L1-type cell adhesion molecules: Distinct roles in synaptic targeting, organization, and function

The Sticky Synapse: Cell Adhesion Molecules and Their Role in Synapse Formation and Maintenance

Volumn , Issue , 2009, Pages 247-263

  Uthaman, Smitha Babu ^a   Godenschwege, Tanja Angela ^a  

^a FLORIDA ATLANTIC UNIVERSITY   (United States)

Author keywords

Ankyrin; Cytoskeleton; Immunoglobulin; L1 CAM; L1 syndrome; Synapse formation

Indexed keywords

EID: 84920126928     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-0-387-92708-4_12     Document Type: Chapter

References (113)

1. Allen MJ and Murphey RK (2007) The chemical component of the mixed GF-TTMn synapse in Drosophila melanogaster uses acetylcholine as its neurotransmitter. Euro J Neurosci 26:439-445.
2. Angeloni D, WeiMHand Lerman MI (1999) Two single nucleotide polymorphisms (SNPs) in the CALL gene for association studies with IQ. Psychiatric genetics 9(3):165-167.
3. Ango F, di Cristo G, Higashiyama H et al. (2004) Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at purkinje axon initial segment. Cell 119:257-272.
4. Arami S, Jucker M, Schachner M et al. (1996) The effect of continuous intraventricular infusion of L1 and NCAM antibodies on spatial learning in rats. Behav Brain Res 81:81-87.
5. Bains JS and Oliet SH (2007) Glia: They make your memories stick! Trends Neurosci 30:417-424.
6. Bayer SA and Altman J (1987) Directions in neurogenetic gradients and patterns of anatomical connections in the telencephalon. Prog Neurobiol 29:57-106.
7. Benson DL, Colman DR and Huntley GW (2001) Molecules, maps and synapse specificity. Nature Rev 2:899-909.
8. Bieber AJ, Snow PM, Hortsch M et al. (1989) Drosophila neuroglian: A member of the immunoglobulin superfamily with extensive homology to the vertebrate neural adhesion molecule L1. Cell 59:447-460.
9. Blaess S, Kammerer RA and Hall H (1998) Structural analysis of the sixth immunoglobulinlike domain of mouse neural cell adhesion molecule L1 and its interactions with alpha(v)- beta3, alpha(IIb)beta3, and alpha5beta1 integrins. J Neurochem 71:2615-2625.
10. Bliss T, Errington M, Fransen E et al. (2000) Long-term potentiation in mice lacking the neural cell adhesion molecule L1. Curr Biol 10:1607-1610.
11. Bouley M, Tian MZ, Paisley K et al. (2000) The L1-type cell adhesion molecule neuroglian influences the stability of neural ankyrin in the Drosophila embryo but not its axonal localization. J Neurosci 20:4515-4523.
12. Bronk P, Wenniger JJ, Dawson-Scully K et al. (2001) Drosophila Hsc70-4 is critical for neurotransmitter exocytosis in vivo. Neuron 30:475-488.
13. Brümmendorf T, Kenwrick S and Rathjen FG (1998) Neural cell recognition molecule L1: from cell biology to human hereditary brain malformations. Curr Opin Neurobiol 8:87-97.
14. Burkarth N, Kriebel M, Kranz EU et al. (2007) Neurofascin regulates the formation of gephyrin clusters and their subsequent translocation to the axon hillock of hippocampal neurons. Mol Cell Neurosci 36:59-70.
15. Caspi M, Atlas R, Kantor A et al. (2000) Interaction between LIS1 and doublecortin, two lissencephaly gene products. Human Mol Genet 9:2205-2213.
16. Castellani V, De Angelis E, Kenwrick S et al. (2002) Cis and trans interactions of L1 with neuropilin-1 control axonal responses to semaphorin 3A. EMBO J 21:6348-6357.
17. Chang KT and Berg DK (2001) Voltage-gated channels block nicotinic regulation of CREB phosphorylation and gene expression in neurons. Neuron 32:855-865.
18. Chen CL, Lampe DJ, Robertson HM et al. (1997) Neuroglian is expressed on cells destined to form the prothoracic glands of Manduca embryos as they segregate from surrounding cells and rearrange during morphogenesis. Dev Biol 181:1-13.
19. Chen L, Ong B and Bennett V (2001) LAD-1, the Caenorhabditis elegans L1CAM homologue, participates in embryonic and gonadal morphogenesis and is a substrate for fibroblast growth factor receptor pathway-dependent phosphotyrosine-based signaling. J Cell Biol 154:841-855.
20. Chen QY, Chen Q, Feng GY et al. (2005) Case-control association study of the close homologue of L1 (CHL1) gene and schizophrenia in the Chinese population. Schizophr Res 73:269-274.
21. Collingridge GL and Bliss TV (1995) Memories of NMDA receptors and LTP. Trends Neurosci 18:54-56.
22. Davey F, Hill M, Falk J et al. (2005) Synapse associated protein 102 is a novel binding partner to the cytoplasmic terminus of neurone-glial related cell adhesion molecule. J Neurochem 94:1243-1253.
23. Davis JQ and Bennett V (1994) Ankyrin binding activity shared by the neurofascin/L1/NrCAM family of nervous system cell adhesion molecules. J Biol Chem 269:27163-27166.
24. De Angelis E, MacFarlane J, Du JS et al. (1999) Pathological missense mutations of neural cell adhesion molecule L1 affect homophilic and heterophilic binding activities. EMBO J 18:4744-4753.
25. De Angelis E, Watkins A, Schafer M et al. (2002) Disease-associated mutations in L1 CAM interfere with ligand interactions and cell-surface expression. Human Mol Genet 11:1-12.
26. Dickson TC, Mintz CD, Benson DL et al. (2002) Functional binding interaction identified between the axonal CAM L1 and members of the ERM family. J Cell Biol 157:1105-1112.
27. Dirks P, Thomas U and Montag D (2006) The cytoplasmic domain of NrCAM binds to PDZ domains of synapse-associated proteins SAP90/PSD95 and SAP97. Euro J Neurosci 24:25-31.
28. Dubreuil RR, MacVicar G, Dissanayake S et al. (1996) Neuroglian-mediated cell adhesion induces assembly of the membrane skeleton at cell contact sites. J Cell Biol 133:647-655.
29. Essrich C, Lorez M, Benson JA et al. (1998) Postsynaptic clustering of major GABAA receptor subtypes requires the gamma 2 subunit and gephyrin. Nature Neurosci 1:563-571.
30. Falk J, Thoumine O, Dequidt C et al. (2004) NrCAM coupling to the cytoskeleton depends on multiple protein domains and partitioning into lipid rafts. Mol Biol Cell 15:4695-4709.
31. Felding-Habermann B, Silletti S, Mei F et al. (1997) A single immunoglobulin-like domain of the human neural cell adhesion molecule L1 supports adhesion by multiple vascular and platelet integrins. J Cell Biol 139:1567-1581.
32. Forni JJ, Romani S, Doherty P et al. (2004) Neuroglian and FasciclinII can promote neurite outgrowth via the FGF receptor Heartless. Mol Cell Neurosci 26:282-291.
33. Fransen E, D'Hooge R, Van Camp G et al. (1998a) L1 knockout mice show dilated ventricles, vermis hypoplasia and impaired exploration patterns. Human Mol Genet 7:999-1009.
34. Fransen E, Lemmon V, Van Camp G et al. (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 Human Genet 3:273-284.
35. Fransen E, Van Camp G, D'Hooge R et al. (1998b) Genotype-phenotype correlation in L1 associated diseases. J Med Genet 35:399-404.
36. Fransen E, Van Camp G, Vits L et al. (1997) L1-associated diseases: clinical geneticists divide, molecular geneticists unite. Human Mol Genet 6:1625-1632.
37. Freeman MR (2005) Glial control of synaptogenesis. Cell 120:292-293.
38. Freund TF and Buzsaki G(1996) Interneurons of the hippocampus. Hippocampus 6:347-470.
39. Frints SG, Marynen P, Hartmann D et al. (2003) CALL interrupted in a patient with nonspecific mental retardation: gene dosage-dependent alteration of murine brain development and behavior. Human Mol Genet 12:1463-1474.
40. Fritschy JM, Harvey RJ and Schwarz G(2008) Gephyrin: Where do we stand, where do we go? Trends Neurosci 31(5):257-264.
41. Garver TD, Ren Q, Tuvia S et al. (1997) Tyrosine phosphorylation at a site highly conserved in the L1 family of cell adhesion molecules abolishes ankyrin binding and increases lateral mobility of neurofascin. J Cell Biol 137:703-714.
42. Gerrow K and EI-Husseini A (2206) Cell adhesion molecules at the synapse. Front Biosci 11:2400-2419.
43. Godenschwege TA, Kristiansen LV, Uthaman SB et al. (2006) A conserved role for Drosophila Neuroglian and human L1-CAM in central-synapse formation. Curr Biol 16:12-23.
44. Greenberg ME, Ziff EB and Greene LA (1986) Stimulation of neuronal acetylcholine receptors induces rapid gene transcription. Science (New York, NY) 234:80-83.
45. Grumet M, Friedlander DR and Edelman GM (1993) Evidence for the binding of Ng-CAM to laminin. Cell Adhes Commun 1:177-190.
46. Grumet M, Mauro V, Burgoon MP et al. (1991) Structure of a new nervous system glycoprotein, Nr-CAM, and its relationship to subgroups of neural cell adhesion molecules. J Cell Biol 113:1399-1412.
47. Haspel J and Grumet M (2003) The L1CAM extracellular region: A multi-domain protein with modular and cooperative binding modes. Front Biosci 8:s1210-s1225.
48. Hassel B, Rathjen FG and Volkmer H (1997) Organization of the neurofascin gene and analysis of developmentally regulated alternative splicing. J Biol Chem 272:28742-28749.
49. Holm J, Hillenbrand R, Steuber V et al. (1996) Structural features of a close homologue of L1 (CHL1) in the mouse: A new member of the L1 family of neural recognition molecules. Eur J Neurosci 8:1613-1629.
50. Horstkorte R, Schachner M, Magyar JP et al. (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.
51. Hortsch M (1996) The L1 family of neural cell adhesion molecules: old proteins performing new tricks. Neuron 17:587-593.
52. Hortsch M (2000) Structural and functional evolution of the L1 family: Are four adhesion molecules better than one? Mol Cell Neurosci 15:1-10.
53. Hortsch M, Bieber AJ, Patel NH et al. (1990) Differential splicing generates a nervous systemspecific form of Drosophila neuroglian. Neuron 4:697-709.
54. Hortsch M, Homer D, Malhotra JD et al. (1998) Structural requirements for outside-in and inside-out signaling by Drosophila neuroglian, a member of the L1 family of cell adhesion molecules. J Cell Biol 142:251-261.
55. Huang ZJ (2006) Subcellular organization of GABAergic synapses: role of ankyrins and L1 cell adhesion molecules. Nature Neurosci 9:163-166.
56. Hutcheson HB, Olson LM, Bradford Y et al. (2004) Examination of NRCAM, LRRN3, KIAA0716, and LAMB1 as autism candidate genes. BMC Med Genet 5:12.
57. Islam R, Kristiansen LV, Romani S et al. (2004) Activation of EGF receptor kinase by L1- mediated homophilic cell interactions. Mol Biol Cell 15:2003-2012.
58. Itoh K, Ozaki M, Stevens B et al. (1997) Activity-dependent regulation of N-cadherin inDRG neurons: differential regulation of N-cadherin, NCAM, and L1 by distinct patterns of action potentials. J Neurobiol 33:735-748.
59. Itoh K, Shimono K and Lemmon V (2005) Dephosphorylation and internalization of cell adhesion molecule L1 induced by theta burst stimulation in rat hippocampus. Mol Cell Neurosci 29:245-249.
60. Itoh K, Stevens B, Schachner M et al. (1995) Regulated expression of the neural cell adhesion molecule L1 by specific patterns of neural impulses. Science (New York, NY) 270:1369-1372.
61. Jenkins SM and Bennett V (2001) Ankyrin-G coordinates assembly of the spectrin-based membrane skeleton, voltage-gated sodium channels, and L1 CAMs at Purkinje neuron initial segments. J Cell Biol 155:739-746.
62. Jenkins SM, Kizhatil K, Kramarcy NR et al. (2001) FIGQY phosphorylation defines discrete populations of L1 cell adhesion molecules at sites of cell-cell contact and in migrating neurons. J Cell Sci 114:3823-3835.
63. Kamiguchi H and Lemmon V (1997) Neural cell adhesion molecule L1: Signaling pathways and growth cone motility. J Neurosci Res 49:1-8.
64. Kamiguchi H and Lemmon V (2000) IgCAMs: bidirectional signals underlying neurite growth. Curr Opin Cell Biol 12:598-605.
65. Kamiguchi H, Long KE, Pendergast M et al. (1998) The neural cell adhesion molecule L1 interacts with the AP-2 adaptor and is endocytosed via the clathrin-mediated pathway. J Neurosci 18:5311-5321.
66. Kenwrick S, Watkins A and De Angelis E (2000) Neural cell recognition molecule L1: relating biological complexity to human disease mutations. Human Mol Genet 9:879-886.
67. Kizhatil K, Wu YX, Sen A et al. (2002) A new activity of doublecortin in recognition of the phospho-FIGQY tyrosine in the cytoplasmic domain of neurofascin. J Neurosci 22:7948-7958.
68. Krueger SR, Kolar A and Fitzsimonds RM (2003) The presynaptic release apparatus is functional in the absence of dendritic contact and highly mobile within isolated axons. Neuron 40:945-957.
69. Kuhn TB, Stoeckli ET, Condrau MA et al. (1991) Neurite outgrowth on immobilized axonin- 1 is mediated by a heterophilic interaction with L1(G4). J Cell Biol 115:1113-1126.
70. Kulahin N, Li S, Hinsby A et al. (2008) Fibronectin type III (FN3) modules of the neuronal cell adhesion molecule L1 interact directly with the fibroblast growth factor (FGF) receptor. Mol Cell Neurosci 37:528-536.
71. Kurumaji A, Nomoto H, Okano T et al. (2001) An association study between polymorphism of L1CAM gene and schizophrenia in a Japanese sample. Am J Med Genet 105:99-104.
72. Law JW, Lee AY, Sun M et al. (2003) Decreased anxiety, altered place learning, and increased CA1 basal excitatory synaptic transmission in mice with conditional ablation of the neural cell adhesion molecule L1. J Neurosci 23:10419-10432.
73. Leonard AS, Davare MA, HorneMC et al. (1998) SAP97 is associated with the alpha-amino- 3-hydroxy-5-methylisoxazole-4-propionic acid receptor GluR1 subunit. J Biol Chem 273:19518-19524.
74. Leshchyns'ka I, Sytnyk V, Richter M et al. (2006) The adhesion molecule CHL1 regulates uncoating of clathrin-coated synaptic vesicles. Neuron 52:1011-1025.
75. Luthi A, Mohajeri H, Schachner M et al. (1996) Reduction of hippocampal long-term potentiation in transgenic mice ectopically expressing the neural cell adhesion molecule L1 in astrocytes. J Neurosci Res 46:1-6.
76. Luthl A, Laurent JP, Figurov A et al. (1994) Hippocampal long-term potentiation and neural cell adhesion molecules L1 and NCAM. Nature 372:777-779.
77. Matsumoto-Miyai K, Ninomiya A, Yamasaki H et al. (2003) NMDA-dependent proteolysis of presynaptic adhesion molecule L1 in the hippocampus by neuropsin. J Neurosci 23:7727-7736.
78. Matzel LD, Babiarz J, Townsend DA, et al. (2008) Neuronal cell adhesion molecule deletion induces a cognitive and behavioral phenotype reflective of impulsivity. Genes, brain, and behavior 7(4):470-480.
79. Mehrke G, Jockusch H, Faissner A et al. (1984) Synapse formation and synaptic activity in mammalian nerve-muscle co-culture are not inhibited by antibodies to neural cell adhesion molecule L1. Neurosci Lett 44:235-239.
80. Mintz CD, Dickson TC, Gripp ML et al. (2003) ERMs colocalize transiently with L1 during neocortical axon outgrowth. J Comp Neurol 464:438-448.
81. Munakata H, Nakamura Y, Matsumoto-Miyai K et al. (2003) Distribution and densitometry mapping of L1-CAM immunoreactivity in the adult mouse brain - light microscopic observation. BMC neuroscience 4:7.
82. Nagaraj K and Hortsch M (2006) Phosphorylation of L1-type cell-adhesion molecules - Ankyrins away! Trends in biochemical sciences 31:544-546.
83. Nakamura Y, Tamura H, Horinouchi K et al. (2006) Role of neuropsin in formation and maturation of Schaffer-collateral L1cam-immunoreactive synaptic boutons. J Cell Sci 119:1341-1349.
84. Nikonenko AG, Sun M, Lepsveridze E et al. (2006) Enhanced perisomatic inhibition and impaired long-term potentiation in the CA1 region of juvenile CHL1-deficient mice. Euro J Neurosci 23:1839-1852.
85. Oleszewski M, Beer S, Katich S et al. (1999) Integrin and neurocan binding to L1 involves distinct Ig domains. J Biol Chem 274:24602-24610.
86. Rathjen FG and Schachner M (1984) Immunocytological and biochemical characterization of a new neuronal cell surface component (L1 antigen) which is involved in cell adhesion. Embo J 3:1-10.
87. Rathjen FG, Wolff JM, Chang S et al. (1987) Neurofascin: A novel chick cell-surface glycoprotein involved in neurite-neurite interactions. Cell 51:841-849.
88. Ren Q and Bennett V(1998) Palmitoylation of neurofascin at a site in the membrane-spanning domain highly conserved among the L1 family of cell adhesion molecules. J Neurochem 70:1839-1849.
89. Rose SP (1996) Cell adhesion molecules and the transition from short- To long-term memory. Journal of physiology, Paris 90(5-6):387-391.
90. Saghatelyan AK, Nikonenko AG, Sun M et al. (2004) Reduced GABAergic transmission and number of hippocampal perisomatic inhibitory synapses in juvenile mice deficient in the neural cell adhesion molecule L1. Mol Cell Neurosci 26:191-203.
91. Sakurai K, Migita O, Toru M et al. (2002) An association between a missense polymorphism in the close homologue of L1 (CHL1, CALL) gene and schizophrenia. Mol Psychiatry 7:412-415.
92. Sakurai T, Ramoz N, Reichert JG et al. (2006) Association analysis of the NrCAM gene in autism and in subsets of families with severe obsessive-compulsive or self-stimulatory behaviors. Psychiatr Genet 16:251-257.
93. Sanes JR, Schachner M and Covault J (1986) Expression of several adhesive macromolecules (N-CAM, L1, J1, NILE, uvomorulin, laminin, fibronectin, and a heparan sulfate proteoglycan) in embryonic, adult, and denervated adult skeletal muscle. J Cell Biol 102:420-431.
94. Sans N, Prybylowski K, Petralia RS et al. (2003) NMDA receptor trafficking through an interaction between PDZ proteins and the exocyst complex. Nature cell biology 5(6):520-530.
95. Schaefer AW, Kamei Y, Kamiguchi H et al. (2002) L1 endocytosis is controlled by a phosphorylation-dephosphorylation cycle stimulated by outside-in signaling by L1. J Cell Biol 157:1223-1232.
96. Schaefer AW, Kamiguchi H, Wong EV et al. (1999) Activation of the MAPK signal cascade by the neural cell adhesion molecule L1 requires L1 internalization. J Biol Chem 274:37965-37973.
97. Scherer M, HellerMand Schachner M(1992) Expression of the Neural Recognition Molecule L1 by Cultured Neural Cells is influenced by K+ and the Glutamate Receptor Agonist NMDA. Eur J Neurosci 4:554-562.
98. Scholey AB, Mileusnic R, Schachner M et al. (1995) A role for a chicken homolog of the neural cell adhesion molecule L1 in consolidation of memory for a passive avoidance task in the chick. Learn Memory (Cold Spring Harbor, NY) 2:17-25.
99. Seabold GK, Burette A, Lim IA et al. (2003) Interaction of the tyrosine kinase Pyk2 with the N-methyl-D-aspartate receptor complex via the Src homology 3 domains of PSD-95 and SAP102. J Biol Chem 278:15040-15048.
100. Silletti S, Mei F, Sheppard D et al. (2000) Plasmin-sensitive dibasic sequences in the third fibronectin-like domain of L1-cell adhesion molecule (CAM) facilitate homomultimerization and concomitant integrin recruitment. J Cell Biol 149:1485-1502.
101. Somogyi P, Tamas G, Lujan R et al. (1998) Salient features of synaptic organisation in the cerebral cortex. Brain Res 26:113-135.
102. Songyang Z, Fanning AS, Fu C et al. (1997) Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science (New York, NY) 275:73-77.
103. Tiunova A, Anokhin KV, Schachner M et al. (1998) Three time windows for amnestic effect of antibodies to cell adhesion molecule L1 in chicks. Neuroreport 9:1645-1648.
104. Todd KJ, Serrano A, Lacaille JC et al. (2006) Glial cells in synaptic plasticity. J Physiol, Paris 99:75-83.
105. Triana-Baltzer GB, Liu Z and Berg DK (2006) Pre- And postsynaptic actions of L1-CAM in nicotinic pathways. Mol Cell Neurosci 33:214-226.
106. Vallee RB, Tai C and Faulkner NE (2001) LIS1: cellular function of a disease-causing gene. Trends Cell Biol 11:155-160.
107. Von Bohlen Und Halbach F, Taylor J and Schachner M(1992) Cell type-specific effects of the neural adhesion molecules L1 and N-CAM on diverse second messenger systems. Euro J Neurosci 4:896-909.
108. Wang X, Zhang W, Cheever T et al. (2008) The C. elegans L1CAM homologue LAD-2 functions as a coreceptor in MAB-20/Sema2 mediated axon guidance. J Cell Biol 180:233-246.
109. Welzl H and Stork (2003) Cell adhesion molecules: key players in memory consolidation? News Physiol Sci 18:147-150.
110. Whittard JD, Sakurai T, Cassella MR et al. (2006) MAP kinase pathway-dependent phosphorylation of the L1-CAM ankyrin binding site regulates neuronal growth. Mol Biol Cell 17:2696-2706.
111. Wolfer DP, Mohajeri HM, Lipp HP et al. (1998) Increased flexibility and selectivity in spatial learning of transgenic mice ectopically expressing the neural cell adhesion molecule L1 in astrocytes. Euro J Neurosci 10:708-717.
112. Yamamoto M, Ueda R, Takahashi K et al. (2006) Control of axonal sprouting and dendrite branching by the Nrg-Ank complex at the neuron-glia interface. Curr Biol 16:1678-1683.
113. Zinsmaier KE and Bronk P (2001) Molecular chaperones and the regulation of neurotransmitter exocytosis. Biochem Pharmacol 62:1-11.