Bassoon and the synaptic ribbon organize Ca2+ channels and vesicles to add release sites and promote refilling

Neuron

Volumn 68, Issue 4, 2010, Pages 724-738

  Frank, Thomas ^a,b,c   Rutherford, Mark A ^a   Strenzke, Nicola ^a,d   Neef, Andreas ^c   Pangršič, Tina ^a   Khimich, Darina ^a   Fetjova, Anna ^e   Gundelfinger, Eckart D ^e   Liberman, M Charles ^d   Harke, Benjamin ^f   Bryan, Keith E ^g   Lee, Amy ^g   Egner, Alexander ^f   Riedel, Dietmar ^f   Moser, Tobias ^a,b,c  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^b INTERNATIONAL MAX PLANCK RESEARCH SCHOOL FOR NEUROSCIENCES   (Germany)

^c Bernstein Center for Computational Neuroscience   (Germany)

^d MASSACHUSETTS EYE AND EAR INFIRMARY   (United States)

^e LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

^f MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^g UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASSOON; CALCIUM CHANNEL; CALCIUM CHANNEL CAV1.3; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL TISSUE; ARTICLE; CALCIUM CURRENT; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; EXOCYTOSIS; HAIR CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; RIBBON SYNAPSE; SYNAPSE; SYNAPSE VESICLE;

ANIMALS; CALCIUM CHANNELS; EXCITATORY POSTSYNAPTIC POTENTIALS; EXOCYTOSIS; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; SYNAPSES; SYNAPTIC VESICLES;

EID: 78449280421     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2010.10.027     Document Type: Article

References (46)

1. Altrock W.D., tom Dieck S., Sokolov M., Meyer A.C., Sigler A., Brakebusch C., Fässler R., Richter K., Boeckers T.M., Potschka H., et al. Functional inactivation of a fraction of excitatory synapses in mice deficient for the active zone protein bassoon. Neuron 2003, 37:787-800.
2. 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.
3. 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, 25:11577-11585.
4. 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. J. Neurosci. 2010, 30:7587-7597.
5. 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. J. Comp. Neurol. 2001, 439:224-234.
6. Dick O., tom Dieck S., Altrock W.D., Ammermüller J., Weiler R., Garner C.C., Gundelfinger E.D., Brandstätter J.H. The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron 2003, 37:775-786.
7. Fernández-Busnadiego R., Zuber B., Maurer U.E., Cyrklaff M., Baumeister W., Lucic V. Quantitative analysis of the native presynaptic cytomatrix by cryoelectron tomography. J. Cell Biol. 2010, 188:145-156.
8. Fouquet W., Owald D., Wichmann C., Mertel S., Depner H., Dyba M., Hallermann S., Kittel R.J., Eimer S., Sigrist S.J. Maturation of active zone assembly by Drosophila Bruchpilot. J. Cell Biol. 2009, 186:129-145.
9. Frank T., Khimich D., Neef A., Moser T. Mechanisms contributing to synaptic Ca2+ signals and their heterogeneity in hair cells. Proc. Natl. Acad. Sci. USA 2009, 106:4483-4488.
10. Furukawa T., Matsuura S. Adaptive rundown of excitatory post-synaptic potentials at synapses between hair cells and eight nerve fibres in the goldfish. J. Physiol. 1978, 276:193-209.
11. Glowatzki E., Grant L., Fuchs P. Hair cell afferent synapses. Curr. Opin. Neurobiol. 2008, 18:389-395.
12. Gomis A., Burrone J., Lagnado L. Two actions of calcium regulate the supply of releasable vesicles at the ribbon synapse of retinal bipolar cells. J. Neurosci. 1999, 19:6309-6317.
13. Goutman J.D., Glowatzki E. Time course and calcium dependence of transmitter release at a single ribbon synapse. Proc. Natl. Acad. Sci. USA 2007, 104:16341-16346.
14. Hallermann S., Fetjova A., Schmidt H., Weyhersmüller A., Silver R.A., Gundelfinger E.D., Eilers J. Bassoon speeds vesicle recruitment at a central excitatory synapse. Neuron 2010, 68:710-723. this issue.
15. Harke B., Keller J., Ullal C.K., Westphal V., Schönle A., Hell S.W. Resolution scaling in STED microscopy. Opt. Express 2008, 16:4154-4162.
16. Harris D.M., Dallos P. Forward masking of auditory nerve fiber responses. J. Neurophysiol. 1979, 42:1083-1107.
17. Holt M., Cooke A., Neef A., Lagnado L. High mobility of vesicles supports continuous exocytosis at a ribbon synapse. Curr. Biol. 2004, 14:173-183.
18. Johnson S.L., Forge A., Knipper M., Münkner S., Marcotti W. Tonotopic variation in the calcium dependence of neurotransmitter release and vesicle pool replenishment at mammalian auditory ribbon synapses. J. Neurosci. 2008, 28:7670-7678.
19. Khimich D., Nouvian R., Pujol R., tom Dieck S., Egner A., Gundelfinger E.D., Moser T. Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature 2005, 434:889-894.
20. Kittel R.J., Wichmann C., Rasse T.M., Fouquet W., Schmidt M., Schmid A., Wagh D.A., Pawlu C., Kellner R.R., Willig K.I., et al. Bruchpilot promotes active zone assembly, Ca2+ channel clustering, and vesicle release. Science 2006, 312:1051-1054.
21. 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.
22. 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. J. Neurosci. 2009, 29:7558-7568.
23. Meyer A.C., Frank T., Khimich D., Hoch G., Riedel D., Chapochnikov N.M., Yarin Y.M., Harke B., Hell S.W., Egner A., Moser T. Tuning of synapse number, structure and function in the cochlea. Nat. Neurosci. 2009, 12:444-453.
24. Moser T., Beutner D. Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse. Proc. Natl. Acad. Sci. USA 2000, 97:883-888.
25. Moser T., Neef A., Khimich D. Mechanisms underlying the temporal precision of sound coding at the inner hair cell ribbon synapse. J. Physiol. 2006, 576:55-62.
26. Mukherjee K., Yang X., Gerber S.H., Kwon H.B., Ho A., Castillo P.E., Liu X., Südhof T.C. Piccolo and bassoon maintain synaptic vesicle clustering without directly participating in vesicle exocytosis. Proc. Natl. Acad. Sci. USA 2010, 107:6504-6509.
27. Neef J., Gehrt A., Bulankina A.V., Meyer A.C., Riedel D., Gregg R.G., Strenzke N., Moser T. The Ca2+ channel subunit beta2 regulates Ca2+ channel abundance and function in inner hair cells and is required for hearing. J. Neurosci. 2009, 29:10730-10740.
28. Neher E., Sakaba T. Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 2008, 59:861-872.
29. Nouvian R., Beutner D., Parsons T.D., Moser T. Structure and function of the hair cell ribbon synapse. J. Membr. Biol. 2006, 209:153-165.
30. Pangršič T., Lasarow L., Reuter K., Takago H., Schwander M., Riedel D., Frank T., Tarantino L.M., Bailey J.S., Strenzke N., et al. Hearing requires otoferlin-dependent efficient replenishment of synaptic vesicles in hair cells. Nat. Neurosci. 2010, 13:869-876.
31. Pauli-Magnus D., Hoch G., Strenzke N., Anderson S., Jentsch T.J., Moser T. Detection and differentiation of sensorineural hearing loss in mice using auditory steady-state responses and transient auditory brainstem responses. Neuroscience 2007, 149:673-684.
32. 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. J. Neurosci. 1990, 10:3664-3684.
33. Rutherford M.A., Roberts W.M. Frequency selectivity of synaptic exocytosis in frog saccular hair cells. Proc. Natl. Acad. Sci. USA 2006, 103:2898-2903.
34. 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 Tissue Res. 1984, 238:437-446.
35. 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.
36. 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.
37. Schoch S., Gundelfinger E.D. Molecular organization of the presynaptic active zone. Cell Tissue Res. 2006, 326:379-391.
38. 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. J. Assoc. Res. Otolaryngol. 2004, 5:376-390.
39. Specht D., tom Dieck S., Ammermüller J., Regus-Leidig H., Gundelfinger E.D., Brandstätter J.H. Structural and functional remodeling in the retina of a mouse with a photoreceptor synaptopathy: Plasticity in the rod and degeneration in the cone system. Eur. J. Neurosci. 2007, 26:2506-2515.
40. Sterling P., Matthews G. Structure and function of ribbon synapses. Trends Neurosci. 2005, 28:20-29.
41. Taberner A.M., Liberman M.C. Response properties of single auditory nerve fibers in the mouse. J. Neurophysiol. 2005, 93:557-569.
42. tom Dieck S., Altrock W.D., Kessels M.M., Qualmann B., Regus H., Brauner D., Fejtová A., Bracko O., Gundelfinger E.D., Brandstätter J.H. Molecular dissection of the photoreceptor ribbon synapse: Physical interaction of Bassoon and RIBEYE is essential for the assembly of the ribbon complex. J. Cell Biol. 2005, 168:825-836.
43. 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. J. Neurophysiol. 2008, 100:1724-1739.
44. Zampini V., Johnson S.L., Franz C., Lawrence N.D., Münkner S., Engel J., Knipper M., Magistretti J., Masetto S., Marcotti W. Elementary properties of CaV1.3 Ca(2+) channels expressed in mouse cochlear inner hair cells. J. Physiol. 2010, 588:187-199.
45. Zenisek D., Horst N.K., Merrifield C., Sterling P., Matthews G. Visualizing synaptic ribbons in the living cell. J. Neurosci. 2004, 24:9752-9759.
46. Zucker R.S., Fogelson A.L. Relationship between transmitter release and presynaptic calcium influx when calcium enters through discrete channels. Proc. Natl. Acad. Sci. USA 1986, 83:3032-3036.