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J. Biol. Chem., Vol. 278, Issue 13, 11057-11064, March 28, 2003
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From the Henry Wellcome Laboratories of Integrated Cell Signaling
and Department of Biochemistry, School of Medical Sciences, University
Walk, University of Bristol, Bristol BS8 1TD and the
We have demonstrated recently (Mitchell, K. J., Pinton, P., Varadi, A., Tacchetti, C., Ainscow, E. K., Pozzan, T., Rizzuto, R., and Rutter, G. A. (2001)
J. Cell Biol. 155, 41-51) that ryanodine receptors
(RyR) are present on insulin-containing secretory vesicles. Here we
show that pancreatic islets and derived
Ryanodine Receptor Type I and Nicotinic Acid Adenine Dinucleotide
Phosphate Receptors Mediate Ca2+ Release from
Insulin-containing Vesicles in Living Pancreatic
-Cells (MIN6)*
, and Department of Cardiology, Wales Heart Research Institute,
University of Wales College of Medicine, Cardiff CF14 4XN,
United Kingdom
-cell lines express type I
and II, but not type III, RyRs. Purified by subcellular fractionation
and membrane immuno-isolation, dense core secretory vesicles were found
to possess a similar level of type I RyR immunoreactivity as
Golgi/endoplasmic reticulum (ER) membranes but substantially less RyR
II than the latter. Monitored in cells expressing appropriately targeted aequorins, dantrolene, an inhibitor of RyR I channels, elevated free Ca2+ concentrations in the secretory vesicle
compartment from 40.1 ± 6.7 to 90.4 ± 14.8 µM
(n = 4, p < 0.01), while having no
effect on ER Ca2+ concentrations. Furthermore, nicotinic
acid adenine dinucleotide phosphate (NAADP), a novel
Ca2+-mobilizing agent, decreased dense core secretory
vesicle but not ER free Ca2+ concentrations in
permeabilized MIN6 -cells, and flash photolysis of caged NAADP
released Ca2+ from a thapsigargin-insensitive
Ca2+ store in single MIN6 cells. Because dantrolene
strongly inhibited glucose-stimulated insulin secretion (from 3.07 ± 0.51-fold stimulation to no significant glucose effect;
n = 3, p < 0.01), we conclude that
RyR I-mediated Ca2+-induced Ca2+ release from
secretory vesicles, possibly potentiated by NAADP, is essential for the
activation of insulin secretion.
*
This work was supported by a Biotechnology and Biological
Sciences Research Council Studentship (to K. J. M.), Wellcome Trust Program Grant 067081, the Human Frontiers Science Program, the Medical
Research Council (UK), and Diabetes UK.The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement" in accordance with 18 U.S.C. Section
1734 solely to indicate this fact.
Copyright © 2003 by The American Society for Biochemistry and Molecular Biology, Inc.
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