FGFs, heparan sulfate and FGFRs: Complex interactions essential for development

BioEssays

Volumn 22, Issue 2, 2000, Pages 108-112

  Ornitz, David M ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR RECEPTOR; HEPARAN SULFATE; HEPARIN;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; DROSOPHILA; GROWTH, DEVELOPMENT AND AGING; PHYSIOLOGY; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION;

ANIMALS; DROSOPHILA; FIBROBLAST GROWTH FACTORS; HEPARIN; HEPARITIN SULFATE; MODELS, BIOLOGICAL; RECEPTORS, FIBROBLAST GROWTH FACTOR; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION;

ANIMALIA;

EID: 0033951768     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1521-1878(200002)22:2<108::AID-BIES2>3.0.CO;2-M     Document Type: Article

References (49)

1. Lin XH, Buff EM, Perrimon N, Michelson AM. Heparan sulfate proteoglycans are essential for FGF receptor signaling during Drosophila embryonic development. Development 1999;126:3715-3723.
2. Kurima K, Warman ML, Krishnan S, Domowicz M, Krueger RC Jr, Deyrup A, Schwartz NB. A member of a family of sulfate-activating enzymes causes murine brachymorphism [published erratum appears in Proc Natl Acad Sci USA 1998 Sep 29;95(20):12071]. Proc Natl Acad Sci USA 1998;95:8681-8615.
3. Satoh H, Susaki M, Shukunami C, Iyama K, Negoro T, Hiraki Y. Functional analysis of diastrophic dysplasia sulfate transporter. Its involvement in growth regulation of chondrocytes mediated by sulfated proteoglycans. J Biol Chem 1998;273:12307-12315.
4. Bullock SL, Fletcher JM, Beddington RS, Wilson VA. Renal agenesis in mice homozygous for a gene trap mutation in the gene encoding heparan sulfate 2-sulfotransferase. Genes Dev 1998;12:1894-1906.
5. Szebenyi G, Fallon JF. Fibroblast growth factors as multifunctional signaling factors. Int Rev Cyt 1999;185:45-106.
6. Wilkie AOM, Morriss-Kay GM, Jones EY, Heath JK. Functions of fibroblast growth factors and their receptors. Curr Biol 1995;5:500-507.
7. Naski MC, Ornitz DM. FGF signaling in skeletal development. Front Biosci 1998;3:D781-D794.
8. Martin GR. The roles of FGFs in the early development of vertebrate limbs. Genes Dev 1998;12:1571-1586.
9. Klambt C, Glazer L, Shilo BZ. breathless, a Drosophila FGF receptor homolog, is essential for migration of tracheal and specific midline glial cells. Genes Dev 1992;6:1668-1678.
10. Lee T, Hacohen N, Krasnow M, Montell DJ, Steinberger D, Reinhartz T, Unsold R, Muller U. Regulated breathless receptor tyrosine kinase activity required to pattern cell migration area branching in the drosophila tracheal system. Genes Dev 1996;10:2912-2921.
11. Sutherland D, Samakovlis C, Krasnow MA. branchless encodes a Drosophila FGF homolog that controls tracheal cell migration and the pattern of branching. Cell 1996;87:1091-1101.
12. Michelson AM, Gisselbrecht S, Zhou Y, Baek KH, Buff EM. Dual functions of the heartless fibroblast growth factor receptor in development of the drosophila embryonic mesoderm. Dev Genet 1998;22:212-229.
13. Beiman M, Shilo BZ, Volk T. Heartless, a Drosophila FGF receptor homolog, is essential for cell migration and establishment of several mesodermal lineages. Genes Dev 1996;10:2993-3002.
14. Gisselbrecht S, Skeath JB, Doe CQ, Michelson AM. Heartless encodes a fibroblast growth factor receptor [Dfr1/Dfgf-r2) involved in the directional migration of early mesodermal cells in the drosophila embryo. Genes Dev 1996; 10:3003-3017.
15. DeVore DL, Horvitz HR, Stern MJ. An FGF receptor signaling pathway is required for the normal cel migrations of the sex myoblasts in C. elegans hermaphrodites. Cell 1995;83:611-620.
16. Burdine RD, Branda CS, Stern MJ. EGL-17(FGF expression coordinates the attraction of the migrating sex myoblasts with vulval induction in C. elegans. Development 1998;125:1083-1093.
17. Burdine RD, Chen EB, Kwok SF, Stern MJ. egl-17 encodes an invertebrate fibroblast growth factor family member required specifically for sex myoblast migration in Caenorhabditis elegans. Proc Natl Acad Sci USA 1997;94:2433-2437.
18. Faham S, Linhardt RJ, Rees DC. Diversity does make a difference: fibroblast growth factor-heparin interactions. Curr Opin Struct Biol 1998;8:578-586
19. Plotnikov AN, Schlessinger J, Hubbard SR, Mohammadi M. Structural basis for FGF receptor dimerization and activation. Cell 1999;98:641-650.
20. Baird A, Schubert D, Ling N, Guillemn R. Receptor-and heparin-binding domains of basic fibroblast growth factor. Proc Natl Acad Sci USA 1988;85: 2324-2328.
21. Eriksson AE, Cousens LS, Weaver LH, Matthews BW. Three-dimensional structure of human basic fibroblast growth factor. Proc Natl Acad Sci USA 1991;88:3441-3445.
22. Moscatelli D. 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 plasmnogen activator production oy bovine capillary endothelial cells. J Cell Physiol 1987;131:123-130.
23. Flaumenhaft R, Moscatelli D, Rifkin DB. Heparin and heparan su fate increase the radius of diffusion and action of basic fibroblast growth factor. J Cell Biol 1990;111:1651-1659.
24. Mach H, Volkin DB, Burke CJ, Middaugh CR, Linhardt RJ, Fromm JR, Loganathan D. Nature of the interaction of heparin with acidic fibroblast growth factor. Biochemistry 1993;32:5480-5489.
25. Herr AB, Ornitz DM, Sasisekharan R, Venkataraman G, Waksman G. Heparin-induced self-association of fibroblast growth factor-2. Evidence for two oligomerization processes. J Biol Chem 1997;272:16382-16389.
26. Moy FJ, Safran M, Seddon AP, Kitchen D, Bohlen P, Aviezer D, Yayon A, Powers R. Properly oriented heparin-decasaccharide-induced dimers are the biologically active form of basic fibroblast growth factor Biochemistry 1997; 36:4782-4791.
27. DiGabriele AD, Lax I, Chen DI, Svahn CM, Jaye M, Schtessinger J, Hendrickson WA. Structure of a heparin-linked biologically active dimer of fibroblast growth factor. Nature 1998;393:812-817.
28. Waksman G, Herr AB. New insights into heparin-induced FGF oligomerization [news]. Nat Struct Biol 1998;5:527-530.
29. Rapraeger AC, Krufka A, Olwin BB. Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science 1991;252: 1705-1708.
30. Yayon A, Klagsbrun M, Esko JD, Leder P, Ornitz DM. Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 1991;64:841-848.
31. Ornitz DM, Yayon A, Flanagan JG, Svahn CM, Levi E, Leder P. 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;12:240-247.
32. McKeehan WL, Wang F, Kan M. The heparan sulfate-fibroblast growth factor family: diversity of structure and function. Prog Nucleic Acid Res Mol Biol 1998;59:135-176.
33. Johnson DE, Williams LT. Structural and functional diversity in the FGF receptor multigene family. Adv Cancer Res 1993;60:1-41.
34. Kan M, Wang F, Xu J, Crabb JW, Hou J, McKeehan WL. An essential heparin-binding domain in the fibroblast growth factor receptor kinase. Science 1993; 259:1918-1921.
35. Chellaiah A, Yuan W, Chellaiah M, Ornitz DM. Mapping ligand binding domains in chimeric FGF receptor molecules: multiple domains determine ligand binding specificity. J Biol Chem 2000; in press.
36. 2-terminal immunoglobulin-like loop 1 in the ectodomain of the fibroblast growth factor (FGF) receptor 1 lowers affinity for both heparin and FGF-1. J Biol Chem 1995;270:10231-10235.
37. Duan D-SR, Werner S, Williams LT. A naturally occurring secreted form of fibroblast growth factor (FGF) receptor 1 binds basic FGF in preference over acidic FGF. J Biol Chem 1992;267:16076-16080.
38. Casu B. Structure and biological activity of heparin. Adv Carbohydr Chem Biochem 1985;43:51-134.
39. Lindahl U. Biosynthesis of heparin and related polysaccharides. In: Land DA, Lindahl U, editors. Heparin: chemical and biological properties, clinical applications. London: Edward Arnold; 1989. p 159-189.
40. Pye DA, Vives RR, Turnbull JE, Hyde P, Gallagher JT. Heparan sulfate oligosaccharides require 6-O-sulfation for promotion of basic fibroblast growth factor mitogenic activity. J Biol Chem 1998;273:22936-22942.
41. Guimond S, Maccarana M, Olwin BB, Lindahl U, Rapraeger AC. Activating and inhibitory heparin sequences for FGF-2 (basic FGF): distinct requirements for FGF-1, FGF-2 and FGF-4. J Biol Chem 1993;268:23906-23914.
42. Rapraeger AC. In the clutches of proteoglycans: how does heparan sulfate regulate FGF binding? Chem Biol 1995;2:645-649.
43. Pye DA, Gallagher JT. Monomer complexes of basic fibroblast growth factor and heparan sulfate oligosaccharides are the minimal functional unit for cell activation. J Biol Chem 1999;274:13456-13461.
44. Hsu YR, Nybo R, Sullivan JK, Costigan V, Spahr CS, Wong C, Jones M, Pentzer AG, Crouse JA, Pacifici RE et al. Heparin is essential for a single keratinocyte growth factor molecule to bind and form a complex with two molecules of the extracellular domain of its receptor. Biochemistry 1999;38: 2523-2534.
45. Herr AB, Xu J, Ornitz DM, Waksman G. Molecular basis for receptor dimerization and activation of signaling by FGF2. In preparation.
46. Zhan W, Hu W, Friesel R, Maciag T. Long term growth factor exposure and differential tyrosine phosphorylation are required for DNA synthesis in BALB/c 3T3 cells. J Biol Chem 1993;268:9611-9620.
47. Roghani M, Mansukhani A, Dell'Era P, Bellosta P, Basilico C, Rifkin DB, Moscatelli D. Heparin increases the affinity of basic fibroblast growth factor for its receptor but is not required for binding. J Biol Chem 1994;269:3976-3984.
48. Aviezer D, Safran M, Yayon A. Heparin differentially regulates the interaction of fibroblast growth factor-4 with FGF receptors 1 and 2. Biochem Biophys Res Comm 1999;263:621-626.
49. Lyon M, Gallagher JT. Bio-specific sequences and domains in heparan sulphate and the regulation of cell growth and adhesion [Review]. Matrix Biol 1998;17:485-493.