Frequency-Dependent Kinetics and Prevalence of Kiss-and-Run and Reuse at Hippocampal Synapses Studied with Novel Quenching Methods

The kinetics of exo-endocytotic recycling could restrict information transfer at central synapses if neurotransmission were entirely reliant on classical full-collapse fusion. Nonclassical fusion retrieval by kiss-and-run would be kinetically advantageous but remains controversial. We used a hydroph...

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Bibliographic Details
Published in:Neuron (Cambridge, Mass.) Mass.), 2006-01, Vol.49 (2), p.243-256
Main Authors: Harata, Nobutoshi C., Choi, Sukwoo, Pyle, Jason L., Aravanis, Alexander M., Tsien, Richard W.
Format: Article
Language:English
Subjects:
Animals
Bromphenol Blue
CELLBIO
Cells, Cultured
Coloring Agents
Electric Stimulation
Endocytosis - physiology
Exocytosis - physiology
Green Fluorescent Proteins - metabolism
Hippocampus - physiology
Kinetics
MOLNEURO
Neurons - physiology
Presynaptic Terminals - physiology
Pyridinium Compounds - metabolism
Quaternary Ammonium Compounds - metabolism
Rats
Rats, Sprague-Dawley
Synapses - physiology
Synaptic Transmission - physiology
Temperature
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Summary:The kinetics of exo-endocytotic recycling could restrict information transfer at central synapses if neurotransmission were entirely reliant on classical full-collapse fusion. Nonclassical fusion retrieval by kiss-and-run would be kinetically advantageous but remains controversial. We used a hydrophilic quencher, bromophenol blue (BPB), to help detect nonclassical events. Upon stimulation, extracellular BPB entered synaptic vesicles and quenched FM1-43 fluorescence, indicating retention of FM dye beyond first fusion. BPB also quenched fluorescence of VAMP (synaptobrevin-2)-EGFP, thus indicating the timing of first fusion of vesicles in the total recycling pool. Comparison with FM dye destaining revealed that kiss-and-run strongly prevailed over full-collapse fusion at low frequency, giving way to a near-even balance at high frequency. Quickening of kiss-and-run vesicle reuse was also observed at higher frequency in the average single vesicle fluorescence response. Kiss-and-run and reuse could enable hippocampal nerve terminals to conserve scarce vesicular resources when responding to widely varying input patterns.
ISSN:0896-6273
1097-4199
DOI:10.1016/j.neuron.2005.12.018