The voltage-gated calcium channel functions as the molecular switch of synaptic transmission

Annual Review of Biochemistry

Volumn 82, Issue , 2013, Pages 607-635

  Atlas, Daphne ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Amperometry; Chromaffin cells; Evoked secretion; Excitosome; Intramembrane signaling; Lanthanides

Indexed keywords

EXCITOSOME; NEUROTRANSMITTER; PROTEIN; SNARE PROTEIN; SYNAPTOTAGMIN I; SYNTAXIN 1A; TRANSMEMBRANE ACTIVATOR AND CAML INTERACTOR; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL;

ACTION POTENTIAL; BINDING AFFINITY; CALCIUM BINDING; CELL MEMBRANE; CONFORMATIONAL TRANSITION; EXOCYTOSIS; HETEROLOGOUS EXPRESSION; MEMBRANE DEPOLARIZATION; MOLECULAR MECHANICS; NEUROSECRETORY CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

ANIMALS; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; EXOCYTOSIS; HUMANS; MODELS, BIOLOGICAL; NEUROENDOCRINE CELLS; SYNAPTIC TRANSMISSION; SYNAPTOTAGMINS;

EID: 84878238928     PISSN: 00664154     EISSN: 15454509     Source Type: Book Series    
DOI: 10.1146/annurev-biochem-080411-121438     Document Type: Review

References (155)

1. Atlas D. 2010. Signaling role of the voltage-gated calcium channel as the molecular on/off-switch of secretion. Cell Signal. 22:1597-603
2. Chapman E 2008. How does synaptotagmin trigger neurotransmitter release? Annu. Rev. Biochem. 77:615-41
3. Südhof TC, Rothman JE. 2009. Membrane fusion: grappling with SNARE and SM proteins. Science 323:47477
4. Lang T, Jahn R. 2008. Core proteins of the secretory machinery. Handb. Exp. Pharmacol. 184:107-27
5. Katz B, Miledi R. 1969. Spontaneous and evoked activity of motor nerve endings in calcium Ringer. J. Physiol. 203:689-706
6. Sabatini BL, Regehr WG. 1996. Timing of neurotransmission at fast synapses in the mammalian brain. Nature 384:170-72
7. Llinas R, Steinberg IZ, Walton K. 1981. Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse. Biophys. J. 33:323-51
8. Almers W. 1994. Synapses. How fast can you get? Nature 367:682-83
9. Südhof TC. 2004. The synaptic vesicle cycle. Annu. Rev. Neurosci. 27:509-47
10. Thomson AM. 2000. Facilitation, augmentation and potentiation at central synapses. Trends Neurosci. 23:305-12
11. Katz B, Miledi R. 1967. The timing of calcium action during neuromuscular transmission. J. Physiol. 189:535-44
12. Harlow ML, Ress D, Stoschek A, Marshall RM, McMahan UJ. 2001. The architecture of active zone material at the frogs neuromuscular junction. Nature 409:479-84
13. Bezprozvanny I, Scheller RH, Tsien RW. 1995. Functional impact of syntaxin on gating of N-type and Q-type calcium channels. Nature 378:623-26
14. Wiser O, Bennett MK, Atlas D. 1996. Functional interaction of syntaxin and SNAP-25 with voltagesensitive L- and N-type Ca2+ channels. EMBO J. 15:4100-10
15. Wiser O, Trus M, Hernandez A, Renstrom E, Barg S, et al. 1999. The voltage sensitive Lc-type Ca2+ channel is functionally coupled to the exocytotic machinery. Proc. Natl. Acad. Sci. USA 96:248-53
16. Wiser O, Tobi D, Trus M, Atlas D. 1997. Synaptotagmin restores kinetic properties of a syntaxinassociated N-type voltage sensitive calcium channel. FEBS Lett. 404:203-7
17. Tobi D, Wiser O, Trus M, Atlas D. 1998. N-type voltage-sensitive calcium channel interacts with syntaxin, synaptotagmin and SNAP-25 in a multiprotein complex. Recept. Channels 6:89-98
18. Zhong H, Yokoyama CT, Scheuer T, Catterall WA. 1999. Reciprocal regulation of P/Q-type Ca2+ channels by SNAP-25, syntaxin and synaptotagmin. Nat. Neurosci. 2:939-41
19. Atlas D. 2001. Functional and physical coupling of voltage-sensitive calcium channels with exocytotic proteins: ramifications for the secretion mechanism. J. Neurochem. 77:972-85
20. Stanley EF. 1993. Single calcium channels and acetylcholine release at a presynaptic nerve terminal. Neuron 11:1007-11
21. Rothman JE. 1994. Mechanisms of intracellular protein transport. Nature 372:55-63
22. Ferro-Novick S, Jahn R. 1994. Vesicle fusion from yeast to man. Nature 370:191-93
23. Sudhof TC, Rizo J. 2011. Synaptic vesicle exocytosis. Cold Spring Harb. Perspect. Biol. 3:a005637
24. Jahn R, Scheller RH. 2006. SNAREs-engines for membrane fusion. Nat. Rev. Mol. Cell Biol. 7:631-43
25. Söllner T, Whiteheart SW, Brunner M, Erdjument-Bromage H, Geromanos S, et al. 1993. SNAP receptors implicated in vesicle targeting and fusion. Nature 362:31824
26. van den Bogaart G, Thutupalli S, Risselada JH, Meyenberg K, Holt M, et al. 2011. Synaptotagmin-1 may be a distance regulator acting upstream of SNARE nucleation. Nat. Struct. Mol. Biol. 18:805-12
27. Schiavo G, Benfenati F, Poulain B, Rossetto O, Polverino de Laureto P, et al. 1992. Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 359:832-35
28. Blasi J, Chapman ER, Link E, Binz T, Yamasaki S, et al. 1993. Botulinum neurotoxin A selectively cleaves the synaptic protein SNAP-25. Nature 365:160-63
29. Blasi J, Chapman ER, Yamasaki S, Binz T, Niemann H, Jahn R. 1993. Botulinum neurotoxin C1 blocks neurotransmitter release by means of cleaving HPC-1/syntaxin. EMBO J. 12:4821-28
30. Schiavo G, Santucci A, Dasgupta BR, Mehta PP, Jontes J, et al. 1993. Botulinum neurotoxins serotypes A and E cleave SNAP-25 at distinct COOH-terminal peptide bonds. FEBS Lett. 335:99-103
31. Kyoung M, Srivastava A, Zhang Y, Diao J, Vrljic M, et al. In vitro system capable of differentiating fast Ca2+-triggered content mixing from lipid exchange for mechanistic studies of neurotransmitter release. Proc. Natl. Acad. Sci. USA 108:E304-13
32. Südhof TC. 2012. Calcium control of neurotransmitter release. Cold Spring Harb. Perspect. Biol. 4:a011353
33. Hayashi T, McMahon H, Yamasaki S, Binz T, Hata Y, et al. 1994. Synaptic vesicle membrane fusion complex: action of clostridial neurotoxins on assembly. EMBO J. 13:5051-61
34. Sutton RB, Fasshauer D, Jahn R, Brunger AT. 1998. Crystal structure of a SNARE complex involved in synaptic exocytosis at 2. 4 ä resolution. Nature 395:347-53
35. Yang X, Kaeser-Woo YJ, Pang ZP, Xu W, Südhof TC. 2010. Complexin clamps asynchronous release by blocking a secondary Ca2+-sensor via its accessory αhelix. Neuron 68:907-20
36. Malsam J, Kreye S, Söllner TH. 2008. Membrane fusion: SNAREs and regulation. Cell. Mol. Life Sci. 65:2814-32
37. Kaeser PS, Deng L, Wang Y, Dulubova I, Liu X, et al. 2011. RIM proteins tether Ca2+ channels to presynaptic active zones via a direct PDZ-domain interaction. Cell 144:282-95
38. Perin MS, Fried VA, Mignery GA, Jahn R, Südhof TC. 1990. Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C. Nature 345:260-63
39. Martens S, McMahon HT. 2008. Mechanisms of membrane fusion: disparate players and common principles. Nat. Rev. Mol. Cell Biol. 9:543-56
40. Coussens L, Parker PJ, Rhee L, Yang-Feng TL, Chen E, et al. 1986. Multiple, distinct forms of bovine and human protein kinase C suggest diversity in cellular signaling pathways. Science 233:859-66
41. Shao X, Davletov BA, Sutton RB, Südhof TC, Rizo J. 1996. Bipartite Ca2+-binding motif in C2 domains of synaptotagmin and protein kinase C. Science 273:248-51
42. Ubach J, Zhang X, Shao X, Südhof TC, Rizo J. 1998. Ca2+ binding to synaptotagmin: How many Ca2+ ions bind to the tip of a C2-domain? EMBO J. 17:3921-30
43. Shao X, Li C, Fernandez I, Zhang X, Südhof TC, Rizo J. 1997. Synaptotagmin-syntaxin interaction: the C2 domain as a Ca2+-dependent electrostatic switch. Neuron 18:133-42
44. Bennett MK, Calakos N, Kreiner T, Scheller RH. 1992. Synaptic vesicle membrane proteins interact to form a multimeric complex. J. Cell Biol. 116:761-75
45. Chapman ER, Hanson PI, An S, Jahn R. 1995. Ca2+ regulates the interaction between synaptotagmin and syntaxin 1. J. Biol. Chem. 270:23667-71
46. Geppert M, Goda Y, Hammer RE, Li C, Rosahl TW, et al. 1994. Synaptotagmin I: a major Ca2+ sensor for transmitter release at a central synapse. Cell 79:717-27
47. Cohen R, Elferink LA, Atlas D. 2003. The C2A domain of synaptotagmin alters the kinetics of voltagegated Ca2+ channels Cav1. 2 (Lc-type) and Cav2. 3 (R-type). J. Biol. Chem. 278:9258-66
48. Uellner R, Zvelebil MJ, Hopkins J, Jones J, MacDougall LK, et al. 1997. Perforin is activated by a proteolytic cleavage during biosynthesis which reveals a phospholipid-binding C2 domain. EMBO J. 16:7287-96
49. Edwards AS, Newton AC. 1997. Regulation of protein kinase C βII by its C2 domain. Biochemistry 36:15615-23
50. Nalefski EA, Falke JJ. 1998. Location of the membrane-docking face on the Ca2+-activated C2 domain of cytosolic phospholipase A2. Biochemistry 37:17642-50
51. Williams RL, Katan M. 1996. Structural views of phosphoinositide-specific phospholipase C: signalling the way ahead. Structure 4:1387-94
52. Radhakrishnan A, Stein A, Jahn R, Fasshauer D. 2009. The Ca2+ affinity of synaptotagmin 1 is markedly increased by a specific interaction of its C2B domain with phosphatidylinositol 4, 5-bisphosphate. J. Biol. Chem. 284:25749-60
53. Bai J, Tucker WC, Chapman ER. 2004. PIP2 increases the speed of response of synaptotagmin and steers its membrane-penetration activity toward the plasma membrane. Nat. Struct. Mol. Biol. 11:36-44
54. Arac D, Chen X, Khant HA, Ubach J, Ludtke SJ, et al. 2006. Close membrane-membrane proximity induced by Ca2+-dependent multivalent binding of synaptotagmin-1 to phospholipids. Nat. Struct. Mol. Biol. 13:209-17
55. Cohen-Kutner M, Nachmanni D, Atlas D. 2010. Cav2. 1 (P/Q channel) interactionwith synaptic proteins is essential for depolarization-evoked release. Channels 4:266-77
56. Cohen R, Atlas D. 2004. R-type voltage-gated Ca2+ channel interacts with synaptic proteins and recruits synaptotagmin to the plasma membrane of Xenopus oocytes. Neuroscience 128:831-41
57. Elferink LA, Peterson MR, Scheller RH. 1993. A role for synaptotagmin (p65) in regulated exocytosis. Cell 72:153-59
58. Loewen CA, Lee SM, Shin YK, Reist NE. 2006. C2B polylysine motif of synaptotagmin facilitates a Ca2+-independent stage of synaptic vesicle priming in vivo. Mol. Biol. Cell 17:5211-26
59. Paddock BE, Wang Z, Biela LM, Chen K, Getzy MD, et al. 2011. Membrane penetration by synaptotagmin is required for coupling calcium binding to vesicle fusion in vivo. J. Neurosci. 31:2248-57
60. Kozlov MM, McMahon HT, Chernomordik LV. Protein-driven membrane stresses in fusion and fission. Trends Biochem. Sci. 35:699-706
61. Martens S, Kozlov MM, McMahon HT. 2007. How synaptotagmin promotes membrane fusion. Science 316:1205-8
62. Hui E, Johnson CP, Yao J, Dunning FM, Chapman ER. 2009. Synaptotagmin-mediated bending of the target membrane is a critical step in Ca2+-regulated fusion. Cell 138:709-21
63. Walter AM, Groffen AJ, Sorensen JB, Verhage M. 2011. Multiple Ca2+ sensors in secretion: teammates, competitors or autocrats? Trends Neurosci. 34:487-97
64. Fernndez-Chacin R, Königstorfer A, Gerber SH, Garc J, Matos MF, et al. 2001. Synaptotagmin I functions as a calcium regulator of release probability. Nature 410:4149
65. Xu J, Pang ZP, Shin OH, Südhof TC. 2009. Synaptotagmin-1 functions as aCa2+ sensor for spontaneous release. Nat. Neurosci. 12:759-66
66. Paddock BE, Striegel AR, Hui E, Chapman ER, Reist NE. 2008. Ca2+-dependent, phospholipid-binding residues of synaptotagmin are critical for excitation-secretion coupling in vivo. J. Neurosci. 28:7458-66
67. Davletov B, Perisic O, Williams RL. 1998. Calcium-dependent membrane penetration is a hallmark of the C2 domain of cytosolic phospholipase A2 whereas the C2A domain of synaptotagmin binds membranes electrostatically. J. Biol. Chem. 273:19093-96
68. Kuo W, Herrick DZ, Cafiso DS. Phosphatidylinositol 4, 5-bisphosphate alters synaptotagmin 1 membrane docking and drives opposing bilayers closer together. Biochemistry 50:2633-41
69. DiAntonio A, Schwarz TL. 1994. The effect on synaptic physiology of synaptotagmin mutations in Drosophila. Neuron 12:909-20
70. Chicka MC, Hui E, Liu H, Chapman ER. 2008. Synaptotagmin arrests the SNARE complex before triggering fast, efficient membrane fusion in response to Ca2+. Nat. Struct. Mol. Biol. 15:827-35
71. Zhang X, Kim-Miller MJ, Fukuda M, Kowalchyk JA, Martin TF. 2002. Ca2+-dependent synaptotagmin binding to SNAP-25 is essential for Ca2+-triggered exocytosis. Neuron 34:599-611
72. Oancea E, Meyer T. 1998. Protein kinase C as a molecular machine for decoding calcium and diacylglycerol signals. Cell 95:307-18
73. Sakai N, Sasaki K, Ikegaki N, Shirai Y, Ono Y, Saito N. 1997. Direct visualization of the translocation of the γ-subspecies of protein kinase C in living cells using fusion proteins with green fluorescent protein. J. Cell Biol. 139:1465-76
74. Bruns D, Jahn R. 1995. Real-time measurement of transmitter release from single synaptic vesicles. Nature 377:62-65
75. Trus M, Wiser O, Goodnough MC, Atlas D. 2001. The transmembrane domain of syntaxin 1A negatively regulates voltage-sensitive Ca2+ channels. Neuroscience 104:599-607
76. Cohen R, Marom M, Atlas D. 2007. Depolarization-evoked secretion requires twovicinal transmembrane cysteines of syntaxin 1A. PLoS ONE 2:e1273
77. Hagalili Y, Bachnoff N, Atlas D. 2008. The voltage-gated Ca2+ channel is the Ca2+ sensor protein of secretion. Biochemistry 47:13822-30
78. Atlas D, Wiser O, Trus M. 2001. The voltage-gated Ca2+ channel is the Ca2+ sensor of fast neurotransmitter release. Cell. Mol. Neurobiol. 21:717-31
79. Yoshida A, Oho C, Omori A, Kuwahara R, Ito T, Takahashi M. 1992. HPC-1 is associated with synaptotagmin and ω-conotoxin receptor. J. Biol. Chem. 267:24925-28
80. Robinson IM, Finnegan JM, Monck JR, Wightman RM, Fernandez JM. 1995. Colocalization of calcium entry and exocytotic release sites in adrenal chromaffin cells. Proc. Natl. Acad. Sci. USA 92:2474-78
81. Bokvist K, Eliasson L, Aamaa C, Renstrom E, Rorsman P. 1995. Co-localization of L-type Ca2+ channels and insulin-containing secretory granules and its significance for the initiation of exocytosis in mouse pancreatic B-cells. EMBO J. 14:50-57
82. Sheng ZH, Rettig J, Takahashi M, Catterall WA. 1994. Identification of a syntaxin-binding site on N-type calcium channels. Neuron 13:1303-13
83. Rettig J, Sheng ZH, Kim DK, Hodson CD, Snutch TP, Catterall WA. 1996. Isoform-specific interaction of the α1A subunits of brain Ca2+ channels with the presynaptic proteins syntaxin and SNAP-25. Proc. Natl. Acad. Sci. USA 93:7363-68
84. Ji J, Yang SN, Huang X, Li X, Sheu L, et al. 2002. Modulation of L-type Ca2+ channels by distinct domains within SNAP-25. Diabetes 51:1425-36
85. Catterall WA. 2000. Structure and regulation of voltage-gated Ca2+ channels. Annu. Rev. Cell Dev. Biol. 16:521-55
86. Jarvis SE, Zamponi GW. 2007. Trafficking and regulation of neuronal voltage-gated calcium channels. Curr. Opin. Cell Biol. 19:474-82
87. Mochida S, Sheng ZH, Baker C, Kobayashi H, Catterall WA. 1996. Inhibition of neurotransmission by peptides containing the synaptic protein interaction site of N-type Ca2+ channels. Neuron 17:781-88
88. Rettig J, Heinemann C, Ashery U, Sheng ZH, Yokoyama CT, et al. 1997. Alteration of Ca2+ dependence of neurotransmitter release by disruption of Ca2+ channel/syntaxin interaction. J. Neurosci. 17:6647-56
89. Barg S, Ma X, Eliasson L, Galvanovskis J, Göpel SO, et al. Fast exocytosis with few Ca2+ channels in insulin-secreting mouse pancreatic B cells. Biophys. J. 81:3308-23
90. Wiser O, Cohen R, Atlas D. 2002. Ionic dependence of Ca2+ channel modulation by syntaxin 1A. Proc. Natl. Acad. Sci. USA 99:3968-73
91. Charvin N, Lvque C, Walker D, Berton F, Raymond C, et al. 1997. Direct interaction of the calcium sensor protein synaptotagmin I with a cytoplasmic domain of the α1A subunit of the P/Q-type calcium channel. EMBO J. 16:4591-96
92. Yang SN, Larsson O, Brnstrm R, Bertorello AM, Leibiger B, et al. 1999. Syntaxin 1 interacts with the LD subtype of voltage-gated Ca2+ channels in pancreatic βcells. Proc. Natl. Acad. Sci. USA 96:10164-69
93. Snutch TP, Sutton KG, Zamponi GW. 2001. Voltage-dependent calcium channels-beyond dihydropyridine antagonists. Curr. Opin. Pharmacol. 1:11-16
94. Weiss N, Zamponi GW. 2012. Regulation of voltage-gated calcium channels by synaptic proteins. Adv. Exp. Med. Biol. 740:759-75
95. Rickman C, Davletov B. 2003. Mechanism of calcium-independent synaptotagmin binding to target SNAREs. J. Biol. Chem. 278:5501-4
96. Yoshihara M, Littleton JT. 2002. Synaptotagmin I functions as a calcium sensor to synchronize neurotransmitter release. Neuron 36:897-908
97. Mackler JM, Drummond JA, Loewen CA, Robinson IM, Reist NE. 2002. The C2BCa2+-binding motif of synaptotagmin is required for synaptic transmission in vivo. Nature 418:340-44
98. Rizzoli SO, Betz WJ. 2005. Synaptic vesicle pools. Nat. Rev. Neurosci. 6:57-69
99. Denker A, Bethani I, Kr öhnert K, Körber C, Horstmann H, et al. 2011. A small pool of vesiclesmaintains synaptic activity in vivo. Proc. Natl. Acad. Sci. USA 108:17177-82
100. Cohen R, Schmitt BM, Atlas D. 2005. Molecular identification and reconstitution of depolarizationinduced exocytosis monitored by membrane capacitance. Biophys. J. 89:4364-73
101. Kim MS, Morii T, Sun LX, Imoto K, Mori Y. 1993. Structural determinants of ion selectivity in brain calcium channel. FEBS Lett. 318:145-48
102. Sather WA, McCleskey EW. 2003. Permeation and selectivity in calcium channels. Annu. Rev. Physiol. 65:133-59
103. Cloues RK, Cibulsky SM, Sather WA. 2000. Ion interactions in the high-affinity binding locus of a voltage-gated Ca2+ channel. J. Gen. Physiol. 116:569-86
104. Kuo CC, Hess P. 1993. Ion permeation through the L-type Ca2+ channel in rat phaeochromocytoma cells: two sets of ion binding sites in the pore. J. Physiol. 466:629-55
105. Ellinor PT, Yang J, Sather WA, Zhang JF, Tsien RW. 1995. Ca2+ channel selectivity at a single locus for high-affinity Ca2+ interactions. Neuron 15:1121-32
106. Lerner I, Trus M, Cohen R, Yizhar O, Nussinovitch I, Atlas D. 2006. Ion interaction at the pore of Lc-typeCa2+ channel is sufficient to mediate depolarization-induced exocytosis. J. Neurochem. 97:116-27
107. Trus M, Corkey RF, Nesher R, Richard AM, Deeney JT, et al. 2007. The L-type voltage-gated Ca2+channel is the Ca2+ sensor protein of stimulus-secretion coupling in pancreatic beta cells. Biochemistry 46:14461-67
108. Marom M, Sebag A, Atlas D. 2007. Cations residing at the selectivity filter of the voltage-gated Ca2+- channel modify fusion-pore kinetics. Channels 1:377-86
109. Marom M, Hagalili Y, Sebag A, Tzvier L, Atlas D. 2010. Conformational changes induced in voltagegated calcium channelCav1. 2 by BayK 8644 or FPL64176 modify the kinetics of secretion independently of Ca2+ influx. J. Biol. Chem. 285:6996-7005
110. Marom M, Birnbaumer L, Atlas D. 2011. Membrane depolarization combined with Gq-activated G-protein-coupled receptors induce transient receptor potential channel 1 (TRPC1)-dependent potentiation of catecholamine release. Neuroscience 189:132-45
111. Cena V, Nicolas GP, Sanchez-Garcia P, Kirpekar SM, Garcia AG. 1983. Pharmacological dissection of receptor-associated and voltage-sensitive ionic channels involved in catecholamine release. Neuroscience 10:1455-62
112. Reeves JP, Condrescu M. 2003. Lanthanum is transported by the sodium/calcium exchanger and regulates its activity. Am. J. Physiol. Cell Physiol. 285:C763-70
113. Powis DA, Clark CL. 1996. A difference in the cellular mechanisms of secretion of adrenaline and noradrenaline revealed with lanthanum in bovine chromaffin cells. Neurosci. Lett. 203:131-34
114. Hohaus A, Beyl S, Kudrnac M, Berjukow S, Timin EN, et al. 2005. Structural determinants of L-type channel activation in segment IIS6 revealed by a retinal disorder. J. Biol. Chem. 280:38471-77
115. Wang CT, Grishanin R, Earles CA, Chang PY, Martin TF, et al. 2001. Synaptotagmin modulation of fusion pore kinetics in regulated exocytosis of dense-core vesicles. Science 294:1111-15
116. Breckenridge LJ, Almers W. 1987. Currents through the fusion pore that forms during exocytosis of a secretory vesicle. Nature 328:814-17
117. Feder D, Im MJ, Klein HW, Hekman M, Holzhöfer A, et al. 1986. Reconstitution of β1-adrenoceptordependent adenylate cyclase from purified components. EMBO J. 5:1509-14
118. Xue M, Craig TK, Xu J, Chao HT, Rizo J, Rosenmund C. 2011. Binding of the complexin N terminus to the SNARE complex potentiates synaptic-vesicle fusogenicity. Nat. Struct. Mol. Biol. 17:568-75
119. Maximov A, Tang J, Yang X, Pang ZP, Südhof TC. 2009. Complexin controls the force transfer from SNARE complexes to membranes in fusion. Science 323:516-21
120. Schmitt BM, Koepsell H. 2002. An improved method for real-time monitoring of membrane capacitance in Xenopus laevis oocytes. Biophys. J. 82:1345-57
121. Schiavo G, Poulain B, Rossetto O, Benfenati F, Tauc L, Montecucco C. 1992. Tetanus toxin is a zinc protein and its inhibition of neurotransmitter release and protease activity depend on zinc. EMBO J. 11:3577-83
122. Wang Y, Okamoto M, Schmitz F, Hofmann K, Südhof TC. 1997. Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion. Nature 388:593-98
123. Hibino H, Pironkova R, Onwumere O, Vologodskaia M, Hudspeth AJ, Lesage F. 2002. RIM binding proteins (RBPs) couple Rab3-interacting molecules (RIMs) to voltage-gated Ca2+ channels. Neuron 34:411-23
124. Coppola T, Magnin-Lüthi S, Perret-Menoud V, Gattesco S, Schiavo G, Regazzi R. 2001. Direct interaction of the Rab3 effector RIM with Ca2+ channels, SNAP-25, and synaptotagmin. J. Biol. Chem. 276:32756-62
125. Leveque C, Pupier S, Marqueze B, Geslin L, Kataoka M, et al. 1998. Interaction of cysteine string proteins with the α1A subunit of the P/Q-type calcium channel. J. Biol. Chem. 273:13488-92
126. Schoch S, Dek F, Königstorfer A, Mozhayeva M, Sara Y, et al. 2001. SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science 294:1117-22
127. Lockless SW, Zhou M, MacKinnon R. 2007. Structural and thermodynamic properties of selective ion binding in a K+ channel. PLoS Biol. 5:e121
128. Malasics A, Boda D, Valisk M, Henderson D, Gillespie D. 2010. Simulations of calcium channel block by trivalent cations: Gd3+ competes with permeant ions for the selectivity filter. Biochim. Biophys. Acta 1798:2013-21
129. Arien H, Wiser O, Arkin IT, Leonov H, Atlas D. 2003. Syntaxin 1A modulates the voltage-gated L-type calcium channel (Cav1. 2) in a cooperative manner. J. Biol. Chem. 278:29231-39
130. Cohen R, Schmitt BM, Atlas D. 2008. Reconstitution of depolarization and Ca2+-evoked secretion in Xenopus oocytes monitored by membrane capacitance. Methods Mol. Biol. 440:269-82
131. Sutton KG, McRory JE, Guthrie H, Murphy TH, Snutch TP. 1999. P/Q-type calcium channels mediate the activity-dependent feedback of syntaxin-1A. Nature 401:800-4
132. Bergsman JB, Tsien RW. 2000. Syntaxin modulation of calcium channels in cortical synaptosomes as revealed by botulinum toxin C1. J. Neurosci. 20:4368-78
133. Stanley EF. 2003. Syntaxin I modulation of presynaptic calcium channel inactivation revealed by botulinum toxin C1. Eur. J. Neurosci. 17:1303-5
134. Swaminath G, Deupi X, Lee TW, Zhu W, Thian FS, et al. 2005. Probing the β2 adrenoceptor binding site with catechol reveals differences in binding and activation by agonists and partial agonists. J. Biol. Chem. 280:22165-71
135. Fatt P, Katz B. 1952. Spontaneous subthreshold activity at motor nerve endings. J. Physiol. 117:109-28
136. Manita S, Ross WN. 2009. Synaptic activation and membrane potential changes modulate the frequency of spontaneous elementary Ca2+ release events in the dendrites of pyramidal neurons. J. Neurosci. 29:7833-45
137. Hua Y, Sinha R, Martineau M, Kahms M, Klingauf J. 2010. A common origin of synaptic vesicles undergoing evoked and spontaneous fusion. Nat. Neurosci. 13:1451-53
138. Hua Z, Leal-Ortiz S, Foss SM, Waites CL, Garner CC, et al. 2011. v-SNARE composition distinguishes synaptic vesicle pools. Neuron 71:474-87
139. Chung C, Barylko B, Leitz J, Liu X, Kavalali ET. 2010. Acute dynamin inhibition dissects synaptic vesicle recycling pathways that drive spontaneous and evoked neurotransmission. J. Neurosci. 30:1363-76
140. Fredj NB, Burrone J. 2009. A resting pool of vesicles is responsible for spontaneous vesicle fusion at the synapse. Nat. Neurosci. 12:751-58
141. Groffen AJ, Martens S, Diz Arazola R, Cornelisse LN, Lozovaya N, et al. 2010. Doc2b is a high-affinity Ca2+ sensor for spontaneous neurotransmitter release. Science 327:1614-18
142. Xu J, He L, Wu LG. 2007. Role of Ca2+ channels in short-term synaptic plasticity. Curr. Opin. Neurobiol. 17:352-59
143. Fatt P, Katz B. 1950. Membrane potentials at the motor end-plate. J. Physiol. 111:46p-47p
144. Trapani JG, Nicolson T. 2011. Mechanism of spontaneous activity in afferent neurons of the zebrafish lateral-line organ. J. Neurosci. 31:1614-23
145. McKay BE, Placzek AN, Dani JA. 2007. Regulation of synaptic transmission and plasticity by neuronal nicotinic acetylcholine receptors. Biochem. Pharmacol. 74:1120-33
146. Firestone JA, Browning MD. 1994. Calcium signalling in bovine adrenal chromaffin cells: additive effects of histamine and nicotine. Synapse 17:268-74
147. Wilhelm BG, Groemer TW, Rizzoli SO. 2010. The same synaptic vesicles drive active and spontaneous release. Nat. Neurosci. 13:1454-56
148. Zucker RS, Regehr WG. 2002. Short-term synaptic plasticity. Annu. Rev. Physiol. 64:355-405
149. Katz B, Miledi R. 1968. The role of calcium in neuromuscular facilitation. J. Physiol. 195:481-92
150. Wu LG, Saggau P. 1994. Presynaptic calcium is increased during normal synaptic transmission and paired-pulse facilitation, but not in long-term potentiation in area CA1 of hippocampus. J. Neurosci. 14:645-54
151. Bollmann JH, Sakmann B, Borst JG. 2000. Calcium sensitivity of glutamate release in a calyx-type terminal. Science 289:953-57
152. Schneggenburger R, Neher E. 2000. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406:889-93
153. Yamada WM, Zucker RS. 1992. Time course of transmitter release calculated from simulations of a calcium diffusion model. Biophys. J. 61:671-82
154. Bertram R, Sherman A, Stanley EF. 1996. Single-domain/bound calcium hypothesis of transmitter release and facilitation. J. Neurophysiol. 75:1919-31
155. Gez LS, Hagalili Y, Shainberg A, Atlas D. 2012. Voltage-driven Ca2+ binding at the L-typeCa2+ channel triggers cardiac excitation-contraction coupling prior to Ca2+ influx. Biochemistry 51:9658-66