Role of the Growth-Associated Protein GAP-43 in NCAM-Mediated Neurite Outgrowth

  • Irina KorshunovaEmail author
  • Mark Mosevitsky
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 663)


The neural cell adhesion molecule (NCAM) can regulate actin cytoskeletal dynamics through associations with growth-associated protein-43 (GAP-43). By binding to the fibroblast growth factor receptor (FGFR), NCAM activates intracellular pathways to trigger calcium release, lipid diacylglycerol (DAG) formation, and protein kinase C (PKC) activation to specifically phosphorylate GAP-43 on serine 41. Phosphorylated GAP-43 plays a key role in neurite outgrowth, presumably by promoting actin polymerization. Of all NCAM isoforms, only NCAM-180 takes part in this GAP-43-dependent neurite outgrowth. GAP-43 and NCAM-180 are found in the same plasma membrane domains (rafts), and these two proteins form a functional complex with spectrin that may control cytoskeleton dynamics to induce neurite outgrowth. In the absence of GAP-43, the signaling pathway that depends on NCAM-140 and nonreceptor tyrosine kinase (Fyn) is activated.


NCAM-180 NCAM-140 GAP-43 Signal transduction Lipid rafts Neurite outgrowth 



The authors gratefully acknowledge the financial support of the Danish Medical and Natural Science Research Councils, the Lundbeck Foundation, Danish Cancer Society, European Union 6FP, PROMEMORIA, LSHM-CT-2005-512012, and RFBR grants 06-04-08336 and 06-04-48943.


  1. 1.
    Meiri KF, Saffell JL, Walsh FS et al (1998) Neurite outgrowth stimulated by neural cell adhesion molecules requires growth-associated protein-43 (GAP-43) function and is associated with GAP-43 phosphorylation in growth cones. J Neurosci 18:10429-10437PubMedGoogle Scholar
  2. 2.
    Sasaki Y (2003) New aspects of neurotransmitter release and exocytosis: Rho-kinase-dependent myristoylated alanine-rich C-kinase substrate phosphorylation and regulation of neurofilament structure in neuronal cells. J Pharmacol Sci 93:35-40PubMedGoogle Scholar
  3. 3.
    Dent EW, Meiri KF (1998) Distribution of phosphorylated GAP-43 (neuromodulin) in growth cones directly reflects growth cone behavior. J Neurobiol 35:287-299PubMedGoogle Scholar
  4. 4.
    Hirokawa N (1998) Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science 279:519-526PubMedGoogle Scholar
  5. 5.
    Popov VI, Medvedev NI, Kraev IV et al (2008) A cell adhesion molecule mimetic, FGL peptide, induces alterations in synapse and dendritic spine structure in the dentate gyrus of aged rats: a three-dimensional ultrastructural study. Eur J NeuroSci 27:301-314PubMedGoogle Scholar
  6. 6.
    Routtenberg A, Cantallops I, Zaffuto S et al (2000) Enhanced learning after genetic overexpression of a brain growth protein. Proc Natl Acad Sci USA 97:7657-7662PubMedGoogle Scholar
  7. 7.
    Botto L, Masserini M, Cassetti A et al (2004) Immunoseparation of Prion protein-enriched domains from other detergent-resistant membrane fractions, isolated from neuronal cells. FEBS Lett 557:143-147PubMedGoogle Scholar
  8. 8.
    Caroni P (2001) New EMBO members’ review: actin cytoskeleton regulation through modulation of PI(4, 5)P(2) rafts. EMBO J 20:4332-4336PubMedGoogle Scholar
  9. 9.
    He Q, Meiri KF (2002) Isolation and characterization of detergent-resistant microdomains responsive to NCAM-mediated signaling from growth cones. Mol Cell Neurosci 19:18-31PubMedGoogle Scholar
  10. 10.
    Korshunova I, Novitskaya V, Kiryushko D et al (2007) GAP-43 regulates NCAM-180-mediated neurite outgrowth. J Neurochem 100:1599-1612PubMedGoogle Scholar
  11. 11.
    Niethammer P, Delling M, Sytnyk V et al (2002) Cosignaling of NCAM via lipid rafts and the FGF receptor is required for neuritogenesis. J Cell Biol 157:521-532PubMedGoogle Scholar
  12. 12.
    Crossin KL, Chuong CM, Edelman GM (1985) Expression sequences of cell adhesion molecules. Proc Natl Acad Sci USA 82:6942-6946PubMedGoogle Scholar
  13. 13.
    Chuong CM, Edelman GM (1985) Expression of cell-adhesion molecules in embryonic induction. I. Morphogenesis of nestling feathers. J Cell Biol 101:1009-1026PubMedGoogle Scholar
  14. 14.
    Jacque CM, Jorgensen OS, Bock E (1974) Quantitative studies on the brain specific antigens S-100, GFA, 14-3-2, D1, D2, D3 and C1 in Quaking mouse. FEBS Lett 49:264-266PubMedGoogle Scholar
  15. 15.
    Jorgensen OS (1981) Neuronal membrane D2-protein during rat brain ontogeny. J Neurochem 37:939-946PubMedGoogle Scholar
  16. 16.
    Linnemann D, Bock E (1989) Cell adhesion molecules in neural development. Dev Neurosci 11:149-173PubMedGoogle Scholar
  17. 17.
    Ronn LC, Pedersen N, Jahnsen H et al (1997) Brain plasticity and the neural cell adhesion molecule (NCAM). Adv Exp Med Biol 429:305-322PubMedGoogle Scholar
  18. 18.
    Gennarini G, Hirsch MR, He HT et al (1986) Differential expression of mouse neural cell-adhesion molecule (N-CAM) mRNA species during brain development and in neural cell lines. J Neurosci 6:1983-1990PubMedGoogle Scholar
  19. 19.
    Minana R, Sancho-Tello M, Climent E et al (1998) Intracellular location, temporal expression, and polysialylation of neural cell adhesion molecule in astrocytes in primary culture. Glia 24:415-427PubMedGoogle Scholar
  20. 20.
    Nybroe O, Albrechtsen M, Dahlin J et al (1985) Biosynthesis of the neural cell adhesion molecule: characterization of polypeptide C. J Cell Biol 101:2310-2315PubMedGoogle Scholar
  21. 21.
    Kobayashi S, Vidal I, Pena JD et al (1997) Expression of neural cell adhesion molecule (NCAM) characterizes a subpopulation of type 1 astrocytes in human optic nerve head. Glia 20:262-273PubMedGoogle Scholar
  22. 22.
    Covault J, Sanes JR (1986) Distribution of N-CAM in synaptic and extrasynaptic portions of developing and adult skeletal muscle. J Cell Biol 102:716-730PubMedGoogle Scholar
  23. 23.
    Gaardsvoll H, Krog L, Zhernosekov D et al (1993) Age-related changes in expression of neural cell adhesion molecule (NCAM) in heart: a comparative study of newborn, adult and aged rats. Eur J Cell Biol 61:100-107PubMedGoogle Scholar
  24. 24.
    Wharton J, Gordon L, Walsh FS et al (1989) Neural cell adhesion molecule (N-CAM) expression during cardiac development in the rat. Brain Res 483:170-176PubMedGoogle Scholar
  25. 25.
    Akeson RA, Wujek JR, Roe S et al (1988) Smooth muscle cells transiently express NCAM. Brain Res 464:107-120PubMedGoogle Scholar
  26. 26.
    Klein G, Langegger M, Goridis C et al (1988) Neural cell adhesion molecules during embryonic induction and development of the kidney. Development 102:749-761PubMedGoogle Scholar
  27. 27.
    Ricard CS, Kobayashi S, Pena JDO et al (2000) Selective expression of neural cell adhesion molecule (NCAM)-180 in optic nerve head astrocytes exposed to elevated hydrostatic pressure in vitro. Mol Brain Res 81:62-79PubMedGoogle Scholar
  28. 28.
    Moller CJ, Byskov AG, Roth J et al (1991) NCAM in developing mouse gonads and ducts. Anat Embryol (Berl) 184:541-548Google Scholar
  29. 29.
    Moller CJ, Christgau S, Williamson MR et al (1992) Differential expression of neural cell adhesion molecule and cadherins in pancreatic islets, glucagonomas, and insulinomas. Mol Endocrinol 6:1332-1342PubMedGoogle Scholar
  30. 30.
    Figarella-Branger D, Pellissier JF, Bianco N et al (1992) Expression of various NCAM isoforms in human embryonic muscles: correlation with myosin heavy chain phenotypes. J Neuropathol Exp Neurol 51:12-23PubMedGoogle Scholar
  31. 31.
    Tomasiewicz H, Ono K, Yee D et al (1993) Genetic deletion of a neural cell adhesion molecule variant (N-CAM-180) produces distinct defects in the central nervous system. Neuron 11:1163-1174PubMedGoogle Scholar
  32. 32.
    Shen H, Watanabe M, Tomasiewicz H et al (2001) Genetic deletions of NCAM and PSA impair circadian function in the mouse. Physiol Behav 73:185-193PubMedGoogle Scholar
  33. 33.
    Persohn E, Schachner M (1987) Immunoelectron microscopic localization of the neural cell adhesion molecules L1 and N-CAM during postnatal development of the mouse cerebellum. J Cell Biol 105:569-576PubMedGoogle Scholar
  34. 34.
    Pollerberg EG, Sadoul R, Goridis C et al (1985) Selective expression of the 180-kD component of the neural cell adhesion molecule N-CAM during development. J Cell Biol 101:1921-1929PubMedGoogle Scholar
  35. 35.
    Pollerberg GE, Schachner M, Davoust J (1986) Differentiation state-dependent surface mobilities of two forms of the neural cell adhesion molecule. Nature 324:462-465PubMedGoogle Scholar
  36. 36.
    Pollerberg GE, Burridge K, Krebs KE et al (1987) The 180-kD component of the neural cell adhesion molecule N-CAM is involved in cell-cell contacts and cytoskeleton-membrane interactions. Cell Tissue Res 250:227-236PubMedGoogle Scholar
  37. 37.
    Sytnyk V, Leshchyns’ka I, Delling M et al (2002) Neural cell adhesion molecule promotes accumulation of TGN organelles at sites of neuron-to-neuron contacts. J Cell Biol 159:649-661PubMedGoogle Scholar
  38. 38.
    Linnemann D, Gaardsvoll H, Olsen M et al (1993) Expression of NCAM mRNA and polypeptides in aging rat brain. Int J Dev Neurosci 11:71-81PubMedGoogle Scholar
  39. 39.
    Kramer I, Hall H, Bleistein U et al (1997) Developmentally regulated masking of an intracellular epitope of the 180 kDa isoform of the neural cell adhesion molecule NCAM. J Neurosci Res 49:161-175PubMedGoogle Scholar
  40. 40.
    Touyarot K, Venero C, Sandi C (2004) Spatial learning impairment induced by chronic stress is related to individual differences in novelty reactivity: search for neurobiological correlates. Psychoneuroendocrinology 29:290-305PubMedGoogle Scholar
  41. 41.
    Walmod PS, Kolkova K, Berezin V et al (2004) Zippers make signals: NCAM-mediated molecular interactions and signal transduction. Neurochem Res 29:2015-2035PubMedGoogle Scholar
  42. 42.
    Beggs HE, Baragona SC, Hemperly JJ et al (1997) NCAM140 interacts with the focal adhesion kinase p125fak and the SRC-related tyrosine kinase p59fyn. J Biol Chem 272:8310-8319PubMedGoogle Scholar
  43. 43.
    Kolkova K, Novitskaya V, Pedersen N et al (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
  44. 44.
    Buttner B, Kannicht C, Reutter W et al (2003) The neural cell adhesion molecule is associated with major components of the cytoskeleton. Biochem Biophys Res Commun 310:967-971PubMedGoogle Scholar
  45. 45.
    De Matteis MA, Morrow JS (2000) Spectrin tethers and mesh in the biosynthetic pathway. J Cell Sci 113:2331-2343PubMedGoogle Scholar
  46. 46.
    Dent EW, Gertler FB (2003) Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron 40:209-227PubMedGoogle Scholar
  47. 47.
    Oestreicher AB, De Graan PNE, Gispen WH et al (1997) B-50, the growth associated protein-43: modulation of cell morphology and communication in the nervous system. Prog Neurobiol 53:627-686PubMedGoogle Scholar
  48. 48.
    Frey D, Laux T, Xu L et al (2000) Shared and unique roles of CAP23 and GAP43 in actin regulation, neurite outgrowth, and anatomical plasticity. J Cell Biol 149:1443-1454PubMedGoogle Scholar
  49. 49.
    Gispen WH, Leunissen JLM, Oestreicher AB et al (1985) Presynaptic localization of B-50 phosphoprotein: the (ACTH)-sensitive protein kinase substrate involved in rat brain polyphosphoinositide metabolism. Brain Res 328:381-385PubMedGoogle Scholar
  50. 50.
    Goslin K, Banker G (1990) Rapid changes in the distribution of GAP-43 correlate with the expression of neuronal polarity during normal development and under experimental conditions. J Cell Biol 110:1319-1331PubMedGoogle Scholar
  51. 51.
    Goslin K, Schreyer DJ, Skene JH et al (1990) Changes in the distribution of GAP-43 during the development of neuronal polarity. J Neurosci 10:588-602PubMedGoogle Scholar
  52. 52.
    Maier DL, Mani S, Donovan SL et al (1999) Disrupted cortical map and absence of cortical barrels in growth-associated protein (GAP)-43 knockout mice. Proc Natl Acad Sci USA 96:9397-9402PubMedGoogle Scholar
  53. 53.
    Strittmatter SM, Fankhauser C, Huang PL et al (1995) Neuronal pathfinding is abnormal in mice lacking the neuronal growth cone protein GAP-43. Cell 80:445-452PubMedGoogle Scholar
  54. 54.
    Aigner L, Arber S, Kapfhammer JP et al (1995) Overexpression of the neural growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell 83:269-278PubMedGoogle Scholar
  55. 55.
    Caroni P (1997) Intrinsic neuronal determinants that promote axonal sprouting and elongation. Bioessays 19:767-775PubMedGoogle Scholar
  56. 56.
    Strittmatter SM, Igarashi M, Fishman MC (1994) GAP-43 amino terminal peptides modulate growth cone morphology and neurite outgrowth. J Neurosci 14:5503-5513PubMedGoogle Scholar
  57. 57.
    Sudo Y, Valenzuela D, Beck-Sickinger AG et al (1992) Palmitoylation alters protein activity: blockade of G(o) stimulation by GAP-43. EMBO J 11:2095-2102PubMedGoogle Scholar
  58. 58.
    Mosevitsky MI (2005) Nerve ending “signal” proteins GAP-43, MARCKS, and BASP1. Int Rev Cytol 245:245-325PubMedGoogle Scholar
  59. 59.
    Aarts LH, van der Linden JA, Hage WJ et al (1995) N-terminal cysteines essential for Golgi sorting of B-50 (GAP-43) in PC12 cells. NeuroReport 6:969-972PubMedGoogle Scholar
  60. 60.
    Liang X, Lu Y, Neubert TA et al (2002) Mass spectrometric analysis of GAP-43/neuromodulin reveals the presence of a variety of fatty acylated species. J Biol Chem 277:33032-33040PubMedGoogle Scholar
  61. 61.
    Liu J, Hughes TE, Sessa WC (1997) The first 35áamino acids and fatty acylation sites determine the molecular targeting of endothelial nitric oxide synthase into the Golgi region of cells: a green fluorescent protein study. J Cell Biol 137:1525-1535PubMedGoogle Scholar
  62. 62.
    Skene JH, Virag I (1989) Posttranslational membrane attachment and dynamic fatty acylation of a neuronal growth cone protein, GAP-43. J Cell Biol 108:613-624PubMedGoogle Scholar
  63. 63.
    Zuber MX, Strittmatter SM, Fishman MC (1989) A membrane-targeting signal in the amino terminus of the neuronal protein GAP-43. Nature 341:345-348PubMedGoogle Scholar
  64. 64.
    Aarts LH, Schrama LH, Hage WJ et al (1998) B-50/GAP-43-induced formation of filopodia depends on Rho-GTPase. Mol Biol Cell 9:1279-1292PubMedGoogle Scholar
  65. 65.
    Wiederkehr A, Staple J, Caroni P (1997) The motility-associated proteins GAP-43, MARCKS, and CAP-23 share unique targeting and surface activity-inducing properties. Exp Cell Res 236:103-116PubMedGoogle Scholar
  66. 66.
    Di LM, Pastorino L, Raverdino V et al (1996) Determination of the endogenous phosphorylation state of B-50/GAP-43 and neurogranin in different brain regions by electrospray mass spectrometry. FEBS Lett 389:309-313Google Scholar
  67. 67.
    Huang KP, Huang FL, Chen HC (1999) Hypoxia/ischemia induces dephosphorylation of rat brain neuromodulin/GAP-43 in vivo. J Neurochem 72:1294-1306PubMedGoogle Scholar
  68. 68.
    Spencer SA, Schuh SM, Liu WS et al (1992) GAP-43, a protein associated with axon growth, is phosphorylated at three sites in cultured neurons and rat brain. J Biol Chem 267:9059-9064PubMedGoogle Scholar
  69. 69.
    He Q, Dent EW, Meiri KF (1997) Modulation of actin filament behavior by GAP-43 (neuromodulin) is dependent on the phosphorylation status of serine 41, áthe protein kinase C site. J Neurosci 17:3515-3524PubMedGoogle Scholar
  70. 70.
    Hayashi N, Matsubara M, Titani K et al (1997) Circular dichroism and 1H nuclear magnetic resonance studies on the solution and membrane structures of GAP-43 calmodulin-binding domain. J Biol Chem 272:7639-7645PubMedGoogle Scholar
  71. 71.
    Tejero-Diez P, Rodriguez-Sanchez P, Martin-Cοfreces NB et al (2000) bFGF stimulates GAP-43 phosphorylation at ser41 and modifies its intracellular localization in cultured hippocampal neurons. Mol Cell Neurosci 16:766-780PubMedGoogle Scholar
  72. 72.
    Gamby C, Waage MC, Allen RG et al (1996) Analysis of the role of calmodulin binding and sequestration in neuromodulin (GAP-43) function. J Biol Chem 271:26698-26705PubMedGoogle Scholar
  73. 73.
    Zakharov VV, Mosevitsky MI (2007) M-calpain-mediated cleavage of GAP-43 near Ser41 is negatively regulated by protein kinase C, calmodulin and calpain-inhibiting fragment GAP-43-3. J Neurochem 101:1539-1551PubMedGoogle Scholar
  74. 74.
    Igarashi M, Li WW, Sudo Y et al (1995) Ligand-induced growth cone collapse: amplification and blockade by variant GAP-43 peptides. J Neurosci 15:5660-5667PubMedGoogle Scholar
  75. 75.
    Strittmatter SM, Valenzuela D, Kennedy TE et al (1990) G0 is a major growth cone protein subject to regulation by GAP-43. Nature 344:836-841PubMedGoogle Scholar
  76. 76.
    Aigner L, Caroni P (1993) Depletion of 43-kD growth-associated protein in primary sensory neurons leads to diminished formation and spreading of growth cones. J Cell Biol 123:417-429PubMedGoogle Scholar
  77. 77.
    Aigner L, Caroni P (1995) Absence of persistent spreading, branching, and adhesion in GAP-43-depleted growth cones. J Cell Biol 128:647-660PubMedGoogle Scholar
  78. 78.
    Baetge EE, Hammangt JP (1991) Neurite outgrowth in PC12 cells deficient in GAP-43. Neuron 6:21-30PubMedGoogle Scholar
  79. 79.
    Meiri KF, Hammang JP, Dent EW et al (1996) Mutagenesis of ser41 to ala inhibits the association of GAP-43 with the membrane skeleton of GAP-43-deficient PC12B cells: effects on cell adhesion and the composition of neurite cytoskeleton and membrane. J Neurobiol 29:213-232PubMedGoogle Scholar
  80. 80.
    Soroka V, Kiryushko D, Novitskaya V et al (2002) Induction of Neuronal differentiation by a peptide corresponding to the homophilic binding site of the second Ig module of the neural cell adhesion molecule. J Biol Chem 277:24676-24683PubMedGoogle Scholar
  81. 81.
    Apel ED, Litchfield DW, Clark RH et al (1991) Phosphorylation of neuromodulin (GAP-43) by casein kinase II. Identification of phosphorylation sites and regulation by calmodulin. J Biol Chem 266:10544-10551PubMedGoogle Scholar
  82. 82.
    Pisano MR, Hegazy MG, Reimann EM et al (1988) Phosphorylation of protein B-50 (GAP-43) from adult rat brain cortex by casein kinase II. Biochem Biophys Res Commun 155:1207-1212PubMedGoogle Scholar
  83. 83.
    Edgar MA, Pasinelli P, DeWit M et al (1997) Phosphorylation of the casein kinase II domain of B-50 (GAP-43) in rat cortical growth cones. J Neurochem 69:2206-2215PubMedGoogle Scholar
  84. 84.
    Taniguchi H, Suzuki M, Manenti S et al (1994) A mass spectrometric study on the in vivo posttranslational modification of GAP-43. J Biol Chem 269:22481-22484PubMedGoogle Scholar
  85. 85.
    Botto L, Masserini M, Palestini P (2007) Changes in the composition of detergent-resistant membrane domains of cultured neurons following protein kinase C activation. J Neurosci Res 85:443-450PubMedGoogle Scholar
  86. 86.
    Yang P, Yin X, Rutishauser U (1992) Intercellular space is affected by the polysialic acid content of NCAM. J Cell Biol 116:1487-1496PubMedGoogle Scholar
  87. 87.
    Rutishauser U, Landmesser L (1996) Polysialic acid in the vertebrate nervous system: a promoter of plasticity in cell-cell interactions. Trends Neurosci 19:422-427PubMedGoogle Scholar
  88. 88.
    Alonso G, Prieto M, Legrand A et al (1997) PSA-NCAM and B-50/GAP-43 are coexpressed by specific neuronal systems of the adult rat mediobasal hypothalamus that exhibit remarkable capacities for morphological plasticity. J Comp Neurol 384:181-199PubMedGoogle Scholar
  89. 89.
    Emery DL, Royo NC, Fischer I et al (2003) Plasticity following injury to the adult central nervous system: is recapitulation of a developmental state worth promoting? J Neurotrauma 20:1271-1292PubMedGoogle Scholar
  90. 90.
    Gascon E, Vutskits L, Kiss JZ (2007) Polysialic acid-neural cell adhesion molecule in brain plasticity: from synapses to integration of new neurons. Brain Res Reviews 56:101-118Google Scholar
  91. 91.
    Kiselyov VV, Soroka V, Berezin V et al (2005) Structural biology of NCAM homophilic binding and activation of FGFR. J Neurochem 94:1169-1179PubMedGoogle Scholar
  92. 92.
    Dityatev A, Dityateva G, Sytnyk V et al (2004) Polysialylated neural cell adhesion molecule promotes remodeling and formation of hippocampal synapses. J Neurosci 24:9372-9382PubMedGoogle Scholar
  93. 93.
    Kolkova K, Pedersen N, Berezin V et al (2000) Identification of an amino acid sequence motif in the cytoplasmic domain of the NCAM-140 kDa isoform essential for its neuritogenic activity. J Neurochem 75:1274-1282PubMedGoogle Scholar
  94. 94.
    Kiryushko D, Kofoed T, Skladchikova G et al (2003) A synthetic peptide ligand of neural cell adhesion molecule (NCAM), C3d, promotes neuritogenesis and synaptogenesis and modulates presynaptic function in primary cultures of rat hippocampal neurons. J Biol Chem 278:12325-12334PubMedGoogle Scholar
  95. 95.
    Leshchyns’ka I, Sytnyk V, Morrow JS et al (2003) Neural cell adhesion molecule (NCAM) association with PKCβ2 via βI spectrin is implicated in NCAM-mediated neurite outgrowth. J Cell Biol 161:625-639PubMedGoogle Scholar
  96. 96.
    Riederer BM, Routtenberg A (1999) Can GAP-43 interact with brain spectrin? Mol Brain Res 71:345-348PubMedGoogle Scholar
  97. 97.
    Laux T, Fukami K, Thelen M et al (2000) GAP43, MARCKS, and CAP23 modulate PI(4, 5)P2 at plasmalemmal rafts, and regulate cell cortex actin dynamics through a common mechanism. J Cell Biol 149:1455-1472PubMedGoogle Scholar
  98. 98.
    Schmid RS, Graff RD, Schaller MD et al (1999) NCAM stimulates the Ras-MAPK pathway and CREB phosphorylation in neuronal cells. J Neurobiol 38:542-558PubMedGoogle Scholar
  99. 99.
    Beggs HE, Soriano P, Maness PF (1994) NCAM-dependent neurite outgrowth is inhibited in neurons from Fyn-minus mice. J Cell Biol 127:825-833PubMedGoogle Scholar
  100. 100.
    Cavallaro U, Niedermeyer J, Fuxa M et al (2001) N-CAM modulates tumour-cell adhesion to matrix by inducing FGF-receptor signalling. Nat Cell Biol 3:650-657PubMedGoogle Scholar
  101. 101.
    Crossin KL, Krushel LA (2000) Cellular signaling by neural cell adhesion molecules of the immunoglobulin superfamily. Dev Dyn 218:260-279PubMedGoogle Scholar
  102. 102.
    Bodrikov V, Leshchyns’ka I, Sytnyk V et al (2005) RPTPα is essential for NCAM-mediated p59fyn activation and neurite elongation. J Cell Biol 168:127-139PubMedGoogle Scholar
  103. 103.
    Hartwig JH, Thelen M, Rosen A et al (1992) MARCKS is an actin filament crosslinking protein regulated by protein kinase C and calcium-calmodulin. Nature 356:618-622PubMedGoogle Scholar
  104. 104.
    Mosevitsky MI, Novitskaya VA, Plekhanov AY et al (1994) Neuronal protein GAP-43 is a member of novel group of brain acid-soluble proteins (BASPs). Neurosci Res 19:223-228PubMedGoogle Scholar
  105. 105.
    Mosevitsky MI, Capony JP, Skladchikova GY et al (1997) The BASP1 family of myristoylated proteins abundant in axonal termini. Primary structure analysis and physico-chemical properties. Biochimie 79:373-384PubMedGoogle Scholar
  106. 106.
    Golub T, Caroni P (2005) PI(4, 5)P2-dependent microdomain assemblies capture microtubules to promote and control leading edge motility. J Cell Biol 169:151-165PubMedGoogle Scholar
  107. 107.
    Maekawa S, Taguchi K (2004) Localization of the Cl-ATPase activity on NAP-22 enriched membrane microdomain (raft) of rat brain. Neurosci Lett 362:158-161PubMedGoogle Scholar
  108. 108.
    Maekawa S, Murofushi H, Nakamura S (1994) Inhibitory effect of calmodulin on phosphorylation of NAP-22 with protein kinase C. J Biol Chem 269:19462-19465PubMedGoogle Scholar
  109. 109.
    Korshunova I, Caroni P, Kolkova K et al (2008) Characterization of BASP1-mediated neurite outgrowth. J Neurosci Res 86:2201-2213PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Protein Laboratory, Department of Neuroscience and PharmacologyUniversity of CopenhagenCopenhagenDenmark
  2. 2.Division of Molecular and Radiation Biophysics, Petersburg Nuclear Physics InstituteRussian Academy of SciencesGatchinaRussia

Personalised recommendations