Calcium cooperativity of exocytosis as a measure of Ca 2+ channel domain overlap

Brain Research

Volumn 1398, Issue , 2011, Pages 126-138

  Matveev, Victor ^a   Bertram, Richard ^b   Sherman, Arthur ^c  

^a NEW JERSEY INSTITUTE OF TECHNOLOGY   (United States)

^b FLORIDA STATE UNIVERSITY   (United States)

^c NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Active zone; Calcium buffer; Calcium cooperativity; Calcium diffusion; Channel cooperativity; Current cooperativity; Exocytosis; Modeling; Presynaptic; Synaptic transmission

Indexed keywords

CALCIUM CHANNEL; CALCIUM CHANNEL BLOCKING AGENT; CALCIUM ION; NEUROTRANSMITTER;

CALCIUM TRANSPORT; CONCENTRATION (PARAMETERS); EXOCYTOSIS; MEMBRANE VESICLE; MORPHOLOGY; NEUROCHEMISTRY; NEUROTRANSMITTER RELEASE; NONHUMAN; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; REVIEW; SYNAPSE; SYNAPTIC TRANSMISSION; VOLTAGE CLAMP;

ANIMALS; CALCIUM CHANNELS; CALCIUM SIGNALING; CENTRAL NERVOUS SYSTEM; EXOCYTOSIS; HUMANS; PROTEIN STRUCTURE, TERTIARY; SYNAPSES;

EID: 79958851367     PISSN: 00068993     EISSN: 00068993     Source Type: Journal    
DOI: 10.1016/j.brainres.2011.05.011     Document Type: Review

References (88)

1. 2+ channel trigger secretion with different efficacies in chromaffin cells. Nature 367, 72-76.
2. Augustine, G.J., 1990. Regulation of transmitter release at the squid giant synapse by presynaptic delay rectifier potassium current. J. Physiol. (London) 431, 343-364.
3. Augustine, G.J., Charlton, M.P., 1986. Calcium dependence of presynaptic calcium current and postsynaptic response at the squid giant synapse. J. Physiol. (London) 381, 619-640.
4. Augustine, G.J., Charlton, M.P., Smith, S.J., 1985. Calcium entry and transmitter release at voltage-clamped nerve terminals of squid. J. Physiol. (London) 367, 163-181.
5. Augustine, G.J., Adler, E.M., Charlton, M.P., 1991. The calcium signal for transmitter secretion from presynaptic nerve terminals. Ann. N.Y. Acad. Sci. 635, 365-381.
6. Augustine, G.J., Santamaria, F., Tanaka, K., 2003. Local calcium signaling in neurons. Neuron 40, 331-346. (Pubitemid 37244099)
7. Bertram, R., Smith, G.D., Sherman, A., 1999. Modeling study of the effects of overlapping Ca2+ microdomains on neurotransmitter release. Biophys. J. 76, 735-750. (Pubitemid 29264556)
8. Beutner, D., Voets, T., Neher, E., Moser, T., 2001. Calcium dependence of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse. Neuron 29, 681-690. (Pubitemid 32323941)
9. Bevan, S., Wendon, L.M., 1984. A study of the action of tetanus toxin at rat soleus neuromuscular junctions. J. Physiol. 348, 1-17. (Pubitemid 14061841)
10. Bollmann, J.H., Sakmann, B., Borst, J.G., 2000. Calcium sensitivity of glutamate release in a calyx-type terminal. Science 289, 953-957. (Pubitemid 30659948)
11. Borst, J.G.G., Sakmann, B., 1996. Calcium influx and transmitter release in a fast CNS synapse. Nature 383, 431-434. (Pubitemid 26330830)
12. Borst, J.G.G., Sakmann, B., 1998. Calcium current during a single action potential in a large presynaptic terminal of the rat brainstem. J. Physiol. 506, 143-157. (Pubitemid 28046043)
13. Brandt, A., Khimich, D., Moser, T., 2005. Few CaV1.3 channels regulate the exocytosis of a synaptic vesicle at the hair cell ribbon synapse. J. Neurosci. 25, 11577-11585. (Pubitemid 43098450)
14. 2+ sensors promotes fast and efficient transmitter release at a cortical GABAergic synapse. Neuron 57, 536-545.
15. 2+ channels trigger transmitter release at a central GABAergic synapse. Nat. Neurosci. 13, 19-21.
16. Ceccarelli, B., Grohovaz, F., Hurlbut, W.P., 1979. Freeze-fracture studies of frog neuromuscular junctions during intense release of neurotransmitter. II. Effects of electrical stimulation and high potassium. J. Cell Biol. 81, 178-192.
17. Chad, J.E., Eckert, R., 1984. Calcium domains associated with individual channels can account for anomalous voltage relations of CA-dependent responses. Biophys. J. 45, 993-999.
18. Coggins, M., Zenisek, D., 2009. Evidence that exocytosis is driven by calcium entry through multiple calcium channels in goldfish retinal bipolar cells. J. Neurophysiol. 101, 2601-2619.
19. Cull-Candy, S.G., Lundh, H., Thesleff, S., 1976. Effects of botulinum toxin on neuromuscular transmission in the rat. J. Physiol. 260, 177-203.
20. Dodge, F.A., Rahamimoff, R., 1967. Cooperative action of calcium ions in transmitter release at the neuromuscular junction. J. Physiol. 193, 419-432.
21. Dulon, D., Safieddine, S., Jones, S.M., Petit, C., 2009. Otoferlin is critical for a highly sensitive and linear calcium-dependent exocytosis at vestibular hair cell ribbon synapses. J. Neurosci. 29, 10474-10487.
22. Duncan, G., Rabl, K., Gemp, I., Heidelberger, R., Thoreson, W.B., 2010. Quantitative analysis of synaptic release at the photoreceptor synapse. Biophys. J. 98, 2102-2110.
23. Fedchyshyn, M.J., Wang, L.Y., 2005. Developmental transformation of the release modality at the calyx of Held synapse. J. Neurosci. 25, 4131-4140. (Pubitemid 40563389)
24. Felmy, F., Neher, E., Schneggenburger, R., 2003. Probing the intracellular calcium sensitivity of transmitter release during synaptic facilitation. Neuron 37, 801-811. (Pubitemid 36288552)
25. Fernandez-Chacon, R., Konigstorfer, A., Gerber, S.H., Garcia, J., Matos, M.F., Stevens, C.F., Brose, N., Rizo, J., Rosenmund, C., Sudhof, T.C., 2001. Synaptotagmin I functions as a calcium regulator of release probability. Nature 410, 41-49. (Pubitemid 32225830)
26. Fettiplace, R., Fuchs, P.A., 1999. Mechanisms of hair cell tuning. Annu. Rev. Physiol. 61, 809-834.
27. Fogelson, A.L., Zucker, R.S., 1985. Presynaptic calcium diffusion from various arrays of single channels. Implications for transmitter release and synaptic facilitation. Biophys. J. 48, 1003-1017.
28. Gentile, L., Stanley, E.F., 2005. A unified model of presynaptic release site gating by calcium channel domains. Eur. J. Neurosci. 21, 278-282.
29. 2+ sensor for transmitter release at a central synapse. Cell 79, 717-727.
30. Goda, Y., Stevens, C.F., 1994. Two components of transmitter release at a central synapse. Proc. Natl Acad. Sci. U. S. A. 91, 12942-12946.
31. Goutman, J.D., Glowatzki, E., 2007. Time course and calcium dependence of transmitter release at a single ribbon synapse. Proc. Natl Acad. Sci. U. S. A. 104, 16341-16346.
32. Harlow, M.L., Ress, D., Stoschek, A., Marshall, R.M., McMahan, U.J., 2001. The architecture of active zone material at the frog's neuromuscular junction. Nature 409, 479-484. (Pubitemid 32144346)
33. Heuser, J.E., Reese, T.S., Dennis, M.J., Jan, Y., Jan, L., Evans, L., 1979. Synaptic vesicle exocytosis captured by quick freezing and correlated with quantal transmitter release. J. Cell Biol. 81, 275-300. (Pubitemid 9162935)
34. Iwasaki, S., Takahashi, T., 1998. Developmental changes in calcium channel types mediating synaptic transmission in rat auditory brainstem. J. Physiol. 509 (Pt 2), 419-423. (Pubitemid 28287000)
35. Jarsky, T., Tian, M., Singer, J.H., 2010. Nanodomain control of exocytosis is responsible for the signaling capability of a retinal ribbon synapse. J. Neurosci. 30, 11885-11895.
36. Johnson, S.L., Marcotti, W., Kros, C.J., 2005. Increase in efficiency and reduction in Ca2+ dependence of exocytosis during development of mouse inner hair cells. J. Physiol. 563, 177-191. (Pubitemid 40340374)
37. Johnson, S.L., Forge, A., Knipper, M., Munkner, S., Marcotti, W., 2008. Tonotopic variation in the calcium dependence of neurotransmitter release and vesicle pool replenishment at mammalian auditory ribbon synapses. J. Neurosci. 28, 7670-7678.
38. 2+ dependence of vesicle fusion at auditory ribbon synapses. Nat. Neurosci. 13, 45-52.
39. Katz, B., Miledi, R., 1970. A further study in the role of calcium in synaptic transmission. J. Physiol. 207, 789-801.
40. Keen, E.C., Hudspeth, A.J., 2006. Transfer characteristics of the hair cell's afferent synapse. Proc. Natl Acad. Sci. U. S. A. 103, 5537-5542.
41. 2+-secretion coupling at the rat calyx of Held. J. Physiol. 587, 3009-3023.
42. 2+ chelators. J. Neurophysiol. 72, 825-830.
43. Lester, H.A., 1970. Transmitter release by presynaptic impulses in the squid stellate ganglion. Nature 227, 493-496.
44. 2+ channels in hippocampal mossy fiber boutons. J. Neurosci. 27, 13420-13429.
45. Llinas, R., Sugimori, M., Simon, S.M., 1982. Transmission by presynaptic spike-like depolarization in the squid giant synapse. Proc. Natl Acad. Sci. U. S. A. 79, 2415-2419.
46. Llinás, R., Steinberg, I.Z., Walton, K., 1981. Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse. Biophys. J. 33, 323-352.
47. 2+ sensor for vesicle fusion. Nature 435, 497-501.
48. Luo, F., Dittrich, M., Stiles, J.R., Meriney, S.D., 2008. Quantitative analysis of single channel openings and evoked transmitter release from active zones. Abstracts of the Society for Neuroscience Annual Meeting. . Washington, D.C. Program 34.1.
49. Matveev, V., 2008. CalC (Calcium Calculator) simulation software, release version 6.0.5URL: http://www.calciumcalculator.org.
50. 2+ channel cooperativity of exocytosis. J. Neurosci. 29, 12196-12209.
51. Meinrenken, C.J., Borst, J.G., Sakmann, B., 2002. Calcium secretion coupling at calyx of held governed by nonuniform channel-vesicle topography. J. Neurosci. 22, 1648-1667. (Pubitemid 35386284)
52. Mintz, I.M., Sabatini, B.L., Regehr, W.G., 1995. Calcium control of transmitter release at a cerebellar synapse. Neuron 15, 675-688.
53. Mirghomizadeh, F., Pfister, M., Apaydin, F., Petit, C., Kupka, S., Pusch, C.M., Zenner, H.P., Blin, N., 2002. Substitutions in the conserved C2C domain of otoferlin cause DFNB9, a form of nonsyndromic autosomal recessive deafness. Neurobiol. Dis. 10, 157-164.
54. Nagy, G., Kim, J.H., Pang, Z.P., Matti, U., Rettig, J., Sudhof, T.C., Sorensen, J.B., 2006. Different effects on fast exocytosis induced by synaptotagmin 1 and 2 isoforms and abundance but not by phosphorylation. J. Neurosci. 26, 632-643. (Pubitemid 43237128)
55. Neher, E., 1998a. Vesicle pools and Ca2+ microdomains: new tools for understanding their roles in neurotransmitter release. Neuron 20, 389-399. (Pubitemid 28153073)
56. ++ signals. Cell Calcium 24, 345-357.
57. 2+ triggering of neurotransmitter release in central and neuromuscular synapses. J. Neurosci. 26, 13493-13504.
58. Pumplin, D.W., Reese, T.S., Llinas, R., 1981. Are the presynaptic membrane particles the calcium channels? Proc. Natl Acad. Sci. U. S. A. 78, 7210-7213.
59. Qian, S.M., Delaney, K.R., 1997. Neuromodulation of activity-dependent synaptic enhancement at crayfish neuromuscular junction. Brain Res. 771, 259-270. (Pubitemid 27492104)
60. Qian, J., Noebels, J.L., 2001. Presynaptic Ca2+ channels and neurotransmitter release at the terminal of a mouse cortical neuron. J. Neurosci. 21, 3721-3728. (Pubitemid 32466463)
61. 2+ entry at the mouse motor nerve terminal: role of stochastic factors causing heterogeneity. Neuroscience 51, 657-671.
62. 2+ and asynchronous transmitter release from the same crayfish bouton. J. Physiol. 501, 250-262.
63. Reid, C.A., Clements, J.D., Bekkers, J.M., 1997. Nonuniform distribution of Ca2+ channel subtypes on presynaptic terminals of excitatory synapses in hippocampal cultures. J. Neurosci. 17, 2738-2745. (Pubitemid 27155007)
64. Reid, C.A., Bekkers, J.M., Clements, J.D., 1998. N- and P/Q-type Ca2+ channels mediate transmitter release with a similar cooperativity at rat hippocampal autapses. J. Neurosci. 18, 2849-2855. (Pubitemid 28163215)
65. 2+-channel blockers. Neuron 14, 773-779.
66. Rizo, J., Rosenmund, C., 2008. Synaptic vesicle fusion. Nat. Struct. Mol. Biol. 15, 665-674.
67. Roux, I., Safieddine, S., Nouvian, R., Grati, M., Simmler, M.C., Bahloul, A., Perfettini, I., Le Gall, M., Rostaing, P., Hamard, G., Triller, A., Avan, P., Moser, T., Petit, C., 2006. Otoferlin, defective in a human deafness form, is essential for exocytosis at the auditory ribbon synapse. Cell 127, 277-289. (Pubitemid 44572372)
68. Sabatini, B.L., Regehr, W.G., 1997. Control of neurotransmitter release by presynaptic waveform at the granule cell to Purkinje cell synapse. J. Neurosci. 15, 3425-3435. (Pubitemid 27200572)
69. Sakaba, T., Neher, E., 2001. Quantitative relationship between transmitter release and calcium current at the calyx of held synapse. J. Neurosci. 21, 462-476. (Pubitemid 32107436)
70. Schneggenburger, R., Neher, E., 2000. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406, 889-893.
71. Schneggenburger, R., Neher, E., 2005. Presynaptic calcium and control of vesicle fusion. Curr. Opin. Neurobiol. 15, 266-274.
72. Shahrezaei, V., Cao, A., Delaney, K.R., 2006. Ca2+ from one or two channels controls fusion of a single vesicle at the frog neuromuscular junction. J. Neurosci. 26, 13240-13249. (Pubitemid 46011634)
73. Simon, S.M., Llinas, R.R., 1985. Compartmentalization of the submembrane calcium activity during calcium influx and its significance in transmitter release. Biophys. J. 48, 485-498. (Pubitemid 15238291)
74. Stanley, E.F., 1986. Decline in calcium cooperativity as the basis of facilitation at the squid giant synapse. J. Neurosci. 6, 782-789. (Pubitemid 16134917)
75. Stanley, E.F., 1993. Single calcium channels and acetylcholine release at a presynaptic nerve terminal. Neuron 11, 1007-1011. (Pubitemid 24015275)
76. Stanley, E.F., Reese, T.S., Wang, G.Z., 2003. Molecular scaffold reorganization at the transmitter release site with vesicle exocytosis or botulinum toxin C1. Eur. J. Neurosci. 18, 2403-2407.
77. Stevens, C.F., Sullivan, J.M., 2003. The synaptotagmin C2A domain is part of the calcium sensor controlling fast synaptic transmission. Neuron 39, 299-308. (Pubitemid 36897551)
78. Stewart, B.A., Mohtashami, M., Trimble, W.S., Boulianne, G.L., 2000. SNARE proteins contribute to calcium cooperativity of synaptic transmission. Proc. Natl Acad. Sci. U. S. A. 97, 13955-13960.
79. Sun, J., Pang, Z.P., Qin, D., Fahim, A.T., Adachi, R., Sudhof, T.C., 2007. A dual-Ca2+-sensor model for neurotransmitter release in a central synapse. Nature 450, 676-682. (Pubitemid 350207687)
80. Thoreson, W.B., Rabl, K., Townes-Anderson, E., Heidelberger, R., 2004. A highly Ca2+-sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse. Neuron 42, 595-605. (Pubitemid 38639879)
81. Wu, L.-G., Saggau, P., 1994. Pharmacological identification of two types of presynaptic voltage-dependent calcium channels at CA3-CA1 synapses of the hippocampus. J. Neurosci. 14, 5613-5622.
82. 2+ currents evoke transmitter release at a rat central synapse. Proc. Natl Acad. Sci. U. S. A. 95, 4720-4725.
83. Wu, L.G., Westenbroek, R.E., Borst, J.G., Catterall, W.A., Sakmann, B., 1999. Calcium channel types with distinct presynaptic localization couple differentially to transmitter release in single calyx-type synapses. J. Neurosci. 19, 726-736. (Pubitemid 29036024)
84. Xu, J., Mashimo, T., Sudhof, T.C., 2007. Synaptotagmin-1, -2, and -9: Ca(2+) sensors for fast release that specify distinct presynaptic properties in subsets of neurons. Neuron 54, 567-581. (Pubitemid 46756145)
85. 2+ cooperativity in pituitary gonadotropes. J. Gen. Physiol. 125, 327-334.
86. Yang, Y.M., Fedchyshyn, M.J., Grande, G., Aitoubah, J., Tsang, C.W., Xie, H., Ackerley, C.A., Trimble, W.S., Wang, L.Y., 2010. Septins regulate developmental switching from microdomain to nanodomain coupling of Ca(2+) influx to neurotransmitter release at a central synapse. Neuron 67, 100-115.
87. Yoshikami, D., Bagabaldo, Z., Olivera, B.M., 1989. The inhibitory effects of omega-conotoxins on Ca channels and synapses. Ann. N.Y. Acad. Sci. 560, 230-248.
88. Zucker, R.S., Fogelson, A.L., 1986. Relationship between transmitter release and presynaptic calcium influx when calcium enters through discrete channels. Proc. Natl Acad. Sci. U. S. A. 83, 3032-3036.