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Surface Traffic in Synaptic Membranes

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Synaptic Plasticity

Part of the book series: Advances in Experimental Medicine and Biology ((volume 970))

Abstract

The precision of signal transmission in chemical synapses is highly dependent on the structural alignment between pre- and postsynaptic components. The thermal agitation of transmembrane signaling molecules by surrounding lipid molecules and activity-driven changes in the local protein interaction affinities indicate a dynamic molecular traffic of molecules within synapses. The observation of local protein surface dynamics starts to be a useful tool to determine the contribution of intracellular and extracellular structures in organizing a plastic synapse. Local rearrangements by lateral diffusion in the synaptic and perisynaptic membrane induce fast density changes of signaling molecules and enable the synapse to change efficacy in short time scales. The degree of lateral mobility is restricted by many passive and active interactions inside and outside the membrane. AMPAR at the glutamatergic synapse are the best explored receptors in this respect and reviewed here as an example molecule. In addition, transsynaptic adhesion molecule complexes also appear highly dynamically in the synapse and do further support the importance of local surface traffic in subcellular compartments like synapses.

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References

  • Adesnik, H., Nicoll, R. A., & England, P. M. (2005). Photoinactivation of native AMPA receptors reveals their real-time trafficking. Neuron, 48, 977–985.

    PubMed  CAS  Google Scholar 

  • Allen, J. A., Halverson-Tamboli, R. A., & Rasenick, M. M. (2007). Lipid raft microdomains and neurotransmitter signalling. Nature Reviews Neuroscience, 8, 128–140.

    PubMed  CAS  Google Scholar 

  • Axelrod, D., Koppel, D. E., Schlessinger, J., Elson, E., & Webb, W. W. (1976). Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophysical Journal, 16, 1055–1069.

    PubMed  CAS  Google Scholar 

  • Band, A. M., Ali, H., Vartiainen, M. K., Welti, S., Lappalainen, P., Olkkonen, V. M., & Kuismanen, E. (2002). Endogenous plasma membrane t-SNARE syntaxin 4 is present in rab11 positive endosomal membranes and associates with cortical actin cytoskeleton. FEBS Letters, 531, 513–519.

    PubMed  CAS  Google Scholar 

  • Bannai, H., Levi, S., Schweizer, C., Inoue, T., Launey, T., Racine, V., Sibarita, J. B., Mikoshiba, K., & Triller, A. (2009). Activity-dependent tuning of inhibitory neurotransmission based on GABAAR diffusion dynamics. Neuron, 62, 670–682.

    PubMed  CAS  Google Scholar 

  • Bard, L., Boscher, C., Lambert, M., Mege, R. M., Choquet, D., & Thoumine, O. (2008). A molecular clutch between the actin flow and N-cadherin adhesions drives growth cone migration. Journal of Neuroscience, 28, 5879–5890.

    PubMed  CAS  Google Scholar 

  • Bard, L., Sainlos, M., Bouchet, D., Cousins, S., Mikasova, L., Breillat, C., Stephenson, F. A., Imperiali, B., Choquet, D., & Groc, L. (2010). Dynamic and specific interaction between synaptic NR2-NMDA receptor and PDZ proteins. Proceedings of the National Academy of Sciences of the United States of America, 107, 19561–19566.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • Bats, C., Groc, L., & Choquet, D. (2007). The interaction between Stargazin and PSD-95 regulates AMPA receptor surface trafficking. Neuron, 53, 719–734.

    PubMed  CAS  Google Scholar 

  • Blanpied, T. A., Scott, D. B., & Ehlers, M. D. (2002). Dynamics and regulation of clathrin coats at specialized endocytic zones of dendrites and spines. Neuron, 36, 435–449.

    PubMed  CAS  Google Scholar 

  • Borgdorff, A. J., & Choquet, D. (2002). Regulation of AMPA receptor lateral movements. Nature, 417, 649–653.

    PubMed  CAS  Google Scholar 

  • Breillat, C., Thoumine, O., & Choquet, D. (2007). Characterization of SynCAM surface trafficking using a SynCAM derived ligand with high homophilic binding affinity. Biochemical and Biophysical Research Communications, 359, 655–659.

    PubMed  CAS  Google Scholar 

  • Catterall, W. A., & Few, A. P. (2008). Calcium channel regulation and presynaptic plasticity. Neuron, 59, 882–901.

    PubMed  CAS  Google Scholar 

  • Chan, P. Y., Lawrence, M. B., Dustin, M. L., Ferguson, L. M., Golan, D. E., & Springer, T. A. (1991). Influence of receptor lateral mobility on adhesion strengthening between membranes containing LFA-3 and CD2. The Journal of Cell Biology, 115, 245–255.

    PubMed  CAS  Google Scholar 

  • Charrier, C., Ehrensperger, M. V., Dahan, M., Levi, S., & Triller, A. (2006). Cytoskeleton regulation of glycine receptor number at synapses and diffusion in the plasma membrane. Journal of Neuroscience, 26, 8502–8511.

    PubMed  CAS  Google Scholar 

  • Charrier, C., Machado, P., Tweedie-Cullen, R. Y., Rutishauser, D., Mansuy, I. M., & Triller, A. (2010). A crosstalk between beta1 and beta3 integrins controls glycine receptor and gephyrin trafficking at synapses. Nature Neuroscience, 13, 1388–1395.

    PubMed  CAS  Google Scholar 

  • Chen, L., Chetkovich, D. M., Petralia, R. S., Sweeney, N. T., Kawasaki, Y., Wenthold, R. J., Bredt, D. S., & Nicoll, R. A. (2000). Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature, 408, 936–943.

    PubMed  CAS  Google Scholar 

  • Choquet, D. (2010). Fast AMPAR trafficking for a high-frequency synaptic transmission. European Journal of Neuroscience, 32, 250–260.

    PubMed  Google Scholar 

  • Collingridge, G. L., Isaac, J. T., & Wang, Y. T. (2004). Receptor trafficking and synaptic plasticity. Nature Reviews Neuroscience, 5, 952–962.

    PubMed  CAS  Google Scholar 

  • Dahan, M., Levi, S., Luccardini, C., Rostaing, P., Riveau, B., & Triller, A. (2003). Diffusion dynamics of glycine receptors revealed by single-quantum dot tracking. Science, 302, 442–445.

    PubMed  CAS  Google Scholar 

  • Dalva, M. B., McClelland, A. C., & Kayser, M. S. (2007). Cell adhesion molecules: Signalling functions at the synapse. Nature Reviews Neuroscience, 8, 206–220.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Dequidt, C., Danglot, L., Alberts, P., Galli, T., Choquet, D., & Thoumine, O. (2007). Fast turnover of L1 adhesions in neuronal growth cones involving both surface diffusion and exo/endocytosis of L1 molecules. Molecular Biology of the Cell, 18, 3131–3143.

    PubMed  CAS  Google Scholar 

  • Dityatev, A., Schachner, M., & Sonderegger, P. (2010). The dual role of the extracellular matrix in synaptic plasticity and homeostasis. Nature Reviews Neuroscience, 11, 735–746.

    PubMed  CAS  Google Scholar 

  • Dumoulin, A., Triller, A., & Kneussel, M. (2009). Cellular transport and membrane dynamics of the glycine receptor. Frontiers in Molecular Neuroscience, 2, 28.

    Google Scholar 

  • Dyba, M., Jakobs, S., & Hell, S. W. (2003). Immunofluorescence stimulated emission depletion microscopy. Nature Biotechnology, 21, 1303–1304.

    PubMed  CAS  Google Scholar 

  • Edidin, M. (2003). The state of lipid rafts: From model membranes to cells. Annual Review of Biophysics and Biomolecular Structure, 32, 257–283.

    PubMed  CAS  Google Scholar 

  • Edidin, M., & Fambrough, D. (1973). Fluidity of the surface of cultured muscle fibers. Rapid lateral diffusion of marked surface antigens. The Journal of Cell Biology, 57, 27–37.

    PubMed  CAS  Google Scholar 

  • Ehlers, M. D. (2000). Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron, 28, 511–525.

    PubMed  CAS  Google Scholar 

  • Ehlers, M. D., Heine, M., Groc, L., Lee, M. C., & Choquet, D. (2007). Diffusional trapping of GluR1 AMPA receptors by input-specific synaptic activity. Neuron, 54, 447–460.

    PubMed  CAS  Google Scholar 

  • Featherstone, D. E., & Shippy, S. A. (2008). Regulation of synaptic transmission by ambient extracellular glutamate. The Neuroscientist, 14, 171–181.

    PubMed  CAS  Google Scholar 

  • Feng, W., & Zhang, M. (2009). Organization and dynamics of PDZ-domain-related supramodules in the postsynaptic density. Nature Reviews Neuroscience, 10, 87–99.

    PubMed  CAS  Google Scholar 

  • Fernandes, C. C., Berg, D. K., & Gomez-Varela, D. (2010). Lateral mobility of nicotinic acetylcholine receptors on neurons is determined by receptor composition, local domain, and cell type. Journal of Neuroscience, 30, 8841–8851.

    PubMed  CAS  Google Scholar 

  • Franks, K. M., Stevens, C. F., & Sejnowski, T. J. (2003). Independent sources of quantal variability at single glutamatergic synapses. Journal of Neuroscience, 23, 3186–3195.

    PubMed  CAS  Google Scholar 

  • Frischknecht, R., Heine, M., Perrais, D., Seidenbecher, C. I., Choquet, D., & Gundelfinger, E. D. (2009). Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nature Neuroscience, 12, 897–904.

    PubMed  CAS  Google Scholar 

  • Fromherz, P. (1988). Self-organization of the fluid mosaic of charged channel proteins in membranes. Proceedings of the National Academy of Sciences of the United States of America, 85, 6353–6357.

    PubMed  CAS  Google Scholar 

  • Fu, Y., & Huang, Z. J. (2010). Differential dynamics and activity-dependent regulation of alpha- and beta-neurexins at developing GABAergic synapses. Proceedings of the National Academy of Sciences of the United States of America, 107, 22699–22704.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Gerrow, K., & Triller, A. (2010). Synaptic stability and plasticity in a floating world. Current Opinion in Neurobiology, 20, 631–639.

    PubMed  CAS  Google Scholar 

  • Giannone, G., Hosy, E., Levet, F., Constals, A., Schulze, K., Sobolevsky, A. I., Rosconi, M. P., Gouaux, E., Tampe, R., Choquet, D., & Cognet, L. (2010). Dynamic superresolution imaging of endogenous proteins on living cells at ultra-high density. Biophysical Journal, 99, 1303–1310.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Groc, L., Heine, M., Cognet, L., Brickley, K., Stephenson, F. A., Lounis, B., & Choquet, D. (2004). Differential activity-dependent regulation of the lateral mobilities of AMPA and NMDA receptors. Nature Neuroscience, 7, 695–696.

    PubMed  CAS  Google Scholar 

  • Groc, L., Heine, M., Cousins, S. L., Stephenson, F. A., Lounis, B., Cognet, L., & Choquet, D. (2006). NMDA receptor surface mobility depends on NR2A-2B subunits. Proceedings of the National Academy of Sciences of the United States of America, 103, 18769–18774.

    PubMed  CAS  Google Scholar 

  • Gu, J., Lee, C. W., Fan, Y., Komlos, D., Tang, X., Sun, C., Yu, K., Hartzell, H. C., Chen, G., Bamburg, J. R., & Zheng, J. Q. (2010). ADF/cofilin-mediated actin dynamics regulate AMPA receptor trafficking during synaptic plasticity. Nature Neuroscience, 13, 1208–1215.

    PubMed  CAS  Google Scholar 

  • Gundelfinger, E. D., Frischknecht, R., Choquet, D., & Heine, M. (2010). Converting juvenile into adult plasticity: a role for the brain’s extracellular matrix. European Journal of Neuroscience, 31, 2156–2165.

    PubMed  Google Scholar 

  • Haucke, V., Neher, E., & Sigrist, S. J. (2011). Protein scaffolds in the coupling of synaptic exocytosis and endocytosis. Nature Reviews Neuroscience, 12, 127–138.

    PubMed  CAS  Google Scholar 

  • Hayashi, Y., Shi, S. H., Esteban, J. A., Piccini, A., Poncer, J. C., & Malinow, R. (2000). Driving AMPA receptors into synapses by LTP and CaMKII: Requirement for GluR1 and PDZ domain interaction. Science, 287, 2262–2267.

    PubMed  CAS  Google Scholar 

  • Heine, M., Groc, L., Frischknecht, R., Beique, J. C., Lounis, B., Rumbaugh, G., Huganir, R. L., Cognet, L., & Choquet, D. (2008a). Surface mobility of postsynaptic AMPARs tunes synaptic transmission. Science, 320, 201–205.

    PubMed  CAS  Google Scholar 

  • Heine, M., Thoumine, O., Mondin, M., Tessier, B., Giannone, G., & Choquet, D. (2008b). 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.

    PubMed  CAS  Google Scholar 

  • Hering, H., Lin, C. C., & Sheng, M. (2003). Lipid rafts in the maintenance of synapses, dendritic spines, and surface AMPA receptor stability. Journal of Neuroscience, 23, 3262–3271.

    PubMed  CAS  Google Scholar 

  • Holcman, D., & Triller, A. (2006). Modeling synaptic dynamics driven by receptor lateral diffusion. Biophysical Journal, 91, 2405–2415.

    PubMed  CAS  Google Scholar 

  • Hollmann, M., & Heinemann, S. (1994). Cloned glutamate receptors. Annual Review of Neuroscience, 17, 31–108.

    PubMed  CAS  Google Scholar 

  • Irie, M., Hata, Y., Takeuchi, M., Ichtchenko, K., Toyoda, A., Hirao, K., Takai, Y., Rosahl, T. W., & Sudhof, T. C. (1997). Binding of neuroligins to PSD-95. Science, 277, 1511–1515.

    PubMed  CAS  Google Scholar 

  • Jacob, T. C., Bogdanov, Y. D., Magnus, C., Saliba, R. S., Kittler, J. T., Haydon, P. G., & Moss, S. J. (2005). Gephyrin regulates the cell surface dynamics of synaptic GABAA receptors. Journal of Neuroscience, 25, 10469–10478.

    PubMed  CAS  Google Scholar 

  • Jacob, T. C., Wan, Q., Vithlani, M., Saliba, R. S., Succol, F., Pangalos, M. N., & Moss, S. J. (2009). GABA(A) receptor membrane trafficking regulates spine maturity. Proceedings of the National Academy of Sciences of the United States of America, 106, 12500–12505.

    PubMed  CAS  Google Scholar 

  • Jaskolski, F., Mayo-Martin, B., Jane, D., & Henley, J. M. (2009). Dynamin-dependent membrane drift recruits AMPA receptors to dendritic spines. Journal of Biological Chemistry, 284, 12491–12503.

    PubMed  CAS  Google Scholar 

  • Jewell, J. L., Luo, W., Oh, E., Wang, Z., & Thurmond, D. C. (2008). Filamentous actin regulates insulin exocytosis through direct interaction with syntaxin 4. Journal of Biological Chemistry, 283, 10716–10726.

    PubMed  CAS  Google Scholar 

  • Jonas, P., Major, G., & Sakmann, B. (1993). Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. The Journal of Physiology, 472, 615–663.

    PubMed  CAS  Google Scholar 

  • Kalashnikova, E., Lorca, R. A., Kaur, I., Barisone, G. A., Li, B., Ishimaru, T., Trimmer, J. S., Mohapatra, D. P., & Diaz, E. (2010). SynDIG1: An activity-regulated, AMPA-receptor-interacting transmembrane protein that regulates excitatory synapse development. Neuron, 65, 80–93.

    PubMed  CAS  Google Scholar 

  • Kato, A. S., Gill, M. B., Ho, M. T., Yu, H., Tu, Y., Siuda, E. R., Wang, H., Qian, Y. W., Nisenbaum, E. S., Tomita, S., & Bredt, D. S. (2010). Hippocampal AMPA receptor gating controlled by both TARP and cornichon proteins. Neuron, 68, 1082–1096.

    PubMed  CAS  Google Scholar 

  • Kennedy, M. J., Davison, I. G., Robinson, C. G., & Ehlers, M. D. (2010). Syntaxin-4 defines a domain for activity-dependent exocytosis in dendritic spines. Cell, 141, 524–535.

    PubMed  CAS  Google Scholar 

  • Kessels, H. W., & Malinow, R. (2009). Synaptic AMPA receptor plasticity and behavior. Neuron, 61, 340–350.

    PubMed  CAS  Google Scholar 

  • Kim, C. H., Takamiya, K., Petralia, R. S., Sattler, R., Yu, S., Zhou, W., Kalb, R., Wenthold, R., & Huganir, R. (2005). Persistent hippocampal CA1 LTP in mice lacking the C-terminal PDZ ligand of GluR1. Nature Neuroscience, 8, 985–987.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Kopec, C. D., Real, E., Kessels, H. W., & Malinow, R. (2007). GluR1 links structural and functional plasticity at excitatory synapses. Journal of Neuroscience, 27, 13706–13718.

    PubMed  CAS  Google Scholar 

  • Kusumi, A., Nakada, C., Ritchie, K., Murase, K., Suzuki, K., Murakoshi, H., Kasai, R. S., Kondo, J., & Fujiwara, T. (2005). Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: High-speed single-molecule tracking of membrane molecules. Annual Review of Biophysics and Biomolecular Structure, 34, 351–378.

    PubMed  CAS  Google Scholar 

  • Lee, C. W., Han, J., Bamburg, J. R., Han, L., Lynn, R., & Zheng, J. Q. (2009). Regulation of acetylcholine receptor clustering by ADF/cofilin-directed vesicular trafficking. Nature Neuroscience, 12, 848–856.

    PubMed  CAS  Google Scholar 

  • Lisman, J., Schulman, H., & Cline, H. (2002). The molecular basis of CaMKII function in synaptic and behavioural memory. Nature Reviews Neuroscience, 3, 175–190.

    PubMed  CAS  Google Scholar 

  • Liu, G., Choi, S., & Tsien, R. W. (1999). Variability of neurotransmitter concentration and nonsaturation of postsynaptic AMPA receptors at synapses in hippocampal cultures and slices. Neuron, 22, 395–409.

    PubMed  CAS  Google Scholar 

  • Lu, J., Helton, T. D., Blanpied, T. A., Racz, B., Newpher, T. M., Weinberg, R. J., & Ehlers, M. D. (2007). Postsynaptic positioning of endocytic zones and AMPA receptor cycling by physical coupling of dynamin-3 to Homer. Neuron, 55, 874–889.

    PubMed  CAS  Google Scholar 

  • Makino, H., & Malinow, R. (2009). AMPA receptor incorporation into synapses during LTP: The role of lateral movement and exocytosis. Neuron, 64, 381–390.

    PubMed  CAS  Google Scholar 

  • Malenka, R. C. (2003). Synaptic plasticity and AMPA receptor trafficking. Annals of the New York Academy of Sciences, 1003, 1–11.

    PubMed  CAS  Google Scholar 

  • Manley, S., Gillette, J. M., Patterson, G. H., Shroff, H., Hess, H. F., Betzig, E., & Lippincott-Schwartz, J. (2008). High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nature Methods, 5, 155–157.

    PubMed  CAS  Google Scholar 

  • Marguet, D., Lenne, P. F., Rigneault, H., & He, H. T. (2006). Dynamics in the plasma membrane: How to combine fluidity and order. EMBO Journal, 25, 3446–3457.

    PubMed  CAS  Google Scholar 

  • McAllister, A. K., & Stevens, C. F. (2000). Nonsaturation of AMPA and NMDA receptors at hippocampal synapses. Proceedings of the National Academy of Sciences of the United States of America, 97, 6173–6178.

    PubMed  CAS  Google Scholar 

  • Meier, J., Vannier, C., Serge, A., Triller, A., Choquet, D., & M-247* (2001). Fast and reversible trapping of surface glycine receptors by gephyrin. Nature Neuroscience, 4, 253–260.

    Google Scholar 

  • Meng, Y., Zhang, Y., Jia, Z., & M-508* (2003). Synaptic transmission and plasticity in the absence of AMPA glutamate receptor GluR2 and GluR3. Neuron, 39, 163–176.

    Google Scholar 

  • Miesenbock, G., De Angelis, D. A., & Rothman, J. E. (1998). Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature, 394, 192–195.

    PubMed  CAS  Google Scholar 

  • Milstein, A. D., & Nicoll, R. A. (2008). Regulation of AMPA receptor gating and pharmacology by TARP auxiliary subunits. Trends in Pharmacological Sciences, 29, 333–339.

    PubMed  CAS  Google Scholar 

  • Milstein, A. D., Zhou, W., Karimzadegan, S., Bredt, D. S., & Nicoll, R. A. (2007). TARP subtypes differentially and dose-dependently control synaptic AMPA receptor gating. Neuron, 55, 905–918.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Morimoto-Tomita, M., Zhang, W., Straub, C., Cho, C. H., Kim, K. S., Howe, J. R., & Tomita, S. (2009). Autoinactivation of neuronal AMPA receptors via glutamate-regulated TARP interaction. Neuron, 61, 101–112.

    PubMed  CAS  Google Scholar 

  • Muir, J., Arancibia-Carcamo, I. L., MacAskill, A. F., Smith, K. R., Griffin, L. D., & Kittler, J. T. (2010). NMDA receptors regulate GABAA receptor lateral mobility and clustering at inhibitory synapses through serine 327 on the gamma2 subunit. Proceedings of the National Academy of Sciences of the United States of America, 107, 16679–16684.

    PubMed  CAS  Google Scholar 

  • Nakada, C., Ritchie, K., Oba, Y., Nakamura, M., Hotta, Y., Iino, R., Kasai, R. S., Yamaguchi, K., Fujiwara, T., & Kusumi, A. (2003). Accumulation of anchored proteins forms membrane diffusion barriers during neuronal polarization. Nature Cell Biology, 5, 626–632.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Neher, E., & Sakaba, T. (2008). Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron, 59, 861–872.

    PubMed  CAS  Google Scholar 

  • Newpher, T. M., & Ehlers, M. D. (2008). Glutamate receptor dynamics in dendritic microdomains. Neuron, 58, 472–497.

    PubMed  CAS  Google Scholar 

  • Opazo, P., Labrecque, S., Tigaret, C. M., Frouin, A., Wiseman, P. W., De Koninck, P., & Choquet, D. (2010). CaMKII triggers the diffusional trapping of surface AMPARs through phosphorylation of stargazin. Neuron, 67, 239–252.

    PubMed  CAS  Google Scholar 

  • Panicker, S., Brown, K., & Nicoll, R. A. (2008). Synaptic AMPA receptor subunit trafficking is independent of the C terminus in the GluR2-lacking mouse. Proceedings of the National Academy of Sciences of the United States of America, 105, 1032–1037.

    PubMed  CAS  Google Scholar 

  • Park, M., Penick, E. C., Edwards, J. G., Kauer, J. A., & Ehlers, M. D. (2004). Recycling endosomes supply AMPA receptors for LTP. Science, 305, 1972–1975.

    PubMed  CAS  Google Scholar 

  • Petrini, E. M., Lu, J., Cognet, L., Lounis, B., Ehlers, M. D., & Choquet, D. (2009). Endocytic trafficking and recycling maintain a pool of mobile surface AMPA receptors required for synaptic potentiation. Neuron, 63, 92–105.

    PubMed  CAS  Google Scholar 

  • Poo, M. M. (1985). Mobility and localization of proteins in excitable membranes. Annual Review of Neuroscience, 8, 369–406.

    PubMed  CAS  Google Scholar 

  • Poo, M., Lam, J. W., Orida, N., & Chao, A. W. (1979). Electrophoresis and diffusion in the plane of the cell membrane. Biophysical Journal, 26, 1–21.

    PubMed  CAS  Google Scholar 

  • Pooler, A. M., & McIlhinney, R. A. (2007). Lateral diffusion of the GABAB receptor is regulated by the GABAB2 C terminus. Journal of Biological Chemistry, 282, 25349–25356.

    PubMed  CAS  Google Scholar 

  • Poulopoulos, A., Aramuni, G., Meyer, G., Soykan, T., Hoon, M., Papadopoulos, T., Zhang, M., Paarmann, I., Fuchs, C., Harvey, K., Jedlicka, P., Schwarzacher, S. W., Betz, H., Harvey, R. J., Brose, N., Zhang, W., & Varoqueaux, F. (2009). Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin. Neuron, 63, 628–642.

    PubMed  CAS  Google Scholar 

  • Priel, A., Kolleker, A., Ayalon, G., Gillor, M., Osten, P., & Stern-Bach, Y. (2005). Stargazin reduces desensitization and slows deactivation of the AMPA-type glutamate receptors. Journal of Neuroscience, 25, 2682–2686.

    PubMed  CAS  Google Scholar 

  • Racz, B., Blanpied, T. A., Ehlers, M. D., & Weinberg, R. J. (2004). Lateral organization of endocytic machinery in dendritic spines. Nature Neuroscience, 7, 917–918.

    PubMed  CAS  Google Scholar 

  • Raghavachari, S., & Lisman, J. E. (2004). Properties of quantal transmission at CA1 synapses. Journal of Neurophysiology, 92, 2456–2467.

    PubMed  CAS  Google Scholar 

  • Raman, I. M., & Trussell, L. O. (1995). The mechanism of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate receptor desensitization after removal of glutamate. Biophysical Journal, 68, 137–146.

    PubMed  CAS  Google Scholar 

  • Renner, M., Choquet, D., & Triller, A. (2009a). Control of the postsynaptic membrane viscosity. Journal of Neuroscience, 29, 2926–2937.

    PubMed  CAS  Google Scholar 

  • Renner, M. L., Cognet, L., Lounis, B., Triller, A., & Choquet, D. (2009b). The excitatory postsynaptic density is a size exclusion diffusion environment. Neuropharmacology, 56, 30–36.

    PubMed  CAS  Google Scholar 

  • Renner, M., Lacor, P. N., Velasco, P. T., Xu, J., Contractor, A., Klein, W. L., & Triller, A. (2010). Deleterious effects of amyloid beta oligomers acting as an extracellular scaffold for mGluR5. Neuron, 66, 739–754.

    PubMed  CAS  Google Scholar 

  • Rouach, N., Byrd, K., Petralia, R. S., Elias, G. M., Adesnik, H., Tomita, S., Karimzadegan, S., Kealey, C., Bredt, D. S., Nicoll, R. A. (2005). TARP gamma-8 controls hippocampal AMPA receptor number, distribution and synaptic plasticity. Nature Neuroscience, 8, 1525–1533.

    Google Scholar 

  • Rust, M. B., Gurniak, C. B., Renner, M., Vara, H., Morando, L., Gorlich, A., Sassoe-Pognetto, M., Banchaabouchi, M. A., Giustetto, M., Triller, A., Choquet, D., & Witke, W. (2010). Learning, AMPA receptor mobility and synaptic plasticity depend on n-cofilin-mediated actin dynamics. EMBO Journal, 29, 1889–1902.

    PubMed  CAS  Google Scholar 

  • Sainlos, M., Tigaret, C., Poujol, C., Olivier, N. B., Bard, L., Breillat, C., Thiolon, K., Choquet, D., & Imperiali, B. (2011). Biomimetic divalent ligands for the acute disruption of synaptic AMPAR stabilization. Nature Chemical Biology, 7, 81–91.

    PubMed  CAS  Google Scholar 

  • Saint-Michel, E., Giannone, G., Choquet, D., & Thoumine, O. (2009). Neurexin/neuroligin interaction kinetics characterized by counting single cell-surface attached quantum dots. Biophysical Journal, 97, 480–489.

    PubMed  CAS  Google Scholar 

  • Santamaria, F., Gonzalez, J., Augustine, G. J., & Raghavachari, S. (2010). Quantifying the effects of elastic collisions and non-covalent binding on glutamate receptor trafficking in the post-synaptic density. PLoS Computational Biology, 6, e1000780.

    PubMed  Google Scholar 

  • Savtchenko, L. P., Korogod, S. M., & Rusakov, D. A. (2000). Electrodiffusion of synaptic receptors: A mechanism to modify synaptic efficacy? Synapse, 35, 26–38.

    PubMed  CAS  Google Scholar 

  • Saxton, M. J., & Jacobson, K. (1997). Single-particle tracking: Applications to membrane dynamics. Annual Review of Biophysics and Biomolecular Structure, 26, 373–399.

    PubMed  CAS  Google Scholar 

  • Scheiffele, P., Fan, J., Choih, J., Fetter, R., & Serafini, T. (2000). Neuroligin expressed in nonneuronal cells triggers presynaptic development in contacting axons. Cell, 101, 657–669.

    PubMed  CAS  Google Scholar 

  • Schnell, E., Sizemore, M., Karimzadegan, S., Chen, L., Bredt, D. S., Nicoll, R. A., & M-421* (2002). Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number. Proceedings of the National Academy of Sciences of the United States of America, 99, 13902–13907. Epub 12002 Oct 13901.

    Google Scholar 

  • Schuss, Z., Singer, A., & Holcman, D. (2007). The narrow escape problem for diffusion in cellular microdomains. Proceedings of the National Academy of Sciences of the United States of America, 104, 16098–16103.

    PubMed  CAS  Google Scholar 

  • Schwenk, J., Harmel, N., Zolles, G., Bildl, W., Kulik, A., Heimrich, B., Chisaka, O., Jonas, P., Schulte, U., Fakler, B., & Klocker, N. (2009). Functional proteomics identify cornichon proteins as auxiliary subunits of AMPA receptors. Science, 323, 1313–1319.

    PubMed  CAS  Google Scholar 

  • Scott, L., Zelenin, S., Malmersjo, S., Kowalewski, J. M., Markus, E. Z., Nairn, A. C., Greengard, P., Brismar, H., & Aperia, A. (2006). Allosteric changes of the NMDA receptor trap diffusible dopamine 1 receptors in spines. Proceedings of the National Academy of Sciences of the United States of America, 103, 762–767.

    PubMed  CAS  Google Scholar 

  • Shi, S., Hayashi, Y., Esteban, J. A., & Malinow, R. (2001). Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell, 105, 331–343.

    PubMed  CAS  Google Scholar 

  • Shouval, H. Z. (2005). Clusters of interacting receptors can stabilize synaptic efficacies. Proceedings of the National Academy of Sciences of the United States of America, 102, 14440–14445.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Sylantyev, S., Savtchenko, L. P., Niu, Y. P., Ivanov, A. I., Jensen, T. P., Kullmann, D. M., Xiao, M. Y., & Rusakov, D. A. (2008). Electric fields due to synaptic currents sharpen excitatory transmission. Science, 319, 1845–1849.

    PubMed  CAS  Google Scholar 

  • Tai, C. Y., Mysore, S. P., Chiu, C., & Schuman, E. M. (2007). Activity-regulated N-cadherin endocytosis. Neuron, 54, 771–785.

    PubMed  CAS  Google Scholar 

  • Tallafuss, A., Constable, J. R., & Washbourne, P. (2010). Organization of central synapses by adhesion molecules. European Journal of Neuroscience, 32, 198–206.

    PubMed  Google Scholar 

  • Tardin, C., Cognet, L., Bats, C., Lounis, B., & Choquet, D. (2003). Direct imaging of lateral movements of AMPA receptors inside synapses. EMBO Journal, 22, 4656–4665.

    PubMed  CAS  Google Scholar 

  • Thomas, P., Mortensen, M., Hosie, A. M., Smart, T. G. (2005). Dynamic mobility of functional GABAA receptors at inhibitory synapses. Nature Neuroscience, 8, 889–897.

    Google Scholar 

  • Thoumine, O., Ewers, H., Heine, M., Groc, L., Frischknecht, R., Giannone, G., Poujol, C., Legros, P., Lounis, B., Cognet, L., & Choquet, D. (2008). Probing the dynamics of protein-protein interactions at neuronal contacts by optical imaging. Chemical Reviews, 108, 1565–1587.

    PubMed  CAS  Google Scholar 

  • Thyagarajan, A., & Ting, A. Y. (2010). Imaging activity-dependent regulation of neurexin-neuroligin interactions using trans-synaptic enzymatic biotinylation. Cell, 143, 456–469.

    PubMed  CAS  Google Scholar 

  • Tomita, S., Adesnik, H., Sekiguchi, M., Zhang, W., Wada, K., Howe, J. R., Nicoll, R. A., & Bredt, D. S. (2005). Stargazin modulates AMPA receptor gating and trafficking by distinct domains. Nature, 435, 1052–1058.

    PubMed  CAS  Google Scholar 

  • Toomre, D., & Bewersdorf, J. (2010). A new wave of cellular imaging. Annual Review of Cell and Developmental Biology, 26, 285–314.

    PubMed  CAS  Google Scholar 

  • Tovar, K. R., & Westbrook, G. L. (2002). Mobile NMDA receptors at hippocampal synapses. Neuron, 34, 255–264.

    PubMed  CAS  Google Scholar 

  • Tretter, V., Jacob, T. C., Mukherjee, J., Fritschy, J. M., Pangalos, M. N., & Moss, S. J. (2008). The clustering of GABA(A) receptor subtypes at inhibitory synapses is facilitated via the direct binding of receptor alpha 2 subunits to gephyrin. Journal of Neuroscience, 28, 1356–1365.

    PubMed  CAS  Google Scholar 

  • Tretter, V., & Moss, S. J. (2008). GABA(A) receptor dynamics and constructing GABAergic synapses. Frontiers in Molecular Neuroscience, 1, 7.

    PubMed  Google Scholar 

  • Triller, A., & Choquet, D. (2008). New concepts in synaptic biology derived from single-molecule imaging. Neuron, 59, 359–374.

    PubMed  CAS  Google Scholar 

  • Trussell, L. O., Zhang, S., & Raman, I. M. (1993). Desensitization of AMPA receptors upon multiquantal neurotransmitter release. Neuron, 10, 1185–1196.

    PubMed  CAS  Google Scholar 

  • von Engelhardt, J., Mack, V., Sprengel, R., Kavenstock, N., Li, K. W., Stern-Bach, Y., Smit, A. B., Seeburg, P. H., & Monyer, H. (2010). CKAMP44: A brain-specific protein attenuating short-term synaptic plasticity in the dentate gyrus. Science, 327, 1518–1522.

    Google Scholar 

  • Xie, X., Liaw, J. S., Baudry, M., & Berger, T. W. (1997). Novel expression mechanism for synaptic potentiation: Alignment of presynaptic release site and postsynaptic receptor. Proceedings of the National Academy of Sciences of the United States of America, 94, 6983–6988.

    PubMed  CAS  Google Scholar 

  • Xu-Friedman, M. A., & Regehr, W. G. (2003). Ultrastructural contributions to desensitization at cerebellar mossy fiber to granule cell synapses. Journal of Neuroscience, 23, 2182–2192.

    PubMed  CAS  Google Scholar 

  • Yang, Y. M., Fedchyshyn, M. J., Grande, G., Aitoubah, J., Tsang, C. W., Xie, H., Ackerley, C. A., Trimble, W. S., & Wang, L. Y. (2010). Septins regulate developmental switching from microdomain to nanodomain coupling of Ca(2+) influx to neurotransmitter release at a central synapse. Neuron, 67, 100–115.

    PubMed  CAS  Google Scholar 

  • Young, S. H., & Poo, M. M. (1983). Topographical rearrangement of acetylcholine receptors alters channel kinetics. Nature, 304, 161–163.

    PubMed  CAS  Google Scholar 

  • Yudowski, G. A., Puthenveedu, M. A., & von Zastrow, M. (2006). Distinct modes of regulated receptor insertion to the somatodendritic plasma membrane. Nature Neuroscience, 9, 622–627.

    PubMed  CAS  Google Scholar 

  • Zamanillo, D., Sprengel, R., Hvalby, O., Jensen, V., Burnashev, N., Rozov, A., Kaiser, K. M., Koster, H. J., Borchardt, T., Worley, P., Lubke, J., Frotscher, M., Kelly, P. H., Sommer, B., Andersen, P., Seeburg, P. H., & Sakmann, B. (1999). Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science, 284, 1805–1811.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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. Journal of Neuroscience, 25, 4330–4342.

    PubMed  CAS  Google Scholar 

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  1. Research Group Molecular Physiology, Leibniz Institute for Neurobiology, 39118, Magdeburg, Germany

    Martin Heine

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  1. , PG Neuroplasticity, Leibniz Institute for Neurobiology, Brenneckestraße 6, Magdeburg, 39118, Germany

    Michael R. Kreutz

  2. , Institute of Neuroscience, CR6 CNR-IN Consiglio Nazionale delle Ric, Via Vanvitelli, 32, Milano, 20129, Italy

    Carlo Sala

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Heine, M. (2012). Surface Traffic in Synaptic Membranes. In: Kreutz, M., Sala, C. (eds) Synaptic Plasticity. Advances in Experimental Medicine and Biology, vol 970. Springer, Vienna. https://doi.org/10.1007/978-3-7091-0932-8_9

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