Trans-synaptic adhesion between NGL-3 and LAR regulates the formation of excitatory synapses (original) (raw)

• Yamagata, M., Sanes, J.R. & Weiner, J.A. Synaptic adhesion molecules. Curr. Opin. Cell Biol. 15, 621–632 (2003).
  Article CAS Google Scholar
• Dalva, M.B., McClelland, A.C. & Kayser, M.S. Cell adhesion molecules: signaling functions at the synapse. Nat. Rev. Neurosci. 8, 206–220 (2007).
  Article CAS Google Scholar
• Washbourne, P. et al. Cell adhesion molecules in synapse formation. J. Neurosci. 24, 9244–9249 (2004).
  Article CAS Google Scholar
• Akins, M.R. & Biederer, T. Cell-cell interactions in synaptogenesis. Curr. Opin. Neurobiol. 16, 83–89 (2006).
  Article CAS Google Scholar
• Craig, A.M. & Kang, Y. Neurexin-neuroligin signaling in synapse development. Curr. Opin. Neurobiol. 17, 43–52 (2007).
  Article CAS Google Scholar
• McAllister, A.K. Dynamic aspects of CNS synapse formation. Annu. Rev. Neurosci. 30, 425–450 (2007).
  Article CAS Google Scholar
• Ichtchenko, K. et al. Neuroligin 1: a splice site–specific ligand for beta-neurexins. Cell 81, 435–443 (1995).
  Article CAS Google Scholar
• Scheiffele, P., Fan, J., Choih, J., Fetter, R. & Serafini, T. Neuroligin expressed in non-neuronal cells triggers presynaptic development in contacting axons. Cell 101, 657–669 (2000).
  Article CAS Google Scholar
• Graf, E.R., Zhang, X., Jin, S.X., Linhoff, M.W. & Craig, A.M. Neurexins induce differentiation of GABA and glutamate postsynaptic specializations via neuroligins. Cell 119, 1013–1026 (2004).
  Article CAS Google Scholar
• Biederer, T. et al. SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 297, 1525–1531 (2002).
  Article CAS Google Scholar
• Fogel, A.I. et al. SynCAMs organize synapses through heterophilic adhesion. J. Neurosci. 27, 12516–12530 (2007).
  Article CAS Google Scholar
• Lin, J.C., Ho, W.H., Gurney, A. & Rosenthal, A. The netrin-G1 ligand NGL-1 promotes the outgrowth of thalamocortical axons. Nat. Neurosci. 6, 1270–1276 (2003).
  Article CAS Google Scholar
• Kim, S. et al. NGL family PSD-95–interacting adhesion molecules regulate excitatory synapse formation. Nat. Neurosci. 9, 1294–1301 (2006).
  Article CAS Google Scholar
• Kayser, M.S., McClelland, A.C., Hughes, E.G. & Dalva, M.B. Intracellular and trans-synaptic regulation of glutamatergic synaptogenesis by EphB receptors. J. Neurosci. 26, 12152–12164 (2006).
  Article CAS Google Scholar
• Boucard, A.A., Chubykin, A.A., Comoletti, D., Taylor, P. & Sudhof, T.C. A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to alpha- and beta-neurexins. Neuron 48, 229–236 (2005).
  Article CAS Google Scholar
• Chih, B., Gollan, L. & Scheiffele, P. Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex. Neuron 51, 171–178 (2006).
  Article CAS Google Scholar
• Graf, E.R., Kang, Y., Hauner, A.M. & Craig, A.M. Structure function and splice site analysis of the synaptogenic activity of the neurexin-1 beta LNS domain. J. Neurosci. 26, 4256–4265 (2006).
  Article CAS Google Scholar
• Irie, M. et al. Binding of neuroligins to PSD-95. Science 277, 1511–1515 (1997).
  Article CAS Google Scholar
• Tabuchi, K. et al. A neuroligin-3 mutation implicated in autism increases inhibitory synaptic transmission in mice. Science 318, 71–76 (2007).
  Article CAS Google Scholar
• Jamain, S. et al. Reduced social interaction and ultrasonic communication in a mouse model of monogenic heritable autism. Proc. Natl. Acad. Sci. USA 105, 1710–1715 (2008).
  Article CAS Google Scholar
• Nakashiba, T. et al. Netrin-G1: a novel glycosyl phosphatidylinositol–linked mammalian netrin that is functionally divergent from classical netrins. J. Neurosci. 20, 6540–6550 (2000).
  Article CAS Google Scholar
• Nakashiba, T., Nishimura, S., Ikeda, T. & Itohara, S. Complementary expression and neurite outgrowth activity of netrin-G subfamily members. Mech. Dev. 111, 47–60 (2002).
  Article CAS Google Scholar
• Yin, Y., Miner, J.H. & Sanes, J.R. Laminets: laminin- and netrin-related genes expressed in distinct neuronal subsets. Mol. Cell. Neurosci. 19, 344–358 (2002).
  Article CAS Google Scholar
• Nishimura-Akiyoshi, S., Niimi, K., Nakashiba, T. & Itohara, S. Axonal netrin-Gs transneuronally determine lamina-specific subdendritic segments. Proc. Natl. Acad. Sci. USA 104, 14801–14806 (2007).
  Article Google Scholar
• Zhang, W. et al. Netrin-G2 and netrin-G2 ligand are both required for normal auditory responsiveness. Genes Brain Behav. 7, 385–392 (2008).
  Article CAS Google Scholar
• Aoki-Suzuki, M. et al. A family-based association study and gene expression analyses of netrin-G1 and -G2 genes in schizophrenia. Biol. Psychiatry 57, 382–393 (2005).
  Article CAS Google Scholar
• Johnson, K.G. & Van Vactor, D. Receptor protein tyrosine phosphatases in nervous system development. Physiol. Rev. 83, 1–24 (2003).
  Article CAS Google Scholar
• Stryker, E. & Johnson, K.G. LAR, liprin alpha and the regulation of active zone morphogenesis. J. Cell Sci. 120, 3723–3728 (2007).
  Article CAS Google Scholar
• Serra-Pages, C. et al. The LAR transmembrane protein tyrosine phosphatase and a coiled-coil LAR-interacting protein colocalize at focal adhesions. EMBO J. 14, 2827–2838 (1995).
  Article CAS Google Scholar
• Kypta, R.M., Su, H. & Reichardt, L.F. Association between a transmembrane protein tyrosine phosphatase and the cadherin-catenin complex. J. Cell Biol. 134, 1519–1529 (1996).
  Article CAS Google Scholar
• Zhen, M. & Jin, Y. The liprin protein SYD-2 regulates the differentiation of presynaptic termini in C. elegans. Nature 401, 371–375 (1999).
  CAS PubMed Google Scholar
• Kaufmann, N., DeProto, J., Ranjan, R., Wan, H. & Van Vactor, D. Drosophila liprin-alpha and the receptor phosphatase Dlar control synapse morphogenesis. Neuron 34, 27–38 (2002).
  Article CAS Google Scholar
• Ackley, B.D. et al. The two isoforms of the Caenorhabditis elegans leukocyte-common antigen related receptor tyrosine phosphatase PTP-3 function independently in axon guidance and synapse formation. J. Neurosci. 25, 7517–7528 (2005).
  Article CAS Google Scholar
• Dunah, A.W. et al. LAR receptor protein tyrosine phosphatases in the development and maintenance of excitatory synapses. Nat. Neurosci. 8, 458–467 (2005).
  Article CAS Google Scholar
• O'Grady, P., Thai, T.C. & Saito, H. The laminin-nidogen complex is a ligand for a specific splice isoform of the transmembrane protein tyrosine phosphatase LAR. J. Cell Biol. 141, 1675–1684 (1998).
  Article CAS Google Scholar
• Johnson, K.G. et al. The HSPGs Syndecan and Dallylike bind the receptor phosphatase LAR and exert distinct effects on synaptic development. Neuron 49, 517–531 (2006).
  Article CAS Google Scholar
• Fox, A.N. & Zinn, K. The heparan sulfate proteoglycan syndecan is an in vivo ligand for the Drosophila LAR receptor tyrosine phosphatase. Curr. Biol. 15, 1701–1711 (2005).
  Article CAS Google Scholar
• Yang, T. et al. Leukocyte antigen-related protein tyrosine phosphatase receptor: a small ectodomain isoform functions as a homophilic ligand and promotes neurite outgrowth. J. Neurosci. 23, 3353–3363 (2003).
  Article CAS Google Scholar
• Biederer, T. & Scheiffele, P. Mixed-culture assays for analyzing neuronal synapse formation. Nat. Protoc. 2, 670–676 (2007).
  Article CAS Google Scholar
• Ko, J. et al. SALM synaptic cell adhesion–like molecules regulate the differentiation of excitatory synapses. Neuron 50, 233–245 (2006).
  Article CAS Google Scholar
• Zhang, J.S., Honkaniemi, J., Yang, T., Yeo, T.T. & Longo, F.M. LAR tyrosine phosphatase receptor: a developmental isoform is present in neurites and growth cones and its expression is regional- and cell-specific. Mol. Cell. Neurosci. 10, 271–286 (1998).
  Article CAS Google Scholar
• Pulido, R., Serra-Pages, C., Tang, M. & Streuli, M. 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. Proc. Natl. Acad. Sci. USA 92, 11686–11690 (1995).
  Article CAS Google Scholar
• O'Grady, P., Krueger, N.X., Streuli, M. & Saito, H. Genomic organization of the human LAR protein tyrosine phosphatase gene and alternative splicing in the extracellular fibronectin type-III domains. J. Biol. Chem. 269, 25193–25199 (1994).
  CAS PubMed Google Scholar
• Zhang, J.S. & Longo, F.M. LAR tyrosine phosphatase receptor: alternative splicing is preferential to the nervous system, coordinated with cell growth and generates novel isoforms containing extensive CAG repeats. J. Cell Biol. 128, 415–431 (1995).
  Article CAS Google Scholar
• Patel, M.R. et al. Hierarchical assembly of presynaptic components in defined C. elegans synapses. Nat. Neurosci. 9, 1488–1498 (2006).
  Article CAS Google Scholar
• Dai, Y. et al. SYD-2 Liprin-alpha organizes presynaptic active zone formation through ELKS. Nat. Neurosci. 9, 1479–1487 (2006).
  Article CAS Google Scholar
• Bamji, S.X. et al. Role of beta-catenin in synaptic vesicle localization and presynaptic assembly. Neuron 40, 719–731 (2003).
  Article CAS Google Scholar
• Bamji, S.X., Rico, B., Kimes, N. & Reichardt, L.F. BDNF mobilizes synaptic vesicles and enhances synapse formation by disrupting cadherin-beta-catenin interactions. J. Cell Biol. 174, 289–299 (2006).
  Article CAS Google Scholar
• Majeti, R. & Weiss, A. Regulatory mechanisms for receptor protein tyrosine phosphatases. Chem. Rev. 101, 2441–2448 (2001).
  Article CAS Google Scholar
• Nam, H.J., Poy, F., Krueger, N.X., Saito, H. & Frederick, C.A. Crystal structure of the tandem phosphatase domains of RPTP LAR. Cell 97, 449–457 (1999).
  Article CAS Google Scholar