Extracellular interactome of the FGF receptor-ligand system: Complexities and the relative simplicity of the worm

Developmental Dynamics

Volumn 238, Issue 2, 2009, Pages 277-293

  Polanska, Urszula M ^a   Fernig, David G ^a   Kinnunen, Tarja ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

C. elegans; Development; FGF receptor

Indexed keywords

CADHERIN; CARBOHYDRATE; EPHRIN RECEPTOR A4; FIBROBLAST GROWTH FACTOR RECEPTOR; NERVE CELL ADHESION MOLECULE; PROTEOHEPARAN SULFATE;

CAENORHABDITIS ELEGANS; CELL MIGRATION; ENDOCRINE FUNCTION; GENETIC ANALYSIS; INVERTEBRATE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; WORM;

ALTERNATIVE SPLICING; ANIMALS; AXONS; BINDING SITES; CADHERINS; CAENORHABDITIS ELEGANS; CELL MOVEMENT; EXTRACELLULAR SPACE; FIBROBLAST GROWTH FACTORS; GLUCURONIDASE; HEPARAN SULFATE PROTEOGLYCANS; LIGANDS; NEURAL CELL ADHESION MOLECULES; NEURONS; PROTEIN ISOFORMS; RECEPTORS, FIBROBLAST GROWTH FACTOR; SIGNAL TRANSDUCTION;

CAENORHABDITIS ELEGANS; INVERTEBRATA;

EID: 59649090352     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21757     Document Type: Review

References (200)

1. Aigner A, Butscheid M, Kunkel P, Krause E, Lamszus K, Wellstein A, Czubayko F. 2001. An FGF-binding protein (FGF-BP) exerts its biological function by parallel paracrine stimulation of tumor cell and endothelial cell proliferation through FGF-2 release. Int J Cancer 92:510-517.
2. Aigner A, Ray PE, Czubayko F, Wellstein A. 2002. Immunolocalization of an FGF-binding protein reveals a widespread expression pattern during different stages of mouse embryo development. Histochem Cell Biol 117:1-11.
3. Arking DE, Atzmon G, Arking A, Barzilai N, Dietz HC. 2005. Association between a functional variant of the KLOTHO gene and high-density lipoprotein cholesterol, blood pressure, stroke, and longevity. Circ Res 96:412-418.
4. Arnaout MA, Goodman SL, Xiong JP. 2007. Structure and mechanics of integrin-based cell adhesion. Curr Opin Cell Biol 19:495-507.
5. Arvanitis D, Davy A. 2008. Eph/ephrin signaling: networks. Genes Dev 22:416-429.
6. Aurelio O, Hall DH, Hobert O. 2002. Immunoglobulin-domain proteins required for maintenance of ventral nerve cord organization. Science 295:686-690.
7. Baum PD, Garriga G. 1997. Neuronal migrations and axon fasciculation are disrupted in ina-1 integrin mutants. Neuron 19:51-62.
8. Beer HD, Bittner M, Niklaus G, Munding C, Max N, Goppelt A, Werner S. 2005. The fibroblast growth factor binding protein is a novel interaction partner of FGF-7, FGF-10 and FGF-22 and regulates FGF activity: implications for epithelial repair. Oncogene 24:5269-5277.
9. Beggs HE, Baragona SC, Hemperly JJ, Maness PF. 1997. NCAM140 interacts with the focal adhesion kinase p125(fak) and the SRC-related tyrosine kinase p59(fyn). J Biol Chem 272:8310-8319.
10. Bernfield M, Gotte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, Zako M. 1999. Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68:729-777.
11. Birnbaum D, Popovici C, Roubin R. 2005. A pair as a minimum: the two fibroblast growth factors of the nematode Caenorhabditis elegans. Dev Dyn 232:247-255.
12. Bishop JR, Schuksz M, Esko JD. 2007. Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 446:1030-1037.
13. Bix G, Iozzo RV. 2008. Novel interactions of perlecan: unraveling perlecan's role in angiogenesis. Microsc Res Tech 71:339-348.
14. Borland CZ, Schutzman JL, Stern MJ. 2001. Fibroblast growth factor signaling in Caenorhabditis elegans. Bioessays 23:1120-1130.
15. Bottcher RT, Pollet N, Delius H, Niehrs C. 2004. The transmembrane protein XFLRT3 forms a complex with FGF receptors and promotes FGF signalling. Nat Cell Biol 6:38-44.
16. Branda CS, Stern MJ. 2000. Mechanisms controlling sex myoblast migration in Caenorhabditis elegans hermaphrodites. Dev Biol 226:137-151.
17. Brenner S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71-94.
18. Bribian A, Barallobre MJ, Soussi-Yanicostas N, de Castro F. 2006. Anosmin-1 modulates the FGF-2-dependent migration of oligodendrocyte precursors in the developing optic nerve. Mol Cell Neurosci 33:2-14.
19. Broadbent ID, Pettitt J. 2002. The C. elegans hmr-1 gene can encode a neuronal classic cadherin involved in the regulation of axon fasciculation. Curr Biol 12:59-63.
20. Brooks PC, Clark RA, Cheresh DA. 1994. Requirement of vascular integrin alpha v beta 3 for angiogenesis. Science 264:569-571.
21. Bulow HE, Berry KL, Topper LH, Peles E, Hobert O. 2002. Heparan sulfate proteoglycan-dependent induction of axon branching and axon misrouting by the Kallmann syndrome gene kal-1. Proc Natl Acad Sci U S A 99:6346-6351.
22. Bulow HE, Boulin T, Hobert O. 2004. Differential functions of the C. elegans FGF receptor in axon outgrowth and maintenance of axon position. Neuron 42:367-374.
23. 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 U S A 94:2433-2437.
24. Burdine RD, Branda CS, Stern MJ. 1998. EGL-17(FGF) expression coordinates the attraction of the migrating sex myoblasts with vulval induction in C. elegans. Development 125:1083-1093.
25. Cadman SM, Kim SH, Hu Y, Gonzalez-Martinez D, Bouloux PM. 2007. Molecular pathogenesis of Kallmann's syndrome. Horm Res 67:231-242.
26. Calzada MJ, Sipes JM, Krutzsch HC, Yurchenco PD, Annis DS, Mosher DF, Roberts DD. 2003. Recognition of the N-terminal modules of thrombospondin-1 and thrombospondin-2 by alpha6beta1 integrin. J Biol Chem 278:40679-40687.
27. Camozzi M, Zacchigna S, Rusnati M, Coltrini D, Ramirez-Correa G, Bottazzi B, Mantovani A, Giacca M, Presta M. 2005. Pentraxin 3 inhibits fibroblast growth factor 2-dependent activation of smooth muscle cells in vitro and neointima formation in vivo. Arterioscler Thromb Vasc Biol 25:1837-1842.
28. Camozzi M, Rusnati M, Bugatti A, Bottazzi B, Mantovani A, Bastone A, Inforzato A, Vincenti S, Bracci L, Mastroianni D, Presta M. 2006. Identification of an antiangiogenic FGF2-binding site in the N terminus of the soluble pattern recognition receptor PTX3. J Biol Chem 281:22605-22613.
29. Cariboni A, Maggi R. 2006. Kallmann's syndrome, a neuronal migration defect. Cell Mol Life Sci 63:2512-2526.
30. Cavallaro U, Niedermeyer J, Fuxa M, Christofori G. 2001. N-CAM modulates tumour-cell adhesion to matrix by inducing FGF-receptor signalling. Nat Cell Biol 3:650-657.
31. Chang C, Hopper NA, Sternberg PW. 2000. Caenorhabditis elegans SOS-1 is necessary for multiple RAS-mediated developmental signals. EMBO J 19:3283-3294.
32. Chang Q, Hoefs S, van der Kemp AW, Topala CN, Bindels RJ, Hoenderop JG. 2005. The beta-glucuronidase klotho hydrolyzes and activates the TRPV5 channel. Science 310:490-493.
33. Chen EB, Branda CS, Stern MJ. 1997. Genetic enhancers of sem-5 define components of the gonad-independent guidance mechanism controlling sex myoblast migration in Caenorhabditis elegans hermaphrodites. Dev Biol 182:88-100.
34. Chen L, Ong B, Bennett V. 2001. LAD-1, the Caenorhabditis elegans L1CAM homologue, participates in embryonic and gonadal morphogenesis and is a substrate for fibroblast growth factor receptor pathway-dependent phosphotyrosine-based signaling. J Cell Biol 154:841-855.
35. Chong LD, Park EK, Latimer E, Friesel R, Daar IO. 2000. Fibroblast growth factor receptor-mediated rescue of x-ephrin B1-induced cell dissociation in Xenopus embryos. Mol Cell Biol 20:724-734.
36. Choung PH, Seo BM, Chung CP, Yamada KM, Jang JH. 2002. Synergistic activity of fibronectin and fibroblast growth factor receptors on neuronal adhesion and neurite extension through extracellular signal-regulated kinase pathway. Biochem Biophys Res Commun 295:898-902.
37. Christensen C, Lauridsen JB, Berezin V, Bock E, Kiselyov VV. 2006. The neural cell adhesion molecule binds to fibroblast growth factor receptor 2. FEBS Lett 580:3386-3390.
38. Clark SG, Stern MJ, Horvitz HR. 1992. C. elegans cell-signalling gene sem-5 encodes a protein with SH2 and SH3 domains. Nature 356:340-344.
39. Czubayko F, Smith RV, Chung HC, Wellstein A. 1994. Tumor growth and angiogenesis induced by a secreted binding protein for fibroblast growth factors. J Biol Chem 269:28243-28248.
40. Czubayko F, Liaudet-Coopman ED, Aigner A, Tuveson AT, Berchem GJ, Wellstein A. 1997. A secreted FGF-binding protein can serve as the angiogenic switch in human cancer. Nat Med 3:1137-1140.
41. Derycke L, Morbidelli L, Ziche M, De Wever O, Bracke M, Van Aken E. 2006. Soluble N-cadherin fragment promotes angiogenesis. Clin Exp Metastasis 23:187-201.
42. DeVore DL, Horvitz HR, Stern MJ. 1995. An FGF receptor signaling pathway is required for the normal cell migrations of the sex myoblasts in C. elegans hermaphrodites. Cell 83:611-620.
43. Dixon SJ, Alexander M, Fernandes R, Ricker N, Roy PJ. 2006. FGF negatively regulates muscle membrane extension in Caenorhabditis elegans. Development 133:1263-1275.
44. Dode C, Hardelin JP. 2004. Kallmann syndrome: fibroblast growth factor signaling insufficiency? J Mol Med 82:725-734.
45. Dode C, Levilliers J, Dupont JM, De Paepe A, Le Du N, Soussi-Yanicostas N, Coimbra RS, Delmaghani S, Compain-Nouaille S, Baverel F, Pecheux C, Le Tessier D, Cruaud C, Delpech M, Speleman F, Vermeulen S, Amalfitano A, Bachelot Y, Bouchard P, Cabrol S, Carel JC, Delemarre-van de Waal H, Goulet-Salmon B, Kottler ML, Richard O, Sanchez-Franco F, Saura R, Young J, Petit C, Hardelin JP. 2003. Loss-of-function mutations in FGFR1 cause autosomal dominant Kallmann syndrome. Nat Genet 33:463-465.
46. Doherty P, Williams G, Williams EJ. 2000. CAMs and axonal growth: a critical evaluation of the role of calcium and the MAPK cascade. Mol Cell Neurosci 16:283-295.
47. Duchesne L, Tissot B, Rudd TR, Dell A, Fernig DG. 2006. N-glycosylation of fibroblast growth factor receptor 1 regulates ligand and heparan sulfate co-receptor binding. J Biol Chem 281:27178-27189.
48. Eswarakumar VP, Lax I, Schlessinger J. 2005. Cellular signaling by fibroblast growth factor receptors. Cytokine Growth Factor Rev 16:139-149.
49. Feige JJ, Bradley JD, Fryburg K, Farris J, Cousens LC, Barr PJ, Baird A. 1989. Differential effects of heparin, fibronectin, and laminin on the phosphorylation of basic fibroblast growth factor by protein kinase C and the catalytic subunit of protein kinase A. J Cell Biol 109:3105-3114.
50. Fleming TC, Wolf FW, Garriga G. 2005. Sensitized genetic backgrounds reveal a role for C. elegans FGF EGL-17 as a repellent for migrating CAN neurons. Development 132:4857-4867.
51. Ford-Perriss M, Turner K, Guimond S, Apedaile A, Haubeck HD, Turnbull J, Murphy M. 2003. Localisation of specific heparan sulfate proteoglycans during the proliferative phase of brain development. Dev Dyn 227:170-184.
52. Forni JJ, Romani S, Doherty P, Tear G. 2004. Neuroglian and FasciclinII can promote neurite outgrowth via the FGF receptor Heartless. Mol Cell Neurosci 26:282-291.
53. Forrester WC, Garriga G. 1997. Genes necessary for C. elegans cell and growth cone migrations. Development 124:1831-1843.
54. Francavilla C, Loeffler S, Piccini D, Kren A, Christofori G, Cavallaro U. 2007. Neural cell adhesion molecule regulates the cellular response to fibroblast growth factor. J Cell Sci 120:4388-4394.
55. Furthauer M, Lin W, Ang SL, Thisse B, Thisse C. 2002. Sef is a feedback-induced antagonist of Ras/MAPK-mediated FGF signalling. Nat Cell Biol 4:170-174.
56. Gao AG, Lindberg FP, Dimitry JM, Brown EJ, Frazier WA. 1996. Thrombospondin modulates alpha v beta 3 function through integrin-associated protein. J Cell Biol 135:533-544.
57. Garcia-Alonso L, Romani S, Jimenez F. 2000. The EGF and FGF receptors mediate neuroglian function to control growth cone decisions during sensory axon guidance in Drosophila. Neuron 28:741-752.
58. Gettner SN, Kenyon C, Reichardt LF. 1995. Characterization of beta pat-3 heterodimers, a family of essential integrin receptors in C. elegans. J Cell Biol 129:1127-1141.
59. Ghiselli G, Eichstetter I, Iozzo RV. 2001. A role for the perlecan protein core in the activation of the keratinocyte growth factor receptor. Biochem J 359:153-163.
60. Gilchrist EJ, Moerman DG. 1992. Mutations in the sup-38 gene of Caenorhabditis elegans suppress muscle-attachment defects in unc-52 mutants. Genetics 132:431-442.
61. Gonzalez-Martinez D, Kim SH, Hu Y, Guimond S, Schofield J, Winyard P, Vannelli GB, Turnbull J, Bouloux PM. 2004. Anosmin-1 modulates fibroblast growth factor receptor 1 signaling in human gonadotropin-releasing hormone olfactory neuroblasts through a heparan sulfate-dependent mechanism. J Neurosci 24:10384-10392.
62. Goodman SJ, Branda CS, Robinson MK, Burdine RD, Stern MJ. 2003. Alternative splicing affecting a novel domain in the C. elegans EGL-15 FGF receptor confers functional specificity. Development 130:3757-3766.
63. Groth C, Lardelli M. 2002. The structure and function of vertebrate fibroblast growth factor receptor 1. Int J Dev Biol 46:393-400.
64. Guimond SE, Turnbull JE. 1999. Fibroblast growth factor receptor signalling is dictated by specific heparan sulphate saccharides. Curr Biol 9:1343-1346.
65. Gumbiner BM. 2005. Regulation of cadherin-mediated adhesion in morphogenesis. Nat Rev Mol Cell Biol 6:622-634.
66. Haines BP, Wheldon LM, Summerbell D, Heath JK, Rigby PW. 2006. Regulated expression of FLRT genes implies a functional role in the regulation of FGF signalling during mouse development. Dev Biol 297:14-25.
67. Han M, Sternberg PW. 1990. let-60, a gene that specifies cell fates during C. elegans vulval induction, encodes a ras protein. Cell 63:921-931.
68. Harada T, Morooka T, Ogawa S, Nishida E. 2001. ERK induces p35, a neuron-specific activator of Cdk5, through induction of Egr1. Nat Cell Biol 3:453-459.
69. Hazan RB, Phillips GR, Qiao RF, Norton L, Aaronson SA. 2000. Exogenous expression of N-cadherin in breast cancer cells induces cell migration, invasion, and metastasis. J Cell Biol 148:779-790.
70. Huang P, Stern MJ. 2004. FGF signaling functions in the hypodermis to regulate fluid balance in C. elegans. Development 131:2595-2604.
71. Huang P, Stern MJ. 2005. FGF signaling in flies and worms: more and more relevant to vertebrate biology. Cytokine Growth Factor Rev 16:151-158.
72. Huang CC, Hall DH, Hedgecock EM, Kao G, Karantza V, Vogel BE, Hutter H, Chisholm AD, Yurchenco PD, Wadsworth WG. 2003. Laminin alpha subunits and their role in C. elegans development. Development 130:3343-3358.
73. Hudson ML, Kinnunen T, Cinar HN, Chisholm AD. 2006. C. elegans Kallmann syndrome protein KAL-1 interacts with syndecan and glypican to regulate neuronal cell migrations. Dev Biol 294:352-365.
74. Hulit J, Suyama K, Chung S, Keren R, Agiostratidou G, Shan W, Dong X, Williams TM, Lisanti MP, Knudsen K, Hazan RB. 2007. N-cadherin signaling potentiates mammary tumor metastasis via enhanced extracellular signal-regulated kinase activation. Cancer Res 67:3106-3116.
75. Hutter H, Vogel BE, Plenefisch JD, Norris CR, Proenca RB, Spieth J, Guo C, Mastwal S, Zhu X, Scheel J, Hedgecock EM. 2000. Conservation and novelty in the evolution of cell adhesion and extracellular matrix genes. Science 287:989-994.
76. Imura A, Iwano A, Tohyama O, Tsuji Y, Nozaki K, Hashimoto N, Fujimori T, Nabeshima Y. 2004. Secreted Klotho protein in sera and CSF: implication for post-translational cleavage in release of Klotho protein from cell membrane. FEBS Lett 565:143-147.
77. Imura A, Tsuji Y, Murata M, Maeda R, Kubota K, Iwano A, Obuse C, Togashi K, Tominaga M, Kita N, Tomiyama K, Iijima J, Nabeshima Y, Fujioka M, Asato R, Tanaka S, Kojima K, Ito J, Nozaki K, Hashimoto N, Ito T, Nishio T, Uchiyama T, Fujimori T, Nabeshima Y. 2007. alpha-Klotho as a regulator of calcium homeostasis. Science 316:1615-1618.
78. Inagaki T, Choi M, Moschetta A, Peng L, Cummins CL, McDonald JG, Luo G, Jones SA, Goodwin B, Richardson JA, Gerard RD, Repa JJ, Mangelsdorf DJ, Kliewer SA. 2005. Fibroblast growth factor 15 functions as an enterohepatic signal to regulate bile acid homeostasis. Cell Metab 2:217-225.
79. Ito S, Fujimori T, Furuya A, Satoh J, Nabeshima Y, Nabeshima Y. 2005. Impaired negative feedback suppression of bile acid synthesis in mice lacking betaKlotho. J Clin Invest 115:2202-2208.
80. Itoh N, Ornitz DM. 2004. Evolution of the Fgf and Fgfr gene families. Trends Genet 20:563-569.
81. Itoh N, Mima T, Mikawa T. 1996. Loss of fibroblast growth factor receptors is necessary for terminal differentiation of embryonic limb muscle. Development 122:291-300.
82. Iwai Y, Usui T, Hirano S, Steward R, Takeichi M, Uemura T. 1997. Axon patterning requires DN-cadherin, a novel neuronal adhesion receptor, in the Drosophila embryonic CNS. Neuron 19:77-89.
83. Jiang BH, Zheng JZ, Vogt PK. 1998. An essential role of phosphatidylinositol 3-kinase in myogenic differentiation. Proc Natl Acad Sci U S A 95:14179-14183.
84. Johnson DE, Williams LT. 1993. Structural and functional diversity in the FGF receptor multigene family. Adv Cancer Res 60:1-41.
85. Kanda S, Shono T, Tomasini-Johansson B, Klint P, Saito Y. 1999. Role of thrombospondin-1-derived peptide, 4N1K, in FGF-2-induced angiogenesis. Exp Cell Res 252:262-272.
86. Karaulanov EE, Bottcher RT, Niehrs C. 2006. A role for fibronectin-leucine-rich transmembrane cell-surface proteins in homotypic cell adhesion. EMBO Rep 7:283-290.
87. Kashyap L, Tabish M. 2007. Alternatively spliced isoforms encoded by cadherin genes from C. elegans genome. Bioinformation 2:50-56.
88. Kato M, Wang H, Kainulainen V, Fitzgerald ML, Ledbetter S, Ornitz DM, 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.
89. Kharitonenkov A, Wroblewski VJ, Koester A, Chen YF, Clutinger CK, Tigno XT, Hansen BC, Shanafelt AB, Etgen GJ. 2007. The metabolic state of diabetic monkeys is regulated by fibroblast growth factor-21. Endocrinology 148:774-781.
90. Kharitonenkov A, Dunbar JD, Bina HA, Bright S, Moyers JS, Zhang C, Ding L, Micanovic R, Mehrbod SF, Knierman MD, Hale JE, Coskun T, Shanafelt AB. 2008. FGF-21/FGF-21 receptor interaction and activation is determined by betaKlotho. J Cell Physiol 215:1-7.
91. Kim SH, Hu Y, Cadman S, Bouloux P. 2008. Diversity in fibroblast growth factor receptor 1 regulation: learning from the investigation of Kallmann syndrome. J Neuroendocrinol 20:141-163.
92. Kinnunen T. 2006. The importance of specific sulfate modifications in heparan sulfate functions. Trends Glycosci Glycotechnol 18:185-195.
93. Kiselyov VV. 2008. NCAM and the FGF-receptor. Neurochem Res [epub ahead of print].
94. Kiselyov VV, Skladchikova G, Hinsby AM, Jensen PH, Kulahin N, Soroka V, Pedersen N, Tsetlin V, Poulsen FM, Berezin V, Bock E. 2003. Structural basis for a direct interaction between FGFR1 and NCAM and evidence for a regulatory role of ATP. Structure 11:691-701.
95. Kiselyov VV, Soroka V, Berezin V, Bock E. 2005. Structural biology of NCAM homophilic binding and activation of FGFR. J Neurochem 94:1169-1179.
96. Knox S, Merry C, Stringer S, Melrose J, Whitelock J. 2002. Not all perlecans are created equal: interactions with fibroblast growth factor (FGF) 2 and FGF receptors. J Biol Chem 277:14657-14665.
97. Kohl R, Antoine M, Olwin BB, Dickson C, Kiefer P. 2000. Cysteine-rich fibroblast growth factor receptor alters secretion and intracellular routing of fibroblast growth factor 3. J Biol Chem 275:15741-15748.
98. Kokel M, Borland CZ, DeLong L, Horvitz HR, Stern MJ. 1998. clr-1 encodes a receptor tyrosine phosphatase that negatively regulates an FGF receptor signaling pathway in Caenorhabditis elegans. Genes Dev 12:1425-1437.
99. Kolek OI, Hines ER, Jones MD, LeSueur LK, Lipko MA, Kiela PR, Collins JF, Haussler MR, Ghishan FK. 2005. 1alpha, 25-Dihydroxyvitamin D3 upregulates FGF23 gene expression in bone: the final link in a renal-gastrointestinal-skeletal axis that controls phosphate transport. Am J Physiol Gastrointest Liver Physiol 289:G1036-G1042.
100. Kovalenko D, Yang X, Chen PY, Nadeau RJ, Zubanova O, Pigeon K, Friesel R. 2006. A role for extracellular and transmembrane domains of Sef in Sef-mediated inhibition of FGF signaling. Cell Signal 18:1958-1966.
101. Kramer KL, Yost HJ. 2003. Heparan sulfate core proteins in cell-cell signaling. Annu Rev Genet 37:461-484.
102. Kristiansen LV, Hortsch M. 2008. Fasciclin II: the NCAM ortholog in Drosophila melanogaster. Neurochem Res [Epub ahead of print].
103. Kulahin N, Li S, Hinsby A, Kiselyov V, Berezin V, Bock E. 2008. Fibronectin type III (FN3) modules of the neuronal cell adhesion molecule L1 interact directly with the fibroblast growth factor (FGF) receptor. Mol Cell Neurosci 37:528-536.
104. Kuro-o M. 2006. Klotho as a regulator of fibroblast growth factor signaling and phosphate/calcium metabolism. Curr Opin Nephrol Hypertens 15:437-441.
105. Kuro-o M, Matsumura Y, Aizawa H, Kawaguchi H, Suga T, Utsugi T, Ohyama Y, Kurabayashi M, Kaname T, Kume E, Iwasaki H, Iida A, Shiraki-Iida T, Nishikawa S, Nagai R, Nabeshima YI. 1997. Mutation of the mouse klotho gene leads to a syndrome resembling ageing. Nature 390:45-51.
106. Kurosu H, Ogawa Y, Miyoshi M, Yamamoto M, Nandi A, Rosenblatt KP, Baum MG, Schiavi S, Hu MC, Moe OW, Kuro-o M. 2006. Regulation of fibroblast growth factor-23 signaling by klotho. J Biol Chem 281:6120-6123.
107. Kurosu H, Choi M, Ogawa Y, Dickson AS, Goetz R, Eliseenkova AV, Mohammadi M, Rosenblatt KP, Kliewer SA, Kuro-o M. 2007. Tissue-specific expression of betaKlotho and fibroblast growth factor (FGF) receptor isoforms determines metabolic activity of FGF19 and FGF21. J Biol Chem 282:26687-26695.
108. Kurosu H, Yamamoto M, Clark JD, Pastor JV, Nandi A, Gurnani P, McGuinness OP, Chikuda H, Yamaguchi M, Kawaguchi H, Shimomura I, Takayama Y, Herz J, Kahn CR, Rosenblatt KP, Kuro-o M. 2005. Suppression of aging in mice by the hormone Klotho. Science 309:1829-1833.
109. Lacy SE, Bonnemann CG, Buzney EA, Kunkel LM. 1999. Identification of FLRT1, FLRT2, and FLRT3: a novel family of transmembrane leucine-rich repeat proteins. Genomics 62:417-426.
110. Lametsch R, Rasmussen JT, Johnsen LB, Purup S, Sejrsen K, Petersen TE, Heegaard CW. 2000. Structural characterization of the fibroblast growth factor-binding protein purified from bovine prepartum mammary gland secretion. J Biol Chem 275:19469-19474.
111. Lee M, Cram EJ, Shen B, Schwarzbauer JE. 2001. Roles for beta(pat-3) integrins in development and function of Caenorhabditis elegans muscles and gonads. J Biol Chem 276:36404-36410.
112. Li R, Manela J, Kong Y, Ladisch S. 2000. Cellular gangliosides promote growth factor-induced proliferation of fibroblasts. J Biol Chem 275:34213-34223.
113. Lin X, Buff EM, Perrimon N, Michelson AM. 1999. Heparan sulfate proteoglycans are essential for FGF receptor signaling during Drosophila embryonic development. Development 126:3715-3723.
114. Lo TW, Branda CS, Huang P, Sasson IE, Goodman SJ, Stern MJ. 2008. Different isoforms of the C. elegans FGF receptor are required for attraction and repulsion of the migrating sex myoblasts. Dev Biol 318:268-275.
115. Maggi R, Cariboni A, Zaninetti R, Samara A, Stossi F, Pimpinelli F, Giacobini P, Consalez GG, Rugarli E, Piva F. 2005. Factors involved in the migration of neuroendocrine hypothalamic neurons. Arch Ital Biol 143:171-178.
116. Maness PF, Schachner M. 2007. Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat Neurosci 10:19-26.
117. Matsubara Y, Kawasaki I, Urushiyama S, Yasuda T, Shirakata M, Iino Y, Shibuya H, Yamanashi Y. 2007. The adaptor-like protein ROG-1 is required for activation of the Ras-MAP kinase pathway and meiotic cell cycle progression in Caenorhabditis elegans. Genes Cells 12:407-420.
118. Memon F, El-Abbadi M, Nakatani T, Taguchi T, Lanske B, Razzaque MS. 2008. Does Fgf23-klotho activity influence vascular and soft tissue calcification through regulating mineral ion metabolism? Kidney Int [epub ahead of print].
119. Merz DC, Alves G, Kawano T, Zheng H, Culotti JG. 2003. UNC-52/perlecan affects gonadal leader cell migrations in C. elegans hermaphrodites through alterations in growth factor signaling. Dev Biol 256:173-186.
120. Meuillet E, Cremel G, Dreyfus H, Hicks D. 1996a. Differential modulation of basic fibroblast and epidermal growth factor receptor activation by ganglioside GM3 in cultured retinal Muller glia. Glia 17:206-216.
121. Meuillet E, Cremel G, Hicks D, Dreyfus H. 1996b. Ganglioside effects on basic fibroblast and epidermal growth factor receptors in retinal glial cells. J Lipid Mediat Cell Signal 14:277-288.
122. Minniti AN, Labarca M, Hurtado C, Brandan E. 2004. Caenorhabditis elegans syndecan (SDN-1) is required for normal egg laying and associates with the nervous system and the vulva. J Cell Sci 117:5179-5190.
123. Miyamoto S, Teramoto H, Gutkind JS, Yamada KM. 1996. Integrins can collaborate with growth factors for phosphorylation of receptor tyrosine kinases and MAP kinase activation: roles of integrin aggregation and occupancy of receptors. J Cell Biol 135:1633-1642.
124. Moerman DG, Hutter H, Mullen GP, Schnabel R. 1996. Cell autonomous expression of perlecan and plasticity of cell shape in embryonic muscle of Caenorhabditis elegans. Dev Biol 173:228-242.
125. Mongiat M, Taylor K, Otto J, Aho S, Uitto J, Whitelock JM, Iozzo RV. 2000. The protein core of the proteoglycan perlecan binds specifically to fibroblast growth factor-7. J Biol Chem 275:7095-7100.
126. Mongiat M, Otto J, Oldershaw R, Ferrer F, Sato JD, Iozzo RV. 2001. Fibroblast growth factor-binding protein is a novel partner for perlecan protein core. J Biol Chem 276:10263-10271.
127. Moore KB, Mood K, Daar IO, Moody SA. 2004. Morphogenetic movements underlying eye field formation require interactions between the FGF and ephrinB1 signaling pathways. Dev Cell 6:55-67.
128. Murai KK, Pasquale EB. 2003. 'Eph'ective signaling: forward, reverse and crosstalk. J Cell Sci 116:2823-2832.
129. Nabeshima Y. 2008. [The discovery of alpha-Klotho and FGF23 unveiled new insight into calcium and phosphate homeostasis]. Clin Calcium 18:923-934.
130. Nelson FK, Riddle DL. 1984. Functional study of the Caenorhabditis elegans secretory-excretory system using laser microsurgery. J Exp Zool 231:45-56.
131. Nishimune H, Bernreuther C, Carroll P, Chen S, Schachner M, Henderson CE. 2005. Neural adhesion molecules L1 and CHL1 are survival factors for motoneurons. J Neurosci Res 80:593-599.
132. Ogawa Y, Kurosu H, Yamamoto M, Nandi A, Rosenblatt KP, Goetz R, Eliseenkova AV, Mohammadi M, Kuro-o M. 2007. BetaKlotho is required for metabolic activity of fibroblast growth factor 21. Proc Natl Acad Sci U S A 104:7432-7437.
133. Ori A, Wilkinson MC, Fernig DG. 2008. The heparanome and regulation of cell function: structures, functions and challenges. Front Biosci 13:4309-4338.
134. Ornitz DM, Itoh N. 2001. Fibroblast growth factors. Genome Biol 2:REVIEWS3005.
135. Park EK, Warner N, Bong YS, Stapleton D, Maeda R, Pawson T, Daar IO. 2004. Ectopic EphA4 receptor induces posterior protrusions via FGF signaling in Xenopus embryos. Mol Biol Cell 15:1647-1655.
136. Pickering JG, Uniyal S, Ford CM, Chau T, Laurin MA, Chow LH, Ellis CG, Fish J, Chan BM. 1997. Fibroblast growth factor-2 potentiates vascular smooth muscle cell migration to platelet-derived growth factor: upregulation of alpha2beta1 integrin and disassembly of actin filaments. Circ Res 80:627-637.
137. Pocock R, Benard CY, Shapiro L, Hobert O. 2008. Functional dissection of the C. elegans cell adhesion molecule SAX-7, a homologue of human L1. Mol Cell Neurosci 37:56-68.
138. Poliakov A, Cotrina M, Wilkinson DG. 2004. Diverse roles of eph receptors and ephrins in the regulation of cell migration and tissue assembly. Dev Cell 7:465-480.
139. Presta M, Rusnati M, Urbinati C, Sommer A, Ragnotti G. 1991. Biologically active synthetic fragments of human basic fibroblast growth factor (bFGF): identification of two Asp-Gly-Arg-containing domains involved in the mitogenic activity of bFGF in endothelial cells. J Cell Physiol 149:512-524.
140. Rahmoune H, Chen HL, Gallagher JT, Rudland PS, Fernig DG. 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.
141. Rapraeger AC, Krufka A, Olwin BB. 1991. Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science 252:1705-1708.
142. Razzaque MS, Lanske B. 2006. Hypervitaminosis D and premature aging: lessons learned from Fgf23 and Klotho mutant mice. Trends Mol Med 12:298-305.
143. Razzaque MS, Lanske B. 2007. The emerging role of the fibroblast growth factor-23-klotho axis in renal regulation of phosphate homeostasis. J Endocrinol 194:1-10.
144. Razzaque MS, Sitara D, Taguchi T, St-Arnaud R, Lanske B. 2006. Premature aging-like phenotype in fibroblast growth factor 23 null mice is a vitamin D-mediated process. FASEB J 20:720-722.
145. Rhiner C, Gysi S, Frohli E, Hengartner MO, Hajnal A. 2005. Syndecan regulates cell migration and axon guidance in C. elegans. Development 132:4621-4633.
146. Rogalski TM, Williams BD, Mullen GP, Moerman DG. 1993. Products of the unc-52 gene in Caenorhabditis elegans are homologous to the core protein of the mammalian basement membrane heparan sulfate proteoglycan. Genes Dev 7:1471-1484.
147. Rogalski TM, Gilchrist EJ, Mullen GP, Moerman DG. 1995. Mutations in the unc-52 gene responsible for body wall muscle defects in adult Caenorhabditis elegans are located in alternatively spliced exons. Genetics 139:159-169.
148. Ron D, Fuchs Y, Chorev DS. 2008. Know thy Sef: a novel class of feedback antagonists of receptor tyrosine kinase signaling. Int J Biochem Cell Biol 40:2040-2052.
149. 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 18:6741-6747.
150. Rugarli EI, Di Schiavi E, Hilliard MA, Arbucci S, Ghezzi C, Facciolli A, Coppola G, Ballabio A, Bazzicalupo P. 2002. The Kallmann syndrome gene homolog in C. elegans is involved in epidermal morphogenesis and neurite branching. Development 129:1283-1294.
151. Rusnati M, Tanghetti E, Dell'Era P, Gualandris A, Presta M. 1997. alphavbeta3 integrin mediates the cell-adhesive capacity and biological activity of basic fibroblast growth factor (FGF-2) in cultured endothelial cells. Mol Biol Cell 8:2449-2461.
152. Rusnati M, Tanghetti E, Urbinati C, Tulipano G, Marchesini S, Ziche M, Presta M. 1999. Interaction of fibroblast growth factor-2 (FGF-2) with free gangliosides: biochemical characterization and biological consequences in endothelial cell cultures. Mol Biol Cell 10:313-327.
153. Rusnati M, Urbinati C, Tanghetti E, Dell'Era P, Lortat-Jacob H, Presta M. 2002. Cell membrane GM1 ganglioside is a functional coreceptor for fibroblast growth factor 2. Proc Natl Acad Sci U S A 99:4367-4372.
154. Rusnati M, Camozzi M, Moroni E, Bottazzi B, Peri G, Indraccolo S, Amadori A, Mantovani A, Presta M. 2004. Selective recognition of fibroblast growth factor-2 by the long pentraxin PTX3 inhibits angiogenesis. Blood 104:92-99.
155. Sanchez-Heras E, Howell FV, Williams G, Doherty P. 2006. The fibroblast growth factor receptor acid box is essential for interactions with N-cadherin and all of the major isoforms of neural cell adhesion molecule. J Biol Chem 281:35208-35216.
156. Santulli RJ, Kinney WA, Ghosh S, Decorte BL, Liu L, Tuman RW, Zhou Z, Huebert N, Bursell SE, Clermont AC, Grant MB, Shaw LC, Mousa SA, Galemmo RA, Jr., Johnson DL, Maryanoff BE, Damiano BP. 2008. Studies with an orally bioavailable alpha V integrin antagonist in animal models of ocular vasculopathy: retinal neovascularization in mice and retinal vascular permeability in diabetic rats. J Pharmacol Exp Ther 324:894-901.
157. Sasakura H, Inada H, Kuhara A, Fusaoka E, Takemoto D, Takeuchi K, Mori I. 2005. Maintenance of neuronal positions in organized ganglia by SAX-7, a Caenorhabditis elegans homologue of L1. EMBO J 24:1477-1488.
158. Sasson IE, Stern MJ. 2004. FGF and PI3 kinase signaling pathways antagonistically modulate sex muscle differentiation in C. elegans. Development 131:5381-5392.
159. Schmid RS, Graff RD, Schaller MD, Chen S, Schachner M, Hemperly JJ, Maness PF. 1999. NCAM stimulates the Ras-MAPK pathway and CREB phosphorylation in neuronal cells. J Neurobiol 38:542-558.
160. Schutzman JL, Borland CZ, Newman JC, Robinson MK, Kokel M, Stern MJ. 2001. The Caenorhabditis elegans EGL-15 signaling pathway implicates a DOS-like multisubstrate adaptor protein in fibroblast growth factor signal transduction. Mol Cell Biol 21:8104-8116.
161. Selfors LM, Schutzman JL, Borland CZ, Stern MJ. 1998. soc-2 encodes a leucine-rich repeat protein implicated in fibroblast growth factor receptor signaling. Proc Natl Acad Sci U S A 95:6903-6908.
162. Sharma B, Handler M, Eichstetter I, Whitelock JM, Nugent MA, Iozzo RV. 1998. Antisense targeting of perlecan blocks tumor growth and angiogenesis in vivo. J Clin Invest 102:1599-1608.
163. Shimizu A, Tada K, Shukunami C, Hiraki Y, Kurokawa T, Magane N, Kurokawa-Seo M. 2001. A novel alternatively spliced fibroblast growth factor receptor 3 isoform lacking the acid box domain is expressed during chondrogenic differentiation of ATDC5 cells. J Biol Chem 276:11031-11040.
164. Slevin M, Kumar S, He X, Gaffney J. 1999. Physiological concentrations of gangliosides GM1, GM2 and GM3 differentially modify basic-fibroblast-growth- factor-induced mitogenesis and the associated signalling pathway in endothelial cells. Int J Cancer 82:412-423.
165. Smith SM, West LA, Hassell JR. 2007. The core protein of growth plate perlecan binds FGF-18 and alters its mitogenic effect on chondrocytes. Arch Biochem Biophys 468:244-251.
166. Soussi-Yanicostas N, Hardelin JP, Arroyo-Jimenez MM, Ardouin O, Legouis R, Levilliers J, Traincard F, Betton JM, Cabanie L, Petit C. 1996. Initial characterization of anosmin-1, a putative extracellular matrix protein synthesized by definite neuronal cell populations in the central nervous system. J Cell Sci 109(pt 7):1749-1757.
167. Soussi-Yanicostas N, Faivre-Sarrailh C, Hardelin JP, Levilliers J, Rougon G, Petit C. 1998. Anosmin-1 underlying the X chromosome-linked Kallmann syndrome is an adhesion molecule that can modulate neurite growth in a cell-type specific manner. J Cell Sci 111(pt 19):2953-2965.
168. Soussi-Yanicostas N, de Castro F, Julliard AK, Perfettini I, Chedotal A, Petit C. 2002. Anosmin-1, defective in the X-linked form of Kallmann syndrome, promotes axonal branch formation from olfactory bulb output neurons. Cell 109:217-228.
169. Stern MJ, Horvitz HR. 1991. A normally attractive cell interaction is repulsive in two C. elegans mesodermal cell migration mutants. Development 113:797-803.
170. Sulston JE, Horvitz HR. 1977. Post-embryonic cell lineages of the nematode, Caenorhabditis elegans. Dev Biol 56:110-156.
171. Suyama K, Shapiro I, Guttman M, Hazan RB. 2002. A signaling pathway leading to metastasis is controlled by N-cadherin and the FGF receptor. Cancer Cell 2:301-314.
172. Suzuki M, Uehara Y, Motomura-Matsuzaka K, Oki J, Koyama Y, Kimura M, Asada M, Komi-Kuramochi A, Oka S, Imamura T. 2008. {beta}klotho is required for fibroblast growth factor (FGF) 21 signaling through FGF receptor (FGFR) 1c and FGFR3c. Mol Endocrinol 22:1006-1014.
173. Takagi J. 2007. Structural basis for ligand recognition by integrins. Curr Opin Cell Biol 19:557-564.
174. Tanghetti E, Ria R, Dell'Era P, Urbinati C, Rusnati M, Ennas MG, Presta M. 2002. Biological activity of substrate-bound basic fibroblast growth factor (FGF2): recruitment of FGF receptor-1 in endothelial cell adhesion contacts. Oncogene 21:3889-3897.
175. Taraboletti G, Belotti D, Borsotti P, Vergani V, Rusnati M, Presta M, Giavazzi R. 1997. The 140-kilodalton antiangiogenic fragment of thrombospondin-1 binds to basic fibroblast growth factor. Cell Growth Differ 8:471-479.
176. Tassi E, Al-Attar A, Aigner A, Swift MR, McDonnell K, Karavanov A, Wellstein A. 2001. Enhancement of fibroblast growth factor (FGF) activity by an FGF-binding protein. J Biol Chem 276:40247-40253.
177. Toledo MS, Suzuki E, Handa K, Hakomori S. 2004. Cell growth regulation through GM3-enriched microdomain (glycosynapse) in human lung embryonal fibroblast WI38 and its oncogenic transformant VA13. J Biol Chem 279:34655-34664.
178. Tsang M, Friesel R, Kudoh T, Dawid IB. 2002. Identification of Sef, a novel modulator of FGF signalling. Nat Cell Biol 4:165-169.
179. Tsou R, Isik FF. 2001. Integrin activation is required for VEGF and FGF receptor protein presence on human microvascular endothelial cells. Mol Cell Biochem 224:81-89.
180. Tzeng SF, Deibler GE, DeVries GH. 1999. Myelin basic protein and myelin basic protein peptides induce the proliferation of Schwann cells via ganglioside GM1 and the FGF receptor. Neurochem Res 24:255-260.
181. Uniewicz KA, Fernig DG. 2008. Neuropilins: a versatile partner of extracellular molecules that regulate development and disease. Front Biosci 13:4339-4360.
182. Urakawa I, Yamazaki Y, Shimada T, Iijima K, Hasegawa H, Okawa K, Fujita T, Fukumoto S, Yamashita T. 2006. Klotho converts canonical FGF receptor into a specific receptor for FGF23. Nature 444:770-774.
183. Utton MA, Eickholt B, Howell FV, Wallis J, Doherty P. 2001. Soluble N-cadherin stimulates fibroblast growth factor receptor dependent neurite outgrowth and N-cadherin and the fibroblast growth factor receptor co-cluster in cells. J Neurochem 76:1421-1430.
184. Varas L, Ohlsson LB, Honeth G, Olsson A, Bengtsson T, Wiberg C, Bockermann R, Jarnum S, Richter J, Pennington D, Johnstone B, Lundgren-Akerlund E, Kjellman C. 2007. Alpha10 integrin expression is up-regulated on fibroblast growth factor-2-treated mesenchymal stem cells with improved chondrogenic differentiation potential. Stem Cells Dev 16:965-978.
185. Walsh FS, Doherty P. 1997. Neural cell adhesion molecules of the immunoglobulin superfamily: role in axon growth and guidance. Annu Rev Cell Dev Biol 13:425-456.
186. Wang X, Kweon J, Larson S, Chen L. 2005. A role for the C. elegans L1CAM homologue lad-1/sax-7 in maintaining tissue attachment. Dev Biol 284:273-291.
187. Wang X, Zhang W, Cheever T, Schwarz V, Opperman K, Hutter H, Koepp D, Chen L. 2008. The C. elegans L1CAM homologue LAD-2 functions as a coreceptor in MAB-20/Sema2 mediated axon guidance. J Cell Biol 180:233-246.
188. West DC, Rees CG, Duchesne L, Patey SJ, Terry CJ, Turnbull JE, Delehedde M, Heegaard CW, Allain F, Vanpouille C, Ron D, Fernig DG. 2005. Interactions of multiple heparin binding growth factors with neuropilin-1 and potentiation of the activity of fibroblast growth factor-2. J Biol Chem 280:13457-13464.
189. Wheelock MJ, Johnson KR. 2003. Cadherin-mediated cellular signaling. Curr Opin Cell Biol 15:509-514.
190. Whittard JD, Sakurai T, Cassella MR, Gazdoiu M, Felsenfeld DP. 2006. MAP kinase pathway-dependent phosphorylation of the L1-CAM ankyrin binding site regulates neuronal growth. Mol Biol Cell 17:2696-2706.
191. Wiedemann M, Trueb B. 2000. Characterization of a novel protein (FGFRL1) from human cartilage related to FGF receptors. Genomics 69:275-279.
192. Williams BD, Waterston RH. 1994. Genes critical for muscle development and function in Caenorhabditis elegans identified through lethal mutations. J Cell Biol 124:475-490.
193. Williams EJ, Furness J, Walsh FS, Doherty P. 1994. Activation of the FGF receptor underlies neurite outgrowth stimulated by L1, N-CAM, and N-cadherin. Neuron 13:583-594.
194. Williams EJ, Williams G, Howell FV, Skaper SD, Walsh FS, Doherty P. 2001. Identification of an N-cadherin motif that can interact with the fibroblast growth factor receptor and is required for axonal growth. J Biol Chem 276:43879-43886.
195. Yayon A, Klagsbrun M, Esko JD, Leder P, Ornitz DM. 1991. Cell surface, heparin-like molecules are required for binding of basic fibroblast growth factor to its high affinity receptor. Cell 64:841-848.
196. Yokote H, Fujita K, Jing X, Sawada T, Liang S, Yao L, Yan X, Zhang Y, Schlessinger J, Sakaguchi K. 2005. Trans-activation of EphA4 and FGF receptors mediated by direct interactions between their cytoplasmic domains. Proc Natl Acad Sci U S A 102:18866-18871.
197. Yu C, Wang F, Kan M, Jin C, Jones RB, Weinstein M, Deng CX, McKeehan WL. 2000. Elevated cholesterol metabolism and bile acid synthesis in mice lacking membrane tyrosine kinase receptor FGFR4. J Biol Chem 275:15482-15489.
198. Zallen JA, Kirch SA, Bargmann CI. 1999. Genes required for axon pathfinding and extension in the C. elegans nerve ring. Development 126:3679-3692.
199. Zhou Z, Zuber ME, Burrus LW, Olwin BB. 1997. Identification and characterization of a fibroblast growth factor (FGF) binding domain in the cysteine-rich FGF receptor. J Biol Chem 272:5167-5174.
200. Zuber ME, Zhou Z, Burrus LW, Olwin BB. 1997. Cysteine-rich FGF receptor regulates intracellular FGF-1 and FGF-2 levels. J Cell Physiol 170:217-227.