The DOI matches its Crossref record; 54 of the 54 references it cites were found in a registry or an index.
Ultrafast endocytosis at mouse hippocampal synapses
Open accessAbstract
To sustain neurotransmission, synaptic vesicles and their associated proteins must be recycled locally at synapses. Synaptic vesicles are thought to be regenerated approximately 20 s after fusion by the assembly of clathrin scaffolds or in approximately 1 s by the reversal of fusion pores via 'kiss-and-run' endocytosis. Here we use optogenetics to stimulate cultured hippocampal neurons with a single stimulus, rapidly freeze them after fixed intervals and examine the ultrastructure using electron microscopy--'flash-and-freeze' electron microscopy. Docked vesicles fuse and collapse into the membrane within 30 ms of the stimulus. Compensatory endocytosis occurs within 50 to 100 ms at sites flanking the active zone. Invagination is blocked by inhibition of actin polymerization, and scission is blocked by inhibiting dynamin. Because intact synaptic vesicles are not recovered, this form of recycling is not compatible with kiss-and-run endocytosis; moreover, it is 200-fold faster than clathrin-mediated endocytosis. It is likely that 'ultrafast endocytosis' is specialized to restore the surface area of the membrane rapidly.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Several recent studies suggest that synaptic vesicle endocytosis is mediated by clathrin-independent ultrafast endocytosis at mammalian central synapses and is tightly coupled to exocytosis in time and space5–9.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [5]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Thus, the actin ring surrounding the active zone is likely essential for ultrafast endocytosis5.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [5]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Indeed, ultrafast endocytosis initiates as fast as 20–50 ms after exocytosis and completes within 100 ms5–7.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [5]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“In this pathway, endocytic invaginations always form at the edge of the active zone5–7.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [5]
Experimental — accuracy not yet measuredThe source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Following exocytosis, synaptic vesicles are recovered through clathrin-mediated, ultrafast, bulk, or kiss-and-run endocytic pathways.”
From Molecular Physiology of the Neuronal Synapse (2026) · cites this paper as [32]
Experimental — accuracy not yet measured
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“Ultrafast endocytosis occurs rapidly, within 50–100 milliseconds following stimulation, capturing approximately four vesicles at the very edge of the active zone [32]. This mechanism is specialized for rapidly restoring the surface area of the presynaptic membrane and is kinetically distinct from both kiss-and-run and clathrin-mediated endocytosis [33].”
From Molecular Physiology of the Neuronal Synapse (2026) · cites this paper as [32]
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“Several recent studies suggest that synaptic vesicle endocytosis is mediated by clathrin-independent ultrafast endocytosis at mammalian central synapses and is tightly coupled to exocytosis in time and space5–9.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [5]
The cited source says what the claim attributes to it.
In the citing paper
“Consistent with our previous work5, treatment with DMSO (control) did not affect ultrafast endocytosis, while Latrunculin A treatment completely blocked it (Fig. 2c, d; more micrographs in Supplementary Fig. 4).”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [5]
The cited source says what the claim attributes to it.
In the citing paper
“Importantly, the timing and the location of endocytic pit formation quantitatively recapitulates endocytic events observed by ultrastructural analysis5,6.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [5]
The cited source says what the claim attributes to it.
In the citing paper
“Filamentous actin (F-actin) is essential for the initiation of ultrafast endocytosis5.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [5]
The cited source says what the claim attributes to it.
In the citing paper
“When neurons are treated with Latrunculin A, which sequesters monomeric actin (G-actin) and perturbs F-actin formation12,13, ultrafast endocytosis fails completely, with no induction of membrane pit formation5.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [5]
The cited source says what the claim attributes to it.
In the citing paper
“Interestingly, ultrafast endocytosis is compensatory - the membrane area of endocytic vesicles is roughly equal to the total surface area of synaptic vesicles exocytosed5,6”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [5]
The cited source says what the claim attributes to it.
In the citing paper
“Kiss-and-run is a rapid mechanism that involves a transient opening of a fusion pore, allowing for neurotransmitter release without full collapse of the SV into the plasma membrane [30]. The vesicle is then rapidly retrieved, often within approximately one second [31,32].”
From Molecular Physiology of the Neuronal Synapse (2026) · cites this paper as [32]
The cited source says what the claim attributes to it.
In the citing paper
“Key proteins involved include clathrin itself and dynamin, which mediates the scission of the budding vesicle from the plasma membrane [32].”
From Molecular Physiology of the Neuronal Synapse (2026) · cites this paper as [32]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Computer Visualization of Three-Dimensional Image Data Using IMOD
Kremer, J. R., Mastronarde, D. N., & McIntosh, J. R. (1996) · Journal of Structural Biology · doi:10.1006/jsbi.1996.0013 · Cited by 5,530
Molecular mechanism and physiological functions of clathrin-mediated endocytosis
McMahon, H. T., & Boucrot, E. (2011) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3151 · Cited by 2,223
Heuser, J. E., & Reese, T. S. (1973) · The Journal of Cell Biology · doi:10.1083/jcb.57.2.315 · Cited by 2,147
Germline Transmission and Tissue-Specific Expression of Transgenes Delivered by Lentiviral Vectors
Lois, C., Hong, E. J., Pease, S., Brown, E. J., & Baltimore, D. (2002) · Science · doi:10.1126/science.1067081 · Cited by 1,992
Dynasore, a Cell-Permeable Inhibitor of Dynamin
Macia, E., Ehrlich, M., Massol, R., Boucrot, E., Brunner, C., & Kirchhausen, T. (2006) · Developmental Cell · doi:10.1016/j.devcel.2006.04.002 · Cited by 1,958
TrakEM2 Software for Neural Circuit Reconstruction
Cardona, A., Saalfeld, S., Schindelin, J., Arganda‐Carreras, I., Preibisch, S., Longair, M., Tomančák, P., Hartenstein, V., & Douglas, R. J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0038011 · Cited by 1,009
Gunaydin, L. A., Yizhar, O., Berndt, A., Sohal, V. S., Deisseroth, K., & Hegemann, P. (2010) · Nature Neuroscience · doi:10.1038/nn.2495 · Cited by 757
Latrunculins: Novel Marine Toxins That Disrupt Microfilament Organization in Cultured Cells
Spector, I., Shochet, N. R., Kashman, Y., & Groweiss, A. (1983) · Science · doi:10.1126/science.6681676 · Cited by 750
Granseth, B., Odermatt, B., Royle, S. J., & Lagnado, L. (2006) · Neuron · doi:10.1016/j.neuron.2006.08.029 · Cited by 686
Varoqueaux, F., Sigler, A., Rhee, J.-S., Brose, N., Enk, C., Reim, K., & Rosenmund, C. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.122623799 · Cited by 619
Self-citation
Cited by
Sorted by citations
Items 601–607 of 607
Advances in electrochemical methods for exocytosis analysis
Chu, P., Pan, C., & Yu, P. (2026) · Journal of Electroanalytical Chemistry · doi:10.1016/j.jelechem.2026.120571
The characteristics of synaptic vesicle dynamics at hippocampal mossy fiber terminals
Miyano, R. (n.d.) · Institutional Repositories DataBase (IRDB) · doi:10.14988/0000029596
Strategies for time-resolved cryogenic electrontomography of transient cellular processes
Jakobi, A. J. (2026) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2026.103385
Caputo, M., Gubar, O. S., Tóth, P., Darracq, E., Chasserot‐Golaz, S., Ory, S., Gasman, S., & Vitale, N. (2026) · Advances in Biological Regulation · doi:10.1016/j.jbior.2026.101187
Etude du rôle de la protéine Alix dans l'endocytose
Mercier, V. (2015) · theses.fr (ABES) · doi:10.70675/a5a25dfbzdf73z493ezb82fzaa0aeaf7bc42
Étude du cycle des vésicules synaptiques en microscopie électronique sans fixateur
Horellou, S. (2014) · theses.fr (ABES) · doi:10.70675/6204cf75z644fz4f53za2a6z4e01e179daa8
Metadata
- Authors
- Watanabe, S., Rost, B. R., Camacho-Pérez, M., Davis, M. W., Söhl-Kielczynski, B., Rosenmund, C., & Jorgensen, E. M.
- Affiliations
- Howard Hughes Medical Institute (US)
- Charité – Universitätsmedizin Berlin (DE)
- Corresponding author
- Rosenmund, Christian
- Venue
- Nature
- Published
- 2013-12-04
- Volume
- 504
- Issue
- 7479
- Pages
- 242-247
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC3957339
- OpenAlex
- W2093450191
- Cited by
- 607
- References
- 54
- Citations by year
- 2026: 26 · 2025: 40 · 2024: 44 · 2023: 47 · 2022: 53 · 2021: 44 · 2020: 53 · 2019: 62 · 2018: 51 · 2017: 54 · 2016: 36 · 2015: 58 · 2014: 38 · 2013: 1
- FWCI
- 25.72
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- DZNE Pub (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institute of Neurological Disorders and Stroke (R37NS034307, NS034307, R01NS034307)
- 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, clathrin-mediated endocytosis, dynamin, actin polymerization, hippocampal synapses, neurotransmission, membrane internalization, active zone, optogenetic stimulation
- MeSH terms
- Actins, Action Potentials, Animals, Endocytosis, Exocytosis, Hippocampus, Membrane Fusion, Microscopy, Electron, Synaptic Transmission, Rhodopsin, Synapses, Synaptic Vesicles, Time Factors, Dynamins, Mice
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
