Pathological missense mutations of neural cell adhesion molecule L1 affect homophilic and heterophilic binding activities

EMBO Journal

Volumn 18, Issue 17, 1999, Pages 4744-4753

  De Angelis, Elena ^a   MacFarlane, John ^a   Du, Jian Sheng ^a   Yeo, Giles ^a   Hicks, Ray ^a   Rathjen, Fritz G ^b   Kenwrick, Sue ^a   Brümmendorf, Thomas ^b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

Axonin 1; Cell adhesion molecules; F11; L11CAM; X linked hydrocephalus

Indexed keywords

AXONIN 1; CELL SURFACE IMMUNOGLOBULIN; HETEROPHILE ANTIGEN; NERVE CELL ADHESION MOLECULE;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; BINDING AFFINITY; BRAIN DISEASE; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DISEASE SEVERITY; GENE MUTATION; HUMAN; MISSENSE MUTATION; MORTALITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN;

ANIMALS; CELL ADHESION MOLECULES, NEURONAL; CELL MEMBRANE; COS CELLS; HAND DEFORMITIES; HUMANS; HYDROCEPHALUS; LEUKOCYTE L1 ANTIGEN COMPLEX; LINKAGE (GENETICS); MEMBRANE GLYCOPROTEINS; MENTAL RETARDATION; MODELS, BIOLOGICAL; MODELS, GENETIC; MUTAGENESIS; MUTATION, MISSENSE; NEURAL CELL ADHESION MOLECULES; PARAPLEGIA; PROTEIN BINDING; RECOMBINANT FUSION PROTEINS; RECOMBINANT PROTEINS; TIME FACTORS; X CHROMOSOME;

EID: 0033200228     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.17.4744     Document Type: Article

References (52)

1. Bateman, A., Jouet, M., MacFarlane, J., Du, J.-S., Kenwrick, S. and Chothia, C. (1996) Outline structure of the human L1 cell adhesion molecule and the sites where mutations cause neurological disorders. EMBO J., 15, 6050-6059.
2. Brümmendorf, T. and Rathjen, F.G. (1995) Cell adhesion molecules 1. Immunoglobulin superfamily. Protein Profile, 2, 963-1108.
3. Brümmendorf, T. and Rathjen, F.G. (1996) Structure/function relationships of axon-associated adhesion receptors of the imimmoglobulin superfamily. Curr. Opin. Neurobiol., 6, 584-593.
4. Brümmendorf, T., Hubert, M., Treubert, U., Leuschner, R., Tarnok, A. and Rathjen , F.G. (1993) The axonal recognition molecule F11 is a multifunctional protein: specific domains mediate interactions with Ng-CAM and restrictin. Neuron, 10, 711-727.
5. Brümmendorf, T., Kenwrick, S. and Rathjen, F.G. (1998) Neural cell recognition molecule L1: from cell biology to human hereditary brain malformations. Curr. Opin. Neurobiol., 8, 87-97.
6. Buchstaller, A., Kunz, S., Berger, P., Kunz, B., Ziegler, U., Rader, C. and Sonderegger, P. (1996) 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.
7. Buttiglione, M., Revest, J.M., Pavlou, O., Karagogeos , D., Furley, A., Rougon, G. and Faivre Sarrailh, C. (1998) A functional interaction between the neuronal adhesion molecules TAG-1 and F3 modulates neurite outgrowth and fasciculation of cerebellar granule cells. J. Neurosci., 18, 6853-6870.
8. Chothia, C. and Jones, E. (1997) The molecular structure of cell adhesion molecules. Annu. Rev. Biochem., 66, 823-862.
9. Cohen, N.R., Taylor, J.S.H., Scott, L.B., Guillery, R.W., Soriano, P. and Furley, A.J. (1997) Errors in corticospinal axon guidance in mice lacking the neural cell adhesion molecule L1. Curr. Biol., 8, 26-33.
10. Dahme, M., Bartsch, U., Martini, R., Anliker, B., Schachner, M. and Mantei, N. (1997) Disruption of the mouse L1 gene leads to malformations of the nervous system. Nature Genet., 17, 346-349.
11. Doherty, P., Williams, E. and Walsh, F. (1995) A soluble form of L1 glycoprotein stimulates neurite outgrowth. Neuron, 14, 57-66.
12. Du, Y.-Z., Dickerson, C., Aylsworth, A. and Schwartz, C. (1998a) A silent mutation, C924T (G308G), in the L1CAM gene results in X-linked hydrocephalus (HSAS). J. Med. Genet., 35, 456-462.
13. Du, Y.-Z., Srivastava, A. and Schwartz, C. (1998b) Multiple exon screening using restriction endonuclease fingerprinting (REF): detection of six novel mutations in the L1 cell adhesion molecule (L1CAM) gene. Hum. Mutat., 11, 222-230.
14. Fransen, E. et al. (1998a) L1 knockout mice show dilated ventricles, vermis hypoplasia and impaired exploration patterns. Hum. Mol. Genet., 7, 999-1009.
15. Fransen, E., Van Camp, G., D'Hooge, R., Vits, L. and Willems, P. (1998b) Genotype-phenotype corelation in L1-associated diseases. J. Med. Genet., 35, 399-404.
16. Fransen, E., Van Camp, G., Vits, L. and Willems, P.J. (1997) L1-associated diseases: clinical geneticists divide, molecular geneticists unite. Hum. Mol. Genet., 6, 1625-1632.
17. Galvin, B., Hart, K., Meyer, A. and Webster, M.K. (1996) Constitutive receptor activation by Crouzon syndrome mutations in fibroblast growth factor receptor (FGFR)2 and FGFR2/Neu chimeras. Proc. Natl Acad. Sci. USA, 93, 7894-7899.
18. Gennarini, G., Cibelli, G., Rougor, G., Mattei, M.G. and Goridis, C. (1989) The mouse neuronal cell surface protein F3: a phosphatidylinositol-anchored member of the immunoglobulin superfamily related to chicken contactin. J. Cell Biol., 109, 775-788.
19. Hasler, T.H., Rader, C., Stoeckli, E.T., Zuellig, R.A. and Sonderegger, P. (1993) cDNA cloning, structural features and eucaryotic expression of human TAG-1/axonin-1. Eur. J. Biochem., 211, 329-339.
20. Hlavin, M.L. and Lemmon, V. (1991) Molecular structure and functional testing of human L1CAM. Genomics, 11, 416-423.
21. Holm, J., Appel, F. and Schachner, M. (1994) Several extracellular domains of the neural cell adhesion molecule L1 are involved in homophilic interactions. J. Neurosci. Res., 42, 9-20.
22. Jouet, M. and Kenwrick, S. (1995) Gene analysis of L1 neural cell adhesion molecule in prenatal diagnosis of hydrocephalus. Lancet, 345, 161-162.
23. Jouet, M., Feldman, E., Yates, J., Donnai, D., Paterson, J., Siggers.D. and Kenwrick , S. (1993) Refining the genetic location of the gene for X-linked hydrocephalus within Xq28. J. Med. Genet., 30, 214-217.
24. Jouet, M. et al. (1994) X-linked spastic paraplegia (SPG1), MASA syndrome and X-linked hydrocephalus result from mutations in the L1 gene. Nature Genet., 7, 402-407.
25. Kamiguchi, H. and Lemmon, V. (1997) Neural cell adhesion molecule L1: signalling pathways and growth cone motility. J. Neurosci. Res., 49, 1-8.
26. Ke, S.-H. and Madison, E. (1997) Rapid and efficient site-directed mutagenesis by single-tube 'megaprimer' PCR method. Nucleic Acids Res., 25, 3371-3372.
27. Kenwrick, S. and Doherty, P. (1998) Neural cell adhesion molecule L1: relating disease to function. BioEssays, 20, 668-675.
28. Kenwrick, S., Jouet, M. and Donnai, D. (1996) X-linked hydrocephalus and MASA syndrome. J. Med. Genet., 33, 59-65.
29. Krawczak, M., Reiss, R. and Cooper, D. (1992) The mutational spectrum of single base-pair substitutions in mRNA splice junctions of human genes: causes and consequences. Hum. Genet., 90, 41-54.
30. Kuhn, T.B., Stoeckli, E.T., Condrau, M.A., Rathjen, F.G. and Sonderegger, P. (1991) Neurite outgrowth on immobilized axonin-1 is mediated by a heterophilic interaction with L1 (G4). J. Cell Biol., 115, 1113-1126.
31. Kunz, S. et al. (1998) Neurite fasciculation mediated by complexes of axonin-1 and NgCAM. J. Cell Biol., 143, 1673-1690.
32. Lemmon, V., Farr, K.L. and Lagenaur, C. (1989) L1-mediated axon outgrowth occurs via a homophilic binding mechanism. Neuron, 2, 1597-1603.
33. Morales, G., Hubert, M., Brümmendorf, T., Treubert, U., Tarnok, A., Schwarz, U. and Rathjen, F.G. (1993) Induction of axonal growth by heterophilic interaction between the cell surface recognition proteins F11 and NrCAM/Bravo. Neuron, 11, 1113-1122.
34. Neilson, K. and Friesel, R. (1996) Ligand-independent activation of fibroblast growth factor receptor point mutations in the extracellular, transmembrane and kinase domains. J. Biol. Chem., 271, 25049-25057.
35. Rader, C. and Sonderegger, P. (1998) Structural features of neural immunoglobulin superfamily adhesion molecules. In Sonderegger, P. (ed.), Ig Superfamily Molecules in the Nervous System. Harwood Academic, Amsterdam, The Netherlands, pp. 1-22.
36. Rader, C., Kunz, B., Lierheimer, R., Giger, R., Berger, P., Tittman, T., Gross, H. and Sonderegger, P. (1996) Implications for the domain arrangement of axonin-1 derived from the mapping of its NgCAM binding site. EMBO J., 15, 2056-2068.
37. Rosenthal, A., Jouet, M. and Kenwrick, S. (1992) Aberrant splicing of L1CAM mRNA associated with X-linked hydrocephalus. Nature Genet., 2, 107-112.
38. Sakurai, T., Lustig, M., Nativ, M., Hemperley, J., Schlessinger, J., Peles, E. and Grumet, M. (1997) Induction of neurite outgrowth through contactin and NrCAM by extracellular regions of glial receptor tyrosine phosphataseβ. J. Cell Biol., 136, 907-918.
39. Saugier-Veber, P. et al. (1998) Identification of novel L1CAM mutations using fluorescence-assisted mismatch analysis. Hum. Mutat., 12, 259-266.
40. Simmons, D. (1993) Cloning cell surface molecules by transient expression in mammalian cells. In Hartley, D. (ed.). Cellular Interactions in Development. A Practical Approach. IRL Press, Oxford, UK, pp. 93-127.
41. Stoeckli, E.T., Ziegler, U., Bleiker, A.J., Groscurth, P. and Sonderegger, P. (1996) Clustering and functional cooperation of NgCAM and axonin-1 in the substratum-contact area of growth cones. Dev. Biol., 177, 15-29.
42. Su, X.-D., Gastinel, L., Vaughn, D., Faye, I., Poon, P. and Bjorkman, P. (1998) Crystal structure of hemolin: a horseshoe shape with implications for homophilic adhesion. Science, 281, 991-995.
43. Suter, D.M., Pollerberg, G.E., Buchstaller, A., Giger, R.J., Dreyer, W.J. and Sonderegger, P. (1995) Binding between the neural cell adhesion molecules axonin-1 and NrCAM/Bravo is involved in neuron-glia interaction. J. Cell Biol., 131, 1067-1081.
44. Treubert, U. and Brümmendorf, T. (1998) Functional cooperation of β1-integrins and members of the Ig superfamily in neurite outgrowth induction. J. Neurosci., 18, 1795-1805.
45. Vits, L. et al. (1994) MASA syndrome is due to mutations in the neural cell adhesion gene L1CAM. Nature Genet., 7, 408-413.
46. Volkmer, H., Leuschner, R., Zacharias, U. and Rathjen, F.G. (1996) Neurofascin induces neuntes by heterophilic interactions with axonal NrCAM while NrCAM requires F11 on the axonal surface to extend neurites. J. Cell. Biol., 135, 1059-1069.
47. 1 which promote attachment and neurite formation of tectal cells. J. Cell Biol., 142, 1083-1093.
48. Wolff, J.M., Frank, R., Mujoo, K., Spiro, R.C., Reisfeld, R.A. and Rathjen, F.G. (1988) A human brain glycoprotein related to the mouse cell adhesion molecule L1. J. Biol. Chem., 263, 11943-11947.
49. Yamasaki, M., Arita, N., Hiraga, S., Izumoto, S., Morimoto, K., Nakatani, S., Fujitani, K., Sato, N. and Hayakawa, T. (1995) A clinical and neuroradiological study of X-linked hydrocephalus in Japan. J. Neurosurg., 83, 50-55.
50. Yamasaki, M., Thompson, P. and Lemmon, V. (1997) CRASH syndrome: mutations in L1CAM correlate with severity of the disease. Neuropediatrics, 28, 175-178.
51. Zhao, X. and Siu, C.-H. (1995) Colocalisation of the homophilic binding site and the neuritogenic activity of the cell adhesion molecule L1 to its second Ig domain. J. Biol. Chem., 270, 29413-29421.
52. Zhao, X., Yip, P. and Siu, C.-H. (1998) Identification of a homophilic binding site in immunoglobulin-like domain 2 of the cell adhesion molecule L1. J. Neurochem., 71, 960-971.