65
Original Paper
Cell Physiol Biochem 2007;20:65-74
Accepted: February 08, 2007
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The K
ATP
Channel is Critical for Calcium
Sequestration into Non-ER Compartments in
Mouse Pancreatic Beta Cells
Martina Düfer
1
, Dirk Haspel
1
, Peter Krippeit-Drews
1
, Mandy Kelm
1
,
Felicia Ranta
4
, Roland Nitschke
5
, Susanne Ullrich
4
, Lydia Aguilar-
Bryan
2
, Joseph Bryan
3
and Gisela Drews
1
1
Institute of Pharmacy, Department of Pharmacology, University of Tübingen,
2
Departments of Medicine
and
3
Molecular and Cellular Biology, Baylor College of Medicine, Houston, Texas,
4
Institute of Physiology,
University of Tübingen,
5
Institute of Biology I, Life Imaging Center, University of Freiburg
Prof. Dr. Gisela Drews
Institute of Pharmacy, Department of Pharmacology, University of Tübingen
Auf der Morgenstelle 8, D-72076 Tübingen (Germany)
Tel. +49-7071-2977559, Fax +49-7071-295382
E-Mail gisela.drews@uni-tuebingen.de
Key Words
Cyclopiazonic acid Cytosolic calcium concentration
FCCP K
ATP
channels Mitochondrial Ca
2+
storage
Ratiometric pericam Sulfonylureas Sur1KO mice
Abstract
K
ATP
channel activity influences beta cell Ca
2+
homeostasis by regulating Ca
2+
influx through L-type
Ca
2+
channels. The present paper demonstrates that
loss of K
ATP
channel activity due to pharmacologic or
genetic ablation affects Ca
2+
storage in intracellular
organelles. ATP depletion, by the mitochondrial
inhibitor FCCP, led to Ca
2+
release from the
endoplasmic reticulum (ER) of wildtype beta cells.
Blockade of ER Ca
2+
ATPases by cyclopiazonic acid
abolished the FCCP-induced Ca
2+
transient. In beta
cells treated with K
ATP
channel inhibitors FCCP elicited
a significantly larger Ca
2+
transient. Cyclopiazonic acid
did not abolish this Ca
2+
transient suggesting that non-
ER compartments are recruited as additional Ca
2+
stores in beta cells lacking K
ATP
channel activity.
Genetic ablation of K
ATP
channels in SUR1KO mice
produced identical results. In INS-1 cells transfected
with a mitochondrial-targeted Ca
2+
-sensitive
fluorescence dye (ratiometric pericam) the increase
in mitochondrial Ca
2+
evoked by tolbutamide was 5-
fold larger compared to 15 mM glucose. These data
show that genetic or pharmacologic ablation of K
ATP
channel activity conveys Ca
2+
release from a non-ER
store. Based on the sensitivity to FCCP and the
property of tolbutamide to increase mitochondrial Ca
2+
it is suggested that mitochondria are the recruited
store. The change in Ca
2+
sequestration in beta cells
treated with insulinotropic antidiabetics may have
implications for beta cell survival and the therapeutic
use of these drugs.
Introduction
An increase in the cytosolic Ca
2+
concentration
([Ca
2+
]
c
) is essential for stimulus-secretion coupling in
pancreatic beta cells because Ca
2+
constitutes the trigger
signal for the exocytosis of insulin. Glucose, the most
important natural beta cell fuel, induces closure of K
ATP
channels via changes in the ATP/ADP ratio which lead