Tyrosine phosphorylation at a site highly conserved in the L1 family of cell adhesion molecules abolishes ankyrin binding and increases lateral mobility of neurofascin

Journal of Cell Biology

Volumn 137, Issue 3, 1997, Pages 703-714

  Garver, Timothy D ^a   Ren, Qun ^c   Tuvia, Shmuel ^a   Bennett, Vann ^a,b,c  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; CELL ADHESION MOLECULE; SPECTRIN; TYROSINE;

ANIMAL CELL; ANIMAL TISSUE; NEUROBLASTOMA CELL; NONHUMAN; PHOSPHORYLATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; PROTEIN TRANSPORT; RAT; REGULATORY MECHANISM; REVIEW;

AMINO ACID SEQUENCE; ANIMALS; ANKYRINS; CELL ADHESION MOLECULES; CELL ADHESION MOLECULES, NEURONAL; DETERGENTS; HYDROQUINONES; MEMBRANE FLUIDITY; MOLECULAR SEQUENCE DATA; NERVE GROWTH FACTORS; PHOSPHOTYROSINE; PROTEIN BINDING; PROTEIN-TYROSINE KINASES; PROTEIN-TYROSINE-PHOSPHATASE; RATS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; SOLUBILITY;

EID: 0031006110     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.137.3.703     Document Type: Review

References (53)

1. Akiyama, S.K., S.S. Yamada, K.M. Yamada, and S.E LaFlamme. 1994. Transmembrane signal transduction by integrin cytoplasmic domains expressed in single-subunit chimeras. J. Biol. Chem. 269:15961-15964.
2. Arroyo, A.G., M.R. Campanero, P. Sanchez-Mateos, J.M. Zapata, M.A. Ursa, M.A. del Pozo, and F. Sanchez-Madrid. 1994. Induction of tyrosine phosphorylation during ICAM-3 and LFA-1-mediated intercellular adhesion and its regulation by the CD45 tyrosine phosphatase. J. Cell Biol. 126:1277-1286.
3. Balsamo, J., T. Leung, H. Ernst, M.K. Zanin, and S. Hoffman. 1996. Regulated binding of PTP1B-like phosphatase to N-cadherin: control of cadherin-mediated adhesion by dephosphorylation of β-catenin. J. Cell Biol. 134:801-813.
4. Bastmeyer, M., H. Ott, C.A. Leppert, and C.A. Stuermer. 1995. Fish E587 glycoprotein, a member of the L1 family of cell adhesion molecules, participates in axon fasciculation and the age-related order of ganglion cell axons in the goldfish retina. J. Cell Biol. 130:969-976.
5. Brady-Kalnay, S.M. and N.K. Tonks. 1995. Protein tyrosine phosphatases as adhesion receptors. Curr. Opin. Cell Biol. 7:650-657.
6. Brady-Kalnay, S.M., D.L. Rimm, and N.K. Tonks. 1995. Receptor protein tyrosine phosphatase PTPmu associates with cadherins and catenins in vivo. J. Cell Biol. 130:977-986.
7. Brittis, P.A., and J. Silver. 1995. Multiple factors govern intraretinal axon guidance: a time-lapse study. Mol. Cell. Neurosci. 6:413-432.
8. Brittis, P.A., V. Lemmon, U. Rutishauser, and J. Silver. 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.
9. Brummendorf, T., and F.G. Rathjen. 1993. Axonal glycoproteins with immunoglobulin- and fibronectin type III-related domains in vertebrates: structural features, binding activities, and signal transduction. J. Neurochem. 61:1207-1219.
10. Chang, S., F.G. Rathgen, and J.A. Raper. 1987. Extension of neurites on axons is impaired by antibodies against specific neural cell surface glycoproteins. J. Cell Biol. 104:355-362.
11. Cullen, B.R. 1986. Trans-Activation of human immunodeficiency virus occurs via a bimodal mechanism. Cell. 46:973-982.
12. Davis, J.Q., and V. Bennett. 1983. Brain spectrin. Isolation of subunits and formation of hybrids with erythrocyte spectrin subunits. J. Biol. Chem. 258: 7757-7766.
13. Davis, J.Q., and V. Bennett. 1984. 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.
14. Davis, J.Q., and V. Bennett. 1994. Ankyrin-binding activity shared by the neurofascin/L1/NrCAM family of nervous system cell adhesion molecules. J. Biol. Chem. 262:27163-27166.
15. Davis, J.Q., T. McLaughlin, and V. Bennett. 1993. Ankyrin-binding proteins related to nervous system cell adhesion molecules: candidates to provide transmembrane and intercellular connections in adult brain. J. Cell Biol. 232:121-133.
16. Davis, J.Q., S. Lambert, and V. Bennett. 1996. Molecular composition of the node of Ranvier: identification of ankyrin-binding cell adhesion molecules neurofascin (Mucin+/Third FNIII Domain-) and NrCAM at nodal axon segments. J. Cell Biol. 135:1355-1367.
17. Doherty, P., E.J. Williams, and F.S. Walsh. 1995. A soluble chimeric form of the L1 glycoprotein stimulates neurite outgrowth. Neuron. 14:57-66.
18. Dubreuil, R.R., S. MacVicar, C. Dissanayake, C. Liu, D. Homer, and M. Hortsch. 1996. Neuroglian-mediated cell adhesion induces assembly of the membrane skeleton at cell contact sites. J. Cell Biol. 133:647-655.
19. Felsenfeld, D.P., M.A. Hynes, K.M. Skoler, A.J. Furley, and T.M. Jessell. 1994. TAG-1 can mediate hemophilic binding, but neurite outgrowth on TAG-1 requires an L1-like molecule and beta 1 integrins. Neuron. 12:675-690.
20. Grumet, M. 1991. Cell adhesion molecules and their subgroups in the nervous system. Curr. Opin. Neurobiol. 1:370-376.
21. Hankin, M.H., and C.F. Lagenaur. 1994. Cell adhesion molecules in the early developing mouse retina: retinal neurons show preferential outgrowth in vitro on L1 but not N-CAM. J. Neurobiol. 25:472-487.
22. Hortsch, M. 1996. The L1 family of neural cell adhesion molecules: old proteins performing new tricks. Neuron. 17:587-593.
23. Hortsch, M., and C. Goodman. 1991. Cell and substrate adhesion molecules. Annu. Rev. Cell Biol. 7:505-557.
24. Hoschuetzky, H., H. Aberle, and R. Kemler. 1994. Beta-catenin mediates the interaction of the cadherin-catenin complex with epidermal growth factor receptor. J. Cell Biol. 127:1375-1380.
25. Ignelzi, M.A., D.R. Miller, P. Soriano, and P.F. Maness. 1994. Impaired neurite outgrowth of src-minus cerebellar neurons of the cell adhesion molecule L1. Neuron. 12:873-884.
26. Itoh, K., B. Stevens, M. Schachner, and R.D. Fields. 1995. Regulated expression of the neural cell adhesion molecule L1 by specific patterns of neural impulses. Science (Wash. DC). 270:1369-1372.
27. Jouet, M., A. Rosenthal, G. Armstrong, J. MacFarlane, R. Stevenson, J. Paterson, A. Metzenberg, V. Ionasescu, K. Temple, and S. Kenwrick. 1994. X-linked spastic paraplegia (SPG1), MASA syndrome and X-linked hydrocephalus result from mutations in the L1 gene. Nat. Genet. 7:402-407.
28. Klinz, S.G., M. Schachner, and P.F. Maness. 1995. L1 and N 1/2 CAM antibodies trigger protein phosphatase activity in growth cone-enriched membranes. J. Neurochem. 65:84-95.
29. Krypta, R.M, H. Su, and L.F. Reichardt. 1996. Association between a transmembrane protein tyrosine phosphatase and the cadherin-catenin complex. J. Cell Biol. 134:1519-1529.
30. Landmesser, L., L. Dahm, K. Schultz, and U. Rutishauser. 1988. Distinct roles for adhesion molecules during innervation of embryonic chick muscle. Dev. Biol. 130:645-670.
31. Law, D.A., L. Nannizzi-Alaimo, and D.R. Phillips. 1996. Outside-in integrin signal transduction Alpha IIb beta 3-(GP IIb IIIa) tyrosine phosphorylation induced by platelet aggregation. J. Biol. Chem. 271:10811-10815.
32. Liljelund, P., P. Ghosh, and A.N. van den Pol. 1994. Expression of the neural axon adhesion molecule L1 in the developing and adult rat brain. J. Biol. Chem. 269:32886-32895.
33. Lochter, A., J. Taylor, K.H. Braunewell, J. Holm, and M. Schachner. 1995. Control of neuronal morphology in vitro: interplay between adhesive substrate forces and molecular instruction. J. Neurosci. Res. 42:145-158.
34. Luthl, A., J.P. Laurent, A. Figurov, D. Muller, and M. Schachner. 1994. Hippocampal long-term potentiation and neural cell adhesion molecules L1 and NCAM. Nature (Lond.). 373:777-779.
35. Magyar-Lehmann, S., T. Frei, and M. Schachner. 1995. Fasciculation of granule cell neurites is responsible for the perpendicular orientation of small inhibitory interneurons in mouse cerebellar microexplant cultures in vitro. Eur. J. Neurosci. 7:1460-1471.
36. Matsuyoshi, N., M. Hamaguchi, S. Taniguchi, A. Nagafuchi, S. Tsukita, and M. Takeichi. 1992. Cadherin-mediated cell-cell adhesion is perturbed by v-src tyrosine phosphorylation in metastatic fibroblasts. J. Cell Biol. 118:703-714.
37. 3- anion exchanger. J. Biol. Chem. 270:31298-31302.
38. Rathjen, F.G., and T.M. Jessel. 1991. Glycoproteins that regulate the growth and guidance of vertebrate axons: domains and dynamics of the immunoglobulin/fibronectin type III superfamily. Neurosciences. 3:297-307.
39. Rosenthal, A., M. Jouet, and S. Kenwrick. 1992. Aberrant splicing of neural cell adhesion molecule L1 mRNA in a family with X-linked hydrocephalus. Nat. Genet. 2:107-112.
40. Sadoul, R., F. Kirchhoff, and M. Schachner. 1989. A protein kinase activity is associated with and specifically phosphorylates the neural cell adhesion molecule L1. J. Neurochem. 53:1471-1478.
41. Schlaepfer, D.D., S.K. Hanks, T. Hunter, and P. van der Geer. 1994. Integrin-mediated signal transduction linked to Ras pathway by Grb2 binding to focal adhesion kinase. Nature (Lond.). 372:786-791.
42. Shibamoto, S., M. Hayakawa, K. Takeuchi, T. Hori, K. Miyazawa, N. Kitamura, K.R. Johnson, M.J. Wheelock, N. Matsuyoshi, M. Takeichi, et al. 1995. Association of p120, a tyrosine kinase substrate, with E-cadherin/catenin complexes. J. Cell Biol. 128:949-957.
43. Sondereggger, P., and F.G. Rathgan. 1992. Regulation of axonal growth in the vertebrate nervous system by interactions between glycoproteins belonging to two subgroups of the immunoglobulin superfamily. J. Cell Biol. 119:1387-1394.
44. Stallcup, W.B., and L. Beasley. 1985. Involvement of the nerve growth factor-inducible large external glycoprotein (NILE) in neurite fasciculation in primary cultures of rat brain. Proc. Natl. Acad. Sci. USA. 82:1276-1280.
45. van den Pol, A.N., and W.T. Kim. 1993. NILE/L1 and NCAM-polysialic acid expression on growing axons of isolated neurons. J. Comp. Neurol. 332:237-257.
46. Williams, E.J., J. Furness, F.S. Walsh, and P. Doherty. 1994a. Activation of the FGF receptor underlies neurite outgrowth stimulated by L1, N-CAM, and N-Cadherin. Neuron. 13:583-594.
47. Williams, E.J., F.S. Walsh, and P. Doherty. 1994b. Tyrosine kinase inhibitors can differentially inhibit integrin-dependent and CAM-stimulated neurite outgrowth. J. Cell Biol. 124:1029-1037.
48. Williams, E.J., F.S. Walsh, and P. Doherty. 1994c. The production of arachidonic acid can account for calcium channel activation in the second messenger pathways underlying neurite outgrowth stimulated by N-CAM, N-Cadherin, and L1. J. Neurochem. 62:1231-1234.
49. Williams, E.J., J. Furness, F.S. Walsh, and P. Doherty. 1994d. Characterization of the second messenger pathway underlying neurite outgrowth stimulated by FGF. Development. 120:1685-1693.
50. Wong, E.V., S. Kenwrick, P. Willems, and V. Lemmon. 1995. Mutations in the cell adhesion molecule L1 cause mental retardation. J. Neurochem. 66:779-786.
51. Wong, E.V., A.W. Schaefer, G. Landreth, and V. Lemmon. 1996. Involvement of p90rsk in neurite outgrowth mediated by the cell adhesion molecule L1. J. Biol. Chem. 271:18217-18223.
52. Wood, P.M., M. Schachner, and R.P. Bunge. 1990. Inhibition of Schwann cell myelination in vitro by an antibody to the L1 adhesion molecule. J. Neurosci. 10:3635-3645.
53. Zhao, X., and C.H. Siu. 1995. Colocalization of the homophilic binding site and the neuritogenic activity of the cell adhesion molecule L1 to its second Ig-like domain. J. Biol. Chem. 270:29413-29421.