Coordinated behavior of mitochondria in both space and time: A reactive oxygen species-activated wave of mitochondrial depolarization

Nathan R. Brady, Steven P. Elmore, Johannes J.H.G.M. Van Beek, Klaas Krab, Pierre J. Courtoy, Louis Hue, Hans V. Westerhoff

Research output: Contribution to journalArticlepeer-review

98 Scopus citations

Abstract

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.

Original languageEnglish (US)
Pages (from-to)2022-2034
Number of pages13
JournalBiophysical journal
Volume87
Issue number3
DOIs
StatePublished - Sep 2004
Externally publishedYes

ASJC Scopus subject areas

  • Biophysics

Fingerprint

Dive into the research topics of 'Coordinated behavior of mitochondria in both space and time: A reactive oxygen species-activated wave of mitochondrial depolarization'. Together they form a unique fingerprint.

Cite this