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J Biol Chem, Vol. 274, Issue 29, 20197-20205, July 16, 1999

Uptake and Release of Ca2+ by the Endoplasmic Reticulum Contribute to the Oscillations of the Cytosolic Ca2+ Concentration Triggered by Ca2+ Influx in the Electrically Excitable Pancreatic B-cell

Patrick GilonDagger , Abdelilah ArredouaniDagger , Philippe Gailly**, Jesper GromadaDagger Dagger , and Jean-Claude HenquinDagger

From the Dagger  Unité d'Endocrinologie et Métabolisme, and the ** Unité de Physiologie Générale des Muscles, University of Louvain Faculty of Medicine, Av. Hippocrate 55, 1200 Brussels, Belgium and the Dagger Dagger  Department of Islet Cell Physiology, Islet Discovery Research, Novo Nordisk A/S, Novo Alle, 2880 Bagsvaerd, Denmark

The role of intracellular Ca2+ pools in oscillations of the cytosolic Ca2+ concentration ([Ca2+]c) triggered by Ca2+ influx was investigated in mouse pancreatic B-cells. [Ca2+]c oscillations occurring spontaneously during glucose stimulation or repetitively induced by pulses of high K+ (in the presence of diazoxide) were characterized by a descending phase in two components. A rapid decrease in [Ca2+]c coincided with closure of voltage-dependent Ca2+ channels and was followed by a slower phase independent of Ca2+ influx. Blocking the SERCA pump with thapsigargin or cyclopiazonic acid accelerated the rising phase of [Ca2+]c oscillations and increased their amplitude, which suggests that the endoplasmic reticulum (ER) rapidly takes up Ca2+. It also suppressed the slow [Ca2+]c recovery phase, which indicates that this phase corresponds to the slow release of Ca2+ that was taken up by the ER during the upstroke of the [Ca2+]c transient. Glucose promoted the buffering capacity of the ER and amplified the slow [Ca2+]c recovery phase. The slow phase induced by high K+ pulses was not affected by modulators of Ca2+- or inositol 1,4,5-trisphosphate-induced Ca2+ release, did not involve a depolarization-induced Ca2+ release, and was also observed at the end of a rapid rise in [Ca2+]c triggered from caged Ca2+. It is attributed to passive leakage of Ca2+ from the ER. We suggest that the ER displays oscillations of the Ca2+ concentration ([Ca2+]ER) concomitant and parallel to [Ca2+]c. The observation that thapsigargin depolarizes the membrane of B-cells supports the proposal that the degree of Ca2+ filling of the ER modulates the membrane potential. Therefore, [Ca2+]ER oscillations occurring during glucose stimulation are likely to influence the bursting behavior of B-cells and eventually [Ca2+]c oscillations.

Copyright © 1999 by The American Society for Biochemistry and Molecular Biology, Inc.


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