Molecular anatomy and physiology of exocytosis in sensory hair cells

Cell Calcium

Volumn 52, Issue 3-4, 2012, Pages 327-337

  Rutherford, Mark A ^a   PangrŠič, Tina ^a,b  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^b UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

Active zone; Calcium; Exocytosis; Hair cell; Hearing; Neurotransmission; Pool; Ribeye; Synaptic protein; Synaptic ribbon; Synaptic vesicle

Indexed keywords

BINDING PROTEIN; C TERMINAL BINDING PROTEIN 1; C TERMINAL BINDING PROTEIN 2; CALCIUM CHANNEL CAV1.3; CALCIUM ION; MEMBRANE PROTEIN; MOLECULAR SCAFFOLD; OTOFERLIN; SNARE PROTEIN; SYNAPTOBREVIN 1; SYNAPTOBREVIN 2; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNTAXIN 1; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL;

ARTICLE; AUDITORY STIMULATION; CELL FUSION; CELL STRUCTURE; CELLULAR DISTRIBUTION; COMPLEX FORMATION; EXOCYTOSIS; FUNCTIONAL ANATOMY; HAIR CELL; HUMAN; MOLECULAR DOCKING; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NEUROMODULATION; NEUROSECRETORY CELL; NONHUMAN; PRESYNAPTIC DENSITY; PRIORITY JOURNAL; PROTEIN LOCALIZATION; STRUCTURE ACTIVITY RELATION; SYNAPSE; SYNAPSE RIBBON; SYNAPTIC TRANSMISSION;

ANIMALIA;

EID: 84865759735     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2012.05.008     Document Type: Article

References (184)

1. Fuchs P.A., Glowatzki E., Moser T. The afferent synapse of cochlear hair cells. Current Opinion in Neurobiology 2003, 13:452-458.
2. Nouvian R., Beutner D., Parsons T.D., Moser T. Structure and function of the hair cell ribbon synapse. The Journal of Membrane Biology 2006, 209:153-165.
3. Moser T., Neef A., Khimich D. Mechanisms underlying the temporal precision of sound coding at the inner hair cell ribbon synapse. The Journal of Physiology 2006, 576:55-62.
4. Moser T., Brandt A., Lysakowski A. Hair cell ribbon synapses. Cell and Tissue Research 2006, 326:347-359.
5. Sewell W.F. The relation between the endocochlear potential and spontaneous activity in auditory nerve fibres of the cat. The Journal of Physiology 1984, 347:685-696.
6. Taberner A.M., Liberman M.C. Response properties of single auditory nerve fibers in the mouse. Journal of Neurophysiology 2005, 93:557-569.
7. Rutherford M.A., Chapochnikov N.M., Moser T. Spike encoding of neurotransmitter release timing by spiral ganglion neurons of the cochlea. The Journal of Neuroscience 2012, 32:4773-4789.
8. Russell I.J., Sellick P.M. Intracellular studies of hair cells in the mammalian cochlea. The Journal of Physiology 1978, 284:261-290.
9. Brown M.C., Nuttall A.L., Masta R.I. Intracellular recordings from cochlear inner hair cells: effects of stimulation of the crossed olivocochlear efferents. Science 1983, 222:69-72.
10. Dallos P. Response characteristics of mammalian cochlear hair cells. The Journal of Neuroscience 1985, 5:1591-1608.
11. Parsons T.D., Lenzi D., Almers W., Roberts W.M. Calcium-triggered exocytosis and endocytosis in an isolated presynaptic cell: capacitance measurements in saccular hair cells. Neuron 1994, 13:875-883.
12. Moser T., Beutner D. Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse. Proceedings of the National Academy of Sciences of the United States of America 2000, 97:883.
13. Keen E.C., Hudspeth A.J. Transfer characteristics of the hair cell's afferent synapse. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:5537-5542.
14. 2+ signals and their heterogeneity in hair cells. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:4483-4488.
15. Trapani J.G., Nicolson T. Mechanism of spontaneous activity in afferent neurons of the Zebrafish lateral-line organ. The Journal of Neuroscience 2011, 31:1614-1623.
16. 2+ channels. Cell 2000, 102:89-97.
17. 2+ channels in transmitter release from mammalian inner hair cells. II. Single-neuron activity. Journal of Neurophysiology 2002, 87:2734-2740.
18. Brandt A., Striessnig J., Moser T. CaV1. 3 channels are essential for development and presynaptic activity of cochlear inner hair cells. The Journal of Neuroscience 2003, 23:10832-10840.
19. 2+ channel gene results in deafness but no vestibular defect in mice. Journal of the Association for Research in Otolaryngology 2004, 5:215-226.
20. Catterall W.A. Voltage-gated calcium channels. Cold Spring Harbor Perspective Biology 2011, 3:a003947.
21. Glowatzki E., Fuchs P.A. Transmitter release at the hair cell ribbon synapse. Nature Neuroscience 2002, 5:147-154.
22. Seal R.P., Akil O., Yi E., et al. Sensorineural deafness and seizures in mice lacking vesicular glutamate transporter 3. Neuron 2008, 57:263-275.
23. Ruel J., Emery S., Nouvian R., et al. Impairment of SLC17A8 encoding vesicular glutamate transporter-3, VGLUT3, underlies nonsyndromic deafness DFNA25 and inner hair cell dysfunction in null mice. American Journal of Human Genetics 2008, 83:278-292.
24. Obholzer N., Wolfson S., Trapani J.G., et al. Vesicular glutamate transporter 3 is required for synaptic transmission in zebrafish hair cells. The Journal of Neuroscience 2008, 28:2110-2118.
25. Khimich D., Nouvian R., Pujol R., et al. Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature 2005, 434:889-894.
26. Goutman J.D., Glowatzki E. Time course and calcium dependence of transmitter release at a single ribbon synapse. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:16341-16346.
27. Goutman J.D., Glowatzki E. Short-term facilitation modulates size and timing of the synaptic response at the inner hair cell ribbon synapse. The Journal of Neuroscience 2011, 31:7974-7981.
28. Safieddine S., Wenthold R.J. SNARE complex at the ribbon synapses of cochlear hair cells: analysis of synaptic vesicle- and synaptic membrane-associated proteins. The European Journal of Neuroscience 1999, 11:803-812.
29. Uthaiah R.C., Hudspeth A.J. Molecular anatomy of the hair cell's ribbon synapse. The Journal of Neuroscience 2010, 30:12387-12399.
30. Beurg M., Michalski N., Safieddine S., et al. Control of exocytosis by synaptotagmins and otoferlin in auditory hair cells. The Journal of Neuroscience 2010, 30:13281-13290.
31. Reisinger E., Bresee C., Neef J., et al. Probing the functional equivalence of otoferlin and synaptotagmin 1 in exocytosis. The Journal of Neuroscience 2011, 31:4886-4895.
32. Strenzke N., Chanda S., Kopp-Scheinpflug C., et al. Complexin-I is required for high-fidelity transmission at the endbulb of held auditory synapse. The Journal of Neuroscience 2009, 29:7991-8004.
33. Nouvian R., Neef J., Bulankina A.V., et al. Exocytosis at the hair cell ribbon synapse apparently operates without neuronal SNARE proteins. Nature Neuroscience 2011, 14:411-413.
34. Yasunaga S., Grati M., Cohen-Salmon M., et al. A mutation in OTOF, encoding otoferlin, a FER-1-like protein, causes DFNB9, a nonsyndromic form of deafness. Nature Genetics 1999, 21:363-369.
35. Roux I., Safieddine S., Nouvian R., et al. Otoferlin, defective in a human deafness form, is essential for exocytosis at the auditory ribbon synapse. Cell 2006, 127:277-289.
36. PangrŠič T., Lasarow L., Reuter K., et al. Hearing requires otoferlin-dependent efficient replenishment of synaptic vesicles in hair cells. Nature Neuroscience 2010, 13:869-876.
37. Schmitz F., Königstorfer A., Südhof T.C. RIBEYE, a component of synaptic ribbons: a protein's journey through evolution provides insight into synaptic ribbon function. Neuron 2000, 28:857-872.
38. Zenisek D., Horst N.K., Merrifield C., Sterling P., Matthews G. Visualizing synaptic ribbons in the living cell. The Journal of Neuroscience 2004, 24:9752-9759.
39. tom Dieck S., Altrock W.D., Kessels M.M., et al. Molecular dissection of the photoreceptor ribbon synapse: physical interaction of Bassoon and RIBEYE is essential for the assembly of the ribbon complex. The Journal of Cell Biology 2005, 168:825-836.
40. Dick O., tom Dieck S., Altrock W.D., et al. The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron 2003, 37:775-786.
41. 2+ channels and vesicles to add release sites and promote refilling. Neuron 2010, 68:724-738.
42. Buran B.N., Strenzke N., Neef A., Gundelfinger E.D., Moser T., Liberman M.C. Onset coding is degraded in auditory nerve fibers from mutant mice lacking synaptic ribbons. The Journal of Neuroscience 2010, 30:7587.
43. Liberman M.C. Morphological differences among radial afferent fibers in the cat cochlea: an electron-microscopic study of serial sections. Hearing Research 1980, 3:45-63.
44. Lenzi D., Runyeon J.W., Crum J., Ellisman M.H., Roberts W.M. Synaptic vesicle populations in saccular hair cells reconstructed by electron tomography. The Journal of Neuroscience 1999, 19:119.
45. Lenzi D., Crum J., Ellisman M.H., Roberts W.M. Depolarization redistributes synaptic membrane and creates a gradient of vesicles on the synaptic body at a ribbon synapse. Neuron 2002, 36:649-659.
46. Rutherford M.A., Roberts W.M. Frequency selectivity of synaptic exocytosis in frog saccular hair cells. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:2898.
47. LoGiudice L., Sterling P., Matthews G. Mobility and turnover of vesicles at the synaptic ribbon. The Journal of Neuroscience 2008, 28:3150.
48. Snellman J., Mehta B., Babai N., et al. Acute destruction of the synaptic ribbon reveals a role for the ribbon in vesicle priming. Nature Neuroscience 2011, 14:1135-1141.
49. Parsons T.D., Sterling P. Synaptic ribbon. Conveyor belt or safety belt?. Neuron 2003, 37:379-382.
50. Furukawa T., Kuno M., Matsuura S. Quantal analysis of a decremental response at hair cell-afferent fibre synapses in the goldfish sacculus. The Journal of Physiology 1982, 322:181-195.
51. Sterling P., Matthews G. Structure and function of ribbon synapses. Trends in Neurosciences 2005, 28:20-29.
52. 2+ nanodomains beneath the ribbon promote highly synchronous multivesicular release at hair cell synapses. The Journal of Neuroscience 2011, 31:16637-16650.
53. Jackman S.L., Choi S.-Y., Thoreson W.B., Rabl K., Bartoletti T.M., Kramer R.H. Role of the synaptic ribbon in transmitting the cone light response. Nature Neuroscience 2009, 12:303-310.
54. Vollrath L., Spiwoks-Becker I. Plasticity of retinal ribbon synapses. Microscopy Research and Technique 1996, 35:472-487.
55. Merchan-Perez A., Liberman M.C. Ultrastructural differences among afferent synapses on cochlear hair cells: correlations with spontaneous discharge rate. The Journal of Comparative Neurology 1996, 371:208-221.
56. Kantardzhieva A.V., Peppi M., Lane W.S., Sewell W.F. Protein composition of immunoprecipitated synaptic ribbons. Journal of Proteome Research 2011, 11:1163-1174.
57. Magupalli V.G., Schwarz K., Alpadi K., Natarajan S., Seigel G.M., Schmitz F. Multiple RIBEYE-RIBEYE interactions create a dynamic scaffold for the formation of synaptic ribbons. The Journal of Neuroscience 2008, 28:7954-7967.
58. Weigert R., Silletta M.G., Spanò S., et al. CtBP/BARS induces fission of Golgi membranes by acylating lysophosphatidic acid. Nature 1999, 402:429-433.
59. Chinnadurai G. CtBP, an unconventional transcriptional corepressor in development and oncogenesis. Molecular Cell 2002, 9:213-224.
60. Corda D., Colanzi A., Luini A. The multiple activities of CtBP/BARS proteins: the Golgi view. Trends in Cell Biology 2006, 16:167-173.
61. Schmitz F. The making of synaptic ribbons: how they are built and what they do. The Neuroscientist 2009, 15:611-624.
62. Schwarz K., Natarajan S., Kassas N., Vitale N., Schmitz F. The synaptic ribbon is a site of phosphatidic acid generation in ribbon synapses. The Journal of Neuroscience 2011, 31:15996-16011.
63. Kooijman E.E., Chupin V., De Kruijff B., Burger K.N.J. Modulation of membrane curvature by phosphatidic acid and lysophosphatidic acid. Traffic 2003, 4:162-174.
64. Cazzolli R., Shemon A.N., Fang M.Q., Hughes W.E. Phospholipid signalling through phospholipase D and phosphatidic acid. IUBMB Life 2006, 58:457-461.
65. Oude Weernink P.A., López de Jesús M., Schmidt M. Phospholipase D signaling: orchestration by PIP2 and small GTPases. Naunyn-Schmiedebergs Archives of Pharmacology 2007, 374:399-411.
66. Bader M.-F., Vitale N. Phospholipase D in calcium-regulated exocytosis: lessons from chromaffin cells. Biochimica Et Biophysica Acta (BBA): Molecular and Cell Biology of Lipids 2009, 1791:936-941.
67. Antonescu C.N., Danuser G., Schmid S.L. Phosphatidic acid plays a regulatory role in clathrin-mediated endocytosis. Molecular Biology of the Cell 2010, 21:2944-2952.
68. Dick O., Hack I., Altrock W.D., Garner C.C., Gundelfinger E.D., Brandstätter J.H. Localization of the presynaptic cytomatrix protein Piccolo at ribbon and conventional synapses in the rat retina: comparison with Bassoon. The Journal of Comparative Neurology 2001, 439:224-234.
69. Cases-Langhoff C., Voss B., Garner A.M., et al. Piccolo, a novel 420kDa protein associated with the presynaptic cytomatrix. European Journal of Cell Biology 1996, 69:214-223.
70. Fenster S.D., Chung W.J., Zhai R., et al. Piccolo, a presynaptic zinc finger protein structurally related to bassoon. Neuron 2000, 25:203-214.
71. Ko J., Na M., Kim S., Lee J.-R., Kim E. Interaction of the ERC family of RIM-binding proteins with the liprin-α family of multidomain proteins. Journal of Biological Chemistry 2003, 278:42377-42385.
72. Takao-Rikitsu E., Mochida S., Inoue E., et al. Physical and functional interaction of the active zone proteins, CAST, RIM1, and Bassoon, in neurotransmitter release. The Journal of Cell Biology 2004, 164:301-311.
73. Gundelfinger E.D., Fejtova A. Molecular organization and plasticity of the cytomatrix at the active zone. Current Opinion in Neurobiology 2011, 10.1016/j.conb.2011.10.005.
74. Dresbach T., Hempelmann A., Spilker C., et al. Functional regions of the presynaptic cytomatrix protein bassoon: significance for synaptic targeting and cytomatrix anchoring. Molecular and Cellular Neuroscience 2003, 23:279-291.
75. Altrock W.D., tom Dieck S., Sokolov M., et al. Functional inactivation of a fraction of excitatory synapses in mice deficient for the active zone protein bassoon. Neuron 2003, 37:787-800.
76. Roberts W.M., Jacobs R.A., Hudspeth A.J. Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells. The Journal of Neuroscience 1990, 10:3664-3684.
77. Saito K., Hama K. A freeze-fracture study of afferent and efferent synapses of hair cells in the sensory epithelium of the organ of Corti in the guinea pig. Cell and Tissue Research 1984, 238:437-446.
78. Mukherjee K., Yang X., Gerber S.H., et al. Piccolo and bassoon maintain synaptic vesicle clustering without directly participating in vesicle exocytosis. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:6504.
79. Hallermann S., Fejtova A., Schmidt H., et al. Bassoon speeds vesicle reloading at a central excitatory synapse. Neuron 2010, 68:710-723.
80. Rimm D.L., Koslov E.R., Kebriaei P., Cianci C.D., Morrow J.S. Alpha 1(E)-catenin is an actin-binding and -bundling protein mediating the attachment of F-actin to the membrane adhesion complex. Proceedings of the National Academy of Sciences of the United States of America 1995, 92:8813-8817.
81. Fenster S.D., Kessels M.M., Qualmann B., et al. Interactions between piccolo and the actin/dynamin-binding protein abp1 link vesicle endocytosis to presynaptic active zones. Journal of Biological Chemistry 2003, 278:20268-20277.
82. 2+ channel in insulin granule exocytosis. The Journal of Biological Chemistry 2004, 279:7956-7961.
83. Ohara-Imaizumi M., Ohtsuka T., Matsushima S., et al. ELKS, a protein structurally related to the active zone-associated protein CAST, is expressed in pancreatic β cells and functions in insulin exocytosis: interaction of ELKS with exocytotic machinery analyzed by total internal reflection fluorescence microscopy. Molecular Biology of the Cell 2005, 16:3289-3300.
84. Mittelstaedt T., Alvaréz-Baron E., Schoch S. RIM proteins and their role in synapse function. Biological Chemistry 2010, 391:599-606.
85. 2+ channel density and vesicle docking at the presynaptic active zone. Neuron 2011, 69:304-316.
86. Deng L., Kaeser P.S., Xu W., Südhof T.C. RIM proteins activate vesicle priming by reversing autoinhibitory homodimerization of Munc13. Neuron 2011, 69:317-331.
87. 2+ channels and Rab3-interacting molecules (RIMs): new insights into stimulus-secretion coupling. Biochimica Et Biophysica Acta (BBA): Biomembranes 2012, 1818:551-558.
88. 2+ channels to presynaptic active zones via a direct PDZ-domain interaction. Cell 2011, 144:282-295.
89. 2+ channels, SNAP-25, and synaptotagmin. The Journal of Biological Chemistry 2001, 276:32756-32762.
90. 2+ channel gating by Rab3 interacting molecule. Molecular and Cellular Neuroscience 2010, 44:246-259.
91. 2+ channels. Neuron 2002, 34:411-423.
92. Chen J., Billings S.E., Nishimune H. Calcium channels link the muscle-derived synapse organizer laminin B2 to Bassoon and CAST/Erc2 to organize presynaptic active zones. The Journal of Neuroscience 2011, 31:512-525.
93. 2+ channels in hippocampal mossy fiber synaptic transmission and long-term potentiation. Neuron 1994, 12:261-269.
94. Sheets L., Trapani J.G., Mo W., Obholzer N., Nicolson T. Ribeye is required for presynaptic CaV1.3a channel localization and afferent innervation of sensory hair cells. Development 2011, 138:1309-1319.
95. Baig S.M., Koschak A., Lieb A., et al. Loss of Cav1.3 (CACNA1D) function in a human channelopathy with bradycardia and congenital deafness. Nature Neuroscience 2011, 14:77-84.
96. Tucker T., Fettiplace R. Confocal imaging of calcium microdomains and calcium extrusion in turtle hair cells. Neuron 1995, 15:1323-1335.
97. 2+ at individual presynaptic active zones of hair cells from the bullfrog's sacculus. Proceedings of the National Academy of Sciences of the United States of America 1996, 93:9527-9532.
98. Zenisek D., Davila V., Wan L., Almers W. Imaging calcium entry sites and ribbon structures in two presynaptic cells. The Journal of Neuroscience 2003, 23:2538.
99. Brandt A., Khimich D., Moser T. Few CaV1. 3 channels regulate the exocytosis of a synaptic vesicle at the hair cell ribbon synapse. The Journal of Neuroscience 2005, 25:11577.
100. Schneggenburger R., Neher E. Presynaptic calcium and control of vesicle fusion. Current Opinion in Neurobiology 2005, 15:266-274.
101. 2+ channel abundance and function in inner hair cells and is required for hearing. The Journal of Neuroscience 2009, 29:10730.
102. 2+ channel [alpha] 1 subunit contains an endoplasmic reticulum retention signal antagonized by the [beta] subunit. Neuron 2000, 25:177-190.
103. Altier C., Garcia-Caballero A., Simms B., et al. The Cav[beta] subunit prevents RFP2-mediated ubiquitination and proteasomal degradation of L-type channels. Nature Neuroscience 2010, 14:173-180.
104. Morgans C.W., Gaughwin P., Maleszka R. Expression of the alpha1F calcium channel subunit by photoreceptors in the rat retina. Molecular Vision 2001, 7:202-209.
105. McRory J.E., Hamid J., Doering C.J., et al. The CACNA1F gene encodes an L-type calcium channel with unique biophysical properties and tissue distribution. The Journal of Neuroscience 2004, 24:1707-1718.
106. Gomez-Ospina N., Tsuruta F., Barreto-Chang O., Hu L., Dolmetsch R. The C terminus of the L-type voltage-gated calcium channel Ca(V)1.2 encodes a transcription factor. Cell 2006, 127:591-606.
107. Zhang H., Fu Y., Altier C., Platzer J., Surmeier D.J., Bezprozvanny I. CaV1.2 and CaV1.3 neuronal L-type calcium channels: differential targeting and signaling to pCREB. European Journal of Neuroscience 2006, 23:2297-2310.
108. Grant L., Fuchs P. Calcium- and calmodulin-dependent inactivation of calcium channels in inner hair cells of the rat cochlea. Journal of Neurophysiology 2008, 99:2183-2193.
109. Johnson S.L., Marcotti W. Biophysical properties of CaV1.3 calcium channels in gerbil inner hair cells. The Journal of Physiology 2008, 586:1029-1042.
110. Lee S., Briklin O., Hiel H., Fuchs P. Calcium-dependent inactivation of calcium channels in cochlear hair cells of the chicken. The Journal of Physiology 2007, 583:909-922.
111. 2+-feedback to Cav1. 3 channels in mouse auditory hair cells. The Journal of Physiology 2007, 585:791-803.
112. Striessnig J. C-terminal tailoring of L-type calcium channel function. The Journal of Physiology 2007, 585:643-644.
113. 2+-dependent inactivation of CaV1.3 channels by calcium binding proteins of auditory hair cells. The Journal of Neuroscience 2006, 26:10677-10689.
114. Schnee M.E., Ricci A.J. Biophysical and pharmacological characterization of voltage-gated calcium currents in turtle auditory hair cells. The Journal of Physiology 2003, 549:697-717.
115. 2+-dependent inactivation. The Journal of Neuroscience 2003, 23:6041-6049.
116. Meyer A.C., Moser T. Structure and function of cochlear afferent innervation. Current Opinion in Otolaryngology & Head and Neck Surgery 2010, 18:441-446.
117. Meyer A.C., Frank T., Khimich D., et al. Tuning of synapse number, structure and function in the cochlea. Nature Neuroscience 2009, 12:444-453.
118. 2+ channels in mouse inner hair cells. Nature Neuroscience 2011, 14:1109-1111.
119. Schnee M.E., Lawton D.M., Furness D.N., Benke T.A., Ricci A.J. Auditory hair cell-afferent fiber synapses are specialized to operate at their best frequencies. Neuron 2005, 47:243-254.
120. Li G.L., Keen E., Andor-Ardó D., Hudspeth A.J., von Gersdorff H. The unitary event underlying multiquantal EPSCs at a hair cell's ribbon synapse. The Journal of Neuroscience 2009, 29:7558.
121. Grant L., Yi E., Glowatzki E. Two modes of release shape the postsynaptic response at the inner hair cell ribbon synapse. The Journal of Neuroscience 2010, 30:4210-4220.
122. Yi E., Roux I., Glowatzki E. Dendritic HCN channels shape excitatory postsynaptic potentials at the inner hair cell afferent synapse in the mammalian cochlea. Journal of Neurophysiology 2010, 103:2532-2543.
123. Tong G., Jahr C.E. Multivesicular release from excitatory synapses of cultured hippocampal neurons. Neuron 1994, 12:51-59.
124. Stevens C.F., Wang Y. Facilitation and depression at single central synapses. Neuron 1995, 14:795-802.
125. Rodriguez-Contreras A., Yamoah E.N. Direct measurement of single-channel Ca(2+) currents in bullfrog hair cells reveals two distinct channel subtypes. The Journal of Physiology 2001, 534:669-689.
126. Zampini V., Johnson S.L., Franz C., et al. Elementary properties of CaV1.3 Ca(2+) channels expressed in mouse cochlear inner hair cells. The Journal of Physiology 2010, 588:187-199.
127. Rutherford M.A., Roberts W.M. Spikes and membrane potential oscillations in hair cells generate periodic afferent activity in the frog sacculus. The Journal of Neuroscience 2009, 29:10025-10037.
128. 2+ channel domain overlap. Brain Research 2011, 1398:126-138.
129. 2+. Biophysical Journal 1994, 67:2546-2557.
130. Heidelberger R., Heinemann C., Neher E., Matthews G. Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 1994, 371:513-515.
131. Beutner D., Voets T., Neher E., Moser T. Calcium dependence of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse. Neuron 2001, 29:681-690.
132. Schneggenburger R., Neher E. Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 2000, 406:889-893.
133. Bollmann J.H., Sakmann B., Borst J.G.G. Calcium sensitivity of glutamate release in a calyx-type terminal. Science 2000, 289:953-957.
134. Augustine G.J., Adler E.M., Charlton M.P. The calcium signal for transmitter secretion from presynaptic nerve terminals. Annals of the New York Academy of Sciences 1991, 635:365-381.
135. Borst J.G.G., Sakmann B. Calcium influx and transmitter release in a fast CNS synapse. Nature 1996, 383:431-434.
136. Meinrenken C.J., Borst J.G.G., Sakmann B. Calcium secretion coupling at calyx of held governed by nonuniform channel-vesicle topography. The Journal of Neuroscience 2002, 22:1648-1667.
137. 2+ channel cooperativity of exocytosis. The Journal of Neuroscience 2009, 29:12196-12209.
138. 2+-sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse. Neuron 2004, 42:595-605.
139. Bartoletti T.M., Jackman S.L., Babai N., Mercer A.J., Kramer R.H., Thoreson W.B. Release from the cone ribbon synapse under bright light conditions can be controlled by the opening of only a few Ca(2+) channels. Journal of Neurophysiology 2011, 106:2922-2935.
140. Jarsky T., Tian M., Singer J.H. Nanodomain control of exocytosis is responsible for the signaling capability of a retinal ribbon synapse. The Journal of Neuroscience 2010, 30:11885-11895.
141. Stanley E.F. The calcium channel and the organization of the presynaptic transmitter release face. Trends in Neurosciences 1997, 20:404-409.
142. 2+ channels and sensors of exocytosis at fast mammalian synapses. Nature Reviews. Neuroscience 2012, 13:7-21.
143. Spassova M.A., Avissar M., Furman A.C., Crumling M.A., Saunders J.C., Parsons T.D. Evidence that rapid vesicle replenishment of the synaptic ribbon mediates recovery from short-term adaptation at the hair cell afferent synapse. Journal of the Association for Research in Otolaryngology 2004, 5:376-390.
144. Wittig J.H., Parsons T.D. Synaptic ribbon enables temporal precision of hair cell afferent synapse by increasing the number of readily releasable vesicles: a modeling study. Journal of Neurophysiology 2008, 100:1724-1739.
145. Siegel J.H. Spontaneous synaptic potentials from afferent terminals in the guinea pig cochlea. Hearing Research 1992, 59:85-92.
146. Rodríguez-Ballesteros M., del Castillo F.J., Martín Y., et al. Auditory neuropathy in patients carrying mutations in the otoferlin gene (OTOF). Human Mutation 2003, 22:451-456.
147. Varga R., Kelley P., Keats B., et al. Non-syndromic recessive auditory neuropathy is the result of mutations in the otoferlin (OTOF) gene. Journal of Medical Genetics 2003, 40:45-50.
148. Ramakrishnan N.A., Drescher M.J., Drescher D.G. Direct interaction of otoferlin with syntaxin 1A, SNAP-25, and the L-type voltage-gated calcium channel Cav1.3. The Journal of Biological Chemistry 2009, 284:1364-1372.
149. Johnson C.P., Chapman E.R. Otoferlin is a calcium sensor that directly regulates SNARE-mediated membrane fusion. The Journal of Cell Biology 2010, 191:187-197.
150. Schwander M., Sczaniecka A., Grillet N., et al. A forward genetics screen in mice identifies recessive deafness traits and reveals that pejvakin is essential for outer hair cell function. The Journal of Neuroscience 2007, 27:2163-2175.
151. Roux I., Hosie S., Johnson S.L., et al. Myosin VI is required for the proper maturation and function of inner hair cell ribbon synapses. Human Molecular Genetics 2009, 18:4615-4628.
152. Heidrych P., Zimmermann U., Kuhn S., et al. Otoferlin interacts with myosin VI: implications for maintenance of the basolateral synaptic structure of the inner hair cell. Human Molecular Genetics 2009, 18:2779-2790.
153. Dulon D., Safieddine S., Jones S.M., Petit C. Otoferlin is critical for a highly sensitive and linear calcium-dependent exocytosis at vestibular hair cell ribbon synapses. The Journal of Neuroscience 2009, 29:10474-10487.
154. Chapman E.R. How does synaptotagmin trigger neurotransmitter release?. Annual Review of Biochemistry 2008, 77:615-641.
155. Littleton J.T., Stern M., Perin M., Bellen H.J. Calcium dependence of neurotransmitter release and rate of spontaneous vesicle fusions are altered in Drosophila synaptotagmin mutants. PNAS 1994, 91:10888-10892.
156. 2+-triggered exocytosis. Current Opinion in Cell Biology 2010, 22:496-505.
157. 2+ dependence of vesicle fusion at auditory ribbon synapses. Nature Neuroscience 2010, 13:45-52.
158. 2+ binding. The Journal of Biological Chemistry 1997, 272:14314-14319.
159. Südhof T.C. Synaptotagmins: why so many?. The Journal of Biological Chemistry 2002, 277:7629-7632.
160. Young S.M., Neher E. Synaptotagmin has an essential function in synaptic vesicle positioning for synchronous release in addition to its role as a calcium sensor. Neuron 2009, 63:482-496.
161. Jahn R., Scheller R.H. SNAREs-engines for membrane fusion. Nature Reviews Molecular Cell Biology 2006, 7:631-643.
162. Rizo J., Rosenmund C. Synaptic vesicle fusion. Nature Structural & Molecular Biology 2008, 15:665-674.
163. Sørensen J.B. Conflicting views on the membrane fusion machinery and the fusion pore. Annual Review of Cell and Developmental Biology 2009, 25:513-537.
164. Sudhof T.C., Rothman J.E. Membrane fusion: grappling with SNARE and SM proteins. Science 2009, 323:474-477.
165. Blasi J., Chapman E.R., Link E., et al. Botulinum neurotoxin A selectively cleaves the synaptic protein SNAP-25. Nature 1993, 365:160-163.
166. Schiavo G., Rossetto O., Catsicas S., et al. Identification of the nerve terminal targets of botulinum neurotoxin serotypes A, D, and E. The Journal of Biological Chemistry 1993, 268:23784-23787.
167. Schiavo G., Matteoli M., Montecucco C. Neurotoxins affecting neuroexocytosis. Physiological Reviews 2000, 80:717-766.
168. Nystuen A., Schwendinger J., Sachs A., Yang A., Haider N. A null mutation in VAMP1/synaptobrevin is associated with neurological defects and prewean mortality in the lethal-wasting mouse mutant. Neurogenetics 2007, 8:1-10.
169. Schoch S., Deák F., Königstorfer A., et al. SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science 2001, 294:1117-1122.
170. Borisovska M., Zhao Y., Tsytsyura Y., et al. v-SNAREs control exocytosis of vesicles from priming to fusion. The EMBO Journal 2005, 24:2114-2126.
171. Washbourne P., Thompson P.M., Carta M., et al. Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nature Neuroscience 2002, 5:19-26.
172. Bock J.B., Matern H.T., Peden A.A., Scheller R.H. A genomic perspective on membrane compartment organization. Nature 2001, 409:839-841.
173. Kloepper T.H., Kienle C.N., Fasshauer D. An elaborate classification of SNARE proteins sheds light on the conservation of the eukaryotic endomembrane system. Molecular Biology of the Cell 2007, 18:3463-3471.
174. 2+-dependent neurotransmitter release. Cell 2001, 104:71-81.
175. Wojcik S.M., Brose N. Regulation of membrane fusion in synaptic excitation-secretion coupling: speed and accuracy matter. Neuron 2007, 55:11-24.
176. Brose N. For better or for worse: complexins regulate SNARE function and vesicle fusion. Traffic 2008, 9:1403-1413.
177. Tang J., Maximov A., Shin O.-H., Dai H., Rizo J., Südhof T.C. A complexin/synaptotagmin 1 switch controls fast synaptic vesicle exocytosis. Cell 2006, 126:1175-1187.
178. Morgans C.W., Brandstätter J.H., Kellerman J., Betz H., Wässle H. A SNARE complex containing syntaxin 3 is present in ribbon synapses of the retina. The Journal of Neuroscience 1996, 16:6713.
179. Zanazzi G., Matthews G. The molecular architecture of ribbon presynaptic terminals. Molecular Neurobiology 2009, 39:130-148.
180. Reim K., Wegmeyer H., Brandstätter J.H., et al. Structurally and functionally unique complexins at retinal ribbon synapses. The Journal of Cell Biology 2005, 169:669.
181. Reim K., Regus-Leidig H., Ammermüller J., et al. Aberrant function and structure of retinal ribbon synapses in the absence of complexin 3 and complexin 4. Journal of Cell Science 2009, 122:1352-1361.
182. Fritzsch B., Beisel K.W., Hansen L.A. The molecular basis of neurosensory cell formation in ear development: a blueprint for hair cell and sensory neuron regeneration?. Bioessays 2006, 28:1181-1193.
183. Freyer L., Aggarwal V., Morrow B.E. Dual embryonic origin of the mammalian otic vesicle forming the inner ear. Development 2011, 138:5403-5414.
184. Popper A.N., Fay R.R. Evolution of the ear and hearing: issues and questions. Brain, Behavior and Evolution 1997, 50:213-221.