Advertisement

Synaptic Cell Adhesion Molecules

  • Olena Bukalo
  • Alexander Dityatev
Part of the Advances in Experimental Medicine and Biology book series (volume 970)

Abstract

During development of the nervous system following axon pathfinding, synaptic connections are established between neurons. Specific cell adhesion molecules (CAMs) accumulate at pre- and postsynaptic sites and trigger synaptic differentiation through interactions with intra- and extracellular scaffolds. These interactions are important to align pre- and postsynaptic transduction machineries and to couple the sites of cell-to-cell adhesion to the cytoskeleton and signaling complexes necessary to accumulate and recycle presynaptic vesicles, components of exo- and endocytic zones, and postsynaptic receptors. In mature brains, CAMs contribute to regulation of synaptic efficacy and plasticity, partially via direct interactions with postsynaptic neurotransmitter receptors and presynaptic voltage-gated ion channels. This chapter is to highlight the major classes of synaptic CAMs, their multiple functions, and the multistage concerted interactions between different CAMs and other components of synapses.

Keywords

Cell adhesion NCAM Scaffold Synaptic plasticity Synaptogenesis 

Notes

Acknowledgments

The work in the authors’ laboratories is supported by the Italian Institute of Technology, San Paolo Foundation, and the Government of the Russian Federation (AD) and by NICHD funding for intramural research (OB). We thank Dr. Philip Lee for his careful and critical reading of this manuscript. We sincerely apologize to all those colleagues whose work is not cited here because of space considerations.

References

  1. Andreyeva, A., Leshchyns’ka, I., Knepper, M., Betzel, C., Redecke, L., Sytnyk, V., & Schachner, M. (2010). CHL1 is a selective organizer of the presynaptic machinery chaperoning the SNARE complex. PloS One, 5, e12018.PubMedCrossRefGoogle Scholar
  2. Ango, F., di Cristo, G., Higashiyama, H., Bennett, V., Wu, P., & Huang, Z. J. (2004). Ankyrin-based subcellular gradient of neurofascin, an immunoglobulin family protein, directs GABAergic innervation at purkinje axon initial segment. Cell, 119, 257–272.PubMedCrossRefGoogle Scholar
  3. Aoto, J., Ting, P., Maghsoodi, B., Xu, N., Henkemeyer, M., & Chen, L. (2007). Postsynaptic ephrinB3 promotes shaft glutamatergic synapse formation. The Journal of Neuroscience, 27, 7508–7519.PubMedCrossRefGoogle Scholar
  4. Armstrong, J. N., Saganich, M. J., Xu, N. J., Henkemeyer, M., Heinemann, S. F., & Contractor, A. (2006). B-ephrin reverse signaling is required for NMDA-independent long-term potentiation of mossy fibers in the hippocampus. The Journal of Neuroscience, 26, 3474–3481.PubMedCrossRefGoogle Scholar
  5. Bamji, S. X., Shimazu, K., Kimes, N., Huelsken, J., Birchmeier, W., Lu, B., & Reichardt, L. F. (2003). Role of beta-catenin in synaptic vesicle localization and presynaptic assembly. Neuron, 40, 719–731.PubMedCrossRefGoogle Scholar
  6. Barker, A. J., & Ullian, E. M. (2008). New roles for astrocytes in developing synaptic circuits. Communicative & Integrative Biology, 1, 207–211.CrossRefGoogle Scholar
  7. Barrow, S. L., Constable, J. R., Clark, E., El-Sabeawy, F., McAllister, A. K., & Washbourne, P. (2009). Neuroligin1: A cell adhesion molecule that recruits PSD-95 and NMDA receptors by distinct mechanisms during synaptogenesis. Neural Development, 4, 17.PubMedCrossRefGoogle Scholar
  8. Becker, C. G., Artola, A., Gerardy-Schahn, R., Becker, T., Welzl, H., & 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.PubMedCrossRefGoogle Scholar
  9. Benson, D. L., Yoshihara, Y., & Mori, K. (1998). Polarized distribution and cell type-specific localization of telencephalin, an intercellular adhesion molecule. Journal of Neuroscience Research, 52, 43–53.PubMedCrossRefGoogle Scholar
  10. Berninghausen, O., Rahman, M. A., Silva, J. P., Davletov, B., Hopkins, C., & Ushkaryov, Y. A. (2007). Neurexin Ibeta and neuroligin are localized on opposite membranes in mature central synapses. Journal of Neurochemistry, 103, 1855–1863.PubMedCrossRefGoogle Scholar
  11. Biederer, T., & Sudhof, T. C. (2001). CASK and protein 4.1 support F-actin nucleation on neurexins. Journal of Biological Chemistry, 276, 47869–47876.PubMedGoogle Scholar
  12. Biederer, T., Sara, Y., Mozhayeva, M., Atasoy, D., Liu, X., Kavalali, E. T., & Sudhof, T. C. (2002). SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science, 297, 1525–1531.PubMedCrossRefGoogle Scholar
  13. Bliss, T., Errington, M., Fransen, E., Godfraind, J. M., Kauer, J. A., Kooy, R. F., Maness, P. F., & Furley, A. J. (2000). Long-term potentiation in mice lacking the neural cell adhesion molecule L1. Current Biology, 10, 1607–1610.PubMedCrossRefGoogle Scholar
  14. Bourgin, C., Murai, K. K., Richter, M., & Pasquale, E. B. (2007). The EphA4 receptor regulates dendritic spine remodeling by affecting beta1-integrin signaling pathways. The Journal of Cell Biology, 178, 1295–1307.PubMedCrossRefGoogle Scholar
  15. Bouzioukh, F., Wilkinson, G. A., Adelmann, G., Frotscher, M., Stein, V., & Klein, R. (2007). Tyrosine phosphorylation sites in ephrinB2 are required for hippocampal long-term potentiation but not long-term depression. The Journal of Neuroscience, 27, 11279–11288.PubMedCrossRefGoogle Scholar
  16. Bozdagi, O., Shan, W., Tanaka, H., Benson, D. L., & Huntley, G. W. (2000). Increasing numbers of synaptic puncta during late-phase LTP: N-cadherin is synthesized, recruited to synaptic sites, and required for potentiation. Neuron, 28, 245–259.PubMedCrossRefGoogle Scholar
  17. Bozdagi, O., Wang, X. B., Nikitczuk, J. S., Anderson, T. R., Bloss, E. B., Radice, G. L., Zhou, Q., Benson, D. L., & Huntley, G. W. (2010). Persistence of coordinated long-term potentiation and dendritic spine enlargement at mature hippocampal CA1 synapses requires N-cadherin. The Journal of Neuroscience, 30, 9984–9989.PubMedCrossRefGoogle Scholar
  18. Bukalo, O., Fentrop, N., Lee, A. Y., Salmen, B., Law, J. W., Wotjak, C. T., Schweizer, M., Dityatev, A., & Schachner, M. (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. The Journal of Neuroscience, 24, 1565–1577.PubMedCrossRefGoogle Scholar
  19. Chan, S. A., Polo-Parada, L., Landmesser, L. T., & Smith, C. (2005). Adrenal chromaffin cells exhibit impaired granule trafficking in NCAM knockout mice. Journal of Neurophysiology, 94, 1037–1047.PubMedCrossRefGoogle Scholar
  20. Chang, K., Seabold, G. K., Wang, C. Y., & Wenthold, R. J. (2010). Reticulon 3 is an interacting partner of the SALM family of adhesion molecules. Journal of Neuroscience Research, 88, 266–274.PubMedCrossRefGoogle Scholar
  21. Chih, B., Engelman, H., & Scheiffele, P. (2005). Control of excitatory and inhibitory synapse formation by neuroligins. Science, 307, 1324–1328.PubMedCrossRefGoogle Scholar
  22. Chih, B., Gollan, L., & Scheiffele, P. (2006). Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex. Neuron, 51, 171–178.PubMedCrossRefGoogle Scholar
  23. Chubykin, A. A., Atasoy, D., Etherton, M. R., Brose, N., Kavalali, E. T., Gibson, J. R., & Sudhof, T. C. (2007). Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron, 54, 919–931.PubMedCrossRefGoogle Scholar
  24. Contractor, A., Rogers, C., Maron, C., Henkemeyer, M., Swanson, G. T., & Heinemann, S. F. (2002). Trans-synaptic Eph receptor-ephrin signaling in hippocampal mossy fiber LTP. Science, 296, 1864–1869.PubMedCrossRefGoogle Scholar
  25. Dahlhaus, R., Hines, R. M., Eadie, B. D., Kannangara, T. S., Hines, D. J., Brown, C. E., Christie, B. R., & El-Husseini, A. (2010). Overexpression of the cell adhesion protein neuroligin-1 induces learning deficits and impairs synaptic plasticity by altering the ratio of excitation to inhibition in the hippocampus. Hippocampus, 20, 305–322.PubMedCrossRefGoogle Scholar
  26. Dalva, M. B., Takasu, M. A., Lin, M. Z., Shamah, S. M., Hu, L., Gale, N. W., & Greenberg, M. E. (2000). EphB receptors interact with NMDA receptors and regulate excitatory synapse formation. Cell, 103, 945–956.PubMedCrossRefGoogle Scholar
  27. de Wit, J., Sylwestrak, E., O’Sullivan, M. L., Otto, S., Tiglio, K., Savas, J. N., Yates, J. R., 3rd, Comoletti, D., Taylor, P., & Ghosh, A. (2009). LRRTM2 interacts with neurexin1 and regulates excitatory synapse formation. Neuron, 64, 799–806.PubMedCrossRefGoogle Scholar
  28. Dean, C., Scholl, F. G., Choih, J., DeMaria, S., Berger, J., Isacoff, E., & Scheiffele, P. (2003). Neurexin mediates the assembly of presynaptic terminals. Nature Neuroscience, 6, 708–716.PubMedCrossRefGoogle Scholar
  29. Deininger, K., Eder, M., Kramer, E. R., Zieglgansberger, W., Dodt, H. U., Dornmair, K., Colicelli, J., & Klein, R. (2008). The Rab5 guanylate exchange factor Rin1 regulates endocytosis of the EphA4 receptor in mature excitatory neurons. Proceedings of the National Academy of Sciences of the United States of America, 105, 12539–12544.PubMedCrossRefGoogle Scholar
  30. Dickinson, B. A., Jo, J., Seok, H., Son, G. H., Whitcomb, D. J., Davies, C. H., Sheng, M., Collingridge, G. L., & Cho, K. (2009). A novel mechanism of hippocampal LTD involving muscarinic receptor-triggered interactions between AMPARs. GRIP and liprin-alpha. Molecular Brain, 2, 18.PubMedCrossRefGoogle Scholar
  31. Dityatev, A., & Rusakov, D. A. (2011). Molecular signals of plasticity at the tetrapartite synapse. Current Opinion in Neurobiology, 21, 353–359.PubMedCrossRefGoogle Scholar
  32. Dityatev, A., & Schachner, M. (2003). Extracellular matrix molecules and synaptic plasticity. Nature Reviews Neuroscience, 4, 456–468.PubMedCrossRefGoogle Scholar
  33. Dityatev, A., Dityateva, G., & Schachner, M. (2000). Synaptic strength as a function of post-versus presynaptic expression of the neural cell adhesion molecule NCAM. Neuron, 26, 207–217.PubMedCrossRefGoogle Scholar
  34. Dityatev, A., Dityateva, G., Sytnyk, V., Delling, M., Toni, N., Nikonenko, I., Muller, D., & Schachner, M. (2004). Polysialylated neural cell adhesion molecule promotes remodeling and formation of hippocampal synapses. The Journal of Neuroscience, 24, 9372–9382.PubMedCrossRefGoogle Scholar
  35. Dunah, A. W., Hueske, E., Wyszynski, M., Hoogenraad, C. C., Jaworski, J., Pak, D. T., Simonetta, A., Liu, G., & Sheng, M. (2005). LAR receptor protein tyrosine phosphatases in the development and maintenance of excitatory synapses. Nature Neuroscience, 8, 458–467.PubMedGoogle Scholar
  36. Eckhardt, M., Bukalo, O., Chazal, G., Wang, L., Goridis, C., Schachner, M., Gerardy-Schahn, R., Cremer, H., & Dityatev, A. (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. The Journal of Neuroscience, 20, 5234–5244.PubMedGoogle Scholar
  37. Ethell, I. M., Irie, F., Kalo, M. S., Couchman, J. R., Pasquale, E. B., & Yamaguchi, Y. (2001). EphB/syndecan-2 signaling in dendritic spine morphogenesis. Neuron, 31, 1001–1013.PubMedCrossRefGoogle Scholar
  38. Fogel, A. I., Akins, M. R., Krupp, A. J., Stagi, M., Stein, V., & Biederer, T. (2007). SynCAMs organize synapses through heterophilic adhesion. The Journal of Neuroscience, 27, 12516–12530.PubMedCrossRefGoogle Scholar
  39. Fu, W. Y., et al. (2007). Cdk5 regulates EphA4-mediated dendritic spine retraction through an ephexin1-dependent mechanism. Nature Neuroscience, 10, 67–76.PubMedCrossRefGoogle Scholar
  40. Furutani, Y., Matsuno, H., Kawasaki, M., Sasaki, T., Mori, K., & Yoshihara, Y. (2007). Interaction between telencephalin and ERM family proteins mediates dendritic filopodia formation. The Journal of Neuroscience, 27, 8866–8876.PubMedCrossRefGoogle Scholar
  41. Futai, K., Kim, M. J., Hashikawa, T., Scheiffele, P., Sheng, M., & Hayashi, Y. (2007). Retrograde modulation of presynaptic release probability through signaling mediated by PSD-95-neuroligin. Nature Neuroscience, 10, 186–195.PubMedCrossRefGoogle Scholar
  42. Fux, C. M., Krug, M., Dityatev, A., Schuster, T., & Schachner, M. (2003). NCAM180 and glutamate receptor subtypes in potentiated spine synapses: An immunogold electron microscopic study. Molecular and Cellular Neuroscience, 24, 939–950.PubMedCrossRefGoogle Scholar
  43. Galuska, S. P., et al. (2010). Synaptic cell adhesion molecule SynCAM 1 is a target for polysialylation in postnatal mouse brain. Proceedings of the National Academy of Sciences of the United States of America, 107, 10250–10255.PubMedCrossRefGoogle Scholar
  44. Giagtzoglou, N., Ly, C. V., & Bellen, H. J. (2009). Cell adhesion, the backbone of the synapse: “vertebrate” and “invertebrate” perspectives. Cold Spring Harbor Perspectives in Biology, 1, a003079.PubMedCrossRefGoogle Scholar
  45. Gibson, J. R., Huber, K. M., & Sudhof, T. C. (2009). Neuroligin-2 deletion selectively decreases inhibitory synaptic transmission originating from fast-spiking but not from somatostatin-positive interneurons. The Journal of Neuroscience, 29, 13883–13897.PubMedCrossRefGoogle Scholar
  46. Graf, E. R., Zhang, X., Jin, S. X., Linhoff, M. W., & Craig, A. M. (2004). Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell, 119, 1013–1026.PubMedCrossRefGoogle Scholar
  47. Grunwald, I. C., Korte, M., Wolfer, D., Wilkinson, G. A., Unsicker, K., Lipp, H. P., Bonhoeffer, T., & Klein, R. (2001). Kinase-independent requirement of EphB2 receptors in hippocampal synaptic plasticity. Neuron, 32, 1027–1040.PubMedCrossRefGoogle Scholar
  48. Grunwald, I. C., Korte, M., Adelmann, G., Plueck, A., Kullander, K., Adams, R. H., Frotscher, M., Bonhoeffer, T., & Klein, R. (2004). Hippocampal plasticity requires postsynaptic ephrinBs. Nature Neuroscience, 7, 33–40.PubMedCrossRefGoogle Scholar
  49. Guan, H., & Maness, P. F. (2010). Perisomatic GABAergic innervation in prefrontal cortex is regulated by ankyrin interaction with the L1 cell adhesion molecule. Cerebral Cortex, 20, 2684–2693.PubMedCrossRefGoogle Scholar
  50. Hammond, M. S., Sims, C., Parameshwaran, K., Suppiramaniam, V., Schachner, M., & 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.PubMedCrossRefGoogle Scholar
  51. Hashimoto, T., Yamada, M., Maekawa, S., Nakashima, T., & Miyata, S. (2008). IgLON cell adhesion molecule Kilon is a crucial modulator for synapse number in hippocampal neurons. Brain Research, 1224, 1–11.PubMedCrossRefGoogle Scholar
  52. Hashimoto, T., Maekawa, S., & Miyata, S. (2009). IgLON cell adhesion molecules regulate synaptogenesis in hippocampal neurons. Cell Biochemistry and Function, 27, 496–498.PubMedCrossRefGoogle Scholar
  53. Heine, M., Thoumine, O., Mondin, M., Tessier, B., Giannone, G., & Choquet, D. (2008). Activity-independent and subunit-specific recruitment of functional AMPA receptors at neurexin/neuroligin contacts. Proceedings of the National Academy of Sciences of the United States of America, 105, 20947–20952.PubMedCrossRefGoogle Scholar
  54. Henderson, J. T., Georgiou, J., Jia, Z., Robertson, J., Elowe, S., Roder, J. C., & Pawson, T. (2001). The receptor tyrosine kinase EphB2 regulates NMDA-dependent synaptic function. Neuron, 32, 1041–1056.PubMedCrossRefGoogle Scholar
  55. Henkemeyer, M., Itkis, O. S., Ngo, M., Hickmott, P. W., & Ethell, I. M. (2003). Multiple EphB receptor tyrosine kinases shape dendritic spines in the hippocampus. The Journal of Cell Biology, 163, 1313–1326.PubMedCrossRefGoogle Scholar
  56. Hering, H., Lin, C. C., & Sheng, M. (2003). Lipid rafts in the maintenance of synapses, dendritic spines, and surface AMPA receptor stability. The Journal of Neuroscience, 23, 3262–3271.PubMedGoogle Scholar
  57. Honda, T., et al. (2006). Involvement of nectins in the formation of puncta adherentia junctions and the mossy fiber trajectory in the mouse hippocampus. Molecular and Cellular Neuroscience, 31, 315–325.PubMedCrossRefGoogle Scholar
  58. Hortsch, M., Nagaraj, K., & Godenschwege, T. A. (2009). The interaction between L1-type proteins and ankyrins–a master switch for L1-type CAM function. Cellular and Molecular Biology Letters, 14, 57–69.PubMedCrossRefGoogle Scholar
  59. Hoy, J. L., Constable, J. R., Vicini, S., Fu, Z., & Washbourne, P. (2009). SynCAM1 recruits NMDA receptors via protein 4.1B. Molecular and Cellular Neuroscience, 42, 466–483.PubMedCrossRefGoogle Scholar
  60. Irie, F., & Yamaguchi, Y. (2002). EphB receptors regulate dendritic spine development via intersectin, Cdc42 and N-WASP. Nature Neuroscience, 5, 1117–1118.PubMedCrossRefGoogle Scholar
  61. Israely, I., Costa, R. M., Xie, C. W., Silva, A. J., Kosik, K. S., & Liu, X. (2004). Deletion of the neuron-specific protein delta-catenin leads to severe cognitive and synaptic dysfunction. Current Biology, 14, 1657–1663.PubMedCrossRefGoogle Scholar
  62. Jung, S. Y., et al. (2010). Input-specific synaptic plasticity in the amygdala is regulated by neuroligin-1 via postsynaptic NMDA receptors. Proceedings of the National Academy of Sciences of the United States of America, 107, 4710–4715.PubMedCrossRefGoogle Scholar
  63. Jungling, K., Eulenburg, V., Moore, R., Kemler, R., Lessmann, V., & Gottmann, K. (2006). N-cadherin transsynaptically regulates short-term plasticity at glutamatergic synapses in embryonic stem cell-derived neurons. The Journal of Neuroscience, 26, 6968–6978.PubMedCrossRefGoogle Scholar
  64. Kayser, M. S., McClelland, A. C., Hughes, E. G., & Dalva, M. B. (2006). Intracellular and trans-synaptic regulation of glutamatergic synaptogenesis by EphB receptors. The Journal of Neuroscience, 26, 12152–12164.PubMedCrossRefGoogle Scholar
  65. Kayser, M. S., Nolt, M. J., & Dalva, M. B. (2008). EphB receptors couple dendritic filopodia motility to synapse formation. Neuron, 59, 56–69.PubMedCrossRefGoogle Scholar
  66. Kim, S., Burette, A., Chung, H. S., Kwon, S. K., Woo, J., Lee, H. W., Kim, K., Kim, H., Weinberg, R. J., & Kim, E. (2006). NGL family PSD-95-interacting adhesion molecules regulate excitatory synapse formation. Nature Neuroscience, 9, 1294–1301.PubMedCrossRefGoogle Scholar
  67. Kim, J., et al. (2008). Neuroligin-1 is required for normal expression of LTP and associative fear memory in the amygdala of adult animals. Proceedings of the National Academy of Sciences of the United States of America, 105, 9087–9092.PubMedCrossRefGoogle Scholar
  68. Kleene, R., Cassens, C., Bahring, R., Theis, T., Xiao, M. F., Dityatev, A., Schafer-Nielsen, C., Doring, F., Wischmeyer, E., & Schachner, M. (2010). Functional consequences of the interactions among the neural cell adhesion molecule NCAM, the receptor tyrosine kinase TrkB, and the inwardly rectifying K+ channel KIR3.3. Journal of Biological Chemistry, 285, 28968–28979.PubMedCrossRefGoogle Scholar
  69. Klein, R. (2009). Bidirectional modulation of synaptic functions by Eph/ephrin signaling. Nature Neuroscience, 12, 15–20.PubMedCrossRefGoogle Scholar
  70. Ko, J., Na, M., Kim, S., Lee, J. R., & Kim, E. (2003). Interaction of the ERC family of RIM-binding proteins with the liprin-alpha family of multidomain proteins. Journal of Biological Chemistry, 278, 42377–42385.PubMedCrossRefGoogle Scholar
  71. Ko, J., Kim, S., Chung, H. S., Kim, K., Han, K., Kim, H., Jun, H., Kaang, B. K., & Kim, E. (2006). SALM synaptic cell adhesion-like molecules regulate the differentiation of excitatory synapses. Neuron, 50, 233–245.PubMedCrossRefGoogle Scholar
  72. Ko, J., Fuccillo, M. V., Malenka, R. C., & Sudhof, T. C. (2009). LRRTM2 functions as a neurexin ligand in promoting excitatory synapse formation. Neuron, 64, 791–798.PubMedCrossRefGoogle Scholar
  73. Kochlamazashvili, G., et al. (2010). Neural cell adhesion molecule-associated polysialic acid regulates synaptic plasticity and learning by restraining the signaling through GluN2B-containing NMDA receptors. The Journal of Neuroscience, 30, 4171–4183.PubMedCrossRefGoogle Scholar
  74. Kwon, S. K., Woo, J., Kim, S. Y., Kim, H., & Kim, E. (2010). Trans-synaptic adhesions between netrin-G ligand-3 (NGL-3) and receptor tyrosine phosphatases LAR, protein-tyrosine phosphatase delta (PTPdelta), and PTPsigma via specific domains regulate excitatory synapse formation. Journal of Biological Chemistry, 285, 13966–13978.PubMedCrossRefGoogle Scholar
  75. Lauren, J., Airaksinen, M. S., Saarma, M., & Timmusk, T. (2003). A novel gene family encoding leucine-rich repeat transmembrane proteins differentially expressed in the nervous system. Genomics, 81, 411–421.PubMedCrossRefGoogle Scholar
  76. Law, J. W., Lee, A. Y., Sun, M., Nikonenko, A. G., Chung, S. K., 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. The Journal of Neuroscience, 23, 10419–10432.PubMedGoogle Scholar
  77. Leshchyns’ka, I., Sytnyk, V., Richter, M., Andreyeva, A., Puchkov, D., & Schachner, M. (2006). The adhesion molecule CHL1 regulates uncoating of clathrin-coated synaptic vesicles. Neuron, 52, 1011–1025.PubMedCrossRefGoogle Scholar
  78. Lim, S. T., Lim, K. C., Giuliano, R. E., & Federoff, H. J. (2008). Temporal and spatial localization of nectin-1 and l-afadin during synaptogenesis in hippocampal neurons. The Journal of Comparative Neurology, 507, 1228–1244.PubMedCrossRefGoogle Scholar
  79. Linhoff, M. W., Lauren, J., Cassidy, R. M., Dobie, F. A., Takahashi, H., Nygaard, H. B., Airaksinen, M. S., Strittmatter, S. M., & Craig, A. M. (2009). An unbiased expression screen for synaptogenic proteins identifies the LRRTM protein family as synaptic organizers. Neuron, 61, 734–749.PubMedCrossRefGoogle Scholar
  80. Lodge, A. P., Howard, M. R., McNamee, C. J., & Moss, D. J. (2000). Co-localisation, heterophilic interactions and regulated expression of IgLON family proteins in the chick nervous system. Molecular Brain Research, 82, 84–94.PubMedCrossRefGoogle Scholar
  81. Mah, W., Ko, J., Nam, J., Han, K., Chung, W. S., & Kim, E. (2010). Selected SALM (synaptic adhesion-like molecule) family proteins regulate synapse formation. The Journal of Neuroscience, 30, 5559–5568.PubMedCrossRefGoogle Scholar
  82. Majima, T., Ogita, H., Yamada, T., Amano, H., Togashi, H., Sakisaka, T., Tanaka-Okamoto, M., Ishizaki, H., Miyoshi, J., & Takai, Y. (2009). Involvement of afadin in the formation and remodeling of synapses in the hippocampus. Biochemical and Biophysical Research Communications, 385, 539–544.PubMedCrossRefGoogle Scholar
  83. Marrs, G. S., Theisen, C. S., & Bruses, J. L. (2009). N-cadherin modulates voltage activated calcium influx via RhoA, p120-catenin, and myosin-actin interaction. Molecular and Cellular Neuroscience, 40, 390–400.PubMedCrossRefGoogle Scholar
  84. Matsuno, H., Okabe, S., Mishina, M., Yanagida, T., Mori, K., & Yoshihara, Y. (2006). Telencephalin slows spine maturation. The Journal of Neuroscience, 26, 1776–1786.PubMedCrossRefGoogle Scholar
  85. Mendez, P., De Roo, M., Poglia, L., Klauser, P., & Muller, D. (2010). N-cadherin mediates plasticity-induced long-term spine stabilization. The Journal of Cell Biology, 189, 589–600.PubMedCrossRefGoogle Scholar
  86. Meyer, G., Varoqueaux, F., Neeb, A., Oschlies, M., & Brose, N. (2004). The complexity of PDZ domain-mediated interactions at glutamatergic synapses: A case study on neuroligin. Neuropharmacology, 47, 724–733.PubMedCrossRefGoogle Scholar
  87. Missler, M., Zhang, W., Rohlmann, A., Kattenstroth, G., Hammer, R. E., Gottmann, K., & Sudhof, T. C. (2003). Alpha-neurexins couple Ca2+ channels to synaptic vesicle exocytosis. Nature, 423, 939–948.PubMedCrossRefGoogle Scholar
  88. Miyata, S., Matsumoto, N., Taguchi, K., Akagi, A., Iino, T., Funatsu, N., & Maekawa, S. (2003). Biochemical and ultrastructural analyses of IgLON cell adhesion molecules, Kilon and OBCAM in the rat brain. Neuroscience, 117, 645–658.PubMedCrossRefGoogle Scholar
  89. Mizoguchi, A., et al. (2002). Nectin: An adhesion molecule involved in formation of synapses. The Journal of Cell Biology, 156, 555–565.PubMedCrossRefGoogle Scholar
  90. Morellini, F., Lepsveridze, E., Kahler, B., Dityatev, A., & 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.PubMedCrossRefGoogle Scholar
  91. Muller, D., Wang, C., Skibo, G., Toni, N., Cremer, H., Calaora, V., Rougon, G., & Kiss, J. Z. (1996). PSA-NCAM is required for activity-induced synaptic plasticity. Neuron, 17, 413–422.PubMedCrossRefGoogle Scholar
  92. Muller, D., Djebbara-Hannas, Z., Jourdain, P., Vutskits, L., Durbec, P., Rougon, G., & Kiss, J. Z. (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 United States of America, 97, 4315–4320.PubMedCrossRefGoogle Scholar
  93. Murai, K. K., Misner, D., & Ranscht, B. (2002). Contactin supports synaptic plasticity associated with hippocampal long-term depression but not potentiation. Current Biology, 12, 181–190.PubMedCrossRefGoogle Scholar
  94. Murai, K. K., Nguyen, L. N., Koolpe, M., McLennan, R., Krull, C. E., & Pasquale, E. B. (2003). Targeting the EphA4 receptor in the nervous system with biologically active peptides. Molecular and Cellular Neuroscience, 24, 1000–1011.PubMedCrossRefGoogle Scholar
  95. Murase, S., Mosser, E., & Schuman, E. M. (2002). Depolarization drives beta-Catenin into neuronal spines promoting changes in synaptic structure and function. Neuron, 35, 91–105.PubMedCrossRefGoogle Scholar
  96. Nakamura, K., 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.PubMedCrossRefGoogle Scholar
  97. Nam, C. I., & Chen, L. (2005). Postsynaptic assembly induced by neurexin-neuroligin interaction and neurotransmitter. Proceedings of the National Academy of Sciences of the United States of America, 102, 6137–6142.PubMedCrossRefGoogle Scholar
  98. Nikonenko, A. G., Sun, M., Lepsveridze, E., Apostolova, I., Petrova, I., Irintchev, A., Dityatev, A., & Schachner, M. (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.PubMedCrossRefGoogle Scholar
  99. Nishimura-Akiyoshi, S., Niimi, K., Nakashiba, T., & Itohara, S. (2007). Axonal netrin-Gs transneuronally determine lamina-specific subdendritic segments. Proceedings of the National Academy of Sciences of the United States of America, 104, 14801–14806.PubMedCrossRefGoogle Scholar
  100. Nuriya, M., & Huganir, R. L. (2006). Regulation of AMPA receptor trafficking by N-cadherin. Journal of Neurochemistry, 97, 652–661.PubMedCrossRefGoogle Scholar
  101. Oka, S., Mori, K., & Watanabe, Y. (1990). Mammalian telencephalic neurons express a segment-specific membrane glycoprotein, telencephalin. Neuroscience, 35, 93–103.PubMedCrossRefGoogle Scholar
  102. Okuda, T., Yu, L. M., Cingolani, L. A., Kemler, R., & Goda, Y. (2007). Beta-Catenin regulates excitatory postsynaptic strength at hippocampal synapses. Proceedings of the National Academy of Sciences of the United States of America, 104, 13479–13484.PubMedCrossRefGoogle Scholar
  103. Olsen, O., et al. (2005). Neurotransmitter release regulated by a MALS-liprin-alpha presynaptic complex. The Journal of Cell Biology, 170, 1127–1134.PubMedCrossRefGoogle Scholar
  104. Penzes, P., Beeser, A., Chernoff, J., Schiller, M. R., Eipper, B. A., Mains, R. E., & Huganir, R. L. (2003). Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin. Neuron, 37, 263–274.PubMedCrossRefGoogle Scholar
  105. Pimenta, A. F., Reinoso, B. S., & Levitt, P. (1996). Expression of the mRNAs encoding the limbic system-associated membrane protein (LAMP): II. Fetal rat brain. The Journal of Comparative Neurology, 375, 289–302.PubMedCrossRefGoogle Scholar
  106. Polo-Parada, L., Bose, C. M., & Landmesser, L. T. (2001). Alterations in transmission, vesicle dynamics, and transmitter release machinery at NCAM-deficient neuromuscular junctions. Neuron, 32, 815–828.PubMedCrossRefGoogle Scholar
  107. Polo-Parada, L., Plattner, F., Bose, C., & Landmesser, L. T. (2005). NCAM 180 acting via a conserved C-terminal domain and MLCK is essential for effective transmission with repetitive stimulation. Neuron, 46, 917–931.PubMedCrossRefGoogle Scholar
  108. Poulopoulos, A., et al. (2009). Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin. Neuron, 63, 628–642.PubMedCrossRefGoogle Scholar
  109. Prange, O., Wong, T. P., Gerrow, K., Wang, Y. T., & El-Husseini, A. (2004). A balance between excitatory and inhibitory synapses is controlled by PSD-95 and neuroligin. Proceedings of the National Academy of Sciences of the United States of America, 101, 13915–13920.PubMedCrossRefGoogle Scholar
  110. Pulido, R., Serra-Pages, C., Tang, M., & Streuli, M. (1995). The LAR/PTP delta/PTP sigma subfamily of transmembrane protein-tyrosine-phosphatases: Multiple human LAR, PTP delta, and PTP sigma isoforms are expressed in a tissue-specific manner and associate with the LAR-interacting protein LIP.1. Proceedings of the National Academy of Sciences of the United States of America, 92, 11686–11690.PubMedCrossRefGoogle Scholar
  111. Rafuse, V. F., Polo-Parada, L., & Landmesser, L. T. (2000). Structural and functional alterations of neuromuscular junctions in NCAM-deficient mice. The Journal of Neuroscience, 20, 6529–6539.PubMedGoogle Scholar
  112. Ramser, E. M., Wolters, G., Dityateva, G., Dityatev, A., Schachner, M., & Tilling, T. (2010). The 14-3-3zeta protein binds to the cell adhesion molecule L1, promotes L1 phosphorylation by CKII and influences L1-dependent neurite outgrowth. PloS One, 5, e13462.PubMedCrossRefGoogle Scholar
  113. Richter, M., Murai, K. K., Bourgin, C., Pak, D. T., & Pasquale, E. B. (2007). The EphA4 receptor regulates neuronal morphology through SPAR-mediated inactivation of Rap GTPases. The Journal of Neuroscience, 27, 14205–14215.PubMedCrossRefGoogle Scholar
  114. Robbins, E. M., Krupp, A. J., Perez de Arce, K., Ghosh, A. K., Fogel, A. I., Boucard, A., Sudhof, T. C., Stein, V., & Biederer, T. (2010). SynCAM 1 adhesion dynamically regulates synapse number and impacts plasticity and learning. Neuron, 68, 894–906.PubMedCrossRefGoogle Scholar
  115. Rodenas-Ruano, A., Perez-Pinzon, M. A., Green, E. J., Henkemeyer, M., & Liebl, D. J. (2006). Distinct roles for ephrinB3 in the formation and function of hippocampal synapses. Developmental Biology, 292, 34–45.PubMedCrossRefGoogle Scholar
  116. Rutishauser, U. (2008). Polysialic acid in the plasticity of the developing and adult vertebrate nervous system. Nature Reviews Neuroscience, 9, 26–35.PubMedCrossRefGoogle Scholar
  117. Saghatelyan, A. K., Nikonenko, A. G., Sun, M., Rolf, B., Putthoff, P., Kutsche, M., Bartsch, U., Dityatev, A., & Schachner, M. (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.PubMedCrossRefGoogle Scholar
  118. Saglietti, L., et al. (2007). Extracellular interactions between GluR2 and N-cadherin in spine regulation. Neuron, 54, 461–477.PubMedCrossRefGoogle Scholar
  119. Sakurai, K., Toyoshima, M., Ueda, H., Matsubara, K., Takeda, Y., Karagogeos, D., Shimoda, Y., & Watanabe, K. (2009). Contribution of the neural cell recognition molecule NB-3 to synapse formation between parallel fibers and Purkinje cells in mouse. Developmental Neurobiology, 69, 811–824.PubMedCrossRefGoogle Scholar
  120. Sakurai, K., Toyoshima, M., Takeda, Y., Shimoda, Y., & Watanabe, K. (2010). Synaptic formation in subsets of glutamatergic terminals in the mouse hippocampal formation is affected by a deficiency in the neural cell recognition molecule NB-3. Neuroscience Letters, 473, 102–106.PubMedCrossRefGoogle Scholar
  121. Sara, Y., Biederer, T., Atasoy, D., Chubykin, A., Mozhayeva, M. G., Sudhof, T. C., & Kavalali, E. T. (2005). Selective capability of SynCAM and neuroligin for functional synapse assembly. The Journal of Neuroscience, 25, 260–270.PubMedCrossRefGoogle Scholar
  122. Schapitz, I. U., et al. (2010). Neuroligin 1 is dynamically exchanged at postsynaptic sites. The Journal of Neuroscience, 30, 12733–12744.PubMedCrossRefGoogle Scholar
  123. Schoch, S., Castillo, P. E., Jo, T., Mukherjee, K., Geppert, M., Wang, Y., Schmitz, F., Malenka, R. C., & Sudhof, T. C. (2002). RIM1alpha forms a protein scaffold for regulating neurotransmitter release at the active zone. Nature, 415, 321–326.PubMedCrossRefGoogle Scholar
  124. Schuster, T., Krug, M., Hassan, H., & Schachner, M. (1998). Increase in proportion of hippocampal spine synapses expressing neural cell adhesion molecule NCAM180 following long-term potentiation. Journal of Neurobiology, 37, 359–372.PubMedCrossRefGoogle Scholar
  125. Seabold, G. K., Wang, P. Y., Chang, K., Wang, C. Y., Wang, Y. X., Petralia, R. S., & Wenthold, R. J. (2008). The SALM family of adhesion-like molecules forms heteromeric and homomeric complexes. Journal of Biological Chemistry, 283, 8395–8405.PubMedCrossRefGoogle Scholar
  126. Senkov, O., Sun, M., Weinhold, B., Gerardy-Schahn, R., Schachner, M., & 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. The Journal of Neuroscience, 26, 10888–109898.PubMedCrossRefGoogle Scholar
  127. Shimoda, Y., & Watanabe, K. (2009). Contactins: Emerging key roles in the development and function of the nervous system. Cell Adhesion & Migration, 3, 64–70.CrossRefGoogle Scholar
  128. Siddiqui, T. J., Pancaroglu, R., Kang, Y., Rooyakkers, A., & Craig, A. M. (2010). LRRTMs and neuroligins bind neurexins with a differential code to cooperate in glutamate synapse development. The Journal of Neuroscience, 30, 7495–7506.PubMedCrossRefGoogle Scholar
  129. Silverman, J. B., Restituito, S., Lu, W., Lee-Edwards, L., Khatri, L., & Ziff, E. B. (2007). Synaptic anchorage of AMPA receptors by cadherins through neural plakophilin-related arm protein AMPA receptor-binding protein complexes. The Journal of Neuroscience, 27, 8505–8516.PubMedCrossRefGoogle Scholar
  130. Stagi, M., Fogel, A. I., & Biederer, T. (2010). SynCAM 1 participates in axo-dendritic contact assembly and shapes neuronal growth cones. Proceedings of the National Academy of Sciences of the United States of America, 107, 7568–7573.PubMedCrossRefGoogle Scholar
  131. Stan, A., Pielarski, K. N., Brigadski, T., Wittenmayer, N., Fedorchenko, O., Gohla, A., Lessmann, V., Dresbach, T., & Gottmann, K. (2010). Essential cooperation of N-cadherin and neuroligin-1 in the transsynaptic control of vesicle accumulation. Proceedings of the National Academy of Sciences of the United States of America, 107, 11116–11121.PubMedCrossRefGoogle Scholar
  132. Stoenica, L., Senkov, O., Gerardy-Schahn, R., Weinhold, B., Schachner, M., & 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.PubMedCrossRefGoogle Scholar
  133. Sytnyk, V., Leshchyns’ka, I., Delling, M., Dityateva, G., Dityatev, A., & Schachner, M. (2002). Neural cell adhesion molecule promotes accumulation of TGN organelles at sites of neuron-to-neuron contacts. The Journal of Cell Biology, 159, 649–661.PubMedCrossRefGoogle Scholar
  134. Sytnyk, V., Leshchyns’ka, I., Nikonenko, A. G., & Schachner, M. (2006). NCAM promotes assembly and activity-dependent remodeling of the postsynaptic signaling complex. The Journal of Cell Biology, 174, 1071–1085.PubMedCrossRefGoogle Scholar
  135. Tabuchi, K., Biederer, T., Butz, S., & Sudhof, T. C. (2002). CASK participates in alternative tripartite complexes in which Mint 1 competes for binding with caskin 1, a novel CASK-binding protein. The Journal of Neuroscience, 22, 4264–4273.PubMedGoogle Scholar
  136. Takasu, M. A., Dalva, M. B., Zigmond, R. E., & Greenberg, M. E. (2002). Modulation of NMDA receptor-dependent calcium influx and gene expression through EphB receptors. Science, 295, 491–495.PubMedCrossRefGoogle Scholar
  137. Tallafuss, A., Constable, J. R., & Washbourne, P. (2010). Organization of central synapses by adhesion molecules. European Journal of Neuroscience, 32, 198–206.PubMedCrossRefGoogle Scholar
  138. Tanaka, H., Shan, W., Phillips, G. R., Arndt, K., Bozdagi, O., Shapiro, L., Huntley, G. W., Benson, D. L., & Colman, D. R. (2000). Molecular modification of N-cadherin in response to synaptic activity. Neuron, 25, 93–107.PubMedCrossRefGoogle Scholar
  139. Taniguchi, H., Gollan, L., Scholl, F. G., Mahadomrongkul, V., Dobler, E., Limthong, N., Peck, M., Aoki, C., & Scheiffele, P. (2007). Silencing of neuroligin function by postsynaptic neurexins. The Journal of Neuroscience, 27, 2815–2824.PubMedCrossRefGoogle Scholar
  140. Thomas, L. A., Akins, M. R., & Biederer, T. (2008). Expression and adhesion profiles of SynCAM molecules indicate distinct neuronal functions. The Journal of Comparative Neurology, 510, 47–67.PubMedCrossRefGoogle Scholar
  141. Tian, L., Stefanidakis, M., Ning, L., Van Lint, P., Nyman-Huttunen, H., Libert, C., Itohara, S., Mishina, M., Rauvala, H., & Gahmberg, C. G. (2007). Activation of NMDA receptors promotes dendritic spine development through MMP-mediated ICAM-5 cleavage. The Journal of Cell Biology, 178, 687–700.PubMedCrossRefGoogle Scholar
  142. Tolias, K. F., Bikoff, J. B., Kane, C. G., Tolias, C. S., Hu, L., & Greenberg, M. E. (2007). The Rac1 guanine nucleotide exchange factor Tiam1 mediates EphB receptor-dependent dendritic spine development. Proceedings of the National Academy of Sciences of the United States of America, 104, 7265–7270.PubMedCrossRefGoogle Scholar
  143. Uemura, T., Lee, S. J., Yasumura, M., Takeuchi, T., Yoshida, T., Ra, M., Taguchi, R., Sakimura, K., & Mishina, M. (2010). Trans-synaptic interaction of GluRdelta2 and Neurexin through Cbln1 mediates synapse formation in the cerebellum. Cell, 141, 1068–1079.PubMedCrossRefGoogle Scholar
  144. Vaithianathan, T., Matthias, K., Bahr, B., Schachner, M., Suppiramaniam, V., Dityatev, A., & Steinhauser, C. (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.PubMedCrossRefGoogle Scholar
  145. Varoqueaux, F., Aramuni, G., Rawson, R. L., Mohrmann, R., Missler, M., Gottmann, K., Zhang, W., Sudhof, T. C., & Brose, N. (2006). Neuroligins determine synapse maturation and function. Neuron, 51, 741–754.PubMedCrossRefGoogle Scholar
  146. Wang, C. Y., Chang, K., Petralia, R. S., Wang, Y. X., Seabold, G. K., & Wenthold, R. J. (2006). A novel family of adhesion-like molecules that interacts with the NMDA receptor. The Journal of Neuroscience, 26, 2174–2183.PubMedCrossRefGoogle Scholar
  147. Woo, J., Kwon, S. K., Choi, S., Kim, S., Lee, J. R., Dunah, A. W., Sheng, M., & Kim, E. (2009). Trans-synaptic adhesion between NGL-3 and LAR regulates the formation of excitatory synapses. Nature Neuroscience, 12, 428–437.PubMedCrossRefGoogle Scholar
  148. Woolfrey, K. M., et al. (2009). Epac2 induces synapse remodeling and depression and its disease-associated forms alter spines. Nature Neuroscience, 12, 1275–1284.PubMedCrossRefGoogle Scholar
  149. Xie, Z., Photowala, H., Cahill, M. E., Srivastava, D. P., Woolfrey, K. M., Shum, C. Y., Huganir, R. L., & Penzes, P. (2008). Coordination of synaptic adhesion with dendritic spine remodeling by AF-6 and kalirin-7. The Journal of Neuroscience, 28, 6079–6091.PubMedCrossRefGoogle Scholar
  150. Yamada, A., Irie, K., Deguchi-Tawarada, M., Ohtsuka, T., & Takai, Y. (2003). Nectin-dependent localization of synaptic scaffolding molecule (S-SCAM) at the puncta adherentia junctions formed between the mossy fibre terminals and the dendrites of pyramidal cells in the CA3 area of the mouse hippocampus. Genes to Cells, 8, 985–994.PubMedCrossRefGoogle Scholar
  151. Yamada, M., Hashimoto, T., Hayashi, N., Higuchi, M., Murakami, A., Nakashima, T., Maekawa, S., & Miyata, S. (2007). Synaptic adhesion molecule OBCAM; synaptogenesis and dynamic internalization. Brain Research, 1165, 5–14.PubMedCrossRefGoogle Scholar
  152. Yasuda, S., et al. (2007). Activity-induced protocadherin arcadlin regulates dendritic spine number by triggering N-cadherin endocytosis via TAO2beta and p38 MAP kinases. Neuron, 56, 456–471.PubMedCrossRefGoogle Scholar
  153. Zhang, W., Rohlmann, A., Sargsyan, V., Aramuni, G., Hammer, R. E., Sudhof, T. C., & Missler, M. (2005). Extracellular domains of alpha-neurexins participate in regulating synaptic transmission by selectively affecting N- and P/Q-type Ca2+ channels. The Journal of Neuroscience, 25, 4330–4342.PubMedCrossRefGoogle Scholar
  154. Zhang, C., Atasoy, D., Arac, D., Yang, X., Fucillo, M. V., Robison, A. J., Ko, J., Brunger, A. T., & Sudhof, T. C. (2010). Neurexins physically and functionally interact with GABA(A) receptors. Neuron, 66, 403–416.PubMedCrossRefGoogle Scholar
  155. Zhou, L., Martinez, S. J., Haber, M., Jones, E. V., Bouvier, D., Doucet, G., Corera, A. T., Fon, E. A., Zisch, A. H., & Murai, K. K. (2007). EphA4 signaling regulates phospholipase Cgamma1 activation, cofilin membrane association, and dendritic spine morphology. The Journal of Neuroscience, 27, 5127–5138.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag/WIen 2012

Authors and Affiliations

  1. 1.National Institute of Child Health and Human Development, National Institutes of HealthBethesdaUSA
  2. 2.Department of Neuroscience and Brain TechnologiesIstituto Italiano di TecnologiaGenovaItaly
  3. 3.Laboratory for Brain Extracellular Matrix ResearchUniversity of Nizhny NovgorodNizhny NovgorodRussia

Personalised recommendations