Ca2+ and calmodulin initiate all forms of endocytosis during depolarization at a nerve terminal

Wu, L.G., Ryan, T.A. & Lagnado, L. Modes of vesicle retrieval at ribbon synapses, calyx-type synapses and small central synapses. J. Neurosci. 27, 11793–11802 (2007).

von Gersdorff, H. & Matthews, G. Inhibition of endocytosis by elevated internal calcium in a synaptic terminal. Nature 370, 652–655 (1994).

Sankaranarayanan, S. & Ryan, T.A. Calcium accelerates endocytosis of vSNAREs at hippocampal synapses. Nat. Neurosci. 4, 129–136 (2001).

Neves, G., Gomis, A. & Lagnado, L. Calcium influx selects the fast mode of endocytosis in the synaptic terminal of retinal bipolar cells. Proc. Natl. Acad. Sci. USA 98, 15282–15287 (2001).

Poskanzer, K.E., Fetter, R.D. & Davis, G.W. Discrete residues in the c(2)b domain of synaptotagmin I independently specify endocytic rate and synaptic vesicle size. Neuron 50, 49–62 (2006).

Wu, W., Xu, J., Wu, X.S. & Wu, L.G. Activity-dependent acceleration of endocytosis at a central synapse. J. Neurosci. 25, 11676–11683 (2005).

Wu, L.G. & Betz, W.J. Nerve activity, but not intracellular calcium, determines the time course of endocytosis at the frog neuromuscular junction. Neuron 17, 769–779 (1996).

Artalejo, C.R., Henley, J.R., McNiven, M.A. & Palfrey, H.C. Rapic endocytosis coupled to exocytosis in adrenal chromaffin cells involves Ca2+, GTP, and dynamin, but not clathrin. Proc. Natl. Acad. Sci. USA 92, 8328–8332 (1995).

Granseth, B., Odermatt, B., Royle, S.J. & Lagnado, L. Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses. Neuron 51, 773–786 (2006).

Jockusch, W.J., Praefcke, G.J., McMahon, H.T. & Lagnado, L. Clathrin-dependent and clathrin-independent retrieval of synaptic vesicles in retinal bipolar cells. Neuron 46, 869–878 (2005).

Richards, D.A., Guatimosim, C. & Betz, W.J. Two endocytic recycling routes selectively fill two vesicle pools in frog motor nerve terminals. Neuron 27, 551–559 (2000).

Holt, M., Cooke, A., Wu, M.M. & Lagnado, L. Bulk membrane retrieval in the synaptic terminal of retinal bipolar cells. J. Neurosci. 23, 1329–1339 (2003).

Thomas, P., Lee, A.K., Wong, J.G. & Almers, W. A triggered mechanism retrieves membrane in seconds after Ca2+-stimulated exocytosis in single pituitary cells. J. Cell Biol. 124, 667–675 (1994).

Renden, R. & von Gersdorff, H. Synaptic vesicle endocytosis at a CNS nerve terminal: faster kinetics at physiological temperatures and increased endocytotic capacity during maturation. J. Neurophysiol. 98, 3349–3359 (2007).

Gandhi, S.P. & Stevens, C.F. Three modes of synaptic vesicular recycling revealed by single-vesicle imaging. Nature 423, 607–613 (2003).

Smith, C. & Neher, E. Multiple forms of endocytosis in bovine adrenal chromaffin cells. J. Cell Biol. 139, 885–894 (1997).

Balaji, J. & Ryan, T.A. Single-vesicle imaging reveals that synaptic vesicle exocytosis and endocytosis are coupled by a single stochastic mode. Proc. Natl. Acad. Sci. USA 104, 20576–20581 (2007).

Beutner, D., Voets, T., Neher, E. & Moser, T. Calcium dependence of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse. Neuron 29, 681–690 (2001).

Ceccarelli, B. & Hurlbut, W.P. Ca2+-dependent recycling of synaptic vesicles at the frog neuromuscular junction. J. Cell Biol. 87, 297–303 (1980).

Henkel, A.W. & Betz, W.J. Monitoring of black widow spider venom (BWSV) induced exo- and endocytosis in living frog motor nerve terminals with FM1–43. Neuropharmacology 34, 1397–1406 (1995).

Ramaswami, M., Krishnan, K.S. & Kelly, R.B. Intermediates in synaptic vesicle recycling revealed by optical imaging of Drosophila neuromuscular junctions. Neuron 13, 363–375 (1994).

Marks, B. & McMahon, H.T. Calcium triggers calcineurin-dependent synaptic vesicle recycling in mammalian nerve terminals. Curr. Biol. 8, 740–749 (1998).

Cousin, M.A. & Robinson, P.J. Ba2+ does not support synaptic vesicle retrieval in rat cerebrocortical synaptosomes. Neurosci. Lett. 253, 1–4 (1998).

Gad, H., Low, P., Zotova, E., Brodin, L. & Shupliakov, O. Dissociation between Ca2+-triggered synaptic vesicle exocytosis and clathrin-mediated endocytosis at a central synapse. Neuron 21, 607–616 (1998).

Balaji, J., Armbruster, M. & Ryan, T.A. Calcium control of endocytic capacity at a CNS synapse. J. Neurosci. 28, 6742–6749 (2008).

von Gersdorff, H. & Borst, J.G. Short-term plasticity at the calyx of held. Nat. Rev. Neurosci. 3, 53–64 (2002).

Yamashita, T., Hige, T. & Takahashi, T. Vesicle endocytosis requires dynamin-dependent GTP hydrolysis at a fast CNS synapse. Science 307, 124–127 (2005).

Xu, J. et al. GTP-independent rapid and slow endocytosis at a central synapse. Nat. Neurosci. 11, 45–53 (2008).

Wu, X.S. et al. The origin of quantal size variation: vesicular glutamate concentration plays a significant role. J. Neurosci. 27, 3046–3056 (2007).

Sätzler, K. et al. Three-dimensional reconstruction of a calyx of Held and its postsynaptic principal neuron in the medial nucleus of the trapezoid body. J. Neurosci. 22, 10567–10579 (2002).

Kushmerick, C., Renden, R. & von Gersdorff, H. Physiological temperatures reduce the rate of vesicle pool depletion and short-term depression via an acceleration of vesicle recruitment. J. Neurosci. 26, 1366–1377 (2006).

Wu, W. & Wu, L.G. Rapid bulk endocytosis and its kinetics of fission pore closure at a central synapse. Proc. Natl. Acad. Sci. USA 104, 10234–10239 (2007).

Artalejo, C.R., Elhamdani, A. & Palfrey, H.C. Calmodulin is the divalent cation receptor for rapid endocytosis, but not exocytosis, in adrenal chromaffin cells. Neuron 16, 195–205 (1996).

Neher, E. & Sakaba, T. Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 59, 861–872 (2008).

Sun, J. et al. A dual-Ca2+-sensor model for neurotransmitter release in a central synapse. Nature 450, 676–682 (2007).

Xu, J. & Wu, L.G. The decrease in the presynaptic calcium current is a major cause of short-term depression at a calyx-type synapse. Neuron 46, 633–645 (2005).

Borst, J.G.G. & Sakmann, B. Calcium influx and transmitter release in a fast CNS synapse. Nature 383, 431–434 (1996).

Tadross, M.R., Dick, I.E. & Yue, D.T. Mechanism of local and global Ca2+ sensing by calmodulin in complex with a Ca2+ channel. Cell 133, 1228–1240 (2008).

Kopp-Scheinpflug, C., Tolnai, S., Malmierca, M.S. & Rubsamen, R. The medial nucleus of the trapezoid body: comparative physiology. Neuroscience 154, 160–170 (2008).

Malgaroli, A. et al. Presynaptic component of long-term potentiation visualized at individual hippocampal synapses. Science 268, 1624–1628 (1995).

Murthy, V.N. & Stevens, C.F. Reversal of synaptic vesicle docking at central synapses. Nat. Neurosci. 2, 503–507 (1999).

Ryan, T.A., Reuter, H. & Smith, S.J. Optical detection of a quantal presynaptic membrane turnover. Nature 388, 478–482 (1997).

Pyle, J.L., Kavalali, E.T., Piedras-Renteria, E.S. & Tsien, R.W. Rapid reuse of readily releasable pool vesicles at hippocampal synapses. Neuron 28, 221–231 (2000).

Rizzoli, S.O. & Betz, W.J. The structural organization of the readily releasable pool of synaptic vesicles. Science 303, 2037–2039 (2004).

Nucifora, P.G. & Fox, A.P. Barium triggers rapid endocytosis in calf adrenal chromaffin cells. J. Physiol. (Lond.) 508, 483–494 (1998).

Clayton, E.L., Evans, G.J. & Cousin, M.A. Activity-dependent control of bulk endocytosis by protein dephosphorylation in central nerve terminals. J. Physiol. (Lond.) 585, 687–691 (2007).

Nicholson-Tomishima, K. & Ryan, T.A. Kinetic efficiency of endocytosis at mammalian CNS synapses requires synaptotagmin I. Proc. Natl. Acad. Sci. USA 101, 16648–16652 (2004).

Xu, J., Mashimo, T. & Sudhof, T.C. Synaptotagmin-1, -2 and -9: Ca2+ sensors for fast release that specify distinct presynaptic properties in subsets of neurons. Neuron 54, 567–581 (2007).

Augustine, G.J. & Neher, E. Calcium requirements for secretion in bovine chromaffin cells. J. Physiol. (Lond.) 450, 247–271 (1992).

Sankaranarayanan, S. & Ryan, T.A. Real-time measurements of vesicle-SNARE recycling in synapses of the central nervous system. Nat. Cell Biol. 2, 197–204 (2000).