Endothelial proteoglycans inhibit bFGF binding and mitogenesis

Journal of Cellular Physiology

Volumn 172, Issue 2, 1997, Pages 209-220

  Forsten, Kimberly E ^a   Courant, Natalie A ^a   Nugent, Matthew A ^b  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR; HEPARAN SULFATE; HEPARIN; PROTEOGLYCAN;

ANIMAL CELL; AORTA; ARTICLE; BINDING AFFINITY; CATTLE; CELL PROLIFERATION; CELL SURFACE; MITOGENESIS; NONHUMAN; PRIORITY JOURNAL; VASCULAR DISEASE; VASCULAR ENDOTHELIUM; VASCULAR SMOOTH MUSCLE;

ANIMALS; CATTLE; CELL DIVISION; CHEMICAL FRACTIONATION; ENDOTHELIUM, VASCULAR; FIBROBLAST GROWTH FACTOR 2; MITOSIS; MUSCLE, SMOOTH, VASCULAR; PROTEOGLYCANS;

ANIMALIA; BOS TAURUS;

EID: 0030752271     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4652(199708)172:2<209::AID-JCP8>3.0.CO;2-S     Document Type: Article

References (68)

1. Arakawa, T., Wen, J., and Philo, J.S. (1994). Stoichiometry of heparin binding to basic fibroblast growth factor. Arch. Biochem. Biophys., 305:267-273.
2. Aviezer, D., Hecht, D., Safran, M., Elsinger, M., David, G., and Yayon, A. (1994) Perlecan, basai lamina proteoglycan, promotes basic fibroblast growth factor-receptor binding, mitogenesis, and angiogenesis. Cell, 79:1005-1013.
3. Bassols, A., and Massague, J. (1988) Transforming growth factor b regulates the expression and structure of extracellular matrix chondroitin/dermatan sulfate proteoglycans. J. Biol. Chem., 263:30393045.
4. Benitz, W.E., Kelley, R.T., Anderson, C.M., Lorant, D.E., and Bernfield, M. (1990) Endothelial heparan sulfate proteoglycan. I. Inhibitory effects on smooth muscle cell proliferation. Am. J. Respir. Cell Mol. Biol., 2:13-24.
5. Bjornsson, T.D., Dryjski, D.M., Tluezek, J., Mennie, R., Ronan, J., Mellin, T.N., and Thomas, K.A. (1991) Acidic fibroblast growth factor promotes vascular repair. Proc. Natl. Acad. Sei. U.S.A., 55:8661-8665.
6. Brown, K.J., Hendry, I.A., and Parish, C.R. (1995) Evidence that carboxyl-reduced heparin fails to potentiate acidic fibroblast growth factor activity due to an inability to interact with cell surface heparin receptors. Exp. Cell Res., 217:132-139.
7. Castellot, J.J., Addonizio, M.L., Rosenberg, R.D., and Karnovsky, M.J. (1981) Cultured endothelial cells produce a heparin-like inhibitor of smooth muscle cell growth. J. Cell Biol., 30:372-379.
8. Castellot, J.J., Rosenberg, R.D., and Karnovsky, M.J. (1984) Endothelium, heparin, and the regulation of vascular smooth muscle cell growth. Biology of Endothelial Cells. Jaffe, E.A. (Ed.) Martinus Nijhoff, Boston.
9. Castellot, J.J., Wong, K., Herman, B., Hoover, R.L., Albertini, D.F., Wright, T.C., Caleb, B.L., and Karnovsky, M.J. (1985) Binding and internalization of heparin by vascular smooth muscle cells. J. Cell. Physiol., 723:13-20.
10. Chamberlain, J.P. (1979) Flourographic detection of radioactivity in polyacrylamide gels with the water soluble four sodium salicylate. Anal. Biochem., 95:132-135.
11. Clowes, A.W., and Karnovsky, M.J. (1977) Suppression by heparin of smooth muscle cell proliferation in injured arteries. Nature (Lond.), 265:625-626.
12. Cook, P.W., Ashton, N.M., Karkaria, C.E., Siess, B.C., and Shipley, G.D. (1995) Differential effects of a heparin antagonist (hexadimethrine) or chlorate on amphiregulin, basic fibroblast growth factor, and heparin-binding EGF-like growth factor activity. J. Cell. Physiol., 763:418-429.
13. Dodge, A.B., Lu, X., and D'Amore, P.A. (1993) Density-dependent endothelial cell production of an inhibitor of smooth muscle cell growth. J. Cell. Biochem., 53:21-31.
14. Edelman, E.R., and Karnovsky, M.J. (1994) Contrasting effects of the intermittent and continuous administration of heparin in experimental restenosis. Circulation, 89:110-176.
15. Edelman, E.R., Nugent, M.A., Smith, L.T., and Karnovsky, M.J. (1992) Basic fibroblast growth factor enhances the coupling of intimai hyperplasia and proliferation of vasa vasorum in injured rat arteries. J. Clin. Invest., 59:465-473.
16. Edelman, E.R., Nugent, M.A., and Karnovsky, M.J. (1993) Perivascular and intravenous administration of basic fibroblast growth factor: Vascular and solid organ deposition. Proc. Natl. Acad. Sei. U.S.A., 90:1513-1517.
17. Fannon, M., and Nugent, M.A. (1996) FGF binds its receptors, is internalized and stimulates DNA synthesis in Balb/c3T3 cells in the absence of heparan sulfates. J. Biol. Chem., 277:17949-17956.
18. Farndale, R.W., Buttle, D.J., and Barrett, A.J. (1986) Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim. Biophys. Acta, 553:173-177.
19. Fishman, J.A., Ryan, G.B., and Karnovsky, M.J. (1975) Endothelial regeneration in the rat carotid artery and significance of endothelial denudation in the pathogenesis of myointimal thickening. Lab. Invest. 32:339-351.
20. Fritze, L., Reilly, C., and Rosenberg, R. (1985) An antiproliferative heparan sulfate species produced by postconfluent smooth muscle cells. J. Cell. Biol., 700:1041-1049.
21. Gimbrone, M.A. (1976) Culture of vascular endothelium. Prog. Hemost. Thromb., 3:1-28.
22. Hardingham, T.E., and Fosang, A.J. (1992) Proteoglycans: many forms and many functions. FASEB J., 6:861-870.
23. Hovingh, P., Piepkorn, M., and Linker, A. (1993) Differentially expressed patterns of glycosaminoglycan structure in heparan sulfate proteoglycans and free chains. Eur. J. Biochem., 277:777-779.
24. lozzo, R.V., Cohen, I.R., Grassei, S., and Murdoch, A.D. (1994) The biology of perlecan: the multifaceted heparan sulphate proteoglycan of basement membranes and pericellular matrices. Biochem. J., 302:625-639.
25. Ip, J.H., Fuster, V., Badimon, L., Badimon, J., Taubman, M.B., and Chesebro, J.H. (1990) Syndromes of accelerated atherosclerosis: role of vascular injury and smooth muscle proliferation. J. Am. Coll. Cardiol., 75:1667-1687.
26. Ishai-Michaeli, R., Svahn, C.M., Weber, M., Chajek-Shaul, T., Korner, G., Ekre, H.-P., and Vlodavsky, I. (1992) Importance of size and sulfation of heparin in release of basic fibroblast growth factor from the vascular endothelium and extracellular matrix. Biochemistry, 37:2080-2088.
27. Jackson, R.L., Busch, S.J., and Cardin, A.D. (1991) Glycosaminoglycans: molecular properties, protein interactions, and role in physiological processes. Physiol. Rev., 77:481-539.
28. Karnovsky, M.J., Castellot, J.J., Costa, G.M., and Rosenberg, R.D. (1985) Effects of heparin on vascular smooth muscle cell proliferation. Interaction of Platelets with the Vessel Wall. Dates, J.A., Hawiger, J., and Ross, R. Williams and Wilkens, Baltimore (Eds.). 147163.
29. Kalo, M., Wang, H., Bernfield, M., Gallagher, J.T., and Turnbull, J.E. (1994) Cell surface syndecan-1 on distinct cell types differs in fine structure and ligand binding of its heparan sulfate chains. J. Biol. Chem., 269:18881-18890.
30. Klagsbrun, M., and Baird, A. (1991) A dual receptor system is required for basic fibroblast growth factor activity. Cell, 67:229:-231.
31. Klagsbrun, M., and Edelman, E.R. (1989) Biological and biochemical properties of fibroblasts growth factors-Implications for the pathogenesis of atherosclerosis. Arteriosclerosis, 9:269-278.
32. Knauer, D.J., Wiley, H.S., and Cunningham, D.D. (1984) Relationship between epidermal growth factor receptor occupancy and mitogenic response. J. Biol. Chem., 259:5623-5631.
33. Letourneur, D., Caleb, B.L., and Castellot, J.J. (1995a) Heparin binding, internalization, and metabolism in vascular smooth muscle cells: I. Upregulation of heparin binding correlates with antiproliferative activity. J. Cell. Physiol., 765:676-686.
34. Letourneur, D., Caleb, B.L., and Castellot, J.J. (1995W Heparin binding, internalization, and metabolism in vascular smooth muscle cells: II. Degradation and secretion in sensitive and resistant cells. J. Cell Physiol., 765:687-695.
35. Lindner, V., and Reidy, M.A. (1991) Proliferation of smooth muscle cells after vascular injury is inhibited by an antibody against basic fibroblast growth factor. Proc. Natl. Acad. Sei. U.S.A., 88:3739-3743.
36. Lindner, V., Lappi, D.A., Baird, A., Majack, R.A., and Reidy, M.A. (1991) Role of basic fibroblast growth factor in vascular lesion formation. Circ. Res., 68:106-113.
37. Lindner, V., Oison, N.E., Clowes, A.W., and Reidy, M.A. (1992) Inhibition of smooth muscle cell proliferation in injured rat arteries interaction of heparin with basic fibroblast growth factor. J. Clin. Invest., 90:2044-2049.
38. Lowe-Krentz, L.J., Thompson, K., and Patton II, W.A. (1992) Heparin release and nonreleasable forms of heparan sulfate proteoglycan are found on the surfaces of cultured porcine aortic endothelial cells. Mol. Cell. Biochem., 709:51-60.
39. Mason, I.J. (1994) The ins and outs of fibroblast growth factors. Cell, 75:547-552.
40. McBride, W., Lange, R.A., and Hillis, L.D. (1988) Restenosis after successful coronary angioplasty: pathophysiology and prevention. N. Engl. J. Med., 378:1734-1738.
41. Nathan, A., Nugent, M.A., and Edelman, E.R. (1995) Tissue engineered perivascular endothelial cell implants regulate vascular injury. Proc. Natl. Acad. Sei. USA, 92:8130-8134.
42. Noonan, D.M., Fülle, A., Valente, P., Cai, S., Horigan, E., Sasaki, M., Yamada, Y., and Hassell, J.R. (1991) The complete sequence of perlecan, a basement membrane heparan sulfate proteoglycan, reveals extensive similarity with laminin A chain, low density lipoprotein-receptor, and the neural cell adhesion molecule. J. Biol. Chem., 266:22939-22947.
43. Nugent, M.A., and Edelman, E.R. (1992) Kinetics of basic fibroblast growth factor binding to its receptor and heparan sulfate proteoglycan: A mechanism for cooperativity. Biochemistry, 37:8876-8883.
44. Nugent, M.A., Karnovsky, M.J., and Edelman, E.R. (1993) Vascular cell-derived heparan sulfate shows coupled inhibition of basic fibroblast growth factor binding and mitogenesis in vascular smooth muscle cells. Circ. Res., 73:1051-1060.
45. Nugent, M.A., Dowd, C.J., Ryan, W.J., Courant, N.A., and Forsten, K.E. (1996) Endothelial cell proteoglycans inhibit bFGF binding, mitogenesis and angiogenesis. Invest. Ophthal. Vis. Sei., 37:S88.
46. Ohno, H., Blackwell, J., Jamieson, A.M., Carrino, D.A., and Caplan, A.I. (1986) Calibration of the relative molecular mass of proteoglycan subunit by column chromatography on Sepharose CL-2B. Biochem. J., 235:553-557.
47. O'Keefe, J.H., and Hartzler, G.O. (1989) Restenosis after coronary angioplasty. J. Invest. Cardiol., 7:109-122.
48. Olwin, B.B., and Rapraeger, A. (1992) Repression of myogenic differentiation by aFGF, bFGF, and K-FGF is dependent on cellular heparan sulfate. J. Cell Biol., 778:631-639.
49. Ornitz, D.M., Yayon, A., Flanagan, J.G., Svahn, C.M., Levi, E., and Leder, P. (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., 72:240-247.
50. Ornitz, D.M., Herr, A.B., Nilsson, M., Westman, J., Svahn, C.-M., and Waksman, G. (1995) FGF binding and FGF receptor activation by synthetic heparan-derived di- and trisaccharides. Science, 268:432-436.
51. Piepkorn, M., Hovingh, P., and Linker, A. (1991) Proteoglycan and glycosaminoglycan free chain expression in keratinocytes, endothelium, and mesenchymal cells. Biochem. Biophys. Res. Commun., 779:1281-1288.
52. Prestrelski, S.J., Fox, G.M., and Arakawa, T. (1992) Binding ofheparin to basic fibroblast growth factor induces a conformational change. Arch. Biochem. Biophys., 293:314-319.
53. Rapraeger, A.C., Krufka, A., and Olwin, B.B. (1991) Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science, 252:1705-1708.
54. Roghani, M., Mansukhani, A., Dell'Era, P., Bellosta, P., Basilico, C., Rifkin, D.B., and Moscatelli, D. (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.
55. Ross, R. (1971) Smooth muscle cells. II: Growth of smooth muscle in culture and formation of elastic fibers. J. Cell Biol., 50:172-186.
56. Ruoslahti, E., and Yamaguchi, Y. (1991) Proteoglycans as modulators of growth factor activities. Cell, 64:867-869.
57. Sanderson, R.D., Turnbull, J.E., Gallagher, J.T., and Lander, A.D. (1994) Fine structure of heparan sulfate regulates syndecan-1 function and cell behavior. J. Biol. Chem., 269:13100-13106.
58. Schwartz, S.M., Stemerman, M.B., and Benditt, E.P. (1975) The aortic intima II. Repair of the aortic lining after mechanical denudation. Am. J. Pathol., 87:15-42.
59. Shirotani, M., Yui, Y., and Kawai, C. (1993) Restenosis after coronary angioplasty: Pathogenesis of neointimal thickening initiated by endothelial loss. Endothelium, 7:5-22.
60. Spivak-Kroizman, T., Lemmon, M.A., Dikic, I., Ladbury, J.E., Pinchasi, D., Huang, J., Jaye, M., Crumley, G., Schlessinger, J., and Lax, I. (1994) Heparin-induced oligomerization of FGF molecules is responsible for FGF receptor dimerization, activation, and cell proliferation. Cell, 79:1015-1024.
61. Takahashi, J.A., Fukumoto, M., Kozai, Y., Ito, N., Oda, Y., Kikuchi, H., and Hatanaka, M. (1991) Inhibition of cell growth and tumorigenesis of human glioblastoma cells by a neutralizing antibody against human basic fibroblast growth factor. FEBS., 288:65-71.
62. Turnbull, J.E., and Gallagher, J.T. (1993) Heparan sulphate: Functional role as a modulator of fibroblast growth factor activity. Biochem. Soc. Trans., 27:477-482.
63. Vijayagopal, P., Ciolino, H.P., and Berenson, G.S. (1992) Endothelial cell-conditioned medium modulates the synthesis and structure of proteoglycans in vascular smooth muscle cells. Biochim. Biophys. Acta, 7735:129-140.
64. Walker, A., Turnbull, J.E., and Gallagher, J.T. (1994) Specific heparan sulfate saccharides mediate the activity of basic fibroblast growth factor. J. Biol. Chem., 269:931-935.
65. Wasteson, A. (1971) A method for the determination of the molecular weight and molecular-weight distribution of chondroitin sulfate. J. Chromatogr., 59:87-97.
66. Whitelock, J.M., Murdoch, A.D., lozzo, R.V., and Underwood, P.A. (1996) The degradation of human endothelial cell-derived perlecan and release of bound basic fibroblast growth factor by stromelysin, collagenase, plasmin, and heparanases. J. Biol. Chem., 277:1007910086.
67. Yanagishita, M., and Hascall, V.C. (1992) Cell surface heparan sulfate proteoglycans. J. Biol. Chem., 267:9451-9454.
68. Yayon, A., Klagsburn, M., Esko, J.D., Leder, P., and Ornitz, D.M. (1991) Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell, 64:841-848.