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Glucose stimulates Ca2+ influx and insulin secretion in 2-week-old beta-cells lacking ATP-sensitive K+ channels.

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Szollosi, Andras [UCL] Nenquin, Myriam [UCL] Aguilar-Bryan, Lydia Bryan, Joseph Henquin, Jean-Claude [UCL]

In adult beta-cells glucose-induced insulin secretion involves two mechanisms (a) a K(ATP) channel-dependent Ca(2+) influx and rise of cytosolic [Ca(2+)](c) and (b) a K(ATP) channel-independent amplification of secretion without further increase of [Ca(2+)](c). Mice lacking the high affinity sulfonylurea receptor (Sur1KO), and thus K(ATP) channels, have been developed as a model of congenital hyperinsulinism. Here, we compared [Ca(2+)](c) and insulin secretion in overnight cultured islets from 2-week-old normal and Sur1KO mice. Control islets proved functionally mature: the magnitude and biphasic kinetics of [Ca(2+)](c) and insulin secretion changes induced by glucose, and operation of the amplifying pathway, were similar to adult islets. Sur1KO islets perifused with 1 mm glucose showed elevation of both basal [Ca(2+)](c) and insulin secretion. Stimulation with 15 mm glucose produced a transient drop of [Ca(2+)](c) followed by an overshoot and a sustained elevation, accompanied by a monophasic, 6-fold increase in insulin secretion. Glucose also increased insulin secretion when [Ca(2+)](c) was clamped by KCl. When Sur1KO islets were cultured in 5 instead of 10 mm glucose, [Ca(2+)](c) and insulin secretion were unexpectedly low in 1 mm glucose and increased following a biphasic time course upon stimulation by 15 mm glucose. This K(ATP) channel-independent first phase [Ca(2+)](c) rise was attributed to a Na(+)-, Cl(-)-, and Na(+)-pump-independent depolarization of beta-cells, leading to Ca(2+) influx through voltage-dependent calcium channels. Glucose indeed depolarized Sur1KO islets under these conditions. It is suggested that unidentified potassium channels are sensitive to glucose and subserve the acute and long-term metabolic control of [Ca(2+)](c) in beta-cells without functional K(ATP) channels.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès libre
Publication date 2007
Journal information "Journal of Biological Chemistry" - Vol. 282, no. 3, p. 1747-1756 (2007)
Peer reviewed yes
Publisher American Society for Biochemistry and Molecular Biology, Inc. ((United States) Baltimore, MD)
issn 0021-9258
e-issn 1083-351X
Publication status Publié
Affiliation UCL - MD/FSIO - Département de physiologie et pharmacologie
MESH Subject ATP-Binding Cassette Transporters - genetics ; Adenosine Triphosphate - chemistry ; Animals ; Calcium - metabolism ; Cyclic AMP - metabolism ; Glucose - metabolism ; Humans ; Insulin - metabolism - secretion ; Insulin-Secreting Cells - metabolism ; Islets of Langerhans - metabolism ; Kinetics ; Mice ; Mice, Inbred C57BL ; Mice, Knockout ; Potassium Channels - chemistry - genetics ; Potassium Channels, Inwardly Rectifying - genetics ; Receptors, Drug - genetics
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Bibliographic reference Szollosi, Andras ; Nenquin, Myriam ; Aguilar-Bryan, Lydia ; Bryan, Joseph ; Henquin, Jean-Claude. Glucose stimulates Ca2+ influx and insulin secretion in 2-week-old beta-cells lacking ATP-sensitive K+ channels.. In: Journal of Biological Chemistry, Vol. 282, no. 3, p. 1747-1756 (2007)
Permanent URL http://hdl.handle.net/2078.1/12770