The Coupling between Synaptic Vesicles and Ca2+ Channels Determines Fast Neurotransmitter Release

Neuron

Volumn 53, Issue 4, 2007, Pages 563-575

  Wadel, Kristian ^a   Neher, Erwin ^a   Sakaba, Takeshi ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

CELLBIO; MOLNEURO; SYSNEURO

Indexed keywords

CALCIUM CHANNEL;

ACTION POTENTIAL; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; DEPLETION; ELECTROPHYSIOLOGY; NEUROTRANSMITTER RELEASE; NONHUMAN; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; SYNAPSE VESICLE;

ANIMALS; ANIMALS, NEWBORN; BENZOTHIADIAZINES; BRAIN STEM; CALCIUM; CALCIUM CHANNELS; DIPEPTIDES; ELECTRIC STIMULATION; EXCITATORY AMINO ACID AGENTS; LASERS; MODELS, BIOLOGICAL; NEURONS; PATCH-CLAMP TECHNIQUES; PHOTOLYSIS; PRESYNAPTIC TERMINALS; R-SNARE PROTEINS; RATS; SYNAPSES; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES; TETANUS TOXIN; TIME FACTORS;

EID: 33846785411     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2007.01.021     Document Type: Article

References (63)

1. Adler E.M., Augustine G.J., Duffy S.N., and Charlton M.P. Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse. J. Neurosci. 11 (1991) 1496-1507
2. Augustin I., Rosenmund C., Südhof T.C., and Brose N. Munc13-1 is essential for fusion competence of glutamatergic synaptic vesicles. Nature 400 (1999) 457-461
3. Bollmann J.H., Sakmann B., and Borst J.G.G. Calcium sensitivity of glutamate release in a calyx-type terminal. Science 289 (2000) 953-957
4. 2+ signal. Nat. Neurosci. 8 (2005) 426-434
5. Borst J.G.G., and Sakmann B. Calcium influx and transmitter release in a fast CNS synapse. Nature 383 (1996) 431-434
6. Calakos N., and Scheller R. Vesicle-associated membrane protein and synaptophysin are associated on the synaptic vesicle. J. Biol. Chem. 269 (1994) 24534-24537
7. 2+ channelopathy. Neuron 43 (2005) 387-400
8. Cornille F., Deloye F., Fournie-Zaluski M.C., Roques B.P., and Poulain B. Inhibition of neurotransmitter release by synthetic proline-rich peptide shows that the N-terminal domain of vesicle-associated membrane protein/synaptobrevin is critical for neuro-exocytsosis. J. Biol. Chem. 270 (1995) 16825-16832
9. Dittman J.S., and Regehr W.G. Calcium dependence and recovery kinetics of presynaptic depression at the climbing fiber to purkinje cell synapse. J. Neurosci. 18 (1998) 6147-6162
10. Dobrunz L.E., Huang E.P., and Stevens C.F. Very short-term plasticity in hippocampal synapses. Proc. Natl. Acad. Sci. USA 94 (1997) 14843-14847
11. Escobar A.L., Velez P., Kin A.M., Cituento F., Fill M., and Vergara J.L. Kinetic properties of DM-Nitrophen and calcium indicators; rapid transient response to flash photolysis. Pflugers Arch. 434 (1997) 615-631
12. Fedchyshyn M.J., and Wang L.Y. Developmental transformation of the release modality at the calyx of held synapse. J. Neurosci. 25 (2005) 4131-4140
13. 2+-binding proteins calretinin and parvalbumin at the calyx of Held of rats and mice. Eur. J. Neurosci. 20 (2004) 1473-1482
14. Foster K.A., and Regehr W.G. Variance-mean analysis in the presence of a rapid antagonist indicates vesicle depletion underlies depression at the climbing fiber synapse. Neuron 43 (2004) 119-131
15. 2+ sensor for neurotransmitter release at a central synapse. Cell 79 (1994) 717-727
16. Goda Y., and Stevens C.F. Two components of transmitter release at a central synapse. Proc. Natl. Acad. Sci. USA 91 (1994) 12942-12946
17. Hallermann S., Pawlu C., Jonas P., and Heckmann M. A large pool of releasable vesicles in a cortical glutamatergic synapse. Proc. Natl. Acad. Sci. USA 100 (2003) 8975-8980
18. Hefft S., and Jonas P. Asynchronous GABA release generates long-lasting inhibition at a principal interneuron-principal neuron synapse. Nat. Neurosci. 8 (2005) 1319-1328
19. 2+-triggered exocytosis in presynaptic terminals. Neuron 17 (1996) 501-512
20. Ishikawa T., Sahara Y., and Takahashi T. A single packet of transmitter does not saturate postsynaptic glutamate receptors. Neuron 34 (2002) 613-621
21. Kandler K., and Friauf E. Prenatal and postnatal-development of efferent connections of the cochlear nucleus in the rat. J. Comp. Neurol. 328 (1993) 161-184
22. Katz B. The Release of Neural Transmitter Substances (1969), Liverpool University Press, Liverpool, UK
23. 2+ channel clustering, and vesicle release. Science 312 (2006) 1051-1054
24. Koike-Tani M., Saitoh N., and Takahashi T. Mechanisms underlying developmental speeding in AMPA-EPSC decay time at the calyx of Held. J. Neurosci. 25 (2005) 199-207
25. Llinas R., Sugimori M., and Silver R.B. Microdomains of high calcium concentration in a presynaptic terminal. Science 256 (1992) 677-679
26. 2+ sensor for vesicle fusion. Nature 435 (2005) 497-501
27. Lu T., and Trussell L.O. Inhibitory transmission mediated by asynchronous transmitter release. Neuron 26 (2000) 683-694
28. McMahon H.T., Bolshakov V.Y., Janz R., Hammer R.E., Siegelbaum S.A., and Südhof T.C. Synaptophysin, a major synaptic vesicle protein, is not essential for neurotransmitter release. Proc. Natl. Acad. Sci. USA 93 (1996) 4760-4764
29. Meinrenken C.J., Borst J.G.G., and Sakmann B. Calcium secretion coupling at calyx of Held governed by nonuniform channel-vesicle topography. J. Neurosci. 22 (2002) 1648-1667
30. 2+ channels to synaptic vesicle exocytosis. Nature 423 (2003) 939-948
31. 2+ channels. Neuron 17 (1996) 781-788
32. Moulder K.L., and Mennerick S. Reluctant vesicles contribute to the total readily releasable pool in glutamatergic hippocampal neurons. J. Neurosci. 25 (2005) 3842-3850
33. Neher E., and Sakaba T. Combining deconvolution and noise analysis for the estimation of transmitter release rates at the calyx of Held. J. Neurosci. 21 (2001) 444-461
34. Neher E., and Sakaba T. Estimating transmitter release rates from postsynaptic current fluctuations. J. Neurosci. 21 (2001) 9638-9654
35. 2+ channel/Syntaxin interaction. J. Neurosci. 17 (1997) 6647-6656
36. Roberts W.M., Jacobs R.A., and Hudspeth A.J. Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells. J. Neurosci. 10 (1990) 3664-3684
37. Rosenmund C., and Stevens C.F. Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16 (1996) 1197-1207
38. 2+ buffers in facilitating and depressing nerve terminals of pyramidal cells in layer 2/3 of the rat neocortex indicates a target cell-specific difference in presynaptic calcium dynamics. J. Physiol. 531 (2001) 807-826
39. Sakaba T. Roles of the fast-releasing and the slowly releasing vesicles in synaptic transmission at the calyx of Held. J. Neurosci. 26 (2006) 5863-5871
40. Sakaba T., and Neher E. Quantitative relationship between transmitter release and calcium current at the calyx of Held synapse. J. Neurosci. 21 (2001) 462-476
41. Sakaba T., and Neher E. Calmodulin mediates rapid recruitment of fast-releasing synaptic vesicles at a calyx-type synapse. Neuron 32 (2001) 1119-1131
42. Sakaba T., and Neher E. Direct modulation of synaptic vesicle priming by GABAB receptor activation at a glutamatergic synapse. Nature 424 (2003) 775-778
43. Sakaba T., Stein A., Jahn R., and Neher E. Distinct kinetic changes in neurotransmitter release after SNARE protein cleavage. Science 309 (2005) 491-494
44. Sara Y., Virmani T., Deak F., Liu X.R., and Kavalali E.T. An isolated pool of vesicles recycles at rest and drives spontaneous neurotransmission. Neuron 45 (2005) 563-573
45. Sätzler K., Sohl L.F., Bollmann J.H., Borst J.G.G., Frotscher M., Sakmann B., and Lübke J.H.R. Three-dimensional reconstruction of a calyx of Held and its postsynaptic principal neuron in the medial nucleus of the trapezoid body. J. Neurosci. 22 (2002) 10567-10579
46. Scheuss V., Schneggenburger R., and Neher E. Separation of presynaptic and postsynaptic contributions to depression by covariance analysis of successive EPSCs at the calyx of Held synapse. J. Neurosci. 22 (2002) 728-739
47. Schneggenburger R. Ca2+ Uncaging in Nerve Terminals. In: Yuste R., and Konnerth A. (Eds). Imaging in Neuroscience and Development (2005), CSHL Press, Woodbury, NY 415-419
48. Schneggenburger R., and Neher E. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406 (2000) 889-893
49. Schneggenburger R., Meyer A., and Neher E. Released fraction and total size of a pool of immediately available transmitter quanta at a calyx synapse. Neuron 23 (1999) 399-409
50. Schneggenburger R., Sakaba T., and Neher E. Vesicle pools and short-term synaptic depression: lessons from a large synapse. Trends Neurosci. 25 (2002) 206-212
51. Silver R.A., Momiyama A., and Cull-Candy S.G. Locus of frequency-dependent depression identified with multiple-probability fluctuation analysis at rat climbing fibre-Purkinje cell synapses. J. Physiol. 510 (1998) 881-902
52. Smith C., Moser T., Xu T., and Neher E. Cytosolic Ca2+ acts by two separate pathways to modulate the supply of release-competent vesicles in chromaffin cells. Neuron 20 (1998) 1243-1253
53. Stevens C.F. Neurotransmitter release at central synapses. Neuron 40 (2003) 381-388
54. Stevens C.F., and Wesseling J.F. Activity-dependent modulation of the rate at which synaptic vesicles become available to undergo exocytosis. Neuron 21 (1998) 415-424
55. Takahashi T., Forsythe I.D., Tsujimoto T., Barnes-Davies M., and Onodera K. Presynaptic calcium current modulation by a metabotropic glutamate receptor. Science 274 (1996) 594-597
56. Verhage M., Maia A.S., Plomp J.J., Brussaard A.B., Heeroma J.H., Vermeer H., Toonen R.F., Hammer R.E., van den Berg T.K., Missler M., et al. Synaptic assembly of the brain in the absence of neurotransmitter secretion. Science 287 (2000) 864-869
57. von Gersdorff H., and Borst J.G.G. Short-term plasticity at the calyx of Held. Nat. Rev. Neurosci. 3 (2002) 53-64
58. Wadiche J.I., and Jahr C.E. Multivesicular release at climbing fiber-Purkinje cell synapses. Neuron 32 (2001) 301-313
59. Wang L.Y., and Kaczmarek L.K. High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature 394 (1998) 384-388
60. Wu L.G., and Borst J.G.G. The reduced release probability of releasable vesicles during recovery from short-term synaptic depression. Neuron 23 (1999) 821-832
61. Xu-Friedmann M., and Regehr W.G. Probing fundamental aspects of synaptic transmission with strontium. J. Neurosci. 20 (2000) 4414-4422
62. Zucker R.S. Exocytosis: a molecular and physiological perspective. Neuron 17 (1996) 1049-1055
63. Zucker R.S., and Regehr W.G. Short-term synaptic plasticity. Annu. Rev. Physiol. 64 (2002) 355-405