The C264Y missense mutation in the extracellular domain of L1 impairs protein trafficking in vitro and in vivo

Journal of Neuroscience

Volumn 23, Issue 1, 2003, Pages 277-286

  Rünker, Annette E ^a   Bartsch, Udo ^a   Nave, Klaus Armin ^b   Schachner, Melitta ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

Author keywords

Adhesion molecule; Human disease; L1; Missense mutation; Protein trafficking; Transgenic mouse

Indexed keywords

NERVE CELL ADHESION MOLECULE; PROTEIN; PROTEIN C264Y; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL SURFACE; CONTROLLED STUDY; EMBRYO; ENDOPLASMIC RETICULUM; GENE EXPRESSION; GENE LOCATION; GENE MUTATION; GENETIC TRANSFECTION; IN VITRO STUDY; IN VIVO STUDY; MISSENSE MUTATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN VARIANT; TRANSGENIC MOUSE;

EID: 0037220860     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-01-00277.2003     Document Type: Article

References (54)

1. Appel F, Holm J, Conscience JF, von Bohlen und Halbach F, Faissner A, James P, Schachner M (1995) Identification of the border between fibronectin type III homologous repeats 2 and 3 of the neural cell adhesion molecule L1 as a neurite outgrowth promoting and signal transducing domain. J Neurobiol 28:297-312.
2. Bateman A, Jouet M, MacFarlane J, Du JS, Kenwrick S, 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.
3. Bennett V, Chen L (2001) Ankyrins and cellular targeting of diverse membrane proteins to physiological sites. Curr Opin Cell Biol 13:61-67.
4. Bone LJ, Deschenes SM, Balice-Gordon RJ, Fischbeck KH, Scherer SS (1997) Connexin32 and X-linked Charcot-Marie-Tooth disease. Neurobiol Dis 4:221-230.
5. Bross P, Corydon TJ, Andresen BS, Jorgensen MM, Bolund L, Gregersen N (1999) Protein misfolding and degradation in genetic diseases. Hum Mutat 14:186-198.
6. Brümmendorf T, Kenwrick S, Rathjen FG (1998) Neural cell recognition molecule L1: From cell biology to human hereditary brain malformations. Curr Opin Neurobiol 8:87-97.
7. Burden-Gulley SM, Pendergast M, Lemmon V (1997) The role of cell adhesion molecule L1 in axonal extension, growth cone motility, and signal transduction. Cell Tissue Res 290:415-422.
8. Cohen NR, Taylor JS, Scott LB, Guillery RW, Soriano P, Furley AJ (1998) Errors in corticospinal axon guidance in mice lacking the neural cell adhesion molecule L1. Curr Biol 8:26-33.
9. Crossin KL, Krushel LA (2000) Cellular signaling by neural cell adhesion molecules of the immunoglobulin superfamily. Dev Dyn 218:260-279.
10. 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.
11. De Angelis E, MacFarlane J, Du JS, Yeo G, Hicks R, Rathjen FG, Kenwrick S, Brummendorf T (1999) Pathological missense mutations of neural cell adhesion molecule L1 affect homophilic and heterophilic binding activities. EMBO J 18:4744-4753.
12. De Angelis E, Watkins A, Schafer M, Brummendorf T, Kenwrick S (2002) Disease-associated mutations in L1 CAM interfere with ligand interactions and cell-surface expression. Hum Mol Genet 11:1-12.
13. Demyanenko GP, Tsai AY, Maness PF (1999) Abnormalities in neuronal process extension, hippocampal development, and the ventricular system of L1 knock-out mice. J Neurosci 19:4907-4920.
14. Demyanenko GP, Shibata Y, Maness PF (2001) Altered distribution of dopaminergic neurons in the brain of L1 null mice. Dev Brain Res 126:21-30.
15. Deschenes SM, Walcott JL, Wexler TL, Scherer SS, Fischbeck KH (1997) Altered trafficking of mutant connexin32. J Neurosci 17:9077-9084.
16. Faissner A, Teplow DB, Kubler D, Keilhauer G, Kinzel V, Schachner M (1985) Biosynthesis and membrane topography of the neural cell adhesion molecule L1. EMBO J 4:3105-3113.
17. Fransen E, Lemmon V, van Camp G, Vits L, Coucke P, Willems PJ (1995) CRASH syndrome: Clinical spectrum of corpus callosum hypoplasia, retardation, adducted thumbs, spastic paraparesis and hydrocephalus due to mutations in one single gene, L1. Eur J Hum Genet 3:273-284.
18. Fransen E, van Camp G, D'Hooge R, Vits L, Willems PJ (1998) Genotypephenotype correlation in L1 associated diseases. J Med Genet 35:399-404.
19. Frederick JM, Krasnoperova V, Hoffmann K, Church-Kopish J, Ruther K, Howes K, Lem J, Baehr W (2001) Mutant rhodopsin transgene expression on a null background. Invest Ophthalmol Vis Sci 42:826-833.
20. Gow A, Southwood CM, Lazzarini RA (1998) Disrupted proteolipid protein trafficking results in oligodendrocyte apoptosis in an animal model of Pelizaeus-Merzbacher disease. J Cell Biol 140:925-934.
21. Haney CA, Sahenk Z, Li C, Lemmon VP, Roder J, Trapp BD (1999) Heterophilic binding of L1 on unmyelinated sensory axons mediates Schwann cell adhesion and is required for axonal survival. J Cell Biol 146:1173-1184.
22. Helenius A, Aebi M (2001) Intracellular functions of N-linked glycans. Science 291:2364-2369.
23. Hogan BLM, Beddington R, Constantini F, Lacy E (1994) Manipulating the Mouse Embryo: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
24. Jensen TJ, Loo MA, Pind S, Williams DB, Goldberg AL, Riordan JR (1995) Multiple proteolytic systems, including the proteasome, contribute to CFTR processing. Cell 83:129-135.
25. Jouet M, Rosenthal A, MacFarlane J, Kenwrick S, Donnai D (1993) A missense mutation confirms the L1 defect in X-linked hydrocephalus (HSAS). Nat Genet 4:331.
26. Jung M, Sommer I, Schachner M, Nave KA (1996) Monoclonal antibody O10 defines a conformationally sensitive cell-surface epitope of proteo-lipid protein (PLP): Evidence that PLP misfolding underlies dysmyelination in mutant mice. J Neurosci 16:7920-7929.
27. Kallunki P, Edelman GM, Jones FS (1997) Tissue-specific expression of the L1 cell adhesion molecule is modulated by the neural restrictive silencer element. J Cell Biol 138:1343-1354.
28. Kallunki P, Edelman GM, Jones FS (1998) The neural restrictive silencer element can act as both a repressor and enhancer of L1 cell adhesion molecule gene expression during postnatal development. Proc Natl Acad Sci USA 95:3233-3238.
29. Kenwrick S, Watkins A, De Angelis E (2000) Neural cell recognition molecule L1: Relating biological complexity to human disease mutations. Hum Mol Genet 9:879-886.
30. Lemmon V, Farr KL, Lagenaur C (1989) L1-mediated axon outgrowth occurs via a homophilic binding mechanism. Neuron 2:1597-1603.
31. Mahadeva R, Stewart S, Bilton D, Lomas DA (1998) Alpha-1 antitrypsin deficiency alleles and severe cystic fibrosis lung disease. Thorax 53:1022-1024.
32. Meech R, Kallunki P, Edelman GM, Jones FS (1999) A binding site for homeodomain and Pax proteins is necessary for L1 cell adhesion molecule gene expression by Pax-6 and bone morphogenetic proteins. Proc Natl Acad Sci USA 96:2420-2425.
33. Michaelis RC, Du YZ, Schwartz CE (1998) The site of a missense mutation in the extracellular Ig or FN domains of LICAM influences infant mortality and the severity of X linked hydrocephalus. J Med Genet 35:901-904.
34. Michelson P, Hartwig C, Schachner M, Gal A, Veske A, Finckh U (2002) Missense mutations in the extracellular domain of the human neural cell adhesion molecule L1 reduce neurite outgrowth of murine cerebellar neurons. Hum Mutat, in press.
35. 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.
36. Moos M, Tacke R, Scherer H, Teplow D, Fruh K, Schachner M (1988) Neural adhesion molecule L1 as a member of the immunoglobulin superfamily with binding domains similar to fibronectin. Nature 334:701-703.
37. Moulding HD, Martuza RL, Rabkin SD (2000) Clinical mutations in the L1 neural cell adhesion molecule affect cell-surface expression. J Neurosci 20:5696-5702.
38. Needham LK, Thelen K, Maness PF (2001) Cytoplasmic domain mutations of the L1 cell adhesion molecule reduce L1-ankyrin interactions. J Neurosci 21:1490-1500.
39. Olsson JE, Gordon JW, Pawlyk BS, Roof D, Hayes A, Molday RS, Mukai S, Cowley GS, Berso EL, Dryja TP (1992) Transgenic mice with a rhodopsin mutation (Pro23 His): A mouse model of autosomal dominant retinitis pigmentosa. Neuron 282:266-270.
40. Parodi AJ (2000) Protein glycosylation and its role in protein folding. Annu Rev Biochem 69:69-93.
41. Rolf B, Kutsche M, Bartsch U (2001) Severe hydrocephalus in L1-deficient mice. Brain Res 891:247-252.
42. Sadoul K, Sadoul R, Faissner A, Schachner M (1988) Biochemical characterization of different molecular forms of the neural cell adhesion molecule L1. J Neurochem 50:510-521.
43. Sadoul R, Kirchhoff F, Schachner M (1989) A protein kinase activity is associated with and specifically phosphorylates the neural cell adhesion molecule L1. J Neurochem 53:1471-1478.
44. Schneider AM, Griffiths IR, Readhead C, Nave KA (1994) Dominant-negative action of the jimpy mutation in mice complemented with an autosomal transgene for myelin proteolipid protein. Proc Natl Acad Sci USA 92:4447-4451.
45. Takeda Y, Asou H, Murakami Y, Miura M, Kobayashi M, Uyemura K (1996) A nonneuronal isoform of cell adhesion molecule L1: Tissue-specific expression and functional analysis. J Neurochem 66:2338-2349.
46. Thelen K, Kedar V, Panicker AK, Schmid RS, Midkiff BR, Manness PF (2002) The neural cell adhesion molecule L1 potentiates integrin-dependent cell migration to extracellular matrix proteins. J Neurosci 22:4918-4931.
47. Van Camp G, Fransen E, Vits L, Raes G, Willems PJ (1996) A locus-specific mutation database for the neural cell adhesion molecule LICAM (Xq28). Hum Mutat 8:391.
48. Ward CL, Kopito RR (1994) Intracellular turnover of cystic fibrosis trans-membrane conductance regulator. Inefficient processing and rapid degradation of wild-type and mutant proteins. J Biol Chem 269:25710-25718.
49. Ward CL, Omura S, Kopito RR (1995) Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 83:121-127.
50. Weller S, Gartner J (2001) Genetic and clinical aspects of X-linked hydrocephalus (L1 disease): Mutations in the LICAM gene. Hum Mutat 18:1-12.
51. Wu Y, Whitman I, Molmenti E, Moore K, Hippenmeyer P, Perlmutter DH (1994) A lack in intracellular degradation of mutant alpha1-antitrypsin correlates with the liver disease phenotype in homozygous PiZZ alpha1-antitrypsin deficiency. Proc Natl Acad Sci USA 91:9014-9018.
52. Yamasaki M, Thompson P, Lemmon V (1997) CRASH syndrome: Mutations in LICAM correlate with severity of the disease. Neuropediatrics 28:175-178.
53. Zhao X, Yip PM, Siu CH (1998) Identification of a homophilic binding site in immunoglobulin-like domain 2 of the cell adhesion molecule L1. J Neurochem 71:960-971.
54. Zisch AH, Stallcup WB, Chong LD, Dahlin-Huppe K, Voshol J, Schachner M, Pasquale EB (1997) Tyrosine phosphorylation of L1 family adhesion molecules: Implication of the Eph kinase Cek5. J Neurosci Res 47:655-665.