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Clathrin regenerates synaptic vesicles from endosomes
Open accessAbstract
Ultrafast endocytosis can retrieve a single, large endocytic vesicle as fast as 50-100 ms after synaptic vesicle fusion. However, the fate of the large endocytic vesicles is not known. Here we demonstrate that these vesicles transition to a synaptic endosome about one second after stimulation. The endosome is resolved into coated vesicles after 3 s, which in turn become small-diameter synaptic vesicles 5-6 s after stimulation. We disrupted clathrin function using RNA interference (RNAi) and found that clathrin is not required for ultrafast endocytosis but is required to generate synaptic vesicles from the endosome. Ultrafast endocytosis fails when actin polymerization is disrupted, or when neurons are stimulated at room temperature instead of physiological temperature. In the absence of ultrafast endocytosis, synaptic vesicles are retrieved directly from the plasma membrane by clathrin-mediated endocytosis. These results may explain discrepancies among published experiments concerning the role of clathrin in synaptic vesicle endocytosis.
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“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 [7]
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“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 [7]
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“Based on the reliance of ultrafast endocytosis on F-actin7 and the high sensitivity of actin polymerization to temperature change74–76, we attribute this result to a slowed actin turnover at the room temperature7.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [7]
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“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 [7]
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“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 [7]
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“When ultrafast endocytosis is blocked, a slow clathrin-mediated endocytic pathway can kick in7 - this is consistent with observations from live-cell imaging of endocytosis68–70.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [7]
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“In our previous study, we demonstrated that ultrafast endocytosis fails when neurons are incubated at room temperature for 5 min prior to experiments – this failure is compensated by clathrin-mediated endocytosis7.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [7]
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“When ultrafast endocytosis is blocked, clathrin-mediated endocytosis takes its place7.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [7]
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BackgroundRetromer in Synaptic Function and Pathology
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BackgroundRamezani, M., Wilkes, M. M., Das, T., Holowka, D., Eliezer, D., & Baird, B. A. (2019) · npj Parkinson s Disease · doi:10.1038/s41531-019-0084-6 · Cited by 27
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BackgroundInfluentialSynaptopathy: presynaptic convergence in frontotemporal dementia and amyotrophic lateral sclerosis
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“67,73 This suggested that while CME initiates at the plasma membrane, it completes on either large UFE/ADBE invaginations or presynaptic endosomes.”
BackgroundHenkels, K. M., Miller, T. E., Ganesan, R., Wilkins, B. A., Fite, K., & Gómez-Cambronero, J. (2016) · Oncotarget · doi:10.18632/oncotarget.9685 · Cited by 25
“A recycling mechanism is also described in the postsynaptic termini of neurons after clathrin-medicated endocytosis, ultrafast endocytosis and endosomal budding close a cycle [47].”
BackgroundYu, S.-C., Jánosi, B., Liewald, J. F., Wabnig, S., & GOTTSCHALK, A. R. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00196 · Cited by 28
Metabolic regulation of single synaptic vesicle exo- and endocytosis in hippocampal synapses
Myeong, J., Stunault, M. I., Klyachko, V. A., & Ashrafi, G. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114218 · Cited by 25
“18,25,26 At present, it is not known to what extent glycolytic or mitochondrial ATP production powers single-AP-driven vesicle release and retrieval.”
Caputo, M., Gubar, O. S., Tóth, P., Vitale, N., Gasman, S., & Ory, S. (2025) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2025.110441 · Cited by 25
“CME plays a crucial role in replenishing the reserve vesicle pool (157) and in completing faster clathrin-independent mechanisms, which may be insufficient to fully retrieve all synaptic vesicle components remaining in the plasma membrane (158, 159).”
Nakakubo, Y., Abe, S., Yoshida, T., Takami, C., Isa, M., Wojcik, S. M., Brose, N., Takamori, S., & Hori, T. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108040 · Cited by 23
Local regulation of extracellular vesicle traffic by the synaptic endocytic machinery
Blanchette, C. R., Scalera, A. L., Harris, K. P., Zhao, Z., Dresselhaus, E. C., Koles, K., Yeh, A. R., Apiki, J. K., Stewart, B. A., & Rodal, A. A. (2022) · The Journal of Cell Biology · doi:10.1083/jcb.202112094 · Cited by 25
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“Dynamin can regulate actin function through direct and indirect interactions (65, 82), and actin is important for bulk (68– 70) and ultrafast endocytosis (72).”
BackgroundPresynaptic Kv3 channels are required for fast and slow endocytosis of synaptic vesicles
Wu, X., Subramanian, S., Zhang, Y., Shi, B., Xia, J., Li, T., Guo, X., El‐Hassar, L., Szigeti‐Buck, K., Henao‐Mejia, J., et al. (2021) · Neuron · doi:10.1016/j.neuron.2021.01.006 · Cited by 25
“F-actin is involved in mediating not only slow and rapid endocytosis, but also other forms of endocytosis, such as bulk endocytosis, endocytosis overshoot and ultrafast endocytosis at large calyx nerve terminals and small, conventional hippocampal boutons (Soykan et al., 2017; Watanabe et al., 2014; Wu et al., 2016).”
BackgroundBrill, S. E., Maraslioglu-Sperber, A., Kurz, C., Kramer, F., Fuhr, M. F., Singh, A., & Friauf, E. (2021) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2020.560008 · Cited by 23
Synaptotagmin-1 is a bidirectional Ca 2+ sensor for neuronal endocytosis
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“Recently, emerging evidence has shown that temperature is an important factor involved in exocytosis–endocytosis coupling, and clathrin may mediate endocytosis mainly at room temperature, whereas ultrafast endocytosis is dominant at physiological temperature (27, 42).”
BackgroundCheung, G. T. Y., & Cousin, M. A. (2019) · Journal of Neurochemistry · doi:10.1111/jnc.14862 · Cited by 23
“FM1-43-loaded SVs were then immediately depleted after dye loading by sequentially unloading the RRP (60 action potentials at 30 Hz) and then the reserve pool (three 400 action potential trains at 40 Hz).”
BackgroundInfluentialTertrais, M., Bouleau, Y., Emptoz, A., Belleudy, S., Sutton, R. B., Petit, C., Safieddine, S., & Dulon, D. (2019) · The Journal of Neuroscience · doi:10.1523/jneurosci.1550-18.2018 · Cited by 49
“Previous studies have revealed the existence of ultrafast endocytosis with a time constant of 50 ms in mouse hippocampal synapses (Watanabe et al., 2013b, 2014).”
BackgroundGFP nanobodies reveal recently-exocytosed pHluorin molecules
Seitz, K. J., & Rizzoli, S. O. (2019) · Scientific Reports · doi:10.1038/s41598-019-44262-8 · Cited by 22
Synaptic vesicles are “primed” for fast clathrin-mediated endocytosis at the ribbon synapse
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Adaptor protein-3 produces synaptic vesicles that release phasic dopamine
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“Clathrin and its heterotetrameric adaptor protein AP-2 regenerate SVs either directly from the plasma membrane (14) or immediately after an ultrafast form of endocytosis (15-17).”
Dynamin 1xA interacts with Endophilin A1 via its spliced long C-terminus for ultrafast endocytosis
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“We applied 10 action potentials at 20 Hz — this stimulation protocol also induces ultrafast endocytosis (Watanabe et al, 2014, 2018).”
Self-citationKiss-and-Run Is a Significant Contributor to Synaptic Exocytosis and Endocytosis in Photoreceptors
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“Impact of Endocytosis Inhibitors on Uptake of Large and Small Dyes Different modes of synaptic endocytosis depend differently on clathrin and dynamin in different cells (Artalejo et al., 1995; Granseth et al., 2006; Ferguson et al., 2007; Watanabe et al., 2014; Kononenko and Haucke, 2015).”
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“…the plasma membrane adaptor AP-2 is required for vesicle regeneration from bulk endosome-like organelles in central nerve terminals (Kononenko et al., 2014; Watanabe et al., 2014), but it is not known how long it takes for vesicles to bud from the endosome-like organelles after bulk endocytosis.”
BackgroundMolecular mechanics underlying flat-to-round membrane budding in live secretory cells
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“In addition, ultrafast endocytosis occurs within 50 –100 ms without forming clathrin coats at the site flanking the active zone in mouse hippocampal synapses, which is mediated by actin polymerization and dynamin to restore the surface area of the membrane rapidly (Watanabe et al., 2013, 2014).”
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Myosin light chain kinase facilitates endocytosis of synaptic vesicles at hippocampal boutons
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“2014) and the ultrafast clathrin-independent endocytosis in physiological temperature (Watanabe et al. 2014), but not endocytosis induced by action potentials of lower frequency (Sankaranarayanan et al.”
BackgroundHaase, J. K., Grudzinska‐Goebel, J., Müller, H. K., Münster‐Wandowski, A., Chow, E., Wynne, K. J., Farsi, Z., Zander, J.-F., & Ahnert‐Hilger, G. (2017) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.6b00437 · Cited by 19
Endosomal phosphatidylinositol 3-phosphate controls synaptic vesicle cycling and neurotransmission
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“…and quality control, and the exo-endocytic trafficking of postsynaptic receptors during synaptic plasticity (Park et al , 2004; Uytterhoeven et al , 2011; van der Sluijs & Hoogenraad, 2011; Saheki & De Camilli, 2012; Rizzoli, 2014; Watanabe et al , 2014; Wu et al , 2014; Chanaday et al , 2019).”
Prioritized docking of synaptic vesicles provided by a rapid recycling pathway
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“Re-acidification might be much slower than membrane retrieval, particularly during fast endocytosis, which may be mediated by bulk endocytosis and the formation of transient endosomes that then bud off synaptic vesicles (Figure 1; de Lange et al., 2003; Watanabe et al., 2014).”
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Clathrin-associated carriers enable recycling through a kiss-and-run mechanism
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“Subsequently, these ELVs are consumed by Clathrin-dependent SV reformation from the ELVmembrane (Watanabe et al., 2014).”
MethodCalcium-Independent Exo-endocytosis Coupling at Small Central Synapses
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“Clathrin, a triskelion vesicle coat protein, has long been proposed to be a fundamental component of the retrieval of SV components from the plasma membrane (Royle and Lagnado, 2010; Saheki and De Camilli, 2012); however, recent findings suggest that the reuptake pathway for SV material after evoked fusion is clathrin…”
BackgroundResultInfluentialSelf-citationBlumrich, E., Nicholson-Fish, J. C., Pronot, M., Davenport, E. C., Kurian, D., Cole, A. R., Smillie, K. J., & Cousin, M. A. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112633 · Cited by 16
SynapseNet: Deep learning for automatic synapse reconstruction
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“Neuronal monolayer cultures from newborn C57/BL6J mice were cultured on astrocyte-bearing sapphire disks as described previously by Watanabe et al. (2014).”
Park, J., Cho, O. Y., Kim, J. A., & Chang, S. (2016) · Scientific Reports · doi:10.1038/srep31807 · Cited by 16
PICK1 Controls Activity-Dependent Synaptic Vesicle Cargo Retrieval
Yong, X. L. H., Cousin, M. A., & Anggono, V. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.108312 · Cited by 16
Clathrin-mediated endocytosis cooperates with bulk endocytosis to generate vesicles
Arpino, G., Somasundaram, A., Shin, W., Ge, L., Villarreal, S. A., Chan, C. Y., Ashery, U., Shupliakov, O., Taraska, J. W., & Wu, L. (2022) · iScience · doi:10.1016/j.isci.2022.103809 · Cited by 16
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“…19, 2017 retrieval via endocytic intermediates upstream of clathrin-coat assembly (Clayton et al., 2008; Cheung et al., 2010; Kononenko et al., 2014; Watanabe et al., 2013, 2014), a decreased density of HRP+ SVs was observed only at the end of the stimulus in KIAA1107-KD terminals compared to…”
BackgroundGuzman, G. A., Guzman, R. E., Jordan, N., & Hidalgo, P. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00125 · Cited by 17
Li, H., Datunashvili, M., Reyes, R. C., & Voglmaier, S. M. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.926794 · Cited by 15
“Clathrin independent endocytosis may also use clathrin adaptors (Watanabe et al., 2014; Lopez-Hernandez et al., 2022).”
BackgroundKontaxi, C., Kim, N., & Cousin, M. A. (2023) · Journal of Neurochemistry · doi:10.1111/jnc.15848 · Cited by 15
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“Moreover, it can be maintained at low-frequency firing and maintain pre-synaptic homeostasis to a certain level when fast mechanisms of endocytosis are disturbed (Busch et al., 2014 ; Vargas et al., 2014; Xu et al., 2016 ) and CME prevails at room temperature (Watanabe et al., 2014 ).”
BackgroundSynapsin Is Required for Dense Core Vesicle Capture and cAMP-Dependent Neuropeptide Release
Yu, S.-C., Costa, W. S., Liewald, J. F., Shao, J., & GOTTSCHALK, A. R. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2631-20.2021 · Cited by 15
How do you recognize and reconstitute a synaptic vesicle after fusion?
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Monitoring activity-dependent bulk endocytosis with the genetically-encoded reporter VAMP4-pHluorin
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“These results are in accordance with previous studies, which suggest that clathrin-mediated endocytosis (CME) is displaced to endosomal intermediates at physiological temperatures (López-Hernández et al., 2022 ; Soykan et al., 2017; Watanabe et al., 2014 ).”
Endocytic proteins: An expanding repertoire of presynaptic functions
Tehran, D. A., & Maritzen, T. (2022) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2022.01.004 · Cited by 14
Imaging Endocytosis Dynamics in Health and Disease
Tagliatti, E., & Cortese, K. (2022) · Membranes · doi:10.3390/membranes12040393 · Cited by 15
“This process is clathrin-mediated [32].”
Xu, H., Osés-Prieto, J. A., Khvotchev, M. V., Jain, S., Liang, J., Burlingame, A. L., & Edwards, R. H. (2023) · Nature Neuroscience · doi:10.1038/s41593-023-01434-0 · Cited by 14
Clathrin mediates membrane fission and budding by constricting membrane pores
Wei, L., Guo, X., Haimov, E., Obashi, K., Lee, S. H., Shin, W., Sun, M., Chan, C. Y., Sheng, J., Zhang, Z., et al. (2024) · Cell Discovery · doi:10.1038/s41421-024-00677-w · Cited by 17
Wabnig, S., Liewald, J. F., Yu, S.-C., & GOTTSCHALK, A. R. (2015) · PLoS ONE · doi:10.1371/journal.pone.0135584 · Cited by 14
“In the terminal, SVs undergo a constant cycle: 1) After clathrin-mediated budding from endosomes [7], they are acidified and filled with transmitter by specific transporters using the proton gradient.”
BackgroundMolecular Signatures Underlying Synaptic Vesicle Cargo Retrieval
Mori, Y., & Takamori, S. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00422 · Cited by 15
“This mode of endocytosis was predominant when experiments were performed at physiological temperatures (∼35◦C) (Watanabe et al., 2014).”
BackgroundInfluentialAn optimized approach using cryofixation for high-resolution 3D analysis by FIB-SEM
Guo, J., Wang, G., Tang, W., Song, D., Wang, X., Hong, J., & Zhang, Z. (2020) · Journal of Structural Biology · doi:10.1016/j.jsb.2020.107600 · Cited by 14
Intersectin and endophilin condensates prime synaptic vesicles for release site replenishment
Ogunmowo, T. H., Hoffmann, C., Patel, C., Pepper, R., wang, H., Gowrisankaran, S., Idel, J., Ho, A. S., Raychaudhuri, S., Maher, B. J., et al. (2025) · Nature Neuroscience · doi:10.1038/s41593-025-02002-4 · Cited by 14
“EM image analysis was performed as previously described 4,5,7,21,36,57,78,79 .”
Self-citationHydrophobic Mismatch Controls the Mode of Membrane-Mediated Interactions of Transmembrane Peptides
Kondrashov, O. V., Kuzmin, P. I., & Akimov, S. A. (2022) · Membranes · doi:10.3390/membranes12010089 · Cited by 13
Mahapatra, S., & Lou, X. (2016) · The Journal of Physiology · doi:10.1113/jp271937 · Cited by 13
“It was reported that ultrafast endocytosis occurs only at physiological temperature but not at room temperature (Watanabe et al. 2014), while bulk endocytosis still operates robustly at room temperature (Hayashi et al.”
BackgroundInfluentialVesicular movements in the growth cone
Nozumi, M., & Igarashi, M. (2017) · Neurochemistry International · doi:10.1016/j.neuint.2017.09.011 · Cited by 13
Arriagada-Díaz, J., Prado‐Vega, L., Cárdenas, A. M., Ardiles, Á. O., & González‐Jamett, A. M. (2020) · The Neuroscientist · doi:10.1177/1073858420974313 · Cited by 12
Postsynaptic Neuroligin-1 Mediates Presynaptic Endocytosis During Neuronal Activity
Luo, J. K., Melland, H., Nithianantharajah, J., & Gordon, S. L. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.744845 · Cited by 13
“, 2017), which is essential for multiple vesicle retrieval pathways, including ultrafast and bulk endocytosis (Watanabe et al., 2014; Wu et al., 2016; Soykan et al., 2017).”
BackgroundCurrent gaps in basic science knowledge of botulinum neurotoxin biological actions
Rossetto, O., Pirazzini, M., & Montecucco, C. (2015) · Toxicon · doi:10.1016/j.toxicon.2015.07.002 · Cited by 13
Reversal of cell, circuit and seizure phenotypes in a mouse model of DNM1 epileptic encephalopathy
Bonnycastle, K., Dobson, K. L., Blumrich, E., Gajbhiye, A., Davenport, E. C., Pronot, M., Steinruecke, M., Trost, M., Gonzalez‐Sulser, A., & Cousin, M. A. (2023) · Nature Communications · doi:10.1038/s41467-023-41035-w · Cited by 12
“Recent studies have revealed that the majorityofintermediatesformeddirectlyfromthepresynapticplasma membrane are endosomes, which then shed SVs to re fi ll the recycling pool 19,20 .”
Cano, R., & Tabares, L. (2016) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2016.00012 · Cited by 12
Remodelling of membrane tubules by the actin cytoskeleton
Allard, A., Santos, R. L. D., & Campillo, C. C. (2021) · Biology of the Cell · doi:10.1111/boc.202000148 · Cited by 12
“Formins sit at the polymerising end of filaments and stimulate their parallel elongation forming structures in cells like filopodia or microvilli (Watanabe et al., 2014; Evangelista et al., 2003), among others.”
BackgroundYue, H., Bieberich, E., & Xu, J. (2017) · The Journal of Physiology · doi:10.1113/jp274275 · Cited by 12
“Previous studies have reported that activation of bulk endocytosis and ultrafast endocytosis underlies the acceleration of endocytosis under intense activity (Cheung & Cousin, 2013; Kokotos & Cousin, 2015) and elevated temperature (Watanabe et al. 2013, 2014), respectively.”
BackgroundResultInfluentialClayton, E. L., Bonnycastle, K., Isaacs, A. M., Cousin, M. A., & Schorge, S. (2021) · Journal of Neurochemistry · doi:10.1111/jnc.15551 · Cited by 12
Presynaptic Proteins and Their Roles in Visual Processing by the Retina
Thoreson, W. B., & Zenisek, D. (2024) · Annual Review of Vision Science · doi:10.1146/annurev-vision-101322-111204 · Cited by 12
“These endosomes later merge into larger endosomes, and while clathrin is not involved in the initial retrieval step, it contributes to regenerating synaptic vesicles from these large endosomes (Gan & Watanabe 2018, Watanabe et al. 2014).”
Biogenesis and reformation of synaptic vesicles
Bolz, S., & Haucke, V. (2024) · The Journal of Physiology · doi:10.1113/jp286554 · Cited by 12
“There is a general consensus that clathrin and clathrin-associated adaptors play a central role in SV reformation (Chanaday et al., 2019; Gan & Watanabe, 2018; Heerssen et al., 2008; Heuser & Reese, 1973; Kononenko et al., 2014; Maycox et al., 1992; Watanabe et al., 2014) (Fig.”
InfluentialDynamin 1 controls vesicle size and endocytosis at hippocampal synapses
Shi, B., Jin, Y., & Wu, L. (2022) · Cell Calcium · doi:10.1016/j.ceca.2022.102564 · Cited by 12
Temperature-dependent structural plasticity of hippocampal synapses
Feng, Z., Saha, L., Dritsa, C., Wan, Q., & Glebov, O. O. (2022) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2022.1009970 · Cited by 11
“Previous studies have utilized various experimental systems and employed widely disparate cooling regimes and time scales both in vitro and in vivo, ranging from 4 to 35C and minutes to days, respectively (Roelandse and Matus, 2004; Micheva and Smith, 2005; Kushmerick et al., 2006; Watanabe et al., 2014).”
BackgroundMethodAdvances in imaging ultrastructure yield new insights into presynaptic biology
Bruckner, J. J., Zhan, H., & O’Connor-Giles, K. M. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00196 · Cited by 12
“Recent work suggests that the terminal may be able to shift between slow and ultrafast endocytosis depending on the vesicular requirements as dictated by temperature or neuronal activity (Micheva and Smith, 2005; Granseth et al., 2006; Renden and von Gersdorff, 2007; Watanabe et al., 2014; Kononenko and Haucke, 2015).”
BackgroundMeasuring Synaptic Vesicle Endocytosis in Cultured Hippocampal Neurons
Villarreal, S. A., Lee, S. H., & Wu, L. (2017) · Journal of Visualized Experiments · doi:10.3791/55862 · Cited by 12
G protein-coupled receptor trafficking and signaling: new insights into the enteric nervous system
Carbone, S., Veldhuis, N. A., Gondin, A. B., & Poole, D. P. (2019) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00406.2018 · Cited by 11
“An additional limitation to the use of existing endocytosis inhibitors is their established effects on neurotransmitter release and uptake (53).”
BackgroundDiCello, J. J., Rajasekhar, P., Eriksson, E. M., Saito, A., Gondin, A. B., Veldhuis, N. A., Canals, M., Carbone, S., & Poole, D. P. (2019) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00085.2019 · Cited by 11
The readily retrievable pool of synaptic vesicles
Krishnan, S., & Klingauf, J. (2023) · Biological Chemistry · doi:10.1515/hsz-2022-0298 · Cited by 10
Current molecular approaches to investigate pre‐synaptic dysfunction
Harper, C. B., & Smillie, K. J. (2021) · Journal of Neurochemistry · doi:10.1111/jnc.15316 · Cited by 11
“The utility of these techniques is being pushed further still with the combination of super- resolution imaging techniques and EM, allowing the determination of the location of individual protein molecules in a cellular context (Clarke & Royle, 2018; Shu et al. 2011; Watanabe et al. 2014).”
MethodZhang, L., Wang, Y., Dong, Y., Pant, A., Liu, Y., Masserman, L., Xu, Y., McLaughlin, R. N., & Bai, J. (2022) · Developmental Cell · doi:10.1016/j.devcel.2022.02.021 · Cited by 12
Regulation of vesicular trafficking by Parkinson's disease-associated genes
Imai, Y., & Inoshita, T. (2015) · AIMS molecular science · doi:10.3934/molsci.2015.4.461 · Cited by 10
“Similarly, oligomers of αSynuclein induce SV clustering and decrease the motility of SVs in the synapses [29].”
BackgroundInfluentialRelease Mode Dynamically Regulates the RRP Refilling Mechanism at Individual Hippocampal Synapses
Kim, Y., Lee, U., Choi, C., & Chang, S. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.3029-19.2020 · Cited by 10
“Although the recently discovered ultrafast endocytosis occurs on a timescale of ;100ms, it requires actin polymerization and takes an additional 5-10 s to produce releasable vesicles (Watanabe et al., 2014); thus, it does not account for our results.”
ResultAP2 Regulates Thickveins Trafficking to Attenuate NMJ Growth Signaling in Drosophila
Choudhury, S. D., Dwivedi, M. K., Pippadpally, S., Patnaik, A., Mishra, S., Raghu, P., & Kumar, V. (2022) · eNeuro · doi:10.1523/eneuro.0044-22.2022 · Cited by 12
“However, the critical role of CME in generating vesicles from endosome-like structures following bulk membrane endocytosis cannot be ruled out (Watanabe et al., 2014).”
BackgroundInfluentialA nanoscale resolution view on synaptic vesicle dynamics
Maschi, D., & Klyachko, V. A. (2014) · Synapse · doi:10.1002/syn.21795 · Cited by 10
“…of the much lower density of the protein machinery in Synapse the plasma membrane required for fusion and by recent studies arguing against the role for clathrin in synaptic vesicle endocytosis from the plasma membrane in central synapses (Watanabe et al., 2013b, 2014; Kononenko et al., 2014).”
BackgroundA deep look at synaptic dynamics
Marx, V. (2014) · Nature · doi:10.1038/515293a · Cited by 10
Slow or fast? A tale of synaptic vesicle recycling
Watanabe, S. (2015) · Science · doi:10.1126/science.aad2996 · Cited by 10
Self-citationEich, M., Dembla, E., Wahl, S., Dembla, M., Schwarz, K., & Schmitz, F. (2017) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2017.00230 · Cited by 10
“…in membrane fission at distinct endomembrane systems, e.g., the Golgi apparatus and endosomes (Cao et al., 1998; Jones et al., 1998; McNiven et al., 2000; Praefcke and McMahon, 2004; Schulze et al., 2013; Kononenko et al., 2014; Watanabe et al., 2014; Arlt et al., 2015; Soykan et al., 2016).”
BackgroundSmall molecules targeting endocytic uptake and recycling pathways
Placidi, G., Mattu, C., Ciardelli, G., & Campa, C. C. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1125801 · Cited by 12
“, basket, disk-shaped or tetramers, respectively), thus helping the budding of vesicles from donor membranes (Van Jaarsveld et al., 1981; Chaudhary et al., 2014; Kononenko et al., 2014; Watanabe et al., 2014; Shvets et al., 2015; Han et al., 2020; Porta et al., 2022; Singh et al., 2022).”
BackgroundSNARE Proteins in Synaptic Vesicle Fusion
Palfreyman, M. T., West, S. E., & Jørgensen, E. M. (2023) · Advances in neurobiology · doi:10.1007/978-3-031-34229-5_4 · Cited by 10
The molecular infrastructure of glutamatergic synapses in the mammalian forebrainPreprint
Peukes, J., Lovatt, C., Leistner, C., Boulanger, J., Morado, D. R., Fuller, M. J., Kukulski, W., Zhu, F., Komiyama, N. H., Briggs, J. A. G., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.02.19.432002 · Cited by 8
Synaptotagmin-11 Inhibits Synaptic Vesicle Endocytosis via Endophilin A1
Wang, Y., Zhu, Y., Li, W., Yan, S., Li, C., Ma, K., Hu, M., Du, C., Fu, L., Sun, J., et al. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.1348-21.2023 · Cited by 8
Miki, T., Okamoto, Y., Ueno-Umegai, M., Toyofuku, R., Hattori, S., & Sakaba, T. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2402152121 · Cited by 8
Dagar, S., Teng, Z., & Gottmann, K. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.713693 · Cited by 8
Rho GTPase signaling and mDia facilitate endocytosis via presynaptic actin
Oevel, K., Hohensee, S., Kumar, A., Rosas-Brugada, I., Bartolini, F., Soykan, T., & Haucke, V. (2023) · eLife · doi:10.7554/elife.92755 · Cited by 12
Montenegro, M., Bayonés, L., Moya‐Díaz, J., Borassi, C., Toscani, A. M., Gallo, L. I., & Marengo, F. D. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.15276 · Cited by 7
Metadata
- Authors
- Watanabe, S., Trimbuch, T., Camacho-Pérez, M., Rost, B. R., Brokowski, B., Söhl-Kielczynski, B., Felies, A., Davis, M. W., Rosenmund, C., & Jorgensen, E. M.
- Affiliations
- Howard Hughes Medical Institute (US)
- Charité – Universitätsmedizin Berlin (DE)
- German Center for Neurodegenerative Diseases (DE)
- Corresponding author
- Rosenmund, Christian
- Venue
- Nature
- Published
- 2014-10-08
- Volume
- 515
- Issue
- 7526
- Pages
- 228-233
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC4291189
- OpenAlex
- W2029980283
- Cited by
- 333
- References
- 49
- Citations by year
- 2026: 17 · 2025: 30 · 2024: 29 · 2023: 26 · 2022: 33 · 2021: 26 · 2020: 32 · 2019: 29 · 2018: 20 · 2017: 33 · 2016: 22 · 2015: 29 · 2014: 7
- FWCI
- 15.12
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- 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
- clathrin, synaptic vesicle recycling, coated vesicles, clathrin-mediated endocytosis, actin polymerization, temperature dependence, optogenetic stimulation, high-pressure freezing, axon terminals, synaptic vesicle fusion
- MeSH terms
- Animals, Cell Membrane, Clathrin, Endocytosis, Humans, Endosomes, Synaptic Vesicles, Temperature, Mice
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