Abstract
In the CNS communication between neurons occurs at synapses by secretion of neurotransmitter via exocytosis of synaptic vesicles (SVs) at the active zone. Given the limited number of SVs in presynaptic boutons a fast and efficient recycling of exocytosed membrane and proteins by triggered compensatory endocytosis is required to maintain neurotransmission. Thus, pre-synapses feature a unique tight coupling of exo- and endocytosis in time and space resulting in the reformation of SVs with uniform morphology and well-defined molecular composition. This rapid response requires early stages of endocytosis at the peri-active zone to be well choreographed to ensure reformation of SVs with high fidelity. The pre-synapse can address this challenge by a specialized membrane microcompartment, where a pre-sorted and pre-assembled readily retrievable pool (RRetP) of endocytic membrane patches is formed, consisting of the vesicle cargo, presumably bound within a nucleated Clathrin and adaptor complex. This review considers evidence for the RRetP microcompartment to be the primary organizer of presynaptic triggered compensatory endocytosis.
Funding source: Deutsche Forschungsgemeinschaft
Award Identifier / Grant number: SFB 1348 A02
Award Identifier / Grant number: SFB 944 P5
Acknowledgments
We would like to thank our colleague Dr. Martin Kahms for proofreading this manuscript. This work was supported by grants of the German Research Foundation to JK (DFG: SFB 944 P5 and SFB 1348 A02).
-
Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
-
Research funding: This work was financially supported by the Deutsche Forschungsgemeinschaft (SFB 1348 A02, SFB 944 P5).
-
Conflict of interest statement: The authors declare no conflicts of interest regarding this article.
References
Almeida-Souza, L., Frank, R.A.W., García-Nafría, J., Colussi, A., Gunawardana, N., Johnson, C.M., Yu, M., Howard, G., Andrews, B., Vallis, Y., et al.. (2018). A flat BAR protein promotes actin polymerization at the base of clathrin-coated pits. Cell 174: 325–337.e14, https://doi.org/10.1016/j.cell.2018.05.020.Search in Google Scholar PubMed PubMed Central
Angleson, J.K. and Betz, W.J. (1997). Monitoring secretion in real time: capacitance, amperometry and fluorescence compared. Trends Neurosci. 20: 281–287, https://doi.org/10.1016/s0166-2236(97)01083-7.Search in Google Scholar PubMed
Armbruster, R.R., Begun, J.W., and Duncan, A.K. (2009). An in-house learning laboratory for patient-centered innovation. J. Healthc. Qual. 31: 10–17, https://doi.org/10.1111/j.1945-1474.2009.00004.x.Search in Google Scholar PubMed
Avinoam, O., Schorb, M., Beese, C.J., Briggs, J.A.G., and Kaksonen, M. (2015). ENDOCYTOSIS. Endocytic sites mature by continuous bending and remodeling of the clathrin coat. Science 348: 1369–1372, https://doi.org/10.1126/science.aaa9555.Search in Google Scholar PubMed
Beck, K.A. and Keen, J.H. (1991). Interaction of phosphoinositide cycle intermediates with the plasma membrane-associated clathrin assembly protein AP-2. J. Biol. Chem. 266: 4442–4447, https://doi.org/10.1016/s0021-9258(20)64342-3.Search in Google Scholar
Bhave, M., Mino, R.E., Wang, X., Lee, J., Grossman, H.M., Lakoduk, A.M., Danuser, G., Schmid, S.L., and Mettlen, M. (2020). Functional characterization of 67 endocytic accessory proteins using multiparametric quantitative analysis of CCP dynamics. Proc. Natl. Acad. Sci. U.S.A. 117: 31591–31602, https://doi.org/10.1073/pnas.2020346117.Search in Google Scholar PubMed PubMed Central
Blondeau, F., Ritter, B., Allaire, P.D., Wasiak, S., Girard, M., Hussain, N.K., Angers, A., Legendre-Guillemin, V., Roy, L., Boismenu, D., et al.. (2004). Tandem MS analysis of brain clathrin-coated vesicles reveals their critical involvement in synaptic vesicle recycling. Proc. Natl. Acad. Sci. U.S.A. 101: 3833–3838, https://doi.org/10.1073/pnas.0308186101.Search in Google Scholar PubMed PubMed Central
Brod, J., Hellwig, A., and Wieland, F.T. (2020). Epsin but not AP-2 supports reconstitution of endocytic clathrin-coated vesicles. FEBS Lett. 594: 2227–2239, https://doi.org/10.1002/1873-3468.13801.Search in Google Scholar PubMed
Bucher, D., Frey, F., Sochacki, K.A., Kummer, S., Bergeest, J.-P., Godinez, W.J., Kräusslich, H.-G., Rohr, K., Taraska, J.W., Schwarz, U.S., et al.. (2018). Clathrin-adaptor ratio and membrane tension regulate the flat-to-curved transition of the clathrin coat during endocytosis. Nat. Commun. 9: 1109, https://doi.org/10.1038/s41467-018-03533-0.Search in Google Scholar PubMed PubMed Central
Busch, D.J., Houser, J.R., Hayden, C.C., Sherman, M.B., Lafer, E.M., and Stachowiak, J.C. (2015). Intrinsically disordered proteins drive membrane curvature. Nat. Commun. 6: 7875, https://doi.org/10.1038/ncomms8875.Search in Google Scholar PubMed PubMed Central
Ceccarelli, B., Hurlbut, W.P., and Mauro, A. (1973). Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J. Cell Biol. 57: 499–524, https://doi.org/10.1083/jcb.57.2.499.Search in Google Scholar PubMed PubMed Central
Chen, Y., Yong, J., Martínez-Sánchez, A., Yang, Y., Wu, Y., de Camilli, P., Fernández-Busnadiego, R., and Wu, M. (2019). Dynamic instability of clathrin assembly provides proofreading control for endocytosis. J. Cell Biol. 218: 3200–3211, https://doi.org/10.1083/jcb.201804136.Search in Google Scholar PubMed PubMed Central
Clayton, E.L. and Cousin, M.A. (2008). Differential labelling of bulk endocytosis in nerve terminals by FM dyes. Neurochem. Int. 53: 51–55, https://doi.org/10.1016/j.neuint.2008.06.002.Search in Google Scholar PubMed
Clayton, E.L. and Cousin, M.A. (2009). The molecular physiology of activity-dependent bulk endocytosis of synaptic vesicles. J. Neurochem. 111: 901–914, https://doi.org/10.1111/j.1471-4159.2009.06384.x.Search in Google Scholar PubMed PubMed Central
Cocucci, E., Aguet, F., Boulant, S., and Kirchhausen, T. (2012). The first five seconds in the life of a clathrin-coated pit. Cell 150: 495–507, https://doi.org/10.1016/j.cell.2012.05.047.Search in Google Scholar PubMed PubMed Central
Cocucci, E., Gaudin, R., and Kirchhausen, T. (2014). Dynamin recruitment and membrane scission at the neck of a clathrin-coated pit. Mol. Biol. Cell 25: 3595–3609, https://doi.org/10.1091/mbc.e14-07-1240.Search in Google Scholar
Cremona, O., Di Paolo, G., Wenk, M.R., Lüthi, A., Kim, W.T., Takei, K., Daniell, L., Nemoto, Y., Shears, S.B., Flavell, R.A., et al.. (1999). Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell 99: 179–188, https://doi.org/10.1016/s0092-8674(00)81649-9.Search in Google Scholar PubMed
Dannhauser, P.N. and Ungewickell, E.J. (2012). Reconstitution of clathrin-coated bud and vesicle formation with minimal components. Nat. Cell Biol. 14: 634–639, https://doi.org/10.1038/ncb2478.Search in Google Scholar PubMed
Dannhauser, P.N., Platen, M., Böning, H., Ungewickell, H., Schaap, I.A.T., and Ungewickell, E.J. (2015). Effect of clathrin light chains on the stiffness of clathrin lattices and membrane budding. Traffic 16: 519–533, https://doi.org/10.1111/tra.12263.Search in Google Scholar PubMed
Das, J., Tiwari, M., and Subramanyam, D. (2021). Clathrin light chains: not to be taken so lightly. Front. Cell Dev. Biol. 9: 774587, https://doi.org/10.3389/fcell.2021.774587.Search in Google Scholar PubMed PubMed Central
Diril, M.K., Wienisch, M., Jung, N., Klingauf, J., and Haucke, V. (2006). Stonin 2 is an AP-2-dependent endocytic sorting adaptor for synaptotagmin internalization and recycling. Dev. Cell 10: 233–244, https://doi.org/10.1016/j.devcel.2005.12.011.Search in Google Scholar PubMed
Dittman, J. and Ryan, T.A. (2009). Molecular circuitry of endocytosis at nerve terminals. Annu. Rev. Cell Dev. Biol. 25: 133–160, https://doi.org/10.1146/annurev.cellbio.042308.113302.Search in Google Scholar PubMed
Doherty, G.J. and McMahon, H.T. (2009). Mechanisms of endocytosis. Annu. Rev. Biochem. 78: 857–902, https://doi.org/10.1146/annurev.biochem.78.081307.110540.Search in Google Scholar PubMed
Eisenberg, E. and Greene, L.E. (2007). Multiple roles of auxilin and hsc70 in clathrin-mediated endocytosis. Traffic 8: 640–646, https://doi.org/10.1111/j.1600-0854.2007.00568.x.Search in Google Scholar PubMed
Ferguson, S.M., Brasnjo, G., Hayashi, M., Wölfel, M., Collesi, C., Giovedi, S., Raimondi, A., Gong, L.-W., Ariel, P., Paradise, S., et al.. (2007). A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science 316: 570–574, https://doi.org/10.1126/science.1140621.Search in Google Scholar PubMed
Fernández-Alfonso, T., Kwan, R., and Ryan, T.A. (2006). Synaptic vesicles interchange their membrane proteins with a large surface reservoir during recycling. Neuron 51: 179–186, https://doi.org/10.1016/j.neuron.2006.06.008.Search in Google Scholar PubMed
Ford, M.G., Pearse, B.M., Higgins, M.K., Vallis, Y., Owen, D.J., Gibson, A., Hopkins, C.R., Evans, P.R., and McMahon, H.T. (2001). Simultaneous binding of PtdIns(4,5)P2 and clathrin by AP180 in the nucleation of clathrin lattices on membranes. Science 291: 1051–1055, https://doi.org/10.1126/science.291.5506.1051.Search in Google Scholar PubMed
Foss, S.M., Li, H., Santos, M.S., Edwards, R.H., and Voglmaier, S.M. (2013). Multiple dileucine-like motifs direct VGLUT1 trafficking. J. Neurosci. 33: 10647–10660, https://doi.org/10.1523/jneurosci.5662-12.2013.Search in Google Scholar PubMed PubMed Central
Gandhi, S.P. and Stevens, C.F. (2003). Three modes of synaptic vesicular recycling revealed by single-vesicle imaging. Nature 423: 607–613, https://doi.org/10.1038/nature01677.Search in Google Scholar PubMed
Gauthier-Kemper, A., Kahms, M., and Klingauf, J. (2015). Restoring synaptic vesicles during compensatory endocytosis. Essays Biochem. 57: 121–134, https://doi.org/10.1042/bse0570121.Search in Google Scholar PubMed
Gimber, N., Tadeus, G., Maritzen, T., Schmoranzer, J., and Haucke, V. (2015). Diffusional spread and confinement of newly exocytosed synaptic vesicle proteins. Nat. Commun. 6: 8392, https://doi.org/10.1038/ncomms9392.Search in Google Scholar PubMed PubMed Central
Gordon, S.L. and Cousin, M.A. (2016). The iTRAPs: guardians of synaptic vesicle cargo retrieval during endocytosis. Front. Synaptic Neurosci. 8: 1, https://doi.org/10.3389/fnsyn.2016.00001.Search in Google Scholar PubMed PubMed Central
Gordon, S.L., Leube, R.E., and Cousin, M.A. (2011). Synaptophysin is required for synaptobrevin retrieval during synaptic vesicle endocytosis. J. Neurosci. 31: 14032–14036, https://doi.org/10.1523/jneurosci.3162-11.2011.Search in Google Scholar PubMed PubMed Central
Gundelfinger, E.D. and Fejtova, A. (2012). Molecular organization and plasticity of the cytomatrix at the active zone. Curr. Opin. Neurobiol. 22: 423–430, https://doi.org/10.1016/j.conb.2011.10.005.Search in Google Scholar PubMed
Haucke, V., Neher, E., and Sigrist, S.J. (2011). Nature reviews. Neuroscience 12: 127–138, https://doi.org/10.1038/nrn2948. 21304549.Search in Google Scholar PubMed
Henne, W.M., Boucrot, E., Meinecke, M., Evergren, E., Vallis, Y., Mittal, R., and McMahon, H.T. (2010). FCHo proteins are nucleators of clathrin-mediated endocytosis. Science 328: 1281–1284, https://doi.org/10.1126/science.1188462.Search in Google Scholar PubMed PubMed Central
Heuser, J.E. and Anderson, R.G. (1989). Hypertonic media inhibit receptor-mediated endocytosis by blocking clathrin-coated pit formation. J. Cell Biol. 108: 389–400, https://doi.org/10.1083/jcb.108.2.389.Search in Google Scholar PubMed PubMed Central
Heuser, J.E. and Reese, T.S. (1973). Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 57: 315–344, https://doi.org/10.1083/jcb.57.2.315.Search in Google Scholar PubMed PubMed Central
Heuser, J. (1980). Three-dimensional visualization of coated vesicle formation in fibroblasts. J. Cell Biol. 84: 560–583, https://doi.org/10.1083/jcb.84.3.560.Search in Google Scholar PubMed PubMed Central
Hirst, J., Miller, S.E., Taylor, M.J., von Mollard, G.F., and Robinson, M.S. (2004). EpsinR is an adaptor for the SNARE protein Vti1b. Mol. Biol. Cell 15: 5593–5602, https://doi.org/10.1091/mbc.e04-06-0468.Search in Google Scholar PubMed PubMed Central
Hollopeter, G., Lange, J.J., Zhang, Y., Vu, T.N., Gu, M., Ailion, M., Lambie, E.J., Slaughter, B.D., Unruh, J.R., Florens, L., et al.. (2014). The membrane-associated proteins FCHo and SGIP are allosteric activators of the AP2 clathrin adaptor complex. Elife 3: e03648.10.7554/eLife.03648Search in Google Scholar PubMed PubMed Central
Höning, S., Ricotta, D., Krauss, M., Späte, K., Spolaore, B., Motley, A., Robinson, M., Robinson, C., Haucke, V., and Owen, D.J. (2005). Phosphatidylinositol-(4,5)-bisphosphate regulates sorting signal recognition by the clathrin-associated adaptor complex AP2. Mol. Cell 18: 519–531, https://doi.org/10.1016/j.molcel.2005.08.001.Search in Google Scholar
Hosoi, N., Holt, M., and Sakaba, T. (2009). Calcium dependence of exo- and endocytotic coupling at a glutamatergic synapse. Neuron 63: 216–229, https://doi.org/10.1016/j.neuron.2009.06.010.Search in Google Scholar PubMed
Hua, Y., Sinha, R., Thiel, C.S., Schmidt, R., Hüve, J., Martens, H., Hell, S.W., Egner, A., and Klingauf, J. (2011). A readily retrievable pool of synaptic vesicles. Nat. Neurosci. 14: 833–839, https://doi.org/10.1038/nn.2838.Search in Google Scholar PubMed
Hua, Y., Woehler, A., Kahms, M., Haucke, V., Neher, E., and Klingauf, J. (2013). Blocking endocytosis enhances short-term synaptic depression under conditions of normal availability of vesicles. Neuron 80: 343–349, https://doi.org/10.1016/j.neuron.2013.08.010.Search in Google Scholar PubMed
Jahn, R. and Scheller, R.H. (2006). SNAREs—engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 7: 631–643, https://doi.org/10.1038/nrm2002.Search in Google Scholar PubMed
Jakob, B., Kochlamazashvili, G., Jäpel, M., Gauhar, A., Bock, H.H., Maritzen, T., and Haucke, V. (2017). Intersectin 1 is a component of the Reelin pathway to regulate neuronal migration and synaptic plasticity in the hippocampus. Proc. Natl. Acad. Sci. U.S.A. 114: 5533–5538, https://doi.org/10.1073/pnas.1704447114.Search in Google Scholar PubMed PubMed Central
Jäpel, M., Gerth, F., Sakaba, T., Bacetic, J., Yao, L., Koo, S.-J., Maritzen, T., Freund, C., and Haucke, V. (2020). Intersectin-mediated clearance of SNARE complexes is required for fast neurotransmission. Cell Rep. 30: 409–420.e6, https://doi.org/10.1016/j.celrep.2019.12.035.Search in Google Scholar PubMed
Kahms, M. and Klingauf, J. (2018). Novel pH-sensitive lipid based exo-endocytosis tracers reveal fast intermixing of synaptic vesicle pools. Front. Cell. Neurosci. 12: 18, https://doi.org/10.3389/fncel.2018.00018.Search in Google Scholar PubMed PubMed Central
Kanaseki, T. and Kadota, K. (1969). The “vesicle in a basket”. A morphological study of the coated vesicle isolated from the nerve endings of the Guinea pig brain, with special reference to the mechanism of membrane movements. J. Cell Biol. 42: 202–220, https://doi.org/10.1083/jcb.42.1.202.Search in Google Scholar PubMed PubMed Central
Kim, S.H. and Ryan, T.A. (2009). Synaptic vesicle recycling at CNS snapses without AP-2. J. Neurosci. 29: 3865–3874, https://doi.org/10.1523/jneurosci.5639-08.2009.Search in Google Scholar
Kirchhausen, T. (1993). Coated pits and coated vesicles—sorting it all out. Curr. Opin. Struct. Biol. 3: 182–188, https://doi.org/10.1016/s0959-440x(05)80150-2.Search in Google Scholar
Kirchhausen, T. (2009). Imaging endocytic clathrin structures in living cells. Trends Cell Biol. 19: 596–605, https://doi.org/10.1016/j.tcb.2009.09.002.Search in Google Scholar PubMed PubMed Central
Klingauf, J., Kavalali, E.T., and Tsien, R.W. (1998). Kinetics and regulation of fast endocytosis at hippocampal synapses. Nature 394: 581–585, https://doi.org/10.1038/29079.Search in Google Scholar PubMed
Koh, T.-W., Korolchuk, V.I., Wairkar, Y.P., Jiao, W., Evergren, E., Pan, H., Zhou, Y., Venken, K.J.T., Shupliakov, O., Robinson, I.M., et al.. (2007). Eps15 and Dap160 control synaptic vesicle membrane retrieval and synapse development. J. Cell Biol. 178: 309–322, https://doi.org/10.1083/jcb.200701030.Search in Google Scholar PubMed PubMed Central
Kokotos, A.C. and Cousin, M.A. (2015). Synaptic vesicle generation from central nerve terminal endosomes. Traffic 16: 229–240, https://doi.org/10.1111/tra.12235.Search in Google Scholar PubMed
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). Compromised fidelity of endocytic synaptic vesicle protein sorting in the absence of stonin 2. Proc. Natl. Acad. Sci. U.S.A. 110: E526–E535, https://doi.org/10.1073/pnas.1218432110.Search in Google Scholar PubMed PubMed Central
Koo, S.J., Markovic, S., Puchkov, D., Mahrenholz, C.C., Beceren-Braun, F., Maritzen, T., Dernedde, J., Volkmer, R., Oschkinat, H., and Haucke, V. (2011). SNARE motif-mediated sorting of synaptobrevin by the endocytic adaptors clathrin assembly lymphoid myeloid leukemia (CALM) and AP180 at synapses. Proc. Natl. Acad. Sci. U.S.A. 108: 13540–13545, https://doi.org/10.1073/pnas.1107067108.Search in Google Scholar PubMed PubMed Central
Koo, S.J., Kochlamazashvili, G., Rost, B., Puchkov, D., Gimber, N., Lehmann, M., Tadeus, G., Schmoranzer, J., Rosenmund, C., Haucke, V., et al.. (2015). Vesicular synaptobrevin/VAMP2 levels guarded by AP180 control efficient neurotransmission. Neuron 88: 330–344, https://doi.org/10.1016/j.neuron.2015.08.034.Search in Google Scholar PubMed
Kovtun, O., Dickson, V.K., Kelly, B.T., Owen, D.J., and Briggs, J.A.G. (2020). Architecture of the AP2/clathrin coat on the membranes of clathrin-coated vesicles. Sci. Adv. 6: eaba8381, https://doi.org/10.1126/sciadv.aba8381.Search in Google Scholar PubMed PubMed Central
Kukulski, W., Schorb, M., Kaksonen, M., and Briggs, J.A.G. (2012). Plasma membrane reshaping during endocytosis is revealed by time-resolved electron tomography. Cell 150: 508–520, https://doi.org/10.1016/j.cell.2012.05.046.Search in Google Scholar PubMed
Lee, D.-W., Wu, X., Eisenberg, E., and Greene, L.E. (2006). Recruitment dynamics of GAK and auxilin to clathrin-coated pits during endocytosis. J. Cell Sci. 119: 3502–3512, https://doi.org/10.1242/jcs.03092.Search in Google Scholar PubMed
Leitz, J. and Kavalali, E.T. (2016). Ca2+ dependence of synaptic vesicle endocytosis. Neuroscientist 22: 464–476, https://doi.org/10.1177/1073858415588265.Search in Google Scholar PubMed
Martens, S. and McMahon, H.T. (2008). Mechanisms of membrane fusion: disparate players and common principles. Nat. Rev. Mol. Cell Biol. 9: 543–556, https://doi.org/10.1038/nrm2417.Search in Google Scholar PubMed
Maycox, P.R., Link, E., Reetz, A., Morris, S.A., and Jahn, R. (1992). Clathrin-coated vesicles in nervous tissue are involved primarily in synaptic vesicle recycling. J. Cell Biol. 118: 1379–1388, https://doi.org/10.1083/jcb.118.6.1379.Search in Google Scholar PubMed PubMed Central
McMahon, H.T. and Boucrot, E. (2011). Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat. Rev. Mol. Cell Biol. 12: 517–533, https://doi.org/10.1038/nrm3151.Search in Google Scholar PubMed
Meyerholz, A., Hinrichsen, L., Groos, S., Esk, P.-C., Brandes, G., and Ungewickell, E.J. (2005). Effect of clathrin assembly lymphoid myeloid leukemia protein depletion on clathrin coat formation. Traffic 6: 1225–1234, https://doi.org/10.1111/j.1600-0854.2005.00355.x.Search in Google Scholar PubMed
Miesenböck, G., de Angelis, D.A., and Rothman, J.E. (1998). Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394: 192–195, https://doi.org/10.1038/28190.Search in Google Scholar PubMed
Miller, T.M. and Heuser, J.E. (1984). Endocytosis of synaptic vesicle membrane at the frog neuromuscular junction. J. Cell Biol. 98: 685–698, https://doi.org/10.1083/jcb.98.2.685.Search in Google Scholar PubMed PubMed Central
Miller, S.E., Mathiasen, S., Bright, N.A., Pierre, F., Kelly, B.T., Kladt, N., Schauss, A., Merrifield, C.J., Stamou, D., Höning, S., et al.. (2015). CALM regulates clathrin-coated vesicle size and maturation by directly sensing and driving membrane curvature. Dev. Cell 33: 163–175, https://doi.org/10.1016/j.devcel.2015.03.002.Search in Google Scholar PubMed PubMed Central
Morris, K.L., Jones, J.R., Halebian, M., Wu, S., Baker, M., Armache, J.-P., Avila Ibarra, A., Sessions, R.B., Cameron, A.D., Cheng, Y., et al.. (2019). Cryo-EM of multiple cage architectures reveals a universal mode of clathrin self-assembly. Nat. Struct. Mol. Biol. 26: 890–898, https://doi.org/10.1038/s41594-019-0292-0.Search in Google Scholar PubMed PubMed Central
Mueller, V.J., Wienisch, M., Nehring, R.B., and Klingauf, J. (2004). Monitoring clathrin-mediated endocytosis during synaptic activity. J. Neurosci. 24: 2004–2012, https://doi.org/10.1523/jneurosci.4080-03.2004.Search in Google Scholar
Murthy, V.N. and Stevens, C.F. (1998). Synaptic vesicles retain their identity through the endocytic cycle. Nature 392: 497–501, https://doi.org/10.1038/33152.Search in Google Scholar PubMed
Newton, A.J., Kirchhausen, T., and Murthy, V.N. (2006). Inhibition of dynamin completely blocks compensatory synaptic vesicle endocytosis. Proc. Natl. Acad. Sci. U.S.A. 103: 17955–17960, https://doi.org/10.1073/pnas.0606212103.Search in Google Scholar PubMed PubMed Central
Nonet, M.L., Holgado, A.M., Brewer, F., Serpe, C.J., Norbeck, B.A., Holleran, J., Wei, L., Hartwieg, E., Jorgensen, E.M., and Alfonso, A. (1999). UNC-11, a Caenorhabditis elegans AP180 homologue, regulates the size and protein composition of synaptic vesicles. Mol. Biol. Cell 10: 2343–2360, https://doi.org/10.1091/mbc.10.7.2343.Search in Google Scholar PubMed PubMed Central
Park, B.-C., Yim, Y.-I., Zhao, X., Olszewski, M.B., Eisenberg, E., and Greene, L.E. (2015). The clathrin-binding and J-domains of GAK support the uncoating and chaperoning of clathrin by Hsc70 in the brain. J. Cell Sci. 128: 3811–3821, https://doi.org/10.1242/jcs.171058.Search in Google Scholar PubMed PubMed Central
Pearse, B.M. (1975). Coated vesicles from pig brain: purification and biochemical characterization. J. Mol. Biol. 97: 93–98, https://doi.org/10.1016/s0022-2836(75)80024-6.Search in Google Scholar PubMed
Petralia, R.S., Wang, Y.-X., Indig, F.E., Bushlin, I., Wu, F., Mattson, M.P., and Yao, P.J. (2013). Reduction of AP180 and CALM produces defects in synaptic vesicle size and density. NeuroMolecular Med. 15: 49–60, https://doi.org/10.1007/s12017-012-8194-x.Search in Google Scholar PubMed PubMed Central
Raimondi, A., Ferguson, S.M., Lou, X., Armbruster, M., Paradise, S., Giovedi, S., Messa, M., Kono, N., Takasaki, J., Cappello, V., et al.. (2011). Overlapping role of dynamin isoforms in synaptic vesicle endocytosis. Neuron 70: 1100–1114, https://doi.org/10.1016/j.neuron.2011.04.031.Search in Google Scholar PubMed PubMed Central
Rajappa, R., Gauthier-Kemper, A., Böning, D., Hüve, J., and Klingauf, J. (2016). Synaptophysin 1 clears synaptobrevin 2 from the presynaptic active zone to prevent short-term depression. Cell Rep. 14: 1369–1381, https://doi.org/10.1016/j.celrep.2016.01.031.Search in Google Scholar PubMed
Redlingshöfer, L., McLeod, F., Chen, Y., Camus, M.D., Burden, J.J., Palomer, E., Briant, K., Dannhauser, P.N., Salinas, P.C., and Brodsky, F.M. (2020). Clathrin light chain diversity regulates membrane deformation in vitro and synaptic vesicle formation in vivo. Proc. Natl. Acad. Sci. U.S.A. 117: 23527–23538, https://doi.org/10.1073/pnas.2003662117.Search in Google Scholar PubMed PubMed Central
Robinson, M.S. (2015). Forty years of clathrin-coated vesicles. Traffic 16: 1210–1238, https://doi.org/10.1111/tra.12335.Search in Google Scholar PubMed
Roth, T.F. and Porter, K.R. (1964). Yolk protein uptake in the oocyte of the mosquito Aedes aegyptii L. J. Cell Biol. 20: 313–332, https://doi.org/10.1083/jcb.20.2.313.Search in Google Scholar PubMed PubMed Central
Ryan, T.A., Reuter, H., Wendland, B., Schweizer, F.E., Tsien, R.W., and Smith, S.J. (1993). The kinetics of synaptic vesicle recycling measured at single presynaptic boutons. Neuron 11: 713–724, https://doi.org/10.1016/0896-6273(93)90081-2.Search in Google Scholar PubMed
Sakaba, T., Kononenko, N.L., Bacetic, J., Pechstein, A., Schmoranzer, J., Yao, L., Barth, H., Shupliakov, O., Kobler, O., Aktories, K., et al.. (2013). Fast neurotransmitter release regulated by the endocytic scaffold intersectin. Proc. Natl. Acad. Sci. U.S.A. 110: 8266–8271, https://doi.org/10.1073/pnas.1219234110.Search in Google Scholar PubMed PubMed Central
Sankaranarayanan, S. and Ryan, T.A. (2000). Real-time measurements of vesicle-SNARE recycling in synapses of the central nervous system. Nat. Cell Biol. 2: 197–204, https://doi.org/10.1038/35008615.Search in Google Scholar PubMed
Scheele, U., Kalthoff, C., and Ungewickell, E. (2001). Multiple interactions of auxilin 1 with clathrin and the AP-2 adaptor complex. J. Biol. Chem. 276: 36131–36138, https://doi.org/10.1074/jbc.m106511200.Search in Google Scholar PubMed
Schikorski, T. and Stevens, C.F. (1997). Quantitative ultrastructural analysis of hippocampal excitatory synapses. J. Neurosci. 17: 5858–5867, https://doi.org/10.1523/jneurosci.17-15-05858.1997.Search in Google Scholar PubMed PubMed Central
Schmid, E.M., Ford, M.G.J., Burtey, A., Praefcke, G.J.K., Peak-Chew, S.-Y., Mills, I.G., Benmerah, A., and McMahon, H.T. (2006). Role of the AP2 β-appendage hub in recruiting partners for clathrin-coated vesicle assembly. PLoS Biol. 4: e262, https://doi.org/10.1371/journal.pbio.0040262.Search in Google Scholar PubMed PubMed Central
Shin, W., Ge, L., Arpino, G., Villarreal, S.A., Hamid, E., Liu, H., Zhao, W.-D., Wen, P.J., Chiang, H.-C., and Wu, L.-G. (2018). Visualization of membrane pore in live cells reveals a dynamic-pore theory governing fusion and endocytosis. Cell 173: 934–945.e12, https://doi.org/10.1016/j.cell.2018.02.062.Search in Google Scholar PubMed PubMed Central
Shin, W., Wei, L., Arpino, G., Ge, L., Guo, X., Chan, C.Y., Hamid, E., Shupliakov, O., Bleck, C.K.E., and Wu, L.-G. (2021). Preformed Ω-profile closure and kiss-and-run mediate endocytosis and diverse endocytic modes in neuroendocrine chromaffin cells. Neuron 109: 3119–3134.e5, https://doi.org/10.1016/j.neuron.2021.07.019.Search in Google Scholar PubMed
Shupliakov, O., Löw, P., Grabs, D., Gad, H., Chen, H., David, C., Takei, K., de Camilli, P., and Brodin, L. (1997). Synaptic vesicle endocytosis impaired by disruption of dynamin-SH3 domain interactions. Science 276: 259–263, https://doi.org/10.1126/science.276.5310.259.Search in Google Scholar PubMed
Sochacki, K.A., Dickey, A.M., Strub, M.-P., and Taraska, J.W. (2017). Endocytic proteins are partitioned at the edge of the clathrin lattice in mammalian cells. Nat. Cell Biol. 19: 352–361, https://doi.org/10.1038/ncb3498.Search in Google Scholar PubMed PubMed Central
Sochacki, K.A., Heine, B.L., Haber, G.J., Jimah, J.R., Prasai, B., Alfonzo-Méndez, M.A., Roberts, A.D., Somasundaram, A., Hinshaw, J.E., and Taraska, J.W. (2021). The structure and spontaneous curvature of clathrin lattices at the plasma membrane. Dev. Cell 56: 1131–1146.e3, https://doi.org/10.1016/j.devcel.2021.03.017.Search in Google Scholar PubMed PubMed Central
Südhof, T.C. (2012). The presynaptic active zone. Neuron 75: 11–25, https://doi.org/10.1016/j.neuron.2012.06.012.Search in Google Scholar PubMed PubMed Central
Takamori, S., Holt, M., Stenius, K., Lemke, E.A., Grønborg, M., Riedel, D., Urlaub, H., Schenck, S., Brügger, B., Ringler, P., et al.. (2006). Molecular anatomy of a trafficking organelle. Cell 127: 831–846, https://doi.org/10.1016/j.cell.2006.10.030.Search in Google Scholar PubMed
Takei, K., McPherson, P.S., Schmid, S.L., and de Camilli, P. (1995). Tubular membrane invaginations coated by dynamin rings are induced by GTP-gamma S in nerve terminals. Nature 374: 186–190, https://doi.org/10.1038/374186a0.Search in Google Scholar PubMed
Taylor, M.J., Perrais, D., and Merrifield, C.J. (2011). A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol. 9: e1000604, https://doi.org/10.1371/journal.pbio.1000604.Search in Google Scholar PubMed PubMed Central
Taylor, M.J., Lampe, M., and Merrifield, C.J. (2012). A feedback loop between dynamin and actin recruitment during clathrin-mediated endocytosis. PLoS Biol. 10: e1001302, https://doi.org/10.1371/journal.pbio.1001302.Search in Google Scholar PubMed PubMed Central
Ungewickell, E. and Branton, D. (1981). Assembly units of clathrin coats. Nature 289: 420–422, https://doi.org/10.1038/289420a0.Search in Google Scholar PubMed
van der Kloot, W. (1991). The regulation of quantal size. Prog. Neurobiol. 36: 93–130, https://doi.org/10.1016/0301-0082(91)90019-w.Search in Google Scholar PubMed
Vanden Berghe, P. and Klingauf, J. (2007). Spatial organization and dynamic properties of neurotransmitter release sites in the enteric nervous system. Neuroscience 145: 88–99, https://doi.org/10.1016/j.neuroscience.2006.11.048.Search in Google Scholar PubMed
Voglmaier, S.M., Kam, K., Yang, H., Fortin, D.L., Hua, Z., Nicoll, R.A., and Edwards, R.H. (2006). Distinct endocytic pathways control the rate and extent of synaptic vesicle protein recycling. Neuron 51: 71–84, https://doi.org/10.1016/j.neuron.2006.05.027.Search in Google Scholar PubMed
Walther, K., Diril, M.K., Jung, N., and Haucke, V. (2004). Functional dissection of the interactions of stonin 2 with the adaptor complex AP-2 and synaptotagmin. Proc. Natl. Acad. Sci. U.S.A. 101: 964–969, https://doi.org/10.1073/pnas.0307862100.Search in Google Scholar PubMed PubMed Central
Watanabe, S., Rost, B.R., Camacho-Pérez, M., Davis, M.W., Söhl-Kielczynski, B., Rosenmund, C., and Jorgensen, E.M. (2013). Ultrafast endocytosis at mouse hippocampal synapses. Nature 504: 242–247, https://doi.org/10.1038/nature12809.Search in Google Scholar PubMed PubMed Central
Watanabe, S., Trimbuch, T., Camacho-Pérez, M., Rost, B.R., Brokowski, B., Söhl-Kielczynski, B., Felies, A., Davis, M.W., Rosenmund, C., and Jorgensen, E.M. (2014). Clathrin regenerates synaptic vesicles from endosomes. Nature 515: 228–233, https://doi.org/10.1038/nature13846.Search in Google Scholar PubMed PubMed Central
Wienisch, M. and Klingauf, J. (2006). Vesicular proteins exocytosed and subsequently retrieved by compensatory endocytosis are nonidentical. Nat. Neurosci. 9: 1019–1027, https://doi.org/10.1038/nn1739.Search in Google Scholar PubMed
Willig, K.I., Rizzoli, S.O., Westphal, V., Jahn, R., and Hell, S.W. (2006). STED microscopy reveals that synaptotagmin remains clustered after synaptic vesicle exocytosis. Nature 440: 935–939, https://doi.org/10.1038/nature04592.Search in Google Scholar PubMed
Willy, N.M., Colombo, F., Huber, S., Smith, A.C., Norton, E.G., Kural, C., and Cocucci, E. (2021a). CALM supports clathrin-coated vesicle completion upon membrane tension increase. Proc. Natl. Acad. Sci. U.S.A. 118: e2010438118.10.1073/pnas.2010438118Search in Google Scholar PubMed PubMed Central
Willy, N.M., Ferguson, J.P., Akatay, A., Huber, S., Djakbarova, U., Silahli, S., Cakez, C., Hasan, F., Chang, H.C., Travesset, A., et al.. (2021b). De novo endocytic clathrin coats develop curvature at early stages of their formation. Dev. Cell 56: 3146–3159.e5, https://doi.org/10.1016/j.devcel.2021.10.019.Search in Google Scholar PubMed
Wu, L.G. and Betz, W.J. (1996). Nerve activity but not intracellular calcium determines the time course of endocytosis at the frog neuromuscular junction. Neuron 17: 769–779, https://doi.org/10.1016/s0896-6273(00)80208-1.Search in Google Scholar PubMed
Wu, X.-S., McNeil, B.D., Xu, J., Fan, J., Xue, L., Melicoff, E., Adachi, R., Bai, L., and Wu, L.-G. (2009). Ca(2+) and calmodulin initiate all forms of endocytosis during depolarization at a nerve terminal. Nat. Neurosci. 12: 1003–1010, https://doi.org/10.1038/nn.2355.Search in Google Scholar PubMed PubMed Central
Wu, X.-S., Elias, S., Liu, H., Heureaux, J., Wen, P.J., Liu, A.P., Kozlov, M.M., and Wu, L.-G. (2017). Membrane tension inhibits rapid and slow endocytosis in secretory cells. Biophys. J. 113: 2406–2414, https://doi.org/10.1016/j.bpj.2017.09.035.Search in Google Scholar PubMed PubMed Central
Yim, Y.-I., Scarselletta, S., Zang, F., Wu, X., Lee, D.-W., Kang, Y.-S., Eisenberg, E., and Greene, L.E. (2005). Exchange of clathrin, AP2 and epsin on clathrin-coated pits in permeabilized tissue culture cells. J. Cell Sci. 118: 2405–2413, https://doi.org/10.1242/jcs.02356.Search in Google Scholar PubMed
Yim, Y.-I., Sun, T., Wu, L.-G., Raimondi, A., de Camilli, P., Eisenberg, E., and Greene, L.E. (2010). Endocytosis and clathrin-uncoating defects at synapses of auxilin knockout mice. Proc. Natl. Acad. Sci. U.S.A. 107: 4412–4417, https://doi.org/10.1073/pnas.1000738107.Search in Google Scholar PubMed PubMed Central
Yong, X.L.H., Cousin, M.A., and Anggono, V. (2020). PICK1 controls activity-dependent synaptic vesicle cargo retrieval. Cell Rep. 33: 108312, https://doi.org/10.1016/j.celrep.2020.108312.Search in Google Scholar PubMed
Yu, Y., Chu, P.-Y., Bowser, D.N., Keating, D.J., Dubach, D., Harper, I., Tkalcevic, J., Finkelstein, D.I., and Pritchard, M.A. (2008). Mice deficient for the chromosome 21 ortholog Itsn1 exhibit vesicle-trafficking abnormalities. Hum. Mol. Genet. 17: 3281–3290, https://doi.org/10.1093/hmg/ddn224.Search in Google Scholar PubMed
Zeno, W.F., Hochfelder, J.B., Thatte, A.S., Wang, L., Gadok, A.K., Hayden, C.C., Lafer, E.M., and Stachowiak, J.C. (2021). Clathrin senses membrane curvature. Biophys. J. 120: 818–828, https://doi.org/10.1016/j.bpj.2020.11.324.Search in Google Scholar
Zhang, Q., Li, Y., and Tsien, R.W. (2009). The dynamic control of kiss-and-run and vesicular reuse probed with single nanoparticles. Science 323: 1448–1453, https://doi.org/10.1126/science.1167373.Search in Google Scholar PubMed PubMed Central
Zhao, W.-D., Hamid, E., Shin, W., Wen, P.J., Krystofiak, E.S., Villarreal, S.A., Chiang, H.-C., Kachar, B., and Wu, L.-G. (2016). Hemi-fused structure mediates and controls fusion and fission in live cells. Nature 534: 548–552, https://doi.org/10.1038/nature18598.Search in Google Scholar PubMed PubMed Central
© 2023 Walter de Gruyter GmbH, Berlin/Boston
Articles in the same Issue
- Frontmatter
- Highlight: Physiology and Dynamics of Cellular Microcompartments
- Highlight: on the past and the future of cellular microcompartments
- Nuclear redox processes in land plant development and stress adaptation
- The readily retrievable pool of synaptic vesicles
- Loss of respiratory complex I subunit NDUFB10 affects complex I assembly and supercomplex formation
- Modulation of self-organizing circuits at deforming membranes by intracellular and extracellular factors
- Computational resolution in single molecule localization – impact of noise level and emitter density
- Setting up a data management infrastructure for bioimaging
- Molecular insights into endolysosomal microcompartment formation and maintenance
- The role of lysosomes in lipid homeostasis
- Membrane damage and repair: a thin line between life and death
- Neuronal stress granules as dynamic microcompartments: current concepts and open questions
- Molecular determinants of protein half-life in chloroplasts with focus on the Clp protease system
- Neprilysin 4: an essential peptidase with multifaceted physiological relevance
- Determinants of synergistic cell-cell interactions in bacteria
- Drosophila collagens in specialised extracellular matrices
Articles in the same Issue
- Frontmatter
- Highlight: Physiology and Dynamics of Cellular Microcompartments
- Highlight: on the past and the future of cellular microcompartments
- Nuclear redox processes in land plant development and stress adaptation
- The readily retrievable pool of synaptic vesicles
- Loss of respiratory complex I subunit NDUFB10 affects complex I assembly and supercomplex formation
- Modulation of self-organizing circuits at deforming membranes by intracellular and extracellular factors
- Computational resolution in single molecule localization – impact of noise level and emitter density
- Setting up a data management infrastructure for bioimaging
- Molecular insights into endolysosomal microcompartment formation and maintenance
- The role of lysosomes in lipid homeostasis
- Membrane damage and repair: a thin line between life and death
- Neuronal stress granules as dynamic microcompartments: current concepts and open questions
- Molecular determinants of protein half-life in chloroplasts with focus on the Clp protease system
- Neprilysin 4: an essential peptidase with multifaceted physiological relevance
- Determinants of synergistic cell-cell interactions in bacteria
- Drosophila collagens in specialised extracellular matrices