Single calcium channel domain gating of synaptic vesicle fusion at fast synapses; analysis by graphic modeling

Channels

Volumn 9, Issue 5, 2015, Pages 324-333

  Stanley, Elise F ^a  

^a UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

Calcium channel; Microdomain; Nanodomain; Overlapping domain; Presynaptic; Single channel synaptic vesicle; Single domain; Transmitter release

Indexed keywords

CALCIUM; NEURONAL CALCIUM SENSOR; VOLTAGE GATED CALCIUM CHANNEL; CALCIUM CHANNEL N TYPE;

ARTICLE; CALCIUM BINDING; CELL FUSION; CHANNEL GATING; GRAPHIC MODEL; MODEL; NEUROMUSCULAR JUNCTION; PRESYNAPTIC MEMBRANE; PROTEIN DOMAIN; SIMULATION; SYNAPSE; SYNAPSE VESICLE; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; METABOLISM; MOUSE; PROTEIN MULTIMERIZATION; PROTEIN TERTIARY STRUCTURE; RAT; XENOPUS;

ANIMALS; CALCIUM CHANNELS, N-TYPE; ION CHANNEL GATING; MICE; MODELS, NEUROLOGICAL; NEUROMUSCULAR JUNCTION; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; RATS; SYNAPTIC VESICLES; XENOPUS;

EID: 84978296341     PISSN: 19336950     EISSN: 19336969     Source Type: Journal    
DOI: 10.1080/19336950.2015.1098793     Document Type: Article

References (89)

1. Dodge FA Jr, Rahamimoff R. Co-operative action of calcium ions in transmitter release at the neuromuscular junction. J Physiol (Lond.) 1967; 193: 419-32; PMID: 6065887; http://dx.doi.org/10.1113/jphysiol.1967.sp008367
2. Stanley EF. Decline in calcium cooperativity as the basis of facilitation at the squid giant synapse. J Neurosci 1986; 6: 782-9; PMID: 2870141
3. Bollmann JH, Sakmann B, Borst JG. Calcium sensitivity of glutamate release in a calyx-type terminal. Science 2000; 289: 953-7; PMID: 10937999; http://dx.doi.org/10.1126/science.289.5481.953
4. 2+ signal. Nat Neurosci 2005; 8, 426-34; PMID: 15750590
5. Simon SM, Llinas RR. Compartmentalization of the submembrane calcium activity during calcium influx and its significance in transmitter release. Biophys J 1985; 48: 485-98; PMID: 2412607; http://dx.doi.org/10.1016/S0006-3495(85)83804-2
6. Zucker RS, Fogelson AL. Relationship between transmitter release and presynaptic calcium influx when calcium enters through discrete channels. Proc Natl Acad Sci U S A 1986; 83: 3032-6; PMID: 2422666; http://dx.doi.org/10.1073/pnas.83.9.3032
7. Schneggenburger R, Neher E. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature(Lond.) 2000; 406: 889-93; http://dx.doi.org/10.1038/35022702
8. Branco T, Staras K. The probability of neurotransmitter release: variability and feedback control at single synapses. Nat Rev Neurosci 2009; 10: 373-83; PMID: 19377502; http://dx.doi.org/10.1038/nrn2634
9. Llinas RR, Steinberg IZ, Walton K. Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse. Biophys J 1981; 33: 323-51; PMID: 6261850; http://dx.doi.org/10.1016/S0006-3495(81)84899-0
10. Chad JE, Eckert R. Calcium domains associated with individual channels can account for anomalous voltage relations of Ca-dependent responses. Biophys J 1984; 45: 993-99; PMID: 6329349; http://dx.doi.org/10.1016/S0006-3495(84)84244-7
11. Augustine GJ, Charlton MP. Calcium dependence of presynaptic calcium current and post-synaptic response at the squid giant synapse. J Physiol (Lond.) 1986; 381: 619-40; PMID: 2442355; http://dx.doi.org/10.1113/jphysiol.1986.sp016347
12. Fogelson AL, Zucker RS. Presynaptic calcium diffusion from various arrays of single channels. Biophys J 1985; 48: 1003-7; PMID: 2418887; http://dx.doi.org/10.1016/S0006-3495(85)83863-7
13. Yoshikami D, Bagaboldo Z, Olivera BM. The inhibitory effects of omega-conotoxins on Ca channel and synapses. Ann N Y Acad Sci 1989; 560: 230-48; PMID: 2545135; http://dx.doi.org/10.1111/j.1749-6632.1989.tb24100.x
14. Augustine GJ. Regulation of transmitter release at the squid giant synapse by presynaptic delayed rectifier potassium current. J Physiol (Lond.) 1990; 431: 343-64; PMID: 1983120; http://dx.doi.org/10.1113/jphysiol.1990.sp018333
15. Adler EM, Augustine GJ, Duffy SN, Charlton MP. Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse. J Neurosci 1991; 11, 1496-507; PMID: 1675264
16. Augustine GJ, Adler EM, Charlton MP. The calcium signal for transmitter secretion from presynaptic nerve terminals. Ann NY Acad Sci 1991; 635: 365-81; http://dx.doi.org/10.1111/j.1749-6632.1991.tb36505.x
17. Stanley EF. Single calcium channels and acetylcholine release at a presynaptic nerve terminal. Neuron 1993; 11: 1007-11; PMID: 8274272; http://dx.doi.org/10.1016/0896-6273(93)90214-C
18. Matveev V, Bertram R, Sherman A. Calcium cooperativity of exocytosis as a measure of Ca(2)C channel domain overlap. Brain Res 2011; 1398: 126-38; PMID: 21621748
19. 2+ microdomains on neurotransmitter release. Biophys J 1999; 76: 735-50; PMID: 9929478; http://dx.doi.org/10.1016/S0006-3495(99)77240-1
20. Mulligan SJ, Davison I, Delaney KR. Mitral cell presynaptic Ca(2C) influx and synaptic transmission in frog amygdala. Neuroscience 2001; 104: 137-51; PMID: 11311538; http://dx.doi.org/10.1016/S0306-4522(01)00057-4
21. Wachman ES, Poage RE, Stiles JR, Farkas DL, Meriney SD. Spatial distribution of calcium entry evoked by single action potentials within the presynaptic active zone. J Neurosci 2004; 24: 2877-85; PMID: 15044526; http://dx.doi.org/10.1523/JNEUROSCI.1660-03.2004
22. Gentile L, Stanley EF. A unified model of presynaptic release site gating by calcium channel domains. Eur J Neurosci 2005; 21: 278-82; PMID: 15654866; http://dx.doi.org/10.1111/j.1460-9568.2004.03841.x
23. Brandt A, Khimich D, Moser T. Few CaV1.3 channels regulate the exocytosis of a synaptic vesicle at the hair cell ribbon synapse. J Neurosci 2005; 25: 11577-85; PMID: 16354915; http://dx.doi.org/10.1523/JNEUROSCI.3411-05.2005
24. 2+ from one or two channels controls fusion of a single vesicle at the frog neuromuscular junction. J Neurosci 2006; 26: 13240-9; PMID: 17182774; http://dx.doi.org/10.1523/JNEUROSCI.1418-06.2006
25. Eggermann E, Bucurenciu I, Goswami SP, Jonas P. Nanodomain coupling between Ca(2) channels and sensors of exocytosis at fast mammalian synapses. Nat Rev Neurosci 2011; 13: 7-21; PMID: 22183436; http://dx.doi.org/10.1038/nrn3125
26. 2+ sensors promotes fast and efficient transmitter release at a cortical GABAergic synapse. Neuron 2008; 57: 536-45; PMID: 18304483; http://dx.doi.org/10.1016/j.neuron.2007.12.026
27. 2+ channels in the active zone shapes neurotransmitter release from Schaffer collateral synapses. J Neurosci 2012; 32: 18157-76; PMID: 23238730; http://dx.doi.org/10.1523/JNEUROSCI.3827-12.2012
28. 2+ channels and exocytosis at sensory synapses. J Physiol 2013; 591: 3167-78; PMID: 23459757; http://dx.doi.org/10.1113/jphysiol.2012.249482
29. Tarr TB, Dittrich M, Meriney SD. Are unreliable release mechanisms conserved from NMJ to CNS? Trends Neurosci 2013; 36: 14-22; PMID: 23102681; http://dx.doi.org/10.1016/j.tins.2012.09.009
30. 2+ channels carry the largest current: implications for nanodomains and transmitter release. Nat Neurosci 2010; 13, 1348-50; PMID: 20953196; http://dx.doi.org/10.1038/nn.2657
31. 2+] at the month of a calcium channel. J Neurosci 1997; 17: 6961-73; PMID: 9278532
32. 2+ channel cooperativity of exocytosis. J Neurosci 2009; 29: 12196-209; PMID: 19793978; http://dx.doi.org/10.1523/JNEUROSCI.0263-09.2009
33. Robitaille R, Adler EM, Charlton MP. Strategic location of calcium channels at transmitter release sites of frog neuromuscular synapses. Neuron 1990; 5: 773-9; PMID: 1980068; http://dx.doi.org/10.1016/0896-6273(90)90336-E
34. Heuser JE, Reese TS, Landis DMD. Functional changes in frog neuromuscular junctions studied with freeze fracture. J Neurocytol 1974; 3, 109-31; PMID: 4596345; http://dx.doi.org/10.1007/BF01111936
35. Pumplin DW, Reese TS, Llinas RR. Are the presynaptic membrane particles the calcium channels? Proc Natl Acad Sci U S A 1981; 78: 7210-3; PMID: 6273920; http://dx.doi.org/10.1073/pnas.78.11.7210
36. Venzin M, Sandri C, Akert K, Wyss UR. Membrane associated particles of the presynaptic active zone in rat spinal cord. A morphometric analysis. Bain Res 1977; 130: 393-404.
37. Luo F, Dittrich M, Stiles JR, Meriney SD. Single-pixel optical fluctuation analysis of calcium channel function in active zones of motor nerve terminals. J Neurosci 2011; 31: 11268-81; PMID: 21813687; http://dx.doi.org/10.1523/JNEUROSCI.1394-11.2011
38. Luo F, Dittrich M, Cho S, Stiles JR, Meriney SD. Transmitter release is evoked with low probability predominately by calcium flux through single channel openings at the frog neuromuscular junction. J Neurophysiol 2015; 113(7): 2480-9.
39. Stanley EF. The calcium channel and the organization of the presynaptic transmitter release face. TINS 1997; 20: 404-9; PMID: 9292969
40. Fedchyshyn MJ, Wang LY. Developmental transformation of the release modality at the calyx of held synapse. J Neurosci 2005; 25, 4131-40; PMID: 15843616; http://dx.doi.org/10.1523/JNEUROSCI.0350-05.2005
41. Wang LY, Neher E, Taschenberger H. Synaptic vesicles in mature calyx of Held synapses sense higher nanodomain calcium concentrations during action potentialevoked glutamate release. J Neurosci 2008; 28: 14450-8; PMID: 19118179; http://dx.doi.org/10.1523/ JNEUROSCI.4245-08.2008
42. 2+-secretion coupling at the rat calyx of Held. J Physiol 2009; 587: 3009-23; PMID: 19403608; http://dx.doi.org/10.1113/jphysiol.2009.172387
43. 2+. Nat Neurosci 2010; 13, 838-44; PMID: 20562869; http://dx.doi.org/10.1038/nn.2576
44. Schneggenburger R, Han Y, Kochubey O. Ca(2C) channels and transmitter release at the active zone. Cell Calcium 2012; 52: 199-207; PMID: 22682961; http://dx.doi.org/10.1016/j.ceca.2012.04.011
45. Erazo-Fischer E, Striessnig J, Taschenberger H. The role of physiological afferent nerve activity during in vivo maturation of the calyx of Held synapse. J Neurosci 2007; 27, 1725-37; PMID: 17301180; http://dx.doi.org/10.1523/JNEUROSCI.4116-06.2007
46. 2+ current and its efficacy in triggering transmitter release at the developing calyx of held synapse. J Neurosci 2006; 26, 5698-708; PMID: 16723526; http://dx.doi.org/10.1523/ JNEUROSCI.4889-05.2006
47. Iwasaki S, Takahashi T. Developmental regulation of transmitter release at the calyx of Held in rat auditory brainstem. J Physiol 2001; 534: 861-71; PMID: 11483715; http://dx.doi.org/10.1111/j.1469-7793.2001.00861.x
48. Jewett DL, Romano MN. Neonatal development of auditory system potentials averaged from the scalp of rat and cat. Brain Res 1972; 36: 101-15; PMID: 5008374; http://dx.doi.org/10.1016/0006-8993(72)90769-X
49. Borst JG, Sakmann B. Calcium influx and transmitter release in a fast CNS synapse. Nature(Lond.) 1996; 383: 431-5; http://dx.doi.org/10.1038/383431a0
50. Fedchyshyn MJ, Wang LY. Activity-dependent changes in temporal components of neurotransmission at the juvenile mouse calyx of Held synapse. J Physiol 2007; 581: 581-602; PMID: 17347264; http://dx.doi.org/10.1113/jphysiol.2007.129833
51. Indriati DW, Kamasawa N, Matsui K, Meredith AL, Watanabe M, Shigemoto R. Quantitative localization of Cav2.1 (P/Q-type) voltage-dependent calcium channels in Purkinje cells: somatodendritic gradient and distinct somatic coclustering with calcium-activated potassium channels. J Neurosci 2013; 33: 3668-78; PMID: 23426693; http://dx.doi.org/10.1523/JNEUROSCI.2921-12.2013
52. Nakamura Y, Harada H, Kamasawa N, Matsui K, Rothman JS, Shigemoto R, Silver RA, DiGregorio DA, Takahashi T. Nanoscale distribution of presynaptic Ca (2C) channels and its impact on vesicular release during development. Neuron 2015; 85: 145-58; PMID: 25533484; http://dx.doi.org/10.1016/j.neuron.2014.11.019
53. Stanley EF. Presynaptic calcium channels and the transmitter release mechanism. Ann N Y Acad Sci 1993; 681: 368-72; PMID: 8102841; http://dx.doi.org/10.1111/j.1749-6632.1993.tb22915.x
54. Sheng J, He L, Zheng H, Xue L, Luo F, Shin W, Sun T, Kuner T, Yue DT, Wu LG. Calcium-channel number critically influences synaptic strength and plasticity at the active zone. Nat Neurosci 2012; 15, 998-1006; PMID: 22683682; http://dx.doi.org/10.1038/nn.3129
55. Thomson AM. Facilitation, augmentation and potentiation at central synapses. Trends Neurosci 2000; 23: 305-12; PMID: 10856940; http://dx.doi.org/10.1016/S0166-2236(00)01580-0
56. Gonzalez JC, Lignani G, Maroto M, Baldelli P, Hernandez-Guijo JM. Presynaptic muscarinic receptors reduce synaptic depression and facilitate its recovery at hippocampal GABAergic synapses. Cereb Cortex 2014; 24: 1818-31; http://dx.doi.org/10.1093/cercor/bht032
57. Wang LY, Fedchyshyn MJ, Yang YM. Action potential evoked transmitter release in central synapses: insights from the developing calyx of Held. Mol Brain 2009; 2: 36; PMID: 19939269; http://dx.doi.org/10.1186/1756-6606-2-36
58. 2+ Microdomain and Neurotransmitter Exocytosis: A Monte Carlo Study. Biophys J 2004; 87: 2352-64; PMID: 15454435; http://dx.doi.org/10.1529/biophysj.104.043380
59. 2+ signal for phasic transmitter release at the rat calyx of Held. J Physiol 2003; 547: 665-89; PMID: 12562955
60. Stanley EF. The calcium channel and the organization of the presynaptic transmitter release face. Trends Neurosci 1997; 20: 404-9; PMID: 9292969; http://dx.doi.org/10.1016/S0166-2236(97)01091-6
61. Koike-Tani M, Kanda T, Saitoh N, Yamashita T, Takahashi T. Involvement of AMPA receptor desensitization in short-term synaptic depression at the calyx of Held in developing rats. J Physiol 2008; 586: 2263-75; http://dx.doi.org/10.1113/jphysiol.2007.142547
62. Iwasaki S, Takahashi T. Developmental changes in calcium channel types mediating synaptic transmission in rat auditory brainstem. J Physiol (Lond) 1998; 509: 419-23; PMID: 9575291; http://dx.doi.org/10.1111/j.1469-7793.1998.419bn.x
63. Matveev V. Calcium-Dependent Exocytosis, Biophysical Models of in Encyclopedia of Computational Neuroscience (eds. Jaeger D, Jung R) 1-17 (Springer New York, 2014).
64. Bennett MR, Farnell L, Gibson WG. The probability of quantal secretion within an array of calcium channels of an active zone. Biophys J 2000; 78: 2222-40; PMID: 10777722; http://dx.doi.org/10.1016/S0006-3495(00)76770-1
65. Bertram R, Sherman AD, Stanley EF. The single domain/bound calcium hypothesis of transmitter release and facilitation. J Neurophysiol 1996; 75: 1919-31; PMID: 8734591
66. 2+-sensor saturation for neurotransmitter release. J Neurophysiol 2005; 94: 1912-9; PMID: 15888526; http://dx.doi.org/10.1152/jn.00256.2005
67. Meinrenken CJ, Borst JG, Sakmann B. Calcium secretion coupling at calyx of held governed by nonuniform channel-vesicle topography. J Neurosci 2002; 22: 1648-67; PMID: 11880495
68. 2+ channels and release sensors at a plastic hippocampal synapse. Science 2014; 343: 665-70; PMID: 24503854; http://dx.doi.org/10.1126/science.1244811
69. Soldo BL, Giovannucci DR, Stuenkel EL, Moises HC. Ca(2C) and frequency dependence of exocytosis in isolated somata of magnocellular supraoptic neurones of the rat hypothalamus. J Physiol 2004; 555: 699-711; PMID: 14645448; http://dx.doi.org/10.1113/jphysiol.2003.051136
70. Baur D, Bornschein G, Althof D, Watanabe M, Kulik A, Eilers J, Schmidt H. Developmental tightening of cerebellar cortical synaptic influx-release coupling. J Neurosci 2015; 35: 1858-71; PMID: 25653347; http://dx.doi.org/10.1523/JNEUROSCI.2900-14.2015
71. Okawa H, Hoon M, Yoshimatsu T, Della SL, Wong RO. Illuminating the multifaceted roles of neurotransmission in shaping neuronal circuitry. Neuron 2014; 83: 1303-18; PMID: 25233313; http://dx.doi.org/10.1016/j.neuron.2014.08.029
72. 2+ influx and exocytosis in sensory hair cells. Proc Natl Acad Sci U S A 2015; 112, E1028-37; PMID: 25691754; http://dx.doi.org/10.1073/pnas.1416424112
73. Schmidt H, Brachtendorf S, Arendt O, Hallermann S, Ishiyama S, Bornschein G, Gall D, Schiffmann SN, Heckmann M, Eilers J. Nanodomain coupling at an excitatory cortical synapse. Curr Biol 2013; 23: 244-9; PMID: 23273895; http://dx.doi.org/10.1016/j.cub.2012.12.007
74. Bucurenciu I, Bischofberger J, Jonas P. A small number of open Ca(2C) channels trigger transmitter release at a central GABAergic synapse. Nat Neurosci 2010; 13, 19-21; PMID: 20010820; http://dx.doi.org/10.1038/nn.2461
75. 2+ Channels around Docked Vesicles Explains Release Control by Multiple Channels at a CNS Synapse. PLoS Comput Biol 2015; 11: e1004253; PMID: 25951120; http://dx.doi.org/10.1371/journal.pcbi.1004253
76. Harlow ML, Szule JA, Xu J, Jung JH, Marshall RM, McMahan UJ. Alignment of synaptic vesicle macromolecules with the macromolecules in active zone material that direct vesicle docking. PLoS ONE 2013; 8: e69410; PMID: 23894473; http://dx.doi.org/10.1371/journal.pone.0069410
77. Nagwaney S, Harlow ML, Jung JH, Szule JA, Ress D, Xu J, Marshall RM, McMahan UJ. Macromolecular connections of active zone material to docked synaptic vesicles and presynaptic membrane at neuromuscular junctions of mouse. J Comp Neurol 2009; 513: 457-68; PMID: 19226520; http://dx.doi.org/10.1002/cne.21975
78. Harlow M, Ress D, Koster A, Marshall RM, Schwarz M, McMahan UJ. Dissection of active zones at the neuromuscular junction by EM tomography. J Physiol Paris 1998; 92: 75-8; PMID: 9782447; http://dx.doi.org/10.1016/S0928-4257(98)80141-1
79. Mochida S, Westenbroek RE, Yokoyama CT, Zhong H, Myers SJ, Scheuer T, Itoh K, Catterall WA. Requirement for the synaptic protein interaction site for reconstitution of synaptic transmission by P/Q-type calcium channels. Proc Natl Acad Sci U S A 2003; 100: 2819-24; PMID: 12601156; http://dx.doi.org/10.1073/pnas.262787699
80. Wong FK, Li Q, Stanley EF. Synaptic vesicle capture by CaV2.2 calcium channels. Front Cell Neurosci 2013; 7: 101; PMID: 23874268
81. 2+ channels and snare proteins in neurotransmitter release. Ann N Y Acad Sci 1999; 868: 144-59; PMID: 10414292; http://dx.doi.org/10.1111/j.1749-6632.1999.tb11284.x
82. Sheng ZH, Westenbroek RE, Catterall WA. Physical link and functional coupling of presynaptic calcium channels and the synaptic vesicle docking/fusion machinery. J Bioenerg Biomembr 1998; 30, 335-45; PMID: 9758330; http://dx.doi.org/10.1023/A: 1021985521748
83. Llinas RR, Sugimori M, Simon SM. Transmission by presynaptic spike-like depolarization in the squid giant synapse. Proc Natl Acad Sci U S A 1982; 79: 2415-9; PMID: 6954549; http://dx.doi.org/10.1073/pnas.79.7.2415
84. Luvisetto S, Fellin T, Spagnolo M, Hivert B, Brust PF, Harpold MM, Stauderman KA, Williams ME, Pietrobon D. Modal gating of human CaV2.1 (P/Q-type) calcium channels: I. The slow and the fast gating modes and their modulation by β subunits. J Gen Physiol 2004; 124: 445-61; PMID: 15504896; http://dx.doi.org/10.1085/jgp.200409034
85. Stanley EF. PresyNaptic calcium channels: why is P selected before N? Biophys J 2015; 108: 451-2; PMID: 25650909; http://dx.doi.org/10.1016/j.bpj.2014.12.021
86. 2+. J Neurophysiol 1999; 81: 634-42; PMID: 10036266
87. Parnas H, Segel LA. A theoretical explanation for some effects of calcium on the facilitation of neurotransmitter release. J Theor Biol 1980; 84: 3-29; PMID: 6106090; http://dx.doi.org/10.1016/S0022-5193(80)81035-6
88. Haydon PG, Henderson E, Stanley EF. Localization of individual calcium channels at the release face of a presynaptic nerve terminal. Neuron 1994; 13: 1275-80; PMID: 7993621; http://dx.doi.org/10.1016/0896-6273(94)90414-6
89. Stanley EF, Reese TS, Wang GZ. Molecular scaffold reorganization at the transmitter release site with vesicle exocytosis or botulinum toxin C1. Eur J Neurosci 2003; 18: 2403-7; PMID: 14622203; http://dx.doi.org/10.1046/j.1460-9568.2003.02948.x