Nanoscale-Targeted Patch-Clamp Recordings of Functional Presynaptic Ion Channels

Neuron

Volumn 79, Issue 6, 2013, Pages 1067-1077

  Novak, Pavel ^a,b   Gorelik, Julia ^c   Vivekananda, Umesh ^d   Shevchuk, AndrewI ^a,e   Ermolyuk, YaroslavS ^d   Bailey, RussellJ ^b   Bushby, AndrewJ ^b   Moss, GuyW J ^f   Rusakov, DmitriA ^d   Klenerman, David ^g   Kullmann, Dimitri M ^d   Volynski, KirillE ^d   Korchev, YuriE ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^f UNIVERSITY COLLEGE LONDON   (United Kingdom)

^g UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CHANNEL; CHLORIDE CHANNEL; ION CHANNEL; POTASSIUM CHANNEL; SODIUM CHANNEL; VOLTAGE GATED CALCIUM CHANNEL; CALCIUM; FLUORESCENT DYE;

ANIMAL CELL; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FLUORESCENCE MICROSCOPY; IMAGING; ION CONDUCTANCE; LABORATORY AUTOMATION; NONHUMAN; PATCH CLAMP; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SEMIAUTOMATION; SUPERRESOLUTION SCANNING ION CONDUCTANCE IMAGING; SYNAPSE; THREE DIMENSIONAL IMAGING; ANIMAL; BIOPHYSICS; CELL CULTURE; CHANNEL GATING; CYTOLOGY; DENDRITIC SPINE; ELECTRODE; ELECTROSTIMULATION; HIPPOCAMPUS; MEMBRANE POTENTIAL; METABOLISM; NERVE CELL; NEWBORN; PHYSIOLOGY; SCANNING TUNNELING MICROSCOPY; SYNAPTOSOME; ULTRASTRUCTURE;

ANIMALS; ANIMALS, NEWBORN; BIOPHYSICAL PHENOMENA; CALCIUM; CELLS, CULTURED; DENDRITIC SPINES; ELECTRIC STIMULATION; ELECTRODES; FLUORESCENT DYES; HIPPOCAMPUS; IMAGING, THREE-DIMENSIONAL; ION CHANNEL GATING; ION CHANNELS; MEMBRANE POTENTIALS; MICROSCOPY, SCANNING TUNNELING; NEURONS; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; RATS;

EID: 84884391704     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.07.012     Document Type: Article

References (42)

1. Ariel P., Ryan T.A. Optical mapping of release properties in synapses. Front. Neural Circuits 2010, 4:18.
2. Berninghausen O., Rahman M.A., Silva J.P., Davletov B., Hopkins C., Ushkaryov Y.A. Neurexin Ibeta and neuroligin are localized on opposite membranes in mature central synapses. J.Neurochem. 2007, 103:1855-1863.
3. Bischofberger J., Engel D., Li L., Geiger J.R., Jonas P. Patch-clamp recording from mossy fiber terminals in hippocampal slices. Nat. Protoc. 2006, 1:2075-2081.
4. Böhle T., Benndorf K. Facilitated giga-seal formation with a just originated glass surface. Pflugers Arch. 1994, 427:487-491.
5. 2+ sensors promotes fast and efficient transmitter release at a cortical GABAergic synapse. Neuron 2008, 57:536-545.
6. 2+ channelopathy. Neuron 2004, 43:387-400.
7. Debanne D., Campanac E., Bialowas A., Carlier E., Alcaraz G. Axon physiology. Physiol. Rev. 2011, 91:555-602.
8. Delmas P., Abogadie F.C., Buckley N.J., Brown D.A. Calcium channel gating and modulation by transmitters depend on cellular compartmentalization. Nat. Neurosci. 2000, 3:670-678.
9. 2+ influx and bouton size at small central synapses. PLoS Biol. 2012, 10:e1001396.
10. Gaffield M.A., Betz W.J. Imaging synaptic vesicle exocytosis and endocytosis with FM dyes. Nat. Protoc. 2006, 1:2916-2921.
11. Gorelik J., Gu Y., Spohr H.A., Shevchuk A.I., Lab M.J., Harding S.E., Edwards C.R., Whitaker M., Moss G.W., Benton D.C., et al. Ion channels in small cells and subcellular structures can be studied with a smart patch-clamp system. Biophys. J. 2002, 83:3296-3303.
12. Gorelik J., Shevchuk A., Ramalho M., Elliott M., Lei C., Higgins C.F., Lab M.J., Klenerman D., Krauzewicz N., Korchev Y. Scanning surface confocal microscopy for simultaneous topographical and fluorescence imaging: application to single virus-like particle entry into a cell. Proc. Natl. Acad. Sci. USA 2002, 99:16018-16023.
13. Gu Y., Gorelik J., Spohr H.A., Shevchuk A., Lab M.J., Harding S.E., Vodyanoy I., Klenerman D., Korchev Y.E. High-resolution scanning patch-clamp: new insights into cell function. FASEB J. 2002, 16:748-750.
14. Hallermann S., Pawlu C., Jonas P., Heckmann M. A large pool of releasable vesicles in a cortical glutamatergic synapse. Proc. Natl. Acad. Sci. USA 2003, 100:8975-8980.
15. 2+ channel density and vesicle docking at the presynaptic active zone. Neuron 2011, 69:304-316.
16. Harlow M.L., Ress D., Stoschek A., Marshall R.M., McMahan U.J. The architecture of active zone material at the frog's neuromuscular junction. Nature 2001, 409:479-484.
17. 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.
18. Hoppa M.B., Lana B., Margas W., Dolphin A.C., Ryan T.A. α2δ expression sets presynaptic calcium channel abundance and release probability. Nature 2012, 486:122-125.
19. Hosokawa Y., Sandri G., Panfili E., Cherubini E. Characterization of a voltage-dependent anionic channel in fused synaptosomes isolated from rat hippocampi. Neurosci. Lett. 1994, 169:167-170.
20. 2+-activated K+ channels in glutamatergic hippocampal terminals and their role in spike repolarization and regulation of transmitter release. J.Neurosci. 2001, 21:9585-9597.
21. 2+ channels to presynaptic active zones via a direct PDZ-domain interaction. Cell 2011, 144:282-295.
22. Koester H.J., Johnston D. Target cell-dependent normalization of transmitter release at neocortical synapses. Science 2005, 308:863-866.
23. Korchev Y.E., Bashford C.L., Milovanovic M., Vodyanoy I., Lab M.J. Scanning ion conductance microscopy of living cells. Biophys. J. 1997, 73:653-658.
24. Li Y., Tsien R.W. pHTomato, a red, genetically encoded indicator that enables multiplex interrogation of synaptic activity. Nat. Neurosci. 2012, 15:1047-1053.
25. Li H., Foss S.M., Dobryy Y.L., Park C.K., Hires S.A., Shaner N.C., Tsien R.Y., Osborne L.C., Voglmaier S.M. Concurrent imaging of synaptic vesicle recycling and calcium dynamics. Front Mol. Neurosci. 2011, 4:34.
26. Mochida S., Westenbroek R.E., Yokoyama C.T., Zhong H., Myers S.J., Scheuer T., Itoh K., Catterall W.A. Requirement for the synaptic protein interaction site for reconstitution of synaptic transmission by P/Q-type calcium channels. Proc. Natl. Acad. Sci. USA 2003, 100:2819-2824.
27. Nomura K., Sokabe M. Anion channels from rat brain synaptosomal membranes incorporated into planar bilayers. J.Membr. Biol. 1991, 124:53-62.
28. Novak P., Li C., Shevchuk A.I., Stepanyan R., Caldwell M., Hughes S., Smart T.G., Gorelik J., Ostanin V.P., Lab M.J., et al. Nanoscale live-cell imaging using hopping probe ion conductance microscopy. Nat. Methods 2009, 6:279-281.
29. Oltedal L., Mørkve S.H., Veruki M.L., Hartveit E. Patch-clamp investigations and compartmental modeling of rod bipolar axon terminals in aninvitro thin-slice preparation of the mammalian retina. J.Neurophysiol. 2007, 97:1171-1187.
30. Rheinlaender J., Schaffer T. Image formation, resolution, and height measurement in scanning ion conductance microscopy. J.Appl. Physiol. 2009, 105:094905.
31. Rizo J., Rosenmund C. Synaptic vesicle fusion. Nat. Struct. Mol. Biol. 2008, 15:665-674.
32. Ruiz A., Campanac E., Scott R.S., Rusakov D.A., Kullmann D.M. Presynaptic GABAA receptors enhance transmission and LTP induction at hippocampal mossy fiber synapses. Nat. Neurosci. 2010, 13:431-438.
33. Sasaki T., Matsuki N., Ikegaya Y. Targeted axon-attached recording with fluorescent patch-clamp pipettes in brain slices. Nat. Protoc. 2012, 7:1228-1234.
34. Schikorski T., Stevens C.F. Quantitative ultrastructural analysis of hippocampal excitatory synapses. J.Neurosci. 1997, 17:5858-5867.
35. Schneggenburger R., Forsythe I.D. The calyx of Held. Cell Tissue Res. 2006, 326:311-337.
36. 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.
37. 2+ and cellular dynamics: combined scanning ion conductance and optical microscopy to study contracting cardiac myocytes. Biophys. J. 2001, 81:1759-1764.
38. Shu Y., Hasenstaub A., Duque A., Yu Y., McCormick D.A. Modulation of intracortical synaptic potentials by presynaptic somatic membrane potential. Nature 2006, 441:761-765.
39. Südhof T.C., Rothman J.E. Membrane fusion: grappling with SNARE and SM proteins. Science 2009, 323:474-477.
40. Sun X.P., Schlichter L.C., Stanley E.F. Single-channel properties of BK-type calcium-activated potassium channels at a cholinergic presynaptic nerve terminal. J.Physiol. 1999, 518:639-651.
41. 2+ channel clusters persist at isolated presynaptic terminals. Eur. J. Neurosci. 2006, 23:1391-1396.
42. Ying L., Bruckbauer A., Rothery A.M., Korchev Y.E., Klenerman D. Programmable delivery of DNA through a nanopipet. Anal. Chem. 2002, 74:1380-1385.