Constitutive sharing of recycling synaptic vesicles between presynaptic boutons.
The synaptic vesicle cycle is vital for sustained neurotransmitter release. It has been assumed that functional synaptic vesicles are replenished autonomously at individual presynaptic terminals. Here we tested this assumption by using FM dyes in combination with fluorescence recovery after photobleaching and correlative light and electron microscopy in cultured rat hippocampal neurons. After photobleaching, synapses acquired recently recycled FM dye-labeled vesicles originating from nonphotobleached synapses by a process requiring dynamic actin turnover. The imported vesicles entered the functional pool at their host synapses, as revealed by the exocytic release of the dye upon stimulation. FM1-43 photoconversion and ultrastructural analysis confirmed the incorporation of imported vesicles into the presynaptic terminal, where they mixed with the native vesicle pools. Our results demonstrate that synaptic vesicle recycling is not confined to individual presynaptic terminals as is widely believed; rather, a substantial proportion of recycling vesicles are shared constitutively between boutons.
Darcy
Kevin J
KJ
MRC Laboratory for Molecular Cell Biology and Cell Biology Unit, University College London, Gower Street, London WC1E 6BT, UK.
Staras
Kevin
K
Collinson
Lucy M
LM
Goda
Yukiko
Y
D000818:Animals; D000831:Animals, Newborn; D002451:Cell Compartmentation / Q000502:physiology; D002478:Cells, Cultured; D004705:Endocytosis / Q000502:physiology; D005089:Exocytosis / Q000502:physiology; D006624:Hippocampus / Q000502:physiology* / Q000648:ultrastructure; D008561:Membrane Fusion / Q000502:physiology; D046529:Microscopy, Electron, Transmission; D009434:Neural Pathways / Q000502:physiology / Q000648:ultrastructure; D017729:Presynaptic Terminals / Q000502:physiology* / Q000648:ultrastructure; D011726:Pyridinium Compounds; D000644:Quaternary Ammonium Compounds; D051381:Rats; D013570:Synaptic Membranes / Q000378:metabolism / Q000648:ultrastructure; D009435:Synaptic Transmission / Q000502:physiology*; D013572:Synaptic Vesicles / Q000502:physiology* / Q000648:ultrastructure
C092350:FM 4-64; C073804:FM1 43; D011726:Pyridinium Compounds; D000644:Quaternary Ammonium Compounds