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Subplasmalemmal endoplasmic reticulum controls K_Ca channel activity upon stimulation with a moderate histamine concentration in a human umbilical vein endothelial cell line

Maud Frieden *, Roland Malli *, Mariana Samardzija, Nicolas Demaurex † and Wolfgang F. Graier

This study was designed to elucidate the role of the subplasmalemmal endoplasmic reticulum (sER) in autacoid-induced stimulation of Ca²⁺-dependent K⁺ channels in the umbilical vein endothelial cell-derived cell line EA.hy926. Cells were transfected with the Ca²⁺ probe cameleon targeted to the ER for visualization of the ER network. A patch pipette was then placed close to or far (> 5 µm away) from the sER, single channel recordings (patch clamp technique) were monitored simultaneously with measurements of either ER Ca²⁺ concentration (using the Ca²⁺ probe Cam4-ER) or cytosolic free Ca²⁺ concentration ([Ca²⁺]_i; using fura-2) using a deconvolution imaging device. A voltage-dependent, large conductance Ca²⁺-dependent K⁺ channel (BK_Ca; single channel conductance (), 250 pS) was found. At membrane potentials of +40 and -40 mV, the EC₅₀ for Ca²⁺ was 2.7 and 49.7 µM, respectively. In the vicinity of the sER, the BK_Ca channel activity induced by 10 µM histamine was 32 times higher (open probability (P_o) = 0.083 ± 0.026) than in areas away from the sER (P_o = 0.0026 ± 0.002). However, at supramaximal histamine stimulation (100 µM), BK_Ca channel activation was similar in patches in the vicinity of or away from the sER (P_o = 0.18 ± 0.09 and 0.25 ± 0.07, respectively). In contrast to BK_Ca channel activity, ER Ca²⁺ depletion (Cam4-ER) and elevation of [Ca²⁺]_i in response to 10 and 100 µM histamine were not influenced by the pipette position. We conclude that in endothelial cells, the activation of BK_Ca channels in response to moderate histamine concentration essentially depends on the proximity of the sER domains to the mouth of this K⁺ channel. These findings further support our concept of the subplasmalemmal Ca²⁺ control unit (SCCU) and add the local activation of Ca²⁺-activated K⁺-channels to the function of the SCCU.

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