Exocytosis at the ribbon synapse of retinal bipolar cells studied in patches of presynaptic membrane

Journal of Neuroscience

Volumn 23, Issue 7, 2003, Pages 2706-2714

  Llobet, Artur ^a   Cooke, Anne ^a   Lagnado, Leon ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

Calcium; Capacitance; Endocytosis; Exocytosis; Synaptic terminal; Vesicle

Indexed keywords

ION CHANNEL;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; ELECTRON MICROSCOPY; ENDOCYTOSIS; EXOCYTOSIS; GOLDFISH; MEMBRANE DEPOLARIZATION; MEMBRANE POTENTIAL; MEMBRANE VESICLE; NEUROTRANSMITTER RELEASE; NONHUMAN; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RETINA BIPOLAR GANGLION CELL; SYNAPTIC MEMBRANE;

EID: 0037387064     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-07-02706.2003     Document Type: Article

References (49)

1. Albillos A, Dernick G, Horstmann H, Almers W, Alvarez de Toledo G, Lindau M (1997) The exocytotic event in chromaffin cells revealed by patch amperometry. Nature 389:509-512.
2. Ales E, Tabares L, Poyato JM, Valero V, Lindau M, Alvarez de Toledo G (1999) High calcium concentrations shift the mode of exocytosis to the kiss-and-run mechanism. Nat Cell Biol 1:40-44.
3. Atwood HL, Karunanithi S (2002) Diversification of synaptic strength: presynaptic elements. Nat Rev Neurosci 3:497-516.
4. Borst JG, Sakmann B (1996) Calcium influx and transmitter release in a fast CNS synapse. Nature 383:431-434.
5. Burns ME, Augustine GJ (1995) Synaptic structure and function: dynamic organization yields architectural precision. Cell 83:187-194.
6. 2+ influx in the synaptic terminal of depolarizing bipolar cells from the goldfish retina. J Physiol (Lond) 505:571-584.
7. Burrone J, Lagnado L (2000) Synaptic depression and the kinetics of exocytosis in retinal bipolar cells. J Neurosci 20:568-578.
8. Burrone J, Neves G, Gomis A, Cooke A, Lagnado L (2002) Endogenous calcium buffers regulate fast exocytosis in the synaptic terminal of retinal bipolar cells. Neuron 33:101-112.
9. Chow RH, Klingauf J, Heinemann C, Zucker RS, Neher E (1996) Mechanisms determining the time course of secretion in neuroendocrine cells. Neuron 16:369-376.
10. Debus K, Lindau M (2000) Resolution of patch capacitance recordings and of fusion pore conductances in small vesicles. Biophys J 78:2983-2997.
11. Debus K, Hartmann J, Kilic G, Lindau M (1995) Influence of conductance changes on patch clamp capacitance measurements using a lock-in amplifier and limitations of the phase tracking technique. Biophys J 69:2808-2822.
12. Fettiplace R, Fuchs PA (1999) Mechanisms of hair cell tuning. Annu Rev Physiol 61:809-834.
13. Gillis K (1995) Techniques for membrane capacitance measurements. In: Single channel recording, Ed 2 (Sakmann B, Neher E, eds), pp 155-197. New York: Plenum.
14. Gomis A, Burrone J, Lagnado L (1999) Two actions of calcium regulate the supply of releasable vesicles at the ribbon synapse of retinal bipolar cells. J Neurosci 19:6309-6317.
15. Gray EG, Pease HL (1971) On understanding the organisation of the retinal receptor synapses. Brain Res 35:1-15.
16. Henkel AW, Meiri H, Horstmann H, Lindau M, Almers W (2000) Rhythmic opening and closing of vesicles during constitutive exo- and endocytosis in chromaffin cells. EMBO J 19:84-93.
17. Hille B (2001) Ion channels of excitable membranes, Ed 3. Sunderland, MA: Sinauer Associates.
18. Horrigan FT, Bookman RJ (1994) Releasable pools and the kinetics of exocytosis in adrenal chromaffin cells. Neuron 13:1119-1129.
19. Hsu SF, Jackson MB (1996) Rapid exocytosis and endocytosis in nerve terminals of the rat posterior pituitary. J Physiol 494:539-553.
20. + channels at fluorescently labeled presynaptic active zones of hair cells. Proc Natl Acad Sci USA 91:7578-7582.
21. Kaneko A, Tachibana M (1985) A voltage-clamp analysis of membrane currents in solitary bipolar cells dissociated from Carassius auratus. J Physiol (Lond) 358:131-152.
22. Klyachko VA, Jackson MB (2002) Capacitance steps and fusion pores of small and large-dense-core vesicles in nerve terminals. Nature 418:89-92.
23. Lagnado L, Gomis A, Job C (1996) Continuous vesicle cycling in the synaptic terminal of retinal bipolar cells. Neuron 17:957-967.
24. Lenzi D, Runyeon JW, Crum J, Ellisman MH, Roberts WM (1999) Synaptic vesicle populations in saccular hair cells reconstructed by electron tomography. J Neurosci 19:119-132.
25. Lindau M, Stuenkel EL, Nordmann JJ (1992) Depolarization, intracellular calcium and exocytosis in single vertebrate nerve endings. Biophys J 61:19-30.
26. McManus OB (1990) Calcium-activated potassium channels: regulation by calcium. J Bioenerg Biomembr 23:537-560.
27. Mennerick S, Matthews G (1996) Ultrafast exocytosis elicited by calcium current in synaptic terminals of retinal bipolar neurons. Neuron 17:1241-1249.
28. Moser T, Beutner D (2000) Kinetics of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse of the mouse. Proc Natl Acad Sci USA 97:883-888.
29. 2+ microdomains: new tools for understanding their roles in neurotransmitter release. Neuron 20:389-399.
30. Neher E, Marty A (1982) Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells. Proc Natl Acad Sci USA 79:6712-6716.
31. Neher E, Zucker RS (1993) Multiple calcium-dependent processes related to secretion in bovine chromaffin cells. Neuron 10:21-30.
32. Neves G, Lagnado L (1999) The kinetics of exocytosis and endocytosis in the synaptic terminal of goldfish retinal bipolar cells. J Physiol (Lond) 515:181-202.
33. Neves G, Gomis A, Lagnado L (2001) Calcium influx selects the fast mode of endocytosis in the synaptic terminal of retinal bipolar cells. Proc Natl Acad Sci USA 98:15282-15287.
34. Parsons TD, Coorssen JR, Horstmann H, Almers W (1995) Docked granules, the exocytic burst, and the need for ATP hydrolysis in endocrine cells. Neuron 15:1085-1096.
35. Rae JL, Levis RA (1992) A method for exceptionally low noise single channel recordings. Pflügers Arch 420:618-620.
36. Rieke F, Schwartz EA (1994) A cGMP-gated current can control exocytosis at cone synapses. Neuron 13:863-873.
37. Roberts WM (1993) Spatial calcium buffering in saccular hair cells. Nature 363:74-76.
38. Roberts WM, Jacobs RA, Hudspeth AJ (1990) Colocalization of ion channels involved in frequency selectivity and synaptic transmission at presynaptic active zones of hair cells. J Neurosci 10:3664-3684.
39. Robinson IM, Finnegan JM, Monck JR, Wightman RM, Fernandez JM (1995) Colocalization of calcium entry and exocytotic release sites in adrenal chromaffin cells. Proc Natl Acad Sci USA 92:2474-2478.
40. Rosenmund C, Stevens CF (1996) Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16:1197-1207.
41. Sakaba T, Neher E (2001) Quantitative relationship between transmitter release and calcium current at the calyx of Held synapse. J Neurosci 21:462-476.
42. Sakmann B, Neher E (1995) Geometric parameters of pipettes and membrane patches. In: Single channel recording, Ed 2 (Sakmann B, Neher E, eds), pp 637-650. New York: Plenum.
43. Smith C, Neher E (1997) Multiple forms of endocytosis in bovine adrenal chromaffin cells. J Cell Biol 139:885-894.
44. Tachibana M, Okada T (1991) Release of endogenous excitatory amino acids from ON-type bipolar cells isolated from the goldfish retina. J Neurosci 11:2199-2208.
45. Tucker TR, Fettiplace R (1996) Monitoring calcium in turtle hair cells with a calcium-activated potassium channel. J Physiol 494:613-626.
46. von Gersdorff H, Matthews G (1994) Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals. Nature 367:735-739.
47. von Gersdorff H, Vardi E, Matthews G, Sterling P (1996) Evidence that vesicles on the synaptic ribbon of retinal bipolar neurons can be rapidly released. Neuron 16:1221-1227.
48. + channels. Nat Neurosci 3:566-571.
49. Zenisek D, Steyer JA, Almers W (2000) Transport, capture and exocytosis of single synaptic vesicles at active zones. Nature 406:849-854.