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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

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Gilon, Patrick [UCL] Arredouani, Abdelilah [UCL] Gailly, Philippe [UCL] Gromada, Jesper Henquin, Jean-Claude [UCL]

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.

Document type Article de périodique (Journal article) – Article de recherche – Journal Article, Research Support, Non-U.S. Gov't
Access type Accès libre
Publication date 1999
Language Anglais
Journal information "Journal of Biological Chemistry" - Vol. 274, no. 29, p. 20197-20205 (1999)
Peer reviewed yes
Publisher American Society for Biochemistry and Molecular Biology, Inc. ((United States) Baltimore)
issn 0021-9258
e-issn 1083-351X
Publication status Publié
Affiliations UCL - MD/FSIO - Département de physiologie et pharmacologie
UCL - (SLuc) Service de neurologie
UCL - (SLuc) Service d'endocrinologie et de nutrition
MESH Subject Animals ; Calcium - metabolism ; Cells, Cultured ; Cytosol - metabolism ; Endoplasmic Reticulum - metabolism ; Female ; Glucose - pharmacology ; Ion Transport ; Islets of Langerhans - drug effects - metabolism - physiology ; Membrane Potentials ; Mice
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Bibliographic reference Gilon, Patrick ; Arredouani, Abdelilah ; Gailly, Philippe ; Gromada, Jesper ; Henquin, Jean-Claude. 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. In: Journal of Biological Chemistry, Vol. 274, no. 29, p. 20197-20205 (1999)
Permanent URL http://hdl.handle.net/2078.1/13018