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.
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1 November 1998
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November 01 1998
The Calcium Sensitivity of Individual Secretory Vesicles Is Invariant with the Rate of Calcium Delivery
Paul S. Blank,
Paul S. Blank
From the *Laboratory of Cellular and Molecular Biophysics, National Institute of Child Health and Human Development; and ‡Computational Biology and Engineering Laboratory, Center for Information Technology, National Institutes of Health, Bethesda, Maryland 20892
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Steven S. Vogel,
Steven S. Vogel
From the *Laboratory of Cellular and Molecular Biophysics, National Institute of Child Health and Human Development; and ‡Computational Biology and Engineering Laboratory, Center for Information Technology, National Institutes of Health, Bethesda, Maryland 20892
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Myoung-Soon Cho,
Myoung-Soon Cho
From the *Laboratory of Cellular and Molecular Biophysics, National Institute of Child Health and Human Development; and ‡Computational Biology and Engineering Laboratory, Center for Information Technology, National Institutes of Health, Bethesda, Maryland 20892
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Doron Kaplan,
Doron Kaplan
From the *Laboratory of Cellular and Molecular Biophysics, National Institute of Child Health and Human Development; and ‡Computational Biology and Engineering Laboratory, Center for Information Technology, National Institutes of Health, Bethesda, Maryland 20892
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Devang Bhuva,
Devang Bhuva
From the *Laboratory of Cellular and Molecular Biophysics, National Institute of Child Health and Human Development; and ‡Computational Biology and Engineering Laboratory, Center for Information Technology, National Institutes of Health, Bethesda, Maryland 20892
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James Malley,
James Malley
From the *Laboratory of Cellular and Molecular Biophysics, National Institute of Child Health and Human Development; and ‡Computational Biology and Engineering Laboratory, Center for Information Technology, National Institutes of Health, Bethesda, Maryland 20892
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Joshua Zimmerberg
Joshua Zimmerberg
From the *Laboratory of Cellular and Molecular Biophysics, National Institute of Child Health and Human Development; and ‡Computational Biology and Engineering Laboratory, Center for Information Technology, National Institutes of Health, Bethesda, Maryland 20892
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Paul S. Blank
From the *Laboratory of Cellular and Molecular Biophysics, National Institute of Child Health and Human Development; and ‡Computational Biology and Engineering Laboratory, Center for Information Technology, National Institutes of Health, Bethesda, Maryland 20892
Steven S. Vogel
From the *Laboratory of Cellular and Molecular Biophysics, National Institute of Child Health and Human Development; and ‡Computational Biology and Engineering Laboratory, Center for Information Technology, National Institutes of Health, Bethesda, Maryland 20892
Myoung-Soon Cho
From the *Laboratory of Cellular and Molecular Biophysics, National Institute of Child Health and Human Development; and ‡Computational Biology and Engineering Laboratory, Center for Information Technology, National Institutes of Health, Bethesda, Maryland 20892
Doron Kaplan
From the *Laboratory of Cellular and Molecular Biophysics, National Institute of Child Health and Human Development; and ‡Computational Biology and Engineering Laboratory, Center for Information Technology, National Institutes of Health, Bethesda, Maryland 20892
Devang Bhuva
From the *Laboratory of Cellular and Molecular Biophysics, National Institute of Child Health and Human Development; and ‡Computational Biology and Engineering Laboratory, Center for Information Technology, National Institutes of Health, Bethesda, Maryland 20892
James Malley
From the *Laboratory of Cellular and Molecular Biophysics, National Institute of Child Health and Human Development; and ‡Computational Biology and Engineering Laboratory, Center for Information Technology, National Institutes of Health, Bethesda, Maryland 20892
Joshua Zimmerberg
From the *Laboratory of Cellular and Molecular Biophysics, National Institute of Child Health and Human Development; and ‡Computational Biology and Engineering Laboratory, Center for Information Technology, National Institutes of Health, Bethesda, Maryland 20892
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: [email protected]
Portions of this work have been previously presented in abstract form (Blank, P.S., M.S. Cho, S.S. Vogel, D. Kaplan, D. Bhuva, A. Kang, J. Malley, and J. Zimmerberg. 1997. J. Gen. Physiol. 110:17a).
Dr. Kaplan's present address is Israel Institute for Biological Research, Ness-Ziona, Israel 70400. Dr. Vogel's present address is Medical College of Georgia, Augusta, GA 30912-2630.
Received:
January 12 1998
Accepted:
September 15 1998
Online ISSN: 1540-7748
Print ISSN: 0022-1295
1998
J Gen Physiol (1998) 112 (5): 569–576.
Article history
Received:
January 12 1998
Accepted:
September 15 1998
Citation
Paul S. Blank, Steven S. Vogel, Myoung-Soon Cho, Doron Kaplan, Devang Bhuva, James Malley, Joshua Zimmerberg; The Calcium Sensitivity of Individual Secretory Vesicles Is Invariant with the Rate of Calcium Delivery . J Gen Physiol 1 November 1998; 112 (5): 569–576. doi: https://doi.org/10.1085/jgp.112.5.569
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