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J Neurophysiol 88: 98-106, 2002;
0022-3077/02 $5.00
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The Journal of Neurophysiology Vol. 88 No. 1 July 2002, pp. 98-106
Copyright ©2002 by the American Physiological Society

Roles of ATP in Depletion and Replenishment of the Releasable Pool of Synaptic Vesicles

Ruth Heidelberger,1 Peter Sterling,2 and Gary Matthews3

 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-gamma 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-gamma 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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