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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.”
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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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“Another key study (referred to in the final paragraph of the Pearse paper) was the work by John Heuser and Tom Reese implicating coated vesicles in the recycling of synaptic vesicle membrane (5), although the exact contribution of coated vesicles to this pathway remains hotly debated even up until the present day (6-9…”
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InfluentialBuilding endocytic pits without clathrin
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BackgroundSynaptic vesicles transiently dock to refill release sites
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Self-citationExosomes Mediate Epithelium–Mesenchyme Crosstalk in Organ Development
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“Indeed, this component is faster than the full time course of vesicle regeneration described for ultrafast endocytosis (3–10 s; Watanabe et al., 2014) and seemingly could only be attributed to kiss-and-run.”
BackgroundInfluentialSelf-citationMembrane-associated periodic skeleton is a signaling platform for RTK transactivation in neurons
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“Thus, it is a particularly interesting candidate to investigate in the context of ultrafast endocytosis, in which the steps of membrane endocytosis and clathrin-mediated vesicle formation are separated in both time and space (Watanabe et al., 2014).”
InfluentialSelf-citationSynaptic Vesicle Recycling Pathway Determines Neurotransmitter Content and Release Properties
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Self-citationActin Is Crucial for All Kinetically Distinguishable Forms of Endocytosis at Synapses
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Self-citationUnconventional endocytic mechanisms
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“…Park et al., 2018) diverting SV cargo via a slower endocytosis mode (Clayton, Sue, & Smillie, 2010; Smillie, Pawson, Perkins, Jackson, & Cousin, 2013) or disrupting the replenishment of specific SV pools (Cheung et al., 2010; Granseth & Lagnado, 2008; Junge et al., 2004; Watanabe et al., 2014).”
BackgroundInfluentialMultiple Roles of Actin in Exo- and Endocytosis
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VAMP4 Is an Essential Cargo Molecule for Activity-Dependent Bulk Endocytosis
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“These are ultrafast endocytosis (Watanabe et al., 2013, 2014), clathrin-mediated endocytosis (CME), which is prevalent during mild stimulation (Granseth et al., 2006), and activity-dependent bulk endocytosis (ADBE), which is only triggered during intense neuronal activity (Clayton et al., 2008;…”
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“Alternatively, if SVs lose their identity during multiple rounds of exo-/endocytosis (7, 8), specific mechanisms exist to orchestrate high-fidelity SV protein sorting, either directly at the plasma membrane via slow clathrin-mediated endocytosis (CME) or at endosome-like vacuoles generated by fast clathrin-independent…”
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“In Figures 2J and S4B traces exemplify APs and ChR2-mediated currents (IChR2).”
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“This cargo selection occurs regardless of the endocytosis mode via which SVs are formed and can occur at either the plasma membrane or presynaptic endosomes (Ivanova et al., 2021; Kononenko et al., 2014; Watanabe et al., 2014).”
BackgroundCoupling of exocytosis and endocytosis at the presynaptic active zone
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“Functional synaptic vesicles require recycling from the plasma membrane or endosomal structures, as revealed by in vitro studies in vertebrate and invertebrate models, and by the localization and composition of nerve terminal derived vesicles (Heuser and Reese, 1973; Maycox et al., 1992; Fa undez et al., 1998; Di Paol…”
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“The function of endosomal structures at the synaptic terminal is still elusive, but a role in both regeneration of SVs and SV protein sorting and renewal has been described (Hoopmann et al., 2010; Watanabe et al., 2014; Wucherpfennig et al., 2003; Uytterhoeven et al., 2011; Fernandes et al., 2014).”
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“The lack of clathrin dependence of SV endocytosis is particularly pertinent in experiments performed at physiological temperatures (Kononenko et al., 2014; Watanabe et al., 2014; Delvendahl et al., 2016).”
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“Moreover, persistent signaling from glutamate receptors at the plasma membrane results in excitotoxicity and eventual neuronal cell death (78,79), and CME is essential for the retrieval of synaptic vesicles after neurotransmitter release (80-83).”
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“Such endocytic sorting for SVs has been suggested in recent high-pressure freeze experiments (27).”
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Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis
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“In our previous study, we demonstrated that ultrafast endocytosis fails when neurons are incubated at room temperature for 5min prior to experiments – this failure is compensated by clathrin-mediated endocytosis 7 .”
InfluentialSelf-citationYakoubi, R., Rollenhagen, A., von Lehe, M., Miller, D., Walkenfort, B., Hasenberg, M., Sätzler, K., & Lübke, J. H. R. (2019) · eLife · doi:10.7554/elife.48373 · Cited by 54
HIV-1 Nef hijacks clathrin coats by stabilizing AP-1:Arf1 polygons
Shen, Q.-T., Ren, X., Zhang, R., Lee, I., & Hurley, J. H. (2015) · Science · doi:10.1126/science.aac5137 · Cited by 50
“Clathrin coats can be generated on synaptic endosomes within a span of 2 s (38), a pathway that most likely involves the Arf1-activated AP-1 and/or AP-3 complexes.”
BackgroundBabu, L. P. A., Wang, H.-Y., Eguchi, K., Guillaud, L., & Takahashi, T. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1571-19.2019 · Cited by 43
Redlingshöfer, L., McLeod, F., Chen, Y., Camus, M., Burden, J., Palomer, E., Briant, K., Dannhauser, P. N., Salinas, P., & Brodsky, F. (2020) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.2003662117 · Cited by 40
“SV recycling can either be achieved by direct regeneration of SVs through clathrin-mediated endocytosis from the plasma membrane at low-frequency stimulus, or through clathrin-independent mechanisms, which predominantly mediate retrieval of SV components from the plasma membrane under high stimulus (2, 27, 28, 33, 52).”
BackgroundMethodInfluentialBouazza‐Arostegui, B., Camacho, M., Brockmann, M. M., Zobel, S., & Rosenmund, C. (2022) · Journal of Neuroscience · doi:10.1523/jneurosci.1945-21.2022 · Cited by 49
“A scramble RNA (scRNA) sequence served in both shRNA constructs as control (Watanabe et al., 2014).”
MethodSelf-citationRegulation of synaptic activity by snapin‐mediated endolysosomal transport and sorting
Giovanni, J. D., & Sheng, Z. (2015) · The EMBO Journal · doi:10.15252/embj.201591125 · Cited by 51
“Endosomes were confirmed as sorting intermediates for SV recycling (Hoopmann et al, 2010; Uytterhoeven et al, 2011; Watanabe et al, 2014), and SVs contain various endosomal proteins as a result (Takamori et al, 2006; Morgan et al, 2013).”
Time course and temperature dependence of synaptic vesicle endocytosis
Chanaday, N. L., & Kavalali, E. T. (2018) · FEBS Letters · doi:10.1002/1873-3468.13268 · Cited by 53
Kokotos, A. C., Peltier, J., Davenport, E. C., Trost, M., & Cousin, M. A. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1809189115 · Cited by 50
“UFE forms large vesicles from a subcellular region directly adjacent to the presynaptic active zone, with SVs shed from synaptic endosomes within 2 to 3 s (4, 5).”
BackgroundUncoupling endosomal CLC chloride/proton exchange causes severe neurodegeneration
Weinert, S., Gimber, N., Deuschel, D. A., Stuhlmann, T., Puchkov, D., Farsi, Z., Ludwig, C. F., Novarino, G., López‐Cayuqueo, K. I., Planells‐Cases, R., et al. (2020) · The EMBO Journal · doi:10.15252/embj.2019103358 · Cited by 47
“The expression of ClC-3 on endosomes, the presence of endosomal structures in synaptic boutons (Watanabe et al , 2014; Milosevic, 2018), and the presence of the endosomal marker rab4 and lysosomal cathepsin D in LP2 fractions (Fig EV4B) suggest that the abundance of ClC-3 on SVs might even be lower.”
SynBot is an open-source image analysis software for automated quantification of synapses
Savage, J. T., Ramirez, J. J., Risher, W. C., Wang, Y., Irala, D., & Eroğlu, Ç. (2024) · Cell Reports Methods · doi:10.1016/j.crmeth.2024.100861 · Cited by 53
From Nanoparticles to Cancer Nanomedicine: Old Problems with New Solutions
Chiang, C., Cheng, M., & Lin, C.-H. (2021) · Nanomaterials · doi:10.3390/nano11071727 · Cited by 49
“The nanoparticle with a larger size around 150 nm was up taken by clathrinmediated pathway, while smaller nanoparticles of about 50 nm by clathrin-independent endocytosis [29,30].”
BackgroundMembrane transformations of fusion and budding
Wu, L., & Chan, C. Y. (2024) · Nature Communications · doi:10.1038/s41467-023-44539-7 · Cited by 55
Dysfunction of Synaptic Vesicle Endocytosis in Parkinson’s Disease
Zou, L., Tian, Y., & Zhang, Z. (2021) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2021.619160 · Cited by 44
“be approximately divided into the following main steps (Südhof, 2004; Watanabe et al., 2014; Watanabe and Boucrot, 2017): (1) Neurotransmitters are pumped into the vesicles through the neurotransmitter transporter on the surface of the vesicles; (2) The vesicles are transported to the near-activated area of the presyn…”
BackgroundMcAdam, R. L., Morton, A., Gordon, S. L., Alterman, J. F., Khvorova, A., Cousin, M. A., & Smillie, K. J. (2019) · Neurobiology of Disease · doi:10.1016/j.nbd.2019.104637 · Cited by 46
Organization and dynamics of SNARE proteins in the presynaptic membrane
Milovanović, D., & Jahn, R. (2015) · Frontiers in Physiology · doi:10.3389/fphys.2015.00089 · Cited by 42
The structure and function of presynaptic endosomes
Jähne, S., Rizzoli, S. O., & Helm, M. S. (2015) · Experimental Cell Research · doi:10.1016/j.yexcr.2015.04.017 · Cited by 44
Lou, X. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00066 · Cited by 39
Hsc70 Ameliorates the Vesicle Recycling Defects Caused by Excess α-Synuclein at Synapses
Banks, S. M. L., Medeiros, A. T., McQuillan, M., Busch, D. J., Ibarraran-Viniegra, A. S., Roy, S., Sousa, R., Lafer, E. M., & Morgan, J. R. (2020) · eNeuro · doi:10.1523/eneuro.0448-19.2020 · Cited by 41
“, 2018), and because clathrin-mediated vesicle budding is also critical for other modes of SV recycling such as ultrafast and bulk endocytosis (Watanabe et al., 2014; Gan and Watanabe, 2018; Chanaday et al., 2019), we set out to determine in this study exactly how excess -synuclein impacts clathrinNew Research 4 of 18”
BackgroundMechanisms of neuronal survival safeguarded by endocytosis and autophagy
Overhoff, M., Bruyckere, E. D., & Kononenko, N. L. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.15194 · Cited by 40
“Interestingly, the depletion of Clathrin by lentiviral short hairpin RNA (Watanabe et al., 2014) or KO of AP-2(μ) in neurons (Kononenko et al., 2014) results in the reduction in properly shaped synaptic vesicles, whereas synaptic vesicle membrane retrieval is largely unaffected (Kononenko et al., 2014).”
BackgroundInfluentialDysfunction of Endocytic Kinase AAK1 in ALS
Shi, B., Conner, S. D., & Liu, J. (2014) · International Journal of Molecular Sciences · doi:10.3390/ijms151222918 · Cited by 41
“[31], which solidified the requirement of clathrin in regenerating synaptic vesicles, it is possible that AAK1 might play an important regulatory role in synaptic vesicle recycling.”
BackgroundSynaptotagmin 1-triggered lipid signaling facilitates coupling of exo- and endocytosis.
Bolz, S., Kaempf, N., Puchkov, D., Krauss, M., Russo, G., Soykan, T., Schmied, C., Lehmann, M., Müller, R., Schultz, C., et al. (2023) · Neuron · doi:10.1016/j.neuron.2023.08.016 · Cited by 31
Rollenhagen, A., Ohana, O., Sätzler, K., Hilgetag, C. C., Kuhl, D., & Lübke, J. H. R. (2018) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2018.00024 · Cited by 45
“Spatial Distribution of Synaptic Vesicles Within the L5B Excitatory Synaptic Boutons Another key determinant for synaptic efficacy, strength, Pr and plasticity is the size and organization of the pool of synaptic vesicles, in particular, that of the RRP and the RP (Schikorski and Stevens, 2001; Denker et al., 2009; De…”
BackgroundVentimiglia, D., & Bargmann, C. I. (2017) · eLife · doi:10.7554/elife.31234 · Cited by 39
Synaptic Vesicle Generation from Central Nerve Terminal Endosomes
Kokotos, A. C., & Cousin, M. A. (2014) · Traffic · doi:10.1111/tra.12235 · Cited by 40
“This is not an issue for ultrafast endocytosis however, as uptake of cationized ferritin into ultrafast endosomes occurs after 1 second with its donation to SVs within 3 seconds (32).”
InfluentialIntegration of Synaptic Vesicle Cargo Retrieval with Endocytosis at Central Nerve Terminals
Cousin, M. A. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00234 · Cited by 38
“An obligatory requirement for clathrin during endocytosis from the plasma membrane has recently been questioned (Kononenko et al., 2014; Watanabe et al., 2014; Soykan et al., 2017).”
BackgroundInfluentialLight-coupled cryo-plunger for time-resolved cryo-EM
Yoder, N., Jalali‐Yazdi, F., Noreng, S., Houser, A. M., Baconguis, I., & Gouaux, E. (2020) · Journal of Structural Biology · doi:10.1016/j.jsb.2020.107624 · Cited by 40
“Furthermore, leveraging photolabile compounds has been instrumental in the study of many biological systems and has met with particular success in the field of neuroscience research (Callaway and Yuste, 2002; Eder et al., 2004; Korkotian et al., 2004; Watanabe et al., 2013; Watanabe et al., 2014).”
BackgroundClathrin packets move in slow axonal transport and deliver functional payloads to synapses
Ganguly, A., Sharma, R. V., Boyer, N. P., Wernert, F., Phan, S., Boassa, D., Parra‐Rivas, L. A., Das, U., Caillol, G., Han, X., et al. (2021) · Neuron · doi:10.1016/j.neuron.2021.08.016 · Cited by 39
López-Hernández, T., Takenaka, K.-I., Mori, Y., Kongpracha, P., Nagamori, S., Haucke, V., & Takamori, S. (2021) · eLife · doi:10.7554/elife.71198 · Cited by 38
Grünewald, B., Lange, M. D., Werner, C. D., O’Leary, A., Weishaupt, A., Popp, S., Pearce, D. A., Wiendl, H., Reif, A., Pape, H., et al. (2017) · eLife · doi:10.7554/elife.28685 · Cited by 38
“(Luiro et al., 2004; Lojewski et al., 2014; Watanabe et al., 2014; Lou et al., 2012).”
Choudhury, S. D., Mushtaq, Z., Reddy‐Alla, S., Balakrishnan, S. S., Thakur, R. S., Krishnan, K. S., Raghu, P., Ramaswami, M., & Kumar, V. (2016) · Genetics · doi:10.1534/genetics.115.183863 · Cited by 36
“…during CME at the synapses and hence is believed to be essential for SV retrieval and regeneration of SVs for subsequent rounds of neurotransmitter release (Gonzalez-Gaitan and Jackle 1997; Collins et al. 2002; Heerssen et al. 2008; Cheung et al. 2010; Gu et al. 2013; Watanabe et al. 2014).”
BackgroundNew Mendelian Disorders of Painlessness
Nahorski, M. S., Chen, Y., & Woods, C. G. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.08.010 · Cited by 37
The axonal endolysosomal and autophagic systems
Kuijpers, M., Tehran, D. A., Haucke, V., & Soykan, T. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.15287 · Cited by 38
“…from the plasma membrane have been postulated to undergo subsequent fusion to generate larger synaptic endosome-like structures from which SVs are subsequently reformed via clathrin/ AP-2 mediated budding (Cheung et al., 2010; Kononenko et al., 2014; Watanabe et al., 2014; Wu et al., 2014).”
BackgroundActin Cytoskeleton and Action Potentials: Forgotten Connections
Baluška, F., & Mancuso, S. (2019) · Plant cell monographs · doi:10.1007/978-3-030-33528-1_5 · Cited by 34
Role of actin in organelle trafficking in neurons
Venkatesh, K., Mathew, A., & Koushika, S. P. (2019) · Cytoskeleton · doi:10.1002/cm.21580 · Cited by 38
“Additionally, Clathrin-independent endocytosis at the synapse (Soykan et al., 2017; S. Watanabe et al., 2013; S. Watanabe et al., 2014) is mediated by Formin (mDia1) dependent actin polymerization (Soykan et al., 2017).”
BackgroundSynapsEM: Computer-Assisted Synapse Morphometry
Watanabe, S., Davis, M. W., Kusick, G. F., Iwasa, J., & Jorgensen, E. M. (2020) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2020.584549 · Cited by 34
Self-citationMembrane mechanics dictate axonal pearls-on-a-string morphology and function
Griswold, J. M., Bonilla-Quintana, M., Pepper, R., Lee, C. T., Raychaudhuri, S., Ma, S., Gan, Q., Syed, S., Zhu, C., Bell, M. K., et al. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01813-1 · Cited by 43
Self-citationMarkert, S. M., Skoruppa, M., Yu, B., Mulcahy, B., Zhen, M., Gao, S., Sendtner, M., & Stigloher, C. (2020) · Biology Open · doi:10.1242/bio.055129 · Cited by 34
“After endocytosis, vesicles are regenerated in a clathrin-dependent manner (Watanabe et al., 2014).”
BackgroundJung, J. H., Kirk, L. M., Bourne, J. N., & Harris, K. M. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2018653118 · Cited by 32
Multicolor Caged dSTORM Resolves the Ultrastructure of Synaptic Vesicles in the Brain
Lehmann, M., Gottschalk, B., Puchkov, D., Schmieder, P., Schwagerus, S., Hackenberger, C. P. R., Haucke, V., & Schmoranzer, J. (2015) · Angewandte Chemie International Edition · doi:10.1002/anie.201505138 · Cited by 33
Neuronal Signaling Involved in Neuronal Polarization and Growth: Lipid Rafts and Phosphorylation
Igarashi, M., Honda, A., Kawasaki, A., & Nozumi, M. (2020) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2020.00150 · Cited by 32
“…Tararuk et al., 2006), including neurogenesis (Amura et al., 2005; Xu et al., 2014; Lim et al., 2015), neuronal migration (Kawauchi et al., 2003; Westerlund et al., 2011; Myers et al., 2014, 2020; Kawauchi, 2015), polarization (Slater et al., 2013), and axon growth and guidance (Oliva et al.,…”
BackgroundUltrastructural and functional fate of recycled vesicles in hippocampal synapses
Rey, S. A., Smith, C. A., Fowler, M. W., Crawford, F., Burden, J. J., & Staras, K. (2015) · Nature Communications · doi:10.1038/ncomms9043 · Cited by 28
Watanabe, S. (2016) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2016.00024 · Cited by 30
Self-citationWinner, B. M., Bodt, S. M. L., & McNutt, P. M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21228715 · Cited by 29
“However, rec nt stu ies i i t t at clathrin lso mediates SV biogenesis from synaptic endosom under physiological conditions [38,39], including endosomes formed during ADBE and UFE [40].”
BackgroundInfluentialBrain‐specific functions of the endocytic machinery
Camblor‐Perujo, S., & Kononenko, N. L. (2021) · FEBS Journal · doi:10.1111/febs.15897 · Cited by 33
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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