Multiple Roles of Calcium Ions in the Regulation of Neurotransmitter Release

Neuron

Volumn 59, Issue 6, 2008, Pages 861-872

  Neher, Erwin ^a   Sakaba, Takeshi ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; CALCIUM ION;

ACTION POTENTIAL; BINDING SITE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; DATA ANALYSIS; HUMAN; MOLECULAR DOCKING; NERVE CELL PLASTICITY; NEUROTRANSMITTER RELEASE; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ACTION POTENTIALS; ANIMALS; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; EXOCYTOSIS; HUMANS; NEURONAL PLASTICITY; NEUROTRANSMITTER AGENTS; SECOND MESSENGER SYSTEMS; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 52049106127     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2008.08.019     Document Type: Review

References (138)

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. Andrews-Zwilling Y.S., Kawabe H., Reim K., Varoqueaux F., and Brose N. Binding to Rab3A-interacting molecule RIM regulates the presynaptic recruitment of Munc13-1 and ubMunc13-2. J. Biol. Chem. 281 (2006) 19720-19731
3. Atwood H.L., and Karunanithi S. Diversification of synaptic strength: presynaptic elements. Nat. Rev. Neurosci. 3 (2002) 497-516
4. 2+ channels in insulin-secreting mouse pancreatic B cells. Biophys. J. 81 (2001) 3308-3323
5. Betz W.J., and Wu L.G. Synaptic transmission - kinetics of synaptic-vesicle recycling. Curr. Biol. 5 (1995) 1098-1101
6. Betz A., Ashery U., Rickmann M., Augustin I., Neher E., Südhof T.C., Rettig J., and Brose N. Munc13-1 is a presynaptic phorbol ester receptor that enhances neurotransmitter release. Neuron 21 (1998) 123-136
7. Beutner D., Voets T., Neher E., and Moser T. Calcium dependence of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse. Neuron 29 (2001) 681-690
8. 2+ Entry. Science 292 (2001) 293-297
9. Blackmer T., Larsen E.C., Bartleson C., Kowalchyk J.A., Yoon E.J., Preininger A.M., Alford S., Hamm H.E., and Martin T.F.J. G protein beta gamma directly regulates SNARE protein fusion machinery for secretory granule exocytosis. Nat. Neurosci. 8 (2005) 421-425
10. Blasi J., Chapman E.R., Lin E., Bin Z., Yamasaki T., De S., Camilli P., Südhof T.C., Niemann H., and Jahn R. Botulinum neurotoxin-A selectively cleave the synaptic protein SNAP-25. Nature 365 (1993) 160-163
11. 2+ buffer saturation underlies paired pulse facilitation in calbindin-D28k-containing terminals. Neuron 38 (2003) 79-88
12. 2+ signal. Nat. Neurosci. 8 (2005) 426-434
13. 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
14. Borisovska M., Zhao Y., Tsytsyura Y., Glyvuk N., Takamori S., Matti U., Rettig J., Südhof T., and Bruns D. v-SNAREs control exocytosis of vesicles from priming to fusion. EMBO J. 24 (2005) 2114-2126
15. Borst J.G.G., and Sakmann B. Calcium influx and transmitter release in a fast CNS synapse. Nature 383 (1996) 431-434
16. Borst J.G.G., and Sakmann B. Facilitation of presynaptic calcium currents in the rat brainstem. J. Physiol. 513 (1998) 149-155
17. Borst J.G.G., Helmchen F., and Sakmann B. Pre- and postsynaptic whole-cell recordings in the medial nucleus of the trapezoid body of the rat. J. Physiol. 489 (1995) 825-840
18. 2+ sensors promotes fast and efficient transmitter release at a cortical GABAergic synapse. Neuron 57 (2008) 536-545
19. Chen Y.A., and Scheller R.H. SNARE-mediated membrane fusion. Nat. Rev. Mol. Cell Biol. 2 (2001) 98-106
20. Cuttle M.F., Tsujimoto T., Forsythe I.D., and Takahashi T. Facilitation of the presynaptic calcium current at an auditory synapse in rat brainstem. J. Physiol. 512 (1998) 723-729
21. Dickman D.K., Lu Z., Meinertzhagen I.A., and Schwarz T.L. A slowed classical pathway rather than kiss-and-run mediates endocytosis at synapses lacking Synaptojanin and Endophilin. Cell 123 (2005) 521-533
22. DiGregorio D.A., Peskoff A., and Vergara J.L. Measurement of action potential-induced presynaptic calcium domains at a cultured neuromuscular junction. J. Neurosci. 19 (1999) 7846-7859
23. 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
24. Dittman J.S., Kreitzer A.C., and Regehr W.G. Interplay between facilitation, depression, and residual calcium at three presynaptic terminals. J. Neurosci. 20 (2000) 1374-1385
25. Dulubova I., Lou X.L., Lu J., Huryeva I., Alam A., Schneggenburger R., Sudhof T.C., and Rizo J. A Munc13/RIM/Rab3 tripartite complex: from priming to plasticity?. EMBO J. 24 (2005) 2839-2850
26. 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
27. Felmy F., Neher E., and Schneggenburger R. Probing the intracellular calcium sensitivity of transmitter release during synaptic facilitation. Neuron 37 (2003) 801-811
28. Ferguson S.M., Brasnjo G., Hayashi M., Wölfel M., Collesi C., Giovedi S., Raimondi A., Gong L.-W., Ariel P., Paradise S., et al. A selective activity-dependent requirement for Dynamin 1 in synaptic vesicle endocytosis. Science 316 (2007) 570-574
29. Forsythe I.D. Direct patch recording from identified presynaptic terminals mediating glutamatergic EPSCs in the rat CNS, in vitro. J. Physiol. 479 (1994) 381-387
30. Forsythe I.D., Tsujimoto T., Barnes-Davies M., Cuttle M.F., and Takahashi T. Inactivation of presynaptic calcium current contributes to synaptic depression at a fast central synapse. Neuron 20 (1998) 797-807
31. Foster K.A., Kreitzer A.C., and Regehr W.G. Interaction of postsynaptic receptor saturation with presynaptic mechanisms produces a reliable synapse. Neuron 36 (2002) 1115-1126
32. 2+ buffers in axons of cultured Aplysia neurons. Neuron 18 (1997) 473-481
33. Gerachshenko T., Blackmer T., Yoon E.J., Bartleson C., Hamm H.E., and Alford S. G beta gamma acts at the C terminus of SNAP-25 to mediate presynaptic inhibition. Nat. Neurosci. 8 (2005) 597-605
34. Gromada J., Hoy M., Renstrom E., Bokvist K., Eliasson L., Gopel S., and Rorsman P. CaM kinase II-dependent mobilization of secretory granules underlies acetylcholine-induced stimulation of exocytosis in mouse pancreatic B-cells. J. Physiol. 518 (1999) 745-759
35. 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
36. Hamill O.P., Marty A., Neher E., Sakmann B., and Sigworth F.J. Improved patch-clamp techniques for high resolution current recording from cells and cell-free membrane. Pflugers Arch. 391 (1981) 85-100
37. Harata N.C., Aravanis A.M., and Tsien R.W. Kiss-and-run and full-collapse fusion as modes of exo-endocytosis in neurosecretion. J. Neurochem. 97 (2006) 1546-1570
38. Haydon P.G., Henderson E., and Stanley E.F. Localization of individual calcium channels at the release face of a presynaptic nerve terminal. Neuron 13 (1994) 1275-1280
39. He L.M., Wu X.S., Mohan R., and Wu L.G. Two modes of fusion pore opening revealed by cell-attached recordings at a synapse. Nature 444 (2006) 102-105
40. Hefft S., and Jonas P. Asynchronous GABA release generates long-lasting inhibition at a hippocampal interneuron-principal neuron synapse. Nat. Neurosci. 9 (2006) 1388-1396
41. Heidelberger R., Heinemann C., Neher E., and Matthws G. Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 371 (1994) 513-515
42. Helmchen F., Borst J.G.G., and Sakmann B. Calcium dynamics associated with a single action potential in a CNS presynaptic terminal. Biophys. J. 72 (1997) 1458-1471
43. Hermann J., Pecka M., von Gersdorff H., Grothe B., and Klug A. Synaptic transmission at the calyx of Held under in vivo-like activity levels. J. Neurophysiol. 98 (2007) 807-820
44. Hessler N.A., Shirke A.M., and Malinow R. The probability of transmitter release at a mammalian central synapse. Nature 366 (1993) 569-572
45. Hosoi N., Sakaba T., and Neher E. Quantitative analysis of calcium-dependent vesicle recruitment and its functional role at the calyx of Held synapse. J. Neurosci. 27 (2007) 14286-14298
46. 2+-triggered exocytosis in presynaptic terminals. Neuron 17 (1996) 501-512
47. Inchauspe C.G., Martini F.J., Forsythe I.D., and Uchitel O.D. Functional compensation of P/Q by N-type channels blocks short-term plasticity at the calyx of held presynaptic terminal. J. Neurosci. 24 (2004) 10379-10383
48. Illies C., Gromada J., Fiume R., Leibiger B., Yu J., Juhl K., Yang S.N., Barma D.K., Falck J.R., Saiardi A., et al. Requirement of inositol pyrophosphates for full exocytotic capacity in pancreatic beta cells. Science 318 (2007) 1299-1302
49. Ishikawa T., Kaneko M., Shin H.S., and Takahashi T. Presynaptic N-type and P/Q-type Ca2+ channels mediating synaptic transmission at the calyx of held of mice. J. Physiol. 568 (2005) 199-209
50. Iwasaki S., and Takahashi T. Developmental regulation of transmitter release at the calyx of Held in rat auditory brainstem. J. Physiol. 354 (2001) 861-871
51. Jockusch W.J., Speidel D., Sigler A., Sørensen J.B., Varoqueaux F., Rhee J.S., and Brose N. CAPS-1 and CAPS-2 are essential synaptic vesicle priming proteins. Cell 131 (2007) 796-808
52. 2+ sensor/effector complex that controls short-term synaptic plasticity. Cell 118 (2004) 389-401
53. Katz B., and Miledi R. Role of calcium in neuromuscular facilitation. J. Physiol. 195 (1968) 481-492
54. Kavalali E.T. Multiple vesicle recycling pathways in central synapses and their impact on neurotransmission. J. Physiol. 585 (2007) 669-679
55. Kawasaki F., Hazen M., and Ordway R.W. Fast synaptic fatigue in shibire mutants reveals a rapid requirement for dynamin in synaptic vesicle membrane trafficking. Nat. Neurosci. 3 (2000) 859-860
56. 2+-triggered exocytosis. Cell 131 (2007) 351-363
57. Khanna R., Li Q., Schlichter L.C., and Stanley E.F. The transmitter release-site CaV2.2 channel cluster is linked to an endocytosis coat protein complex. Eur. J. Neurosci. 26 (2007) 560-574
58. 2+ clearance at the calyx of Held. J. Neurosci. 25 (2005) 6057-6065
59. 2+ channel clustering, and vesicle release. Science 312 (2006) 1051-1054
60. Klyachko V.A., and Jackson M.B. Capacitance steps and fusion pores of small and large-dense-core vesicles in nerve terminals. Nature 418 (2002) 89-92
61. Koike-Tani M., Kanda T., Saitoh N., Yamashita T., and Takahashi T. Involvement of AMPA receptor desensitization in short-term synaptic depression at the calyx of Held in developing rats. J. Physiol. 568 (2008) 2263-2275
62. Kopp-Scheinpflug C., Lippe W.R., Dörrscheidt G.J., and Rübsamen R. The medial nucleus of the trapezoid body in the gerbil is more than a relay: Comparison of pre- and postsynaptic activity. J. Assoc. Res. Otolaryngol. 4 (2003) 1-23
63. Kreitzer A.C., and Regehr W.G. Modulation of transmission during trains at a cerebellar synapse. J. Neurosci. 20 (2000) 1348-1357
64. Kushmerick C., Renden R., and 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 (2006) 1366-1377
65. Li Z.Y., Burrone J., Tyler W.J., Hartman K.N., Albeanu D.F., and Murthy V.N. Synaptic vesicle recycling studied in transgenic mice expressing synaptopHluorin. Proc. Natl. Acad. Sci. USA 102 (2005) 6131-6136
66. Llinas R., Sugimori M., and Silver R.B. Microdomains of high calcium concentration in a presynaptic terminal. Science 256 (1992) 677-679
67. 2+ sensor for vesicle fusion. Nature 435 (2005) 497-501
68. Lu T., and Trussell L.O. Inhibitory transmission mediated by asynchronous transmitter release. Neuron 26 (2000) 683-694
69. 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
70. Mennerick S., and Matthews G. Ultrafast exocytosis elicited by calcium current in synaptic terminals of retinal bipolar neurons. Neuron 17 (1996) 1241-1249
71. Millar A.G., Zucker R.S., Ellis-Davies G.C.R., Charlton M.P., and Atwood H.L. Calcium sensitivity of neurotransmitter release differs at phasic and tonic synapses. J. Neurosci. 25 (2005) 3113-3125
72. 2+ sensor proteins mediates short-term synaptic plasticity. Neuron 57 (2008) 210-216
73. Moser T., and Beutner D. Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse. Proc. Natl. Acad. Sci. USA 97 (2000) 883-888
74. 2+ and short-term facilitation. J. Neurosci. 27 (2007) 2261-2271
75. Nagy G., Kim J.H., Pang Z.P., Matti U., Rettig J., Südhof T.C., and Sørensen J.B. Different effects on fast exocytosis induced by Synaptotagmin 1 and 2 isoforms and abundance but not by phosphorylation. J. Neurosci. 26 (2006) 632-643
76. 2+] at the mouth of a calcium channel. J. Neurosci. 17 (1997) 6961-6973
77. ++ signals. Cell Calcium 24 (1998) 345-357
78. Neher E. A comparison between exocytic control mechanisms in adrenal chromaffin cells and a glutamatergic synapse. Pflugers Arch. 453 (2006) 261-268
79. Neher E., and Marty A. Discrete changes of cell-membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells. Proc. Natl. Acad. Sci. USA 79 (1982) 6712-6716
80. 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
81. Neher E., and Sakaba T. Estimating transmitter release rates from postsynaptic current fluctuations. J. Neurosci. 21 (2001) 9638-9654
82. Nicholson-Tomishima K., and Ryan T.A. Kinetic efficiency of endocytosis at mammalian CNS synapses requires synaptotagmin I. Proc. Natl. Acad. Sci. USA 101 (2004) 16648-16652
83. Regehr W.G., Delaney K.R., and Tank D.W. The role of presynaptic calcium in short-term enhancement at the hippocampal mossy fiber synapse. J. Neurosci. 14 (1994) 523-537
84. 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
85. Roos J., and Kelly R.B. The endocytic machinery in nerve terminals surrounds sites of exocytosis. Curr. Biol. 9 (1999) 1411-1414
86. Rosenmund C., Clements J.D., and Westbrook G.L. Nonuniform probability of release at a hippocampal synapse. Science 262 (1993) 754-757
87. Rosenmund C., Sigler A., Augustin I., Reim K., Brose N., and Rhee J.S. Differential control of vesicle priming and short-term plasticity by Munc13 isoforms. Neuron 33 (2002) 411-424
88. 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
89. 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
90. 2+-dependent steps controlling synaptic vesicle fusion and replenishment at the cerebellar basket cell terminal. Neuron 57 (2008) 406-419
91. 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
92. Sakaba T., and Neher E. Calmodulin mediates rapid recruitment of fast-releasing synaptic vesicles at a calyx-type synapse. Neuron 32 (2001) 1119-1131
93. Sakaba T., and Neher E. Involvement of actin polymerization in vesicle recruitment at the calyx of Held synapse. J. Neurosci. 23 (2003) 837-846
94. Sakaba T., and Neher E. Direct modulation of synaptic vesicle priming by GABA(B) receptor activation at a glutamatergic synapse. Nature 424 (2003) 775-778
95. Sakaba T., Stein A., Jahn R., and Neher E. Distinct kinetic changes in neurotransmitter release after SNARE protein cleavage. Science 309 (2005) 491-494
96. Sätzler K., Söhl L.F., Bollmann J.H., Borst J.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
97. Scheuss V., Taschenberger H., and Neher E. Kinetics of both synchronous and asynchronous quantal release during trains of action potential-evoked EPSCs at the rat calyx of Held. J. Physiol. 585 (2007) 361-381
98. Schiavo G., Matteoli M., and Montecucco C. Neurotoxins affecting neuroexocytosis. Physiol. Rev. 80 (2000) 717-766
99. Schneggenburger R., and Neher E. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406 (2000) 889-893
100. Sorensen J.B. Formation, stabilisation and fusion of the readily releasable pool of secretory vesicles. Pflugers Arch. 448 (2004) 347-362
101. Sorensen J.B., Nagy G., Varoqueaux F., Nehring R.B., Brose N., Wilson M.C., and Neher E. Differential control of the releasable vesicle pools by SNAP-25 splice variants and SNAP-23. Cell 114 (2003) 75-86
102. Sorensen J.B., Wiederhold K., Muller E.M., Milosevic I., Nagy G., de Groot B.L., Grubmuller H., and Fasshauer D. Sequential N- to C-terminal SNARE complex assembly drives priming and fusion of secretory vesicles. EMBO J. 25 (2006) 955-966
103. Stanley E.F. Single calcium channels and acetylcholine release at a presynaptic nerve terminal. Neuron 11 (1993) 1007-1011
104. 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
105. Sun J.Y., and Wu L.G. Fast kinetics of exocytosis revealed by simultaneous measurements of presynaptic capacitance and postsynaptic currents at a central synapse. Neuron 30 (2001) 171-182
106. 2+-sensor model for neurotransmitter release in a central synapse. Nature 450 (2007) 676-682
107. Takahashi T., Hori T., Kajikawa Y., and Tsujimoto T. The role of GTP-binding protein activity in fast central synaptic transmission. Science 289 (2000) 460-463
108. Taschenberger H., and von Gersdorff H. Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J. Neurosci. 20 (2000) 9162-9173
109. Teng H.B., and Wilkinson R.S. Clathrin-mediated endocytosis near active zones in snake motor boutons. J. Neurosci. 20 (2000) 7986-7993
110. 2+ receptor controls the final steps in peptide secretion from pituitary melanotrophs. Neuron 11 (1993) 93-104
111. 2+-sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse. Neuron 42 (2004) 595-605
112. Trudeau L.E., Fang Y., and Haydon P.G. Modulation of an early step in the secretory machinery in hippocampal nerve terminals. Proc. Natl. Acad. Sci. USA 95 (1997) 7163-7168
113. Trussell L.O., Zhang S., and Raman I.M. Desensitization of AMPA receptors upon multiquantal neurotransmitter release. Neuron 10 (1993) 1185-1196
114. Varela J.A., Sen K., Gibson J., Fost J., Abbott L.F., and Nelson S.B. A quantitative description of short-term plasticity at excitatory synapses in layer2/3 of rat primary visual cortex. J. Neurosci. 17 (1997) 7926-7940
115. Verstreken P., Kjaerulff O., Lloyd T.E., Atkinson R., Zhou Y., Meinertzhagen I.A., and Bellen H.J. Endophilin mutations block clathrin-mediated endocytosis but not neurotransmitter release. Cell 109 (2002) 101-112
116. 2+-dependent steps leading to secretion in chromaffin cells from mouse adrenal slices. Neuron 28 (2000) 537-545
117. Von Rüden L., and Neher E. A Ca-dependent early step in the release of catecholamines from adrenal chromaffin cells. Science 262 (1993) 1061-1065
118. Wadel K., Neher E., and Sakaba T. The coupling between synaptic vesicles and Ca2+ channels determines fast neurotransmitter release. Neuron 53 (2007) 563-575
119. Walmsley B., Edwards F.R., and Tracey D.J. Nonuniform release probabilities underlie quantal synaptic transmission at a mammalian excitatory central synapse. J. Neurophysiol. 60 (1988) 889-908
120. 2+. J. Gen. Physiol. 124 (2004) 653-662
121. Wang L.Y., and Kaczmarek L.K. High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature 394 (1998) 384-388
122. Weimer R.M., Gracheva E.O., Meyrignac O., Miller K.G., Richmond J.E., and Bessereau J.L. UNC-13 and UNC-10/Rim localize synaptic vesicles to specific membrane domains. J. Neurosci. 31 (2006) 8040-8047
123. ++-dependent vesicle pool dynamics and short-term synaptic depression. Biophys. J. 77 (1999) 2418-2429
124. Wienisch M., and Klingauf J. Vesicular proteins exocytosed and subsequently retrieved by compensatory endocytosis are nonidentical. Nat. Neurosci. 9 (2006) 1019-1027
125. Wierda K.D.B., Toonen R.F.G., de Wit H., Brussaard A.B., and Verhage M. Interdependence of PKC-dependent and PKC-independent pathways for presynaptic plasticity. Neuron 54 (2007) 275-290
126. Wölfel M., Lou X.L., and Schneggenburger R. A mechanism intrinsic to the vesicle fusion machinery determines fast and slow transmitter release at a large CNS synapse. J. Neurosci. 27 (2007) 3198-3210
127. Worden M.K., Bykhovskaia M., and Hackett J.T. Facilitation at the lobster neuromuscular junction: A stimulus-dependent mobilization model. J. Neurophysiol. 78 (1997) 417-428
128. 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
129. Wu Y., Kawasaki F., and Ordway R.W. Properties of short-term synaptic depression at larval neuromuscular synapses in wild-type and temperature-sensitive paralytic mutants of drosophila. J. Neurophysiol. 93 (2005) 2396-2405
130. Xu J.H., and 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 (2005) 633-645
131. 2+ sensors for fast release that specify distinct presynaptic properties in subsets of neurons. Neuron 54 (2007) 567-581
132. Xu-Friedman M.A., and Regehr W.G. Presynaptic strontium dynamics and synaptic transmission. Biophys. J. 76 (1999) 2029-2042
133. Xue M.S., Stradomska A., Chen H.M., Brose N., Zhang W.Q., Rosenmund C., and Reim K. Complexins facilitate neurotransmitter release at excitatory and inhibitory synapses in mammalian central nervous system. Proc. Natl. Acad. Sci. USA 105 (2008) 7875-7880
134. 2+-sensitive pool of granules is regulated by glucose and protein kinases in insulin-secreting INS-1 cells. J. Gen. Physiol. 124 (2004) 641-651
135. Zenisek D., Steyer J.A., and Almers W. Transport, capture and exocytosis of single synaptic vesicles at active zones. Nature 406 (2000) 849-854
136. Zucker R.S. Changes in statistics of transmitter release during facilitaion. J. Physiol. 229 (1973) 787-810
137. Zucker R.S. Exocytosis: A molecular and physiological perspective. Neuron 17 (1996) 1049-1055
138. Zucker R.S., and Regehr W.G. Short-term synaptic plasticity. Annu. Rev. Physiol. 64 (2002) 355-405