The DOI matches its Crossref record; 157 of the 157 references it cites were found in a registry or an index.
Molecular Circuitry of Endocytosis at Nerve Terminals
Abstract
Presynaptic terminals are specialized compartments of neurons responsible for converting electrical signals into secreted chemicals. This self-renewing process of chemical synaptic transmission is accomplished by the calcium-triggered fusion of neurotransmitter-containing vesicles with the plasma membrane and subsequent retrieval and recycling of vesicle components. Whereas the release of neurotransmitters has been studied for over 50 years, the process of synaptic vesicle endocytosis has remained much more elusive. The advent of imaging techniques suited to monitor membrane retrieval at presynaptic terminals and the discovery of the molecules that orchestrate endocytosis have revolutionized our understanding of this critical trafficking event.
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“After exocytosis, vesicle membrane must be retrieved from the plasma membrane through endocytosis to keep the area of the plasma membrane constant and maintain a sufficient number of synaptic vesicles at presynapses1–4.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [3]
In the citing paper
“After exocytosis, vesicle membrane must be retrieved from the plasma membrane through endocytosis to keep the area of the plasma membrane constant and maintain a sufficient number of synaptic vesicles at presynapses1–4.”
From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [3]
Citations
Cites
Intermolecular and Surface Forces
Israelachvili, J. N. (2011) · Elsevier eBooks · doi:10.1016/c2009-0-21560-1 · Cited by 8,241
An Introduction to Systems Biology: Design Principles of Biological Circuits
Alon, U. (2006) · doi:10.1201/9781420011432 · Cited by 2,825
Südhof, T. C. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.26.041002.131412 · Cited by 2,547
Molecular anatomy of a trafficking organelle
Takamori, S., Holt, M., Stenius, K., Lemke, E. A., Grønborg, M., Riedel, D., Urlaub, H., Schenck, S., Brügger, B., Ringler, P., et al. (2006) · Cell · doi:10.1016/j.cell.2006.10.030 · Cited by 2,373
Water-Soluble Quantum Dots for Multiphoton Fluorescence Imaging in Vivo
Larson, D. R., Zipfel, W. R., Williams, R. M., Clark, S. W., Bruchez, M. P., Wise, F. W., & Webb, W. W. (2003) · Science · doi:10.1126/science.1083780 · Cited by 2,290
Quantal components of the end‐plate potential
del Castillo, J., & Katz, B. (1954) · The Journal of Physiology · doi:10.1113/jphysiol.1954.sp005129 · Cited by 2,201
Heuser, J. E., & Reese, T. S. (1973) · The Journal of Cell Biology · doi:10.1083/jcb.57.2.315 · Cited by 2,147
Curvature of clathrin-coated pits driven by epsin
Ford, M. G. J., Mills, I. G., Peter, B. J., Vallis, Y., Praefcke, G. J. K., Evans, P. R., & McMahon, H. T. (2002) · Nature · doi:10.1038/nature01020 · Cited by 1,019
A 38,000-dalton membrane protein (p38) present in synaptic vesicles.
Jahn, R., SCHIEBLER, W., Ouimet, C. C., & Greengard, P. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.12.4137 · Cited by 851
TURNOVER OF TRANSMITTER AND SYNAPTIC VESICLES AT THE FROG NEUROMUSCULAR JUNCTION
Ceccarelli, B., Hurlbut, W. P., & Mauro, A. (1973) · The Journal of Cell Biology · doi:10.1083/jcb.57.2.499 · Cited by 837
Research works printed but not linked: 1
- De Camilli P, 2001, Synapses, 217
Cited by
Sorted by citations
Dynamin, a membrane-remodelling GTPase
Ferguson, S. M., & Camilli, P. V. D. (2012) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3266 · Cited by 1,027
“However, endocytosis, and clathrin-mediated endocytosis in particular, also has a specialized role in nerve terminals, mediating the local recycling of synaptic vesicle membranes after exocytosi”
BackgroundActivity-driven local ATP synthesis is required for synaptic function
Rangaraju, V., Calloway, N., & Ryan, T. A. (2014) · Cell · doi:10.1016/j.cell.2013.12.042 · Cited by 836
“We treat one of the processes driven by calcium signals as the third category: exocytosis of synaptic vesicles and the ensuing synaptic vesicle cycle (Dittman and Ryan, 2009).”
Self-citationUltrafast endocytosis at mouse hippocampal synapses
Watanabe, S., Rost, B. R., Camacho-Pérez, M., Davis, M. W., Söhl-Kielczynski, B., Rosenmund, C., & Jorgensen, E. M. (2013) · Nature · doi:10.1038/nature12809 · Cited by 607
von Kleist, L., Stahlschmidt, W., Bulut, H., Gromova, K. V., Puchkov, D., Robertson, M. J., MacGregor, K. A., Tomilin, N. V., Pechstein, A., Chau, N., et al. (2011) · Cell · doi:10.1016/j.cell.2011.06.025 · Cited by 569
“Unlike CME in nonneuronal cells endocytic reformation of SVs in neurons is strictly coupled to stimulation-dependent exocytosis resulting in a wave of endocytic activity (Dittman and Ryan, 2009).”
InfluentialSaheki, Y., & De Camilli, P. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005645 · Cited by 457
“Some general principles apply to clathrinmediated endocytosis in all cellular contexts (Conner and Schmid 2003; Jung and Haucke 2007; Dittman and Ryan 2009; Kirchhausen 2009; McMahon and Boucrot 2011; Taylor et al. 2011).”
BackgroundSingle-Molecule Localization Microscopy in Eukaryotes
Sauer, M., & Heilemann, M. (2017) · Chemical Reviews · doi:10.1021/acs.chemrev.6b00667 · Cited by 400
Milošević, I., Giovedì, S., Lou, X., Raimondi, A., Collesi, C., Shen, H., Paradise, S., O'Toole, E. T., Ferguson, S. M., Cremona, O., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.08.029 · Cited by 357
“Clathrin-mediated endocytosis is a major pathway for SV recycling (Dittman and Ryan, 2009; Heuser and Reese, 1973).”
Krebs, C. E., Karkheiran, S., Powell, J., Cao, M., Makarov, V., Darvish, H., Paolo, G. D., Walker, R. H., Shahidi, G. A., Buxbaum, J. D., et al. (2013) · Human Mutation · doi:10.1002/humu.22372 · Cited by 336
Synucleins Regulate the Kinetics of Synaptic Vesicle Endocytosis
Vargas, K. J., Makani, S., Davis, T., Westphal, C. H., Castillo, P. E., & Chandra, S. S. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4787-13.2014 · Cited by 324
“Comparison of -Syn KO and dynamin 1, 3 KO synapses Clathrin-mediated SV endocytosis is temporally organized into distinct steps— cargo recruitment by endocytic adaptors, membrane bending, bud invagination, bud neck scission by dynamins to generate a free CCV, and uncoating to release a nascent SV (Dittman and Ryan, 20…”
BackgroundProtein scaffolds in the coupling of synaptic exocytosis and endocytosis
Haucke, V., Neher, E., & Sigrist, S. J. (2011) · Nature reviews. Neuroscience · doi:10.1038/nrn2948 · Cited by 298
“Exocytosed synaptic vesicle membrane proteins and lipids in turn are recycled at the endocytic or periactive zone ( Box 1 ) that surrounds the release site , to restore functional synaptic vesicle pools for reuse and to ensure long-term functionality of the synaps”
BackgroundVos, M. H. (2010) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2010.00139 · Cited by 307
“…hippocampal neurons (Balaji et al., 2008) suggest that extracellular Ca2+ might actually be required only to increase the endocytic capacity of the presynaptic membrane under conditions of intense stimulation, in order to compensate the large influx of exocytic material (Dittman and Ryan, 2009).”
Dynamin triple knockout cells reveal off target effects of commonly used dynamin inhibitors
Park, R. J.-H., Shen, H., Liu, L., Liu, X., Ferguson, S. M., & Camilli, P. V. D. (2013) · Journal of Cell Science · doi:10.1242/jcs.138578 · Cited by 251
“In neurons, clathrin-mediated endocytosis is additionally implicated in neurotransmission because of its role in the endocytic recycling of synaptic vesicles at nerve terminals (Brodin et al., 2000; Dittman and Ryan, 2009; Heuser and Reese, 1973; Saheki and De Camilli, 2012).”
BackgroundUltrafast endocytosis at Caenorhabditis elegans neuromuscular junctions
Watanabe, S., Liu, Q., Davis, M. W., Hollopeter, G., Thomas, N., Jorgensen, N. B., & Jorgensen, E. M. (2013) · eLife · doi:10.7554/elife.00723 · Cited by 248
“Clathrin-mediated endocytosis is thought to take place lateral to the active zone, by the relatively slow (∼20 s; Miller and Heuser, 1984) recruitment of clathrin machinery (Rizzoli and Jahn, 2007; Dittman and Ryan, 2009).”
BackgroundPerspectives on Kiss-and-Run: Role in Exocytosis, Endocytosis, and Neurotransmission
Alabi, A. A., & Tsien, R. W. (2011) · Annual Review of Physiology · doi:10.1146/annurev-physiol-020911-153305 · Cited by 261
SYMPOSIUM REVIEW: Phosphoinositides: lipid regulators of membrane proteins
Falkenburger, B. H., Jensen, J. B., Dickson, E. J., Suh, B., & Hille, B. (2010) · The Journal of Physiology · doi:10.1113/jphysiol.2010.192153 · Cited by 251
“Since synaptic vesicles normally can be recycled in seconds (Dittman & Ryan, 2009), all of these events and the subsequent refilling with neurotransmitter and docking are quick.”
Overlapping Role of Dynamin Isoforms in Synaptic Vesicle Endocytosis
Raimondi, A., Ferguson, S. M., Lou, X., Armbruster, M., Paradise, S., Giovedì, S., Messa, M., Kono, N., Takasaki, J., Cappello, V., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.04.031 · Cited by 242
“On the presynaptic side, it is implicated in the recycling of synaptic vesicle membranes (Dittman and Ryan, 2009; Granseth et al., 2006; Jung and Haucke, 2007; Murthy and De Camilli, 2003).”
Self-citationThe Calyx of Held Synapse: From Model Synapse to Auditory Relay
Borst, J. G. G., & van Hoeve, J. S. S. (2011) · Annual Review of Physiology · doi:10.1146/annurev-physiol-020911-153236 · Cited by 225
BAR Domain Scaffolds in Dynamin-Mediated Membrane Fission
Daumke, O., Roux, A., & Haucke, V. (2014) · Cell · doi:10.1016/j.cell.2014.02.017 · Cited by 239
“Indeed, variations in the size of synaptic vesicles formed by CME have been observed at synapses from a variety of endocytic protein mutants (Dittman and Ryan, 2009; Ferguson et al., 2007; Saheki and De Camilli, 2012).”
Molecular Mechanisms of Presynaptic Membrane Retrieval and Synaptic Vesicle Reformation
Kononenko, N. L., & Haucke, V. (2015) · Neuron · doi:10.1016/j.neuron.2014.12.016 · Cited by 220
Kononenko, N. L., Puchkov, D., Classen, G. A. E., Walter, A. M., Pechstein, A., Sawade, L., Kaempf, N., Trimbuch, T., Lorenz, D., Rosenmund, C., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.05.007 · Cited by 212
“Early studies of frog neuromuscular junctions (Heuser and Reese, 1973) and subsequent work on mammalian synapses have suggested that SVs reform by clathrin/AP-2mediated endocytosis (CME) from the plasma membrane (Dittman and Ryan, 2009; Granseth et al., 2006; Kim and Ryan, 2009; Saheki and De Camilli, 2012), a pathway…”
InfluentialAxon Regeneration Pathways Identified by Systematic Genetic Screening in C. elegans
Chen, L., Wang, Z., Ghosh‐Roy, A., Hubert, T., Yan, D., O'Rourke, S., Bowerman, B. A., Wu, Z., Jin, Y., & Chisholm, A. D. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.009 · Cited by 196
“These are ‘‘core module’’ proteins or ‘‘secondary effectors’’ in SV endocytosis (Dittman and Ryan, 2009).”
Soykan, T., Kaempf, N., Sakaba, T., Vollweiter, D., Goerdeler, F., Puchkov, D., Kononenko, N. L., & Haucke, V. (2017) · Neuron · doi:10.1016/j.neuron.2017.02.011 · Cited by 178
The low synaptic release probability in vivo
Borst, J. G. G. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2010.03.003 · Cited by 177
Chang-Ileto, B., Frère, S. G. A., Chan, R., Voronov, S. V., Roux, A., & Paolo, G. D. (2011) · Developmental Cell · doi:10.1016/j.devcel.2010.12.008 · Cited by 180
“…recruited to sites of endocytosis by the Src homology 3 (SH3) domain-containing protein, endophilin (Gad et al., 2000; Ringstad et al., 1997), although various other endocytic SH3 proteins have been reported to interact with Synj1, such as amphiphysin and intersectin (Dittman and Ryan, 2009).”
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Humeau, Y., & Choquet, D. (2019) · Nature Neuroscience · doi:10.1038/s41593-019-0480-6 · Cited by 158
Koo, S. J., Marković, S., Puchkov, D., Mahrenholz, C. C., Beceren‐Braun, F., Maritzen, T., Dernedde, J., Volkmer, R., Oschkinat, H., & Haucke, V. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1107067108 · Cited by 142
“How such coupling is achieved remains unknown, but may involve adaptordependent sorting mechanisms (34, 35) and/or SV protein clustering (27).”
BackgroundThe Emerging Role of the Lysosome in Parkinson’s Disease
Navarro-Romero, A., Montpeyó, M., & Martínez‐Vicente, M. (2020) · Cells · doi:10.3390/cells9112399 · Cited by 139
“Endocytosis has a special relevance in the brain, given that it is involved in essential functions such as neurotransmitter and neurotrophic signaling [24,25].”
BackgroundBai, J., Hu, Z., Dittman, J. S., Pym, E. C. G., & Kaplan, J. M. (2010) · Cell · doi:10.1016/j.cell.2010.09.024 · Cited by 135
Self-citationSynaptic Vesicle Endocytosis in Different Model Systems
Gan, Q., & Watanabe, S. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00171 · Cited by 133
“However, the large size of the quantum dots might have affected the biophysics of fusion pore opening and vesicle collapse (Dittman and Ryan, 2009).”
BackgroundMechanisms of polarized membrane trafficking in neurons — Focusing in on endosomes
Lasiecka, Z. M., & Winckler, B. (2011) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2011.06.013 · Cited by 136
“In dendrites, local recycling has been demonstrated especially well for pre- and post-synaptic sites (reviewed in Dittman and Ryan, 2009; Kennedy and Ehlers, 2006; Schweizer and Ryan, 2006).”
Visualizing presynaptic function
Kavalali, E. T., & Jorgensen, E. M. (2014) · Nature Neuroscience · doi:10.1038/nn.3578 · Cited by 126
A Bcl-xL–Drp1 complex regulates synaptic vesicle membrane dynamics during endocytosis
Li, H., Alavian, K. N., Lazrove, E., Mehta, N., Jones, A., Zhang, P., Licznerski, P., Graham, M. M., Uo, T., Guo, J., et al. (2013) · Nature Cell Biology · doi:10.1038/ncb2791 · Cited by 123
Helbig, I., López-Hernández, T., Shor, O., Galer, P. D., Ganesan, S., Pendziwiat, M., Rademacher, A., Ellis, C. A., Hümpfer, N., Schwarz, N., et al. (2019) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2019.04.001 · Cited by 119
Harnessing the Power of the Endosome to Regulate Neural Development
Yap, C. C., & Winckler, B. (2012) · Neuron · doi:10.1016/j.neuron.2012.04.015 · Cited by 121
The architecture of an excitatory synapse
Chua, J. J. E., Kindler, S., Boyken, J., & Jahn, R. (2010) · Journal of Cell Science · doi:10.1242/jcs.052696 · Cited by 125
“Neurexins, which localize to presynaptic membranes, bind to an extracellular esterase-like domain that is present on postsynaptic neuroligins (Dalva et al., 2007).”
BackgroundSuper-resolving Microscopy in Neuroscience
Werner, C. D., Sauer, M., & Geis, C. (2021) · Chemical Reviews · doi:10.1021/acs.chemrev.0c01174 · Cited by 113
Dynamin is primed at endocytic sites for ultrafast endocytosis
Imoto, Y., Raychaudhuri, S., Ma, Y., Fenske, P., Sandoval, E., Itoh, K., Blumrich, E., Matsubayashi, H. T., Mamer, L., Zarebidaki, F., et al. (2022) · Neuron · doi:10.1016/j.neuron.2022.06.010 · Cited by 103
Vesicular Synaptobrevin/VAMP2 Levels Guarded by AP180 Control Efficient Neurotransmission
Koo, S. J., Kochlamazashvili, G., Rost, B. R., Puchkov, D., Gimber, N., Lehmann, M., Tadeus, G., Schmoranzer, J., Rosenmund, C., Haucke, V., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.08.034 · Cited by 107
Baumgart, J. P., Zhou, Z., Hara, M., Cook, D. C., Hoppa, M. B., Ryan, T. A., & Hemmings, H. C. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1500525112 · Cited by 99
“Neurotransmitter release is determined by the highly cooperative relationship between Ca entry and SV exocytosis, and by the number of docked and primed vesicles (readily releasable pool) (24).”
BackgroundSelf-citationPresynaptic function in health and disease
Waites, C. L., & Garner, C. C. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.03.004 · Cited by 96
Zhang, H., Wang, Y., Wong, J. J. L., Lim, K., Liou, Y., Wang, H., & Yu, F. (2014) · Developmental Cell · doi:10.1016/j.devcel.2014.06.014 · Cited by 93
Synaptic vesicle trafficking and Parkinson's disease
Esposito, G., Clara, F. A., & Verstreken, P. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20916 · Cited by 101
Dynamics of the mouse brain cortical synaptic proteome during postnatal brain development
Gonzalez‐Lozano, M. A., Klemmer, P., Gebuis, T., Hassan, C., van Nierop, P., van Kesteren, R. E., Smit, A. B., & Li, K. W. (2016) · Scientific Reports · doi:10.1038/srep35456 · Cited by 87
An overview of the synaptic vesicle lipid composition
Binotti, B., Jahn, R., & Pérez-Lara, Á. (2021) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2021.108966 · Cited by 92
“while keeping identity and integrity of the vesicle itself [56,87,102,116] (Fig.”
BackgroundCompromised fidelity of endocytic synaptic vesicle protein sorting in the absence of stonin 2
Kononenko, N. L., Diril, M. K., Puchkov, D., Kintscher, M., Koo, S. J., Pfuhl, G., Winter, Y., Wienisch, M., Klingauf, J., Breustedt, J., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1218432110 · Cited by 91
“This phenotype differs strikingly from the depletion of SVs observed in mice or flies lacking other endocytic proteins (4, 5, 21, 32) or stonin in invertebrates (27, 29, 31).”
BackgroundInfluentialXu, J., Luo, F., Zhang, Z., Xue, L., Wu, X., Chiang, H., Shin, W., & Wu, L. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.03.010 · Cited by 86
“4), a clathrin-dependent form of endocytosis (Dittman and Ryan, 2009).”
BackgroundJensen, T. P., Zheng, K., Cole, N., Marvin, J. S., Looger, L. L., & Rusakov, D. A. (2019) · Nature Communications · doi:10.1038/s41467-019-09216-8 · Cited by 83
AP2 hemicomplexes contribute independently to synaptic vesicle endocytosis
Gu, M., Liu, Q., Watanabe, S., Sun, L., Hollopeter, G., Grant, B. D., & Jørgensen, E. M. (2013) · eLife · doi:10.7554/elife.00190 · Cited by 75
“Nonetheless, the predominant mechanism for synaptic vesicle endocytosis is thought to be mediated via AP2 and clathrin (Dittman and Ryan, 2009).”
The pathology roadmap in Parkinson disease
Surmeier, D. J., & Sulzer, D. (2013) · Prion · doi:10.4161/pri.23582 · Cited by 74
Intersectin 1: a versatile actor in the synaptic vesicle cycle
Pechstein, A., Shupliakov, O., & Haucke, V. (2010) · Biochemical Society Transactions · doi:10.1042/bst0380181 · Cited by 78
Kakumoto, T., & Nakata, T. (2013) · PLoS ONE · doi:10.1371/journal.pone.0070861 · Cited by 75
“To further confirm the endocytotic retrieval of PIP3-rich membranes, we examined the dynamics of a membranous protein known to be endocytosed at nerve terminals [37].”
BackgroundModes and Regulation of Endocytic Membrane Retrieval in Mouse Auditory Hair Cells
Neef, J., Jung, S., Wong, A. B., Reuter, K., Pangršič, T., Chakrabarti, R., Kügler, S., Lenz, C., Nouvian, R., Boumil, R. M., et al. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.3313-13.2014 · Cited by 69
“Which modes of endocytosis—“kiss-and-run” endocytosis, clathrin-mediated endocytosis (CME), or bulk endocytosis (for review, see Wu, 2004, 2007; Smith et al., 2008; Clayton and Cousin, 2009; Dittman and Ryan, 2009; Royle and Lagnado, 2010; Ferguson and De Camilli, 2012)— underlie these two types of membrane retrieval…”
BackgroundSNARE Regulatory Proteins in Synaptic Vesicle Fusion and Recycling
Sauvola, C. W., & Littleton, J. T. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.733138 · Cited by 69
“To support further rounds of release, membrane proteins must be re-segregated and SV material selectively internalized to form new vesicles (Dittman and Ryan, 2009; Gan and Watanabe, 2018; Chanaday et al., 2019).”
BackgroundWahl, S., Katiyar, R., & Schmitz, F. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.5048-12.2013 · Cited by 66
“In general, different forms of endocytosis involve different sets of proteins (for review, see Wu et al., 2007; Dittman and Ryan, 2009; Doherty and McMahon, 2009; Donaldson et al., 2009; Scita and Di Fiori, 2010; Sandvig et al., 2011; Saheki and De Camilli, 2012).”
BackgroundTwo Clathrin Adaptor Protein Complexes Instruct Axon-Dendrite Polarity
Li, P., Merrill, S. A., Jørgensen, E. M., & Shen, K. (2016) · Neuron · doi:10.1016/j.neuron.2016.04.020 · Cited by 64
“Instead, since AP-2 is known to be involved in the endocytosis at the presynaptic terminals (Dittman and Ryan, 2009; Gu et al., 2008, 2013), it is likely that the defective axonal localization in dpy-23/AP-2m mutants is caused by the dysfunction of AP-2 at the presynaptic region.”
Kaempf, N., Kochlamazashvili, G., Puchkov, D., Maritzen, T., Bajjalieh, S. M., Kononenko, N. L., & Haucke, V. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1501627112 · Cited by 63
Diffusional spread and confinement of newly exocytosed synaptic vesicle proteins
Gimber, N., Tadeus, G., Maritzen, T., Schmoranzer, J., & Haucke, V. (2015) · Nature Communications · doi:10.1038/ncomms9392 · Cited by 59
Wu, X.-S., Zhang, Z., Zhao, W.-D., Wang, D.-S., Luo, F., & Wu, L.-G. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.04.020 · Cited by 64
“CaN is thus not considered a key player, like clathrin and dynamin, in vesicle endocytosis (Dittman and Ryan, 2009; Saheki and De Camilli, 2012; Wu et al., 2014).”
Coupling of exocytosis and endocytosis at the presynaptic active zone
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“In addition, endocytosis restores membrane tension and is a prerequisite for the reformation of SVs, which are needed to replenish the releasable SV pool (Dittman and Ryan, 2009; Kononenko and Haucke, 2015; Murthy and De Camilli, 2003; Soykan et al., 2016).”
BackgroundSong, P., Peng, W., Sauvé, V., Fakih, R., Xie, Z., Ysselstein, D., Krainc, T., Wong, Y. C., Mencacci, N. E., Savas, J. N., et al. (2023) · Neuron · doi:10.1016/j.neuron.2023.08.018 · Cited by 62
The SNARE Proteins SNAP25 and Synaptobrevin Are Involved in Endocytosis at Hippocampal Synapses
Zhang, Z., Wang, D., Sun, T., Xu, J., Chiang, H., Shin, W., & Wu, L. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.0301-13.2013 · Cited by 66
“, 2011), both of which may be involved in endocytosis (Zhang et al., 1998; Dittman and Ryan, 2009).”
BackgroundIn vivo synaptic recovery following optogenetic hyperstimulation
Kittelmann, M., Liewald, J. F., Hegermann, J., Schultheis, C., Brauner, M., Costa, W. S., Wabnig, S., Eimer, S., & GOTTSCHALK, A. R. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1305679110 · Cited by 62
“These processes are followed by retrieval of membrane and proteins from the plasma membrane (PM) via endocytosis (4, 5).”
BackgroundMitchell, N. A., Petralia, R. S., Yao, P. J., Currier, D. G., Wang, Y., Kim, A., & Mattson, M. P. (2012) · Journal of Cell Science · doi:10.1242/jcs.105080 · Cited by 61
“Shh-induced presynaptic terminals are functional Synaptic vesicle endocytosis is an essential process that determines the function of a synapse (Dittman and Ryan, 2009).”
BackgroundWestphalen, R. I., Desai, K., & Hemmings, H. C. (2012) · British Journal of Anaesthesia · doi:10.1093/bja/aes448 · Cited by 59
Functionally heterogeneous synaptic vesicle pools support diverse synaptic signalling
Chamberland, S., & Tóth, K. (2015) · The Journal of Physiology · doi:10.1113/jp270194 · Cited by 59
“Most of these vesicles are docked at the active zone or located in its vicinity, where activation of release machinery can trigger their release with short latency (Schikorski & Stevens, 2001; Dittman & Ryan, 2009).”
BackgroundRoyle, S., & Lagnado, L. (2010) · Traffic · doi:10.1111/j.1600-0854.2010.01104.x · Cited by 58
“Most synaptic terminals in the brain contain no more than 100–200 vesicles, so the maintenance of communication depends on vesicles being recycled from the surface after fusion (3,4).”
InfluentialSpatial and temporal integration of signalling networks regulating pollen tube growth
Zonia, L. E. (2010) · Journal of Experimental Botany · doi:10.1093/jxb/erq073 · Cited by 57
Synaptotagmin‐11 inhibits clathrin‐mediated and bulk endocytosis
Wang, C., Wang, Y., Hu, M., Chai, Z., Wu, Q., Huang, R., Han, W., Zhang, C. X., & Zhou, Z. (2015) · EMBO Reports · doi:10.15252/embr.201540689 · Cited by 57
“Elevated neuronal activity also elicits bulk endocytosis when large areas of plasma membrane are internalized [1,2,4].”
AP‐2 reduces amyloidogenesis by promoting BACE1 trafficking and degradation in neurons
Bera, S., Camblor‐Perujo, S., Barca, E. C., Negrete‐Hurtado, A., Racho, J., Bruyckere, E. D., Wittich, C., Ellrich, N., Martins, S., Adjaye, J., et al. (2020) · EMBO Reports · doi:10.15252/embr.201947954 · Cited by 55
“AP-2 is a heterotetrameric complex comprised of a , b , l , and r subunits that links clathrin and other endocytic proteins to sites of clathrin-mediated endocytosis (CME) [26].”
InfluentialPan, P., Marrs, J., & Ryan, T. A. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.651711 · Cited by 54
Self-citationDeleterious effects of soluble amyloid-β oligomers on multiple steps of synaptic vesicle trafficking
Park, J., Jang, M., & Chang, S. (2013) · Neurobiology of Disease · doi:10.1016/j.nbd.2013.03.004 · Cited by 57
“Synaptic vesicle components are recycled through a local exo-endocytic pathway in presynaptic nerve terminals, and recent studies have revealed some of the molecular details of this process (Dittman and Ryan, 2009; Murthy and De Camilli, 2003).”
BackgroundZhang, Y., McCartney, A. J., Zolov, S. N., Ferguson, C., Meisler, M. H., Sutton, M. A., & Weisman, L. S. (2012) · The EMBO Journal · doi:10.1038/emboj.2012.200 · Cited by 56
“Accordingly, the endosomal system in neurons has both general and specialized pathways, such as long-range trafficking along neurites (Ibáñez, 2007), as well as specialized recycling in both the presynaptic and postsynaptic terminals (Kennedy and Ehlers, 2006; Dittman and Ryan, 2009).”
Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis
Ogunmowo, T. H., Jing, H., Raychaudhuri, S., Kusick, G. F., Imoto, Y., Li, S., Itoh, K., Ma, Y., Jafri, H., Dalva, M. B., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-38595-2 · Cited by 51
Botulinum Neurotoxin Serotype C Associates with Dual Ganglioside Receptors to Facilitate Cell Entry
Karalewitz, A., Fu, Z., Baldwin, M. R., Kim, J. P., & Barbieri, J. T. (2012) · Journal of Biological Chemistry · doi:10.1074/jbc.m112.404244 · Cited by 51
“This suggests the dual receptors for HCR/C are present on the plasma membrane and that SV exocytosis may not be necessary to expose BoNT/C receptors but rather may enhance entry because of the compensatory increase in SV endocytosis following depolarization (32).”
BackgroundRegulation of Synaptic Vesicle Budding and Dynamin Function by an EHD ATPase
Jakobsson, J., Ackermann, F., Andersson, F., Larhammar, D., Löw, P., & Brodin, L. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.1289-11.2011 · Cited by 44
“…modes of synaptic vesicle endocytosis have been suggested to occur at nerve terminals: clathrin-mediated endocytosis, kiss-and-run recapture, and bulk endocytosis (Takei et al., 1996; Clayton et al., 2008; Dittman and Ryan, 2009; Granseth et al., 2009; Zhang et al., 2009; Hoopmann et al., 2010).”
BackgroundMultiple Dileucine-like Motifs Direct VGLUT1 Trafficking
Foss, S., Li, H., Santos, M., Edwards, R. H., & Voglmaier, S. M. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.5662-12.2013 · Cited by 51
“Since NT3 VGLUT1-pH relies on the C-terminal motif for endocytosis, this motif must depend primarily on AP-2, consistent with the role of AP-2 and this motif in compensatory endocytosis (Dittman and Ryan, 2009; Kim and Ryan, 2009; Royle and Lagnado, 2010).”
BackgroundTakeda, T., Kozai, T., Yangxs, H., Ishikuro, D., Seyama, K., Kumagai, Y., Abe, T., Yamada, H., Uchihashi, T., Ando, T., et al. (2018) · eLife · doi:10.7554/elife.30246 · Cited by 52
“Besides amphiphysin, other BAR domain proteins, endophilin and syndapin, are also implicated in synaptic vesicle recycling (Dittman and Ryan, 2009; Koch et al., 2011; Milosevic et al., 2011).”
BackgroundVesicular Sterols Are Essential for Synaptic Vesicle Cycling
Dason, J. S., Smith, A. J., Marin, L., & Charlton, M. P. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4132-10.2010 · Cited by 49
“…(Martin, 2000; Yoshinaka et al., 2004; Jia et al., 2006; Lv et al., 2008), the many adapter proteins involved in endocytosis (for review, see Dittman and Ryan, 2009) might disperse (Geumann et al., 2010) or it might be energetically difficult to reinsert cholesterol into the densely packed…”
BackgroundPechstein, A., Gerth, F., Milošević, I., Jäpel, M., Eichhorn‐Grünig, M., Vorontsova, O. V., Bacetic, J., Maritzen, T., Shupliakov, O., Freund, C., et al. (2014) · EMBO Reports · doi:10.15252/embr.201439260 · Cited by 51
“Neurotransmission is mediated by the fusion of synaptic vesicles (SVs) with the presynaptic membrane, followed by compensatory endocytosis and clathrin-mediated SV reformation [1–3].”
Role of Phosphoinositides at the Neuronal Synapse
Frère, S. G. A., Chang-Ileto, B., & Paolo, G. D. (2012) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-94-007-3015-1_5 · Cited by 48
“Remarkably, acute manipulations of actin dynamics in mammalian hippocampal synapses with actin drugs have relatively minor consequences on the SV cycle (Dittman and Ryan, 2009, Sankaranarayanan et al., 2003).”
BackgroundCa2+-dependent regulation of synaptic vesicle endocytosis
Yamashita, T. (2012) · Neuroscience Research · doi:10.1016/j.neures.2012.02.012 · Cited by 47
Shi, Y., Stefan, C. J., Rue, S. M., Teis, D., & Emr, S. D. (2011) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-05-0440 · Cited by 46
“, resensitization of β-adrenergic receptors; Hanyaloglu and von Zastrow, 2008), the recycling of synaptic vesicle proteins necessary for neurotransmitter release at the synapse (Dittman and Ryan, 2009), and the delivery of glucose transporters (e.”
Ultrastructural organization of presynaptic terminals
Siksou, L., Triller, A., & Marty, S. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.12.003 · Cited by 44
Stonin 2 Is a Major Adaptor Protein for Clathrin-Mediated Synaptic Vesicle Retrieval
Willox, A. K., & Royle, S. (2012) · Current Biology · doi:10.1016/j.cub.2012.05.048 · Cited by 44
“Although the involvement of clathrin and dynamin in synaptic vesicle retrieval is clear, it is unknown which adaptor proteins are used to sort the essential components into the vesicle [1, 4, 6].”
Synaptojanin cooperates in vivo with endophilin through an unexpected mechanism
Dong, Y., Gou, Y., Li, Y., Liu, Y., & Bai, J. (2015) · eLife · doi:10.7554/elife.05660 · Cited by 43
“Our results reveal an unexpected mechanism whereby the Sac1 domain displays a non-catalytic function to support coordinated action between synaptojanin and endophilin at synapses.”
BackgroundMaturation of a PKG-Dependent Retrograde Mechanism for Exoendocytic Coupling of Synaptic Vesicles
Eguchi, K., Nakanishi, S., Takagi, H., Taoufiq, Z., & Takahashi, T. (2012) · Neuron · doi:10.1016/j.neuron.2012.03.028 · Cited by 45
“Among them, CME is the best understood and is the predominant route of synaptic vesicle endocytosis (Cousin and Robinson, 2001; Granseth et al., 2006; Jung and Haucke, 2007; Dittman and Ryan, 2009; Haucke et al., 2011).”
InfluentialTurning CALM into excitement: AP180 and CALM in endocytosis and disease
Maritzen, T., Koo, S. J., & Haucke, V. (2012) · Biology of the Cell · doi:10.1111/boc.201200008 · Cited by 44
“…membrane sites recruit clathrin and accessory factors to drive CCP maturation, progressive membrane invagination and finally fission via the large GTPase dynamin (Faelber et al., 2011; Ford et al., 2011) [reviewed in (Dittman and Ryan, 2009; McMahon and Boucrot, 2011; Wieffer et al., 2009)].”
BackgroundPERK-Mediated Unfolded Protein Response Activation and Oxidative Stress in PARK20 Fibroblasts
Amodio, G., Moltedo, O., Fasano, D., Zerillo, L., Oliveti, M., Pietro, P. D., Faraonio, R., Barone, P., Pellecchia, M. T., Rosa, A. D., et al. (2019) · Frontiers in Neuroscience · doi:10.3389/fnins.2019.00673 · Cited by 48
“Additionally, the Synj1 protein also contains a COOHterminal proline rich region that retains the ability to interact with SH3 domains of a variety of proteins that regulate its subcellular localization and function (McPherson et al., 1996; Dittman and Ryan, 2009).”
Structure activity relationship of synaptic and junctional neurotransmission
Goyal, R. K., & Chaudhury, A. (2013) · Autonomic Neuroscience · doi:10.1016/j.autneu.2013.02.012 · Cited by 46
“It includes clathrin, dynamin and a family of SH3-domain-containing adaptor proteins (Dittman and Ryan, 2009; Sorensen, 2009).”
LoGiudice, L., Sterling, P., & Matthews, G. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.09.023 · Cited by 42
Zucker, R. S., Kullmann, D. M., & Kaeser, P. S. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-397179-1.00015-4 · Cited by 44
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
“CME has been extensively studied (Jung and Haucke, 2007; Dittman and Ryan, 2009).”
Lou, X. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00066 · Cited by 39
“Second, SVs fuse at AZs and are retrieved by CME at endocytic zones (EZs) (Dittman and Ryan, 2009; Saheki and De Camilli, 2012).”
BackgroundWenzel, E. M., Morton, A., Ebert, K., Welzel, O., Kornhuber, J., Cousin, M. A., & Groemer, T. W. (2012) · PLoS ONE · doi:10.1371/journal.pone.0038188 · Cited by 42
“Kissand-run is an established mechanism of membrane retrieval in neurosecretory and mast cells [3,4,5,6,7], however its contribution at central synapses and neuromuscular junctions remains unclear (discussed in [8]).”
BackgroundA Presynaptic Role for the Cytomatrix Protein GIT in Synaptic Vesicle Recycling
Podufall, J., Tian, R., Knoche, E., Puchkov, D., Walter, A. M., Rosa, S., Quentin, C., Vukoja, A., Jung, N., Lampe, A., et al. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.04.051 · Cited by 42
“Endocytic retrieval of exocytosed SV proteins involves adaptor proteins (Dittman and Ryan, 2009) such as AP-2, stonins (Fergestad and Broadie, 2001; Mullen et al.”
Mechanisms 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
“AP-2 is the major Clathrin adaptor protein for endocytosis (Robinson, 2004), which functions as a heterotetrameric complex comprised of α, β, µ, and σ subunits (Dittman & Ryan, 2009).”
BackgroundCSN complex controls the stability of selected synaptic proteins via a torsinA‐dependent process
Granata, A., Koo, S. J., Haucke, V., Schiavo, G., & Warner, T. T. (2010) · The EMBO Journal · doi:10.1038/emboj.2010.285 · Cited by 40
“…proteins, stonin 2 (STN2), a synaptotagmin-specific sorting adaptor (Maritzen et al, 2010) and the AP2 adaptor complex (Jung and Haucke, 2007; Dittman and Ryan, 2009) were negatively affected by siRNA knockdowns and showed a reduction quantitatively similar &2011 European Molecular Biology…”
BackgroundIntersectin-Mediated Clearance of SNARE Complexes Is Required for Fast Neurotransmission
Jäpel, M., Gerth, F., Sakaba, T., Bacetic, J., Yao, L., Koo, S. J., Maritzen, T., Freund, C., & Haucke, V. (2020) · Cell Reports · doi:10.1016/j.celrep.2019.12.035 · Cited by 42
N-Cadherin Prodomain Processing Regulates Synaptogenesis
Reinés, A. G., Bernier, L., McAdam, R. L., Belkaïd, W., Shan, W., Koch, A., Séguéla, P., Colman, D., & Dhaunchak, A. S. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.0916-12.2012 · Cited by 38
“8) previously described as related to endocytic phenomena (Smith et al., 2008; Dittman and Ryan, 2009).”
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 36
Metadata
- Authors
- Dittman, J., & Ryan, T. A.
- Affiliations
- Weill Cornell Medicine (US)
- Venue
- Annual Review of Cell and Developmental Biology
- Publisher
- Annual Reviews
- Published
- 2009-11-01
- Volume
- 25
- Issue
- 1
- Pages
- 133-160
- ISSN
- 1081-0706 (ISSN-L)
- 1530-8995
- OpenAlex
- W2167118899
- Cited by
- 238
- References
- 157
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 5 · 2023: 7 · 2022: 7 · 2021: 8 · 2020: 20 · 2019: 9 · 2018: 6 · 2017: 9 · 2016: 8 · 2015: 22 · 2014: 27 · 2013: 28 · 2012: 28
- FWCI
- 1.85
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Annual Review of Cell and Developmental Biology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (R01NS036942)
- 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 endocytosis, presynaptic terminals, neurotransmitter release, membrane retrieval, vesicle recycling, calcium-triggered exocytosis, synaptic vesicle trafficking, endocytic machinery
- MeSH terms
- Animals, Cell Membrane, Endocytosis, Synapses, Synaptic Vesicles, Presynaptic Terminals
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