Oxygen sensing by mitochondria at complex III: the paradox of increased reactive oxygen species during hypoxia
Abstract
All eukaryotic cells utilize oxidative phosphorylation to maintain their high‐energy phosphate stores. Mitochondrial oxygen consumption is required for ATP generation, and cell survival is threatened when cells are deprived of O 2. Consequently, all cells have the ability to sense O 2, and to activate adaptive processes that will enhance the likelihood of survival in anticipation that oxygen availability might become limiting. Mitochondria have long been considered a likely site of oxygen sensing, and we propose that the electron transport chain acts as an O 2 sensor by releasing reactive oxygen species (ROS) in response to hypoxia. The ROS released during hypoxia act as signalling agents that trigger diverse functional responses, including activation of gene expression through the stabilization of the transcription factor hypoxia‐inducible factor (HIF)‐α. The primary site of ROS production during hypoxia appears to be complex III. The paradoxical increase in ROS production during hypoxia may be explained by an effect of O 2 within the mitochondrial inner membrane on: (a) the lifetime of the ubisemiquinone radical in complex III; (b) the relative release of mitochondrial ROS towards the matrix compartment versus the intermembrane space; or (c) the ability of O 2 to access the ubisemiquinone radical in complex III. In summary, the process of oxygen sensing is of fundamental importance in biology. An ability to control the oxygen sensing mechanism in cells, potentially using small molecules that do not disrupt oxygen consumption, would open valuable therapeutic avenues that could have a profound impact on a diverse range of diseases.
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Mitochondrial DNA is a sensitive target of excess ROS, subject to an oxidation rate 10- to 20-fold higher than that of nuclear DNA.
“A sensitive target of excess ROS is mitochondrial DNA (Fig. 22), which is subject to an oxidation rate 10- to 20-fold higher than that of nuclear DNA (140, 142, 262).”
From Mitochondrial reactive oxygen species production in excitable cells: Modulators of mitochondrial and cell function (2009) · cites this paper as [142]
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- Authors
- Guzy, R. D., & Schumacker, P. T.
- Affiliations
- Northwestern University (US)
- Venue
- Experimental Physiology
- Publisher
- Wiley
- Published
- 2006-08-21
- Volume
- 91
- Issue
- 5
- Pages
- 807-819
- ISSN
- 0958-0670 (ISSN-L)
- 1469-445X
- OpenAlex
- W1675006565
- Cited by
- 881
- References
- 90
- Citations by year
- 2026: 19 · 2025: 34 · 2024: 28 · 2023: 36 · 2022: 28 · 2021: 44 · 2020: 47 · 2019: 38 · 2018: 33 · 2017: 50 · 2016: 43 · 2015: 65 · 2014: 54 · 2013: 49 · 2012: 48
- FWCI
- 4.03
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Experimental Physiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Heart, Lung, and Blood Institute (HL 32646, HL079650, R01HL035440, R01HL079650, HL35440)
- 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
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Keywords
- hypoxia, reactive oxygen species, cytochrome bc1 complex, electron transport chain, hypoxia-inducible factor alpha, oxidative phosphorylation, oxygen consumption
- MeSH terms
- Animals, Hypoxia, Humans, Mitochondria, Oxygen, Oxygen Consumption, Procollagen-Proline Dioxygenase, Transcription, Genetic, Electron Transport Complex III, Signal Transduction, Reactive Oxygen Species, Hypoxia-Inducible Factor 1
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