Two modes of fusion pore opening revealed by cell-attached recordings at a synapse

Nature

Volumn 444, Issue 7115, 2006, Pages 102-105

  He, Liming ^a   Wu, Xin Sheng ^a   Mohan, Raja ^a   Wu, Ling Gang ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; GENES; GENETIC ENGINEERING;

CALYX-TYPE SYNAPSES; CELL MEMBRANE; SYNAPTIC CURRENTS;

BIODIVERSITY;

CELLS AND CELL COMPONENTS; KINETICS;

ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL FUSION; CELL MEMBRANE CONDUCTANCE; CELL VACUOLE; CONTROLLED STUDY; ELECTRIC CAPACITANCE; ELECTRIC CURRENT; NERVE ENDING; NONHUMAN; POROSITY; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; SYNAPSE;

COLAPTES;

EID: 33750585192     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature05250     Document Type: Article

References (30)

1. Breckenridge, L. J. & Almers, W. Currents through the fusion pore that forms during exocytosis of a secretory vesicle. Nature 328, 814-817 (1987).
2. Lindau, M. & Alvarez de Toledo, G. The fusion pore. Biochim. Biophys. Acta 164, 167-173 (2003).
3. Alvarez, D. T., Fernandez-Chacon, R. & Fernandez, J. M. Release of secretory products during transient vesicle fusion. Nature 363, 554-558 (1993).
4. Heuser, J. E. & Reese, T. S. Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 57, 315-344 (1973).
5. Ceccarelli, B., Hurlbut, W. P. & Mauro, A. Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J. Cell Biol. 57, 499-524 (1973).
6. Fesce, R., Grohovaz, F., Valtorta, F. & Meldolesi, J. Neurotransmitter release, fusion or 'kiss and run'? Trends Cell Biol. 4, 1-4 (1994).
7. Fernandez, J. M., Neher, E. & Gomperts, B. D. Capacitance measurements reveal stepwise fusion events in degranulating mast cells. Nature 312, 453-455 (1984).
8. Aravanis, A. M., Pyle, J. L. & Tsien, R. W. Single synaptic vesicles fusing transiently and successively without loss of identity. Nature 423, 643-647 (2003).
9. Gandhi, S. P. & Stevens, C. F. Three modes of synaptic vesicular recycling revealed by single-vesicle imaging. Nature 423, 607-613 (2003).
10. Fernandez-Alfonso, T. & Ryan, T. A. The kinetics of synaptic vesicle pool depletion at CNS synaptic terminals. Neuron 41, 943-953 (2004).
11. Sun, J. Y., Wu, X. S. & Wu, L. G. Single and multiple vesicle fusion induce different rates of endocytosis at a central synapse. Nature 417, 555-559 (2002).
12. Yamashita, T., Hige, T. & Takahashi, T. Vesicle endocytosis requires dynamin-dependent GTP hydrolysis at a fast CNS synapse. Science 307, 124-127 (2005).
13. Harata, N. C., Choi, S., Pyle, J. L., Aravanis, A. M. & Tsien, R. W. Frequency-dependent kinetics and prevalence of kiss-and-run and reuse at hippocampal synapses studied with novel quenching methods. Neuron 49, 243-256 (2006).
14. Wienisch, M. & Klingauf, J. Vesicular proteins exocytosed and subsequently retrieved by compensatory endocytosis are nonidentical. Nature Neurosci. 9, 1019-1027 (2006).
15. Fernandez-Alfonso, T., Kwan, R. & Ryan, T. A. Synaptic vesicles interchange their membrane proteins with a large surface reservoir during recycling. Neuron 51, 179-186 (2006).
16. Stiles, J. R., Van Helden, D., Bartol, T. M. Jr, Salpeter, E. E. & Salpeter, M. M. Miniature endplate current rise times less than 100 microseconds from improved dual recordings can be modeled with passive acetylcholine diffusion from a synaptic vesicle. Proc. Natl Acad. Sci. USA 93, 5747-5752 (1996).
17. Bruns, D. & Jahn, R. Real-time measurement of transmitter release from single synaptic vesicles. Nature 377, 62-65 (1995).
18. Klyachko, V. A. & Jackson, M. B. Capacitance steps and fusion pores of small and large-dense-core vesicles in nerve terminals. Nature 418, 89-92 (2002).
19. Lenn, N. J. & Reese, T. S. The fine structure of nerve endings in the nucleus of the trapezoid body and the ventral cochlear nucleus. Am. J. Anat. 118, 375-390 (1966).
20. Sätzler, K. et al. Three-dimensional reconstruction of a calyx of Held and its postsynaptic principal neuron in the medial nucleus of the trapezoid body. J. Neurosci. 22, 10567-10579 (2002).
21. Gentet, L. J., Stuart, G. J. & Clements, J. D. Direct measurement of specific membrane capacitance in neurons. Biophys. J. 79, 314-320 (2000).
22. Singer, J. H., Lassova, L., Vardi, N. & Diamond, J. S. Coordinated multivesicular release at a mammalian ribbon synapse. Nature Neurosci. 7, 826-833 (2004).
23. Debus, K. & Lindau, M. Resolution of patch capacitance recordings and of fusion pore conductances in small vesicles. Biophys. J. 78, 2983-2997 (2000).
24. Stiles, J. R., Bartol, T. B., Salpeter, M. M., Salpeter, E. E. & Sejnowski, T. J. in Synapses (eds Cowan, T. C., Sudhof, T. C. & Stevens, C. F.) 681-732 (Johns Hopkins Univ. Press, Baltimore, 2000).
25. Harata, N. et al. Limited numbers of recycling vesicles in small CNS nerve terminals: implications for neural signaling and vesicular cycling. Trends Neurosci. 24, 637-643 (2001).
26. Choi, S., Klingauf, J. & Tsien, R. W. Fusion pore modulation as a presynaptic mechanism contributing to expression of long-term potentiation. Phil. Trans. R. Soc. Lond. B 358, 695-705 (2003).
27. Pawlu, C., DiAntonio, A. & Heckmann, M. Postfusional control of quantal current shape. Neuron 42, 607-618 (2004).
28. Almers, W. et al. Millisecond studies of single membrane fusion events. Ann. NY Acad. Sci. 635, 318-327 (1991).
29. Spruce, A. E., Breckenridge, L. J., Lee, A. K. & Almers, W. Properties of the fusion pore that forms during exocytosis of a mast cell secretory vesicle. Neuron 4, 643-654 (1990).
30. Nielsen, T. A., Digregorio, D. A. & Silver, R. A. Modulation of glutamate mobility reveals the mechanism underlying slow-rising AMPAR EPSCs and the diffusion coefficient in the synaptic cleft. Neuron 42, 757-771 (2004).