Cited by 2,549Cellular transport and secretionNeuroscience and Neuropharmacology ResearchExtracellular vesicles in disease

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THE SYNAPTIC VESICLE CYCLE

Südhof, Thomas C.·2004·Annual Review of Neuroscience

DOI 10.1146/annurev.neuro.26.041002.131412

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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
EVIDENCE FOR RECYCLING OF SYNAPTIC VESICLE MEMBRANE DURING TRANSMITTER RELEASE AT THE FROG NEUROMUSCULAR JUNCTION
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-citation
Synaptotagmin 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-citation
Synaptic 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-citation
Membrane Fusion
Jahn, R., Lang, T., & Südhof, T. C. (2003) · Cell · doi:10.1016/s0092-8674(03)00112-0 · Cited by 1,364
Self-citation
Syntaxin: 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

Show all 208 references

Research works printed but not linked: 6

Akert K, 1971, Adv. Cytopharmacol., 1, 273
Cases-Langhoff C, 1996, Eur. J. Cell Biol., 69, 214
Fischer von Mollard G, 1994, Eur. J. Cell Biol., 65, 319
10.1016/s0896-6273(00)81046-6 · DOI
Meinrenken CJ, 2003, J. Physiol., 547, 665
10.1128/mcb.13.4.2061 · DOI

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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
DOI: 10.1146/annurev.neuro.26.041002.131412
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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