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J. Biol. Chem., Vol. 276, Issue 13, 9971-9977, March 30, 2001

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Ca²⁺-induced Ca²⁺ Release from the Endoplasmic Reticulum Amplifies the Ca²⁺ Signal Mediated by Activation of Voltage-gated L-type Ca²⁺ Channels in Pancreatic -Cells^*

Raf Lemmens, Olof Larsson, Per-Olof Berggren, and Md. Shahidul Islam

From the Rolf Luft Center for Diabetes Research, Department of Molecular Medicine, Endocrine and Diabetes Unit, Karolinska Institutet, Karolinska Hospital, S-171 76 Stockholm, Sweden

Stimulus-secretion coupling in pancreatic -cells involves membrane depolarization and Ca²⁺ entry through voltage-gated L-type Ca²⁺ channels, which is one determinant of increases in the cytoplasmic free Ca²⁺ concentration ([Ca²⁺]_i). We investigated how the endoplasmic reticulum (ER)-associated Ca²⁺ apparatus further modifies this Ca²⁺ signal. When fura-2-loaded mouse -cells were depolarized by KCl in the presence of 3 mM glucose, [Ca²⁺]_i increased to a peak in two phases. The second phase of the [Ca²⁺]_i increase was abolished when ER Ca²⁺ stores were depleted by thapsigargin. The steady-state [Ca²⁺]_i measured at 300 s of depolarization was higher in control cells compared with cells in which the ER Ca²⁺ pools were depleted. The amount of Ca²⁺ presented to the cytoplasm during depolarization as estimated from the integral of the increment in [Ca²⁺]_i over time ([Ca²⁺]_i·dt) was ~30% higher compared with that in the Ca²⁺ pool-depleted cells. neo-thapsigargin, an inactive analog, did not affect [Ca²⁺]_i response. Using Sr²⁺ in the extracellular medium and exploiting the differences in the fluorescence properties of Ca²⁺- and Sr²⁺-bound fluo-3, we found that the incoming Sr²⁺ triggered Ca²⁺ release from the ER. Depolarization-induced [Ca²⁺]_i response was not altered by U73122, an inhibitor of phosphatidylinositol-specific phospholipase C, suggesting that stimulation of the enzyme by Ca²⁺ is not essential for amplification of Ca²⁺ signaling. [Ca²⁺]_i response was enhanced when cells were depolarized in the presence of 3 mM glucose, forskolin, and caffeine, suggesting involvement of ryanodine receptors in the amplification process. Pretreatment with ryanodine (100 µM) diminished the second phase of the depolarization-induced increase in [Ca²⁺]_i. We conclude that Ca²⁺ entry through L-type voltage-gated Ca²⁺ channels triggers Ca²⁺ release from the ER and that such a process amplifies depolarization-induced Ca²⁺ signaling in -cells.

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