The Journal of Cell Biology, Vol 133, 1237-1250, Copyright © 1996 by The Rockefeller University Press

ARTICLES

The synaptic vesicle cycle: a single vesicle budding step involving clathrin and dynamin

K Takei, O Mundigl, L Daniell and P De Camilli
Department of Cell Biology, Yale University School of Medicine, New Haven, Connecticut 06510, USA.

Strong evidence implicates clathrin-coated vesicles and endosome-like vacuoles in the reformation of synaptic vesicles after exocytosis, and it is generally assumed that these vacuoles represent a traffic station downstream from clathrin-coated vesicles. To gain insight into the mechanisms of synaptic vesicle budding from endosome-like intermediates, lysed nerve terminals and nerve terminal membrane subfractions were examined by EM after incubations with GTP gamma S. Numerous clathrin-coated budding intermediates that were positive for AP2 and AP180 immunoreactivity and often collared by a dynamin ring were seen. These were present not only on the plasma membrane (Takei, K., P.S. McPherson, S.L.Schmid, and P. De Camilli. 1995. Nature (Lond.). 374:186-190), but also on internal vacuoles. The lumen of these vacuoles retained extracellular tracers and was therefore functionally segregated from the extracellular medium, although narrow connections between their membranes and the plasmalemma were sometimes visible by serial sectioning. Similar observations were made in intact cultured hippocampal neurons exposed to high K+ stimulation. Coated vesicle buds were generally in the same size range of synaptic vesicles and positive for the synaptic vesicle protein synaptotagmin. Based on these results, we suggest that endosome-like intermediates of nerve terminals originate by bulk uptake of the plasma membrane and that clathrin- and dynamin-mediated budding takes place in parallel from the plasmalemma and from these internal membranes. We propose a synaptic vesicle recycling model that involves a single vesicle budding step mediated by clathrin and dynamin.
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• Blagoveshchenskaya, A. D., Hewitt, E. W., Cutler, D. F. (1999). Di-Leucine Signals Mediate Targeting of Tyrosinase and Synaptotagmin to Synaptic-like Microvesicles within PC12 Cells. Mol. Biol. Cell 10: 3979-3990 [Abstract] [Full Text]  
• Augustine, G. J, Burns, M. E, DeBello, W. M, Hilfiker, S., Morgan, J. R, Schweizer, F. E, Tokumaru, H., Umayahara, K. (1999). Proteins involved in synaptic vesicle trafficking. J. Physiol. 520: 33-41 [Abstract] [Full Text]  
• Hao, W., Luo, Z., Zheng, L., Prasad, K., Lafer, E. M. (1999). AP180 and AP-2 Interact Directly in a Complex That Cooperatively Assembles Clathrin. J. Biol. Chem. 274: 22785-22794 [Abstract] [Full Text]  
• Strasser, J. E., Arribas, M., Blagoveshchenskaya, A. D., Cutler, D. F. (1999). Secretagogue-triggered Transfer of Membrane Proteins from Neuroendocrine Secretory Granules to Synaptic-like Microvesicles. Mol. Biol. Cell 10: 2619-2630 [Abstract] [Full Text]  
• Tebar, F., Bohlander, S. K., Sorkin, A. (1999). Clathrin Assembly Lymphoid Myeloid Leukemia (CALM) Protein: Localization in Endocytic-coated Pits, Interactions with Clathrin, and the Impact of Overexpression on Clathrin-mediated Traffic. Mol. Biol. Cell 10: 2687-2702 [Abstract] [Full Text]  
• Fergestad, T., Davis, W. S., Broadie, K. (1999). The Stoned Proteins Regulate Synaptic Vesicle Recycling in the Presynaptic Terminal. J. Neurosci. 19: 5847-5860 [Abstract] [Full Text]  
• Blagoveshchenskaya, A. D., Hewitt, E. W., Cutler, D. F. (1999). A Complex Web of Signal-dependent Trafficking Underlies the Triorganellar Distribution of P-Selectin in Neuroendocrine PC12 Cells. JCB 145: 1419-1433 [Abstract] [Full Text]  
• Arneson, L. S., Kunz, J., Anderson, R. A., Traub, L. M. (1999). Coupled Inositide Phosphorylation and Phospholipase D Activation Initiates Clathrin-coat Assembly on Lysosomes. J. Biol. Chem. 274: 17794-17805 [Abstract] [Full Text]  
• Teng, H., Cole, J. C., Roberts, R. L., Wilkinson, R. S. (1999). Endocytic Active Zones: Hot Spots for Endocytosis in Vertebrate Neuromuscular Terminals. J. Neurosci. 19: 4855-4866 [Abstract] [Full Text]  
• Zakharenko, S., Chang, S., O'Donoghue, M., Popov, S. V. (1999). Neurotransmitter Secretion along Growing Nerve Processes: Comparison with Synaptic Vesicle Exocytosis. JCB 144: 507-518 [Abstract] [Full Text]  
• Shi, G., Faundez, V., Roos, J., Dell'Angelica, E. C., Kelly, R. B. (1998). Neuroendocrine Synaptic Vesicles Are Formed In Vitro by Both Clathrin-dependent and Clathrin-independent Pathways. JCB 143: 947-955 [Abstract] [Full Text]  
• Seaman, M. N.J., Michael McCaffery, J., Emr, S. D. (1998). A Membrane Coat Complex Essential for Endosome-to-Golgi Retrograde Transport in Yeast. JCB 142: 665-681 [Abstract] [Full Text]  
• Calhoun, B. C., Lapierre, L. A., Chew, C. S., Goldenring, J. R. (1998). Rab11a redistributes to apical secretory canaliculus during stimulation of gastric parietal cells. Am. J. Physiol. Cell Physiol. 275: C163-C170 [Abstract] [Full Text]  
• Zhu, Y., Traub, L. M., Kornfeld, S. (1998). ADP-Ribosylation Factor 1 Transiently Activates High-Affinity Adaptor Protein Complex AP-1 Binding Sites On Golgi Membranes. Mol. Biol. Cell 9: 1323-1337 [Abstract] [Full Text]  
• Wendland, B., Emr, S. D. (1998). Pan1p, Yeast eps15, Functions as a Multivalent Adaptor That Coordinates Protein-Protein Interactions Essential for Endocytosis. JCB 141: 71-84 [Abstract] [Full Text]  
• Volchuk, A., Narine, S., Foster, L. J., Grabs, D., De Camilli, P., Klip, A. (1998). Perturbation of Dynamin II with an Amphiphysin SH3 Domain Increases GLUT4 Glucose Transporters at the Plasma Membrane in 3T3-L1 Adipocytes. DYNAMIN II PARTICIPATES IN GLUT4 ENDOCYTOSIS. J. Biol. Chem. 273: 8169-8176 [Abstract] [Full Text]  
• Burns, M.E., Sasaki, T., Takai, Y., Augustine, G.J. (1998). Rabphilin-3A: A Multifunctional Regulator of Synaptic Vesicle Traffic. JGP 111: 243-255 [Abstract] [Full Text]  
• Thoidis, G., Chen, P., Pushkin, A. V., Vallega, G., Leeman, S. E., Fine, R. E., Kandror, K. V. (1998). Two distinct populations of synaptic-like vesicles from rat brain. Proc. Natl. Acad. Sci. USA 95: 183-188 [Abstract] [Full Text]  
• Partoens, P, Slembrouck, D, Quatacker, J, Baudhuin, P, Courtoy, P., De Potter, W. (1998). Retrieved constituents of large dense-cored vesicles and synaptic vesicles intermix in stimulation-induced early endosomes of noradrenergic neurons. J. Cell Sci. 111: 681-689 [Abstract]  
• Mundigl, O., Ochoa, G.-C., David, C., Slepnev, V. I., Kabanov, A., De Camilli, P. (1998). Amphiphysin I Antisense Oligonucleotides Inhibit Neurite Outgrowth in Cultured Hippocampal Neurons. J. Neurosci. 18: 93-103 [Abstract] [Full Text]  
• Daro, E., Sheff, D., Gomez, M., Kreis, T., Mellman, I. (1997). Inhibition of Endosome Function in CHO Cells Bearing a Temperature-sensitive Defect in the Coatomer (COPI) Component {varepsilon}-COP. JCB 139: 1747-1759 [Abstract] [Full Text]  
• Bauerfeind, R., Takei, K., De Camilli, P. (1997). Amphiphysin I Is Associated with Coated Endocytic Intermediates and Undergoes Stimulation-dependent Dephosphorylation in Nerve Terminals. J. Biol. Chem. 272: 30984-30992 [Abstract] [Full Text]  
• Liu, Y., Edwards, R. H. (1997). Differential Localization of Vesicular Acetylcholine and Monoamine Transporters in PC12 Cells but Not CHO Cells. JCB 139: 907-916 [Abstract] [Full Text]  
• Grimes, M. L., Beattie, E., Mobley, W. C. (1997). A signaling organelle containing the nerve growth factor-activated receptor tyrosine kinase, TrkA. Proc. Natl. Acad. Sci. USA 94: 9909-9914 [Abstract] [Full Text]  
• Faundez, V., Horng, J.-T., Kelly, R. B. (1997). ADP Ribosylation Factor 1 Is Required for Synaptic Vesicle Budding in PC12 Cells. JCB 138: 505-515 [Abstract] [Full Text]  
• Prekeris, R., Terrian, D. M. (1997). Brain Myosin V Is a Synaptic Vesicle-associated Motor Protein: Evidence for a Ca2+-dependent Interaction with the Synaptobrevin-Synaptophysin Complex. JCB 137: 1589-1601 [Abstract] [Full Text]  
• Lindgren, C. A., Emery, D. G., Haydon, P. G. (1997). Intracellular Acidification Reversibly Reduces Endocytosis at the Neuromuscular Junction. J. Neurosci. 17: 3074-3084 [Abstract] [Full Text]  
• Schmidt, A., Hannah, M. J., Huttner, W. B. (1997). Synaptic-like Microvesicles of Neuroendocrine Cells Originate from a Novel Compartment That Is Continuous with the Plasma Membrane and Devoid of Transferrin Receptor. JCB 137: 445-458 [Abstract] [Full Text]  
• Hao, W., Tan, Z., Prasad, K., Reddy, K. K., Chen, J., Prestwich, G. D., Falck, J. R., Shears, S. B., Lafer, E. M. (1997). Regulation of AP-3 Function by Inositides. IDENTIFICATION OF PHOSPHATIDYLINOSITOL 3,4,5-TRISPHOSPHATE AS A POTENT LIGAND. J. Biol. Chem. 272: 6393-6398 [Abstract] [Full Text]  
• Urrutia, R., Henley, J. R., Cook, T., McNiven, M. A. (1997). The dynamins: Redundant or distinct functions for an expanding family of related GTPases?. Proc. Natl. Acad. Sci. USA 94: 377-384 [Abstract] [Full Text]  
• Kraszewski, K., Daniell, L., Mundigl, O., De Camilli, P. (1996). Mobility of Synaptic Vesicles in Nerve Endings Monitored by Recovery from Photobleaching of Synaptic Vesicle-Associated Fluorescence. J. Neurosci. 16: 5905-5913 [Abstract] [Full Text]  
• Kim, K.-M., Valenzano, K. J., Robinson, S. R., Yao, W. D., Barak, L. S., Caron, M. G. (2001). Differential Regulation of the Dopamine D2 and D3 Receptors by G Protein-coupled Receptor Kinases and beta -Arrestins. J. Biol. Chem. 276: 37409-37414 [Abstract] [Full Text]  

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