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The readily retrievable pool of synaptic vesicles

  • Sai Krishnan ORCID logo und Jürgen Klingauf EMAIL logo
Veröffentlicht/Copyright: 6. März 2023
Biological Chemistry
Aus der Zeitschrift Biological Chemistry Band 404 Heft 5

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.

Keywords: clathrin; exocytosis: endocytosis; RRetP; RRP; synapse
Corresponding author: Jürgen Klingauf, Institute of Medical Physics and Biophysics, University of Münster, Robert-Koch Strasse 31, D-48149, Münster, Germany; and Center for Soft Nanoscience, Busso-Peus Strasse 10, D-48149, Münster, Germany, E-mail:

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).

  1. Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.

  2. Research funding: This work was financially supported by the Deutsche Forschungsgemeinschaft (SFB 1348 A02, SFB 944 P5).

  3. 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.03648Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.2010438118Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche 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.Suche in Google Scholar PubMed PubMed Central

Received: 2022-09-29
Accepted: 2023-02-16
Published Online: 2023-03-06
Published in Print: 2023-04-25

© 2023 Walter de Gruyter GmbH, Berlin/Boston

Artikel in diesem Heft

  1. Frontmatter
  2. Highlight: Physiology and Dynamics of Cellular Microcompartments
  3. Highlight: on the past and the future of cellular microcompartments
  4. Nuclear redox processes in land plant development and stress adaptation
  5. The readily retrievable pool of synaptic vesicles
  6. Loss of respiratory complex I subunit NDUFB10 affects complex I assembly and supercomplex formation
  7. Modulation of self-organizing circuits at deforming membranes by intracellular and extracellular factors
  8. Computational resolution in single molecule localization – impact of noise level and emitter density
  9. Setting up a data management infrastructure for bioimaging
  10. Molecular insights into endolysosomal microcompartment formation and maintenance
  11. The role of lysosomes in lipid homeostasis
  12. Membrane damage and repair: a thin line between life and death
  13. Neuronal stress granules as dynamic microcompartments: current concepts and open questions
  14. Molecular determinants of protein half-life in chloroplasts with focus on the Clp protease system
  15. Neprilysin 4: an essential peptidase with multifaceted physiological relevance
  16. Determinants of synergistic cell-cell interactions in bacteria
  17. Drosophila collagens in specialised extracellular matrices
https://doi.org/10.1515/hsz-2022-0298
Schlagwörter für diesen Artikel
clathrin; exocytosis: endocytosis; RRetP; RRP; synapse

Artikel in diesem Heft

  1. Frontmatter
  2. Highlight: Physiology and Dynamics of Cellular Microcompartments
  3. Highlight: on the past and the future of cellular microcompartments
  4. Nuclear redox processes in land plant development and stress adaptation
  5. The readily retrievable pool of synaptic vesicles
  6. Loss of respiratory complex I subunit NDUFB10 affects complex I assembly and supercomplex formation
  7. Modulation of self-organizing circuits at deforming membranes by intracellular and extracellular factors
  8. Computational resolution in single molecule localization – impact of noise level and emitter density
  9. Setting up a data management infrastructure for bioimaging
  10. Molecular insights into endolysosomal microcompartment formation and maintenance
  11. The role of lysosomes in lipid homeostasis
  12. Membrane damage and repair: a thin line between life and death
  13. Neuronal stress granules as dynamic microcompartments: current concepts and open questions
  14. Molecular determinants of protein half-life in chloroplasts with focus on the Clp protease system
  15. Neprilysin 4: an essential peptidase with multifaceted physiological relevance
  16. Determinants of synergistic cell-cell interactions in bacteria
  17. Drosophila collagens in specialised extracellular matrices
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