Calcium microdomains in regulated exocytosis

Cell Calcium

Volumn 40, Issue 5-6, 2006, Pages 423-439

  Oheim, Martin ^a   Kirchhoff, Frank ^b   Stühmer, Walter ^b  

^a INSERM   (France)

^b MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

Author keywords

Astrocyte; Bergmann glia; Ca2+; Calcium; Co localization; Microdomain; Nanodomain; Neurotransmitter release; Regulated secretion; Release site

Indexed keywords

AEQUORIN; CALCIUM ION; NEUROTRANSMITTER; VOLTAGE GATED CALCIUM CHANNEL;

ACTION POTENTIAL; ARTICLE; ASTROCYTE; CALCIUM CELL LEVEL; CALCIUM MOBILIZATION; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL ACTIVATION; CELL COMMUNICATION; CELL MEMBRANE; CELL MEMBRANE DEPOLARIZATION; CELL STRUCTURE; CELLULAR DISTRIBUTION; CEREBELLUM; EXOCYTOSIS; FLUOROMETRY; GLIA CELL; HUMAN; NEUROSECRETORY CELL; NEUROTRANSMITTER RELEASE; PRIORITY JOURNAL; SECRETORY CELL; SQUID; SYNAPSE; SYNAPSE VESICLE;

CEPHALOPODA;

EID: 33750500977     PISSN: 01434160     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceca.2006.08.007     Document Type: Article

References (174)

1. Douglas W.W., and Rubin R.P. The role of calcium in the secretory response of the adrenal medulla to acetylcholine. J. Physiol. 159 (1961) 40-47
2. Douglas W.W. Stimulus-secretion coupling: the concept and clues from chromaffin cells and other cells. Br. J. Pharmacol. 34 (1968) 453-474
3. Katz B., and Miledi R. The timing of calcium action during neuromuscular transmission. J. Physiol. 189 (1967) 535-544
4. Katz B., and Miledi R. Effect of calcium on acetylcholine release from mottor nerve terminals. Proc. R. Soc. Lond. Biol. Sci. 161 (1965) 496
5. Dodge F.A., and Rahamimoff R. Co-operative action of calcium ions in transmitter release at the neuromuscular junction. J. Physiol. 193 (1967) 419-432
6. Katz B. The Release of Neural Transmitter Substances (1969), Thomas, Springfield
7. Miledi R. Transmitter release induced by injection of calcium ions into nerve terminals. Proc. R. Soc. Lond. Biol. Sci. 183 (1973) 421-425
8. Schneggenburger R., and Neher E. Presynaptic calcium and control of vesicle fusion. Curr. Opin. Neurobiol. 15 (2005) 266-274
9. 2+ signal for phasic transmitter release at the calyx of Held. J. Physiol. 547 3 (2003) 665-689
10. Augustine G.J. How does calcium trigger neurotransmitter release?. Curr. Opin. Neurobiol. 11 3 (2001) 320-326
11. 2+ and synaptic plasticity. Cell Calcium 38 3-4 (2005) 355-367
12. Nowycky M.C., and Pinter M.J. Time courses of calcium and calcium-bound buffers following calcium influx in a model cell. Biophys. J. 64 (1993) 77-91
13. 2+ oscillations. Biophys. J. 67 1 (1994) 447-456
14. 2+ microdomains: new tools for understanding their roles in neurotranmitter release. Neuron 20 (1998) 389-399
15. Bauer P.J. The local Ca concentration profile in the vicinity of a Ca channel. Cell Biochem. Biophys. 35 1 (2001) 49-61
16. 2+] at the mouth of a calcium channel. J. Neurosci. 18 (1997) 6961-6973
17. Simon S.M., and Llinas R.R. Compartmentalization of the submembrane calcium activity during calcium influx and its significance in transmitter release. Biophys. J. 48 (1985) 485-498
18. 2+ dependent responses. Biophys. J. 45 (1984) 993-999
19. 2+-triggered exocytosis. Science 298 (2002) 781-785
20. Melamed-Book N., et al. Neuronal calcium sparks and intracelular calcium "noise". Proc. Natl. Acad. Sci. U.S.A. 96 26 (1999) 15217-15221
21. Zucker R.S. Can a synaptic signal arise from noise?. Neuron 38 6 (2003) 845-846
22. Perea G., and Araque A. Glial calcium signaling and neuron-glia communication. Cell Calcium 38 3-4 (2005) 375-382
23. Grosche J., et al. Microdomains for neuron-glia interaction: parallel fiber signaling to Bergmann glial cells. Nat. Neurosci. 2 2 (1999) 139-143
24. Grosche J., Kettenmann H., and Reichenbach A. Bergmann glial cells form distinct morphological structures to interact with cerebellar neurons. J. Neurosci. Res. 68 2 (2002) 138-149
25. Llinas R., Sugimori M., and Silver R.B. The concept of calcium concentration microdomains in synaptic transmission. Neuropharmacology 34 11 (1995) 1443-1451
26. Allbritton N.L., Meyer T., and Stryer L. Range of messenger action of calcium ion and inositol 1,4,5-trisphosphate. Science 258 (1992) 1812-1815
27. 2+ transients in amphibian skeletal muscle fibers. Biophys. J. 85 2 (2003) 1080-1097
28. Neher E. Concentration profiles of intracellular calcium in the presence of a diffusable chelator. In: Heinemann U., et al. (Ed). Exp. Brain Res.-Calcium Electrogenesis and Neuronal Function vol. 14 (1986), Springer, Heidelberg 80-96
29. Roberts W.M. Localization of calcium signals by a mobile calcium buffer in frog saccular hair cells. J. Neurosci. 14 5 (1994) 3246-3462
30. Zenisek D., et al. Imaging calcium entry sites and ribbon structures in two presynaptic cells. J. Neurosci. 23 7 (2003) 2538-2548
31. Marty A., and Neher E. Potassium channels in cultured bovine adrenal chromaffin cells. J. Physiol. (Lond.) 367 (1985) 117-141
32. 2+. Biophys. J. 79 6 (2000) 3009-3018
33. 2+ channels by calmodulin. Sci. STKE 318 (2006) er1
34. Forsythe I.D., et al. Inactivation of presynaptic calcium current contributes to synaptic depression at a fast central synapse. Neuron 20 4 (1998) 797-807
35. 2+/calmodulin binds to and modulates P/Q-type calcium channels. Nature 399 6732 (1999) 155-159
36. i in rat ventricular myocytes. J. Physiol. (Lond.) 574 2 (2006) 509-518
37. 2+ channels: one switch. J. Physiol. (Lond.) 554 2 (2004) 275-283
38. 2+ channels. J. Neurosci. 20 18 (2000) 6830-6838
39. 2+-dependent inactivation. J. Neurosci. 22 23 (2002) 10142-10152
40. 2+ channels. J. Biol. Chem. 281 8 (2006) 4691-4698
41. 2+ channels in chromaffin cells: role of mitochondria. J. Neurosci. 21 8 (2001) 2553-2560
42. Sieber J.J., et al. The SNARE motif is essential for the formation of syntaxin clusters in the plasma membrane. Biophys. J. 90 8 (2006) 2843-2851
43. Willig K.I., et al. STED microscopy reveals that synaptotagmin remains clustered after synaptic vesicle exocytosis. Nature 440 7086 (2006) 935-939
44. 2+ channel clustering, and vesicle release. Science 312 5776 (2006) 1051-1054
45. Egner A., and Hell S.W. Fluorescence microscopy with super-resolved optical sections. Trends Cell Biol. 15 4 (2005) 207-215
46. Westphal V., and Hell S.W. Nanoscale resolution in the focal plane of an optical microscope. Phys. Rev. Lett. 94 14 (2005) 143903
47. Roberts W., Jacobs R., and Hudspeth A. Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells. J. Neurosci. 10 11 (1990) 3664-3684
48. 2+ channels. J. Neurophysiol. 84 3 (2000) 1123-1135
49. Duan K., et al. Control of secretion by temporal patterns of action potentials in adrenal chromaffin cells. J. Neurosci. 23 35 (2003) 11235-11243
50. Llobet A., Cooke A., and Lagnado L. Exocytosis at the ribbon synapse of retinal bipolar cells studied in patches of presynaptic membrane. J. Neurosci. 23 7 (2003) 2706-2714
51. 2+ concentration triggering exocytosis in neuroendocrine cells. PNAS 91 26 (1994) 12765-12769
52. Neher E., and Marty A. Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells. PNAS 79 21 (1982) 6712-6716
53. von Gersdorff H., and Matthews G. Electrophyisology of synaptic vesicle cycling. Annu. Rev. Physiol. 61 1 (1999) 725-752
54. Dernick G., Alvarez de Toledo G., and Lindau M. Exocytosis of single chromaffin granules in cell-free inside-out membrane patches. Nat. Cell Biol. 5 4 (2003) 358-362
55. Tabares L., Lindau M., and Alvarez de Toledo G. Relationship between fusion pore opening and release during mast cell exocytosis studied with patch amperometry. Biochem. Soc. Trans. 31 (2003) 837-841
56. Elhamdani A., Azizi F., and Artalejo C.R. Double patch clamp reveals that transient fusion (kiss-and-run) is a major mechanism of secretion in calf adrenal chromaffin cells: high calcium shifts the mechanism from kiss-and-run to complete fusion. J. Neurosci. 26 11 (2006) 3030-3036
57. Mosharov E.V., and Sulzer D. Analysis of exocytotic events recorded by amperometry. Nat. Methods 2 9 (2005) 651-658
58. Schroeder T., et al. Zones of exocytotic release on bovine adrenal medullary cells in culture. J. Biol. Chem. 269 25 (1994) 17215-17220
59. Robinson I., et al. Colocalization of calcium entry and exocytotic release sites in adrenal chromaffin cells. PNAS 92 7 (1995) 2474-2478
60. 2+ gradients in excitable cells. Biophys. J. 67 2 (1994) 505-514
61. Chen P., et al. Amperometric detection of quantal catecholamine secretion from individual cells on micromachined silicon chips. Anal. Chem. 75 3 (2003) 518-524
62. Huang W.-H., et al. Transport, location, and quantal release monitoring of single cells on a microfluidic device. Anal. Chem. 76 2 (2004) 483-488
63. Hafez I., et al. Electrochemical imaging of fusion pore openings by electrochemical detector arrays. PNAS 102 39 (2005) 13879-13884
64. Sun X., and Gillis K.D. On-chip amperometric measurement of quantal catecholamine release using transparent indium tin oxide electrodes. Anal. Chem. 78 8 (2006) 2521-2525
65. Becherer U., et al. Calcium regulates exocytosis at the level of single vesicles. Nat. Neurosci. 6 (2003) 846-853
66. Steyer J.A., Horstmann H., and Almers W. Transport, docking and exocytosis of single secretory granules in live chromaffin cells. Nature 388 6641 (1997) 474-478
67. Oheim M., et al. The last few milliseconds in the life of a secretory granule. Eur. Biophys. J. 27 2 (1998) 83-98
68. Zenisek D., Steyer J.A., and Almers W. Transport, capture and exocytosis of single synaptic vesicles at active zones. Nature 406 6798 (2000) 849-854
69. Beaumont V., Llobet A., and Lagnado L. Expansion of calcium microdomains regulates fast exocytosis at a ribbon synapse. PNAS 102 30 (2005) 10700-10705
70. 2+ sparks within 200 nm of the sarcolemma of rat ventricular cells: evidence from total internal reflection fluorescence microscopy. Adv. Exp. Med. Biol. 430 (1997) 57-65
71. 2+ oscillations and waves by oscillating translocation and activation of protein kinase C. Curr. Biol. 11 14 (2001) 1089-1097
72. 2+ signaling dynamics in exocrine cells with total internal reflection microscopy. Am. J. Physiol. Gastrointest. Liver Physiol. 291 1 (2006) G146-G155
73. Shin W., and Gillis K.D. Measurement of changes in membrane surface morphology associated with exocytosis using scanning ion conductance microscopy. Biophys. J. 91 6 (2006) L63-L65
74. Llobet A., Beaumont V., and Lagnado L. Real-time measurement of exocytosis and endocytosis using interference of light. Neuron 40 6 (2003) 1075-1086
75. Llinas R., Sugimori M., and Silver R.B. Microdomains of high calcium concentration in a presynaptic terminal. Science 256 (1992) 677-679
76. DiGregorio D.A., and Vergara J.L. Localized detection of action potential-induced presynaptic calcium transients at a Xenopus neuromuscular junction. J. Physiol. (Lond.) 504 (1997) 83-96
77. Sabatini B., and Svoboda K. Analysis of calcium channels in single spoines using optical fluctuation analysis. Nature 408 (2000) 589-593
78. 2+ release at the level of a single sarcomere in skeletal muscle fibres. Nature 367 6465 (1994) 739-741
79. Jordan R., Lemke E.A., and Klingauf J. Visualization of synaptic vesicle movement in intact synaptic boutons using fluorescence fluctuation spectroscopy. Biophys. J. 89 3 (2005) 2091-2102
80. Beierlein M., et al. Presynaptic calcium measurements at physiological temperatures using a new class of dextran coupled indicators. J. Neurophysiol. 92 1 (2004) 591-599
81. 2+ indicator. J. Biol. Chem. 69 13 (1994) 10141-10149
82. 2+-sensitive proteins. Cell Calcium 38 (2005) 213-222
83. 2+ in cellular organelles?. Cell Calcium 38 3-4 (2005) 201-211
84. 2+ concentration changes at the secretory vesicle surface with a recombinant targeted cameleon. Curr. Biol. 9 16 (1999) 915-918
85. Neher E. Usefulness and limitations of linear approximations to the understanding of Ca signals. Cell Calcium 24 (1998) 345-357
86. Neher E. Some quantitative aspects of calcium fluorimetry. In: Yuste R., and Konnerth A. (Eds). Imaging in Neuroscience and Development (2005), CSHL Press, Cold Spring Habor 244-252
87. Burrone J., et al. Endogenous calcium buffers regulate fast exocytosis in the synaptic terminal of retinal bipolar cells. Neuron 33 1 (2002) 101-112
88. 2+ binding proteins and synaptic plasticity. Neurosci. Res. 16 (1993) 1-7
89. Zucker R.S., and Fogelson A.L. Relationship between transmitter release and presynaptic calcium influx when calcium enters through discrete channels. Proc. Natl. Acad. Sci. U.S.A. 83 (1986) 3032-3036
90. 2+ channel. Biophys. J. 71 6 (1996) 3064-3072
91. 2+ channels in live cells. Biophys. J. 81 (2001) 2639-2642
92. Sonnleitner A., and Isacoff E. Single ion channel imaging. Methods Enzymol. 361 (2003) 304-319
93. 2+ channels by total internal reflection fluorescence microscopy. Biophys. J. 86 (2004) 3250-3259
94. 2+ flux through individual muscle acetylcholine receptor channels. J. Gen. Physiol. 126 3 (2005) 179-192
95. Demuro A., and Parker I. Simultaneous ultra-fast multi-focal imaging of localized intracellular calcium transients. 50th Annual Meeting of the Biophysical Society. Salt Lake City. Biophys. J. (2006)
96. Fogelson A.L., and Zucker R.S. Presynaptic calcium diffusion from various arrays of single channels: implications for transmitter release and synaptic facilitation. Biophys. J. 48 (1985) 1003-1007
97. Stern M.D. Buffering of calcium in the vicinity of the channel pore. Cell Calcium 13 (1992) 183-192
98. 2+ ions. Biophys. J. 70 (1996) 2527-2539
99. Bennett M.R., Farnell L., and Gibson W.G. The probability of quantal secretion near a single calcium channel of an active zone. Biophys. J. 78 5 (2000) 2201-2221
100. Sheng Z.-H., et al. Identification of a syntaxin-binding site on N-type calcium channels. Neuron 13 6 (1994) 1303-1313
101. Yokoyama C.T., et al. Mechanism of SNARE protein binding and regulation of Cav2 channels by phosphorylation of the synaptic protein interaction site. Mol. Cell. Neurosci. 28 1 (2005) 1-17
102. Sheng Z.-H., Westenbroek R.E., and Catterall W.A. Physical link and functional coupling of presynaptic calcium channels and the synaptic vesicle docking/fusion machinery. J. Bioenerg. Biomembr. 30 4 (1998) 335-345
103. Llinas R. Calcium and transmitter release in squid synapse. Soc. Neurosci. Symp. 2 (1977) 139-160
104. 2+ microdomains on neurotransmitter release. Biophys. J. 76 (1999) 735-750
105. 2+ signals during repetitive depolarizing stimuli in adrenal chromaffin cells. Biophys. J. 85 5 (2003) 3397-3417
106. Ales E., et al. Depolarization evokes different patterns of calcium signals and exocytosis in bovine and mouse chromaffin cells: the role of mitochondria. Eur. J. Neurosci. 21 1 (2005) 142-150
107. Marengo F.D. Calcium gradients and exocytosis in bovine adrenal chromaffin cells. Cell Calcium 38 2 (2005) 87-99
108. Neher E., and Augustine G.J. Calcium gradients and buffers in bovine chromaffin cells. J. Physiol. 450 (1992) 273-301
109. Augustine G.J., Santamaria F., and Tanaka K. Local calcium signaling in neurons. Neuron 40 2 (2003) 331-346
110. Zhai R.G., and Bellen H.J. The architecture of the active zone in the presynaptic nerve terminal. Physiology 19 5 (2004) 262-270
111. Heuser J.E., Reese T.S., and Landis D.M. Functional changes in frog neuromuscular junctions studied with freeze fracture. J. Neurocytol. 3 1 (1974) 109-131
112. Heuser J.E., et al. Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J. Cell Biol. 81 2 (1979) 275-300
113. 2+ free solution on the structure of the active zones. J. Cell Biol. 81 (1979) 163-177
114. Pumplin D.W., Reese T.S., and Llinas R. Are the presynaptic membrane particles the calcium channels?. Proc. Natl. Acad. Sci. U.S.A. 78 11 (1981) 7210-7213
115. Harlow M.L., et al. The architecture of active zone material at the frog's neuromuscular junction. Nature 409 6819 (2001) 479-484
116. 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
117. Robitaille R., Adler E.M., and Charlton M.P. Calcium channels and calcium-gated potassium channels at the frog neuromuscular junction. J. Physiol. (Paris) 87 1 (1993) 15-24
118. Yamada W.M., and Zucker R.S. Time course of transmitter release calculated from simulations of a calcium diffusion model. Biophys. J. 61 3 (1992) 671-682
119. Bollmann J.H., Sakmann B., and Borst J.G.G. Calcium sensitivity of glutamate release in a calyx-type terminal. Science 289 5481 (2000) 953-957
120. Schneggenburger R., and Neher E. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406 6798 (2000) 889-893
121. 2+-sensor saturation for neurotransmitter release. J. Neurophysiol. 94 3 (2005) 1912-1919
122. Fenwick E.M., Marty A., and Neher E. Sodium and calcium channels in bovine chromaffin cells. J. Physiol. 331 (1982) 599-635
123. Gentile L., and Stanley E.F. A unified model of presynaptic release site gating by calcium channel domains. Eur. J. Neurosci. 21 1 (2005) 278-282
124. 2+ from one or two channels controls fusion of a single vesicle at the frog neuromuscular junction, J. Neurosci., in press.
125. Stanley E.F. The calcium channel and the organziation of the presynaptic transmitter release face. Trends Neurosci. 20 (1997) 404-409
126. Winslow J.L., Duffy S.N., and Charlton M.P. Homosynaptic facilitation of transmitter release in crayfish is not affected by mobile calcium chelators: implications for the residual ionized calcium hypothesis from electrophysiological and computational analyses. J. Neurophysiol. 72 4 (1994) 1769-1793
127. 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 5 (2002) 1648-1667
128. Trommershäuser J., et al. Heterogeneous presynaptic release probabilities: functional relevance for short-term plasticity. Biophys. J. 84 3 (2003) 1563-1579
129. 2+ at a site different from the microdomain where exocytosis occurs in mouse chromaffin cells. Biophys. J. 90 6 (2006) 2027-2037
130. 2+ diffusion near the membrane. Biophys. J. 72 2 (1997) 674-690
131. Voets T., Neher E., and Moser T. Mechanisms underlying phasic and sustained secretion in chromaffin cells from mouse adrenal slices. Neuron 23 3 (1999) 607-615
132. Fulop T., Radabaugh S., and Smith C. Activity-dependent differential transmitter release in mouse adrenal chromaffin cells. J. Neurosci. 25 32 (2005) 7324-7332
133. 2+ signal. Nat. Neurosci. 8 4 (2005) 426-434
134. 2+ buffers and synaptic efficacy. Cell Calcium 37 5 (2005) 489-495
135. 2+ channels, cytoplasmic messengers and proteins of the synaptic vesicle release complex. Trends Pharmacol. Sci. 22 10 (2001) 519-525
136. Jarvis S.E., and Zamponi G.W. Masters or slaves? Vesicle release machinery and the regulation of presynaptic calcium channels. Cell Calcium 37 5 (2005) 483-488
137. 2+ microdomain and neurotransmitter exocytosis: a Monte Carlo study. Biophys. J. 87 4 (2004) 2352-2364
138. Llano I., et al. Presynaptic calcium stores underlie large-amplitude miniature IPSCs and spontaneous calcium transients. Nat. Neurosci. 3 (2000) 1256-1265
139. 2+ entry, and spontaneous transmitter release. Neuron 29 1 (2001) 197-208
140. Sharma G., and Vijayaraghavan S. Modulation of presynaptic store calcium induces release of glutamate and postsynaptic firing. Neuron 38 6 (2003) 929-939
141. Unni V.K., et al. Calcium release from presynaptic ryanodine-sensitive stores is required for long-term depression at hippocampal CA3-CA3 pyramidal neuron synapses. J. Neurosci. 24 43 (2004) 9612-9622
142. Collin T., Marty A., and Llano I. Presynaptic calcium stores and synaptic transmission. Curr. Opin. Neurobiol.: Signal. Mech. 15 3 (2005) 275-281
143. Chuchillo-Ibanez I., et al. Calcium entry, calcium redistribution and exocytosis. Am. N. Y. Acad. Sci. 971 (2002) 108-116
144. 2+ signaling in dendrites of pyramidal neurons. Biophys. J. 70 2 (1996) 1069-1081
145. Carafoli E. The Ca pump of the plasma membrane. J. Biol. Chem. 267 (1992) 2115-2118
146. 2+ homeostasis and exocytosis in rat pancreatic {beta}-cell. Endocrinology 147 3 (2006) 1396-1407
147. 2+ exchanger of chromaffin cells. Ann. N. Y. Acad. Sci. 971 1 (2002) 174-177
148. 2+ stores in astrocytes: role of the plasmalemmal Na/Ca exchanger. Glia 16 4 (1996) 296-305
149. 2+ exchangers in the rat supraoptic magnocellular neuron is polarized to axon terminals. J. Neurosci. 23 37 (2003) 11673-11680
150. 2+ clearance mechanisms in neurohypophysial terminals of the rat. Cell Calcium 37 1 (2005) 45-56
151. 2+ clearance at the calyx of held. J. Neurosci. 25 26 (2005) 6057-6065
152. Israel M., et al. Calcium uptake by cholinergic synaptic vesicles. J. Physiol. (Paris) 76 5 (1980) 479-485
153. 2+ transport and protein phosphorylation in cholinergic synaptic vesicles. Proc. Natl. Acad. Sci. U.S.A. 79 (1982) 5783-5787
154. + antiport activity in synaptic vesicles isolated from sheep brain cortex. Neurosci. Lett. 247 2-3 (1998) 87-90
155. Macleod G.T., et al. Synaptic vesicles: test for a role in presynaptic calcium regulation. J. Neurosci. 24 10 (2004) 2496-2505
156. Mahapatra N.R., et al. A dynamic pool of calcium in catecholamine storage vesicles: exploration in living cells by a novel vesicle-targeted chromogranin a-aequorin chimeric photoprotein. J. Biol. Chem. 279 49 (2004) 51107-51121
157. Fellin T., et al. Bidirectional astrocyte-neuron communication: the many roles of glutamate and ATP. Novartis Found. Symp. 276 (2006) 208-217
158. Perea G., and Araque A. Synaptic information processing by astrocytes. J. Physiol. (Paris) 99 (2006) 92-97
159. Volterra A., and Medolesi J. Astrocytes, from brain glue to communication elements: the revolution continues. Nat. Rev. Neurosci. 6 (2005) 626-640
160. Angulo M.C., et al. Glutamate released from glial cells synchronizes neuronal activity in the hippocampus. J. Neurosci. 24 31 (2004) 6920-6927
161. Verkhratsky A., and Steinhäuser C. Ion channels in glial cells. Brain Res. Brain Res. Rev. 32 (2000) 380-412
162. Zhang Q., and Haydon P.G. Roles for gliotransmission in the nervous system. J. Neural Transm. 112 (2005) 121-125
163. Ye Z.-C., et al. Functional hemichannels in astrocytes: a novel mechanism of glutamate release. J. Neurosci. 23 9 (2003) 3588-3596
164. Rossi D.J., Oshima T., and Attwell D. Glutamate release in severe brain ischaemia is mainly by reversed uptake. Nature 403 6767 (2000) 316-321
165. Szatkowski M., Barbour B., and Attwell D. Non-vesicular release of glutamate from glial cells by reversed electrogenic glutamate uptake. Nature 348 6300 (1990) 443-446
166. Rouach N., Glowinski J., and Giaume C. Activity-dependent neuronal control of gap-junctional communication in astrocytes. J. Cell Biol. 149 7 (2000) 1513-1526
167. 2+-dependent exocytosis in cultured astrocytes. Glia 46 4 (2004) 437-445
168. Zhang Q., et al. Fusion-related release of glutamate from astrocytes. J. Biol. Chem. 279 13 (2004) 12724-12733
169. Bezzi P., et al. Astrocytes contain a vesicular compartment that is competent for regulated exocytosis of glutamate. Nat. Neurosci. 7 6 (2004) 613-620
170. Chen X., et al. "Kiss-and-run" glutamate secretion in cultured and freshly isolated rat hippocampal astrocytes. J. Neurosci. 25 40 (2005) 9236-9243
171. Kirischuk S., et al. Glutamate-triggered calcium signalling in mouse Bergmann glial cells in situ: role of inositol-1,4,5-trisphosphate-mediated intracellular calcium release. Neuroscience 92 3 (1999) 1051-1059
172. Matsui K., Jahr C.E., and Rubio M.E. High-concentration rapid transients of glutamate mediate neural-glial communication via ectopic release. J. Neurosci. 25 33 (2005) 7538-7547
173. T. Fulop, C. Smith, Physiological stimulation regulates exocytic mode through calcium activation of protein kinase C in mouse chromaffin cells, Biochem. J., 2006, doi:10.1042/BJ20060654 (immediate publication).
174. Hille B., et al. Stimulation of exocytosis without a calcium signal. J. Physiol. (Lond.) 520 1 (1999) 23-31