Fusion pore modulation as a presynaptic mechanism contributing to expression of long-term potentiation

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 358, Issue 1432, 2003, Pages 695-705

  Choi, Sukwoo ^a   Klingauf, Jürgen ^b   Tsien, Richard W ^c  

^a Ewha Womans University School of Medicine   (South Korea)

^b MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^c STANFORD UNIVERSITY   (United States)

Author keywords

Fusion pore; L AP5; Long term potentiation; Presynaptic mechanism; Silent synapse

Indexed keywords

NEUROLOGY;

ANIMALIA;

EID: 0038561178     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2002.1249     Document Type: Article

References (54)

1. Bliss, T. V. & Collingridge, G. L. 1993 A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39.
2. Bruns, D. & Jahn, R. 1995 Real-time measurement of transmitter release from single synaptic vesicles. Nature 377, 62-65.
3. Choi, S., Klingauf, J. & Tsien, R. W. 2000 Postfusional regulation of cleft glutamate concentration during LTP at 'silent synapses'. Nature Neurosci. 3, 330-336.
4. Clements, J. D. 1996 Transmitter time course in the synaptic cleft: its role in central synaptic function. Trends Neurosci. 19, 163-171.
5. Clements, J. D. & Westbrook, G. L. 1991 Activation kinetics reveal the number of glutamate and glycine binding sites on the N-methyl-D-aspartate receptor. Neuron 7, 605-613.
6. Clements, J. D., Lester, R. A., Tong, G., Jahr, C. E. & Westbrook, G. L. 1992 The time course of glutamate in the synaptic cleft. Science 258, 1498-1501.
7. Diamond, J. S. & Jahr, C. E. 1997 Transporters buffer synaptically released glutamate on a submillisecond time-scale. J. Neurosci. 17, 4672-4687.
8. Dixon, D. B., Bliss, T. V. P. & Fine, A. 2002 Individual hippocampal synapses express incremental (analog) and bi-directional long-term plasticity. Soc. Neurosci. Abstr. 28, 150.3.
9. Dube, G. R. & Liu, G. 1999 AMPA and NMDA receptors display similar affinity during rapid synaptic-like glutamate applications. Soc. Neurosci. Abstr. 25, 992.
10. Durand, G. M., Kovalchuk, Y. & Konnerth, A. 1996 Long-term potentiation and functional synapse induction in developing hippocampus. Nature 381, 71-75.
11. Emptage, N., Bliss, T. V. P. & Fine, A. 1999 Single synaptic events evoke NMDA receptor mediated release of calcium from internal stores in hippocampal dendritic spines. Neuron 22, 115-124.
12. Fisher, R. J., Pevsner, J. & Burgoyne, R. D. 2001 Control of fusion pore dynamics during exocytosis by Munc 18. Science 291, 875-878.
13. Gasparini, S., Saviane, C., Voronin, L. L. & Cherubini, E. 2000 Silent synapses in the developing hippocampus: lack of functional AMPA receptors or low probability of glutamate release? Proc. Natl Acad. Sci. USA 97, 9741-9746.
14. Gomperts, S. N., Rao, A., Craig, A. M., Malenka, R. C. & Nicoll, R. A. 1998 Postsynaptically silent synapses in single neuron cultures. Neuron 21, 1443-1451.
15. Graham, M. E., Fisher, R. J. & Burgoyne, R. D. 2000 Measurement of exocytosis by amperometry in adrenal chromaffin cells: effects of clostridial neurotoxins and activation of protein kinase C on fusion pore kinetics. Biochimie 82, 469-479.
16. Hayashi, Y., Shi, S. H., Esteban, J. A., Piccini, A., Poncer, J. C. & Malinow, R. 2000 Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287, 2262-2267.
17. Isaac, J. T., Nicoll, R. A. & Malenka, R. C. 1995 Evidence for silent synapses: implications for the expression of LTP. Neuron 15, 427-434.
18. Jonas, P. & Sakmann, B. 1992 Glutamate receptor channels in isolated patches from CA1 and CA3 pyramidal cells of rat hippocampal slices. J. Physiol. (Lond.) 455, 143-171.
19. Jonas, P., Major, G. & Sakmann, B. 1993 Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. J. Physiol. (Lond.) 472, 615-663.
20. Klyachko, V. A. & Jackson, M. B. 2002 Capacitance steps and fusion pores of small and large-dense-core vesicles in nerve terminals. Nature 418, 89-92.
21. Kullmann, D. M. & Asztely, F. 1998 Extrasynaptic glutamate spillover in the hippocampus: evidence and implications. Trends Neurosci. 21, 8-14.
22. Liao, D., Hessler, N. A. & Malinow, R. 1995 Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375, 400-404.
23. Liao, D., Zhang, X., O'Brien, R., Ehler, M. D. & Huganir, R. L. 1999 Regulation of morphological postsynaptic silent synapses in developing hippocampal neurons. Nature Neurosci. 2, 37-43.
24. Liu, G., Choi, S. & Tsien, R. W. 1999 Variability of neurotransmitter concentration and nonsaturation of postsynaptic AMPA receptors at synapses in hippocampal cultures and slices. Neuron 22, 395-409.
25. Lollike, K., Borregaard, N. & Lindau, M. 1998 Capacitance flickers and pseudoflickers of small granules, measured in the cell-attached configuration. Biophys. J. 75, 53-59.
26. McAllister, A. K. & Stevens, C. F. 2000 Nonsaturation of AMPA and NMDA receptors at hippocampal synapses. Proc. Natl Acad. Sci. USA 97, 6173-6178.
27. McNaughton, B. L. & Morris, R. G. M. 1987 Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci. 10, 408-415.
28. Magee, J. C. & Johnston, D. 1997 A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science 275, 209-213.
29. Malgaroli, A. & Tsien, R. W. 1992 Glutamate-induced long-term potentiation of the frequency of miniature synaptic currents in cultured hippocampal neurons. Nature 357, 134-139.
30. Malgaroli, A., Ting, A. E., Wendland, B., Bergamaschi, A., Villa, A., Tsien, R. W. & Scheller, R. H. 1995 Presynaptic component of long-term potentiation visualized at individual hippocampal synapses. Science 268, 1624-1628.
31. Malinow, R. & Tsien, R. W. 1990 Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices. Nature 346, 177-180.
32. Malinow, R., Schulman, H. & Tsien, R. W. 1989 Inhibition of postsynaptic PKC or CaMKII blocks induction but not expression of LTP. Science 245, 862-866.
33. Montgomery, J. M., Palvlidis, P. & Madison, D. V. 2001 Pair recordings reveal all-silent synaptic connections and the postsynaptic expression of long-term potentiation. Neuron 29, 691-701.
34. Nüsser, Z., Lujan, R., O'Brien, R. J., Kamboj, S., Ehler, M. D., Rosen, K. R., Fischbach, G. D. & Huganir, R. L. 1998 Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 21, 545-559.
35. Oertner, T. G., Sabatini, B. L., Nimchinsky, E. A. & Svoboda, K. 2002 Facilitation at single synapses probed with optical quantal analysis. Nature Neurosci. 5, 657-664.
36. 3H]D-2-amino-5-phosphonopentanoic acid binding in rat brain membranes. Neuroscience 26, 17-31.
37. Otmakhova, N. A., Otmakhov, N., Mortenson, L. H. & Lisman, J. E. 2000 Inhibition of the cAMP pathway decreases early long-term potentiation at CA1 hippocampal synapses. J. Neurosci. 20, 4446-4451.
38. Pothos, E. N., Przedborski, S., Davila, V., Schmitz, Y. & Sulzer, D. 1998 D2-Like dopamine autoreceptor activation reduces quantal size in PC12 cells. J. Neurosci. 18, 4106-4118.
39. Pyle, J. L., Kavalali, E. T., Choi, S. & Tsien, R. W. 1999 Visualization of synaptic activity in hippocampal slices with FM1-43 enabled by fluorescence quenching. Neuron 24, 803-808.
40. Raman, I. M. & Trussell, L. O. 1995 The mechanism of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionate receptor desensitization after removal of glutamate. Biophys. J. 68, 137-146.
41. Renger, J. J., Egles, C. & Liu, G. 2001 A developmental switch in neurotransmitter flux enhances synaptic efficacy by affecting AMPA receptor activation. Neuron 29, 469-484.
42. Rosenmund, C., Stern-Bach, Y. & Stevens, C. F. 1998 The tetrameric structure of a glutamate receptor channel. Science 280, 1596-1599.
43. Rusakov, D. A. & Kullmann, D. M. 1998 Extrasynaptic glutamate diffusion in the hippocampus: ultrastructural constraints, uptake, and receptor activation. J. Neurosci. 18, 3158-3170.
44. Ryan, T. A., Ziv, N. E. & Smith, S. J. 1996 Potentiation of evoked vesicle turnover at individually resolved synaptic boutons. Neuron 17, 125-134.
45. 2+ and protein kinase C via distinct mechanisms. EMBO J. 17, 4340-4346.
46. Shi, S. H., Hayashi, Y., Petralia, R. S., Zaman, S. H., Wenthold, R. J., Svoboda, K. & Malinow, R. 1999 Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284, 1811-1816.
47. Shi, S. H., Hayashi, Y., Esteban, J. A. & Malinow, R. 2001 Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105, 331-343.
48. Spruce, A. E., Breckenridge, L. J., Lee, A. K. & Almers, W. 1990 Properties of the fusion pore that forms during exocytosis of a mast cell secretory vesicle. Neuron 4, 643-654.
49. Stanton, P. K., Heinemann, U. & Muller, W. 2001 FM1-43 imaging reveals cGMP-dependent long-term depression of presynaptic transmitter release. J. Neurosci. 21, RC167.
50. Stiles, J. R., Van Helden, D., Bartol Jr, T. M., Salpeter, E. E. & Salpeter, M. M. 1996 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.
51. Wadiche, J. I. & Kavanaugh, M. P. 1998 Macroscopic and microscopic properties of a cloned glutamate transporter/chloride channel. J. Neurosci. 18, 7650-7661.
52. Zakharenko, S. S., Zablow, L. & Siegelbaum, S. A. 2001 Visualization of changes in presynaptic function during long-term synaptic plasticity. Nature Neurosci. 4, 711-717.
53. Zakharenko, S. S., Zablow, L. & Siegelbaum, S. A. 2002 Altered presynaptic vesicle release and cycling during mGluR-dependent LTD. Neuron 35, 1099-1110.
54. Zhou, Z., Misler, S. & Chow, R. H. 1996 Rapid fluctuations in transmitter release from single vesicles in bovine adrenal chromaffin cells. Biophys. J. 70, 1543-1552.