Synaptic vesicles in rat hippocampal boutons recycle to different pools in a use-dependent fashion

Journal of Physiology

Volumn 572, Issue 3, 2006, Pages 707-720

  Vanden Berghe, Pieter ^a   Klingauf, Jürgen ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYAN FLUORESCENT PROTEIN; DYE; POSTSYNAPTIC DENSITY PROTEIN 95;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CELL FATE; CELL KINETICS; CELL LABELING; CELL METABOLISM; CELL TRANSPORT; COLOR; CONTROLLED STUDY; ENDOCYTOSIS; GENETIC TRANSFECTION; HIPPOCAMPUS; MOLECULAR PROBE; NERVE CELL STIMULATION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SYNAPSE VESICLE; BRAIN SYNAPTOSOME; CONFOCAL MICROSCOPY; HIPPOCAMPAL BOUTON; POSTSYNAPTIC POTENTIAL; SIMULATION;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; ELECTRIC STIMULATION; ENDOCYTOSIS; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; NEURONS; PRESYNAPTIC TERMINALS; RATS; SYNAPSES; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES;

EID: 33645821658     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2005.100842     Document Type: Article

References (43)

1. Aravanis AM, Pyle JL & Tsien RW (2003). Single synaptic vesicles fusing transiently and successively without loss of identity. Nature 423, 643-647.
2. Betz WJ & Bewick GS (1992). Optical analysis of synaptic vesicle recycling at the frog neuromuscular junction. Science 255, 200-203.
3. Betz WJ, Bewick GS & Ridge RM (1992). Intracellular movements of fluorescently labeled synaptic vesicles in frog motor nerve terminals during nerve stimulation. Neuron 9, 805-813.
4. Ceccarelli B, Hurlbut WP & Mauro A (1973). Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J Cell Biol 57, 499-524.
5. Chi P, Greengard P & Ryan TA (2003). Synaptic vesicle mobilization is regulated by distinct synapsin I phosphorylation pathways at different frequencies. Neuron 38, 69-78.
6. de Lange RP, de Roos AD & Borst JG (2003). Two modes of vesicle recycling in the rat calyx of Held. J Neurosci 23, 10164-10173.
7. Fernandez-Alfonso T & Ryan TA (2004). The kinetics of synaptic vesicle pool depletion at CNS synaptic terminals. Neuron 41, 943-953.
8. Fesce R, Grohovaz F, Valtorta F & Meldolesi J (1994). Neurotransmitter release: Fusion or 'kiss-and-run'?Trends Cell Biol 4, 1-4.
9. Gandhi SP & Stevens CF (2003). Three modes of synaptic vesicular recycling revealed by single-vesicle imaging. Nature 423, 607-613.
10. Harata N, Pyle JL, Aravanis AM, Mozhayeva M, Kavalali ET & Tsien RW (2001). Limited numbers of recycling vesicles in small CNS nerve terminals: Implications for neural signaling and vesicular cycling. Trends Neurosci 24, 637-643.
11. Hell SW (2003). Toward fluorescence nanoscopy. Nat Biotechnol 21, 1347-1355.
12. Heuser JE & Reese TS (1973). Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J Cell Biol 57, 315-344.
13. Holt M & Jahn R (2004). Neuroscience. Synaptic vesicles in the fast lane. Science 303, 1986-1987.
14. Klingauf J, Kavalali ET & Tsien RW (1998). Kinetics and regulation of fast endocytosis at hippocampal synapses. Nature 394, 581-585.
15. Koenig JH & Ikeda K (1996). Synaptic vesicles have two distinct recycling pathways. J Cell Biol 135, 797-808.
16. 2+ influx through distinct routes controls exocytosis and endocytosis at Drosophila presynaptic terminals. Neuron 41, 101-111.
17. Kuromi H & Kidokoro Y (1998). Two distinct pools of synaptic vesicles in single presynaptic boutons in a temperature-sensitive Drosophila mutant, shibire. Neuron 20, 917-925.
18. Kuromi H & Kidokoro Y (1999). The optically determined size of exo/ endo cycling vesicle pool correlates with the quantal content at the neuromuscular junction of Drosophila larvae. J Neurosci 19, 1557-1565.
19. 2+ at the Drosophila synapse. Neuron 35, 333-343.
20. Lemke EA & Klingauf JK (2005). Single synaptic vesicle tracking in individual hippocampal boutons at rest and during synaptic activity. J Neurosci 25, 11034-11044.
21. Li Z, Burrone J, Tyler WJ, Hartman KN, Albeanu DF & Murthy VN (2005). Synaptic vesicle recycling studied in transgenic mice expressing synaptopHluorin. Proc Natl Acad Sci U S A 102, 6131-6136.
22. Lin MY, Teng H & Wilkinson RS (2005). Vesicles in snake motor terminals comprise one functional pool and utilize a single recycling strategy at all stimulus frequencies. J Physiol 568, 413-421.
23. Miller TM & Heuser JE (1984). Endocytosis of synaptic vesicle membrane at the frog neuromuscular junction. J Cell Biol 98, 685-698.
24. Mueller VJ, Wienisch M, Nehring RB & Klingauf J (2004). Monitoring clathrin-mediated endocytosis during synaptic activity. J Neurosci 24, 2004-2012.
25. Murthy VN & Stevens CF (1998). Synaptic vesicles retain their identity through the endocytic cycle. Nature 392, 497-501.
26. Murthy VN & Stevens CF (1999). Reversal of synaptic vesicle docking at central synapses. Nat Neurosci 2, 503-507.
27. Pieribone VA, Shupliakov O, Brodin L, Hilfiker-Rothenfluh S, Czernik AJ & Greengard P (1995). Distinct pools of synaptic vesicles in neurotransmitter release. Nature 375, 493-497.
28. Pyle JL, Kavalali ET, Piedras-Renteria ES & Tsien RW (2000). Rapid reuse of readily releasable pool vesicles at hippocampal synapses. Neuron 28, 221-231.
29. Richards DA, Guatimosim C & Betz WJ (2000). Two endocytic recycling routes selectively fill two vesicle pools in frog motor nerve terminals. Neuron 27, 551-559.
30. Richards DA, Guatimosim C, Rizzoli SO & Betz WJ (2003). Synaptic vesicle pools at the frog neuromuscular junction. Neuron 39, 529-541.
31. Rizzoli SO & Betz WJ (2004). The structural organization of the readily releasable pool of synaptic vesicles. Science 303, 2037-2039.
32. Rosenmund C & Stevens CF (1996). Definition of the readily releasable pool of vesicles at hippocampal synapses. Neuron 16, 1197-1207.
33. Royle SJ & Lagnado L (2003). Endocytosis at the synaptic terminal. J Physiol 553, 345-355.
34. Ryan TA, Reuter H, Wendland B, Schweizer FE, Tsien RW & Smith SJ (1993). The kinetics of synaptic vesicle recycling measured at single presynaptic boutons. Neuron 11, 713-724.
35. Sankaranarayanan S, Atluri PP & Ryan TA (2003). Actin has a molecular scaffolding, not propulsive, role in presynaptic function. Nat Neurosci 6, 127-135.
36. Sara Y, Mozhayeva MG, Liu X & Kavalali ET (2002). Fast vesicle recycling supports neurotransmission during sustained stimulation at hippocampal synapses. J Neurosci 22, 1608-1617.
37. Schikorski T & Stevens CF (2001). Morphological correlates of functionally defined synaptic vesicle populations. Nat Neurosci 4, 391-395.
38. Schneggenburger R & Neher E (2000). Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406, 889-893.
39. Stevens CF & Tsujimoto T (1995). Estimates for the pool size of releasable quanta at a single central synapse and for the time required to refill the pool. Proc Natl Acad Sci U S A 92, 846-849.
40. Sudhof TC (2000). The synaptic vesicle cycle revisited. Neuron 28, 317-320.
41. Sun JY, Wu XS & Wu LG (2002). Single and multiple vesicle fusion induce different rates of endocytosis at a central synapse. Nature 417, 555-559.
42. Virmani T, Han W, Liu X, Sudhof TC & Kavalali ET (2003). Synaptotagmin 7 splice variants differentially regulate synaptic vesicle recycling. EMBO J 22, 5347-5357.
43. Wu LG & Betz WJ (1996). Nerve activity but not intracellular calcium determines the time course of endocytosis at the frog neuromuscular junction. Neuron 17, 769-779.