Nanoscale Distribution of Presynaptic Ca2+ Channels and Its Impact on Vesicular Release during Development

Neuron

Volumn 85, Issue 1, 2015, Pages 145-158

  Nakamura, Yukihiro ^a,b,c,d   Harada, Harumi ^e,f   Kamasawa, Naomi ^e,h   Matsui, Ko ^e,i   Rothman, JasonS ^g   Shigemoto, Ryuichi ^e,f   Silver, R Angus ^g   DiGregorio, David A ^c,d   Takahashi, Tomoyuki ^a,b  

^a DOSHISHA UNIVERSITY   (Japan)

^b OKINAWA INSTITUTE OF SCIENCE AND TECHNOLOGY GRADUATE UNIVERSITY   (Japan)

^c INSTITUT PASTEUR   (France)

^d CNRS   (France)

^e NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^f INSTITUTE OF SCIENCE AND TECHNOLOGY AUSTRIA   (Austria)

^g UNIVERSITY COLLEGE LONDON   (United Kingdom)

^h MAX PLANCK FLORIDA INSTITUTE FOR NEUROSCIENCE   (United States)

ⁱ TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

EGTAZIC ACID; VOLTAGE GATED CALCIUM CHANNEL; CALCIUM; CALCIUM CHANNEL N TYPE; CALCIUM CHELATING AGENT; VOLTAGE-DEPENDENT CALCIUM CHANNEL (P-Q TYPE);

AMPLITUDE MODULATION; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CALCIUM TRANSPORT; DEVELOPMENT; DEVELOPMENTAL STAGE; DIFFUSION; ELECTRON MICROSCOPY; MOUSE; NERVE CELL; NONHUMAN; RAT; SENSOR; SIMULATION; SYNAPSE VESICLE; ACTION POTENTIAL; ANIMAL; DRUG EFFECTS; EXOCYTOSIS; METABOLISM; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; SYNAPSE; SYNAPTOSOME;

ACTION POTENTIALS; ANIMALS; CALCIUM; CALCIUM CHANNELS, N-TYPE; CALCIUM CHELATING AGENTS; EGTAZIC ACID; EXOCYTOSIS; MICE; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; RATS; SYNAPSES; SYNAPTIC VESICLES;

EID: 84920744764     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.11.019     Document Type: Article

References (59)

1. Atluri P.P., Regehr W.G. Determinants of the time course of facilitation at the granule cell to Purkinje cell synapse. J.Neurosci. 1996, 16:5661-5671.
2. Bennett M.R., Farnell L., Gibson W.G. The probability of quantal secretion within an array of calcium channels of an active zone. Biophys. J. 2000, 78:2222-2240.
3. 2+ signal. Nat. Neurosci. 2005, 8:426-434.
4. Borst J.G., Sakmann B. Calcium influx and transmitter release in a fast CNS synapse. Nature 1996, 383:431-434.
5. 2+ sensors promotes fast and efficient transmitter release at a cortical GABAergic synapse. Neuron 2008, 57:536-545.
6. 2+ channels trigger transmitter release at a central GABAergic synapse. Nat. Neurosci. 2010, 13:19-21.
7. Budisantoso T., Harada H., Kamasawa N., Fukazawa Y., Shigemoto R., Matsui K. Evaluation of glutamate concentration transient in the synaptic cleft of the rat calyx of Held. J.Physiol. 2013, 591:219-239.
8. 2+-binding loop of synaptotagmin with lipid bilayers. J.Biol. Chem. 1998, 273:13995-14001.
9. Chen Z., Cooper B., Kalla S., Varoqueaux F., Young S.M. The Munc13 proteins differentially regulate readily releasable pool dynamics and calcium-dependent recovery at a central synapse. J.Neurosci. 2013, 33:8336-8351.
10. DiGregorio D.A., Peskoff A., Vergara J.L. Measurement of action potential-induced presynaptic calcium domains at a cultured neuromuscular junction. J.Neurosci. 1999, 19:7846-7859.
11. DiGregorio D.A., Rothman J.S., Nielsen T.A., Silver R.A. Desensitization properties of AMPA receptors at the cerebellar mossy fiber granule cell synapse. J.Neurosci. 2007, 27:8344-8357.
12. + channels and sensors of exocytosis at fast mammalian synapses. Nat. Rev. Neurosci. 2012, 13:7-21.
13. 2+ channels. Nat. Neurosci. 2013, 16:1754-1763.
14. Fedchyshyn M.J., Wang L.Y. Developmental transformation of the release modality at the calyx of Held synapse. J.Neurosci. 2005, 25:4131-4140.
15. Fedchyshyn M.J., Wang L.Y. Activity-dependent changes in temporal components of neurotransmission at the juvenile mouse calyx of Held synapse. J.Physiol. 2007, 581:581-602.
16. 2+-binding proteins calretinin and parvalbumin at the calyx of held of rats and mice. Eur. J. Neurosci. 2004, 20:1473-1482.
17. Fujimoto K. Freeze-fracture replica electron microscopy combined with SDS digestion for cytochemical labeling of integral membrane proteins. Application to the immunogold labeling of intercellular junctional complexes. J.Cell Sci. 1995, 108:3443-3449.
18. Hagiwara A., Fukazawa Y., Deguchi-Tawarada M., Ohtsuka T., Shigemoto R. Differential distribution of release-related proteins in the hippocampal CA3 area as revealed by freeze-fracture replica labeling. J.Comp. Neurol. 2005, 489:195-216.
19. Hallermann S., Silver R.A. Sustaining rapid vesicular release at active zones: potential roles for vesicle tethering. Trends Neurosci. 2013, 36:185-194.
20. 2+ channel density and vesicle docking at the presynaptic active zone. Neuron 2011, 69:304-316.
21. Helmchen F., Borst J.G., Sakmann B. Calcium dynamics associated with a single action potential in a CNS presynaptic terminal. Biophys. J. 1997, 72:1458-1471.
22. Holderith N., Lorincz A., Katona G., Rózsa B., Kulik A., Watanabe M., Nusser Z. Release probability of hippocampal glutamatergic terminals scales with the size of the active zone. Nat. Neurosci. 2012, 15:988-997.
23. v2.1 (P/Q-type) voltage-dependent calcium channels in Purkinje cells: somatodendritic gradient and distinct somatic coclustering with calcium-activated potassium channels. J.Neurosci. 2013, 33:3668-3678.
24. Ishikawa T., Nakamura Y., Saitoh N., Li W.B., Iwasaki S., Takahashi T. Distinct roles of Kv1 and Kv3 potassium channels at the calyx of Held presynaptic terminal. J.Neurosci. 2003, 23:10445-10453.
25. Kandler K., Friauf E. Pre- and postnatal development of efferent connections of the cochlear nucleus in the rat. J.Comp. Neurol. 1993, 328:161-184.
26. 2+ channels. Nat. Neurosci. 2007, 10:691-701.
27. 2+-secretion coupling at the rat calyx of Held. J.Physiol. 2009, 587:3009-3023.
28. 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, 586:2263-2275.
29. Kulik A., Nakadate K., Hagiwara A., Fukazawa Y., Luján R., Saito H., Suzuki N., Futatsugi A., Mikoshiba K., Frotscher M., Shigemoto R. Immunocytochemical localization of the alpha 1A subunit of the P/Q-type calcium channel in the rat cerebellum. Eur. J. Neurosci. 2004, 19:2169-2178.
30. Markram H., Roth A., Helmchen F. Competitive calcium binding: implications for dendritic calcium signaling. J.Comput. Neurosci. 1998, 5:331-348.
31. Meinrenken C.J., Borst J.G., Sakmann B. Calcium secretion coupling at calyx of Held governed by nonuniform channel-vesicle topography. J.Neurosci. 2002, 22:1648-1667.
32. Mercer A.J., Chen M., Thoreson W.B. Lateral mobility of presynaptic L-type calcium channels at photoreceptor ribbon synapses. J.Neurosci. 2011, 31:4397-4406.
33. Mintz I.M., Sabatini B.L., Regehr W.G. Calcium control of transmitter release at a cerebellar synapse. Neuron 1995, 15:675-688.
34. v2.1 in cerebellar Purkinje cells regulates competitive excitatory synaptic wiring, cell survival, and cerebellar biochemical compartmentalization. J.Neurosci. 2012, 32:1311-1328.
35. Nadkarni S., Bartol T.M., Sejnowski T.J., Levine H. Modelling vesicular release at hippocampal synapses. PLoS Comput. Biol. 2010, 6:e1000983.
36. Nägerl U.V., Novo D., Mody I., Vergara J.L. Binding kinetics of calbindin-D(28k) determined by flash photolysis of caged Ca(2+). Biophys. J. 2000, 79:3009-3018.
37. Neher E., Augustine G.J. Calcium gradients and buffers in bovine chromaffin cells. J.Physiol. 1992, 450:273-301.
38. Oertel D. The role of timing in the brain stem auditory nuclei of vertebrates. Annu. Rev. Physiol. 1999, 61:497-519.
39. Pan B., Zucker R.S. A general model of synaptic transmission and short-term plasticity. Neuron 2009, 62:539-554.
40. 2+ buffers in facilitating and depressing nerve terminals of pyramidal cells in layer 2/3 of the rat neocortex indicates a target cell-specific difference in presynaptic calcium dynamics. J.Physiol. 2001, 531:807-826.
41. Sakaba T., Neher E. Quantitative relationship between transmitter release and calcium current at the calyx of held synapse. J.Neurosci. 2001, 21:462-476.
42. Sätzler K., Söhl L.F., Bollmann J.H., Borst J.G., Frotscher M., Sakmann B., Lübke J.H. Three-dimensional reconstruction of a calyx of Held and its postsynaptic principal neuron in the medial nucleus of the trapezoid body. J.Neurosci. 2002, 22:10567-10579.
43. Schmidt H., Brachtendorf S., Arendt O., Hallermann S., Ishiyama S., Bornschein G., Gall D., Schiffmann S.N., Heckmann M., Eilers J. Nanodomain coupling at an excitatory cortical synapse. Curr. Biol. 2013, 23:244-249.
44. Schneggenburger R., Neher E. Presynaptic calcium and control of vesicle fusion. Curr. Opin. Neurobiol. 2005, 15:266-274.
45. 2+ channels in the active zone shapes neurotransmitter release from Schaffer collateral synapses. J.Neurosci. 2012, 32:18157-18176.
46. Sheng J., He L., Zheng H., Xue L., Luo F., Shin W., Sun T., Kuner T., Yue D.T., Wu L.G. Calcium-channel number critically influences synaptic strength and plasticity at the active zone. Nat. Neurosci. 2012, 15:998-1006.
47. Stanley E.F. Single calcium channels and acetylcholine release at a presynaptic nerve terminal. Neuron 1993, 11:1007-1011.
48. Südhof T.C. Neurotransmitter release: the last millisecond in the life of a synaptic vesicle. Neuron 2013, 80:675-690.
49. Takahashi T., Hori T., Nakamura Y., Yamashita T. Patch-clamp recording method in slices for studying presynaptic mechanisms. Patch Clamp Techniques: From Beginning to Advanced Protocols 2012, 137-145. Springer Japan, Tokyo. Y. Okada (Ed.).
50. Taschenberger H., von Gersdorff H. Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J.Neurosci. 2000, 20:9162-9173.
51. Taschenberger H., Leão R.M., Rowland K.C., Spirou G.A., von Gersdorff H. Optimizing synaptic architecture and efficiency for high-frequency transmission. Neuron 2002, 36:1127-1143.
52. Taschenberger H., Scheuss V., Neher E. Release kinetics, quantal parameters and their modulation during short-term depression at a developing synapse in the rat CNS. J.Physiol. 2005, 568:513-537.
53. 2+ channels and release sensors at a plastic hippocampal synapse. Science 2014, 343:665-670.
54. Wang L.Y., Fedchyshyn M.J., Yang Y.M. Action potential evoked transmitter release in central synapses: insights from the developing calyx of Held. Mol. Brain 2009, 2:36.
55. 2+ channel synprint site in synaptic vesicle endocytosis. J.Neurosci. 2010, 30:655-660.
56. 2+ channels carry the largest current: implications for nanodomains and transmitter release. Nat. Neurosci. 2010, 13:1348-1350.
57. 2+ clearance in the cytosol of adrenal chromaffin cells. Biophys. J. 1997, 73:532-545.
58. Yang Y.M., Fedchyshyn M.J., Grande G., Aitoubah J., Tsang C.W., Xie H., Ackerley C.A., Trimble W.S., Wang L.Y. Septins regulate developmental switching from microdomain to nanodomain coupling of Ca(2+) influx to neurotransmitter release at a central synapse. Neuron 2010, 67:100-115.
59. 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.