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A Mitochondrial Oscillator Dependent on Reactive Oxygen Species
Open accessAbstract
We describe a unique mitochondrial oscillator that depends on oxidative phosphorylation, reactive oxygen species (ROS), and mitochondrial inner membrane ion channels. Cell-wide synchronized oscillations in mitochondrial membrane potential (Delta Psi(m)), NADH, and ROS production have been recently described in isolated cardiomyocytes, and we have hypothesized that the balance between superoxide anion efflux through inner membrane anion channels and the intracellular ROS scavenging capacity play a key role in the oscillatory mechanism. Here, we formally test the hypothesis using a computational model of mitochondrial energetics and Ca(2+) handling including mitochondrial ROS production, cytoplasmic ROS scavenging, and ROS activation of inner membrane anion flux. The mathematical model reproduces the period and phase of the observed oscillations in Delta Psi(m), NADH, and ROS. Moreover, we experimentally verify model predictions that the period of the oscillator can be modulated by altering the concentration of ROS scavengers or the rate of oxidative phosphorylation, and that the redox state of the glutathione pool oscillates. In addition to its role in cellular dysfunction during metabolic stress, the period of the oscillator can be shown to span a wide range, from milliseconds to hours, suggesting that it may also be a mechanism for physiological timekeeping and/or redox signaling.
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“In endothelial cells, blocking the effect of NO• to compete for O2 at complex IV with an NOS inhibitor enhanced the rate of O2 consumption (respiration) at very low O2 concentrations (89).”
From Mitochondrial reactive oxygen species production in excitable cells: Modulators of mitochondrial and cell function (2009) · cites this paper as [89]
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Mitochondrial ROS-induced ROS release: An update and review
Zorov, D. B., Juhaszova, M., & Sollott, S. J. (2006) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/j.bbabio.2006.04.029 · Cited by 1,099
Mitochondria in homeostasis of reactive oxygen species in cell, tissues, and organism
Ježek, P., & Plecitá‐Hlavatá, L. (2005) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2005.05.013 · Cited by 753
Mitochondrial Signaling in Mammalian Cells Activated by Red and Near‐IR Radiation
Karu, T. I. (2008) · Photochemistry and Photobiology · doi:10.1111/j.1751-1097.2008.00394.x · Cited by 575
Monogenic Mitochondrial Disorders
Koopman, W. J. H., Willems, P. H. G. M., & Smeitink, J. A. M. (2012) · New England Journal of Medicine · doi:10.1056/nejmra1012478 · Cited by 527
Stowe, D. F., & Camara, A. K. S. (2009) · Antioxidants & Redox Signaling · doi:10.1089/ars.2008.2331 · Cited by 471
Metadata
- Authors
- Cortassa, S., Aon, M. A., Winslow, R. L., & O’Rourke, B.
- Affiliations
- Johns Hopkins University (US)
- Venue
- Biophysical Journal
- Publisher
- Elsevier BV
- Published
- 2004-09
- Volume
- 87
- Issue
- 3
- Pages
- 2060-2073
- ISSN
- 0006-3495 (ISSN-L)
- PMC
- PMC1304608
- OpenAlex
- W2058028795
- Cited by
- 235
- References
- 61
- Citations by year
- 2026: 9 · 2025: 7 · 2024: 10 · 2023: 11 · 2022: 13 · 2021: 5 · 2020: 5 · 2019: 4 · 2018: 12 · 2017: 11 · 2016: 12 · 2015: 9 · 2014: 12 · 2013: 17 · 2012: 16
- FWCI
- 3.56
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Biophysical Journal (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Heart, Lung, and Blood Institute (P50-HL52307, R01-HL-60133-01, R01HL105239, R01HL054598, R01HL060133, P50HL052307, R01HL54598)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Redox biology and oxidative stress
- Physical Sciences › Physics and Astronomy › Statistical and Nonlinear Physics › Nonlinear Dynamics and Pattern Formation
- Keywords
- reactive oxygen species, oxidative phosphorylation, cardiomyocytes, mitochondrial ROS production, glutathione redox state, calcium handling, redox signaling
- MeSH terms
- Animals, Calcium, Cytosol, Glutathione, Glutathione Peroxidase, Glutathione Reductase, Guinea Pigs, Hydrogen Peroxide, Image Processing, Computer-Assisted, Kinetics, Lasers, Membrane Potentials, Microscopy, Fluorescence, Mitochondria, Models, Biological, Models, Theoretical, Oligomycins, Oscillometry, Oxygen, Superoxide Dismutase, Reperfusion Injury, Reactive Oxygen Species, Photons, Myocytes, Cardiac
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