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The Journal of Neurophysiology Vol. 88 No. 1 July 2002, pp. 98-106
Copyright ©2002 by the American Physiological Society
1Department of Neurobiology and Anatomy and The W. M. Keck Center for the Neurobiology of Learning and Memory, University of Texas Medical School, Houston, Texas 77030; 2Department of Neuroscience, University of Pennsylvania, Philadelphia, Pennsylvania 19104; and 3Department of Neurobiology and Behavior, State University of New York, Stony Brook, New York 11794-5230
Heidelberger, Ruth,
Peter Sterling, and
Gary Matthews.
Roles of ATP in Depletion and Replenishment of the Releasable
Pool of Synaptic Vesicles. J. Neurophysiol. 88: 98-106, 2002. Synaptic terminals of retinal bipolar
neurons contain a pool of readily releasable synaptic vesicles that
undergo rapid calcium-dependent release. ATP hydrolysis is required for
the functional refilling of this vesicle pool. However, it was unclear
which steps required ATP hydrolysis: delivery of vesicles to their
anatomical release sites or preparation of synaptic vesicles and/or the
secretory apparatus for fusion. To address this, we dialyzed single
synaptic terminals with ATP or the poorly hydrolyzable analogue
ATP-
S and examined the size of the releasable pool, refilling of the releasable pool, and the number of vesicles at anatomical active zones.
After minutes of dialysis with ATP-S, vesicles already in the
releasable pool could still be discharged. This pool was not
functionally refilled despite the fact that its anatomical correlate,
the number of synaptic vesicles tethered to active zone synaptic
ribbons, was completely normal. We conclude 1) because the
existing releasable pool is stable during prolonged inhibition of ATP
hydrolysis, whereas entry into the functional pool is blocked, a
vesicle on entering the pool will tend to remain there until it fuses;
2) because the anatomical pool is unaffected by inhibition of ATP hydrolysis, failure to refill the functional pool is not caused
by failure of vesicle movement; 3) local vesicle movements important for pool refilling and fusion are independent of conventional ATP-dependent motor proteins; and 4) ATP hydrolysis is
required for the biochemical transition of vesicles and/or release
sites to fusion-competent status.
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