Fast endocytosis is inhibited by GABA-mediated chloride influx at a presynaptic terminal

Neuron

Volumn 44, Issue 3, 2004, Pages 469-482

  Hull, Court ^a   Von Gersdorff, Henrique ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID C RECEPTOR BLOCKING AGENT; CALCIUM ION; CHLORIDE ION;

ANIMAL CELL; ARTICLE; CELL ISOLATION; CELL KINETICS; CONTROLLED STUDY; ENDOCYTOSIS; GOLDFISH; MEASUREMENT; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; STATISTICAL SIGNIFICANCE; SYNAPSE;

ANIMALS; BICUCULLINE; CALCIUM; CELLS, CULTURED; CHELATING AGENTS; CHLORIDES; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; EGTAZIC ACID; ENDOCYTOSIS; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; GOLDFISH; IONOPHORES; MEMBRANE POTENTIALS; MICROSCOPY, ELECTRON, TRANSMISSION; MODELS, NEUROLOGICAL; NEURAL INHIBITION; NEURONS; NYSTATIN; PATCH-CLAMP TECHNIQUES; PHOSPHINIC ACIDS; PICROTOXIN; PRESYNAPTIC TERMINALS; PYRIDINES; QUINOXALINES; RETINA; TIME FACTORS; VALINE;

EID: 7044233444     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2004.10.010     Document Type: Article

References (79)

1. 2+, GTP, and dynamin but not clathrin. Proc. Natl. Acad. Sci. USA. 92:1995;8328-8332
2. Beutner D., Voets T., Neher E., Moser T. Calcium dependence of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse. Neuron. 29:2001;681-690
3. Billups D., Attwell D. Control of intracellular chloride concentration and GABA response polarity in rat retinal ON bipolar cells. J. Physiol. 545:2002;183-198
4. Brodin L., Low P., Gad H., Gustafsson J., Pieribone V., Shupliakov O. Sustained neurotransmitter release. new molecular clues Eur. J. Neurosci. 9:1997;2503-2511
5. Burrone J., Neves G., Gomis A., Cooke A., Lagnado L. Endogenous calcium buffers regulate fast exocytosis in the synaptic terminal of retinal bipolar cells. Neuron. 33:2002;101-112
6. Chan S.A., Smith C. Low frequency stimulation of mouse adrenal slices reveals a clathrin-independent, protein kinase C-mediated endocytic mechanism. J. Physiol. 553:2003;707-717
7. - and inhibitory transmitters Mol. Pharmacol. 53:1998;564-572
8. 2+ inhibits dynamin and arrests synaptic vesicle endocytosis at the active zone. J. Neurosci. 20:2000;949-957
9. D'Amico S., Gerday C., Feller G. Structural similarities and evolutionary relationships in chloride-dependent α-amylases. Gene. 253:2000;95-105
10. Dallos P., Fakler B. Prestin, a new type of motor protein. Nat. Rev. Mol. Cell Biol. 3:2002;104-111
11. Daly C., Sugimori M., Moreira J.E., Ziff E.B., Llinás R. Synaptophysin regulates clathrin-independent endocytosis of synaptic vesicles. Proc. Natl. Acad. Sci. USA. 97:2000;6120-6125
12. DeCamilli P., Slepnev V.I., Shupliakov O., Brodin L. Synaptic vesicle endocytosis. Cowen M., Sudhof T.C., Stevens C.F. Synapses. 2001;217-274 The Johns Hopkins University Press, Baltimore
13. Delgado R., Maureira C., Oliva C., Kidokoro Y., Labarca P. Size of vesicle pools, rates of mobilization, and recycling at neuromuscular synapses of a Drosophila mutant, shibire. Neuron. 28:2000;941-953
14. Dong C., Werblin F. Temporal contrast enhancement via GABAC feedback at bipolar terminals in tiger salamander retina. J. Neurophysiol. 79:1998;2171-2180
15. Faundez, V., and Hartzell, H.C. (2004). Intracellular chloride channels: determinants of function in the endosomal pathway. Sci. STKE 2004, re8.
16. Gandhi S., Stevens C.F. Three modes of synaptic vesicular recycling revealed by single-vesicle imaging. Nature. 423:2003;607-613
17. Gray E.G., Pease H.L. On understanding the organization of retinal receptor synapses. Brain Res. 35:1971;1-15
18. Guatimosim C., Hull C., von Gersdorff H., Prado M.A. Okadaic acid disrupts vesicle trafficking in a ribbon-type synapse. J. Neurochem. 82:2002;1047-1057
19. Hartveit E. Reciprocal synaptic interactions between rod bipolar cells and amacrine cells in the rat retina. J. Neurophysiol. 81:1999;2923-2936
20. Heidelberger R. ATP is required at an early step in compensatory endocytosis in synaptic terminals. J. Neurosci. 21:2001;6467-6474
21. Heidelberger R., Matthews G. Calcium influx and calcium current in single synaptic terminals of goldfish retinal bipolar neurons. J. Physiol. 447:1992;235-256
22. Heidelberger R., Zhou Z.-Y., Matthews G. Multiple components of membrane retrieval in synaptic terminals revealed by changes in hydrostatic pressure. J. Neurophysiol. 88:2002;2509-2517
23. Hsu S.-F., Jackson M.B. Rapid exocytosis and endocytosis in nerve terminals of the rat posterior pituitary. J. Physiol. 494:1996;539-553
24. Jentsch T.J., Stein V., Weinreich F., Zdebik A. Molecular structure and physiological function of chloride channels. Phys. Rev. 82:2002;503-568
25. Klingauf J., Kavalali E., Tsien R. Kinetics and regulation of fast endocytosis at hippocampal synapses. Nature. 394:1998;581-585
26. Koenig J., Ikeda K. Synaptic vesicles have two distinct recycling pathways. J. Cell Biol. 135:1996;797-808
27. Kuner T., Augustine G.J. A genetically encoded ratiometric indicator for chloride. capturing chloride transients in cultured hippocampal cells Neuron. 27:2000;447-459
28. Lanius R.A., Pasqualotto B.A., Shaw C.A. Gamma-aminobutyric acid A receptor regulation by a chloride-dependent kinase and a sodium-dependent phosphatase. Brain Res. Mol. Brain Res. 20:1993;192-198
29. 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. 36:2002;649-659
30. Liu J., Sim A., Robinson P. Calcineurin inhibition of dynamin I GTPase activity coupled to nerve terminal depolarization. Science. 265:1994;970-973
31. C receptors confer distinct temporal properties to retinal synaptic responses. J. Neurophysiol. 79:1998;3157-3167
32. Lytle C., Forbush B. III. Regulatory phosphorylation of the secretory Na-K-Cl cotransporter. modulation by cytoplasmic Cl Am. J. Physiol. 270:1996;C437-C448
33. Marandi N., Konnerth A., Garashuk O. Two-photon chloride imaging in neurons of brain slices. Pflugers Arch. 445:2002;357-365
34. Marc R.E., Liu W.-L.S. Fundamental GABAergic amacrine cell circuits in the retina. nested feedback, concatenated inhibition, and axosomatic synapses J. Comp. Neurol. 425:2000;560-582
35. Marks B., McMahon H.T. Calcium triggers calcineurin-dependent synaptic vesicle recycling in mammalian nerve terminals. Curr. Biol. 8:1998;740-749
36. Matthews G., Ayoub G.S., Heidelberger R. Presynaptic inhibition by GABA is mediated via two distinct GABA receptors with novel pharmacology. J. Neurosci. 14:1994;1079-1090
37. McGillem G., Rotolo T., Dacheaux R. GABA responses of rod bipolar cells in rabbit retinal slices. Vis. Neurosci. 17:2000;381-389
38. Mennerick S., Matthews G. Ultrafast exocytosis elicited by calcium current in synaptic terminals of retinal bipolar neurons. Neuron. 17:1996;1241-1249
39. Micheva K., Buchanan J., Holz R., Smith S. Retrograde regulation of synaptic vesicle endocytosis and recycling. Nat. Neurosci. 6:2003;925-932
40. Miller T., Heuser J. Endocytosis of synaptic vesicle membrane at the frog neuromuscular junction. J. Cell Biol. 98:1984;685-698
41. Morgan J.R., Augustine G.J., Lafer E.M. Synaptic vesicle endocytosis. the races, places, and molecular faces Neuromolecular Med. 2:2002;101-114
42. Mueller V.J., Wienisch M., Nehring R.B., Klingauf J. Monitoring clathrin-mediated endocytosis during synaptic activity. J. Neurosci. 24:2004;2004-2012
43. Murray D., Honig B. Electrostatic control of the membrane targeting of C2 domains. Mol. Cell. 9:2002;145-154
44. Neher E., Marty A. Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells. Proc. Natl. Acad. Sci. USA. 79:1982;6712-6716
45. Neves G., Lagnado L. The kinetics of exocytosis and endocytosis in the synaptic terminal of goldfish retinal bipolar cells. J. Physiol. 515:1999;181-202
46. Neves G., Gomis A., Lagnado L. Calcium influx selects for the fast mode of endocytosis in the synaptic terminal of retinal bipolar cells. Proc. Natl. Acad. Sci. USA. 98:2001;15282-15287
47. 2+-dependent Cl current at the presynaptic terminals of goldfish bipolar cells. Neurosci. Res. 23:1995;297-303
48. Paillart C., Li J., Matthews G., Sterling P. Endocytosis and vesicle recycling at a ribbon synapse. J. Neurosci. 23:2003;4092-4099
49. Palmer M.J., Taschenberger H., Hull C., Tremere L., von Gersdorff H. Synaptic activation of presynaptic glutamate transporter currents in nerve terminals. J. Neurosci. 23:2003;4831-4841
50. Parsons T., Lenzi D., Almers W., Roberts W. Calcium-triggered exocytosis and endocytosis in an isolated presynaptic cell. capacitance measurements in saccular hair cells Neuron. 13:1994;875-883
51. Protti D.A., Llano I. Calcium currents and calcium signalling in rod bipolar cells of rat retinal slices. J. Neurosci. 18:1998;3715-3724
52. Ramaswami M., Krishnan K.S., Kelly R.B. Intermediates in synaptic vesicle recycling revealed by optical imaging of Drosophila neuromuscular junctions. Neuron. 13:1994;363-375
53. Richards D.A., Guatimosim C., Betz W.J. Two endocytotic recycling routes selectively fill two vesicle pools in frog motor nerve terminals. Neuron. 27:2000;551-559
54. Rieke F., Schwartz E. Asynchronous transmitter release. control of exocytosis and endocytosis at the salamander rod synapse J. Physiol. 493:1996;1-8
55. Roos J., Kelly R.B. The endocytic machinery in nerve terminals surrounds sites of exocytosis. Curr. Biol. 9:1999;1411-1414
56. Rouze N., Schwartz E. Continuous and transient vesicle cycling at a ribbon synapse. J. Neurosci. 18:1998;8614-8624
57. 2+-induced exocytosis from rat melanotrophs through GTP-binding proteins. Pflügers Arch. 431:1995;76-83
58. Sakaba T., Tachibana M., Matsui K., Minami N. Two components of transmitter release in retinal bipolar cells. exocytosis and mobilization of synaptic vesicles Neurosci. Res. 27:1997;357-370
59. Sankaranarayanan S., Ryan T.A. Calcium accelerates endocytosis of vSNARES at hippocampal synapses. Nat. Neurosci. 4:2001;129-136
60. Sherry D., Yazulla S. Goldfish bipolar cells and axon terminal patterns. a Golgi study J. Comp. Neurol. 329:1993;188-200
61. 2+ entry elicits transient postsynaptic currents at a retinal ribbon synapse. J. Neurosci. 23:2003;10923-10933
62. Smith C., Neher E. Multiple forms of endocytosis in bovine adrenal chromaffin cells. J. Cell Biol. 139:1997;885-894
63. Sun J.-Y., Wu X., Wu L.-G. Single and multiple vesicle fusion induce different rates of endocytosis at a central synapse. Nature. 417:2002;555-559
64. Tachibana M., Kaneko A. Gamma-aminobutyric acid exerts a local inhibitory action on the axon terminal of bipolar cells. evidence for negative feedback from amacrine cells Proc. Natl. Acad. Sci. USA. 84:1987;3501-3505
65. 2+ in snake motor boutons. J. Physiol. 551:2003;103-114
66. Thoreson W.B., Nitzan R., Miller R.F. Chloride efflux inhibits single calcium channel open probability in vertebrate photoreceptors. Chloride imaging and cell-attached patch-clamp recordings Vis. Neurosci. 17:2000;197-206
67. Verstreken P., Kjaeruff O., Lloyd T.E., Atkinson R., Zhou Y., Meinertzhagen I.A., Bellen H.J. Endophilin mutations block clathrin-mediated endocytosis but not neurotransmitter release. Cell. 109:2002;101-112
68. von Gersdorff H., Matthews G. Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals. Nature. 367:1994;735-739. a
69. von Gersdorff H., Matthews G. Inhibition of endocytosis by elevated internal calcium in a synaptic terminal. Nature. 370:1994;652-655. b
70. von Gersdorff H., Vardi E., Matthews G., Sterling P. Evidence that vesicles on the synaptic ribbon of retinal bipolar neurons can be rapidly released. Neuron. 16:1996;1221-1227
71. von Gersdorff H., Sakaba T., Berglund K., Tachibana M. Submillisecond kinetics of glutamate release from a sensory synapse. Neuron. 21:1998;1177-1188
72. von Kriegstein K., Schmitz F., Link E., Sudhof T.C. Distribution of synaptic vesicle proteins in the mammalian retina identifies obligatory and facultative components of ribbon synapses. Eur. J. Neurosci. 11:1999;1335-1348
73. Vu T.Q., Payne J.A., Copenhagen D.R. Localization and developmental expression patterns of the neuronal K-Cl cotransporter (KCC2) in the rat retina. J. Neurosci. 20:2000;1414-1423
74. Witkovsky P., Dowling J. Synaptic relationships in the plexiform layers of carp retina. Z. Zellforsch. Mikrosk. Anat. 100:1969;60-82
75. Wu L.-G., Betz W.J. Nerve activity but not intracellular calcium determines the time course of endocytosis at the frog neuromuscular junction. Neuron. 17:1996;769-779
76. Yao P.J., Coleman P.D., Calkins D.J. High-resolution localization of clathrin assembly protein AP180 in the presynaptic terminals of mammalian neurons. J. Comp. Neurol. 447:2002;152-162
77. Zenisek D., Steyer J.A., Feldman M.E., Almers W. A membrane marker leaves synaptic vesicles in milliseconds after exocytosis in retinal bipolar cells. Neuron. 35:2002;1085-1097
78. Zenisek D., Davila V., Wan L., Almers W. Imaging calcium entry sites and ribbon structures in two presynaptic cells. J. Neurosci. 23:2003;2538-2548
79. Zhang B., Ganetzky B., Bellen H.J., Murthy V.N. Tailoring uniform coats for synaptic vesicles during endocytosis. Neuron. 23:1999;419-422