The DOI matches its Crossref record; 207 of the 208 references it cites were found in a registry or an index.
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.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Citations
Cites
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
Cited by
Sorted by citations
Items 601–700 of 2,549
Lambrecht, N. W. G., Yakubov, I., Zer, C., & Sachs, G. M. (2006) · Physiological Genomics · doi:10.1152/physiolgenomics.00271.2005 · Cited by 66
Fast neurotransmitter release regulated by the endocytic scaffold intersectin
Sakaba, T., Kononenko, N. L., Bacetic, J., Pechstein, A., Schmoranzer, J., Yao, L., Barth, H., Shupliakov, O., Kobler, O., Aktories, K., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1219234110 · Cited by 66
Annexins as Overlooked Regulators of Membrane Trafficking in Plant Cells
Konopka‐Postupolska, D., & Clark, G. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18040863 · Cited by 66
Lieberman, O. J., & Sulzer, D. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.12.028 · Cited by 66
Recycling endosomes in neuronal membrane traffic
Schmidt, M. R., & Haucke, V. (2007) · Biology of the Cell · doi:10.1042/bc20070007 · Cited by 65
Chou, A., Chen, C., Chen, S., Chen, W., Chen, Y.-L., Weng, Y.-S., & Wang, H. (2009) · Neurochemistry International · doi:10.1016/j.neuint.2009.11.003 · Cited by 65
Rozas, J. L., Gómez‐Sánchez, L., Mircheski, J., Linares‐Clemente, P., Nieto-González, J. L., Vázquez, M. E., Luján, R., & Fernández‐Chacón, R. (2012) · Neuron · doi:10.1016/j.neuron.2012.02.019 · Cited by 65
The Voltage-Gated Calcium Channel Functions as the Molecular Switch of Synaptic Transmission
Atlas, D. (2013) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-080411-121438 · Cited by 65
Compartmentalized cAMP signalling in regulated exocytic processes in non-neuronal cells
Szaszák, M., Frank, C., Rosenthal, W., & Klußmann, E. (2007) · Cellular Signalling · doi:10.1016/j.cellsig.2007.10.020 · Cited by 65
Liu, N. L., Dutton, R. J., & Pogliano, K. (2005) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.05004.x · Cited by 65
Schardt, A., Brinkmann, B. G., Mitkovski, M., Sereda, M. W., Werner, H. B., & Nave, K. (2009) · Journal of Neuroscience Research · doi:10.1002/jnr.22005 · Cited by 65
Brain high-throughput multi-omics data reveal molecular heterogeneity in Alzheimer’s disease
Eteleeb, A. M., Novotny, B. C., Tarraga, C. S., Sohn, C., Dhungel, E., Brase, L., Nallapu, A., Buss, J., Farias, F., Bergmann, K., et al. (2024) · PLOS Biology · doi:10.1371/journal.pbio.3002607 · Cited by 64
NMDA receptor-independent LTP in mammalian nervous system
Alkadhi, K. A. (2021) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2020.101986 · Cited by 64
Developmental alterations in the functional properties of excitatory neocortical synapses
Feldmeyer, D., & Radnikow, G. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.169458 · Cited by 64
Leftin, A., Job, C., Beyer, K., & Brown, M. F. (2013) · Journal of Molecular Biology · doi:10.1016/j.jmb.2013.04.002 · Cited by 64
The carboxy-terminal domain of complexin I stimulates liposome fusion
Malsam, J., Seiler, F., Schollmeier, Y., Rusu, P. M., Krause, J. M., & Söllner, T. H. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812813106 · Cited by 64
Weber, J. P., Toft‐Bertelsen, T. L., Mohrmann, R., Delgado-Martínez, I., & Sørensen, J. B. (2014) · PLoS ONE · doi:10.1371/journal.pone.0114033 · Cited by 64
Intersectin associates with synapsin and regulates its nanoscale localization and function
Gerth, F., Jäpel, M., Pechstein, A., Kochlamazashvili, G., Lehmann, M., Puchkov, D., Onofri, F., Benfenati, F., Nikonenko, A. G., Fredrich, K., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1715341114 · Cited by 64
Extracellular matrix remodeling through endocytosis and resurfacing of Tenascin-R
Dankovich, T. M., Kaushik, R., Olsthoorn, L. H. M., Petersen, G. C., Giro, P. E., Kluever, V., Agüi‐Gonzalez, P., Grewe, K., Bao, G., Beuermann, S., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-27462-7 · Cited by 64
Pirc, K., & Ulrih, N. P. (2015) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2015.06.021 · Cited by 64
Sun, H. Y., Lyons, S. A., & Dobrunz, L. E. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.093948 · Cited by 64
A role for V-ATPase subunits in synaptic vesicle fusion?
Far, O. E., & SEAGAR, M. J. (2011) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2011.07234.x · Cited by 63
Do different endocytic pathways make different synaptic vesicles?
Voglmaier, S. M., & Edwards, R. H. (2007) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2007.04.002 · Cited by 63
PIKfyve Negatively Regulates Exocytosis in Neurosecretory Cells
Osborne, S. L., Wen, P. J., Boucheron, C., Nguyen, H. N., Hayakawa, M., Kaizawa, H., Parker, P. J., Vitale, N., & Meunier, F. A. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m704856200 · Cited by 63
Srinivasan, G., Kim, J. H., & von Gersdorff, H. (2008) · Journal of Neurophysiology · doi:10.1152/jn.00949.2007 · Cited by 63
Bedu-Addo, K., Lefièvre, L., Moseley, F. L., Barratt, C. L. R., & Publicover, S. J. (2005) · Molecular Human Reproduction · doi:10.1093/molehr/gah226 · Cited by 63
Egashira, Y., Takase, M., Watanabe, S., Ishida, J., Fukamizu, A., Kaneko, R., Yanagawa, Y., & Takamori, S. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1604527113 · Cited by 63
NMR analysis of the closed conformation of syntaxin-1
Chen, X., Lu, J., Dulubova, I., & Rizo, J. (2008) · Journal of Biomolecular NMR · doi:10.1007/s10858-008-9239-1 · Cited by 63
Synaptic Vesicle Reuse and Its Implications
Kavalali, E. T. (2006) · The Neuroscientist · doi:10.1177/1073858405281852 · Cited by 63
Expansion Microscopy: Scalable and Convenient Super-Resolution Microscopy
Tillberg, P. W., & Chen, F. (2019) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100818-125320 · Cited by 62
Probing the Dynamics of Protein–Protein Interactions at Neuronal Contacts by Optical Imaging
Thoumine, O. R., Ewers, H., Heine, M., Groc, L., Frischknecht, R., Giannone, G., Poujol, C., Legros, P., Lounis, B., Cognet, L., et al. (2008) · Chemical Reviews · doi:10.1021/cr078204m · Cited by 62
Cholesterol, regulated exocytosis and the physiological fusion machine
Churchward, M. A., & Coorssen, J. R. (2009) · Biochemical Journal · doi:10.1042/bj20090969 · Cited by 62
Real‐time imaging of Rab3a and Rab5a reveals differential roles in presynaptic function
Star, E. N., Newton, A. J., & Murthy, V. N. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.092528 · Cited by 62
Large Structural Change in Isolated Synaptic Vesicles upon Loading with Neurotransmitter
Budzinski, K. L., Allen, R. W., Fujimoto, B. S., Kensel-Hammes, P., Belnap, D. M., Bajjalieh, S., & Chiu, D. T. (2009) · Biophysical Journal · doi:10.1016/j.bpj.2009.08.032 · Cited by 62
Ketamine regulates the presynaptic release machinery in the hippocampus
Müller, H. K., Wegener, G., Liebenberg, N., Zarate, C. A., Popoli, M., & Elfving, B. (2013) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2013.03.008 · Cited by 61
The readily-releasable pool dynamically regulates multivesicular release.
Vaden, J. H., Banumurthy, G., Gusarevich, E. S., Overstreet-Wadiche, L., & Wadiche, J. I. (2019) · eLife · doi:10.7554/elife.47434 · Cited by 61
Plastin 3 in health and disease: a matter of balance
Wolff, L., Strathmann, E. A., Müller, I., Mählich, D., Veltman, C., Niehoff, A., & Wirth, B. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03843-5 · Cited by 61
Lagow, R. D., Bao, H., Cohen, E. N., Daniels, R. W., Zuzek, A., Williams, W. H., Macleod, G. T., Sutton, R. B., & Zhang, B. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050072 · Cited by 61
Stimulation inhibits the mobility of recycling peptidergic vesicles in astrocytes
Potokar, M., Stenovec, M., Kreft, M., Kreft, M. E., & Zorec, R. (2007) · Glia · doi:10.1002/glia.20597 · Cited by 61
Elfving, B., Bonefeld, B. E., Rosenberg, R., & Wegener, G. (2008) · Synapse · doi:10.1002/syn.20538 · Cited by 61
Ermolyuk, Y. S., Alder, F. G., Henneberger, C., Rusakov, D. A., Kullmann, D. M., & Volynski, K. E. (2012) · PLoS Biology · doi:10.1371/journal.pbio.1001396 · Cited by 61
SV2A and SV2C are not vesicular Ca2+ transporters but control glucose-evoked granule recruitment
Iezzi, M., Theander, S. S., Janz, R., Loze, C., & Wollheim, C. B. (2005) · Journal of Cell Science · doi:10.1242/jcs.02658 · Cited by 61
Miller, B., & Борисович, Б. И. (2010) · Future Neurology · doi:10.2217/fnl.10.41 · Cited by 61
Wittig, S., Ganzella, M., Barth, M., Kostmann, S., Riedel, D., Pérez-Lara, Á., Jahn, R., & Schmidt, C. (2021) · Nature Communications · doi:10.1038/s41467-021-21102-w · Cited by 60
Lima, R. D. F., Prado, V. F., Prado, M. A. M., & Kushmerick, C. (2010) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2010.06657.x · Cited by 60
Gao, Y., Bezchlibnyk, Y. B., Sun, X., Wang, J., McEwen, B. S., & Young, L. T. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.04.066 · Cited by 60
Xian, X., Liu, T., Yu, J. H., Wang, Y., Miao, Y., Zhang, J., Yu, Y., Ross, C. J., Karasinska, J. M., Hayden, M. R., et al. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0297-09.2009 · Cited by 60
Djordjevic, A. D., Djordjevic, J., Elaković, I., Adžić, M., Matić, G. M., & Radojcic, M. B. (2011) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2011.10.006 · Cited by 60
Ohira, K., Kobayashi, K., Toyama, K., Nakamura, H. K., Shoji, H., Takao, K., Takeuchi, R., Yamaguchi, S., Kataoka, M., Otsuka, S., et al. (2013) · Molecular Brain · doi:10.1186/1756-6606-6-12 · Cited by 60
DGKι regulates presynaptic release during mGluR‐dependent LTD
Yang, J., Seo, J., Nair, R., Han, S., Jang, S., Kim, K., Han, K., Paik, S. K., Choi, J., Lee, S., et al. (2010) · The EMBO Journal · doi:10.1038/emboj.2010.286 · Cited by 60
Yang, X., Ouyang, Y., Kennedy, B. R., & Rothman, S. M. (2005) · The Journal of Physiology · doi:10.1113/jphysiol.2005.088948 · Cited by 60
Rab18 Inhibits Secretory Activity in Neuroendocrine Cells by Interacting with Secretory Granules
Vázquez‐Martínez, R., Cruz-García, D., Durán‐Prado, M., Peinado, J. R., Castano, J. P., & Malagón, M. M. (2007) · Traffic · doi:10.1111/j.1600-0854.2007.00570.x · Cited by 60
Extracellular vesicles as an emerging tool for the early detection of Alzheimer’s disease
Li, T.-R., Wang, X.-N., Sheng, C., Li, Y.-X., Li, F. Z.-T., Sun, Y., & Han, Y. (2019) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2019.111175 · Cited by 60
Synuclein Regulates Synaptic Vesicle Clustering and Docking at a Vertebrate Synapse
Fouke, K. E., Wegman, M. E., Weber, S. A., Brady, E. B., Román‐Vendrell, C., & Morgan, J. R. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.774650 · Cited by 59
Phosphatidic acid and neurotransmission
Raben, D. M., & Barber, C. N. (2016) · Advances in Biological Regulation · doi:10.1016/j.jbior.2016.09.004 · Cited by 59
Synapsin Utilization Differs among Functional Classes of Synapses on Thalamocortical Cells
Kielland, A., Erişir, A., Walaas, S. I., & Heggelund, P. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4631-05.2006 · Cited by 59
Silchenko, A. N., & Tass, P. A. (2007) · Biological Cybernetics · doi:10.1007/s00422-007-0196-7 · Cited by 59
The synaptic vesicle cluster: A source of endocytic proteins during neurotransmitter release
Shupliakov, O. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.03.035 · Cited by 59
High-resolution electron cryomicroscopy of V-ATPase in native synaptic vesicles
Coupland, C. E., Karimi, R., Bueler, S. A., Liang, Y., Courbon, G. M., Di Trani, J. M., Wong, C. J., Saghian, R., Youn, J.-Y., Wang, L.-Y., et al. (2024) · Science · doi:10.1126/science.adp5577 · Cited by 58
Serotonin2Creceptors in the nucleus accumbens are involved in enhanced alcohol‐drinking behavior
Yoshimoto, K., Watanabe, Y., Tanaka, M., & Kimura, M. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08037.x · Cited by 58
Deák, F., Liu, X., Khvotchev, M. V., Li, G., Kavalali, E. T., Sugita, S., & Südhof, T. C. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0898-09.2009 · Cited by 58
Self-citationWegrzyn, J., Bark, S. J., Funkelstein, L., Mosier, C., Yap, A., Kazemi‐Esfarjani, P., Spada, A. R. L., Sigurdson, C. J., O’Connor, D. T., & HOOK, V. Y. H. (2010) · Journal of Proteome Research · doi:10.1021/pr1003104 · Cited by 58
Herrick, D. Z., Kuo, W., Huang, H., Schwieters, C. D., Ellena, J. F., & Cafiso, D. S. (2009) · Journal of Molecular Biology · doi:10.1016/j.jmb.2009.06.007 · Cited by 58
Distinct Domains of Complexins Bind SNARE Complexes and Clamp Fusion in Vitro
Giraudo, C. G., Garcia-Diaz, A., Eng, W. S., Yamamoto, A., Melia, T. J., & Rothman, J. E. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m803478200 · Cited by 58
Yu, H., Rathore, S. S., Davis, E. M., Ouyang, Y., & Shen, J. (2013) · Molecular Biology of the Cell · doi:10.1091/mbc.e12-11-0810 · Cited by 58
DOC2B Acts as a Calcium Switch and Enhances Vesicle Fusion
Friedrich, R., Groffen, A. J. A., Connell, E., van Weering, J. R. T., Gutman, O., Henis, Y. I., Davletov, B. A., & Ashery, U. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0538-08.2008 · Cited by 58
Putative duality of presynaptic events
Borisova, Т., & Borysov, A. (2016) · Reviews in the Neurosciences · doi:10.1515/revneuro-2015-0044 · Cited by 58
Borisova, Т. (2015) · Reviews in the Neurosciences · doi:10.1515/revneuro-2015-0023 · Cited by 58
Dramatic effect of levetiracetam in early-onset epileptic encephalopathy due to STXBP1 mutation
Dilena, R., Striano, P., Traverso, M., Viri, M., Cristofori, G., Tadini, L., Barbieri, S., Romeo, A., & Zara, F. (2015) · Brain and Development · doi:10.1016/j.braindev.2015.07.002 · Cited by 58
Friends and foes in synaptic transmission: the role of tomosyn in vesicle priming
Ashery, U., Bielopolski, N., Barak, B., & Yizhar, O. (2009) · Trends in Neurosciences · doi:10.1016/j.tins.2009.01.004 · Cited by 58
Physiological Activity Depresses Synaptic Function through an Effect on Vesicle Priming
Moulder, K. L., Jiang, X., Taylor, A. A., Olney, J. W., & Mennerick, S. J. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.5498-05.2006 · Cited by 58
What is the function of neuronal AP‐3?
Danglot, L., & Galli, T. (2007) · Biology of the Cell · doi:10.1042/bc20070029 · Cited by 58
Impaired neurotransmission in ether lipid-deficient nerve terminals
Brodde, A., Teigler, A., Brugger, B., Lehmann, W. D., Wieland, F., Berger, J., & Just, W. W. (2012) · Human Molecular Genetics · doi:10.1093/hmg/dds097 · Cited by 57
NPF transporters in synaptic-like vesicles control delivery of iron and copper to seeds
Chao, Z., Wang, Y., Chen, Y., Zhang, C.-Y., Wang, P.-Y., Song, T., Liu, C., Lv, Q., Han, M., Wang, S., et al. (2021) · Science Advances · doi:10.1126/sciadv.abh2450 · Cited by 57
The Role of α-Synuclein in SNARE-mediated Synaptic Vesicle Fusion
Yoo, G., Shin, Y., & Lee, N. K. (2022) · Journal of Molecular Biology · doi:10.1016/j.jmb.2022.167775 · Cited by 57
Deficits in Syntaxin 1 Phosphorylation in Schizophrenia Prefrontal Cortex
Castillo, M. A., Ghose, S., Tamminga, C. A., & Ulery, P. G. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.07.029 · Cited by 57
Calcium signaling complexes in microdomains of polarized secretory cells
Kiselyov, K. I., Wang, X., Shin, D. M., Wj, Z., & Muallem, S. (2006) · Cell Calcium · doi:10.1016/j.ceca.2006.08.009 · Cited by 57
Analysis of synaptic vesicle endocytosis in synaptosomes by high-content screening
Daniel, J. A., Malladi, C. S., Kettle, E., McCluskey, A., & Robinson, P. J. (2012) · Nature Protocols · doi:10.1038/nprot.2012.070 · Cited by 57
Structure and evolution of RIM-BP genes: Identification of a novel family member
Mittelstaedt, T., & Schoch, S. (2007) · Gene · doi:10.1016/j.gene.2007.08.004 · Cited by 57
Two modes of lytic granule fusion during degranulation by natural killer cells
Liu, D., Martina, J. A., Wu, X., Hammer, J. A., & Long, E. O. (2011) · Immunology and Cell Biology · doi:10.1038/icb.2010.167 · Cited by 57
Pocklington, A. J., O’Donovan, M. C., & Owen, M. J. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12489 · Cited by 57
Stenovec, M., Lasič, E., Božić, M., Bobnar, S. T., Stout, R. F., Grubišić, V., Parpura, V., & Zorec, R. (2015) · Molecular Neurobiology · doi:10.1007/s12035-015-9562-y · Cited by 57
Halbgebauer, S., Oeckl, P., Wirth, K., Steinacker, P., & Otto, M. (2016) · Movement Disorders · doi:10.1002/mds.26635 · Cited by 57
Inositol pyrophosphates inhibit synaptotagmin-dependent exocytosis
Lee, T.-S., Lee, J.-Y., Kyung, J. W., Yang, Y., Park, S. J., Lee, S., Pavlovic, I., Kong, B., Jho, Y. S., Jessen, H. J., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1521600113 · Cited by 57
Trapping of Syntaxin1a in Presynaptic Nanoclusters by a Clinically Relevant General Anesthetic
Bademosi, A. T., Steeves, J. B., Karunanithi, S., Zalucki, O. H., Gormal, R. S., Liu, S., Lauwers, E., Verstreken, P., Anggono, V., Meunier, F. A., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2017.12.054 · Cited by 57
Hirano, A. A., Brandstätter, J. H., & Brecha, N. C. (2005) · The Journal of Comparative Neurology · doi:10.1002/cne.20577 · Cited by 57
Gibson, H. E., Reim, K., Brose, N., Morton, A. J., & Jones, S. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04349.x · Cited by 57
Synaptic Vesicle Distribution and Release at Rat Diaphragm Neuromuscular Junctions
Rowley, K. L., Mantilla, C. B., Ermilov, L. G., & Sieck, G. C. (2007) · Journal of Neurophysiology · doi:10.1152/jn.00251.2006 · Cited by 57
Ratnayaka, J. A., Marra, V., Bush, D., Burden, J. J., Branco, T., & Staras, K. (2012) · The Journal of Physiology · doi:10.1113/jphysiol.2011.226688 · Cited by 56
Guerrier, C., Hayes, J. A., Fortin, G., & Holcman, D. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1421997112 · Cited by 56
Long, A., Mahapatra, C. T., Woodruff, E. A., Rohrbough, J. C., Leung, H., Shino, S., An, L., Doerge, R. W., Metzstein, M. M., Pak, W. L., et al. (2010) · Journal of Cell Science · doi:10.1242/jcs.069468 · Cited by 56
Hamanaka, Y., & Meinertzhagen, I. A. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.22268 · Cited by 56
Polymorphism of the COMT, MAO, DAT, NET and 5-HTT Genes, and Biogenic Amines in Parkinson’s Disease
Dorszewska, J., Prendecki, M., Oczkowska, A., Różycka, A., Lianeri, M., & Kozubski, W. P. (2014) · Current Genomics · doi:10.2174/1389202914666131210210241 · Cited by 56
Calcium dependence of neurotransmitter release at a high fidelity synapse
Eshra, A., Schmidt, H., Eilers, J., & Hallermann, S. (2021) · eLife · doi:10.7554/elife.70408 · Cited by 56
Cytotoxic T lymphocyte exocytosis: bring on the SNAREs!
Hong, W. (2005) · Trends in Cell Biology · doi:10.1016/j.tcb.2005.10.003 · Cited by 56
Preliminary in vivo evidence of lower hippocampal synaptic density in cannabis use disorder
D’Souza, D. C., Radhakrishnan, R., Naganawa, M., Ganesh, S., Nabulsi, N., Najafzadeh, S., Ropchan, J., Ranganathan, M., Cortes-Briones, J., Huang, Y., et al. (2021) · Molecular Psychiatry · doi:10.1038/s41380-020-00891-4 · Cited by 55
Bademosi, A. T., Decet, M., Kuenen, S., Calatayud, C., Swerts, J., Gallego, S. F., Schoovaerts, N., Karamanou, S., Louros, N. N., Martin, E., et al. (2023) · Neuron · doi:10.1016/j.neuron.2023.02.001 · Cited by 55
Development of onabotulinumtoxinA for chronic migraine
Whitcup, S. M., Turkel, C. C., DeGryse, R. E., & Brin, M. F. (2014) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12488 · Cited by 55
Accumulation of α-Synuclein Triggered by Presynaptic Dysfunction
Nakata, Y., Yasuda, T., Fukaya, M., Yamamori, S., Itakura, M., Nihira, T., Hayakawa, H., Kawanami, A., Kataoka, M., Nagai, M., et al. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2220-12.2012 · Cited by 55
Kuo, W., Herrick, D. Z., & Cafiso, D. S. (2011) · Biochemistry · doi:10.1021/bi200049c · Cited by 55
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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review