. Metabolism of receptor-bound and matrix-bound basic fibroblast growth factor by bovine capillary endothelial cells. J. Cell Biol. 107:753-759.
31. Goh, K.C., Y.P. Lim, S.H. Ong, C.B. Siak, X. Cao, Y.H. Tan, and G. Guy. 1996. Identification of p90, a prominent tyrosine-phosphorylated protein in fibroblast growth factor-stimulated cells, as 80K-H. J. Biol. Chem. 271:5832-5838.
32. Friesel, R., W.H. Burgess, and T. Maciag. 1989. Heparin-binding growth factor 1 stimulates tyrosine phosphorylation in NIH 3T3 cells. Mol. Cell. Biol. 9: 1857-1865.
33. Ishai-Michaeli, R., A. Eldor, and I. Vlodavsky. 1990. Heparanase activity expressed by platelets, neutrophils and lymphoma cells releases active fibroblast growth factor from extracellular matrix. Cell Regul. 1:833-842.
34. Miao, H.-Q., R. Ishai-Michaeli, R. Atzmon, T. Peretz, and I. Vlodavsky. 1996. Sulfate moieties in the subendothelial extracellular matrix are involved in basic fibroblast growth factor sequestration, dimerization, and stimulation of cell proliferation. J. Biol. Chem. 271:4879-4886.
35. Strom, S.C., and G. Michalopoulos. 1982. Collagen as a substrate for cell growth and differentiation. Methods Enzymol. 82:544-555.
36. Elsdale, T., and J. Bard. 1972. Collagen substrata for studies on cell behavior. J. Cell Biol. 54:626-637.
37. Nicosia, R.F., and A. Ottinetti. 1990. Growth of microvessels in serum-free matrix culture of rat aorta. Lab. Invest. 63:115-122.
38. Roghani, M., A. Mansukhani, P. Dell'Era, P. Bellosta, C. Basilico, D.B. Rifkin, and D. Moscatelli. 1994. Heparin increases the affinity of basic fibroblast growth factor for its receptor but is not required for binding. J. Biol. Chem. 269:3976-3984.
39. Aviezer, D., E. Levy, M. Safran, C. Svahn, E. Buddecke, A. Schmidt, G. David, I. Vlodavsky, and A. Yayon. 1994. Differential structural requirements of heparin and heparan sulfate proteoglycans that promote binding of basic fibroblast growth factor to its receptor. J. Biol. Chem. 269:114-121.
40. Vlodavsky, I., R. Bar-Shavit, G. Korner, and Z. Fuks. 1993. Extracellular matrix-bound growth factors, enzymes and plasma proteins. In Molecular and Cellular Aspects of Basement Membranes. D.H. Rohrbach and R. Timpl, editors. Academic Press Inc., Orlando, FL. 327-343.
41. Pesenti, E., F. Sola, N. Mongelli, M. Grandi, and F. Spreafico. 1992. Suramin prevents neovascularization and tumor growth through blocking of basic fibroblast growth factor activity. Br. J. Cancer. 66:367-372.
42. Mason, I.J. 1994. The ins and outs of fibroblast growth factors. Cell. 78: 547-552.
43. Venkataraman, G., V. Sasisekharan, A.B. Herr, D.M. Ornitz, G. Waksman, C.L. Cooney, R. Langer, and R. Sasisekharan. 1996. Preferential self-association of basic fibroblast growth factor is stabilized by heparin during receptor dimerization and activation. Proc. Natl. Acad. Sci. USA. 93:845-850.
44. Mohammadi, M., I. Dikic, A. Sorokin, W.H. Burgess, M. Jaye, and J. Schlessinger. 1996. Identification of six novel autophosphorylation sites on fibroblast growth factor receptor 1 and elucidation of their importance in receptor activation and signal transduction. Mol. Cell. Biol. 16:977-989.
45. Coughlin, S.R., P.J. Barr, L.S. Cousens, L.J. Fretto, and L.T. Williams. 1988. Acidic and basic fibroblast growth factors stimulate tyrosine kinase activity in vivo. J. Biol. Chem. 263:988-993.
46. Rapraeger, A., A. Krufka, and B.R. Olwin. 1991. Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science (Wash. DC). 252:1705-1708.
47. Gitay-Goren, H., S. Soker, I. Vlodavsky, and G. Neufeld. 1992. Cell surface associated heparin-like molecules are required for the binding of vascular endothelial growth factor (VEGF) to its cell surface receptors. J. Biol. Chem. 267:6093-6098.
48. Guimond, S., M. Maccarana, B.B. Olwin, U. Lindahl, and A.C. Rapraeger. 1993. Activating and inhibitory heparin sequences for FGF-2 (basic FGF). Distinct requirements for FGF-1, FGF-2, and FGF-4. J. Biol. Chem. 268:23906-23914.
49. Sartor, O., C.A. McLellan, C.E. Myers, and M.M. Borner. 1992. Suramin rapidly alters cellular tyrosine phosphorylation in prostate cancer cell lines. J. Clin. Invest. 90:2166-2174.
50. Steinfeld, R., H. van den Berghe, and G. David. 1996. Stimulation of fibroblast growth factor receptor-1 occupancy and signaling by cell surface-associated syndecans and glypican. J. Cell Biol. 133:405-416.
51. Reich-Slotky, R., D. Bonneh-Barkay, E. Shaoul, B. Bluma, C.M. Svahn, and D. Ron. 1994. Differential effect of cell-associated heparan sulfates on the binding of keratinocyte growth factor (KGF) and acidic fibroblast growth factor to the KGF receptor. J. Biol. Chem. 269:32279-32285.
52. Schmidt, A., K. Yoshida, and E. Buddecke. 1992. The antiproliferative activity of arterial heparan sulfate resides in domains enriched with 2-0-sulfated uronic acid residues. J. Biol. Chem. 267:19242-19247.
53. Cushman, M., and S. Kanamathareddy. 1990. Synthesis of the covalent hydrate of the incorrectly assumed structure of aurintricarboxylic acid (ATA). Tetrahedron. 46:1491-1498.