The neural cell adhesion molecules L1 and NCAM-180 act in different steps of neurite outgrowth

Journal of Neuroscience

Volumn 19, Issue 21, 1999, Pages 9469-9479

  Takei, Kohtaro ^a,d   Chan, Timothy A ^a   Wang, Feng Song ^a   Deng, Haiyan ^a   Rutishauser, Urs ^b   Jay, Daniel G ^a,c  

^a HARVARD UNIVERSITY   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Axon guidance; CALI (chromophore assisted laser inactivation); Cell adhesion molecule; Chick dorsal root ganglion neurons; Growth cone motility; Neurite extension

Indexed keywords

NERVE CELL ADHESION MOLECULE; NERVE CELL ADHESION MOLECULE 180; NERVE CELL ADHESION MOLECULE L1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GROWTH REGULATION; NERVE GROWTH; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM;

EID: 0033232985     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-21-09469.1999     Document Type: Article

References (73)

1. Abosch A, Lagenaur CF (1993) Sensitivity of neurite outgrowth to microfilament disruption varies with adhesion molecule substrate. J Neurobiol 21:344-355.
2. Atashi JR, Klinz SG, Ingraham CA, Matten WT, Schachner M, Maness PF (1992) Neural cell adhesion molecules modulate tyrosine phosphorylation of tubulin in nerve growth cone membranes. Neuron 8:831-842.
3. Beggs HE, Soriano P, Maness P (1994) NCAM-dependent neurite outgrowth is inhibited in neurons derived from fyn-minus mice. J Cell Biol 127:825-833.
4. Bennett V, Davis J, Fowler VE (1982) Brain spectrin, a membrane associated protein related in structure and function of erythrocyte spectrin. Nature 299:126-131.
5. Bentley D, Toroian-Raymond A (1986) Disoriented pathfinding by pioneer neurone growth cones deprived of filopodia by cytochalasin treatment. Nature 323:712-715.
6. Bixby JL, Bookman RJ (1996) Intracellular mechanisms of axon growth induction by CAMs and integrins: some unresolved issues. Perspect Dev Neurobiol 4:147-156.
7. 2+-dependent and -independent cell adhesion molecules. Proc Natl Acad Sci USA 84:2555-2559.
8. Bray D (1991) Isolated chick neurons for the study of axon growth. In: Culturing nerve cells. (Banker G, Goslin K, eds), pp 104-120. Cambridge, MA: MIT.
9. Brittis PA, Lemmon V, Rutishauser U, Silver J (1995) Unique changes of ganglion cell growth cone behavior following cell adhesion molecule perturbations: a time-lapse study of the living retina. Mol Cell Neurosci 6:433-449.
10. Burden-Gulley SM, Lemmon V (1996) L1, N-cadherin and laminin induce distinct distribution patterns of cytoskeletal elements in growth cones. Cell Motil Cytoskeleton 35:1-23.
11. Burgoon MP, Grumet M, Mauro V, Edelman GM, Cunningham BA (1991) Structure of the chicken neuron-glia cell-adhesion molecule, NG-CAM -origin of the polypeptides and relation to the Ig superfamily. J Cell Biol 112:1017-1029.
12. Castelo L, Jay DG (1999) Radixin is involved in lamellipodial stability during nerve growth cone motility. Mol Biol Cell 10:1511-1520.
13. Chang S, Rathjen FG, Raper JA (1987) Extension of neuntes on axons is impaired by antibodies against specific neural cell-surface glycoproteins. J Cell Biol 104:355-362.
14. Chang HY, Takei K, Sydor AM, Born T, Rusnak F, Jay DG (1995) Asymmetric retraction of growth cone filopodia following focal inactivation of calcineurin. Nature 376:686-690.
15. Cohen NR, Taylor JSH, Scott LD, Guillery RW Soriano P, Furley AJW (1997) Errors in corticospinal axon guidance in mice lacking the neural cell adhesion molecule L1. Curr Biol 8:26-33.
16. Cremer H, Lange R, Christoph A, Plomann M, Vopper G, Roes J, Brown R, Baldwin S, Kraemer P, Scheff S, Barthels D, Rajewsky K, Wille W (1994) Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 367:455-459.
17. Cremer H, Chazal G, Goridis C, Represa A (1997) NCAM is essential for axonal growth and fasciculation in the hippocampus. Mol Cell Neurosci 8:323-335.
18. Cunningham BA, Hemperly JJ, Murray BA, Prediger EA, Brackenbury R, Edelman GM (1987) Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing. Science 236:799-806.
19. Dahme M, Bartsch U, Martini R, Anliker B, Schachner M, Mantei N (1997) Disruption of the mouse L1 gene leads to malformations of the nervous system. Nat Genet 17:346-349.
20. Davis JQ, Bennett V (1994) Ankyrin binding activity shared by the neurofascin/NrCAM/L1 family of nervous system cell adhesion molecules. J Biol Chem 269:27163-27166.
21. Diamond P, Mallavarapu A, Schnipper J, Booth J, Park L, O'Connor TP, Jay DG (1993) Fasciclin I and II have distinct roles in the development of grasshopper pioneer neurons. Neuron 11:1-20.
22. Doherty P, Barton CH, Dickson G, Seaton P, Rowett LH, Moore SE, Gower HJ, Walsh FS (1989) Neuronal process outgrowth of human sensory neurons on monolayers of cells transfected with cDNAs for five human N-CAM isoforms. J Cell Biol 109:789-798.
23. Doherty P, Smith P, Walsh FS (1996) Shared cell adhesion molecule (CAM) homology domains point to CAMs signalling via FGF receptors. Perspect Dev Neurobiol 4:157-168.
24. Drescher U, Kremoser C, Handwerker C, Loschinger J, Noda M, Bonhoeffer F (1995) In vitro guidance of retinal ganglion axons by RAGS, a 25 kDa tectal protein related to ligands for Eph receptor tyrosine kinases. Cell 82:359-370.
25. Frelinger III AL, Rutishauser U (1986) Topography of NCAM structural and functional determinants II. Placement of monoclonal antibody epitopes. J Cell Biol 103:1729-1737.
26. Goldberg DJ, Burmeister DW (1986) Stages of axon formation: Observations of growth by Aplysia axons in culture using video-enhanced contrast-differential interference contrast microscopy. J Cell Biol 103:1921-1932.
27. Grumet M, Friedlander DR, Edelman GM (1993) Evidence for the binding of Ng-CAM to laminin. Cell Adhes Commun 2:177-190.
28. Hankin MH, Lagenaur CF (1994) Cell adhesion molecules in the early developing mouse retina: Retinal neurons show preferential outgrowth in vitro on L1 bur not NCAM. J Neurobiol 25:472-487.
29. 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 121:1409-1421.
30. Ignelzi MA, Miller DR, Soriano P, Maness PF (1994) Impaired neurite outgrowth of src-minus cerebellar neurons on the cell adhesion molecule L1. Neuron 12:9473-9484.
31. Jay DG (1988) Selective destruction of protein function by chromophore-assisted laser inactivation. Proc Natl Acad Sci USA 85: 5454-5458.
32. Jay DG, Keshishian H (1990) Laser inactivation of fasciclin I disrupts axon adhesion of grasshopper pioneer neurons. Nature 348:548-550.
33. Kadmon G, Kowitz A, Altevogt P, Schachner M (1990) The neural cell adhesion molecule N-CAM enhances L1-dependent cell-cell interac-tions. J Cell Biol 110:193-208.
34. Kamiguchi H, Hlavin ML, Lemmon V (1998) Role of L1 in neural development: what the knockouts tell us. Mol Cell Neurosci 12:48-55.
35. Lagenaur CF, Lemmon V (1987) An L1-like molecule 8D9 antigen, is a potent substrate for neurite extension. Proc Natl Acad Sci USA 84:7753-7757.
36. Landmesser L, Dahm L, Schultz K, Rutishauser U (1988) Distinct roles for adhesion molecules during innervation of embryonic chick muscle. Dev Biol 130:645-670.
37. Lemmon V, McLoon SC (1986) The appearance of an L1-like molecule in the chick primary visual pathway. J Neurosci 6:2987-2994.
38. Lemmon V, Farr KL, Lagenaur C (1989) L1-mediated axon outgrowth via a homophilic binding mechanism. Neuron 2:1597-1603.
39. Letourneau PC (1996) The cytoskeleton in nerve growth cone motility and axonal pathfinding. Perspect Dev Neurobiol 4:111-124.
40. Letourneau PC, Shattuck TA (1989) Distribution and possible interaction of actin-associated proteins and cell adhesion molecules of nerve growth cones. Development 105:505-519.
41. Letourneau PC, Shattuck TA, Ressler AH (1987) "Push" and "pull" in neurite elongation: observations of the effects of different concentrations of cytochalasin B and taxol. Cell Motil Cytoskel 8:193-209.
42. Liao JC, Roider J, Jay DG (1994) Chromophore-assisted laser inactivation of proteins is mediated by the photogeneration of free radicals. Proc Natl Acad Sci USA 91:2659-2663.
43. Liao JC, Berg LJ, Jay DG (1995) Chromophore-assisted laser inactivation of subunits of the T cell receptor in living cells is spatially restricted. Photochem Photobiol 62:923-929.
44. Luo YL, Raible D, Raper, JA (1993) Collapsin - a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 75:217-227.
45. Marsh L, Letourneau P (1984) Growth of neurites without filopodial or lamellipodial activity in the presence of cytochalasin B. J Cell Biol 99:2041-2047.
46. Matten WT, Aubry M, West J, Maness PF (1990) Tubulin is phosphorylated by pp60c-src in nerve growth cone membranes. J Cell Biol 111:1959-1970.
47. Mitchison T, Kirschner M (1988) Cytoskeletal dynamics and nerve growth. Neuron 1:761-772.
48. Miura M, Asou H, Kobayashi M, Uyemura K (1992) Functional expression of a full length cDNA coding for rat neural cell adhesion molecule L1 mediates homophilic intercellular adhesion and migration of cerebellar neurons. J Biol Chem 267:10752-10758.
49. Persohn E, Schachner M (1987) Immunoelectron microscopic localization of the neural cell adhesion molecules L1 and NCAM during postnatal development of the mouse cerebellum. J Cell Biol 105:569-576.
50. Pollerberg E, Burridge K, Krebs KE, Goodman SR, Schachner M (1987) The 180 kD component of the neural cell adhesion molecule NCAM is involved in cell-cell contacts and cytoskeleton-membrane interactions. Cell Tissue Res 250:227-236.
51. Rathjen FG, Schachner M (1984) Immunological and biochemical characterization of a new neuronal cell surface component (L1 antigen) which is involved in cell adhesion. EMBO J 3:1-10.
52. Rathjen FG, Wolff JM, Frank R, Bonhoeffer F, Rutishauser U (1987) Membrane glycoproteins involved in neurite fasciculation. J Cell Biol 104:343-353.
53. Rutishauser U, Edelman GM (1980) Effects of fasciculation of the outgrowth of neurites from spinal ganglia in culture. J Cell Biol 87:370-378.
54. Rutishauser U, Hoffman S, Edelman GM (1982) Binding properties of a cell adhesion molecule from neural tissue. Proc Natl Acad Sci USA 79:685-689.
55. Sabry JH, Tanaka E (1995) Making the connection: cytoskeletal rearrangements during growth cone guidance. Cell 83:171-176.
56. Sabry JH, O'Connor TP, Evans L, Toroian-Raymond A, Kirschner M, Bentley D (1991) Microtubule behavior during guidance of pioneer neuron growth cones in situ. J Cell Biol 115:381-395.
57. Saffell JL, Doherty P, Tiveron MC, Morris RJ, Walsh FS (1995) NCAM requires a cytoplasmic domain to function as a neurite outgrowth-promoting neuronal receptor. Mol Cell Neurosci 6:521-531.
58. Schuch U, Lohse MJ, Schachner M (1988) Neural cell adhesion molecules influence second messenger systems. Neuron 3:13-20.
59. Silver J, Rutishauser U (1984) Guidance of optic axons in vivo by a preformed adhesive pathway on neuroepithelial endfeet. Dev Biol 106:485-499.
60. Stoeckli ET, Ziegler U, Bleiker AJ, Groscurth P, Sonderegger P (1996) Clustering and functional cooperation of Ng-CAM and axonin-1 in the substratum-contact area of growth cones. Dev Biol 177:15-29.
61. Sydor AM, Su AL, Wang FS, Xu A, Jay DG (1996) Talin and vinculin play distinct roles in filopodial motility in the neuronal growth cone. J Cell Biol 134:1197-1207.
62. Takeda, Y, Asou, H, Murakami, Y, Miura, M, Kobayashi, M, Uyemura, K (1996) A nonneuronal isoform of cell adhesion molecule Ll1 tissuespecific expression and functional analysis. J Neurochem 66:2338-2349.
63. Takei K, Shin RM, Inoue T, Kato K, Mikoshiba K (1998) Regulation of nerve growth mediated by inositol 1,4,5-trisphosphate receptors in growth cones. Science 282:1705-1708.
64. Tanaka E, Ho T, Kirschner M (1995) The role of microtubule dynamics in growth cone motility and axonal growth. J Cell Biol 128:139-155.
65. Tomasiewicz H, Ono K, Yee DL, Thompson C, Goridis C, Rutishauser U, Magnuson T (1993) Genetic deletion of a neural cell-adhesion molecule variant (N-CAM-180) produces distinct defects in the central nervous system. Neuron 11:1163-1174.
66. Treloar H, Tomasiewicz H, Magnuson T, Key B (1997) The central pathway of primary olfactory axons is abnormal in mice lacking the N-CAM-180 isoform. J Neurobiol 32:643-658.
67. Wang FS, Jay DG (1996) CALI and the dissection of growth cone motility. Trends Cell Biol 6:442-445.
68. Wang FS, Wolenski JS, Cheney RE, Mooseker MS, Jay DG (1996) Requirement of myosin V in filopodial extension in neuronal growth cones. Science 273:660-663.
69. Watanabe M, Frelinger III AL, Rutishauser U (1986) Topography of NCAM structural and functional determinants I. Classification of monoclonal antibody epitopes. J Cell Biol 103:1721-1727.
70. Williams AF, Barclay AN (1988) The immunoglobulin superfamily-domains for cell surface recognition. Annu Rev Immunol 6:381-405.
71. Williams EJ, Furness J, Walsh FS, Doherty P (1994) Activation of the FGF receptor underlies neurite outgrowth stimulated by L1, NCAM, and N-cadherin. Neuron 13:583-594.
72. Wong EV, Kenwrick S, Willems P, Lemmon V (1995) Mutations in the cell adhesion molecule L1 cause mental retardation. Trends Neurosci 18:168-172.
73. Yip PM, Zhao X, Montgomery AMP, Siu CH (1998) The Arg-Gly-Asp motif of the cell adhesion molecule L1 promotes neurite outgrowth via interaction with the αVβ3 integrin. Mol Biol Cell 9:277-290.