Single Ca2+ channels and exocytosis at sensory synapses

Journal of Physiology

Volumn 591, Issue 13, 2013, Pages 3167-3178

  Kim, Mean Hwan ^a   Li, Geng Lin ^b   von Gersdorff, Henrique ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; PHOSPHOLIPID;

ARTICLE; CALCIUM CURRENT; CELL FUNCTION; CELLULAR DISTRIBUTION; ENDOCYTOSIS; EXOCYTOSIS; FLOW KINETICS; INFORMATION SYSTEM; MULTIVESICULAR BODY; NERVE CELL MEMBRANE STEADY POTENTIAL; NEUROTRANSMITTER RELEASE; NONHUMAN; PHOTORECEPTOR; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN LIPID INTERACTION; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; SYNAPTIC MEMBRANE; ANIMAL; EXCITATORY POSTSYNAPTIC POTENTIAL; PHYSIOLOGY; SYNAPSE; REVIEW;

ANIMALS; CALCIUM CHANNELS; ENDOCYTOSIS; EXCITATORY POSTSYNAPTIC POTENTIALS; EXOCYTOSIS; PHOSPHOLIPIDS; SYNAPSES;

EID: 84879842265     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2012.249482     Document Type: Article

References (88)

1. Augustine GJ, Adler EM & Charlton MP (1991). The calcium signal for transmitter secretion from presynaptic nerve terminals. Ann N Y Acad Sci 635, 365-381.
2. Babai N, Bartoletti TM & Thoreson WB (2010). Calcium regulates vesicle replenishment at the cone ribbon synapse. J Neurosci 30, 15866-15877.
3. 2+ channels. J Neurophysiol 106, 2922-2935.
4. Beaumont V, Llobet A & Lagnado L (2005). Expansion of calcium microdomains regulates fast exocytosis at a ribbon synapse. Proc Natl Acad Sci U S A 102, 10700-10705.
5. 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.
6. Borst JG & Sakmann B (1996). Calcium influx and transmitter release in a fast CNS synapse. Nature 383, 431-434.
7. V1.3 channels regulate the exocytosis of a synaptic vesicle at the hair cell ribbon synapse. J Neurosci 25, 11577-11585.
8. Brockerhoff SE (2011). Phosphoinositides and photoreceptors. Mol Neurobiol 44, 420-425.
9. Buran BN, Strenzke N, Neef A, Gundelfinger ED, Moser T & Liberman MC (2010). Onset coding is degraded in auditory nerve fibers from mutant mice lacking synaptic ribbons. J Neurosci 30, 7587-7597.
10. 2+ channel signaling complexes in neurons. J Neurochem 105, 573-583.
11. Chernomordik LV, Zimmerberg J & Kozlov MM (2006). Membranes of the world unite! J Cell Biol 175, 201-207.
12. 2+ dependent at auditory hair cell synapses. J Neurosci 31, 5682-5692.
13. 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.
14. Copenhagen DR (2004). Excitation in the retina: the flow, filtering, and molecules of visual signaling in the glutamatergic pathways from photoreceptors to ganglion cells. In The Visual Neurosciences, vol. 1, ed. Chalupa LM, Werner JS, pp. 320-333. MIT Press, Cambridge, MA, USA
15. Demb JB & von Gersdorff H (2008). Ultraweak signals can cause synaptic depression and adaptation. Neuron 57, 802-804.
16. Denker A & Rizzoli SO (2010). Synaptic vesicle pools: an update. Front Synap Neurosci 2, 135.
17. v1.2 channels. Proc Natl Acad Sci U S A 109, 1749-1754.
18. Dulon D, Safieddine S, Jones SM & 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.
19. 2+ channels and sensors of exocytosis at fast mammalian synapses. Nat Rev Neurosci 13, 7-21.
20. Edmonds BW, Gregory FD & Schweizer FE (2004). Evidence that fast exocytosis can be predominantly mediated by vesicles not docked at active zones in frog saccular hair cells. J Physiol 560, 439-450.
21. Emran F, Rihel J, Adolph AR & Dowling JE (2010). Zebrafish larvae lose vision at night. Proc Natl Acad Sci U S A 107, 6034-6039.
22. Fedchyshyn MJ & Wang LY (2005). Developmental transformation of the release modality at the calyx of Held synapse. J Neurosci 25, 4131-4140.
23. Furukawa T & Matsuura S (1978). Adaptive rundown of excitatory post-synaptic potentials at synapses between hair cells and eighth nerve fibers in the goldfish. J Physiol 276, 193-209.
24. Glowatzki E & Fuchs PA (2002). Transmitter release at the hair cell ribbon synapse. Nat Neurosci 5, 147-154.
25. Gomis A, Burrone J & Lagnado L (1999). Two actions of calcium regulate the supply of releasable vesicles at the ribbon synapse of retinal bipolar cells. J Neurosci 19, 6309-6317.
26. Goutman JD (2012). Transmitter release from cochlear hair cells is phase locked to cyclic stimuli of different intensities and frequencies. J Neurosci 32, 17025-17035.
27. Goutman JD & 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.
28. Goutman JD & Glowatzki E (2011). Short-term facilitation modulates size and timing of the synaptic response at the inner hair cell ribbon synapse. J Neurosci 31, 7974-7981.
29. 2+ nanodomains beneath the ribbon promote highly synchronous multivesicular release at hair cell synapses. J Neurosci 31, 16637-16650.
30. Griesinger CB, Richards CD & Ashmore JF (2005). Fast vesicle replenishment allows indefatigable signaling at the first auditory synapse. Nature 435, 212-215.
31. Heidelberger R, Thoreson WB & Witkovsky P (2005). Synaptic transmission at retinal ribbon synapses. Prog Retin Eye Res 24, 682-720.
32. Holt M, Cooke A, Neef A & Lagnado L (2004). High mobility of vesicles supports continuous exocytosis at a ribbon synapse. Curr Biol 14, 173-183.
33. Hull C, Studholme K, Yazulla S & von Gersdorff H (2006). Diurnal changes in exocytosis and the number of synaptic ribbons at active zones of an ON-type bipolar cell terminal. J Neurophysiol 96, 2025-2033.
34. Jackman SL, Choi SY, Thoreson WB, Rabl K, Bartoletti TM & Kramer RH (2009). Role of the synaptic ribbon in transmitting the cone light response. Nat Neurosci 12, 303-310.
35. Jarsky T, Cembrowski M, Logan SM, Kath WL, Riecke H, Demb JB, & Singer JH (2011). A synaptic mechanism of retinal adaptation to luminance and contrast. J Neurosci 31, 11003-11015.
36. Jarsky T, Tian M & Singer JH (2010). Nanodomain control of exocytosis is responsible for the signaling capability of a retinal ribbon synapse. J Neurosci 30, 11885-11895.
37. Johnson SL, Franz C, Knipper M & Marcotti W (2009). Functional maturation of the exocytotic machinery at gerbil hair cell ribbon synapses. J Physiol 587, 1715-1726.
38. 2+ dependence of exocytosis during development of mouse inner hair cells. J Physiol 563, 177-191.
39. Kantardzhieva A, Peppi M, Lane WS, & Sewell WF (2012). Protein composition of immunoprecipitated synaptic ribbons. J Proteome Res 11, 1163-1174.
40. Keen EC & Hudspeth AJ (2006). Transfer characteristics of the hair cell's afferent synapse. Proc Natl Acad Sci U S A 103, 5537-5542.
41. 2 at the synapse. Biochim Biophys Acta 1821, 1114-1132.
42. Kushmerick C, Renden R & von Gersdorff H (2006). Physiological temperatures reduce the rate of vesicle pool depletion and short-term depression via an acceleration of vesicle recruitment. J Neurosci 26, 1366-1377.
43. 2+ buffering capacity in the developing rat calyx of Held. Braz J Med Biol Res 42, 94-104.
44. Li GL, Keen E, Andor-Ardo D, Hudspeth AJ & von Gersdorff H (2009). The unitary event underlying multiquantal EPSCs at a hair cell's ribbon synapse. J Neurosci 29, 7558-7568.
45. LoGiudice L, Sterling P & Matthews G (2009). Vesicle recycling at ribbon synapses in the finely branched axon terminals of mouse retinal bipolar neurons. Neuroscience 164, 1546-1556.
46. López-del Hoyo N, Fazioli L, López-Begines S, Fernández-Sánchez L, Cuenca N, Llorens J, de la Villa P & Méndez A (2012). Overexpression of guanylate cyclase activating protein 2 in rod photoreceptors in vivo leads to morphological changes at the synaptic ribbon. PLoS One 7, e42994.
47. Matthews G & Fuchs P (2010). The diverse roles of ribbon synapses in sensory neurotransmission. Nat Rev Neurosci 11, 812-822.
48. Matthews G & Sterling P (2008). Evidence that vesicles undergo compound fusion on the synaptic ribbon. J Neurosci 28, 5403-5411.
49. 2+ channel domain overlap. Brain Res 1398, 126-138.
50. Mehta B, Snellman J, Chen S, Li W & Zenisek D (2013). Synaptic ribbons influence the size and frequency of miniature-like evoked postsynaptic currents. Neuron 77, 516-527.
51. Mennerick S & Matthews G (1996). Ultrafast exocytosis elicited by calcium current in synaptic terminals of retinal bipolar neurons. Neuron 17, 1241-1249.
52. Midorikawa M, Tsukamoto Y, Berglund K, Ishii M & Tachibana M (2007). Different roles of ribbon-associated and ribbon-free active zones in retinal bipolar cells. Nature Neurosci 10, 1268-1276.
53. Moser T & Beutner D (2000). Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse. Proc Natl Acad Sci U S A 97, 883-888.
54. Moser T, Neef A & Khimich D (2006). Mechanisms underlying the temporal precision of sound coding at the inner hair cell ribbon synapse. J Physiol 576, 55-62.
55. Neher E & Sakaba T (2008). Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 59, 861-872.
56. Oesch NW & Diamond JS (2011). Ribbon synapses compute temporal contrast and encode luminance in retinal rod bipolar cells. Nat Neurosci 14, 1555-1561.
57. Palmer MJ, Hull C, Vigh J & von Gersdorff H (2003). Synaptic cleft acidification and modulation of short-term depression by exocytosed protons in retinal bipolar cells. J Neurosci 23, 11332-11341.
58. Palmer MJ & von Gersdorff H (2002). Phasic transmitter release from tonic neurons. Neuron 35, 600-602.
59. Pumplin DW, Reese TS & Llinas R (1981). Are the presynaptic membrane particles the calcium channels Proc Natl Acad Sci U S A 78, 7210-7213.
60. Roberts WM (1994). Localization of calcium signals by a mobile calcium buffer in frog saccular hair cells. J Neurosci 14, 3246-3262.
61. 2+ currents in bullfrog hair cells reveals two distinct channel subtypes. J Physiol 534, 669-689.
62. Rutherford MA, Chapochnikov NM & Moser T (2012). Spike encoding of neurotransmitter release timing by spiral ganglion neurons of the cochlea. J Neurosci 32, 4773-4789.
63. Rutherford MA & Pangršič T (2012). Molecular anatomy and physiology of exocytosis in sensory hair cells. Cell Calcium 52, 327-337.
64. Rutherford MA & Roberts WM (2006). Frequency selectivity of synaptic exocytosis in frog saccular hair cells. Proc Natl Acad Sci U S A 103, 2898-2903.
65. Safieddine S, El-Amraoui A & Petit C (2012). The auditory hair cell ribbon synapse: from assembly to function. Annu Rev Neurosci 35, 509-528.
66. Saviane C & Silver RA (2006). Fast vesicle reloading and a large pool sustain high bandwidth transmission at a central synapse. Nature 439, 983-987.
67. Schmitz F (2009). The making of synaptic ribbons: how they are built and what they do. Neuroscientist 15, 611-624.
68. Schnee ME, Lawton DM, Furness DN, Benke TA & Ricci AJ (2005). Auditory hair cell-afferent fiber synapses are specialized to operate at their best frequencies. Neuron 47, 243-254.
69. Schnee ME, Santos-Sacchi J, Castellano-Muñoz M, Kong JH & Ricci AJ (2011). Calcium-dependent synaptic vesicle trafficking underlies indefatigable release at the hair cell afferent fiber synapse. Neuron 70, 326-338.
70. Schwarz K, Natarajan S, Kassas N, Vitale N & Schmitz F (2011). The synaptic ribbon is a site of phosphatidic acid generation in ribbon synapses. J Neurosci 31, 15996-16011.
71. V1.3 channels regulate synaptic ribbon size and are required for synaptic maintenance in sensory hair cells. J Neurosci 32, 17273-17286.
72. Silver RA, Traynelis SF & Cull-Candy SG (1992). Rapid-time-course miniature and evoked excitatory currents at cerebellar synapses in situ. Nature 355, 163-166.
73. 2+ entry elicits transient postsynaptic currents at a retinal ribbon synapse. J Neurosci 23, 10923-10933.
74. Singer JH, Lassová L, Vardi N & Diamond JS (2004). Coordinated multivesicular release at a mammalian ribbon synapse. Nat Neurosci 7, 826-833.
75. Snellman J, Mehta B, Babai N, Bartoletti TM, Akmentin W, Francis A, Matthews G, Thoreson W & Zenisek D (2011). Acute destruction of the synaptic ribbon reveals a role for the ribbon in vesicle priming. Nat Neurosci 14, 1135-1141.
76. Spassova MA, Avissar M, Furman AC, Crumling MA, Saunders JC & Parsons TD (2004). Evidence that rapid vesicle replenishment of the synaptic ribbon mediates recovery from short-term adaptation at the hair cell afferent synapse. J Assoc Res Otolaryngol 5, 376-390.
77. Striegel AR, Biela LM, Evans CS, Wang Z, Delehoy JB, Sutton RB, Chapman ER & Reist NE (2012). Calcium binding by synaptotagmin's C2A domain is an essential element of the electrostatic switch that triggers synchronous synaptic transmission. J Neurosci 32, 1253-1260.
78. 2+ sensor. Nat Commun 3, 778.
79. 2+-sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse. Neuron 42, 595-605.
80. Trapani JG, Obholzer N, Mo W, Brockerhoff SE & Nicolson T (2009). Synaptojanin1 is required for temporal fidelity of synaptic transmission in hair cells. PLoS Genet 5, e1000480.
81. Uthaiah RC & Hudspeth AJ (2010). Molecular anatomy of the hair cell's ribbon synapse. J Neurosci 30, 12387-12399.
82. von Gersdorff H & Matthews G (1997). Depletion and replenishment of vesicle pools at a ribbon-type synaptic terminal. J Neurosci 17, 1919-1927.
83. von Gersdorff H, Sakaba T, Berglund K & Tachibana M (1998). Submillisecond kinetics of glutamate release from a sensory synapse. Neuron 21, 1177-1188.
84. 2+ channels carry the largest current: implications for nanodomains and transmitter release. Nat Neurosci 13, 1348-1350.
85. Williams C, Chen W, Lee CH, Yaeger D, Vyleta NP & Smith SM (2012). Coactivation of multiple tightly coupled calcium channels triggers spontaneous release of GABA. Nat Neurosci 5, 1195-1197.
86. Wittig Jr. JH & Parsons TD (2008). Synaptic ribbon enables temporal precision of hair cell afferent synapse by increasing the number of readily releasable vesicles: a modeling study. J Neurophysiol 100, 1724-1739.
87. Yi E, Roux I & Glowatzki E (2010). Dendritic HCN channels shape excitatory postsynaptic potentials at the inner hair cell afferent synapse in the mammalian cochlea. J Neurophysiol 103, 2532-2543.
88. 2+ channels expressed in mouse cochlear inner hair cells. J Physiol 588, 187-199.