NCAM and the FGF-Receptor

  • Vladislav V. KiselyovEmail author
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 663)


In this review, the structural biology of interaction between the neural cell adhesion molecule (NCAM) and the fibroblast growth factor (FGF) receptor is described and a possible mechanism of the FGF-receptor activation by NCAM is discussed. Most of the FGF-receptor molecules are thought to be constantly involved in a transient interaction with NCAM. However, the FGF-receptor becomes activated only when NCAM is involved in the trans-homophilic binding (mediating cell-cell adhesion). The trans-homophilic binding between the NCAM molecules is believed to result in the formation of either one- or two-dimensional “zipper”-like arrays of the NCAM molecules, which leads to NCAM clustering and as a result to clustering of the FGF-receptor, which in turn may lead to its activation through a direct receptor-receptor dimerization (and thus activation) due to an increase in the local concentration of the receptor.


Neural cell adhesion molecule NCAM Fibroblast growth factor receptor FGFR 


  1. 1.
    Jørgensen OS, Bock E (1974) Brain specific synaptosomal membrane proteins demonstrated by crossed immunoelectrophoresis. J Neurochem 23:879-880PubMedCrossRefGoogle Scholar
  2. 2.
    Thiery JP, Brackenbury R, Rutishauser U, Edelman GM (1977) Adhesion among neural cells of the chick embryo. II. Purification and characterization of a cell adhesion molecule from neural retina. J Biol Chem 252:6841-6845PubMedGoogle Scholar
  3. 3.
    Paoloni-Giacobino A, Chen H, Antonarakis SE (1997) Cloning of a novel human neural cell adhesion molecule gene (NCAM2) that maps to chromosome region 21q21 and is potentially involved in Down syndrome. Genomics 43:43-51PubMedCrossRefGoogle Scholar
  4. 4.
    Owens GC, Edelman GM, Cunningham BA (1987) Organization of the neural cell adhesion molecule (N-CAM) gene: alternative exon usage as the basis for different membrane-associated domains. Proc Natl Acad Sci USA 84:294-298PubMedCrossRefGoogle Scholar
  5. 5.
    Small SJ, Haines SL, Akeson RA (1988) Polypeptide variation in an N-CAM extracellular immunoglobulin-like fold is developmentally regulated through alternative splicing. Neuron 1:1007-1017PubMedCrossRefGoogle Scholar
  6. 6.
    Dickson G, Gower HJ, Barton CH, Prentice HM, Elsom VL, Moore SE, Cox RD, Quinn C, Putt W, Walsh FS (1987) Human muscle neural cell adhesion molecule (N-CAM): identification of a muscle-specific sequence in the extracellular domain. Cell 50:1119-1130PubMedCrossRefGoogle Scholar
  7. 7.
    Gower HJ, Barton CH, Elsom VL, Thompson J, Moore SE, Dickson G, Walsh FS (1988) Alternative splicing generates a secreted form of N-CAM in muscle and brain. Cell 55:955-964PubMedCrossRefGoogle Scholar
  8. 8.
    Thompson J, Dickson G, Moore SE, Gower HJ, Putt W, Kenimer JG, Barton CH, Walsh FS (1989) Alternative splicing of the neural cell adhesion molecule gene generates variant extracellular domain structure in skeletal muscle and brain. Genes Dev 3:348-357PubMedCrossRefGoogle Scholar
  9. 9.
    Barthels D, Vopper G, Boned A, Cremer H, Wille W (1992) High degree of NCAM diversity generated by alternative RNA Splicing in brain and muscle. Eur J NeuroSci 4:327-337PubMedCrossRefGoogle Scholar
  10. 10.
    Thomsen NK, Soroka V, Jensen PH, Berezin V, Kiselyov VV, Bock E, Poulsen FM (1996) The three-dimensional structure of the first domain of neural cell adhesion molecule. Nat Struct Biol 3:581-585PubMedCrossRefGoogle Scholar
  11. 11.
    Jensen PH, Soroka V, Thomsen NK, Ralets I, Berezin V, Bock E, Poulsen FM (1999) Structure and interactions of NCAM modules 1 and 2, basic elements in neural cell adhesion. Nat Struct Biol 6:486-493PubMedCrossRefGoogle Scholar
  12. 12.
    Kasper C, Rasmussen H, Kastrup JS, Ikemizu S, Jones EY, Berezin V, Bock E, Larsen IK (2000) Structural basis of cell-cell adhesion by NCAM. Nat Struct Biol 7:389-393PubMedCrossRefGoogle Scholar
  13. 13.
    Atkins AR, Chung J, Deechongkit S, Little EB, Edelman GM, Wright PE, Cunningham BA, Dyson HJ (2001) Solution structure of the third immunoglobulin domain of the neural cell adhesion molecule N-CAM: can solution studies define the mechanism of homophilic binding? J Mol Biol 311:161-172PubMedCrossRefGoogle Scholar
  14. 14.
    Soroka V, Kolkova K, Kastrup JS, Diederichs K, Breed J, Kiselyov VV, Poulsen FM, Larsen IK, Welte W, Berezin V, Bock E, Kasper C (2003) Structure and interactions of NCAM Ig1-2-3 suggest a novel zipper mechanism for homophilic adhesion. Structure 11:1291-1301PubMedCrossRefGoogle Scholar
  15. 15.
    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 11:691-701PubMedCrossRefGoogle Scholar
  16. 16.
    Mendiratta SS, Sekulic N, Hernandez-Guzman FG, Close BE, Lavie A, Colley KJ (2006) A novel alpha-helix in the first fibronectin type III repeat of the neural cell adhesion molecule is critical for N-glycan polysialylation. J Biol Chem 281:36052-36059PubMedCrossRefGoogle Scholar
  17. 17.
    Nelson RW, Bates PA, Rutishauser U (1995) Protein determinants for specific polysialylation of the neural cell adhesion molecule. J Biol Chem 270:17171-17179PubMedCrossRefGoogle Scholar
  18. 18.
    Kiss JZ, Rougon G (1997) Cell biology of polysialic acid. Curr Opin Neurobiol 7:640-646PubMedCrossRefGoogle Scholar
  19. 19.
    Rougon G, Hobert O (2003) New insights into the diversity and function of neuronal immunoglobulin superfamily molecules. Annu Rev Neurosci 26:207-238PubMedCrossRefGoogle Scholar
  20. 20.
    Bruses JL, Rutishauser U (2001) Roles, regulation, and mechanism of polysialic acid function during neural development. Biochimie 83:635-643PubMedCrossRefGoogle Scholar
  21. 21.
    Berezin V, Bock E, Poulsen FM (2000) The neural cell adhesion molecule. Curr Opin Drug Discov Devel 3:605-609PubMedGoogle Scholar
  22. 22.
    Cremer H, Chazal G, Goridis C, Represa A (1997) NCAM is essential for axonal growth and fasciculation in the hippocampus. Mol Cell Neurosci 8:323-335PubMedCrossRefGoogle Scholar
  23. 23.
    Cremer H, Chazal G, Carleton A, Goridis C, Vincent JD, Lledo PM (1998) Long-term but not short-term plasticity at mossy fiber synapses is impaired in neural cell adhesion molecule-deficient mice. Proc Natl Acad Sci USA 95:13242-13247PubMedCrossRefGoogle Scholar
  24. 24.
    Rønn LC, Hartz BP, Bock E (1998) The neural cell adhesion molecule (NCAM) in development and plasticity of the nervous system. Exp Gerontol 33:853-864PubMedCrossRefGoogle Scholar
  25. 25.
    Rønn LC, Berezin V, Bock E (2000) The neural cell adhesion molecule in synaptic plasticity and ageing. Int J Dev Neurosci 18:193-199PubMedCrossRefGoogle Scholar
  26. 26.
    Cambon K, Hansen SM, Venero C, Herrero AI, Skibo G, Berezin V, Bock E, Sandi C (2004) A synthetic neural cell adhesion molecule mimetic peptide promotes synaptogenesis, enhances presynaptic function, and facilitates memory consolidation. J Neurosci 24:4197-4204PubMedCrossRefGoogle Scholar
  27. 27.
    Sandi C (2004) Stress, cognitive impairment and cell adhesion molecules. Nat Rev Neurosci 5:917-930PubMedCrossRefGoogle Scholar
  28. 28.
    Rothbard JB, Brackenbury R, Cunningham BA, Edelman GM (1982) Differences in the carbohydrate structures of neural cell-adhesion molecules from adult and embryonic chicken brains. J Biol Chem 257:11064-11069PubMedGoogle Scholar
  29. 29.
    Chuong CM, Edelman GM (1984) Alterations in neural cell adhesion molecules during development of different regions of the nervous system. J Neurosci 4:2354-2368PubMedGoogle Scholar
  30. 30.
    Small SJ, Akeson R (1990) Expression of the unique NCAM VASE exon is independently regulated in distinct tissues during development. J Cell Biol 111:2089-2096PubMedCrossRefGoogle Scholar
  31. 31.
    Seki T, Arai Y (1993) Distribution and possible roles of the highly polysialylated neural cell adhesion molecule (NCAM-H) in the developing and adult central nervous system. Neurosci Res 17:265-290PubMedCrossRefGoogle Scholar
  32. 32.
    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 13:583-594PubMedCrossRefGoogle Scholar
  33. 33.
    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 272:8310-8319PubMedCrossRefGoogle Scholar
  34. 34.
    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 38:542-558PubMedCrossRefGoogle Scholar
  35. 35.
    Kolkova K, Novitskaya V, Pedersen N, Berezin V, Bock E (2000) Neural cell adhesion molecule-stimulated neurite outgrowth depends on activation of protein kinase C and the Ras-mitogen-activated protein kinase pathway. J Neurosci 20:2238-2246PubMedGoogle Scholar
  36. 36.
    Cole GJ, Schubert D, Glaser L (1985) Cell-substratum adhesion in chick neural retina depends upon protein-heparan sulfate interactions. J Cell Biol 100:1192-1199PubMedCrossRefGoogle Scholar
  37. 37.
    Cole GJ, Glaser L (1986) A heparin-binding domain from N-CAM is involved in neural cell-substratum adhesion. J Cell Biol 102:403-412PubMedCrossRefGoogle Scholar
  38. 38.
    Nybroe O, Moran N, Bock E (1989) Equilibrium binding analysis of neural cell adhesion molecule binding to heparin. J Neurochem 52:1947-1949PubMedCrossRefGoogle Scholar
  39. 39.
    Grumet M, Flaccus A, Margolis RU (1993) Functional characterization of chondroitin sulfate proteoglycans of brain: interactions with neurons and neural cell adhesion molecules. J Cell Biol 120:815-824PubMedCrossRefGoogle Scholar
  40. 40.
    Kiselyov VV, Berezin V, Maar TE, Soroka V, Edvardsen K, Schousboe A, Bock E (1997) The first immunoglobulin-like neural cell adhesion molecule (NCAM) domain is involved in double-reciprocal interaction with the second immunoglobulin-like NCAM domain and in heparin binding. J Biol Chem 272:10125-10134PubMedCrossRefGoogle Scholar
  41. 41.
    Probstmeier R, Kuhn K, Schachner M (1989) Binding properties of the neural cell adhesion molecule to different components of the extracellular matrix. J Neurochem 53:1794-1801PubMedCrossRefGoogle Scholar
  42. 42.
    Horstkorte R, Schachner M, Magyar JP, Vorherr T, Schmitz B (1993) The fourth immunoglobulin-like domain of NCAM contains a carbohydrate recognition domain for oligomannosidic glycans implicated in association with L1 and neurite outgrowth. J Cell Biol 121:1409-1421PubMedCrossRefGoogle Scholar
  43. 43.
    Milev P, Maurel P, Haring M, Margolis RK, Margolis RU (1996) TAG-1/axonin-1 is a high-affinity ligand of neurocan, phosphacan/protein-tyrosine phosphatase-zeta/beta, and N-CAM. J Biol Chem 271:15716-15723PubMedCrossRefGoogle Scholar
  44. 44.
    Friedlander DR, Milev P, Karthikeyan L, Margolis RK, Margolis RU, Grumet M (1994) The neuronal chondroitin sulfate proteoglycan neurocan binds to the neural cell adhesion molecules Ng-CAM/L1/NILE and N-CAM, and inhibits neuronal adhesion and neurite outgrowth. J Cell Biol 125:669-680PubMedCrossRefGoogle Scholar
  45. 45.
    Milev P, Friedlander DR, Sakurai T, Karthikeyan L, Flad M, Margolis RK, Grumet M, Margolis RU (1994) Interactions of the chondroitin sulfate proteoglycan phosphacan, the extracellular domain of a receptor-type protein tyrosine phosphatase, with neurons, glia, and neural cell adhesion molecules. J Cell Biol 127:1703-1715PubMedCrossRefGoogle Scholar
  46. 46.
    Storms SD, Kim AC, Tran BH, Cole GJ, Murray BA (1996) NCAM-mediated adhesion of transfected cells to agrin. Cell Adhes Commun 3:497-509PubMedCrossRefGoogle Scholar
  47. 47.
    Paratcha G, Ledda F, Ibanez CF (2003) The neural cell adhesion molecule NCAM is an alternative signaling receptor for GDNF family ligands. Cell 113:867-879PubMedCrossRefGoogle Scholar
  48. 48.
    Dzhandzhugazyan K, Bock E (1993) Demonstration of (Ca(2+)-Mg2+)-ATPase activity of the neural cell adhesion molecule. FEBS Lett 336:279-283PubMedCrossRefGoogle Scholar
  49. 49.
    Dzhandzhugazyan K, Bock E (1997) Demonstration of an extracellular ATP-binding site in NCAM: functional implications of nucleotide binding. Biochemistry 36:15381-15395PubMedCrossRefGoogle Scholar
  50. 50.
    Crossin KL, Tai MH, Krushel LA, Mauro VP, Edelman GM (1997) Glucocorticoid receptor pathways are involved in the inhibition of astrocyte proliferation. Proc Natl Acad Sci USA 94:2687-2692PubMedCrossRefGoogle Scholar
  51. 51.
    Schmitt-Ulms G, Legname G, Baldwin MA, Ball HL, Bradon N, Bosque PJ, Crossin KL, Edelman GM, DeArmond SJ, Cohen FE, Prusiner SB (2001) Binding of neural cell adhesion molecules (N-CAMs) to the cellular prion protein. J Mol Biol 314:1209-1225PubMedCrossRefGoogle Scholar
  52. 52.
    Vutskits L, Djebbara-Hannas Z, Zhang H, Paccaud JP, Durbec P, Rougon G, Muller D, Kiss JZ (2001) PSA-NCAM modulates BDNF-dependent survival and differentiation of cortical neurons. Eur J NeuroSci 13:1391-1402PubMedCrossRefGoogle Scholar
  53. 53.
    Zhang H, Vutskits L, Calaora V, Durbec P, Kiss JZ (2004) A role for the polysialic acid-neural cell adhesion molecule in PDGF-induced chemotaxis of oligodendrocyte precursor cells. J Cell Sci 117:93-103PubMedCrossRefGoogle Scholar
  54. 54.
    Thoulouze MI, Lafage M, Schachner M, Hartmann U, Cremer H, Lafon M (1998) The neural cell adhesion molecule is a receptor for rabies virus. J Virol 72:7181-7190PubMedGoogle Scholar
  55. 55.
    Pollerberg GE, Schachner M, Davoust J (1986) Differentiation state-dependent surface mobilities of two forms of the neural cell adhesion molecule. Nature 324:462-465PubMedCrossRefGoogle Scholar
  56. 56.
    Buttner B, Kannicht C, Reutter W, Horstkorte R (2003) The neural cell adhesion molecule is associated with major components of the cytoskeleton. Biochem Biophys Res Commun 310:967-971PubMedCrossRefGoogle Scholar
  57. 57.
    Ditlevsen DK, Povlsen GK, Berezin V, Bock E (2008) NCAM-induced intracellular signaling revisited. J Neurosci Res 86:727-43Google Scholar
  58. 58.
    Hinsby AM, Berezin V, Bock E (2004) Molecular mechanisms of NCAM function. Front Biosci 9:2227-2244PubMedCrossRefGoogle Scholar
  59. 59.
    Povlsen GK, Ditlevsen DK, Berezin V, Bock E (2003) Intracellular signaling by the neural cell adhesion molecule. Neurochem Res 28:127-141PubMedCrossRefGoogle Scholar
  60. 60.
    Crossin KL, Krushel LA (2000) Cellular signaling by neural cell adhesion molecules of the immunoglobulin superfamily. Dev Dyn 218:260-279PubMedCrossRefGoogle Scholar
  61. 61.
    Rao Y, Wu XF, Gariepy J, Rutishauser U, Siu CH (1992) Identification of a peptide sequence involved in homophilic binding in the neural cell adhesion molecule NCAM. J Cell Biol 118:937-949PubMedCrossRefGoogle Scholar
  62. 62.
    Rao Y, Wu XF, Yip P, Gariepy J, Siu CH (1993) Structural characterization of a homophilic binding site in the neural cell adhesion molecule. J Biol Chem 268:20630-20638PubMedGoogle Scholar
  63. 63.
    Ranheim TS, Edelman GM, Cunningham BA (1996) Homophilic adhesion mediated by the neural cell adhesion molecule involves multiple immunoglobulin domains. Proc Natl Acad Sci USA 93:4071-4075PubMedCrossRefGoogle Scholar
  64. Atkins AR, Osborne MJ, Lashuel HA, Edelman GM, Wright PE, Cunningham BA, Dyson HJ (1999) Association between the first two immunoglobulin-like domains of the neural cell adhesion molecule N-CAM. FEBS Lett 451:162-168PubMedCrossRefGoogle Scholar
  65. 65.
    Kiselyov VV, Soroka V, Berezin V, Bock E (2005) Structural biology of NCAM homophilic binding and activation of FGFR. J Neurochem 94:1169-1179PubMedCrossRefGoogle Scholar
  66. 66.
    Johnson CP, Fujimoto I, Perrin-Tricaud C, Rutishauser U, Leckband D (2004) Mechanism of homophilic adhesion by the neural cell adhesion molecule: use of multiple domains and flexibility. Proc Natl Acad Sci USA 101:6963-6968PubMedCrossRefGoogle Scholar
  67. 67.
    McKeehan WL, Wang F, Kan M (1998) The heparan sulfate-fibroblast growth factor family: diversity of structure and function. Prog Nucleic Acid Res Mol Biol 59:135-176PubMedCrossRefGoogle Scholar
  68. 68.
    Plotnikov AN, Schlessinger J, Hubbard SR, Mohammadi M (1999) Structural basis for FGF receptor dimerization and activation. Cell 98:641-650PubMedCrossRefGoogle Scholar
  69. 69.
    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 407:1029-1034PubMedCrossRefGoogle Scholar
  70. 70.
    Wang F, Kan M, Yan G, Xu J, McKeehan WL (1995) Alternately spliced NH2-terminal immunoglobulin-like Loop I in the ectodomain of the fibroblast growth factor (FGF) receptor 1 lowers affinity for both heparin and FGF-1. J Biol Chem 270:10231-10235PubMedCrossRefGoogle Scholar
  71. 71.
    Olsen SK, Ibrahimi OA, Raucci A, Zhang F, Eliseenkova AV, Yayon A, Basilico C, Linhardt RJ, Schlessinger J, Mohammadi M (2004) Insights into the molecular basis for fibroblast growth factor receptor autoinhibition and ligand-binding promiscuity. Proc Natl Acad Sci USA 101:935-940PubMedCrossRefGoogle Scholar
  72. 72.
    Kiselyov VV, Bock E, Berezin V, Poulsen FM (2006) NMR structure of the first Ig module of mouse FGFR1. Protein Sci 15:1512-1515PubMedCrossRefGoogle Scholar
  73. 73.
    Kiselyov VV, Kochoyan A, Poulsen FM, Bock E, Berezin V (2006) Elucidation of the mechanism of the regulatory function of the Ig1 module of the fibroblast growth factor receptor 1. Protein Sci 15:2318-2322PubMedCrossRefGoogle Scholar
  74. 74.
    Mohammadi M, Olsen SK, Ibrahimi OA (2005) Structural basis for fibroblast growth factor receptor activation. Cytokine Growth Factor Rev 16:107-137PubMedCrossRefGoogle Scholar
  75. 75.
    Niethammer P, Delling M, Sytnyk V, Dityatev A, Fukami K, Schachner M (2002) Cosignaling of NCAM via lipid rafts and the FGF receptor is required for neuritogenesis. J Cell Biol 157:521-532PubMedCrossRefGoogle Scholar
  76. 76.
    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 580:3386-3390PubMedCrossRefGoogle Scholar
  77. 77.
    Neiiendam JL, Kohler LB, Christensen C, Li S, Pedersen MV, Ditlevsen DK, Kornum MK, Kiselyov VV, Berezin V, Bock E (2004) An NCAM-derived FGF-receptor agonist, the FGL-peptide, induces neurite outgrowth and neuronal survival in primary rat neurons. J Neurochem 91:920-935PubMedCrossRefGoogle Scholar
  78. 78.
    Skibo GG, Lushnikova IV, Voronin KY, Dmitrieva O, Novikova T, Klementiev B, Vaudano E, Berezin VA, Bock E (2005) A synthetic NCAM-derived peptide, FGL, protects hippocampal neurons from ischemic insult both in vitro and in vivo. Eur J NeuroSci 22:1589-1596PubMedCrossRefGoogle Scholar
  79. 79.
    Secher T, Novitskaia V, Berezin V, Bock E, Glenthøj B, Klementiev B (2006) A neural cell adhesion molecule-derived fibroblast growth factor receptor agonist, the FGL-peptide, promotes early postnatal sensorimotor development and enhances social memory retention. Neuroscience 141:1289-1299PubMedCrossRefGoogle Scholar
  80. 80.
    Klementiev B, Novikova T, Novitskaya V, Walmod PS, Dmytriyeva O, Pakkenberg B, Berezin V, Bock E (2007) A neural cell adhesion molecule-derived peptide reduces neuropathological signs and cognitive impairment induced by Abeta25-35. Neuroscience 145:209-224PubMedCrossRefGoogle Scholar
  81. 81.
    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 281:35208-35216PubMedCrossRefGoogle Scholar
  82. 82.
    Doherty P, Walsh FS (1996) CAM-FGF receptor interactions: a model for axonal growth. Mol Cell Neurosci 8:99-111CrossRefGoogle Scholar
  83. 83.
    Pantoliano MW, Horlick RA, Springer BA, Van Dyk DE, Tobery T, Wetmore DR, Lear JD, Nahapetian AT, Bradley JD, Sisk WP (1994) Multivalent ligand-receptor binding interactions in the fibroblast growth factor system produce a cooperative growth factor and heparin mechanism for receptor dimerization. Biochemistry 33:10229-10248PubMedCrossRefGoogle Scholar
  84. 84.
    Wang F, Kan M, McKeehan K, Jang JH, Feng S, McKeehan WL (1997) A homeo-interaction sequence in the ectodomain of the fibroblast growth factor receptor. J Biol Chem 272:23887-23895PubMedCrossRefGoogle Scholar
  85. 85.
    Hinsby AM, Olsen JV, Bennett KL, Mann M (2003) Signaling initiated by overexpression of the fibroblast growth factor receptor-1 investigated by mass spectrometry. Mol Cell Proteomics 2:29-36PubMedCrossRefGoogle Scholar
  86. 86.
    Doherty P, Cohen J, Walsh FS (1990) Neurite outgrowth in response to transfected N-CAM changes during development and is modulated by polysialic acid. Neuron 5:209-219PubMedCrossRefGoogle Scholar
  87. 87.
    Sadoul R, Hirn M, Deagostini-Bazin H, Rougon G, Goridis C (1983) Adult and embryonic mouse neural cell adhesion molecules have different binding properties. Nature 304:347-349PubMedCrossRefGoogle Scholar
  88. 88.
    Rutishauser U, Acheson A, Hall AK, Mann DM, Sunshine J (1988) The neural cell adhesion molecule (NCAM) as a regulator of cell-cell interactions. Science 240:53-57PubMedCrossRefGoogle Scholar
  89. 89.
    Yang P, Yin X, Rutishauser U (1992) Intercellular space is affected by the polysialic acid content of NCAM. J Cell Biol 116:1487-1496PubMedCrossRefGoogle Scholar
  90. 90.
    Evans RJ, Derkach V, Surprenant A (1992) ATP mediates fast synaptic transmission in mammalian neurons. Nature 357:503-505PubMedCrossRefGoogle Scholar
  91. 91.
    Edwards FA, Gibb AJ, Colquhoun D (1992) ATP receptor-mediated synaptic currents in the central nervous system. Nature 359:144-147PubMedCrossRefGoogle Scholar
  92. 92.
    Skladchikova G, Ronn LC, Berezin V, Bock E (1999) Extracellular adenosine triphosphate affects neural cell adhesion molecule (NCAM)-mediated cell adhesion and neurite outgrowth. J Neurosci Res 57:207-218PubMedCrossRefGoogle Scholar
  93. 93.
    Itoh N, Ornitz DM (2004) Evolution of the Fgf and Fgfr gene families. Trends Genet 20:563-569PubMedCrossRefGoogle Scholar
  94. 94.
    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 276:11031-11040PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Receptor Systems Biology LaboratoryHagedorn Research Institute, Novo Nordisk A/SGentofteDenmark

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