Abstract
The synaptic vesicle cycle at the nerve terminal consists of vesicle exocytosis with neuro-transmitter release, endocytosis of empty vesicles, and regeneration of fresh vesicles. Of all cellular transport pathways, the synaptic vesicle cycle is the fastest and the most tightly regulated. A convergence of results now allows formulation of molecular models for key steps of the cycle. These developments may form the basis for a mechanistic understanding of higher neural function.
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References
Ferro-Novick, S. & Jahn, R. Nature 370, 191–193 (1994).
Bennett, M. K. & Scheller, R. H. A. Rev. Biochem. 63, 63–100 (1994).
Katz, B. The Release of Neural Transmitter Substances (Liverpool Univ. Press, Liverpool, 1969).
Lloyd, D. P. C. in Handbook of Physiology, Section I: Neurophysiology Vol. II (ed. Magoun, H. W.) 929–949 (American Physiology Society, Washington, DC, 1960).
Rastaad, M., Storm, J. F. & Andersen, P. Eur. J. Neurosci. 4, 113–117 (1992).
Hessler, N. A., Shirke, A. M. & Malinow, R. Nature 366, 569–572 (1993).
Rosenmund, C., Clements, J. D. & Westbrook, G. L. Science 262, 754–757 (1993).
Wickelgren, W. O., Leonard, J. P., Grimes, M. J. & Clark, R. D. J. Neurosci. 5, 1188–1201 (1985).
Heuser, J. E. & Reese, T. S. J. Cell Biol. 57, 315–344 (1973).
Fischer von Mollard, G., Südhof, T. C. & Jahn, R. Eur. J. Cell Biol. 65, 319–326 (1994).
Betz, W. J. & Bewick, G. S. Science 255, 200–203 (1992).
Ryan, T. A. et al. Neuron 11, 713–724 (1993).
Landis, D. M. D., Hall, A. K., Weinstein, L. A. & Reese, T. S. Neuron 1, 201–209 (1988).
Usukura, J. & Yamada, E. Cell Tiss. Res. 247, 483–488 (1987).
Muller, K. J. & Nicholls, J. G. J. Physiol., Lond. 238, 357–369 (1974).
Südhof, T. C. & Jahn, R. Neuron 6, 146–148 (1991).
Nuoffer, C. & Balch, W. E. A. Rev. Biochem. 63, 949–990 (1994).
Simons, K. & Zerial, M. Neuron 11, 789–799 (1993).
Fischer von Mollard, G., Stahl, B., Khokhlatchev, A., Südhof, T. C. & Jahn, R. J. biol. Chem. 269, 10971–10974 (1994).
Gorvel, J.-P., Chavrier, P., Zerial, M. & Gruenberg, J. Cell 64, 915–925 (1991).
Geppert, M. et al. Nature 369, 493–497 (1994).
Li, C. et al. Neuron 13, 885–898 (1994).
Ullrich, O. et al. J. biol. Chem. 268, 18143–18150 (1993).
Stahl, B., Fischer von Mollard, G., Walch-Solimena, C. & Jahn, R. J. biol. Chem. 269, 24770–24776 (1994).
Shirataki, H. et al. Molec. cell. Biol. 13, 2061–2068 (1993).
Söllner, T. et al. Nature 363, 318–324 (1993).
Hayashi, T. et al. EMBO J. 13, 5051–5061 (1994).
Söllner, T., Bennett, M. K., Whiteheart, S. W., Scheller, R. H. & Rothman, J. E. Cell 75, 409–418 (1993).
Pevsner, J. et al. Neuron 13, 353–361 (1994).
McMahon, H. T. & Südhof, T. C. J. biol. Chem. 270, 2213–2217 (1995).
Johnston, P. A. & Südhof, T. C. J. biol. Chem. 265, 8869–8873 (1990).
Calakos, N. & Scheller, R. H. J. biol. Chem. 269, 24534–24537 (1994).
Edelmann, L., Hanson, P. I., Chapman, E. R. & Jahn, R. EMBO J. 14, 224–231 (1995).
Hata, Y., Slaughter, C. A. & Südhof, T. C. Nature 366, 347–351 (1993).
Pevsner, J., Hsu, S.-C. & Scheller, R. H. Proc. natn. Acad. U.S.A. 91, 1445–1449 (1994).
Garcia, E. P., Gatti, E., Butler, M., Burton, J. & De Camilli, P. Proc. natn. Acad. U.S.A. 91, 2003–2007 (1994).
Hosono, R., Sassa, T. & Kuno, S. J. Neurochem. 49, 1820–1823 (1987).
Harrison, S. D., Broadie, K., van de Goor, J. & Rubin, G. M. Neuron 13, 555–556 (1994).
Dascher, C., Ossig, R., Gallwitz, D. & Schmitt, H. D. Molec. cell. Biol. 11, 872–885 (1991).
Brennwald, P. et al. Cell. 79, 245–258 (1994).
Schulze, K. L. et al. Neuron 13, 1099–1108 (1994).
Whiteheart, S. W. et al. J. Cell Biol. 126, 945–954 (1994).
Clary, D. O., Griff, I. C. & Rothman, J. E. Cell 61, 709–721 (1990).
Schiavo, G., Rossetto, O., Benfenati, F., Poulain, B. & Montecucco, C. Ann. N.Y. Acad. Sci. 710, 65–75 (1994).
Südhof, T. C., De Camilli, P., Niemann, H. & Jahn, R. Cell 75, 1–4 (1993).
Rothman, J. E. Nature 372, 55–63 (1994).
Dreyer, F., Mallart, A. & Brigant, J. L. Brain Res. 270, 373–375 (1983).
Hunt, J. M. et al. Neuron 12, 1269–1279 (1994).
Koh, S. A. et al. J. Neurocytol. 22, 995–1005 (1993).
Holz, R. W., Bittner, M. A., Peppers, S. C., Senter, R. A. & Eberhard, D. A. J. biol. Chem. 264, 5412–5419 (1989).
Lawrence, G. W., Weller, U. & Dolly, J. O. Eur. J. Biochem. 222, 325–333 (1994).
Kemble, G. W., Danieli, T. & White, J. M. Cell 76, 383–391 (1994).
Dodge, F. A. & Rahamimoff, R. J. Physiol., Lond. 193, 419–432 (1967).
Brose, N., Petrenko, A. G., Südhof, T. C. & Jahn, R. Science 256, 1021–1025 (1992).
Davletov, B. A. & Südhof, T. C. J. biol. Chem. 268, 26386–26390 (1993).
Davletov, B. A. & Südhof, T. C. J. biol. Chem. 269, 28547–28550 (1994).
Geppert, M. et al. Cell 79, 717–727 (1994).
Bommert, K. et al. Nature 363, 163–165 (1993).
Littleton, J. T., Stern, M., Perin, M. & Bellen, H. J. Proc. natn. Acad. U.S.A. 91, 10888–10892 (1994).
DiAntonio, A. & Schwarz, T. L. Neuron 12, 909–920 (1994).
Heidelberger, R., Heinemann, C., Neher, E. & Matthews, G. Nature 371, 513–515 (1994).
Bennett, M. K., Calakos, N. & Scheller, R. H. Science 257, 255–259 (1992).
Yoshida, A. et al. J. biol. Chem. 267, 25925–25928 (1992).
Li, C. et al. Nature 375, 594–599 (1995).
Petrenko, A. G. et al. Nature 351, 411–414 (1991).
Ushkaryov, Y. A., Petrenko, A. G., Geppert, M. & Südhof, T. C. Science 257, 50–56 (1992).
Geppert, M., Archer, B. T. & Südhof, T. C. J. biol. Chem. 266, 13548–13552 (1991).
Mizuta, M. et al. J. biol. Chem. 269, 11675–11678 (1994).
Hilbush, B. S. & Morgan, J. I. Proc. natn. Acad. U.S.A. 91, 8195–8199 (1994).
Ullrich, U. et al. Neuron 13, 1281–1291 (1994).
von Gersdorff, H. & Matthews, G. Nature 370, 652–655 (1994).
Thomas, P., Lee, A. K., Wong, J. G. & Almers, W. J. Cell Biol. 124, 667–675 (1994).
Miller, T. M. & Heuser, J. E. J. Cell Biol. 98, 685–698 (1984).
Ceccarelli, B. F. & Hurlburt, W. P. Physiol. Rev. 60, 396–441 (1980).
Pfeffer, S. R. & Kelly, R. B. Cell 40, 949–957 (1985).
Maycox, P. R., Link, E., Reetz, A., Morris, S. A. & Jahn, R. J. Cell Biol. (1992).
Koenig, J. H. & Ikeda, K. J. Neurosci. 9, 3844–3860 (1989).
Van der Bliek, A. M. & Meyerowitz, E. M. Nature 351, 411–414 (1991).
Chen, M. S. et al. Nature 351, 583–586 (1991).
Robinson, P. J. et al. Nature 365, 163–166 (1993).
Takei, K., McPherson, P. S., Schmid, S. L. & De Camilli, P. Nature 374, 186–190 (1995).
Lindner, R. & Ungewickell, E. J. biol. Chem. 267, 16567–16573 (1992).
Ceccarelli, B. & Hurlbut, W. P. J. Cell Biol. 87, 297–303 (1980).
Zhang, J. Z., Davletov, B. A., Südhof, T. C. & Anderson, R. G. W. Cell 78, 751–760 (1994).
Wang, L.-H., Südhof, T. C. & Anderson, R. G. W. J. biol. Chem. 270, 10079–10083 (1995).
Umbach, J. A. et al. Neuron 13, 899–907 (1994).
Rothman, J. E. & Schmid, S. L. Cell 46, 5–9 (1986).
Weisskopf, M. G., Zalutsky, R. A. & Nicoll, R. A. Nature 362, 423–427 (1993).
Silva, A. J., Stevens, C. F., Tonegawa, S. & Wang, Y. Science 257, 201–206 (1992).
Grant, S. G. N. et al. Science 258, 1903–1910 (1992).
Abeliovich, A. et al. Cell 75, 1253–1262 (1993).
Greengard, P. Molec. Neurobiol. 1, 81–119 (1987).
Südhof, T. C. et al. Science 245, 1474–1480 (1989).
Petrucci, T. C. & Morrow, J. J. Cell Biol. 105, 1355–1363 (1987).
Bähler, M. & Greengard, P. Nature 326, 704–707 (1987).
Steiner, J. P., Ling, E. & Bennett, V. J. biol. Chem. 262, 905–914 (1987).
Baines, A. J. & Bennett, V. Nature 315, 410–413 (1985).
Baines, A. J. & Bennett, V. Nature 319, 145–147 (1986).
Inui, M., Watanabe, T. & Sobue, K. J. Neurochem. 63, 1917–1923 (1994).
McPherson, P. S. et al. Proc. natn. Acad. Sci. U.S.A. 91, 6486–6490 (1994).
Llinas, R., Gruner, J. A., Sugimori, M., McGuiness, T. L. & Greengard, P. J. Physiol., Lond. 463, 257–282 (1991).
Schaeffer, E., Alder, J., Greengard, P. & Poo, M.-M. Proc. natn. Acad. U.S.A. 91, 3882–3886 (1994).
Rosahl, T. W. et al. Cell 75, 661–670 (1993).
Rosahl, T. W. et al. Nature 375, 488–493 (1995).
Harris, K. M. & Stevens, J. K. J. Neurosci. 8, 4455–4469 (1988).
Harris, K. M. & Stevens, J. K. J. Neurosci. 9, 2982–2997 (1989).
Akert, K., Pfenninger, K., Sandri, C. & Moor, K. in Structure and Function of Synapses (eds Pappas, G. D. & Purpura, D. P.) 67–86 (Raven, New York, 1972).
Stevens, C. F. & Tsujimoto, T. Proc. natn. Acad. Sci. U.S.A. 92, 846–849 (1995).
Jahn, R. & Südhof, T. C. A. Rev. Neurosci. 17, 219–246 (1994).
Liu Y. et al. Cell 70, 539–551 (1992).
Alfonso, A., Grundahl, K., Duerr, J. S., Han, H.-P. & Rand, J. B. Science 261, 617–619 (1993).
Lacey, M. L. & Haimo, L. T. J. biol. Chem. 267, 4793–4798 (1992).
Hall, D. H. & Hedgecock, E. M. Cell 65, 837–847 (1991).
Burton, J. L., Burns, M. E., Gatti, E., Augustine, G. J. & De Camilli, P. EMBO J. 13, 5547–5558 (1994).
Maruyama, I. N. & Brenner, S. Proc. natn. Acad. U.S.A. 88, 5729–5733 (1991).
Sheng, Z.-H., Rettig, J., Takahashi, M. & Catterall, W. A. Neuron 13, 1303–1313 (1994).
Nonet, M. L., Grundahl, K., Meyer, B. J. & Rand, J. B. Cell 73, 1291–1305 (1993).
Schulze, K. L., Broadie, K., Perin, M. S. & Bellen, H. F. Cell 80, 311–320 (1995).
Magazanik, L. G. et al. Neuroscience 46, 181–188 (1992).
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Südhof, T. The synaptic vesicle cycle: a cascade of protein–protein interactions. Nature 375, 645–653 (1995). https://doi.org/10.1038/375645a0
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DOI: https://doi.org/10.1038/375645a0
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