The mitochondrial membrane potential and Ca2+ oscillations in smooth muscle

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Abstract

Ca2+ uptake by mitochondria might both modulate the cytosolic Ca2+ concentration ([Ca2+]c) and depolarize the mitochondrial membrane potential (m) to limit ATP production. To investigate how physiological Ca2+ signaling might affect energy production, m was examined during Ca2+ oscillations in smooth muscle cells. In single, voltage-clamped smooth muscle cells, inhibition of mitochondrial Ca2+ accumulation inhibited inositol (1,4,5)-trisphosphate [Ins(1,4,5)P3]-evoked Ca2+ release and prolonged the time required for restoration of [Ca2+]c following activation of plasmalemmal Ca2+ currents (ICa). Ca2+ could be released from mitochondria immediately (within 15 seconds) after a [Ca2+]c rise evoked by Ins(1,4,5)P3 or ICa. Despite this evidence of mitochondrial Ca2+ accumulation, no change in m was observed during single or repetitive [Ca2+]c oscillations evoked by these conditions. Occasionally, spontaneous, repetitive, persistent Ca2+ oscillations were observed. In these cases, mitochondria displayed stochastic m depolarizations, which were independent both of events in neighboring mitochondria and of the timing of the [Ca2+]c oscillations themselves. Such m depolarizations could be mimicked by increased exposure to either fluorescence excitation light or the m-sensitive dye tetramethylrhodamine ethyl ester (TMRE) and were inhibited by antioxidants (ascorbic acid, catalase, Trolox and TEMPO) or the mitochondrial permeability transition pore (mPTP)-inhibitor cyclosporin A (CsA). Individual mitochondria within smooth muscle cells might depolarize during repetitive Ca2+ oscillations or during oxidative stress but not during the course of single [Ca2+]c transients evoked by Ca2+ influx or store release.
LanguageEnglish
Pages75-85
Number of pages10
JournalJournal of Cell Science
Volume121
Issue number1
DOIs
Publication statusPublished - 1 Jan 2008

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Mitochondrial Membrane Potential
Smooth Muscle
Mitochondria
Smooth Muscle Myocytes
Inositol 1,4,5-Trisphosphate
Catalase
Cyclosporine
Ascorbic Acid
Esters
Oxidative Stress
Coloring Agents
Antioxidants
Adenosine Triphosphate
Fluorescence
Light

Keywords

  • smooth muscle
  • calcium
  • mitochondria
  • membrane potential

Cite this

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title = "The mitochondrial membrane potential and Ca2+ oscillations in smooth muscle",
abstract = "Ca2+ uptake by mitochondria might both modulate the cytosolic Ca2+ concentration ([Ca2+]c) and depolarize the mitochondrial membrane potential (m) to limit ATP production. To investigate how physiological Ca2+ signaling might affect energy production, m was examined during Ca2+ oscillations in smooth muscle cells. In single, voltage-clamped smooth muscle cells, inhibition of mitochondrial Ca2+ accumulation inhibited inositol (1,4,5)-trisphosphate [Ins(1,4,5)P3]-evoked Ca2+ release and prolonged the time required for restoration of [Ca2+]c following activation of plasmalemmal Ca2+ currents (ICa). Ca2+ could be released from mitochondria immediately (within 15 seconds) after a [Ca2+]c rise evoked by Ins(1,4,5)P3 or ICa. Despite this evidence of mitochondrial Ca2+ accumulation, no change in m was observed during single or repetitive [Ca2+]c oscillations evoked by these conditions. Occasionally, spontaneous, repetitive, persistent Ca2+ oscillations were observed. In these cases, mitochondria displayed stochastic m depolarizations, which were independent both of events in neighboring mitochondria and of the timing of the [Ca2+]c oscillations themselves. Such m depolarizations could be mimicked by increased exposure to either fluorescence excitation light or the m-sensitive dye tetramethylrhodamine ethyl ester (TMRE) and were inhibited by antioxidants (ascorbic acid, catalase, Trolox and TEMPO) or the mitochondrial permeability transition pore (mPTP)-inhibitor cyclosporin A (CsA). Individual mitochondria within smooth muscle cells might depolarize during repetitive Ca2+ oscillations or during oxidative stress but not during the course of single [Ca2+]c transients evoked by Ca2+ influx or store release.",
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The mitochondrial membrane potential and Ca2+ oscillations in smooth muscle. / Chalmers, S.; McCarron, J.G.

In: Journal of Cell Science, Vol. 121, No. 1, 01.01.2008, p. 75-85.

Research output: Contribution to journalArticle

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AU - McCarron, J.G.

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AB - Ca2+ uptake by mitochondria might both modulate the cytosolic Ca2+ concentration ([Ca2+]c) and depolarize the mitochondrial membrane potential (m) to limit ATP production. To investigate how physiological Ca2+ signaling might affect energy production, m was examined during Ca2+ oscillations in smooth muscle cells. In single, voltage-clamped smooth muscle cells, inhibition of mitochondrial Ca2+ accumulation inhibited inositol (1,4,5)-trisphosphate [Ins(1,4,5)P3]-evoked Ca2+ release and prolonged the time required for restoration of [Ca2+]c following activation of plasmalemmal Ca2+ currents (ICa). Ca2+ could be released from mitochondria immediately (within 15 seconds) after a [Ca2+]c rise evoked by Ins(1,4,5)P3 or ICa. Despite this evidence of mitochondrial Ca2+ accumulation, no change in m was observed during single or repetitive [Ca2+]c oscillations evoked by these conditions. Occasionally, spontaneous, repetitive, persistent Ca2+ oscillations were observed. In these cases, mitochondria displayed stochastic m depolarizations, which were independent both of events in neighboring mitochondria and of the timing of the [Ca2+]c oscillations themselves. Such m depolarizations could be mimicked by increased exposure to either fluorescence excitation light or the m-sensitive dye tetramethylrhodamine ethyl ester (TMRE) and were inhibited by antioxidants (ascorbic acid, catalase, Trolox and TEMPO) or the mitochondrial permeability transition pore (mPTP)-inhibitor cyclosporin A (CsA). Individual mitochondria within smooth muscle cells might depolarize during repetitive Ca2+ oscillations or during oxidative stress but not during the course of single [Ca2+]c transients evoked by Ca2+ influx or store release.

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