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Modulation of synaptic transmission and plasticity by cell adhesion and repulsion molecules

Published online by Cambridge University Press:  13 August 2009

Alexander Dityatev ,
Olena Bukalo  and
Melitta Schachner
Alexander Dityatev*
Affiliation:
Department of Neuroscience and Brain Technologies, Italian Institute of Technology, Genova, Italy
Olena Bukalo
Affiliation:
National Institutes of Health, National Institute of child Health and Human Development, Bethesda, MD, USA
Melitta Schachner
Affiliation:
Zentrum fuer Molekulare Neurobiologie Hamburg, Falkenried 94, Hamburg, Germany Keck Center for Collaborative Neuroscience and Department of Cell Biology and Neuroscience, Rutgers University, Piscataway, NJ, USA Center for Neuroscience, Shantou University Medical College, Shantou, China
*
Correspondence should be addressed to: Alexander Dityatev, Department of Neuroscience and Brain Technologies, The Italian Institute of Technology, 16163 Genova, Italy phone: +39-010-71781515 fax: +39-010-720321 email: alexander.dityatev@iit.it
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Abstract

Adhesive and repellent molecular cues guide migrating cells and growing neurites during development. They also contribute to synaptic function, learning and memory in adulthood. Here, we review the roles of cell adhesion molecules of the immunoglobulin superfamily (Ig-CAMs) and semaphorins (some of which also contain Ig-like domains) in regulation of synaptic transmission and plasticity. Interestingly, among the seven studied Ig-CAMs, the neuronal cell adhesion molecule proved to be important for all tested forms of hippocampal plasticity, while its associated unusual glycan polysialic acid is necessary and sufficient part for synaptic plasticity only at CA3-CA1 synapses. In contrast, Thy-1 and L1 specifically regulate long-term potentiation (LTP) at synapses formed by entorhinal axons in the dentate gyrus and cornu ammonis, respectively. Contactin-1 is important for long-term depression but not for LTP at CA3-CA1 synapses. Analysis of CHL1-deficient mice illustrates that at intermediate stages of development a deficit in a cell adhesion molecule is compensated but appears as impaired LTP during early and late postnatal development. The emerging mechanisms by which adhesive Ig-CAMs contribute to synaptic plasticity involve regulation of activities of NMDA receptors and L-type Ca2+ channels, signaling via mitogen-activated protein kinase p38, changes in GABAergic inhibition and motility of synaptic elements. Regarding repellent molecules, available data for semaphorins demonstrate their activity-dependent regulation in normal and pathological conditions, synaptic localization of their receptors and their potential to elevate or inhibit synaptic transmission either directly or indirectly.

Keywords

LTPLTDspinecell adhesionsynaptic plasticity
Type
Research Article
Information
Neuron Glia Biology , Volume 4 , Special Issue 3: Cell Adhesion and Extracellular Matrix Molecules in Synaptic Plasticity , August 2008 , pp. 197 - 209
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Anderson, R.B., Turner, K.N., Nikonenko, A.G., Hemperly, J., Schachner, M. and Young, H.M. (2006) The cell adhesion molecule l1 is required for chain migration of neural crest cells in the developing mouse gut. Gastroenterology 130, 1221–1232.CrossRefGoogle ScholarPubMed
Angata, K., Long, J.M., Bukalo, O., Lee, W., Dityatev, A., Wynshaw-Boris, A. et al. (2004) Sialyltransferase ST8Sia-II assembles a subset of polysialic acid that directs hippocampal axonal targeting and promotes fear behavior. Journal of Biological Chemistry 279, 32603–32613.Google Scholar
Ango, F., Wu, C., Van der Want, J.J., Wu, P., Schachner, M. and Huang, Z.J. (2008) Bergmann glia and the recognition molecule CHL1 organize GABAergic axons and direct innervation of Purkinje cell dendrites. PLoS Biology 6, e103.Google Scholar
Barnes, G., Puranam, R.S., Luo, Y. and McNamara, J.O. (2003) Temporal specific patterns of semaphorin gene expression in rat brain after kainic acid-induced status epilepticus. Hippocampus 13, 1–20.CrossRefGoogle ScholarPubMed
Becker, C.G., Artola, A., Gerardy-Schahn, R., Becker, T., Welzl, H. and Schachner, M. (1996) The polysialic acid modification of the neural cell adhesion molecule is involved in spatial learning and hippocampal long-term potentiation. Journal of Neuroscience Research 45, 143–152.Google Scholar
Bliss, T., Errington, M., Fransen, E., Godfraind, J.M., Kauer, J.A., Kooy, R.F. et al. (2000) Long-term potentiation in mice lacking the neural cell adhesion molecule L1. Current Biology 10, 1607–1610.CrossRefGoogle ScholarPubMed
Bouzioukh, F., Daoudal, G., Falk, J., Debanne, D., Rougon, G. and Castellani, V. (2006) Semaphorin3A regulates synaptic function of differentiated hippocampal neurons. European Journal of Neuroscience 23, 2247–2254.Google Scholar
Brennaman, L.H. and Maness, P.F. (2008) NCAM in neuropsychiatric and neurodegenerative disorders. Neurochemical Research [Epub ahead of print] doi: 10.1007/s11064-008-9630-z.CrossRefGoogle Scholar
Brose, K. and Tessier-Lavigne, M. (2000) Slit proteins: key regulators of axon guidance, axonal branching, and cell migration. Current Opinion Neurobiology 10, 95–102.CrossRefGoogle ScholarPubMed
Buhusi, M., Midkiff, B.R., Gates, A.M., Richter, M., Schachner, M. and Maness, P.F. (2003) Close homolog of L1 is an enhancer of integrin-mediated cell migration. Journal of Biological Chemistry 278, 25024–25031.Google Scholar
Bukalo, O., Fentrop, N., Lee, A.Y., Salmen, B., Law, J.W., Wotjak, C.T. et al. (2004) Conditional ablation of the neural cell adhesion molecule reduces precision of spatial learning, long-term potentiation, and depression in the CA1 subfield of mouse hippocampus. Journal of Neuroscience 24, 1565–1577.CrossRefGoogle ScholarPubMed
Burbach, J.P. and van der Zwaag, B. (2009) Contact in the genetics of autism and schizophrenia. Trends in Neuroscience 32, 69–72.Google Scholar
Burgaya, F., Fontana, X., Martínez, A., Montolio, M., Mingorance, A., Simó, S. et al. (2006) Semaphorin 6C leads to GSK-3-dependent growth cone collapse and redistributes after entorhino-hippocampal axotomy. Molecular and Cellular Neuroscience 33, 321–334.CrossRefGoogle ScholarPubMed
Burkhardt, C., Müller, M., Badde, A., Garner, C.C., Gundelfinger, E.D. and Püschel, A.W. (2005) Semaphorin 4B interacts with the post-synaptic density protein PSD-95/SAP90 and is recruited to synapses through a C-terminal PDZ-binding motif. FEBS Letters 579, 3821–3828.Google Scholar
Castellani, V., Chedotal, A., Schachner, M., Faivre-Sarrailh, C. and 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.CrossRefGoogle ScholarPubMed
Castellani, V., De Angelis, E., Kenwrick, S. and Rougon, G. (2002) Cis and trans interactions of L1 with neuropilin-1 control axonal responses to semaphorin 3A. EMBO Journal 21, 6348–6357.CrossRefGoogle ScholarPubMed
Castellani, V., Falk, J. and Rougon, G. (2004) Semaphorin3A-induced receptor endocytosis during axon guidance responses is mediated by L1 CAM. Molecular and Cellular Neuroscience 26, 89–100.CrossRefGoogle ScholarPubMed
Castellani, V. and Rougon, G. (2002) Control of semaphorin signaling. Current Opinion Neurobiology 12, 532–541.CrossRefGoogle ScholarPubMed
Chen, Q.Y., Chen, Q., Feng, G.Y., Lindpaintner, K., Chen, Y., Sun, X. et al. (2005) Case-control association study of the close homologue of L1 (CHL1) gene and schizophrenia in the Chinese population. Schizophrenia Research 73, 269–274.CrossRefGoogle ScholarPubMed
Chen, S., Mantei, N., Dong, L. and Schachner, M. (1999) Prevention of neuronal cell death by neural adhesion molecules L1 and CHL1. Journal of Neurobiology 38, 428–439.3.0.CO;2-6>CrossRefGoogle ScholarPubMed
Cremer, H., Chazal, G., Carleton, A., Goridis, C., Vincent, J.D. and Lledo, P.M. (1998) Long-term but not short-term plasticity at mossy fiber synapses is impaired in neural cell adhesion molecule-deficient mice. Proceedings of the National Academy of Sciences of the U.S.A. 95, 13242–13247.Google Scholar
Curreli, S., Arany, Z., Gerardy-Schahn, R., Mann, D. and Stamatos, N.M. (2007) Polysialylated neuropilin-2 is expressed on the surface of human dendritic cells and modulates dendritic cell-T lymphocyte interactions. Journal of Biological Chemistry 282, 30346–30356.Google Scholar
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 Genetics 17, 346–349.CrossRefGoogle ScholarPubMed
Darnell, J.C., Jensen, K.B., Jin, P., Brown, V., Warren, S.T. and Darnell, R.B. (2001) Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function. Cell 107, 489–499.CrossRefGoogle ScholarPubMed
de Wit, J., Toonen, R.F., Verhaagen, J. and Verhage, M. (2006) Vesicular trafficking of semaphorin 3A is activity-dependent and differs between axons and dendrites. Traffic 7, 1060–1077.Google Scholar
Demyanenko, G.P., Schachner, M., Anton, E., Schmid, R., Feng, G., Sanes, J. et al. (2004) Close homolog of L1 modulates area-specific neuronal positioning and dendrite orientation in the cerebral cortex. Neuron 44, 423–437.Google Scholar
Dickson, T.C., Mintz, C.D., Benson, D.L. and Salton, S.R. (2002) Functional binding interaction identified between the axonal CAM L1 and members of the ERM family. Journal of Cell Biology 157, 1105–1112.Google Scholar
Dityatev, A., Dityateva, G. and Schachner, M. (2000) Synaptic strength as a function of post- versus presynaptic expression of the neural cell adhesion molecule NCAM. Neuron 26, 207–217.Google Scholar
Dityatev, A., Dityateva, G., Sytnyk, V., Delling, M., Toni, N., Nikonenko, I. et al. (2004) Polysialylated neural cell adhesion molecule promotes remodeling and formation of hippocampal synapses. Journal of Neuroscience 24, 9372–9382.CrossRefGoogle ScholarPubMed
Dityatev, A. et al. (2008) NCAM-associated polysialic acid regulates synaptic plasticity by balancing the signaling through NR2A- and NR2B-containing NMDA receptors. FENS Abstracts, 4, 183.4.Google Scholar
Eastwood, S.L., Law, A.J., Everall, I.P. and Harrison, P.J. (2003) The axonal chemorepellant semaphorin 3A is increased in the cerebellum in schizophrenia and may contribute to its synaptic pathology. Molecular Psychiatry 8, 148–155.Google Scholar
Eckhardt, M., Bukalo, O., Chazal, G., Wang, L., Goridis, C., Schachner, M. et al. (2000) Mice deficient in the polysialyltransferase ST8SiaIV/PST-1 allow discrimination of the roles of neural cell adhesion molecule protein and polysialic acid in neural development and synaptic plasticity. Journal of Neuroscience 20, 5234–5244.CrossRefGoogle ScholarPubMed
Empson, R.M., Buckby, L.E., Kraus, M., Bates, K.J., Crompton, M.R., Gundelfinger, E.D. et al. (2006) The cell adhesion molecule neuroplastin-65 inhibits hippocampal long-term potentiation via a mitogen-activated protein kinase p38-dependent reduction in surface expression of GluR1-containing glutamate receptors. Journal of Neurochemistry 99, 850–860.CrossRefGoogle Scholar
Errington, M.L., Bliss, T.V., Morris, R.J., Laroche, S. and Davis, S. (1997) Long-term potentiation in awake mutant mice. Nature 387, 666–667.Google Scholar
Falk, J., Bechara, A., Fiore, R., Nawabi, H., Zhou, H., Hoyo-Becerra, C. et al. (2005) Dual functional activity of semaphorin 3B is required for positioning the anterior commissure. Neuron 48, 63–75.CrossRefGoogle ScholarPubMed
Falk, J., Bonnon, C., Girault, J.A. and Faivre-Sarrailh, C. (2002) F3/contactin, a neuronal cell adhesion molecule implicated in axogenesis and myelination. Biology of the Cell 94, 327–334.CrossRefGoogle ScholarPubMed
Frints, S.G., Marynen, P., Hartmann, D., Fryns, J.P., Steyaert, J., Schachner, M. et al. (2003) CALL interrupted in a patient with non-specific mental retardation: gene dosage-dependent alteration of murine brain development and behavior. Human Molecular Genetics 12, 1463–1474.Google Scholar
Furutani, Y., Matsuno, H., Kawasaki, M., Sasaki, T., Mori, K. and Yoshihara, Y. (2007) Interaction between telencephalin and ERM family proteins mediates dendritic filopodia formation. Journal of Neuroscience 27, 8866–8876.CrossRefGoogle ScholarPubMed
Fux, C.M., Krug, M., Dityatev, A., Schuster, T. and Schachner, M. (2003) NCAM180 and glutamate receptor subtypes in potentiated spine synapses: an immunogold electron microscopic study. Molecular and Cellular Neuroscience 24, 939–950.CrossRefGoogle ScholarPubMed
Good, P.F., Alapat, D., Hsu, A., Chu, C., Perl, D., Wen, X. et al. (2004) A role for semaphorin 3A signaling in the degeneration of hippocampal neurons during Alzheimer's disease. Journal of Neurochemistry 91, 716–736.Google Scholar
Hammond, M.S., Sims, C., Parameshwaran, K., Suppiramaniam, V., Schachner, M. and Dityatev, A. (2006) Neural cell adhesion molecule-associated polysialic acid inhibits NR2B-containing N-methyl-D-aspartate receptors and prevents glutamate-induced cell death. Journal of Biological Chemistry 281, 34859–34869.Google Scholar
Hillenbrand, R., Molthagen, M., Montag, D. and Schachner, M. (1999) The close homologue of the neural adhesion molecule L1 (CHL1): patterns of expression and promotion of neurite outgrowth by heterophilic interactions. European Journal of Neuroscience 11, 813–826.Google Scholar
Hino, H., Mori, K., Yoshihara, Y., Iseki, E., Akiyama, H., Nishimura, T. et al. (1997) Reduction of telencephalin immunoreactivity in the brain of patients with Alzheimer's disease. Brain Research 753, 353–357.CrossRefGoogle ScholarPubMed
Hollrigel, G.S., Morris, R.J. and Soltesz, I. (1998) Enhanced bursts of IPSCs in dentate granule cells in mice with regionally inhibited long-term potentiation. Proceedings Biological Science 265, 63–69.CrossRefGoogle ScholarPubMed
Holst, B.D., Vanderklish, P.W., Krushel, L.A., Zhou, W., Langdon, R.B., McWhirter, J.R. et al. (1998) Allosteric modulation of AMPA-type glutamate receptors increases activity of the promoter for the neural cell adhesion molecule, N-CAM. Proceedings of the National Academy of Sciences of the U.S.A. 95, 2597–2602.Google Scholar
Holtmaat, A.J., Gorter, J.A., De Wit, J., Tolner, E.A., Spijker, S., Giger, R.J. et al. (2003) Transient downregulation of Sema3A mRNA in a rat model for temporal lobe epilepsy. A novel molecular event potentially contributing to mossy fiber sprouting. Experimental Neurology 182, 142–150.CrossRefGoogle Scholar
Hou, S.T., Jiang, S.X. and Smith, R.A. (2008) Permissive and repulsive cues and signalling pathways of axonal outgrowth and regeneration. International Review of Cell and Molecular Biology 267, 125–181.CrossRefGoogle ScholarPubMed
Hsieh, H., Boehm, J., Sato, C., Iwatsubo, T., Tomita, T., Sisodia, S. et al. (2006) AMPAR removal underlies Abeta-induced synaptic depression and dendritic spine loss. Neuron 52, 831–843.CrossRefGoogle ScholarPubMed
Irintchev, A., Koch, M., Needham, L.K., Maness, P. and Schachner, M. (2004) Impairment of sensorimotor gating in mice deficient in the cell adhesion molecule L1 or its close homologue, CHL1. Brain Research 1029, 131–134.CrossRefGoogle ScholarPubMed
Jakovcevski, I., Wu, J., Karl, N., Leshchyns'ka, I., Sytnyk, V., Chen, J. et al. (2007) Glial scar expression of CHL1, the close homolog of the adhesion molecule L1, limits recovery after spinal cord injury. Journal of Neuroscience 27, 7222–7233.Google Scholar
Jorgensen, O.S. and Bock, E. (1974) Brain specific synaptosomal membrane proteins demonstrated by crossed immunoelectrophoresis. Journal of Neurochemistry 23, 879–880.CrossRefGoogle ScholarPubMed
Jouet, M., Rosenthal, A., Armstrong, G., MacFarlane, J., Stevenson, R., Paterson, J. et al. (1994) X-linked spastic paraplegia (SPG1), MASA syndrome and X-linked hydrocephalus result from mutations in the L1 gene. Nature Genetics 7, 402–407.CrossRefGoogle ScholarPubMed
Kadmon, G., Kowitz, A., Altevogt, P. and Schachner, M. (1990) Functional cooperation between the neural adhesion molecules L1 and N-CAM is carbohydrate dependent. Journal of Cell Biology 110, 209–218.CrossRefGoogle ScholarPubMed
Kantor, D.B., Chivatakarn, O., Peer, K.L., Oster, S.F., Inatani, M., Hansen, M.J. et al. (2004) Semaphorin 5A is a bifunctional axon guidance cue regulated by heparan and chondroitin sulfate proteoglycans. Neuron 44, 961–975.CrossRefGoogle ScholarPubMed
Kawaguchi, S.Y. and Hirano, T. (2006) Integrin alpha3beta1 suppresses long-term potentiation at inhibitory synapses on the cerebellar Purkinje neuron. Molecular and Cellular Neuroscience 31, 416–426.CrossRefGoogle ScholarPubMed
Kazarinova-Noyes, K., Malhotra, J.D., McEwen, D.P., Mattei, L.N., Berglund, E.O., Ranscht, B. et al. (2001) Contactin associates with Na+ channels and increases their functional expression. Journal of Neuroscience 21, 7517–7525.Google Scholar
Kesner, R.P. (2007) A behavioral analysis of dentate gyrus function. Progress in Brain Research 163, 567–576.Google Scholar
Kolodkin, A.L., Levengood, D.V., Rowe, E.G., Tai, Y.T., Giger, R.J. and Ginty, D.D. (1997) Neuropilin is a semaphorin III receptor. Cell 90, 753–762.CrossRefGoogle ScholarPubMed
Lamprecht, R. and LeDoux, J. (2004) Structural plasticity and memory. Nature Reviews. Neuroscience 5, 45–54.Google Scholar
Law, J.W., Lee, A.Y., Sun, M., Nikonenko, A.G., Chung, S.K., Dityatev, A. 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. Journal of Neuroscience 23, 10419–10432.Google Scholar
Leyton, L., Schneider, P., Labra, C.V., Ruegg, C., Hetz, C.A., Quest, A.F. et al. (2001) Thy-1 binds to integrin beta(3) on astrocytes and triggers formation of focal contact sites. Current Biology 11, 1028–1038.Google Scholar
Liu, J., Fukunaga, K., Yamamoto, H., Nishi, K. and Miyamoto, E. (1999) Differential roles of Ca(2+)/calmodulin-dependent protein kinase II and mitogen-activated protein kinase activation in hippocampal long-term potentiation. Journal of Neuroscience 19, 8292–8299.CrossRefGoogle ScholarPubMed
Lopez-Fernandez, M.A., Montaron, M.F., Varea, E., Rougon, G., Venero, C., Abrous, D.N. et al. (2007) Upregulation of polysialylated neural cell adhesion molecule in the dorsal hippocampus after contextual fear conditioning is involved in long-term memory formation. Journal of Neuroscience 27, 4552–4561.CrossRefGoogle ScholarPubMed
Lüthi, A., Laurent, J.P., Figurov, A., Muller, D. and Schachner, M. (1994) Hippocampal long-term potentiation and neural cell adhesion molecules L1 and NCAM. Nature 372, 777–779.CrossRefGoogle ScholarPubMed
Lüthi, A., Mohajeri, H., Schachner, M. and Laurent, J.P. (1996) Reduction of hippocampal long-term potentiation in transgenic mice ectopically expressing the neural cell adhesion molecule L1 in astrocytes. Journal of Neuroscience Research 46, 1–6.3.0.CO;2-P>CrossRefGoogle ScholarPubMed
Lynch, G., Rex, C.S., Chen, L.Y. and Gall, C.M. (2008) The substrates of memory: defects, treatments, and enhancement. European Journal of Pharmacology 585, 2–13.Google Scholar
Maness, P.F. and Schachner, M. (2007) Neural recognition molecules of the immunoglobulin superfamily: signaling transducers of axon guidance and neuronal migration. Nature Neuroscience 10, 19–26.Google Scholar
Mann, F., Chauvet, S. and Rougon, G. (2007) Semaphorins in development and adult brain: implication for neurological diseases. Progress in Neurobiology 82, 57–79.Google Scholar
Matsuno, H., Okabe, S., Mishina, M., Yanagida, T., Mori, K. and Yoshihara, Y. (2006) Telencephalin slows spine maturation. Journal of Neuroscience 26, 1776–1786.CrossRefGoogle ScholarPubMed
Mayeux-Portas, V., File, S.E., Stewart, C.L. and Morris, R.J. (2000) Mice lacking the cell adhesion molecule Thy-1 fail to use socially transmitted cues to direct their choice of food. Current Biology 10, 68–75.CrossRefGoogle ScholarPubMed
Melin, M., Carlsson, B., Anckarsater, H., Rastam, M., Betancur, C., Isaksson, A. et al. (2006) Constitutional downregulation of SEMA5A expression in autism. Neuropsychobiology 54, 64–69.CrossRefGoogle ScholarPubMed
Montag-Sallaz, M., Schachner, M. and Montag, D. (2002) Misguided axonal projections, neural cell adhesion molecule 180 mRNA upregulation, and altered behavior in mice deficient for the close homolog of L1. Molecular and Cellular Biology 22, 7967–7981.Google Scholar
Moore, S.W., Tessier-Lavigne, M. and Kennedy, T.E. (2007) Netrins and their receptors. Advances in Experimental and Medical Biology 621, 17–31.Google Scholar
Morellini, F., Lepsveridze, E., Kahler, B., Dityatev, A. and Schachner, M. (2007) Reduced reactivity to novelty, impaired social behavior, and enhanced basal synaptic excitatory activity in perforant path projections to the dentate gyrus in young adult mice deficient in the neural cell adhesion molecule CHL1. Molecular and Cellular Neuroscience 34, 121–136.Google Scholar
Morita, A., Yamashita, N., Sasaki, Y., Uchida, Y., Nakajima, O., Nakamura, F. et al. (2006) Regulation of dendritic branching and spine maturation by semaphorin3A-Fyn signaling. Journal of Neuroscience 26, 2971–2980.Google Scholar
Morris, R. (1992) Thy-1, the enigmatic extrovert on the neuronal surface. Bioessays 14, 715–722.Google Scholar
Morrow, E.M., Yoo, S.Y., Flavell, S.W., Kim, T.K., Lin, Y., Hill, R.S. et al. (2008) Identifying autism loci and genes by tracing recent shared ancestry. Science 321, 218–223.CrossRefGoogle ScholarPubMed
Muller, D., Djebbara-Hannas, Z., Jourdain, P., Vutskits, L., Durbec, P., Rougon, G. et al. (2000) Brain-derived neurotrophic factor restores long-term potentiation in polysialic acid-neural cell adhesion molecule-deficient hippocampus. Proceedings of the National Academy of Sciences of the U.S.A. 97, 4315–4320.Google Scholar
Muller, D., Mendez, P., De Roo, M., Klauser, P., Steen, S. and Poglia, L. (2008) Role of NCAM in spine dynamics and synaptogenesis. Neurochemical Research [Epub ahead of print] doi: 10.1007/s11064-008-9653-5.Google Scholar
Muller, D., Wang, C., Skibo, G., Toni, N., Cremer, H., Calaora, V. et al. (1996) PSA-NCAM is required for activity-induced synaptic plasticity. Neuron 17, 413–422.Google Scholar
Murai, K.K., Misner, D. and Ranscht, B. (2002) Contactin supports synaptic plasticity associated with hippocampal long-term depression but not potentiation. Current Biology 12, 181–190.CrossRefGoogle Scholar
Nägerl, U.V., Eberhorn, N., Cambridge, S.B. and Bonhoeffer, T. (2004) Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron 44, 759–767.CrossRefGoogle ScholarPubMed
Nakamura, K., Manabe, T., Watanabe, M., Mamiya, T., Ichikawa, R., Kiyama, Y. et al. (2001) Enhancement of hippocampal LTP, reference memory and sensorimotor gating in mutant mice lacking a telencephalon-specific cell adhesion molecule. European Journal of Neuroscience 13, 179–189.CrossRefGoogle ScholarPubMed
Nicoll, R.A. and Malenka, R.C. (1995) Contrasting properties of two forms of long-term potentiation in the hippocampus. Nature 377, 115–118.CrossRefGoogle ScholarPubMed
Niisato, K., Fujikawa, A., Komai, S., Shintani, T., Watanabe, E., Sakaguchi, G. et al. (2005) Age-dependent enhancement of hippocampal long-term potentiation and impairment of spatial learning through the Rho-associated kinase pathway in protein tyrosine phosphatase receptor type Z-deficient mice. Journal of Neuroscience 25, 1081–1088.Google Scholar
Nikonenko, A.G., Sun, M., Lepsveridze, E., Apostolova, I., Petrova, I., Irintchev, A. et al. (2006) Enhanced perisomatic inhibition and impaired long-term potentiation in the CA1 region of juvenile CHL1-deficient mice. European Journal of Neuroscience 23, 1839–1852.CrossRefGoogle ScholarPubMed
Nishiyama, M., von Schimmelmann, M.J., Togashi, K., Findley, W.M. and Hong, K. (2008) Membrane potential shifts caused by diffusible guidance signals direct growth-cone turning. Nature Neuroscience 11, 762–771.CrossRefGoogle ScholarPubMed
Nosten-Bertrand, M., Errington, M.L., Murphy, K.P., Tokugawa, Y., Barboni, E., Kozlova, E. et al. (1996) Normal spatial learning despite regional inhibition of LTP in mice lacking Thy-1. Nature 379, 826–829.CrossRefGoogle ScholarPubMed
Oka, S., Mori, K. and Watanabe, Y. (1990) Mammalian telencephalic neurons express a segment-specific membrane glycoprotein, telencephalin. Neuroscience 35, 93–103.CrossRefGoogle ScholarPubMed
Okamoto, K., Nagai, T., Miyawaki, A. and Hayashi, Y. (2004) Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nature Neuroscience 7, 1104–1112.Google Scholar
Pasterkamp, R.J. and Kolodkin, A.L. (2003) Semaphorin junction: making tracks toward neural connectivity. Current Opinion in Neurobiology 13, 79–89.CrossRefGoogle ScholarPubMed
Persohn, E., Pollerberg, G.E. and Schachner, M. (1989) Immunoelectron-microscopic localization of the 180 kD component of the neural cell adhesion molecule N-CAM in postsynaptic membranes. Journal of Comparative Neurology 288, 92–100.CrossRefGoogle ScholarPubMed
Pillai, A.M., Garcia-Fresco, G.P., Sousa, A.D., Dupree, J.L., Philpot, B.D. and Bhat, M.A. (2007) No effect of genetic deletion of contactin-associated protein (CASPR) on axonal orientation and synaptic plasticity. Journal of Neuroscience Research 85, 2318–2331.CrossRefGoogle ScholarPubMed
Pillai-Nair, N., Panicker, A.K., Rodriguiz, R.M., Gilmore, K.L., Demyanenko, G.P., Huang, J.Z. et al. (2005) Neural cell adhesion molecule-secreting transgenic mice display abnormalities in GABAergic interneurons and alterations in behavior. Journal of Neuroscience 25, 4659–4671.Google Scholar
Ponimaskin, E., Voyno-Yasenetskaya, T., Richter, D.W., Schachner, M. and Dityatev, A. (2007) Morphogenic signaling in neurons via neurotransmitter receptors and small GTPases. Molecular Neurobiology 35, 278–287.Google Scholar
Ronn, L.-C., Bock, E., Linnemann, D. and Jahnsen, H. (1995) NCAM-antibodies modulate induction of long-term potentiation in rat hippocampal CA1. Brain Research 677, 145–151.CrossRefGoogle ScholarPubMed
Rutishauser, U. (2008) Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nature Reviews. Neuroscience 9, 26–35.CrossRefGoogle ScholarPubMed
Saghatelyan, A.K., Nikonenko, A.G., Sun, M., Rolf, B., Putthoff, P., Kutsche, 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. Molecular and Cellular Neuroscience 26, 191–203.Google Scholar
Sahay, A., Kim, C.H., Sepkuty, J.P., Cho, E., Huganir, R.L., Ginty, D.D. et al. (2005) Secreted semaphorins modulate synaptic transmission in the adult hippocampus. Journal of Neuroscience 25, 3613–3620.Google Scholar
Sakurai, E., Hashikawa, T., Yoshihara, Y., Kaneko, S., Satoh, M. and Mori, K. (1998) Involvement of dendritic adhesion molecule telencephalin in hippocampal long-term potentiation. Neuroreport 9 881–886Google Scholar
Schlatter, M.C., Buhusi, M., Wright, A.G. and Maness, P.F. (2008) CHL1 promotes Sema3A-induced growth cone collapse and neurite elaboration through a motif required for recruitment of ERM proteins to the plasma membrane. Journal of Neurochemistry 104, 731–744.CrossRefGoogle ScholarPubMed
Schuch, U., Lohse, M.J. and Schachner, M. (1989) Neural cell adhesion molecules influence second messenger systems. Neuron 3, 13–20.CrossRefGoogle ScholarPubMed
Senkov, O., Schachner, M., Engel, A.K. and Dityatev, A. (2008) Restoration of fear memory in NCAM deficient mice by resetting a balance in signaling via NR2A- and NR2B-containing NMDA receptors. FENS Abstracts 4, 214.17.Google Scholar
Senkov, O., Sun, M., Weinhold, B., Gerardy-Schahn, R., Schachner, M. and Dityatev, A. (2006) Polysialylated neural cell adhesion molecule is involved in induction of long-term potentiation and memory acquisition and consolidation in a fear-conditioning paradigm. Journal of Neuroscience 26, 10888–10898.Google Scholar
Shimakawa, S., Suzuki, S., Miyamoto, R., Takitani, K., Tanaka, K., Tanabe, T. et al. (2002) Neuropilin-2 is overexpressed in the rat brain after limbic seizures. Brain Research 956, 67–73.Google Scholar
Shimoda, Y. and Watanabe, K. (2009) Contactins: emerging key roles in the development and function of the nervous system. Cell Adhesion & Migration 3, 64–70.Google Scholar
Skutella, T. and Nitch, R. (2001) New molecules for hippocampal development. Trends in Neuroscience 24, 107–113.Google Scholar
Smalla, K.H., Matthies, H., Langnase, K., Shabir, S., Bockers, T.M., Wyneken, U. et al. (2000) The synaptic glycoprotein neuroplastin is involved in long-term potentiation at hippocampal CA1 synapses. Proceedings of the National Academy of Sciences of the U.S.A. 97, 4327–4332.Google Scholar
Staubli, U., Chun, D. and Lynch, G. (1998) Time-dependent reversal of long-term potentiation by an integrin antagonist. Journal of Neuroscience 18, 3460–3469.Google Scholar
Stoenica, L., Senkov, O., Gerardy-Schahn, R., Weinhold, B., Schachner, M. and Dityatev, A. (2006) In vivo synaptic plasticity in the dentate gyrus of mice deficient in the neural cell adhesion molecule NCAM or its polysialic acid. European Journal of Neuroscience 23, 2255–2264.Google Scholar
Stork, O., Welzl, H., Wolfer, D., Schuster, T., Mantei, N., Stork, S. et al. (2000) Recovery of emotional behaviour in neural cell adhesion molecule (NCAM) null mutant mice through transgenic expression of NCAM180. European Journal of Neuroscience 12, 3291–3306.Google Scholar
Su, K.Y., Chien, W.L., Fu, W.M., Yu, I.S., Huang, H.P., Huang, P.H. et al. (2007) Mice deficient in collapsin response mediator protein-1 exhibit impaired long-term potentiation and impaired spatial learning and memory. Journal of Neuroscience 27, 2513–2524.CrossRefGoogle ScholarPubMed
Suto, F., Tsuboi, M., Kamiya, H., Mizuno, H., Kiyama, Y., Komai, S. et al. (2007) Interactions between plexin-A2, plexin-A4, and semaphorin 6A control lamina-restricted projection of hippocampal mossy fibers. Neuron 53, 535–547.Google Scholar
Sytnyk, V., Leshchyns'ka, I., Nikonenko, A.G. and Schachner, M. (2006) NCAM promotes assembly and activity-dependent remodeling of the postsynaptic signaling complex. Journal of Cell Biology 174, 1071–1085.CrossRefGoogle ScholarPubMed
Tada, T. and Sheng, M. (2006) Molecular mechanisms of dendritic spine morphogenesis. Current Opinion Neurobiology 16, 95–101.Google Scholar
Tamagnone, L. and Comoglio, P.M. (2000) Signalling by semaphorin receptors: cell guidance and beyond. Trends in Cell Biology 10, 377–383.CrossRefGoogle ScholarPubMed
Tamura, H., Fukada, M., Fujikawa, A. and Noda, M. (2006) Protein tyrosine phosphatase receptor type Z is involved in hippocampus-dependent memory formation through dephosphorylation at Y1105 on p190 RhoGAP. Neuroscience Letters 399, 33–38.Google Scholar
Tannahill, L., Klein, R. and Schachner, M. (1995) The neurotrophin receptors TrkA and TrkB are inhibitory for neurite outgrowth. European Journal of Neuroscience 7, 1424–1428.Google Scholar
Tashiro, A., Minden, A. and Yuste, R. (2000) Regulation of dendritic spine morphology by the rho family of small GTPases: antagonistic roles of Rac and Rho. Cerebral Cortex 10, 927–938.Google Scholar
Thiery, J.P., Brackenbury, R., Rutishauser, U. and Edelman, G.M. (1977) Adhesion among neural cells of the chick embryo. II. Purification and characterization of a cell adhesion molecule from neural retina. Journal of Biological Chemistry 252, 6841–6845.Google Scholar
Tian, L., Kilgannon, P., Yoshihara, Y., Mori, K., Gallatin, W.M., Carpen, O. et al. (2000) Binding of T lymphocytes to hippocampal neurons through ICAM-5 (telencephalin) and characterization of its interaction with the leukocyte integrin CD11a/CD18. European Journal of Immunology 30, 810–818.Google Scholar
Vaithianathan, T., Matthias, K., Bahr, B., Schachner, M., Suppiramaniam, V., Dityatev, A. et al. (2004) Neural cell adhesion molecule-associated polysialic acid potentiates alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor currents. Journal of Biological Chemistry 279, 47975–47984.CrossRefGoogle ScholarPubMed
Wang, L.H. and Strittmatter, S.M. (1996) A family of rat CRMP genes is differentially expressed in the nervous system. Journal of Neuroscience 16, 6197–6207.Google Scholar
Wang, Q., Walsh, D.M., Rowan, M.J., Selkoe, D.J. and Anwyl, R. (2004) Block of long-term potentiation by naturally secreted and synthetic amyloid beta-peptide in hippocampal slices is mediated via activation of the kinases c-Jun N-terminal kinase, cyclin-dependent kinase 5, and p38 mitogen-activated protein kinase as well as metabotropic glutamate receptor type 5. Journal of Neuroscience 24, 3370–3378.Google Scholar
Wright, A.G., Demyanenko, G.P., Powell, A., Schachner, M., Enriquez-Barreto, L., Tran, T.S. et al. (2007) Close homolog of L1 and neuropilin 1 mediate guidance of thalamocortical axons at the ventral telencephalon. Journal of Neuroscience 27, 13667–13679.Google Scholar
Yang, J., Houk, B., Shah, J., Hauser, K.F., Luo, Y., Smith, G. et al. (2005) Genetic background regulates semaphorin gene expression and epileptogenesis in mouse brain after kainic acid status epilepticus. Neuroscience 131, 853–869.Google Scholar
Zhou, Q., Homma, K.J. and Poo, M.M. (2004) Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44, 749–757.CrossRefGoogle ScholarPubMed