Mitochondrial respiratory chain-dependent generation of superoxide anion and its release into the intermembrane space

HAN, Derick; WILLIAMS, Everett; CADENAS, Enrique

doi:10.1042/bj3530411

Cited by 593Mitochondrial Function and PathologyRedox biology and oxidative stressCoenzyme Q10 studies and effects

Mitochondrial respiratory chain-dependent generation of superoxide anion and its release into the intermembrane space

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HAN, Derick, WILLIAMS, Everett, CADENAS, Enrique·2001·Biochemical Journal

DOI 10.1042/bj3530411PMC PMC1221585

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Abstract

It has been generally accepted that superoxide anion generated by the mitochondrial respiratory transport chain are vectorially released into the mitochondrial matrix, where they are converted to hydrogen peroxide through the catalytic action of Mn-superoxide dismutase. Release of superoxide anion into the intermembrane space is a controversial topic, partly unresolved by the reaction of superoxide anion with cytochrome c, which faces the intermembrane space and is present in this compartment at a high concentration. This study was aimed at assessing the topological site(s) of release of superoxide anion during respiratory chain activity. To address this issue, mitoplasts were prepared from isolated mitochondria by digitonin treatment to remove portions of the outer membrane along with portions of cytochrome c. EPR analysis in conjunction with spin traps of antimycin-supplemented mitoplasts revealed the formation of a spin adduct of superoxide anion. The EPR signal was (i) abrogated by superoxide dismutase, (ii) decreased competitively by exogenous ferricytochrome c and (iii) broadened by the membrane-impermeable spin-broadening agent chromium trioxalate. These results confirm the production and release of superoxide anion towards the cytosolic side of the inner mitochondrial membrane. In addition, co-treatment of mitoplasts with myxothiazol and antimycin A, resulting in an inhibition of the oxidation of ubiquinol to ubisemiquinone, abolished the EPR signal, thus suggesting that ubisemiquinone autoxidation at the outer site of the complex-III ubiquinone pool is a pathway for superoxide anion formation and subsequent release into the intermembrane space. The generation of superoxide anion towards the intermembrane space requires consideration of the mitochondrial steady-state values for superoxide anion and hydrogen peroxide, the decay pathways of these oxidants in this compartment and the implications of these processes for cytosolic events.

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During inhibition of mitochondrial respiration by hypoxia, O2 was found to redistribute toward nonrespiratory O2-dependent targets such as PHs, so that they no longer registered hypoxia.
“During inhibition of mitochondrial respiration by hypoxia, O2 was found to redistribute toward nonrespiratory O2-dependent targets such as PHs, so that they no longer registered hypoxia (147).”
From Mitochondrial reactive oxygen species production in excitable cells: Modulators of mitochondrial and cell function (2009) · cites this paper as [147]
Nitric oxide, and other inhibitors of mitochondrial respiration, can prevent stabilization of HIF-1α during hypoxia as a result of an increase in PH-dependent degradation of HIF-1α.
“Nitric oxide, and other inhibitors of mitochondrial respiration, can prevent stabilization of HIF-1α during hypoxia as a result of an increase in PH-dependent degradation of HIF-1α (147).”
From Mitochondrial reactive oxygen species production in excitable cells: Modulators of mitochondrial and cell function (2009) · cites this paper as [147]

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Authors: HAN, D., WILLIAMS, E., & CADENAS, E.
Affiliations: University of Southern California (US)
ORCID: HAN, Derick
CADENAS, Enrique
Venue: Biochemical Journal
Publisher: Portland Press Ltd.
Published: 2001-01-08
Volume: 353
Issue: 2
Pages: 411-416
ISSN: 0264-6021 (ISSN-L)
1470-8728
DOI: 10.1042/bj3530411
PMC: PMC1221585
OpenAlex: W1966571906
Cited by: 593
References: 0
Citations by year: 2026: 8 · 2025: 13 · 2024: 17 · 2023: 17 · 2022: 22 · 2021: 36 · 2020: 19 · 2019: 33 · 2018: 18 · 2017: 16 · 2016: 27 · 2015: 29 · 2014: 24 · 2013: 23 · 2012: 32
FWCI: 8.26
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Biochemical Journal (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute on Aging (R01AG016718, 1RO1-AG16718)
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 › Molecular Biology › Coenzyme Q10 studies and effects
Keywords: superoxide, mitochondrial respiratory chain, intermembrane space, cytochrome c, mitoplasts, antimycin A, cytochrome bc1 complex, hydrogen peroxide, superoxide dismutase, myxothiazol
MeSH terms: Animals, Digitonin, Electron Spin Resonance Spectroscopy, Intracellular Membranes, Male, Mitochondria, Liver, Oxalates, Oxidation-Reduction, Superoxides, Electron Transport Complex III, Rats, Wistar, Rats

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Mitochondrial respiratory chain-dependent generation of superoxide anion and its release into the intermembrane space

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