Role of the cytoplasmic domain of the L1 cell adhesion molecule in brain development

Journal of Comparative Neurology

Volumn 518, Issue 7, 2010, Pages 1113-1132

  Nakamura, Yukiko ^a   Lee, Suni ^a,b   Haddox, Candace L ^a   Weaver, Eli J ^a,b   Lemmon, Vance P ^a,b  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b CASE WESTERN RESERVE UNIVERSITY   (United States)

Author keywords

Axon guidance; Fasciculationmyelin; Hydrocephalus; L1 CAM

Indexed keywords

NERVE CELL ADHESION MOLECULE L1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING SITE; BRAIN DEVELOPMENT; CONTROLLED STUDY; EMBRYO; MOTOR PERFORMANCE; MOUSE; MUTANT; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT;

ANIMALS; AXONS; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; BRAIN; CELL CULTURE TECHNIQUES; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MAZE LEARNING; MEMORY; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; MOTOR ACTIVITY; MUTATION; NEURAL CELL ADHESION MOLECULE L1; NEURONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SCIATIC NERVE; SPATIAL BEHAVIOR; TIME FACTORS;

EID: 77949421679     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22267     Document Type: Article

References (87)

1. Alamed J, Wilcock DM, Diamond DM, Gordon MN, Morgan D. 2006. Two-day radial-arm water maze learning and memory task; robust resolution of amyloid-related memory deficits in transgenic mice. Nat Protoc 1:1671-1679.
2. Barbin G, Aigrot MS, Charles P, Foucher A, Grumet M, Schachner M, Zalc B, Lubetzki C. 2004. Axonal cell-adhesion molecule L1 in CNS myelination. Neuron Glia Biol 1:65-72.
3. Brittis PA, Lemmon V, Rutishauser U, Silver J. 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.
4. Buhusi M, Schlatter MC, Demyanenko GP, Thresher R, Maness PF. 2008. L1 interaction with ankyrin regulates mediolateral topography in the retinocollicular projection. J Neurosci 28: 177-188.
5. Castellani V. 2002. The function of neuropilin/L1 complex. Adv Exp Med Biol 515:91-102.
6. Castellani V, Chedotal A, Schachner M, Faivre-Sarrailh C, Rougon G. 2000. Analysis of the L1-deficient mouse phenotype reveals cross-talk between Sema3A and L1 signaling pathways in axonal guidance. Neuron 27:237-249.
7. Castellani V, De Angelis E, Kenwrick S, Rougon G. 2002. Cis and trans interactions of L1 with neuropilin-1 control axonal responses to semaphorin 3A. EMBO J 21:6348-6357.
8. Chen L, Ong B, 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.
9. Cheng L, Itoh K, Lemmon V. 2005a. L1-mediated branching is regulated by two ezrin-radixin-moesin (ERM)-binding sites, the RSLE region and a novel juxtamembrane ERM-binding region. J Neurosci 25:395-403.
10. Cheng L, Lemmon S, Lemmon V. 2005b. RanBPM is an L1-interacting protein that regulates L1-mediated mitogenactivated protein kinase activation. J Neurochem 94:1102-1110.
11. 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.
12. 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.
13. Davis JQ, 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.
14. Demyanenko GP, Shibata Y, Maness PF. 2001. Altered distribution of dopaminergic neurons in the brain of L1 null mice. Brain Res Dev Brain Res 126:21-30.
15. Dequidt C, Danglot L, Alberts P, Galli T, Choquet D, Thoumine O. 2007. Fast turnover of L1 adhesions in neuronal growth cones involving both surface diffusion and exo/endocytosis of L1 molecules. Mol Biol Cell 18:3131-3143.
16. Dickson TC, Mintz CD, Benson DL, Salton SR. 2002. Functional binding interaction identified between the axonal CAM L1 and members of the ERM family. J Cell Biol 157:1105-1112.
17. Dotti CG, Banker GA, Binder LI. 1987. The expression and distribution of the microtubule-associated proteins tau and microtubule-associated protein 2 in hippocampal neurons in the rat in situ and in cell culture. Neuroscience 23:121-130.
18. Felsenfeld DP, Hynes MA, Skoler KM, Furley AJ, Jessell TM. 1994. TAG-1 can mediate homophilic binding, but neurite outgrowth on TAG-1 requires an L1-like molecule and beta 1 integrins. Neuron 12:675-690.
19. Fransen E, Van Camp G, Vits L, Willems PJ. 1997. L1-associated diseases: clinical geneticists divide, molecular geneticists unite. Hum Mol Genet 6:1625-1632.
20. Fransen E, D'Hooge R, Van Camp G, Verhoye M, Sijbers J, Reyniers E, Soriano P, Kamiguchi H, Willemsen R, Koekkoek SK, De Zeeuw CI, De Deyn PP, Van der Linden A, Lemmon V, Kooy RF, Willems PJ. 1998. L1 knockout mice show dilated ventricles, vermis hypoplasia and impaired exploration patterns. Hum Mol Genet 7:999-1009.
21. Garver TD, Ren Q, Tuvia S, Bennett V. 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.
22. Gil OD, Sakurai T, Bradley AE, Fink MY, Cassella MR, Kuo JA, Felsenfeld DP. 2003. Ankyrin binding mediates L1CAM interactions with static components of the cytoskeleton and inhibits retrograde movement of L1CAM on the cell surface. J Cell Biol 162:719-730.
23. Godenschwege TA, Kristiansen LV, Uthaman SB, Hortsch M, Murphey RK. 2006. A conserved role for Drosophila Neuroglian and human L1-CAM in central-synapse formation. Curr Biol 16:12-23.
24. Grumet M, Edelman GM. 1988. Neuron-glia cell adhesion molecule interacts with neurons and astroglia via different binding mechanisms. J Cell Biol 106:487-503.
25. Grumet M, Friedlander DR, Edelman GM. 1993. Evidence for the binding of Ng-CAM to laminin. Cell Adhes Commun 1:177-190.
26. Halliday J, Chow CW, Wallace D, Danks DM. 1986. X linked hydrocephalus: a survey of a 20 year period in Victoria, Australia. J Med Genet 23:23-31.
27. 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.
28. Haspel J, Grumet M. 2003. The L1CAM extracellular region: a multi-domain protein with modular and cooperative binding modes. Front Biosci 8:s1210-1225.
29. Holtzman RN, Garcia L, Koenigsberger R. 1976. Hydrocephalus and congenital clasped thumbs: a case report with electromyographic evaluation. Dev Med Child Neurol 18:521-524.
30. Hortsch M. 1996. The L1 family of neural cell adhesion molecules: old proteins performing new tricks. Neuron 17:587-593.
31. Hortsch M. 2000. Structural and functional evolution of the L1 family: are four adhesion molecules better than one? Mol Cell Neurosci 15:1-10.
32. Hortsch M, Nagaraj K, Godenschwege TA. 2009. The interaction between L1-type proteins and ankyrins-a master switch for L1-type CAM function. Cell Mol Biol Lett 14:57-69.
33. Islam R, Kristiansen LV, Romani S, Garcia-Alonso L, Hortsch M. 2004. Activation of EGF receptor kinase by L1-mediated homophilic cell interactions. Mol Biol Cell 15:2003-2012.
34. Itoh K, Cheng L, Kamei Y, Fushiki S, Kamiguchi H, Gutwein P, Stoeck A, Arnold B, Altevogt P, Lemmon V. 2004. Brain development in mice lacking L1-L1 homophilic adhesion. J Cell Biol 165:145-154.
35. Itoh K, Fushiki S, Kamiguchi H, Arnold B, Altevogt P, Lemmon V. 2005. Disrupted Schwann cell-axon interactions in peripheral nerves of mice with altered L1-integrin interactions. Mol Cell Neurosci 30:131-136.
36. Johnstone M, Goold RG, Fischer I, Gordon-Weeks PR. 1997. The neurofilament antibody RT97 recognises a developmentally regulated phosphorylation epitope on microtubule-associated protein 1B. J Anat 191:229-244.
37. Kamiguchi H, Lemmon V. 1998. A neuronal form of the cell adhesion molecule L1 contains a tyrosine-based signal required for sorting to the axonal growth cone. J Neurosci 18:3749-3756.
38. Kamiguchi H, Lemmon V. 2000a. IgCAMs: bidirectional signals underlying neurite growth. Curr Opin Cell Biol 12:598-605.
39. Kamiguchi H, Lemmon V. 2000b. Recycling of the cell adhesion molecule L1 in axonal growth cones. J Neurosci 20:3676-3686.
40. Kamiguchi H, Hlavin ML, Lemmon V. 1998a. Role of L1 in neural development: what the knockouts tell us. Mol Cell Neurosci 12:48-55.
41. Kamiguchi H, Long KE, Pendergast M, Schaefer AW, Rapoport I, Kirchhausen T, Lemmon V. 1998b. 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.
42. Kanemura Y, Takuma Y, Kamiguchi H, Yamasaki M. 2005. First case of L1CAM gene mutation identified in MASA syndrome in Asia. Congenit Anom (Kyoto) 45:67-69.
43. Kanemura Y, Okamoto N, Sakamoto H, Shofuda T, Kamiguchi H, Yamasaki M. 2006. Molecular mechanisms and neuroimaging criteria for severe L1 syndrome with X-linked hydrocephalus. J Neurosurg 105(5 Suppl):403-412.
44. Kenwrick S, Jouet M, Donnai D. 1996. X linked hydrocephalus and MASA syndrome. J Med Genet 33:59-65.
45. Kuhn TB, Stoeckli ET, Condrau MA, Rathjen FG, Sonderegger P. 1991. Neurite outgrowth on immobilized axonin-1 is mediated by a heterophilic interaction with L1(G4). J Cell Biol 115: 1113-1126.
46. Kulahin N, Li S, Hinsby A, Kiselyov V, Berezin V, Bock E. 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.
47. Lagenaur C, Lemmon V. 1987. An L1-like molecule, the 8D9 antigen, is a potent substrate for neurite extension. Proc Natl Acad Sci U S A 84:7753-7757.
48. Law JW, Lee AY, Sun M, Nikonenko AG, Chung SK, Dityatev A, Schachner M, Morellini F. 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.
49. Liljelund P, Ghosh P, van den Pol AN. 1994. Expression of the neural axon adhesion molecule L1 in the developing and adult rat brain. J Biol Chem 269:32886-32895.
50. Lindner J, Rathjen FG, Schachner M. 1983. L1 mono-and polyclonal antibodies modify cell migration in early postnatal mouse cerebellum. Nature 305:427-430.
51. Macias VR, Day DW, King TE, Wilson GN. 1992. Clasped-thumb mental retardation (MASA) syndrome: confirmation of linkage to Xq28. Am J Med Genet 43:408-414.
52. Maness PF, Schachner M. 2007. Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nat Neurosci 10:19-26.
53. 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 U S A 96:2420-2425.
54. Mintz CD, Dickson TC, Gripp ML, Salton SR, Benson DL. 2003. ERMs colocalize transiently with L1 during neocortical axon outgrowth. J Comp Neurol 464:438-448.
55. Mintz CD, Carcea I, McNickle DG, Dickson TC, Ge Y, Salton SR, Benson DL. 2008. ERM proteins regulate growth cone responses to Sema3A. J Comp Neurol 510:351-366.
56. Montgomery AM, Becker JC, Siu CH, Lemmon VP, Cheresh DA, Pancook JD, Zhao X, Reisfeld RA. 1996. Human neural cell adhesion molecule L1 and rat homologue NILE are ligands for integrin alpha v beta 3. J Cell Biol 132:475-485.
57. Munakata H, Nakamura Y, Matsumoto-Miyai K, Itoh K, Yamasaki H, Shiosaka S. 2003. Distribution and densitometry mapping of L1-CAM immunoreactivity in the adult mouse brain-light microscopic observation. BMC Neurosci 4:7.
58. Nakamura Y, Tamura H, Horinouchi K, Shiosaka S. 2006. Role of neuropsin in formation and maturation of Schaffer-collateral L1cam-immunoreactive synaptic boutons. J Cell Sci 119: 1341-1349.
59. Nishimura K, Yoshihara F, Tojima T, Ooashi N, Yoon W, Mikoshiba K, Bennett V, Kamiguchi H. 2003. L1-dependent neuritogenesis involves ankyrinB that mediates L1-CAM coupling with retrograde actin flow. J Cell Biol 163:1077-1088.
60. Ogawa Y, Schafer DP, Horresh I, Bar V, Hales K, Yang Y, Susuki K, Peles E, Stankewich MC, Rasband MN. 2006. Spectrins and ankyrinB constitute a specialized paranodal cytoskeleton. J Neurosci 26:5230-5239.
61. O'Gorman S, Dagenais NA, Qian M, Marchuk Y. 1997. Protamine-Cre recombinase transgenes efficiently recombine target sequences in the male germ line of mice, but not in embryonic stem cells. Proc Natl Acad Sci U S A 94:14602-14607.
62. Ohyama K, Tan-Takeuchi K, Kutsche M, Schachner M, Uyemura K, Kawamura K. 2004. Neural cell adhesion molecule L1 is required for fasciculation and routing of thalamocortical fibres and corticothalamic fibres. Neurosci Res 48:471-475.
63. Pavlou O, Theodorakis K, Falk J, Kutsche M, Schachner M, Faivre-Sarrailh C, Karagogeos D. 2002. Analysis of interactions of the adhesion molecule TAG-1 and its domains with other immunoglobulin superfamily members. Mol Cell Neurosci 20: 367-381.
64. Pratte M, Rougon G, Schachner M, Jamon M. 2003. Mice deficient for the close homologue of the neural adhesion cell L1 (CHL1) display alterations in emotional reactivity and motor coordination. Behav Brain Res 147:31-39.
65. Rathjen FG, 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.
66. Rolf B, Kutsche M, Bartsch U. 2001. Severe hydrocephalus in L1-deficient mice. Brain Res 891:247-252.
67. Runker AE, Bartsch U, Nave KA, Schachner M. 2003. The C264Y missense mutation in the extracellular domain of L1 impairs protein trafficking in vitro and in vivo. J Neurosci 23:277-286.
68. Ruppert M, Aigner S, Hubbe M, Yagita H, Altevogt P. 1995. The L1 adhesion molecule is a cellular ligand for VLA-5. J Cell Biol 131:1881-1891.
69. Sakurai T, Lustig M, Babiarz J, Furley AJ, Tait S, Brophy PJ, Brown SA, Brown LY, Mason CA, Grumet M. 2001. Overlapping functions of the cell adhesion molecules Nr-CAM and L1 in cerebellar granule cell development. J Cell Biol 154:1259-1273.
70. Sakurai T, Gil OD, Whittard JD, Gazdoiu M, Joseph T, Wu J, Waksman A, Benson DL, Salton SR, Felsenfeld DP. 2008. Interactions between the L1 cell adhesion molecule and ezrin support traction-force generation and can be regulated by tyrosine phosphorylation. J Neurosci Res 86:2602-2614.
71. Sampo B, Kaech S, Kunz S, Banker G. 2003. Two distinct mechanisms target membrane proteins to the axonal surface. Neuron 37:611-624.
72. Schaefer AW, Kamei Y, Kamiguchi H, Wong EV, Rapoport I, Kirchhausen T, Beach CM, Landreth G, Lemmon SK, Lemmon V. 2002. L1 endocytosis is controlled by a phosphorylation-dephosphorylation cycle stimulated by outside-in signaling by L1. J Cell Biol 157:1223-1232.
73. Scotland P, Zhou D, Benveniste H, Bennett V. 1998. Nervous system defects of AnkyrinB (-/-) mice suggest functional overlap between the cell adhesion molecule L1 and 440-kD AnkyrinB in premyelinated axons. J Cell Biol 143:1305-1315.
74. Shin DH, Lee KS, Lee E, Cho SS, Kim J, Kim JW, Kwon BS, Lee HW, Lee WJ. 2003. The correspondence between the labeling patterns of antibody RT97, neurofilaments, microtubule associated protein 1B and tau varies with cell types and development stages of chicken retina. Neurosci Lett 342:167-170.
75. Stallcup WB, Beasley L. 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 U S A 82:1276-1280.
76. Triana-Baltzer GB, Liu Z, Berg DK. 2006. Pre-and postsynaptic actions of L1-CAM in nicotinic pathways. Mol Cell Neurosci 33:214-226.
77. Triana-Baltzer GB, Liu Z, Gounko NV, Berg DK. 2008. Multiple cell adhesion molecules shaping a complex nicotinic synapse on neurons. Mol Cell Neurosci 39:74-82.
78. Tybulewicz VL, Crawford CE, Jackson PK, Bronson RT, Mulligan RC. 1991. Neonatal lethality and lymphopenia in mice with a homozygous disruption of the c-abl proto-oncogene. Cell 65: 1153-1163.
79. Venero C, Tilling T, Hermans-Borgmeyer I, Herrero AI, Schachner M, Sandi C. 2004. Water maze learning and forebrain mRNA expression of the neural cell adhesion molecule L1. J Neurosci Res 75:172-181.
80. Voas MG, Lyons DA, Naylor SG, Arana N, Rasband MN, Talbot WS. 2007. AlphaII-spectrin is essential for assembly of the nodes of Ranvier in myelinated axons. Curr Biol 17:562-568.
81. Weller S, Gartner J. 2001. Genetic and clinical aspects of X-linked hydrocephalus (L1 disease): mutations in the L1CAM gene. Hum Mutat 18:1-12.
82. Whittard JD, Sakurai T, Cassella MR, Gazdoiu M, Felsenfeld DP. 2006. MAP kinase pathway-dependent phosphorylation of the L1-CAM ankyrin binding site regulates neuronal growth. Mol Biol Cell 17:2696-2706.
83. Wiencken-Barger AE, Mavity-Hudson J, Bartsch U, Schachner M, Casagrande VA. 2004. The role of L1 in axon pathfinding and fasciculation. Cereb Cortex 14:121-131.
84. Wisco D, Anderson ED, Chang MC, Norden C, Boiko T, Folsch H, Winckler B. 2003. Uncovering multiple axonal targeting pathways in hippocampal neurons. J Cell Biol 162:1317-1328.
85. Wolfer DP, Mohajeri HM, Lipp HP, Schachner M. 1998. Increased flexibility and selectivity in spatial learning of transgenic mice ectopically expressing the neural cell adhesion molecule L1 in astrocytes. Eur J Neurosci 10:708-717.
86. Yamasaki M, Thompson P, Lemmon V. 1997. CRASH syndrome: mutations in L1CAM correlate with severity of the disease. Neuropediatrics 28:175-178.
87. Yap CC, Nokes RL, Wisco D, Anderson E, Folsch H, Winckler B. 2008. Pathway selection to the axon depends on multiple targeting signals in NgCAM. J Cell Sci 121:1514-1525.