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The Journal of Neuroscience, March 15, 1998, 18(6):2028-2039
Distinct Requirements for Evoked and Spontaneous Release of
Neurotransmitter Are Revealed by Mutations in the
Drosophila Gene neuronal-synaptobrevin
David L.
Deitcher1,
Atsushi
Ueda2,
Bryan A.
Stewart1,
Robert W.
Burgess1,
Yoshi
Kidokoro2, and
Thomas L.
Schwarz1
1 Department of Molecular and Cellular Physiology,
Beckman Center, Stanford University Medical Center, Stanford,
California 94305, and 2 Gunma University School of
Medicine, 3-39-22 Showa-machi, Maebashi, 371 Japan
Two modes of vesicular release of transmitter occur at a synapse:
spontaneous release in the absence of a stimulus and evoked release
that is triggered by Ca2+ influx. These modes often
have been presumed to represent the same exocytotic apparatus
functioning at different rates in different Ca2+
concentrations. To investigate the mechanism of transmitter release, we
have examined the role of synaptobrevin/VAMP, a protein involved in
vesicular docking and/or fusion. We generated a series of mutations, including null mutations, in neuronal-synaptobrevin
(n-syb), the neuronally expressed synaptobrevin gene in
Drosophila. Mutant embryos completely lacking
n-syb form morphologically normal neuromuscular junctions. Electrophysiological recordings from the neuromuscular junction of these mutants reveal that the excitatory synaptic current
evoked by stimulation of the motor neuron is abolished entirely.
However, spontaneous release of quanta from these terminals persists,
although its rate is reduced by 75%. Thus, at least a portion of the
spontaneous "minis" that are seen at the synapse can be generated
by a protein complex that is distinct from that required for an evoked
synaptic response.
Key words:
exocytosis; synaptobrevin; VAMP; Drosophila; synapse; neuromuscular junction; synaptic vesicle; spontaneous release; mini; regulated release
Copyright © 1998 Society for Neuroscience 0270-6474/98/1862028-12$05.00/0
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[Full Text]
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[Full Text]
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[Abstract]
[Full Text]
[PDF]
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