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High calcium concentrations shift the mode of exocytosis to the kiss-and-run mechanism

Nature Cell Biology volume 1, pages 40–44 (1999)Cite this article

Abstract

Exocytosis, the fusion of secretory vesicles with the plasma membrane to allow release of the contents of the vesicles into the extracellular environment, and endocytosis, the internalization of these vesicles to allow another round of secretion, are coupled. It is, however, uncertain whether exocytosis and endocytosis are tightly coupled, such that secretory vesicles fuse only transiently with the plasma membrane before being internalized (the ‘kiss-and-run’ mechanism), or whether endocytosis occurs by an independent process following complete incorporation of the secretory vesicle into the plasma membrane. Here we investigate the fate of single secretory vesicles after fusion with the plasma membrane by measuring capacitance changes and transmitter release in rat chromaffin cells using the cell-attached patch-amperometry technique. We show that raised concentrations of extracellular calcium ions shift the preferred mode of exocytosis to the kiss-and-run mechanism in a calcium-concentration-dependent manner. We propose that, during secretion of neurotransmitters at synapses, the mode of exocytosis is modulated by calcium to attain optimal conditions for coupled exocytosis and endocytosis according to synaptic activity.

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Figure 1: Catecholamine release during fast kiss-and-run and permanent fusion events in rat chromaffin cells, recorded by patch amperometry.
Figure 2: Comparison of fast kiss-and-run and permanent fusion events.
Figure 3: Kiss-and-run kinetics in fast and slow fusion events.
Figure 4: Ca2+ dependence of the closure of the exocytotic fusion pore.
Figure 5: Model for coupled exocytosis and endocytosis, incorporating our experimental results.

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Acknowledgements

We thank J. L. Romero for technical assistance and D. Mir for comments on the manuscript. This work was supported by grants from the Spanish Ministerio de Educación y Cultura (DGES; to G.A.T.), from the Junta de Andalucia (to L.T.), and by the Deutsche Forschungsgemeinschaft (to M.L.). E.A. was supported by a fellowship from DGES.

Correspondence and requests for materials should be addressed to G.A.T.

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Authors and Affiliations

  1. Departamento de Fisiología Médica y Biofísica, Facultad de Medicina, Universidad de Sevilla, Sevilla, 41009 , Spain

    Eva Alés, Lucía Tabares, Juan M. Poyato, Vicente Valero & Guillermo Alvarez de Toledo

  2. School of Applied Engineering and Physics, Cornell University, Ithaca, 14853-2501, New York , USA

    Manfred Lindau

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  1. Eva Alés
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Correspondence to Guillermo Alvarez de Toledo.

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Alés, E., Tabares, L., Poyato, J. et al. High calcium concentrations shift the mode of exocytosis to the kiss-and-run mechanism. Nat Cell Biol 1, 40–44 (1999). https://doi.org/10.1038/9012

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