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

Nature Neuroscience

Volumn 12, Issue 8, 2009, Pages 1003-1010

  Wu, Xin Sheng ^a   McNeil, Benjamin D ^a   Xu, Jianhua ^a   Fan, Junmei ^a   Xue, Lei ^a   Melicoff, Ernestina ^b   Adachi, Roberto ^b   Bai, Li ^a   Wu, Ling Gang ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALMIDAZOLIUM; CALMODULIN; CLATHRIN;

ARTICLE; CALCIUM TRANSPORT; DEPOLARIZATION; ENDOCYTOSIS; EXOCYTOSIS; EXTRACELLULAR CALCIUM; MEMBRANE VESICLE; NERVE ENDING; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; SYNAPTIC TRANSMISSION;

ACTION POTENTIALS; ANIMALS; CALCIUM; CALCIUM SIGNALING; CALMODULIN; CENTRAL NERVOUS SYSTEM; ENDOCYTOSIS; EXOCYTOSIS; MICE; MICE, KNOCKOUT; PRESYNAPTIC TERMINALS; RATS; RATS, WISTAR; SYNAPTIC TRANSMISSION; TIME FACTORS;

EID: 68149171755     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn.2355     Document Type: Article

References (50)

1. 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).
2. von Gersdorff, H. & Matthews, G. Inhibition of endocytosis by elevated internal calcium in a synaptic terminal. Nature 370, 652-655 (1994).
3. Sankaranarayanan, S. & Ryan, T.A. Calcium accelerates endocytosis of vSNAREs at hippocampal synapses. Nat. Neurosci. 4, 129-136 (2001).
4. 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).
5. 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).
6. 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).
7. 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).
8. 2+, GTP, and dynamin, but not clathrin. Proc. Natl. Acad. Sci. USA 92, 8328-8332 (1995).
9. 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).
10. 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).
11. 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).
12. 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).
13. 2+-stimulated exocytosis in single pituitary cells. J. Cell Biol. 124, 667-675 (1994).
14. 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).
15. Gandhi, S.P. & Stevens, C.F. Three modes of synaptic vesicular recycling revealed by single-vesicle imaging. Nature 423, 607-613 (2003).
16. Smith, C. & Neher, E. Multiple forms of endocytosis in bovine adrenal chromaffin cells. J. Cell Biol. 139, 885-894 (1997).
17. 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).
18. 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).
19. 2+-dependent recycling of synaptic vesicles at the frog neuromuscular junction. J. Cell Biol. 87, 297-303 (1980).
20. Henkel, A.W. & Betz, W.J. Monitoring of black widow spider venom (BWSV) induced exoand endocytosis in living frog motor nerve terminals with FM1-43. Neuropharmacology 34, 1397-1406 (1995).
21. 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).
22. Marks, B. & McMahon, H.T. Calcium triggers calcineurin-dependent synaptic vesicle recycling in mammalian nerve terminals. Curr. Biol. 8, 740-749 (1998).
23. 2+does not support synaptic vesicle retrieval in rat cerebrocortical synaptosomes. Neurosci. Lett. 253, 1-4 (1998).
24. 2+-triggered synaptic vesicle exocytosis and clathrin-mediated endocytosis at a central synapse. Neuron 21, 607-616 (1998).
25. Balaji, J., Armbruster, M. & Ryan, T.A. Calcium control of endocytic capacity at a CNS synapse. J. Neurosci. 28, 6742-6749 (2008).
26. von Gersdorff, H. & Borst, J.G. Short-term plasticity at the calyx of held. Nat. Rev. Neurosci. 3, 53-64 (2002).
27. Yamashita, T., Hige, T. & Takahashi, T. Vesicle endocytosis requires dynamin-dependent GTP hydrolysis at a fast CNS synapse. Science 307, 124-127 (2005).
28. Xu, J. et al. GTP-independent rapid and slow endocytosis at a central synapse. Nat. Neurosci. 11, 45-53 (2008).
29. Wu, X.S. et al. The origin of quantal size variation: vesicular glutamate concentration plays a significant role. J. Neurosci. 27, 3046-3056 (2007).
30. 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).
31. 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).
32. 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).
33. 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).
34. Neher, E. & Sakaba, T. Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 59, 861-872 (2008).
35. Sun, J. et al. A dual-Ca2+-sensor model for neurotransmitter release in a central synapse. Nature 450, 676-682 (2007).
36. 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).
37. Borst, J.G.G. & Sakmann, B. Calcium influx and transmitter release in a fast CNS synapse. Nature 383, 431-434 (1996).
38. 2+ channel. Cell 133, 1228-1240 (2008).
39. Kopp-Scheinpflug, C., Tolnai, S., Malmierca, M.S. & Rubsamen, R. The medial nucleus of the trapezoid body: comparative physiology. Neuroscience 154, 160-170 (2008).
40. Malgaroli, A. et al. Presynaptic component of long-term potentiation visualized at individual hippocampal synapses. Science 268, 1624-1628 (1995).
41. Murthy, V.N. & Stevens, C.F. Reversal of synaptic vesicle docking at central synapses. Nat. Neurosci. 2, 503-507 (1999).
42. Ryan, T.A., Reuter, H. & Smith, S.J. Optical detection of a quantal presynaptic membrane turnover. Nature 388, 478-482 (1997).
43. 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).
44. Rizzoli, S.O. & Betz, W.J. The structural organization of the readily releasable pool of synaptic vesicles. Science 303, 2037-2039 (2004).
45. Nucifora, P.G. & Fox, A.P. Barium triggers rapid endocytosis in calf adrenal chromaffin cells. J. Physiol. (Lond.) 508, 483-494 (1998).
46. 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).
47. 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).
48. 2+sensors for fast release that specify distinct presynaptic properties in subsets of neurons. Neuron 54, 567-581 (2007).
49. Augustine, G.J. & Neher, E. Calcium requirements for secretion in bovine chromaffin cells. J. Physiol. (Lond.) 450, 247-271 (1992).
50. 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).