Coordinated Behavior of Mitochondria in Both Space and Time: A Reactive Oxygen Species-Activated Wave of Mitochondrial Depolarization

Reactive oxygen species (ROS) can trigger a transient burst of mitochondrial ROS production via ROS activation of the mitochondrial permeability transition pore (MPTP), a phenomenon termed ROS-induced ROS release (RIRR). The goal of this study was to investigate if the generation of ROS in a discret...

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Bibliographic Details
Published in:Biophysical journal 2004-09, Vol.87 (3), p.2022-2034
Main Authors: Brady, Nathan R., Elmore, Steven P., van Beek, Johannes J.H.G.M., Krab, Klaas, Courtoy, Pierre J., Hue, Louis, Westerhoff, Hans V.
Format: Article
Language:English
Subjects:
1-Methyl-4-phenyl-1,2,3,6-tetrahydropyridine - pharmacology
Animals
Biophysics
Calcium - metabolism
Cell Biophysics
Cells
Image Processing, Computer-Assisted
Kinetics
Light
Membrane Potentials
Membranes
Microscopy, Confocal
Mitochondria - metabolism
Mitochondrial DNA
Models, Biological
Myocytes, Cardiac - metabolism
Oxygen
Permeability
Rabbits
Reactive Oxygen Species
Rotenone - pharmacology
Time Factors
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Summary:Reactive oxygen species (ROS) can trigger a transient burst of mitochondrial ROS production via ROS activation of the mitochondrial permeability transition pore (MPTP), a phenomenon termed ROS-induced ROS release (RIRR). The goal of this study was to investigate if the generation of ROS in a discrete region of a cardiomyocyte could serve to propagate RIRR-mediated mitochondrial depolarizations throughout a cell. Our experiments revealed that localized RIRR activated either RIRR-mediated fluctuations in mitochondrial membrane potential (time period: 3–10 min) or a traveling wave of depolarization of the cell’s mitochondria (velocity: ∼5 μm/min). Both phenomena appeared to be mediated by the mitochondrial permeability transition pore and eventually encompassed the majority of the mitochondrial population of both isolated rat and rabbit cardiomyocytes. Furthermore, depolarization was often reversible; the waves of depolarization were then followed by a rapid (∼40 μm/min) repolarization wave of the mitochondria. We show that the RIRR can function to communicate the mitochondrial permeability transition from one mitochondrion to another in the isolated adult cardiomyocyte.
ISSN:0006-3495
1542-0086
DOI:10.1529/biophysj.103.035097