• 1
    Itoh N & Ornitz DM (2004) Evolution of the Fgf and Fgfr gene families. Trends Genet 20, 563569.
  • 2
    Oulion S, Bertrand S & Escriva H (2012) Evolution of the FGF gene family. Int J Evol Biol 2012, doi:10.1155/2012/298147.
  • 3
    Trueb B (2011) Biology of FGFRL1, the fifth fibroblast growth factor receptor. Cell Mol Life Sci 68, 951964.
  • 4
    Beenken A & Mohammadi M (2009) The FGF family: biology, pathophysiology and therapy. Nat Rev Drug Discovery 8, 235253.
  • 5
    Grose R & Dickson C (2005) Fibroblast growth factor signaling in tumorigenesis. Cytokine Growth Factor Rev 16, 179186.
  • 6
    Presta M, Dell'Era P, Mitola S, Moroni E, Ronca R & Rusnati M (2005) Fibroblast growth factor/fibroblast growth factor receptor system in angiogenesis. Cytokine Growth Factor Rev 16, 159178.
  • 7
    Plotnikov AN, Hubbard SR, Schlessinger J & Mohammadi M (2000) Crystal structures of two FGF–FGFR complexes reveal the determinants of ligand–receptor specificity. Cell 101, 413424.
  • 8
    Plotnikov AN, Schlessinger J, Hubbard SR & Mohammadi M (1999) Structural basis for FGF receptor dimerization and activation. Cell 98, 641650.
  • 9
    Powell AK, Fernig DG & Turnbull JE (2002) Fibroblast growth factor receptors 1 and 2 interact differently with heparin/heparan sulfate. Implications for dynamic assembly of a ternary signaling complex. J Biol Chem 277, 2855428563.
  • 10
    Pellegrini L, Burke DF, von Delft F, Mulloy B & Blundell TL (2000) Crystal structure of fibroblast growth factor receptor ectodomain bound to ligand and heparin. Nature 407, 10291034.
  • 11
    Schlessinger J, Plotnikov AN, Ibrahimi OA, Eliseenkova AV, Yeh BK, Yayon A, Linhardt RJ & Mohammadi M (2000) Crystal structure of a ternary FGF–FGFR–heparin complex reveals a dual role for heparin in FGFR binding and dimerization. Mol Cell 6, 743750.
  • 12
    Lin X, Buff EM, Perrimon N & Michelson AM (1999) Heparan sulfate proteoglycans are essential for FGF receptor signaling during Drosophila embryonic development. Development 126, 37153723.
  • 13
    Duchesne L, Octeau V, Bearon RN, Beckett A, Prior IA, Lounis B & Fernig DG (2012) Transport of fibroblast growth factor 2 in the pericellular matrix is controlled by the spatial distribution of its binding sites in heparan sulfate. PLoS Biol 10, e1001361.
  • 14
    Ori A, Wilkinson MC & Fernig DG (2008) The heparanome and regulation of cell function: structures, functions and challenges. Front Biosci 13, 43094338.
  • 15
    Rudd TR & Yates EA (2012) A highly efficient tree structure for the biosynthesis of heparan sulfate accounts for the commonly observed disaccharides and suggests a mechanism for domain synthesis. Mol BioSyst 8, 14991506.
  • 16
    Kreuger J, Spillmann D, Li JP & Lindahl U (2006) Interactions between heparan sulfate and proteins: the concept of specificity. J Cell Biol 174, 323327.
  • 17
    Xu R, Ori A, Rudd TR, Uniewicz KA, Ahmed YA, Guimond SE, Skidmore MA, Siligardi G, Yates EA & Fernig DG (2012) Diversification of the structural determinants of fibroblast growth factor–heparin interactions: implications for binding specificity. J Biol Chem 287, 4006140073.
  • 18
    Guimond SE, Turnbull JE & Yates EA (2006) Engineered bio-active polysaccharides from heparin. Macromol Biosci 6, 681686.
  • 19
    Ornitz DM, Xu J, Colvin JS, McEwen DG, MacArthur CA, Coulier F, Gao G & Goldfarb M (1996) Receptor specificity of the fibroblast growth factor family. J Biol Chem 271, 1529215297.
  • 20
    Allen BL & Rapraeger AC (2003) Spatial and temporal expression of heparan sulfate in mouse development regulates FGF and FGF receptor assembly. J Cell Biol 163, 637648.
  • 21
    Van Mieghem P (2010) Graph Spectra for Complex Networks. Cambridge University Press, Cambridge.
  • 22
    Ori A, Wilkinson MC & Fernig DG (2011) A systems biology approach for the investigation of the heparin/heparan sulfate interactome. J Biol Chem 286, 1989219904.
  • 23
    Zhang X, Ibrahimi OA, Olsen SK, Umemori H, Mohammadi M & Ornitz DM (2006) Receptor specificity of the fibroblast growth factor family. The complete mammalian FGF family. J Biol Chem 281, 1569415700.
  • 24
    Hoory S, Linial N & Wigderson A (2006) Expander graphs and their applications. Bull Am Math Soc 43, 439561.
  • 25
    Ornitz DM & Itoh N (2001) Fibroblast growth factors. Genome Biol 2, reviews3005.1-reviews3005.12.
  • 26
    Ori A, Free P, Courty J, Wilkinson MC & Fernig DG (2009) Identification of heparin-binding sites in proteins by selective labeling. Mol Cell Proteomics 8, 22562265.
  • 27
    King N, Westbrook MJ, Young SL, Kuo A, Abedin M, Chapman J, Fairclough S, Hellsten U, Isogai Y, Letunic I, et al. (2008) The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 451, 783788.
  • 28
    Burdine RD, Chen EB, Kwok SF & Stern MJ (1997) egl-17 encodes an invertebrate fibroblast growth factor family member required specifically for sex myoblast migration in Caenorhabditis elegans. Proc Natl Acad Sci USA 94, 24332437.
  • 29
    Roubin R, Naert K, Popovici C, Vatcher G, Coulier F, Thierry-Mieg J, Pontarotti P, Birnbaum D, Baillie D & Thierry-Mieg D (1999) let-756, a C. elegans fgf essential for worm development. Oncogene 18, 67416747.
  • 30
    Gryzik T & Muller HA (2004) FGF8-like1 and FGF8-like2 encode putative ligands of the FGF receptor Htl and are required for mesoderm migration in the Drosophila gastrula. Curr Biol 14, 659667.
  • 31
    Stathopoulos A, Tam B, Ronshaugen M, Frasch M & Levine M (2004) pyramus and thisbe: FGF genes that pattern the mesoderm of Drosophila embryos. Genes Dev 18, 687699.
  • 32
    Birnbaum D, Popovici C & Roubin R (2005) A pair as a minimum: the two fibroblast growth factors of the nematode Caenorhabditis elegans. Dev Dyn 232, 247255.
  • 33
    Baird A, Schubert D, Ling N & Guillemin R (1988) Receptor- and heparin-binding domains of basic fibroblast growth factor. Proc Natl Acad Sci USA 85, 23242328.
  • 34
    Faham S, Hileman RE, Fromm JR, Linhardt RJ & Rees DC (1996) Heparin structure and interactions with basic fibroblast growth factor. Science 271, 11161120.
  • 35
    Kinsella L, Chen HL, Smith JA, Rudland PS & Fernig DG (1998) Interactions of putative heparin-binding domains of basic fibroblast growth factor and its receptor, FGFR-1, with heparin using synthetic peptides. Glycoconj J 15, 419422.
  • 36
    Thompson LD, Pantoliano MW & Springer BA (1994) Energetic characterization of the basic fibroblast growth factor–heparin interaction: identification of the heparin binding domain. Biochemistry 33, 38313840.
  • 37
    Springer BA, Pantoliano MW, Barbera FA, Gunyuzlu PL, Thompson LD, Herblin WF, Rosenfeld SA & Book GW (1994) Identification and concerted function of two receptor binding surfaces on basic fibroblast growth factor required for mitogenesis. J Biol Chem 269, 2687926884.
  • 38
    Yeh BK, Igarashi M, Eliseenkova AV, Plotnikov AN, Sher I, Ron D, Aaronson SA & Mohammadi M (2003) Structural basis by which alternative splicing confers specificity in fibroblast growth factor receptors. Proc Natl Acad Sci USA 100, 22662271.
  • 39
    Afratis N, Gialeli C, Nikitovic D, Tsegenidis T, Karousou E, Theocharis AD, Pavao MS, Tzanakakis GN & Karamanos NK (2012) Glycosaminoglycans: key players in cancer cell biology and treatment. FEBS J 279, 11771197.
  • 40
    Militsopoulou M, Lamari F & Karamanos NK (2003) Capillary electrophoresis: a tool for studying interactions of glycans/proteoglycans with growth factors. J Pharmaceut Biomed Anal 32, 823828.
  • 41
    Rudd TR, Uniewicz KA, Ori A, Guimond SE, Skidmore MA, Gaudesi D, Xu R, Turnbull JE, Guerrini M, Torri G, et al. (2010) Comparable stabilisation, structural changes and activities can be induced in FGF by a variety of HS and non-GAG analogues: implications for sequence–activity relationships. Organic Biomol Chem 8, 53905397.
  • 42
    Nikitovic D, Assouti M, Sifaki M, Katonis P, Krasagakis K, Karamanos NK & Tzanakakis GN (2008) Chondroitin sulfate and heparan sulfate-containing proteoglycans are both partners and targets of basic fibroblast growth factor-mediated proliferation in human metastatic melanoma cell lines. Int J Biochem Cell Biol 40, 7283.
  • 43
    Groah SL, Libin A, Spungen M, Nguyen KL, Woods E, Nabili M, Ramella-Roman J & Barritault D (2011) Regenerating matrix-based therapy for chronic wound healing: a prospective within-subject pilot study. Int Wound J 8, 8595.
  • 44
    Lallam-Laroye C, Baroukh B, Doucet P, Barritault D, Saffar JL & Colombier ML (2011) ReGeneraTing agents matrix therapy regenerates a functional root attachment in hamsters with periodontitis. Tissue Eng Part A 17, 23592367.
  • 45
    Rai B, Nurcombe V & Cool SM (2011) Heparan sulfate-based treatments for regenerative medicine. Crit Rev Eukaryot Gene Expr 21, 112.
  • 46
    Murakami M, Elfenbein A & Simons M (2008) Non-canonical fibroblast growth factor signalling in angiogenesis. Cardiovasc Res 78, 223231.
  • 47
    Ke Y, Wilkinson MC, Fernig DG, Smith JA, Rudland PS & Barraclough R (1992) A rapid procedure for production of human basic fibroblast growth factor in Escherichia coli cells. Biochim Biophys Acta 1131, 307310.
  • 48
    Uniewicz KA, Ori A, Xu R, Ahmed Y, Wilkinson MC, Fernig DG & Yates EA (2010) Differential scanning fluorimetry measurement of protein stability changes upon binding to glycosaminoglycans: a screening test for binding specificity. Anal Chem 82, 37963802.
  • 49
    Skidmore MA, Guimond SE, Dumax-Vorzet AF, Atrih A, Yates EA & Turnbull JE (2006) High sensitivity separation and detection of heparan sulfate disaccharides. J Chromatogr A 1135, 5256.
  • 50
    Hussain R, Javorfi T & Siligardi G (2012) Circular dichroism beamline B23 at the Diamond Light Source. J Synchrotron Radiat 19, 132135.
  • 51
    Whitmore L & Wallace BA (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res 32, W668W673.
  • 52
    Whitmore L & Wallace BA (2008) Protein secondary structure analyses from circular dichroism spectroscopy: methods and reference databases. Biopolymers 89, 392400.