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Lateral Diffusion of Excitatory Neurotransmitter Receptors During Synaptogenesis

  • Laurent Groc
  • Martin Heine
  • Laurent Cognet
  • Brahim Lounis
  • Daniel Choquet
Chapter

1. Summary

The understanding of how receptors accumulate within the developing synapse has captured a lot of attention. Lateral diffusion of surface neurotransmitter receptors has emerged as a key pathway to regulate receptor trafficking and surface distribution, in addition to the receptor cycling between intracellular and plasma membrane pools. The neurotransmitter receptor lateral diffusion depends on several factors, such as interactions with other proteins highly enriched within the synaptic structure. During synaptogenesis, receptors aggregate and cluster within developing synapses. As described in this chapter, lateral diffusion of receptors is likely to play an important role in such process since receptor lateral diffusion is high during synaptogenesis, providing favourable conditions for the “capture” of receptors within synaptic contacts. Indeed, the “diffusion-trap” model for receptor accumulation in developing synapses has now gained experimental support from excitatory synapses, although direct evidence to test this model is still lacking due to the absence of adequate tools to precisely control extrasynaptic receptor lateral diffusion. Within the developing synapse, it also emerges that neurotransmitter release generates surface instability of the receptors and their stabilization requires additional factors.

Keywords

Lateral Diffusion Neurotransmitter Receptor Extrasynaptic Receptor Synaptic Area Lateral Diff 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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9. References

  1. 1.
    Axelrod, D., Ravdin, P., Koppel, D.E., Schlessinger, J., Webb, W.W., Elson, E.L., and Podleski, T.R. (1976) Proc Natl Acad Sci U S A 73, 4594–4598.PubMedCrossRefGoogle Scholar
  2. 2.
    Axelrod, D., Koppel, D.E., Schlessinger, J., Elson, E., and Webb, W.W. (1976) Biophys J 16, 1055–1069.PubMedGoogle Scholar
  3. 3.
    Meier, J., Vannier, C., Sergé, A., Triller, A., and Choquet, D. (2001) Nature Neurosci 4, 253–260.PubMedCrossRefGoogle Scholar
  4. 4.
    Sergé, A., Fourgeaud, L., Hémar, A., and Choquet, D. (2002) J Neurosci 22, 3910–3920.PubMedGoogle Scholar
  5. 5.
    Borgdorff, A., and Choquet, D. (2002) Nature 417, 649–653.PubMedCrossRefGoogle Scholar
  6. 6.
    Tovar, K.R., and Westbrook, G.L. (2002) Neuron 34, 255–264.PubMedCrossRefGoogle Scholar
  7. 7.
    Singer, S.J., and Nicolson, G.L. (1972) Science 175, 720–731.PubMedCrossRefGoogle Scholar
  8. 8.
    Kusumi, A., Ike, H., Nakada, C., Murase, K., and Fujiwara, T. (2005) Semin Immunol 17, 3–21.PubMedCrossRefGoogle Scholar
  9. 9.
    Murase, K., Fujiwara, T., Umemura, Y., Suzuki, K., Iino, R., Yamashita, H., Saito, M., Murakoshi, H., Ritchie, K., and Kusumi, A. (2004) Biophys J 86, 4075–4093.PubMedCrossRefGoogle Scholar
  10. 10.
    Saffman, P.G., and Delbruck, M. (1975) Proc Natl Acad Sci U S A 72, 3111–3113.PubMedCrossRefGoogle Scholar
  11. 11.
    Kucik, D.F., Elson, E.L., and Sheetz, M.P. (1999) Biophys J 76, 314–322.PubMedGoogle Scholar
  12. 12.
    Axelrod, D., Ravdin, P., Koppel, D.E., Schlessinger, J., Webb, W.W., Elson, E.L., and Podleski, T.R. (1976) Proc Natl Acad Sci U S A 73, 4594–4598.PubMedCrossRefGoogle Scholar
  13. 13.
    Tardin, C., Cognet, L., Bats, C., Lounis, B., and Choquet, D. (2003) EMBO J 22, 4656–4665.PubMedCrossRefGoogle Scholar
  14. 14.
    Saxton, M.J., and Jacobson, K. (1997) Annu Rev Biophys Biomol Struct 26, 373–399.PubMedCrossRefGoogle Scholar
  15. 15.
    Schnapp, B.J., Gelles, J., and Sheetz, M.P. (1988) Cell Motility Cytoskeleton 10, 47–53.CrossRefGoogle Scholar
  16. 16.
    Geerts, H., De Brabander, M., Nuydens, R., Geuens, S., Moeremans, M., De Mey, J., and Hollenbeck, P. (1987) Biophys J 52, 775–782.PubMedGoogle Scholar
  17. 17.
    Groc, L., Heine, M., Cognet, L., Brickley, K., Stephenson, F.A., Lounis, B., and Choquet, D. (2004) Nat Neurosci 7, 695–696.PubMedCrossRefGoogle Scholar
  18. 18.
    Boyer, D., Tamarat, P., Maali, A., Lounis, B., and Orrit, M. (2002) Science 297, 1160–1163.PubMedCrossRefGoogle Scholar
  19. 19.
    Dickson R.M., Norris D.J., Tzeng Y.L., and Moerner W.E., (1996) Science 274, 966–969.PubMedCrossRefGoogle Scholar
  20. 20.
    Schmidt, T., Schutz, G.J., Baumgartner, W., Gruber, H.J., and Schindler, H. (1996) Proc Natl Acad Sci U S A 93, 2926–2929.PubMedCrossRefGoogle Scholar
  21. 21.
    Harms G.S., Cognet L., Blab G.A., Lommerse P.H.M., Spaink H.P., and Schmidt, T. (2001) Biophys J 80, 2396–2408.PubMedGoogle Scholar
  22. 22.
    Choquet, D., and Triller, A. (2003) Nat Rev Neurosci 4, 251–265.PubMedCrossRefGoogle Scholar
  23. 23.
    Jacobson, K., Sheets, E.D., and Simson, R. (1995) Science 268, 1441–1442.PubMedCrossRefGoogle Scholar
  24. 24.
    Simson, R., Yang, B., Moore, S.E., Doherty, P., Walsh, F.S., and Jacobson, K.A. (1998) Biophys J 74, 297–308.PubMedCrossRefGoogle Scholar
  25. 25.
    Edidin, M., Kuo, S.C., and Sheetz, M.P. (1991) Science 254, 1379–1382.PubMedCrossRefGoogle Scholar
  26. 26.
    Sako, Y., and Kusumi, A. (1995) J Cell Biol 129, 1559–1574.PubMedCrossRefGoogle Scholar
  27. 27.
    Salome, L., Cazeils, J.L., Lopez, A., and Tocanne, J.F. (1998) Eur Biophys J 27, 391–402.PubMedCrossRefGoogle Scholar
  28. 28.
    Edidin, M., Zuniga, M.C., and Sheetz, M.P. (1994) Proc Natl Acad Sci U S A 91, 3378–3382.PubMedCrossRefGoogle Scholar
  29. 29.
    Thoumine, O., Saint-Michel, E., Dequidt, C., Falk, J., Rudge, R., Galli, T., Faivre-Sarrailh, C., and Choquet, D. (2005) Biophys J, 89, L40–42.PubMedCrossRefGoogle Scholar
  30. 30.
    Kusumi, A., and Sako, Y. (1996) Curr Opin Cell Biol 8, 566–574.PubMedCrossRefGoogle Scholar
  31. 31.
    Edidin, M. (2001) Trends Cell Biol 11, 492–496.PubMedCrossRefGoogle Scholar
  32. 32.
    Fujiwara, T., Ritchie, K., Murakoshi, H., Jacobson, K., and Kusumi, A. (2002) J Cell Biol 157, 1071–1081.PubMedCrossRefGoogle Scholar
  33. 33.
    Sheets, E.D., Lee, G.M., Simson, R., and Jacobson, K. (1997) Biochemistry 36, 12449–12458.PubMedCrossRefGoogle Scholar
  34. 34.
    Winckler, B., Forscher, P., and Mellman, I. (1999) Nature 397, 698–701.PubMedCrossRefGoogle Scholar
  35. 35.
    Borgdorff, A.J., and Choquet, D. (2002) Nature 417, 649–653.PubMedCrossRefGoogle Scholar
  36. 36.
    Tovar, K.R., and Westbrook, G.L. (2002) Neuron 34, 255–264.PubMedCrossRefGoogle Scholar
  37. 37.
    Serge, A., Fourgeaud, L., Hemar, A., and Choquet, D. (2002) J Neurosci 22, 3910–3920.PubMedGoogle Scholar
  38. 38.
    Meier, J., Vannier, C., Serge, A., Triller, A., and Choquet, D. (2001) Nat Neurosci 4, 253–260.PubMedCrossRefGoogle Scholar
  39. 39.
    Dahan, M., Lévi, S., and Triller, A. (2003) Science 302, 442–445.PubMedCrossRefGoogle Scholar
  40. 40.
    Thomas, P., Mortensen, M., Hosie, A.M., and Smart, T.G. (2005) Nat Neurosci 8, 889–897.PubMedGoogle Scholar
  41. 41.
    Meissner, O., and Haberlein, H. (2003) Biochemistry 42, 1667–1672.PubMedCrossRefGoogle Scholar
  42. 42.
    Hegener, O., Prenner, L., Runkel, F., Baader, S.L., Kappler, J., and Haberlein, H. (2004) Biochemistry 43, 6190–6199.PubMedCrossRefGoogle Scholar
  43. 43.
    Carroll, R.C., Beattie, E.C., von Zastrow, M., and Malenka, R.C. (2001) Nat Rev Neurosci 2, 315–324.PubMedCrossRefGoogle Scholar
  44. 44.
    Noel, J., Ralph, G.S., Pickard, L., Williams, J., Molnar, E., Uney, J.B., Collingridge, G.L., and Henley, J.M. (1999) Neuron 23, 365–376.PubMedCrossRefGoogle Scholar
  45. 45.
    Blanpied, T.A., Scott, D.B., and Ehlers, M.D. (2002) Neuron 36, 435–449.PubMedCrossRefGoogle Scholar
  46. 46.
    Petralia, R.S., Wang, Y.X., and Wenthold, R.J. (2003) Eur J Neurosci 18, 3207–3217.PubMedCrossRefGoogle Scholar
  47. 47.
    Passafaro, M., Piech, V., and Sheng, M. (2001) Nat Neurosci 4, 917–926.PubMedCrossRefGoogle Scholar
  48. 48.
    Nusser, Z. (2000) Curr Opin Neurobiol 10, 337–341.PubMedCrossRefGoogle Scholar
  49. 49.
    Pin, J.P., and Duvoisin, R. (1995) Neuropharmacology 34, 1–26.PubMedCrossRefGoogle Scholar
  50. 50.
    Kennedy, M.B. (2000) Science 290, 750–754.PubMedCrossRefGoogle Scholar
  51. 51.
    Walikonis, R.S., Jensen, O.N., Mann, M., Provance, D.W., Jr., Mercer, J.A., and Kennedy, M.B. (2000) J Neurosci 20, 4069–4080.PubMedGoogle Scholar
  52. 52.
    Husi, H., Ward, M.A., Choudhary, J.S., Blackstock, W.P., and Grant, S.G. (2000) Nat Neurosci 3, 661–669.PubMedCrossRefGoogle Scholar
  53. 53.
    Bredt, D.S., and Nicoll, R.A. (2003) Neuron 40, 361–379.PubMedCrossRefGoogle Scholar
  54. 54.
    Schnell, E., Sizemore, M., Karimzadegan, S., Chen, L., Bredt, D.S., and Nicoll, R.A. (2002) Proc Natl Acad Sci U S A 99, 13902–13907.PubMedCrossRefGoogle Scholar
  55. 55.
    Lin, J.W., Ju, W., Foster, K., Lee, S.H., Ahmadian, G., Wyszynski, M., Wang, Y.T., and Sheng, M. (2000) Nat Neurosci 3, 1282–1290.PubMedCrossRefGoogle Scholar
  56. 56.
    Zhou, Q., Xiao, M., and Nicoll, R.A. (2001) Proc Natl Acad Sci U S A 98, 1261–1266.PubMedCrossRefGoogle Scholar
  57. 57.
    Garner, C.C., Zhai, R.G., Gundelfinger, E.D., and Ziv, N.E. (2002) Trends Neurosci 25, 243–251.PubMedCrossRefGoogle Scholar
  58. 58.
    Misgeld, T., Kummer, T.T., Lichtman, J.W., and Sanes, J.R. (2005) Proc Natl Acad Sci U S A 102, 11088–11093.PubMedCrossRefGoogle Scholar
  59. 59.
    Young, S.H., and Poo, M.M. (1983) J Neurosci 3, 225–231.PubMedGoogle Scholar
  60. 60.
    Poo, M. (1982) Nature 295, 332–334.PubMedCrossRefGoogle Scholar
  61. 61.
    Schlessinger, J., Koppel, D.E., Axelrod, D., Jacobson, K., Webb, W.W., and Elson, E.L. (1976) Proc Natl Acad Sci U S A 73, 2409–2413.PubMedCrossRefGoogle Scholar
  62. 62.
    Akaaboune, M., Culican, S.M., Turney, S.G., and Lichtman, J.W. (1999) Science 286, 503–507.PubMedCrossRefGoogle Scholar
  63. 63.
    Gally, C., Eimer, S., Richmond, J.E., and Bessereau, J.L. (2004) Nature 431, 578–582.PubMedCrossRefGoogle Scholar
  64. 64.
    Maric, D., Liu, Q.Y., Grant, G.M., Andreadis, J.D., Hu, Q., Chang, Y.H., Barker, J.L., Joseph, J., Stenger, D.A., and Ma, W. (2000) J Neurosci Res 61, 652–662.PubMedCrossRefGoogle Scholar
  65. 65.
    Sah, D.W., Ray, J., and Gage, F.H. (1997) J Neurobiol 32, 95–110.PubMedCrossRefGoogle Scholar
  66. 66.
    Hagimura, N., Tsuzuki, K., Iino, M., Takatsuru, Y., Yoshida, Y., Kishi, S., and Ozawa, S. (2004) Brain Res Dev Brain Res 152, 213–223.PubMedCrossRefGoogle Scholar
  67. 67.
    Tyzio, R., Represa, A., Jorquera, I., Ben-Ari, Y., Gozlan, H., and Aniksztejn, L. (1999) J Neurosci 19, 10372–10382.PubMedGoogle Scholar
  68. 68.
    Matsuzaki, M., Ellis-Davies, G.C., Nemoto, T., Miyashita, Y., Iino, M., and Kasai, H. (2001) Nat Neurosci 4, 1086–1092.PubMedCrossRefGoogle Scholar
  69. 69.
    Bresler, T., Shapira, M., Boeckers, T., Dresbach, T., Futter, M., Garner, C.C., Rosenblum, K., Gundelfinger, E.D., and Ziv, N.E. (2004) J Neurosci 24, 1507–1520.PubMedCrossRefGoogle Scholar
  70. 70.
    Fiala, J.C., Feinberg, M., Popov, V., and Harris, K.M. (1998) J Neurosci 18, 8900–8911.PubMedGoogle Scholar
  71. 71.
    Rasse, T.M. et al. (2005) Nat Neurosci 8, 898–905.PubMedGoogle Scholar
  72. 72.
    Isaac, J.T. (2003) Neuropharmacology 45, 450–460.PubMedCrossRefGoogle Scholar
  73. 73.
    Voronin, L.L., and Cherubini, E. (2004) J Physiol 557, 3–12.PubMedCrossRefGoogle Scholar
  74. 74.
    Myme, C.I., Sugino, K., Turrigiano, G.G., and Nelson, S.B. (2003) J Neurophysiol 90, 771–779.PubMedCrossRefGoogle Scholar
  75. 75.
    Groc, L., Gustafsson, B., and Hanse, E. (2002) J Neurosci 22, 5552–5562.PubMedGoogle Scholar
  76. 76.
    Xiao, M.Y., Wasling, P., Hanse, E., and Gustafsson, B. (2004) Nat Neurosci 7, 236–243.PubMedCrossRefGoogle Scholar
  77. 77.
    Durand, G.M., Kovalchuk, Y., and Konnerth, A. (1996) Nature 381, 71–75.PubMedCrossRefGoogle Scholar
  78. 78.
    Blanpied, T.A., Scott, D.B., and Ehlers, M.D. (2003) Neurobiol Aging 24, 1095–1104.PubMedCrossRefGoogle Scholar
  79. 79.
    Man, H.Y., Lin, J.W., Ju, W.H., Ahmadian, G., Liu, L., Becker, L.E., Sheng, M., and Wang, Y.T. (2000) Neuron 25, 649–662.PubMedCrossRefGoogle Scholar
  80. 80.
    Ehlers, M.D. (2000) Neuron 28, 511–525.PubMedCrossRefGoogle Scholar
  81. 81.
    Iber, D. (2005) Cell Mol Life Sci 62, 206–213.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2006

Authors and Affiliations

  • Laurent Groc
    • 1
  • Martin Heine
    • 1
  • Laurent Cognet
    • 2
  • Brahim Lounis
    • 2
  • Daniel Choquet
    • 1
  1. 1.CNRS UMR 5091Université Bordeaux 2Bordeaux cedexFrance
  2. 2.CNRS UMR 5798Université Bordeaux 1TalenceFrance

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