• Please log in or register to access this feature.
You have free access to this content

Cbln family proteins promote synapse formation by regulating distinct neurexin signaling pathways in various brain regions

  1. Keiko Matsuda1,2,
  2. Michisuke Yuzaki1,2

Article first published online: 17 MAR 2011

DOI: 10.1111/j.1460-9568.2011.07638.x

Issue

European Journal of Neuroscience

European Journal of Neuroscience

Volume 33, Issue 8, pages 1447–1461, April 2011

Additional Information

How to Cite

Matsuda, K. and Yuzaki, M. (2011), Cbln family proteins promote synapse formation by regulating distinct neurexin signaling pathways in various brain regions. European Journal of Neuroscience, 33: 1447–1461. doi: 10.1111/j.1460-9568.2011.07638.x

Author Information

  1. 1

    Department of Physiology, School of Medicine, Keio University, 35 Shinanomachi, Shinjuku-ku, Tokyo 160-8582, Japan

  2. 2

    Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Corporation, Saitama, Japan

*M. Yuzaki, Department of Physiology, as above. E-mail: myuzaki@a5.keio.jp

Publication History

  1. Issue published online: 17 APR 2011
  2. Article first published online: 17 MAR 2011
  3. Received 2 November 2010, revised 9 January 2011, accepted 26 January 2011

SEARCH

SEARCH BY CITATION

ARTICLE TOOLS

View Full Article with Supporting Information (HTML) Get PDF (1752K)

References

  • Black, J.E., Isaacs, K.R., Anderson, B.J., Alcantara, A.A. & Greenough, W.T. (1990) Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc. Natl Acad. Sci. USA, 87, 5568–5572.
  • Boucard, A.A., Chubykin, A.A., Comoletti, D., Taylor, P. & Sudhof, T.C. (2005) A splice code for trans-synaptic cell adhesion mediated by binding of neuroligin 1 to alpha- and beta-neurexins. Neuron, 48, 229–236.
  • Chen, Y., Stevens, B., Chang, J., Milbrandt, J., Barres, B.A. & Hell, J.W. (2008) NS21: re-defined and modified supplement B27 for neuronal cultures. J. Neurosci. Methods, 171, 239–247.
  • Chih, B., Gollan, L. & Scheiffele, P. (2006) Alternative splicing controls selective trans-synaptic interactions of the neuroligin-neurexin complex. Neuron, 51, 171–178.
  • Craig, A.M. & Kang, Y. (2007) Neurexin-neuroligin signaling in synapse development. Curr. Opin. Neurobiol., 17, 43–52.
  • Dean, C., Scholl, F.G., Choih, J., DeMaria, S., Berger, J., Isacoff, E. & Scheiffele, P. (2003) Neurexin mediates the assembly of presynaptic terminals. Nat. Neurosci., 6, 708–716.
  • Fabrichny, I.P., Leone, P., Sulzenbacher, G., Comoletti, D., Miller, M.T., Taylor, P., Bourne, Y. & Marchot, P. (2007) Structural analysis of the synaptic protein neuroligin and its beta-neurexin complex: determinants for folding and cell adhesion. Neuron, 56, 979–991.
  • Fairless, R., Masius, H., Rohlmann, A., Heupel, K., Ahmad, M., Reissner, C., Dresbach, T. & Missler, M. (2008) Polarized targeting of neurexins to synapses is regulated by their C-terminal sequences. J. Neurosci., 28, 12969–12981.
  • Forrest, D., Yuzaki, M., Soares, H.D., Ng, L., Luk, D.C., Sheng, M., Stewart, C.L., Morgan, J.I., Connor, J.A. & Curran, T. (1994) Targeted disruption of NMDA receptor 1 gene abolishes NMDA response and results in neonatal death. Neuron, 13, 325–338.
  • Fukata, Y., Lovero, K.L., Iwanaga, T., Watanabe, A., Yokoi, N., Tabuchi, K., Shigemoto, R., Nicoll, R.A. & Fukata, M. (2010) Disruption of LGI1-linked synaptic complex causes abnormal synaptic transmission and epilepsy. Proc. Natl Acad. Sci. USA, 107, 3799–3804.
  • Fukaya, M., Tsujita, M., Yamazaki, M., Kushiya, E., Abe, M., Akashi, K., Natsume, R., Kano, M., Kamiya, H., Watanabe, M. & Sakimura, K. (2006) Abundant distribution of TARP gamma-8 in synaptic and extrasynaptic surface of hippocampal neurons and its major role in AMPA receptor expression on spines and dendrites. Eur. J. Neurosci., 24, 2177–2190.
    Direct Link:
  • Graf, E.R., Kang, Y., Hauner, A.M. & Craig, A.M. (2006) Structure function and splice site analysis of the synaptogenic activity of the neurexin-1 beta LNS domain. J. Neurosci., 26, 4256–4265.
  • Hall, A.C., Lucas, F.R. & Salinas, P.C. (2000) Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell, 100, 525–535.
  • Hata, Y., Butz, S. & Sudhof, T.C. (1996) CASK: a novel dlg/PSD95 homolog with an N-terminal calmodulin-dependent protein kinase domain identified by interaction with neurexins. J. Neurosci., 16, 2488–2494.
  • Hirai, H. (2001) Ca2+-dependent regulation of synaptic delta2 glutamate receptor density in cultured rat Purkinje neurons. Eur. J. Neurosci., 14, 73–82.
    Direct Link:
  • Hirai, H., Pang, Z., Bao, D., Miyazaki, T., Li, L., Miura, E., Parris, J., Rong, Y., Watanabe, M., Yuzaki, M. & Morgan, J.I. (2005) Cbln1 is essential for synaptic integrity and plasticity in the cerebellum. Nat. Neurosci., 8, 1534–1541.
  • Ichtchenko, K., Hata, Y., Nguyen, T., Ullrich, B., Missler, M., Moomaw, C. & Sudhof, T.C. (1995) Neuroligin 1: a splice site-specific ligand for beta-neurexins. Cell, 81, 435–443.
  • Ichtchenko, K., Nguyen, T. & Sudhof, T.C. (1996) Structures, alternative splicing, and neurexin binding of multiple neuroligins. J. Biol. Chem., 271, 2676–2682.
  • Iijima, T., Miura, E., Matsuda, K., Kamekawa, Y., Watanabe, M. & Yuzaki, M. (2007) Characterization of a transneuronal cytokine family Cbln – regulation of secretion by heteromeric assembly. Eur. J. Neurosci., 25, 1049–1057.
    Direct Link:
  • Iijima, T., Emi, K. & Yuzaki, M. (2009) Activity-dependent repression of Cbln1 expression: mechanism for developmental and homeostatic regulation of synapses in the cerebellum. J. Neurosci., 29, 5425–5434.
  • Ito-Ishida, A., Miura, E., Emi, K., Matsuda, K., Iijima, T., Kondo, T., Kohda, K., Watanabe, M. & Yuzaki, M. (2008) Cbln1 regulates rapid formation and maintenance of excitatory synapses in mature cerebellar Purkinje cells in vitro and in vivo. J. Neurosci., 28, 5920–5930.
  • Johnson-Venkatesh, E.M. & Umemori, H. (2010) Secreted factors as synaptic organizers. Eur. J. Neurosci., 32, 181–190.
    Direct Link:
  • Kakegawa, W., Miyazaki, T., Kohda, K., Matsuda, K., Emi, K., Motohashi, J., Watanabe, M. & Yuzaki, M. (2009) The N-terminal domain of GluD2 (GluRdelta2) recruits presynaptic terminals and regulates synaptogenesis in the cerebellum in vivo. J. Neurosci., 29, 5738–5748.
  • 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.
  • Koehnke, J., Jin, X., Trbovic, N., Katsamba, P.S., Brasch, J., Ahlsen, G., Scheiffele, P., Honig, B., Palmer, A.G. III & Shapiro, L. (2008) Crystal structures of beta-neurexin 1 and beta-neurexin 2 ectodomains and dynamics of splice insertion sequence 4. Structure, 16, 410–421.
  • Kusnoor, S.V., Parris, J., Muly, E.C., Morgan, J.I. & Deutch, A.Y. (2010) Extracerebellar role for Cerebellin1: modulation of dendritic spine density and synapses in striatal medium spiny neurons. J. Comp. Neurol., 518, 2525–2537.
  • Ledda, F., Paratcha, G., Sandoval-Guzman, T. & Ibanez, C.F. (2007) GDNF and GFRalpha1 promote formation of neuronal synapses by ligand-induced cell adhesion. Nat. Neurosci., 10, 293–300.
  • 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.
  • Lomeli, H., Sprengel, R., Laurie, D.J., Kohr, G., Herb, A., Seeburg, P.H. & Wisden, W. (1993) The rat delta-1 and delta-2 subunits extend the excitatory amino acid receptor family. FEBS Lett., 315, 318–322.
  • Matsuda, K., Kondo, T., Iijima, T., Matsuda, S., Watanabe, M. & Yuzaki, M. (2009) Cbln1 binds to specific postsynaptic sites at parallel fiber-Purkinje cell synapses in the cerebellum. Eur. J. Neurosci., 29, 707–717.
    Direct Link:
  • Matsuda, K., Miura, E., Miyazaki, T., Kakegawa, W., Emi, K., Narumi, S., Fukazawa, Y., Ito-Ishida, A., Kondo, T., Shigemoto, R., Watanabe, M. & Yuzaki, M. (2010) Cbln1 is a ligand for an orphan glutamate receptor delta2, a bidirectional synapse organizer. Science, 328, 363–368.
  • Missler, M., Hammer, R.E. & Sudhof, T.C. (1998) Neurexophilin binding to alpha-neurexins. A single LNS domain functions as an independently folding ligand-binding unit. J. Biol. Chem., 273, 34716–34723.
  • Miura, E., Iijima, T., Yuzaki, M. & Watanabe, M. (2006) Distinct expression of Cbln family mRNAs in developing and adult mouse brains. Eur. J. Neurosci., 24, 750–760.
    Direct Link:
  • Miura, E., Matsuda, K., Morgan, J.I., Yuzaki, M. & Watanabe, M. (2009) Cbln1 accumulates and colocalizes with Cbln3 and GluRdelta2 at parallel fiber-Purkinje cell synapses in the mouse cerebellum. Eur. J. Neurosci., 29, 693–706.
    Direct Link:
  • Nguyen, T. & Sudhof, T.C. (1997) Binding properties of neuroligin 1 and neurexin 1beta reveal function as heterophilic cell adhesion molecules. J. Biol. Chem., 272, 26032–26039.
  • Patzke, H. & Ernsberger, U. (2000) Expression of neurexin Ialpha splice variants in sympathetic neurons: selective changes during differentiation and in response to neurotrophins. Mol. Cell. Neurosci., 15, 561–572.
  • Reissner, C., Klose, M., Fairless, R. & Missler, M. (2008) Mutational analysis of the neurexin/neuroligin complex reveals essential and regulatory components. Proc. Natl Acad. Sci. USA, 105, 15124–15129.
  • Schoenmakers, T.J., Visser, G.J., Flik, G. & Theuvenet, A.P. (1992) CHELATOR: an improved method for computing metal ion concentrations in physiological solutions. BioTechniques, 12, 870–874.
  • 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. J. Neurosci., 30, 7495–7506.
  • Sudhof, T.C. (2001). The synaptic cleft and synaptic cell adhesion. In Cowan, M.W., Sudhof, T.C. & Stevens, C.F. (Eds), Synapse. Johns Hopkins Univ. Press, Baltimore, pp. 275–314.
  • Sudhof, T.C. (2008) Neuroligins and neurexins link synaptic function to cognitive disease. Nature, 455, 903–911.
  • Sugita, S., Saito, F., Tang, J., Satz, J., Campbell, K. & Sudhof, T.C. (2001) A stoichiometric complex of neurexins and dystroglycan in brain. J. Cell Biol., 154, 435–445.
  • Sun, H.B., Yokota, H., Chi, X.X. & Xu, Z.C. (2000) Differential expression of neurexin mRNA in CA1 and CA3 hippocampal neurons in response to ischemic insult. Brain Res. Mol. Brain Res., 84, 146–149.
  • Takeuchi, T., Miyazaki, T., Watanabe, M., Mori, H., Sakimura, K. & Mishina, M. (2005) Control of synaptic connection by glutamate receptor δ2 in the adult cerebellum. J. Neurosci., 25, 2146–2156.
  • Terauchi, A., Johnson-Venkatesh, E.M., Toth, A.B., Javed, D., Sutton, M.A. & Umemori, H. (2010) Distinct FGFs promote differentiation of excitatory and inhibitory synapses. Nature, 465, 783–787.
  • 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.
  • Ullrich, B., Ushkaryov, Y.A. & Sudhof, T.C. (1995) Cartography of neurexins: more than 1000 isoforms generated by alternative splicing and expressed in distinct subsets of neurons. Neuron, 14, 497–507.
  • 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.
  • de Wit, J., Sylwestrak, E., O’Sullivan, M.L., Otto, S., Tiglio, K., Savas, J.N., Yates, J.R. III, Comoletti, D., Taylor, P. & Ghosh, A. (2009) LRRTM2 interacts with Neurexin1 and regulates excitatory synapse formation. Neuron, 64, 799–806.
  • Xu, D., Hopf, C., Reddy, R., Cho, R.W., Guo, L., Lanahan, A., Petralia, R.S., Wenthold, R.J., O’Brien, R.J. & Worley, P. (2003) Narp and NP1 form heterocomplexes that function in developmental and activity-dependent synaptic plasticity. Neuron, 39, 513–528.
  • Yuzaki, M. (2008) Cbln and C1q family proteins: new transneuronal cytokines. Cell. Mol. Life Sci., 65, 1698–1705.
  • Yuzaki, M. (2009) New (but old) molecules regulating synapse integrity and plasticity: Cbln1 and the delta2 glutamate receptor. Neuroscience, 162, 633–643.
View Full Article with Supporting Information (HTML) Get PDF (1752K)