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© The Rockefeller University Press, 0022-1295/1998//569/ $5.00
Journal of General Physiology, Volume 112, Number 5, 1998

Article

The Calcium Sensitivity of Individual Secretory Vesicles Is Invariant with the Rate of Calcium Delivery

Paul S. Blank*, Steven S. Vogel*, Myoung-Soon Cho*, Doron Kaplan*, Devang Bhuva*, James Malley{ddagger}, and Joshua Zimmerberg*

From the * Laboratory of Cellular and Molecular Biophysics, National Institute of Child Health and Human Development; and {ddagger} Computational Biology and Engineering Laboratory, Center for Information Technology, National Institutes of Health, Bethesda, Maryland 20892

Differences in the calcium sensitivity of individual secretory vesicles can explain a defining feature of calcium-regulated exocytosis, a graded response to calcium. The role of the time dependence of calcium delivery in defining the observed differences in the calcium sensitivity of sea urchin egg secretory vesicles in vitro was examined. The calcium sensitivity of individual secretory vesicles (i.e., the distribution of calcium thresholds) is invariant over a range of calcium delivery rates from faster than micromolar per millisecond to slower than micromolar per second. Any specific calcium concentration above threshold triggers subpopulations of vesicles to fuse, and the size of these subpopulations is independent of the time course required to reach that calcium concentration. All evidence supports the hypothesis that the magnitude of the free calcium is the single controlling variable that determines the fraction of vesicles that fuse, and that this fraction is established before the application of calcium. Submaximal responses to calcium cannot be attributed to alterations in the calcium sensitivity of individual secretory vesicles arising from the temporal properties of the calcium delivery. Models that attempt to explain the cessation of fusion using changes in the distribution of calcium thresholds arising from the rate of calcium delivery and/or adaptation are not applicable to this system, and thus cannot be general.

Key Words: cytoplasmic vesicles • fertilization • membrane fusion • sea urchins • secretion

Address correspondence to Paul S. Blank, LCMB/NICHD/NIH, Bldg. 10, Rm. 10D14, 10 Center Drive MSC 1855, Bethesda, MD 20892-1855. Fax: 301-480-0857; E-mail: psblank{at}helix.nih.gov


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