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Biophys J, May 2001, p. 2133-2139, Vol. 80, No. 5

Mouse Mast Cell Secretory Granules Can Function as Intracellular Ionic Oscillators

Ivan Quesada,* Wei-Chun Chin,dagger Jordan Steed,dagger Patricia Campos-Bedolla,dagger and Pedro Verdugodagger Dagger

 *Instituto de Bioingenieria, Universidad Miguel Hernández, Alicante 03550, Spain; and  dagger Department of Bioengineering and  Dagger Department of Internal Medicine, University of Washington, Seattle, Washington 98195 USA

Fluorescent Ca2+ probes and digital photo-sectioning techniques were used to directly study the dynamics of Ca2+ in isolated mast cell granules of normal (CB/J) and beige (Bgj/Bgj) mice. The resting intraluminal free Ca2+ concentration ([Ca2+]L) is 25 ± 4.2 µM (mean ± SD, n = 68). Exposure to 3 µM inositol 1,4,5-trisphosphate (InsP3) induced periodic oscillations of luminal Ca2+ ([Ca2+]L) of ~10 µM amplitude and a period around 8-10 s. The [Ca2+]L oscillations were accompanied by a corresponding oscillatory release of [Ca2+]L to the extraluminal space. Control experiments using ruthenium red (2 µM) and thapsigargin (100 nM) ruled out artifacts derived from the eventual presence of mitochondria or endoplasmic reticulum in the isolated granule preparation. Oscillations of [Ca2+]L and Ca2+ release result from a Ca2+/K+ exchange process whereby bound Ca is displaced from the heparin polyanionic matrix by inflow of K+ into the granular lumen via an apamin-sensitive Ca2+-sensitive K+ channel (ASKCa), whereas Ca2+ release takes place via an InsP3-receptor-Ca2+ (InsP3-R) channel. These results are consistent with previous observations of [Ca2+]L oscillations and release in/from the endoplasmic reticulum and mucin granules, and suggest that a highly conserved common mechanism might be responsible for [Ca2+]L oscillations and quantal periodic Ca2+ release in/from intracellular Ca2+ storage compartments.

Biophys J, May 2001, p. 2133-2139, Vol. 80, No. 5
© 2001 by the Biophysical Society   0006-3495/01/05/2133/07  $2.00


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