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 2,201–2,300 of 2,549
Kastning, K. (2005) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-648
Adaptive responses of central cholinergic systems in transgenic mice
Hartmann, J. (2006) · ThinkTech (Texas Tech University)
Regulation of Active Zone Ca2+ Channels
Leal, K., & Mochida, S. (2014) · Springer eBooks · doi:10.1007/978-4-431-55166-9_9
Cell-cycle-dependent trafficking in the endocytic pathway
Bergeland, T. (2008) · NORA - Norwegian Open Research Archives
Role of nogo - a in the intact central nervous system: an in vivo and in vitro approach.
Craveiro, L. M. (2011)
The Role of SAD-1 Kinase in Caenorhabditis elegans Neuronal Circuit Development and Function
Pekar, T. (2013) · TSpace (University of Toronto)
Dervola, K.-S. N. (2015) · NORA - Norwegian Open Research Archives
Effec ts of Heregulin on Muscle: A Biochemical and Histological Analysis
Scholar, D. (2014)
Regulación del uniportador de calcio mitocondrial por MICU1 y MICU2
Matesanz-Isabel, J. (2016) · UVaDOC UVaDOC University of Valladolid Documentary Repository (University of Valladolid) · doi:10.35376/10324/16758
HNRNP K: A NEW PROTEIN IN NEURON DEVELOPMENT AND FUNCTION
Folci, A. (2012) · Archivio Istituzionale della Ricerca (Universita Degli Studi Di Milano) · doi:10.13130/folci-alessandra-chiara_phd2012-03-02
CAUSES AND CONSEQUENCES OF REDUCED EXPRESSION OF SNAP-25 IN NEURONAL NETWORKS
Astis, S. D. (2013) · Archivio Istituzionale della Ricerca (Universita Degli Studi Di Milano) · doi:10.13130/de-astis-silvia_phd2013-01-16
Biochemical and functional characterization of RhoSAP: a RhoGAP of the postsynaptic density
Dahl, J. (2008) · OPen Access Repositorium der Universität Ulm (OPARU) (Ulm University) · doi:10.18725/oparu-1556
Shukla, A. (2016) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-5650
Highlight: Molecular Neurobiology
Thiel, G. (2010) · Biological Chemistry · doi:10.1515/bc.2010.071
Mechanisms of presynaptic CaV2.2 (N-type) modulation.
Chan, A. W. (2008) · TSpace (University of Toronto)
System: Mechanisms and Functions Neurotrophin-Mediated Rapid Signaling in the Central Nervous
Konnerth, A., Meuchel, L. W., Thompson, M. A., Cassivi, S. D., Pabelick, C. M., Vaz, S. H., Jørgensen, T. N., Cristóvão‐Ferreira, S., Duflot, S., Ribeiro, J. A., et al. (2012)
Fluorescent protein calcium sensor for monitoring synaptic transmission
Okorocha, A. E. (2016) · Leicester Research Archive (University of Leicester)
Photooxidation Microscopy: Bridging the Gap Between Fluorescence and Electron Microscopy
Denker, A., & Rizzoli, S. O. (2014) · Neuromethods · doi:10.1007/978-1-62703-983-3_13
Lipid Rafts in Pancreatic Beta- and Alpha-cell Stimulus-secretion Coupling
Xia, F. (2008) · TSpace (University of Toronto)
Ibáñez, T. V. O. (2014) · TDX (Tesis Doctorals en Xarxa)
Fernandes, A. C., Uytterhoeven, V., & Verstreken, P. (2012) · Neuromethods · doi:10.1007/978-1-61779-830-6_6
Presynaptic Terminal Differentiation
Zhen, M. (2007) · Elsevier eBooks · doi:10.1016/b978-012369437-9/50008-6
Saw, N. M. N. (2011) · TSpace (University of Toronto)
Rolling Blackout is required for both phototransduction and synaptic transmission in Drosophila
Huang, F.-D. (2006) · Europe PMC (PubMed Central)
Barth, J., & Volknandt, W. (2011) · Neuromethods · doi:10.1007/978-1-61779-111-6_9
The hair cell porosome: Molecular and synaptic implications
Drescher, D. G. (2014)
The enzymological characterization of the Inositol Phosphatase Synaptojanin
Knott, J. M. M. (2010) · doi:10.25560/5939
Quantitative synaptic vesicle imaging for evaluating neuron activities in neurodegenerative diseases
Fan, J., Xia, X., Dy, J., & Wong, S. T. C. (2011) · Asilomar Conference on Signals, Systems and Computers (ACSSC) · doi:10.1109/acssc.2011.6190033
CELLULAR MECHANISMS OF NEURODEGENERATION
Partanen, S. (2006)
A transcriptional program remodels GABAergic synapses in C. elegans
Petersen, S. C. (2011)
Beis, C. (2016) · Universitätsbibliothek der FU Berlin Hochschulschriftenstelle u. Dokumentenserver · doi:10.17169/refubium-14078
Role of secretory granule heterogeneity in calcium-triggered exocytosis
Rao, T. C. (2016) · Human Biology
Adenosine A2A Receptors and Peripheral Nociception.
Hussey, M. J. (2007) · Surrey Research Insight Open Access (The University of Surrey)
Galkin, M. A. (2016) · Biotechnologia Acta · doi:10.15407/biotech9.06.028
Prashad, R. C. (2012) · TSpace (University of Toronto)
Die Mobilität der synaptischen Vesikel
Kamin, D., & Rizzoli, S. O. (2009) · e-Neuroforum · doi:10.1515/nf-2009-0303
Phosphorylation of Synaptotagmin 4 captures transiting dense core vesicles at active synapses
Bharat, V. (2017) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-6173
Investigation of Protein - Protein Interactions in Clathrin-Mediated Membrane Transport
Jung, N. (2006) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-3235
Structure and Function Relationship of Syntaxin-1 in Neurotransmitter Release
Park, S. (2015) · TSpace (University of Toronto)
Mandad, S. (2017) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-6335
Fulopova, B. (2015) · UTAS Research Repository · doi:10.25959/23238728
Investigation of Endosomal Recycling of Synaptic Vesicles
Hoopmann, P. (2010) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-3146
TRAFFICKING OF ALPHA SECRETASE ADAM10: NEW INSIGHTS INTO THE MOLECULAR MECHANISM OF MODULATION
Saraceno, C. (2012) · Archivio Istituzionale della Ricerca (Universita Degli Studi Di Milano) · doi:10.13130/saraceno-claudia_phd2012-02-08
Study of synaptic vesicle cycling during exo- and endocytosis using optical approaches
Hua, Y. (2012) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-1466
A membrana e seus canais: um modelo computacional de neurônio.
Correale, T. G. (2017) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.3.2017.tde-28062017-095334
Analysis of Myosin VI in Drosophila melanogaster Synaptic Function and Development
Kisiel, M. (2014) · Library and Archives Canada (Government of Canada)
Groffen, A. J. A., Verhage, M., & Regazzi, R. (2006) · Digital Academic REpository of VU University Amsterdam (Vrije Universiteit Amsterdam)
Rett Syndrome Induced Pluripotent Stem Cell-derived Neurons Exhibit Electrophysiological Aberrations
Farra, N. (2012) · TSpace (University of Toronto)
Modeling the biophysical mechanisms of sound encoding at inner hair cell ribbon synapses
Chapochnikov, N. M. (2012) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-2898
The F-box Protein FSN-1 Governs Presynaptic Development in Caenorhabditis elegans
Watkins, N. A. (2011) · TSpace (University of Toronto)
Fernandez, N. A. (2010) · TSpace (University of Toronto)
Calcium Triggered Synaptic Vesicle Exocytosis
Pang, Z. P. (2007)
Investigation of membrane fusion as a function of lateral membrane tension
Kliesch, T.-T. (2017) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-6495
Pre- and Postsynaptic Assembly and Maturation
Sigrist, S. J., & Wichmann, C. (2013) · Elsevier eBooks · doi:10.1016/b978-0-12-397266-8.00008-9
An electrostatic and probabilistic simulation model to describe neurosecretion at the synaptic scale
Macias-Medri, A. E., Liendo, J. A., & Silva, R. J. (2017) · Network Computation in Neural Systems · doi:10.1080/0954898x.2017.1386806
2074v Alpha1-Beta1 and Alpha6-Beta1-Integrin
Etheridge, N., Ridge, J. P., Lewohl, J., & Dodd, P. R. (2008) · Springer eBooks · doi:10.1007/978-3-540-29678-2_5
Activity-dependent bulk endocytosis: control by molecules and signalling cascades
Nicholson-Fish, J. C. (2017) · ERA
GRh1-dependent unconventional protein secretion
Bruns, C. (2013) · LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas)
Studying Protein Organization in Cellular Membranes by High-Resolution Microscopy
Saka, S. K. (2014) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-4715
Charakterisierung des Targetingverhaltens präsynaptischer Proteine
Riemann, D. (2018) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-6846
Elucidating regulators and biomarkers of synaptic stability during neurodegeneration
Hurtado, M. L. (2018)
Kratzke, M. (2012) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-3298
Dynamic Control of Ca 2+ Binding in the C2 Domains of Synaptotagmin 1Preprint
Rock, P. J., Meyer, A. G., Evans, C. S., Chapman, E. R., & Sutton, R. B. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/412031
Resistive Pulse Study of Liposome Stability: Towards Precision and Efficient Drug Delivery
Lin, Y., Liu, X., & Arai, T. (2018) · IEEE/RSJ International Conference on Intelligent Robots and Systems (IROS) · doi:10.1109/iros.2018.8593731
Study of a kinesin adaptor in axonal transport and synapse formation
Dehaghi, T. K. (2019) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-7310
de Sousa, S. R. (2014) · The University of Queensland · doi:10.14264/uql.2018.652
Synaptotagmins ensure speed and efficiency of inhibitory neurotransmitter release
Chen, C. (2018) · Institute of Science and Technology Austria · doi:10.15479/at:ista:th_997
The serine/threonine kinase AKT switches between functional modes of the vesicle release machinery
Ge, L. (2014) · heiDOK (Heidelberg University) · doi:10.11588/heidok.00016511
Martín, A. R. (2019) · Docta Complutense (Universidad Complutense de Madrid)
Role of the NMDA receptor subunit, NR3A, in glutamatergic synapse development
Henson, M. A. (2010) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/s4z0-fd80
McKenzie, C. (2018) · Institute of Science and Technology Austria · doi:10.15479/at:ista:7132
The function of tomosyn in vesicle transport was simulated by the humanized yeast system
Shao, K., Gao, X., & NAKANISHI, H. (2019) · Scientia Sinica Vitae · doi:10.1360/n052018-00240
The endolysosomal system in neuronal physiology and pathology
Sanchez, S. V. (2019)
Bigler, R. L. (2017) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/89rt-7276
Tan, R. P. A. (2019) · UNSWorks (University of New South Wales, Sydney, Australia) · doi:10.26190/unsworks/3749
Evidence for Synaptic Vesicle Binding by the C-terminal of a Short Splice CaV2.1 Calcium Channel
Snidal, C. A. (2018) · TSpace (University of Toronto)
Single-molecule FRET investigation of SNARE-mediated exocytosis regulation
Yin, L. (2018) · Iowa State University Digital Repository (Iowa State University)
Mechanisms of synaptic plasticity mediated by Clathrin Adaptor-protein complexes 1 and 2 in mice
Mishra, R. (2019) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-7514
Development of Nanobodies to Image Synaptic Proteins in Super-Resolution Microscopy
Maidorn, M. (2018) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-7093
Parfentev, I. (2019) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-7615
Nitric Oxide and Synaptic Transmission in the Cerebellum
Collado‐Alsina, A., Rampérez, A., Sánchez‐Prieto, J., & Torres, M. (2019) · Springer eBooks · doi:10.1007/978-3-319-97911-3_112-1
The mechanisms of GABAergic signalling in the peripheral pain pathway
Ramli, R. B. (2019) · White Rose eTheses Online (University of Leeds, The University of Sheffield, University of York)
Neurosecretion: Hypothalamic Somata versus Neurohypophysial Terminals
Dayanithi, G., & Lémos, J. R. (2020) · Masterclass in neuroendocrinology · doi:10.1007/978-3-030-22989-4_2
Torres-Pacheco, L. H. L. (2013) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.9.2013.tde-17012014-115455
Bhumbra, G. S., Dyball, R. E. J., Ueta, Y., & Yamashita, H. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-803592-4.00059-6
Schubert, K. (2020) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-8026
Falconi‐Sobrinho, L. L. (2020) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.17.2020.tde-12022020-170935
Functional Analysis of the Motor Circuit of Juvenile Caenorhabditis elegans
Lu, Y. (2020) · TSpace (University of Toronto)
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
- 2,547
- References
- 208
- Citations by year
- 2026: 63 · 2025: 55 · 2024: 61 · 2023: 73 · 2022: 66 · 2021: 74 · 2020: 76 · 2019: 85 · 2018: 70 · 2017: 105 · 2016: 92 · 2015: 120 · 2014: 118 · 2013: 144 · 2012: 154
- FWCI
- 11.03
- 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