Differential ability of heparan sulfate proteoglycans to assemble the fibroblast growth factor receptor complex in situ

FASEB Journal

Volumn 14, Issue 1, 2000, Pages 137-144

  Chang, Zhen ^a   Meyer, Kristy ^a   Rapraeger, Alan C ^a   Friedl, Andreas ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Basement membrane; Cell signaling; FGF; Skin

Indexed keywords

FIBROBLAST GROWTH FACTOR RECEPTOR; PROTEOHEPARAN SULFATE;

ANIMAL CELL; ARTICLE; BASEMENT MEMBRANE; BINDING AFFINITY; BINDING SITE; CELL GROWTH; GROWTH REGULATION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION;

ANIMALIA;

EID: 0033954312     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fasebj.14.1.137     Document Type: Article

References (45)

1. Klagsbrun, M. (1989) The fibroblast growth factor family-structural and biological properties. Prog. Growth Factor Res. 1, 207-235
2. Goldfarb, M. (1996) Functions of fibroblast growth factors in vertebrate development. Cytokine Growth Factor Rev. 7, 311-325
3. Johnson, D. E., and Williams, L. T. (1993) Structural and functional diversity in the FGF receptor multigene family. Adv. Cancer Res. 60, 1-41
4. 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
5. Yayon, A., Klagsbrun, 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
6. McKeehan, W. L., Wang, F., and Kan, M. (1998) The heparan sulfate-fibroblast growth factor family: diversity of structure and function. Prog. Nucleic Acids Res. Mol. Biol. 59, 135-176
7. 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
8. Kan, M., Wang, F., Xu, J., Crabb, J. W., Hou, J., and McKeehan, W. L. (1993) An essential heparin-binding domain in the fibroblast growth factor receptor kinase. Science 259, 1918-1921
9. Herr, A. B., Ornitz, D. M., Sasisekharan, R., Venkataraman, G., and Waksman, G. (1997) Heparin-induced self-association of fibroblast growth factor-2. Evidence for two oligomerization processes. J. Biol. Chem. 272, 16382-16389
10. Pantoliano, M. W., Horlick, R. A., Springer, B. A., Van Dyk, D. E., Tobery, T., Wetmore, D. R., Lear, J. D., Nahapetian, A. T., Bradley, J. D., and Sisk, W. P. (1994) Multivalent ligand-receptor binding interactions in the fibroblast growth factor system produce a cooperative growth factor and heparin mechanism for receptor dimerization. Biochemistry 33, 10229-10248
11. Springer, B. A., Pantoliano, M. W., Barbera, F. A., Gunyuzlu, P. L., Thompson, L. D., Herblin, W. F., Rosenfeld, S. A., and Book, G. W. (1994) Identification and concerted function of two receptor binding surfaces on basic fibroblast growth factor required for mitogenesis. J. Biol. Chem. 269, 26879-26884
12. Venkataraman, G., Sasisekharan, V., Herr, A. B., Ornitz, D. M., Waksman, G., Cooney, C. L., Langer, R., and Sasisekharan, R. (1996) Preferential self-association of basic fibroblast growth factor is stabilized by heparin during receptor dimerization and activation. Proc. Nail. Acad. Sci. USA 93, 845-850
13. Guimond, S., Maccarana, M., Olwin, B. B., Lindahl, U., and Rapraeger, A. C. (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
14. Soker, S., Goldstaub, D., Svahn, C. M., Vlodavsky, I., Levi, B. Z., and Neufeld, G. (1994) Variations in the size and sulfation of heparin modulate the effect of heparin on the binding of VEGF165 to its receptors. Biochem. Biophys. Res. Commun. 203, 1339-13347
15. Nurcombe, V., Ford, M. D., Wildschut, J. A., and Bartlett, P. F. (1993) Developmental regulation of neural response to FGF-1 and FGF-2 by heparan sulfate proteoglycan. Science 260, 103-106
16. Rapraeger, A. C. (1993) The coordinated regulation of heparan sulfate, syndecans and cell behavior. Curr. Op. Cell Biol. 5, 844-853
17. Rosenberg, R. D., Shworak, N. W., Liu, J., Schwartz, J. J., and Zhang, L. (1997) Heparan sulfate proteoglycans of the cardiovascular system. Specific structures emerge but how is synthesis regulated? J. Clin. Invest. 100, S67-S75
18. Carey, D. J. (1997) Syndecans: multifunctional cell-surface co-receptors. Biochem. J. 327, 1-16
19. Salmivirta, M., Lidholt, K., and Lindahl, U. (1996) Heparan sulfate: a piece of information. FASEB J. 10, 1270-1279
20. Aviezer, D., Hecht, D., Safran, M., Eisinger, M., David, G., and Yayon, A. (1994) Perlecan, basal lamina proteoglycan, promotes basic fibroblast growth factor-receptor binding, mitogenesis, and angiogenesis. Cell 79, 1005-1013
21. Salmivirta, M., Heino, J., and Jalkanen, M. (1992) Basic fibroblast growth factor-syndecan complex at cell surface or immobilized to matrix promotes cell growth. J. Biol. Chem. 267, 17606-17610
22. Filla, M. S., Dam, P., and Rapraeger, A. C. (1998) The cell surface proteoglycan syndecan-1 mediates fibroblast growth factor-2 binding and activity. J. Cell. Physiol. 174, 310-321
23. Bonnehbarkay, D., Shlissel, M., Berman, B., Shaoul, E., Admon, A., Vlodavsky, I., Carey, D. J., Asundi, V. K., Reichslotky, R., and Ron, D. (1997) Identification Of Glypican As a Dual Modulator Of the Biological Activity Of Fibroblast Growth Factors. J. Biol. Chem. 272, 12415-12421
24. Steinfeld, R., Van Den Berghe, H., and David, G. (1996) Stimulation of fibroblast growth factor receptor-1 occupancy and signaling by cell surface-associated syndecans and glypican. J. Cell Biol 133, 405-416
25. Friedl, A., Chang, Z., Tierney, A., and Rapraeger, A. C. (1997) Differential binding of FGF-2 and FGF-7 to basement membrane heparan sulfate: comparison of normal and abnormal human tissues. Am. J. Pathol. 150, 1443-1455
26. 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. 12, 240-247
27. David, G., Bai, X. M., Van der Schueren, B., Cassiman, J. J., and Van den Berghe, H. (1992) Developmental changes in heparan sulfate expression: in situ detection with mAbs. J. Cell Biol 119, 961-975
28. Hoylaerts, M. F., Manes, T., and Millan, J. L. (1997) Mammalian alkaline phosphatases are allosteric enzymes. J. Biol. Chem. 272, 22781-22787
29. Bame, K. J., and Esko, J. D. (1989) Undersulfated heparan sulfate in a Chinese hamster ovary cell mutant defective in heparan sulfate N-sulfotransferase. J. Biol. Chem. 264, 8059-8065
30. Lidholt, K., Weinke, J. L., Kiser, C. S., Lugemwa, F. N., Bame, K. J., Cheifetz, S., Massague, J., Lindahl, U., and Esko, J. D. (1992) A single mutation affects both N-acetylglucosaminyl-transferase and glucuronosyltransferase activities in a Chinese hamster ovary cell mutant defective in heparan sulfate biosynthesis. Proc. Natl. Acad. Sci. USA 89, 2267-2271
31. Ortega, S., Ittmann, M., Tsang, S. H., Ehrlich, M., and Basilico, C. (1998) Neuronal defects and delayed wound healing in mice lacking fibroblast growth factor 2. Proc. Natl. Acad. Sci. USA 95, 5672-5677
32. Krufka, A., Guimond, S., and Rapraeger, A. C. (1996) Two hierarchies of FGF-2 signaling in heparin: mitogenic stimulation and high-affinity binding/receptor transphosphorylation. Biochemistry 35, 11131-11141
33. Folkman, J., Klagsbrun, M., Sasse, J., Wadzinski, M., Ingber, D., and Vlodavsky, I. (1988) A heparin-binding angiogenic protein-basic fibroblast growth factor-is stored within basement membrane. Am. J. Pathol. 130, 393-400
34. Risau, W. (1996) What, if anything, is an angiogenic factor? Cancer Metast. Rev. 15, 149-151
35. Rahmoune, H., Chen, H. L., Gallagher, J. T., Rudland, P. S., and Fernig, D. G. (1998) Interaction of heparan sulfate from mammary cells with acidic fibroblast growth factor (FGF) and basic FGF. Regulation of the activity of basic FGF by high and low affinity binding sites in heparan sulfate. J. Biol. Chem. 273, 7303-7310
36. Turnbull, J. E., Fernig, D. G., Ke, Y., Wilkinson, M. C., and Gallagher, J. T. (1992) Identification of the basic fibroblast growth factor binding sequence in fibroblast heparan sulfate. J. Biol. Chem. 267, 10337-10341
37. Habuchi, H., Kobayashi, M., and Kimata, K. (1998) Molecular characterization and expression of heparan-sulfate 6-sulfotransferase. Complete cDNA cloning in human and partial cloning in Chinese hamster ovary cells. J. Biol. Chem. 273, 9208-9213
38. Kobayashi, M., Habuchi, H., Yoneda, M., Habuchi, O., and Kimata, K. (1997) Molecular cloning and expression of Chinese hamster ovary cell heparan-sulfate 2-sulfotransferase. J. Biol. Chem. 272, 13980-13985
39. Brickman, Y. G., Ford, M. D., Gallagher, J. T., Nurcombe, V., Bartlett, P. F., and Turnbull, J. E. (1998) Structural modification of fibroblast growth factor-binding heparan sulfate at a determinative stage of neural development. J. Biol. Chem. 273, 4350-4359
40. Jayson, G. C., Lyon, M., Paraskeva, C., Turnbull, J. E., Deakin, J. A., and Gallagher, J. T. (1998) Heparan sulfate undergoes specific structural changes during the progression from human colon adenoma to carcinoma in vitro. J. Biol. Chem. 273, 51-57
41. Safaiyan, F., Lindahl, U., and Salmivirta, M. (1998) Selective reduction of 6-O-sulfation in heparan sulfate from transformed mammary epithelial cells. Eur. J. Biochem. 252, 576-582
42. Li, J., Hagner-McWhirter, A., Kjellen, L., Palgi, J., Jalkanen, M., and Lindahl, U. (1997) Biosynthesis of heparin/heparan sulfate. cDNA cloning and expression of D-glucuronyl C5-epimerase from bovine lung. J. Biol. Chem. 272, 28158-28163
43. Subramanian, S. V., Fitzgerald, M. L., and Bernfield, M. (1997) Regulated shedding of syndecan-1 and -4 ectodomains by thrombin and growth factor receptor activation. J. Biol. Chem. 272, 14713-14720
44. Kato, M., Wang, H., Kainulainen, V., Fitzgerald, M. L., Ledbetter, S., Ornitz, D. M., and Bernfield, M. (1998) Physiological degradation converts the soluble syndecan-1 ectodomain from an inhibitor to a potent activator of FGF-2. Nat. Med. 4, 691-697
45. Joseph, S. J., Ford, M. D., Barth, C., Portbury, S., Bartlett, P. F., Nurcombe, V., and Greferath, U. (1996) A proteoglycan that activates fibroblast growth factors during early neuronal development is a perlecan variant. Development 122, 3443-3452