Abstract
RAPID calcium-dependent exocytosis underlies neurotransmitter release from nerve terminals. Despite the fundamental importance of this process, neither the relationship between presynaptic intra-cellular calcium ion concentration ([Ca2+]i) and rate of exocytosis, nor the maximal rate of secretion is known quantitatively. To provide this information, we have used flash photolysis of caged Ca2+ to elevate [Ca2+]i rapidly and uniformly in synaptic terminals, while measuring membrane capacitance as an index of exocytosis and monitoring [Ca2+]i with a Ca2+-indicator dye. When [Ca2+]i was abruptly increased to >10 µM, capacitance rose at a rate that increased steeply with [Ca2+]i. The steepness suggested that at least four calcium ions must bind to activate synaptic vesicle fusion. Half-saturation was at 194 µM, and the maximal rate constant was 2,000–3,000 s–1. A given synaptic vesicle can exocytose with high probability within a few hundred microseconds, if [Ca2+]i rises above lOOµM. These properties provide for the extremely rapid signalling required for neuronal communication.
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References
Ishida, A. T., Stell, W. K. & Lightfoot, D. O. J. comp. Neurol. 191, 315–355 (1980).
Yazulla, S., Studholme, K. M. & Wu, J.-Y. Brain Res. 411, 400–405 (1987).
von Gersdorff, H. & Matthews, G. Nature 367, 735–739 (1994).
Kaplan, J. H. & Ellis Davis, G. C. R. Proc. natn. Acad. Sci. U.S.A. 85, 6571–6575 (1988).
Konishi, M. S., Hollingworth, A. B. & Baylor, S. M. J. gen. Physiol. 97, 271–301 (1991).
Dowling, J. E. in The Retina: An Approachable Part of the Brain 42–80 (Belknap Press, Cambridge MA, 1987).
Katz, B. & Miledi, R. Proc. R. Soc. B161, 483–495 (1965).
Delaney, K. R. & Zucker, R. S. J. Physiol., Lond. 425, 473–498 (1990).
Llinas, R., Steinberg, I. Z. & Walton, K. Biophys. J. 33, 323–351 (1981).
Almers, W. Nature 367, 682–683 (1994).
Parnas, H., Dudel, J. & Parnas, I. Pflügers Arch 406, 121–130 (1986).
Thomas, P., Wong, J. G. & Almers, W. EMBO J. 12, 303–306 (1993).
Thomas, P., Wong, J. G., Lee, A. K. & Almers, W. Neuron 11, 93–104 (1993).
Heinemann, C., Chow, R. H., Neher, E. & Zucker, R. S. Biophys. J. (in the press).
Roberts, W. M., Jacobs, R. A. & Hudspeth, A. J. J. Neurosci. 10, 3664–3684 (1990).
Adler, E. M., Augustine, G. J., Duffy, S. N. & Charleton, M. P. J. Neurosci. 11, 1496–1507 (1991).
Llinas, R., Sugimori, M. & Silver R. B. Science 256, 677–679 (1992).
Augustine, G. J. & Neher, E. J. Physiol., Lond. 450, 247–271 (1992).
Simon, S. M. & Llinas, R. R. Biophys. J. 48, 485–498 (1985).
Zucker, R. S. & Fogelson, A. L. Proc. natn. Acad. Sci. U.S.A. 83, 3032–3036 (1986).
Chad, J. E. & Eckert, R. Biophys. J. 45, 993–999 (1984).
Heidelberger, R. & Matthews, G. J. Physiol., Lond. 447, 235–256 (1992).
Lindau, M. & Neher E. Pflügers Arch. 411, 137–146 (1988).
Chow R. H., von Rüden, L. & Neher, E. Nature 356, 60–63 (1992).
Herrington, J. & Bookman, R. J. PULSE CONTROL V3.0: IGOR XOPs for Patch Clamp Data Acquisition (University of Miami, Miami, 1993).
Zucker, R. S. Cell Calcium 14, 87–100 (1993).
von Gersdorff, H. & Matthews, G. Nature 370, 652–655 (1994).
Grynkiewicz, G. M., Poenie, M. & Tsien, R. Y. J. biol. Chem. 260, 3440–3450 (1985).
McCray, J., Fidler-Lim, N., Ellis-Davis, G. & Kaplan, J. H. Biochemistry 37, 8856–8861 (1992).
Heinemann, C., von Rüden, L., Chow, R. H. & Neher, E. Pflügers Arch. 424, 105–112 (1993).
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Heidelberger, R., Heinemann, C., Neher, E. et al. Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 371, 513–515 (1994). https://doi.org/10.1038/371513a0
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DOI: https://doi.org/10.1038/371513a0
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