Tyrosine and serine phosphorylation of the neural cell adhesion molecule L1 is implicated in its oligomannosidic glycan dependent association with NCAM and neurite outgrowth

European Journal of Cell Biology

Volumn 75, Issue 2, 1998, Pages 97-106

  Heiland, Petra Cornelia ^a   Griffith, Lee Shane ^a   Lange, Rita ^b   Schachner, Melitta ^c   Hertlein, Birgit ^a   Traub, Otto ^a   Schmitz, Brigitte ^a  

^a UNIVERSITY OF BONN   (Germany)

^b UNIVERSITY OF COLOGNE   (Germany)

^c UNIVERSITY OF HAMBURG   (Germany)

Author keywords

Carbohydrate dependent cis interaction; Cell adhesion molecules; Neurite outgrowth; Phosphorylation

Indexed keywords

CARBOHYDRATE BINDING PROTEIN; CELL ADHESION MOLECULE; GLYCAN; GLYCOPEPTIDE; MANNOSIDE; NERVE CELL ADHESION MOLECULE; PHOSPHOSERINE; PHOSPHOTYROSINE;

ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CEREBELLUM; CONTROLLED STUDY; MOLECULAR INTERACTION; MOUSE; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANIMALIA;

EID: 0031885084     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0171-9335(98)80052-6     Document Type: Article

References (63)

1. Atashi, J. R., C. A. Ingraham, S. G. Klinz, W. T. Matten, M. Schachner, P. F. Maness: Neural cell adhesion molecules modulate tyrosine phosphorylation of tubulin in nerve growth cone membranes. Neuron 8, 831-842 (1992).
2. Barthels, D., G. Vopper, A. Boned, H. Cremer, W. Wille: High degree of NCAM diversity generated by alternative RNA splicing in brain and muscle. Eur. J. Neurosci. 4, 327-337 (1992).
3. fyn. J. Biol. Chem. 272, 8310-8319 (1997).
4. Beggs, H. E., P. Soriano, P. F. Maness: NCAM-dependent neurite outgrowth is inhibited in neurons from Fyn-minus mice. J. Cell Biol. 127, 825-833 (1994).
5. 2+ influx and neurite growth in response to purified N-cadherin and laminin. J. Cell Biol. 127, 1461-1475 (1994).
6. Brummendorf, T., M. Hubert, U. Treubert, R. Leuschner, A. Tárnok, F. Rathjen: The axonal recognition molecule F11 is a multifunctional protein: specific domains mediate interactions with Ng-CAM and restrictin. Neuron 10, 711-727 (1993).
7. Buchstaller, A., S. Kunz, P. Berger, B. Kunz, U. Ziegler, C. Rader, P. Sonderegger: Cell adhesion molecules NgCAM and axonin-1 form heterodimers in the neuronal membrane and cooperate in neurite outgrowth promotion. J. Cell Biol. 135, 1593-1607 (1996).
8. Davis, J. Q., V. Bennett: Brain ankyrin - a membrane-associated protein with binding sites for spectrin, tubulin and the cytoplasmic domain of the erythrocyte anion channel. J. Biol. Chem. 259, 13550-13559 (1984).
9. Davis, J. Q., T. McLaughlin, V. Bennett: Ankyrin-binding proteins related to nervous system cell adhesion molecules: candidates to provide transmembrane and intercellular connections in adult brain. J. Cell Biol. 121, 121-133 (1993).
10. DeBernardo, A. P., S. Chang: Heterophilic interactions of DMGRASP: GRASP-NgCAM interactions involved in neurite extension. J. Cell Biol. 133, 657-666 (1996).
11. Doherty, P., F. S. Walsh: CAM-FGF receptor interactions: A model for axonal growth. Mol. Cell. Neurosci. 8, 99-111 (1996).
12. Doherty, P., C. E. C. K. Moolenaar, S. V. Ashton, R. J. A. M. Michaelides, F. S. Walsh: The VASE exon down-regulates the neurite growth promoting activity of N-CAM 140. Nature 356, 791-793 (1992).
13. Dubreuil, R. R., G. MacVicar, S. Dissanayake, C. Liu, D. Homer, M. Hortsch: Neuroglian-mediated cell adhesion induces assembly of the membrane skeleton at cell contact sites. J. Cell Biol. 133, 647-655 (1996).
14. Faissner, A., D. B. Teplow, D. Kübier, G. Keilhauer, V. Kinzel, M. Schachner: Biosynthesis and membrane topography of the neural cell adhesion molecule L1. EMBO J. 4, 3105-3113 (1985).
15. Felsenfeld, D. P., M. A. Hynes, K. M. Skoler, A. J. Furley, T. M. Jessell: TAG-1 can mediate homophilic binding, but neurite outgrowth on TAG-1 requires an L1-like molecule and bl integrins. Neuron 12, 675-690 (1994).
16. Fischer, G., G. Keilhauer, M. Schachner: Comparison of astrocytic morphology, proliferation, marker profile and response to neurons in wild-type and weaver mutant mouse cerebella in culture. Dev. Brain Res. 28, 247-257 (1986).
17. Friedlander, D. R., P. Milev, L. Karthikeyan, R. K. Margolis, R. U. Margolis, M. Grumet: The neuronal chondroitin sulfate proteoglycan neurocan binds the neural cell adhesion molecules Ng-CAM/L1/NILE and N-CAM, and inhibits neuronal adhesion and neurite outgrowth. J. Cell Biol. 125, 669-680 (1994).
18. Garver, T. D., Q. Ren, S. Tuvia, V. Bennett: Tyrosine phosphorylation at a site highly conserved in the LI family of cell adhesion molecules abolishes ankyrin binding and increases lateral mobility of neurofascin. J. Cell Biol. 137, 703-714 (1997).
19. Grumet, M., A. Flaccus, R. U. Margolis: Functional characterization of chondroitin sulfate proteoglycans of brain: interactions with neurons and neural cell adhesion molecules. J. Cell Biol. 120, 815-824 (1993).
20. Grumet, M., D. R. Friedlander, G. M. Edelmann: Evidence for the binding of Ng-CAM to laminin. Cell Adhes. Commun. 1, 177-190 (1993).
21. Hayase, T., K. G. Rice, K. M. Dziegielewska, M. Kuhlenschmidt, T. Reilly, Y. C. Lee: Comparison of N-glycosides of fetuins from different species and human a2-HS-glycoprotein. Biochemistry 31, 4915-4921 (1992).
22. Heiland, P. C., B. Hertlein, O. Traub, L. S. Griffith, B. Schmitz: The neural adhesion molecule L1 is phosphorylated on tyrosine and serine residues. NeuroReport 7, 2675-2678 (1996).
23. Heiland, P. C., L. S. Griffith, M. Schachner, B. Schmitz: Phosphorylation of the neural cell adhesion molecule L1 is involved in oligomannosidic glycan-mediated interaction with NCAM and neurite outgrowth. Glycoconj. J. 12, 521 (1995).
24. Heukeshoven, J., R. Dernick: Improved silver staining procedure for fast staining in PhastSystem development unit. I. Staining of sodium dodecyl sulfate gels. Electrophoresis 9, 28-32 (1988).
25. Horstkorte, R., M. Schachner, J. P. Magyar, T. Vorherr, B. Schmitz: The fourth immunoglobulin-like domain of NCAM contains a carbohydrate recognition domain for oligomannosidic gly- cans implicated in association with L1 and neunte outgrowth. J. Cell Biol. 121, 1409-1421 (1993).
26. Hortsch, M.: The L1 family of neural cell adhesion molecules: Old proteins performing new tricks. Neuron 17, 587-593 (1996).
27. Ignelzi, M. A., D. R. Miller, P. Soriano, P. F. Maness: Impaired neurite outgrowth of src-minus cerebellar neurons on the cell adhesion molecule L1. Neuron 12, 873-884 (1994).
28. Jouet, M., A. Moncla, J. Paterson, C. McKeown, A. Fryer, N. Carpenter, E. Holmberg, C. Wadelius, S. Kenwrick: New domains of neural cell-adhesion molecule L1 implicated in X-linked hydrocephalus and MASA syndrome. Am. J. Hum. Genet. 56, 1304-1314 (1995).
29. Kadmon, G., F. von Bohlen und Halbach, R. Horstkorte, M. Eckert, P. Altevogt, M. Schachner: Evidence for cis interaction and cooperative signalling by the heat-stable antigen nectadrin (murine CD24) and the cell adhesion molecule L1 in neurons. Eur. J. Neurosci. 7, 993-1004 (1995).
30. Klinz, S. G., M. Schachner, P. F. Maness: L1 and N-CAM antibodies trigger protein phosphatase activity in growth coneenriched membranes. J. Neurochem. 65, 84-95 (1995).
31. Kobayashi, M., M. Miura, H. Asou, K. Uyemura: Molecular cloning of cell adhesion molecule L1 from human nervous tissue: a comparison of the primary sequences of L1 molecules of different origin. Biochim. Biophys. Acta 1090, 238-240 (1991).
32. Kolodkin, A. L., D. J. Matthes, C. S. Goodman: The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 75, 1389-1399 (1993).
33. Kücherer, A., A. Faissner, M. Schachner: The novel carbohydrate epitope L3 is shared by some neural cell adhesion molecules. J. Cell Biol. 104, 1597-1602 (1987).
34. Kuhn,T. B., E. T Stoeckli, M. A. Condrau, F. G. Rathjen, P. Sonderegger: Neurite outgrowth on immobilized axonin-1 is mediated by a heterophilic interaction with LI (G4). J. Cell Biol. 115, 1113-1126 (1991).
35. Kunz, S., U. Ziegler, B. Kunz, P. Sonderegger: Intracellular signaling is changed after clustering of the neural cell adhesion molecules axonin-1 and NgCAM during neurite fasciculation. J. Cell Biol. 135, 253-267 (1996).
36. 4. Nature 227, 680-685 (1970).
37. Leconte, I., C. Auzan, A. Deban, B. Rossi, E. Clauser: N-linked oligosaccharide chains of the insulin receptor β subunit are essential for transmembrane signaling. J. Biol. Chem. 267, 17415-17423 (1992).
38. Liu, L., S. Haines, R. Shew, R. A. Akeson: Axon growth is enhanced by NCAM lacking the VASE exon when expressed in either the growth substrate or the growing axon. J. Neurosci. Res. 35, 327-345 (1993).
39. Lüthi, A. L., J.-P. Laurent, A. Figurov, D. Müller, M. Schachner: Hippocampal long-term potentiation and neural cell adhesion molecules LI and NCAM. Nature 372, 777-779 (1994).
40. Milev, P., D. R. Friedlander, T. Sakurai, L. Karthikeyan, M. Flad, R. K. Margolis, M. Grumet, R. U. Margolis: 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, 1703-1715 (1994).
41. Milev, P., B. Meyer-Puttlitz, R. K. Margolis, R. U. Margolis: Complex-type asparagine-linked oligosaccharides on phosphacan and protein-tyrosine phosphatase-z/b mediate their binding to neural cell adhesion molecules and tenascin. J. Biol. Chem. 70, 24650-24653 (1995).
42. 3. J. Cell Biol. 132, 475-485 (1996).
43. Morales, G., M. Hubert, T. Brümmendorf, U. Treubert, A. Tarnok, U. Schwarz, F. G. Rathjen: Induction of axonal growth by heterophilic interactions between the cell surface recognition protein F11 and Nr-CAM/Bravo. Neuron 11, 1113-1122 (1993).
44. Olive, S., C. Dubois, M. Schachner, G. Rougon: The F3 neuronal glycosylphosphatidylinositol-linked molecule is localized to glycolipid-enriched membrane subdomains and interacts with L1 and Fyn kinase in cerebellum. J. Neurochem. 65, 2307-2317 (1995).
45. Persohn, E., M. Schachner: Tmmunoelectron microscopic localization of the neural cell adhesion molecules L1 and N-CAM during postnatal development of the mouse cerebellum. J. Cell Biol. 105, 569-576 (1987).
46. Rathjen, F. G., M. Schachner: Immunocytological and biochemical characterization of a new neuronal cell surface component (L1 antigen) which is involved in cell adhesion. EMBO J. 3, 1-10 (1984).
47. Retzier, C., W. Göhring, U. Rauch: Analysis of neurocan structures interacting with the neural cell adhesion molecule N-CAM. J. Biol. Chem. 271, 27304-27310 (1996).
48. Ruppert, M., S. Aigner, M. Hubbe, H. Yagita, P. Altevogt: The L1 adhesion molecule is a cellular ligand for VLA-5. J. Cell Biol. 131, 1881-1891 (1995).
49. Sadoul, R., F. Kirchhoff, M. Schachner: A protein kinase activity is associated with and specifically phosphorylates the neural cell adhesion molecule L1. J. Neurochem. 53, 1471-1478 (1989).
50. Saffell, J. L., F. S. Walsh, P. Doherty: Expression of NCAM containing VASE in neurons can account for a developmental loss in their neurite outgrowth response to NCAM in a cellular substratum. J. Cell Biol. 125, 427-436 (1994).
51. Saffell, J. L., E. J. Williams, I. J. Mason, F. S. Walsh, P. Doherty: Expression of a dominant negative FGF receptor inhibits axonal growth and FGF receptor phosphorylation stimulated by CAMs. Neuron 18, 231-242 (1997).
52. Schmidt, C., V. Künemund, E. S. Wintergerst, B. Schmitz, M. Schachner: CD9 of mouse brain is implicated in neurite outgrowth and cell migration in vitro and is associated with the a 6/b1 integrin and the neural adhesion molecule L1. J. Neurosci. Res. 43, 12-31 (1996).
53. Schmitz, B., J. Peter-Katalinic, H. Egge, M. Schachner: Monoclonal antibody raised against membrane glycoproieins from mouse brain recognizes N-linked oligomannosidic glycans. Glycobiology 3, 609-617 (1993).
54. deleted in proof.
55. Springer, T. A.: Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell 76, 301-314 (1994).
56. Traub, O., J. Look, D. Paul, K. Willecke: Cyclic adenosine monophosphate slimulates biosynthesis and phosphorylation of the 26 kDa gap junction protein in cultured mouse hepatocytes. Eur. J. Cell Biol. 43, 48-54 (1987).
57. Von Boxberg, Y., R. Wütz, U. Schwarz: Use of the biotin-avidin system for labelling, isolation and characterization of neural cellsurface proteins. Eur. J. Biochem. 190, 249-256 (1990).
58. Walsh, F. S., J. Furness, S. E. Moore, S. Ashton, P. Doherty: Use of the neural cell adhesion molecule VASE exon by neurons is associated with a specific down-regulation of neural cell adhesion molecule-dependent neurite outgrowth in the developing cerebellum and hippocampus. J. Neurochem. 59, 1959-1962 (1992).
59. Williams, E. J., J. Furness, F. S. Walsh, P. Doherty: Activation of the FGF receptor underlies neurite outgrowth stimulated by L1, N-CAM, and N-Cadherin. Neuron 13, 583-594 (1994).
60. Wong, E. V., A. W. Schaefer, G. Landreth, V. Lemmon: Casein kinase II phosphorylates the neural cell adhesion molecule L1. J. Neurochem. 66, 779-786 (1996).
61. rsk in neurite outgrowth mediated by the cell adhesion molecule L1. J. Biol. Chem. 271, 18217-18223 (1996).
62. Zanetta, J.-P, C. Alonso, J.-C. Michalski: Interleukin 2 is a lectin that associates its receptor with the T-cell receptor complex. Biochem. J. 318, 49-53 (1996).
63. Zisch, A. H., W. B. Stallcup, L. D. Chong, K. Dahlin-Huppe, J. Voshol, M. Schachner, E. B. Pasquale: Tyrosine phosphorylation of L1 family adhesion molecules: Implication of the eph kinase Cek5. J. Neurosci. Res. 47, 655-665 (1997).