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THE SYNAPTIC VESICLE CYCLE
Abstract
▪ Abstract Neurotransmitter release is mediated by exocytosis of synaptic vesicles at the presynaptic active zone of nerve terminals. To support rapid and repeated rounds of release, synaptic vesicles undergo a trafficking cycle. The focal point of the vesicle cycle is Ca 2+-triggered exocytosis that is followed by different routes of endocytosis and recycling. Recycling then leads to the docking and priming of the vesicles for another round of exo- and endocytosis. Recent studies have led to a better definition than previously available of how Ca 2+ triggers exocytosis and how vesicles recycle. In particular, insight into how Munc18-1 collaborates with SNARE proteins in fusion, how the vesicular Ca 2+ sensor synaptotagmin 1 triggers fast release, and how the vesicular Rab3 protein regulates release by binding to the active zone proteins RIM1α and RIM2α has advanced our understanding of neurotransmitter release. The present review attempts to relate these molecular data with physiological results in an emerging view of nerve terminals as macromolecular machines.
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Short-Term Synaptic Plasticity
Zucker, R. S., & Regehr, W. G. (2002) · Annual Review of Physiology · doi:10.1146/annurev.physiol.64.092501.114547 · Cited by 5,068
SNAP receptors implicated in vesicle targeting and fusion
Söllner, T. H., Whiteheart, S. W., Brunner, M., Erdjument‐Bromage, H., Geromanos, S. J., Tempst, P., & Rothman, J. E. (1993) · Nature · doi:10.1038/362318a0 · Cited by 3,239
Heuser, J. E., & Reese, T. S. (1973) · The Journal of Cell Biology · doi:10.1083/jcb.57.2.315 · Cited by 2,147
The synaptic vesicle cycle: a cascade of protein–protein interactions
Südhof, T. C. (1995) · Nature · doi:10.1038/375645a0 · Cited by 1,991
Self-citationSynaptotagmin I: A major Ca2+ sensor for transmitter release at a central synapse
Geppert, M., Goda, Y., Hammer, R. E., Li, C., Rosahl, T. W., Stevens, C. F., & Südhof, T. C. (1994) · Cell · doi:10.1016/0092-8674(94)90556-8 · Cited by 1,483
Self-citationSynaptic assembly of the brain in the absence of neurotransmitter secretion.
Verhage, M., Maia, A., Plomp, J., Brussaard, A., Heeroma, J., Vermeer, H., Toonen, R., Hammer, R., van den Berg, T. K., Missler, M., et al. (2000) · Science · doi:10.1126/science.287.5454.864 · Cited by 1,387
Self-citationJahn, R., Lang, T., & Südhof, T. C. (2003) · Cell · doi:10.1016/s0092-8674(03)00112-0 · Cited by 1,364
Self-citationSyntaxin: A Synaptic Protein Implicated in Docking of Synaptic Vesicles at Presynaptic Active Zones
Bennett, M. K., Calakos, N., & Scheller, R. H. (1992) · Science · doi:10.1126/science.1321498 · Cited by 1,263
SNARE-mediated membrane fusion
Chen, Y. A., & Scheller, R. H. (2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35052017 · Cited by 1,133
Definition of the readily releasable pool of vesicles at hippocampal synapses.
Rosenmund, C., & Stevens, C. (1996) · Neuron · doi:10.1016/s0896-6273(00)80146-4 · Cited by 1,084
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Malenka, R. C., & Bear, M. F. (2004) · Neuron · doi:10.1016/j.neuron.2004.09.012 · Cited by 3,968
SNAREs — engines for membrane fusion
Jahn, R., & Scheller, R. H. (2006) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2002 · Cited by 2,635
Molecular anatomy of a trafficking organelle
Takamori, S., Holt, M., Stenius, K., Lemke, E. A., Grønborg, M., Riedel, D., Urlaub, H., Schenck, S., Brügger, B., Ringler, P., et al. (2006) · Cell · doi:10.1016/j.cell.2006.10.030 · Cited by 2,373
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Südhof, T. C. (2008) · Nature · doi:10.1038/nature07456 · Cited by 1,849
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Catterall, W. A. (2011) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a003947 · Cited by 1,628
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Willig, K. I., Rizzoli, S. O., Westphal, V., Jahn, R., & Hell, S. W. (2006) · Nature · doi:10.1038/nature04592 · Cited by 1,236
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Rizzuto, R., & Pozzan, T. (2005) · Physiological Reviews · doi:10.1152/physrev.00004.2005 · Cited by 1,234
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Azmi, A. S., Bao, B., & Sarkar, F. H. (2013) · Cancer and Metastasis Reviews · doi:10.1007/s10555-013-9441-9 · Cited by 1,187
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Jahn, R., & Fasshauer, D. (2012) · Nature · doi:10.1038/nature11320 · Cited by 1,004
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Sheng, M., & Hoogenraad, C. C. (2007) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.76.060805.160029 · Cited by 1,003
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Chandra, S. S., Gallardo, G., Fernández‐Chacón, R., Schlüter, O. M., & Südhof, T. C. (2005) · Cell · doi:10.1016/j.cell.2005.09.028 · Cited by 990
Self-citationRizzoli, S. O., & Betz, W. J. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1583 · Cited by 975
SLC6 Neurotransmitter Transporters: Structure, Function, and Regulation
Kristensen, A. S., Andersen, J., Jørgensen, T. N., Sørensen, L., Eriksen, J., Loland, C. J., Strømgaard, K., & Gether, U. (2011) · Pharmacological Reviews · doi:10.1124/pr.108.000869 · Cited by 874
Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy.
Cingolani, L. A., & Goda, Y. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2373 · Cited by 831
Skeletal muscle: A review of molecular structure and function, in health and disease
Mukund, K., & Subramaniam, S. (2019) · WIREs Systems Biology and Medicine · doi:10.1002/wsbm.1462 · Cited by 805
Video-Rate Far-Field Optical Nanoscopy Dissects Synaptic Vesicle Movement
Westphal, V., Rizzoli, S. O., Lauterbach, M. A., Kamin, D., Jahn, R., & Hell, S. W. (2008) · Science · doi:10.1126/science.1154228 · Cited by 799
SV2 Is the Protein Receptor for Botulinum Neurotoxin A
Dong, M., Yeh, F. L., Tepp, W. H., Dean, C., Johnson, E. A., Janz, R., & Chapman, E. R. (2006) · Science · doi:10.1126/science.1123654 · Cited by 777
Composition of isolated synaptic boutons reveals the amounts of vesicle trafficking proteins
Wilhelm, B. G., Mandad, S., Truckenbrodt, S., Kröhnert, K., Schäfer, C., Rammner, B., Koo, S. J., Claßen, G. A., Krauss, M., Haucke, V., et al. (2014) · Science · doi:10.1126/science.1252884 · Cited by 770
Roux, I., Safieddine, S., Nouvian, R., Grati, M., Simmler, M., Bahloul, A., Perfettini, I., Gall, M. L., Rostaing, P., Hamard, G., et al. (2006) · Cell · doi:10.1016/j.cell.2006.08.040 · Cited by 753
Mechanisms of membrane fusion: disparate players and common principles
Martens, S., & McMahon, H. T. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2417 · Cited by 733
Hong, W. (2005) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2005.03.014 · Cited by 648
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Catterall, W. A., & Few, A. P. (2008) · Neuron · doi:10.1016/j.neuron.2008.09.005 · Cited by 647
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Seino, S., & Shibasaki, T. (2005) · Physiological Reviews · doi:10.1152/physrev.00001.2005 · Cited by 573
Saitsu, H., Kato, M., Mizuguchi, T., Hamada, K., Osaka, H., Tohyama, J., Uruno, K., Kumada, S., Nishiyama, K., Nishimura, A., et al. (2008) · Nature Genetics · doi:10.1038/ng.150 · Cited by 564
Rizo, J., & Rosenmund, C. (2008) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1450 · Cited by 552
Impaired dopamine release and synaptic plasticity in the striatum of PINK1 -deficient mice
Kitada, T., Pisani, A., Porter, D. R., Yamaguchi, H., Tscherter, A., Martella, G., Bonsi, P., Zhang, C., Pothos, E. N., & Shen, J. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0702717104 · Cited by 550
Single-Neuron Sequencing Analysis of L1 Retrotransposition and Somatic Mutation in the Human Brain
Evrony, G. D., Cai, X., Lee, E., Hills, L. B., Elhosary, P. C., Lehmann, H. S., Parker, J. J., Atabay, K. D., Gilmore, E. C., Poduri, A., et al. (2012) · Cell · doi:10.1016/j.cell.2012.09.035 · Cited by 548
How Does Synaptotagmin Trigger Neurotransmitter Release?
Chapman, E. R. (2008) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.77.062005.101135 · Cited by 547
Bellen, H. J., Tong, C., & Tsuda, H. (2010) · Nature reviews. Neuroscience · doi:10.1038/nrn2839 · Cited by 544
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Südhof, T. C., & Rizo, J. (2011) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005637 · Cited by 539
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Kamei, M., Saunders, W. B., Bayless, K. J., Dye, L., Davis, G. E., & Weinstein, B. M. (2006) · Nature · doi:10.1038/nature04923 · Cited by 532
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Martens, S., Kozlov, M. M., & McMahon, H. T. (2007) · Science · doi:10.1126/science.1142614 · Cited by 528
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Ferguson, S. M., Brasnjo, G., Hayashi, M., Wölfel, M., Collesi, C., Giovedì, S., Raimondi, A., Gong, L., Ariel, P., Paradise, S., et al. (2007) · Science · doi:10.1126/science.1140621 · Cited by 516
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Sudhof, T. C. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a011353 · Cited by 502
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Knödler, A., Feng, S., Zhang, J., Zhang, X., Das, A. K., Peränen, J., & Guo, W. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002401107 · Cited by 493
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Shen, J., Tareste, D. C., Paumet, F., Rothman, J. E., & Melia, T. J. (2007) · Cell · doi:10.1016/j.cell.2006.12.016 · Cited by 487
Lower synaptic density is associated with depression severity and network alterations
Holmes, S. E., Scheinost, D., Finnema, S. J., Naganawa, M., Davis, M. T., DellaGioia, N., Nabulsi, N., Matuskey, D., Angarita, G. A., Pietrzak, R. H., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-09562-7 · Cited by 484
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Tang, J., Maximov, A., Shin, O., Dai, H., Rizo, J., & Südhof, T. C. (2006) · Cell · doi:10.1016/j.cell.2006.08.030 · Cited by 474
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Basile, G. D. S., Ménasché, G., & Fischer, A. (2010) · Nature reviews. Immunology · doi:10.1038/nri2803 · Cited by 469
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Branco, T., & Staras, K. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2634 · Cited by 467
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Wu, L., Hamid, E., Shin, W., & Chiang, H. (2013) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021113-170305 · Cited by 462
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Chen, X., Tomchick, D. R., Kovrigin, E., Araç, D., Machius, M., Südhof, T. C., & Rizo, J. (2002) · Neuron · doi:10.1016/s0896-6273(02)00583-4 · Cited by 455
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Antonucci, F., Rossi, C., Gianfranceschi, L., Rossetto, O., & Caleo, M. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0375-08.2008 · Cited by 454
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Harris, K. M., & Weinberg, R. J. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005587 · Cited by 452
Wickner, W. T., & Schekman, R. W. (2008) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1451 · Cited by 449
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Shibasaki, T., Takahashi, H., Miki, T., Sunaga, Y., Matsumura, K., Yamanaka, M., Zhang, C., Tamamoto, A., Satoh, T., Miyazaki, J.-I., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707054104 · Cited by 425
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Pobbati, A. V., Stein, A., & Fasshauer, D. (2006) · Science · doi:10.1126/science.1129486 · Cited by 397
Yu, C., Power, J., Barnea, G., O'Donnell, S., Brown, H. E. V., Osborne, J., Axel, R., & Gogos, J. A. (2004) · Neuron · doi:10.1016/s0896-6273(04)00224-7 · Cited by 397
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Bridi, J. C., & Hirth, F. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00080 · Cited by 396
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Rizo, J., & Südhof, T. C. (2012) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-101011-155818 · Cited by 394
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Larance, M., Ramm, G., Stöckli, J., van Dam, E. M., Winata, S. C., Wasinger, V. C., Simpson, F., Graham, M. W., Junutula, J. R., Guilhaus, M., et al. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m503897200 · Cited by 392
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Zhang, Q., Li, Y., & Tsien, R. W. (2009) · Science · doi:10.1126/science.1167373 · Cited by 379
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Ma, C., Li, W., Xu, Y., & Rizo, J. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2047 · Cited by 363
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Han, Y., Kaeser, P. S., Südhof, T. C., & Schneggenburger, R. (2011) · Neuron · doi:10.1016/j.neuron.2010.12.014 · Cited by 354
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Schoch, S., & Gundelfinger, E. D. (2006) · Cell and Tissue Research · doi:10.1007/s00441-006-0244-y · Cited by 346
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van Spronsen, M., & Hoogenraad, C. C. (2010) · Current Neurology and Neuroscience Reports · doi:10.1007/s11910-010-0104-8 · Cited by 345
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Shin, N., Jeong, H., Kwon, J., Heo, H. Y., Kwon, J. J., Yun, H. J., Kim, C.-H., Han, B., Tong, Y., Shen, J., et al. (2008) · Experimental Cell Research · doi:10.1016/j.yexcr.2008.02.015 · Cited by 345
Presynaptic calcium and control of vesicle fusion
Schneggenburger, R., & Neher, E. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.05.006 · Cited by 344
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Pankratov, Y. V., Lalo, U., Verkhratsky, A., & North, R. A. (2006) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-006-0061-x · Cited by 340
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Siksou, L., Rostaing, P., Lechaire, J., Boudier, T., Ohtsuka, T., Fejtová, A., Kao, H., Greengard, P., Gundelfinger, E. D., Triller, A., et al. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1773-07.2007 · Cited by 340
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Xu, J., Mashimo, T., & Südhof, T. C. (2007) · Neuron · doi:10.1016/j.neuron.2007.05.004 · Cited by 336
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Christoffel, D. J., Golden, S. A., & Russo, S. J. (2011) · Reviews in the Neurosciences · doi:10.1515/rns.2011.044 · Cited by 334
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Vargas, K. J., Makani, S., Davis, T., Westphal, C. H., Castillo, P. E., & Chandra, S. S. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4787-13.2014 · Cited by 324
Proteomic Analysis of in Vivo Phosphorylated Synaptic Proteins
Collins, M. O., Yu, L., Coba, M. P., Husi, H., Campuzano, I., Blackstock, W. P., Choudhary, J. S., & Grant, S. G. N. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m411220200 · Cited by 320
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Su, S. C., & Tsai, L. (2011) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-092910-154023 · Cited by 318
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DeFazio, R. A., Dvoryanchikov, G. A., Maruyama, Y., Kim, J. W., Pereira, E., Roper, S. D., & Chaudhari, N. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0515-06.2006 · Cited by 316
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Choi, B.-K., Choi, M., Kim, J.-Y., Yang, Y., Lai, Y., Kweon, D., Lee, N. K., & Shin, Y. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1218424110 · Cited by 312
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Müller, C. S., Haupt, A., Bildl, W., Schindler, J., Knaus, H., Meissner, M., Rammner, B., Striessnig, J., Flockerzi, V., Fakler, B., et al. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1005940107 · Cited by 306
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Gerdes, H.-H., Bukoreshtliev, N. V., & Barroso, J. F. V. (2007) · FEBS Letters · doi:10.1016/j.febslet.2007.03.071 · Cited by 304
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Hiesinger, P. R., Fayyazuddin, A., Mehta, S., Rosenmund, T., Schulze, K. L., Zhai, R. G., Verstreken, P., Cao, Y., Zhou, Y., Kunz, J., et al. (2005) · Cell · doi:10.1016/j.cell.2005.03.012 · Cited by 302
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Telesford, Q. K., Simpson, S. L., Burdette, J. H., Hayasaka, S., & Laurienti, P. J. (2011) · Brain Connectivity · doi:10.1089/brain.2011.0055 · Cited by 299
Musazzi, L., Milanese, M., Farisello, P., Zappettini, S., Tardito, D., Barbiero, V. S., Bonifacino, T., Mallei, A., Baldelli, P., Racagni, G., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0008566 · Cited by 299
Brett, C. L., Tukaye, D. N., Mukherjee, S., & Rao, R. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-11-0999 · Cited by 297
Wheeler, D. G., Groth, R. D., Ma, H., Barrett, C. F., Owen, S. F., Safa, P., & Tsien, R. W. (2012) · Cell · doi:10.1016/j.cell.2012.03.041 · Cited by 296
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Gerber, S. H., Rah, J.-C., Min, S.-W., Liu, X., de Wit, H., Dulubova, I., Meyer, A. C., Rizo, J., Arancillo, M., Hammer, R. E., et al. (2008) · Science · doi:10.1126/science.1163174 · Cited by 294
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Sato, S., Omori, Y., Katoh, K., Kondo, M., Kanagawa, M., Miyata, K., Funabiki, K., Koyasu, T., Kajimura, N., Miyoshi, T., et al. (2008) · Nature Neuroscience · doi:10.1038/nn.2160 · Cited by 290
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Self-citationYap, K., Lim, Z. Q., Khandelia, P., Friedman, B., & Makeyev, E. V. (2012) · Genes & Development · doi:10.1101/gad.188037.112 · Cited by 286
Williams, O. W., Sharafkhaneh, A., Kim, V., Dickey, B. F., & Evans, C. M. (2006) · American Journal of Respiratory Cell and Molecular Biology · doi:10.1165/rcmb.2005-0436sf · Cited by 286
Analysis of synaptic transmission in Caenorhabditis elegans using an aldicarb-sensitivity assay
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Synaptic Vesicle Pools and Dynamics
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“Following presynaptic neuronal depolarization, calcium channels open, permitting the influx of calcium and triggering the fusion of vesicles with the membrane, resulting in the exocytosis of glutamate into the synapse [15].”
BackgroundLRRK2 Controls Synaptic Vesicle Storage and Mobilization within the Recycling Pool
Piccoli, G., Condliffe, S. B., Bauer, M., Giesert, F., Boldt, K., Astis, S. D., Meixner, A., Sarioglu, H., Weisenhorn, D. M. V., Wurst, W., et al. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3730-10.2011 · Cited by 282
SNARE Proteins: One to Fuse and Three to Keep the Nascent Fusion Pore Open
Shi, L., Shen, Q.-T., Kiel, A., Wang, J., Wang, H., Melia, T. J., Rothman, J. E., & Pincet, F. (2012) · Science · doi:10.1126/science.1214984 · Cited by 278
Structure and Function of the Hair Cell Ribbon Synapse
Nouvian, R., Beutner, D., Parsons, T. D., & Moser, T. (2006) · The Journal of Membrane Biology · doi:10.1007/s00232-005-0854-4 · Cited by 278
Metadata
- Authors
- Südhof, T. C.
- Affiliations
- Howard Hughes Medical Institute (US)
- Corresponding author
- Südhof, Thomas C.
- ORCID
- Südhof, Thomas C.
- Venue
- Annual Review of Neuroscience
- Publisher
- Annual Reviews
- Published
- 2004-07-21
- Volume
- 27
- Issue
- 1
- Pages
- 509-547
- ISSN
- 0147-006X (ISSN-L)
- 1545-4126
- OpenAlex
- W2154100802
- Semantic Scholar
- 8fb9e39827068555cd78a397fd6915cb9eb0d08a
- Cited by
- 2,491
- References
- 208
- Citations by year
- 2026: 48 · 2025: 50 · 2024: 59 · 2023: 67 · 2022: 68 · 2021: 72 · 2020: 77 · 2019: 86 · 2018: 68 · 2017: 97 · 2016: 88 · 2015: 115 · 2014: 113 · 2013: 137 · 2012: 150
- FWCI
- 8.50
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Annual Review of Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Keywords
- synaptic vesicle recycling, neurotransmitter release, exocytosis, endocytosis, vesicle recycling, calcium-triggered exocytosis, Munc18-1, SNARE proteins, synaptotagmin-1, Rab3, active zone, presynaptic terminals
- MeSH terms
- Animals, Central Nervous System, Exocytosis, Humans, Membrane Fusion, Nerve Tissue Proteins, Synaptic Transmission, Synaptic Vesicles, Presynaptic Terminals, Neurotransmitter Agents, Calcium Signaling
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