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J. Biol. Chem., Vol. 278, Issue 12, 10807-10815, March 21, 2003
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From the In endothelial cells, local
Ca2+ release from superficial endoplasmic reticulum
(ER) activates BKCa channels. The resulting hyperpolarization promotes capacitative Ca2+ entry (CCE),
which, unlike BKCa channels, is inhibited by high Ca2+. To understand how the coordinated activation of
plasma membrane ion channels with opposite Ca2+ sensitivity
is orchestrated, the individual contribution of mitochondria and ER in
regulation of subplasmalemmal Ca2+ concentration
([Ca2+]pm) was investigated. For organelle
visualization, cells were transfected with DsRed and yellow cameleon
targeted to mitochondria and ER. The patch pipette was placed far from
any organelle (L1), close to ER (L3), or mitochondria (L2) and activity
of BKCa channels was used to estimate local
[Ca2+]pm. Under standard patch conditions
(130 mM K+ in the bath), histamine increased
[Ca2+]pm at L1 and L3 to ~1.6
µM, whereas close to mitochondria
[Ca2+]pm remained unchanged. If mitochondria
moved apart from the pipette or in the presence of carbonyl
cyanide-4-trifluoromethoxyphenylhyrazone, [Ca2+]pm at L2 increased in response to
histamine. Under standard patch conditions Ca2+ entry was
negligible due to cell depolarization. Using a physiological patch
approach (5.6 mM K+ in the bath), changes in
[Ca2+]pm to histamine could be monitored
without cell depolarization and, thus, in conditions where
Ca2+ entry occurred. Here, histamine induced an initial
transient Ca2+ elevation to
Mitochondria Efficiently Buffer Subplasmalemmal Ca2+
Elevation during Agonist Stimulation*
,, and¶
Department of Medical Biochemistry & Medical
Molecular Biology, University of Graz, Graz 8010, Austria and the
§ Department of Physiology, University of Geneva, 1211 Geneva 4, Switzerland
3.5 µM followed
by a long lasting plateau at ~1.2 µM in L1 and L3,
whereas mitochondria kept neighboring
[Ca2+]pm low during stimulation. Thus,
superficial mitochondria and ER generate local domains of low and high
Ca2+ allowing simultaneous activation of BKCa
and CCE, despite their opposite Ca2+ sensitivity.
*
This work was supported by the Austrian Funds (Grants SFB
714 and P-14586-PHA to W. F. G.), the Austrian National Bank (Grants P7542 to W. F. G. and P7902 to R. M., respectively), and the Swiss National Funds (Grant 31-56902.99). The Department of Medical Biochemistry & Medical Molecular Biology is a member of the Institutes of Basic Medical Sciences at the University of Graz and was supported by the infrastructure program (Grant UGP4) of the Austrian ministry of
education, science and culture.The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement" in accordance with 18 U.S.C. Section
1734 solely to indicate this fact.
Copyright © 2003 by The American Society for Biochemistry and Molecular Biology, Inc.
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