High Phosphorylation Efficiency and Depression of Uncoupled Respiration in Mitochondria under Hypoxia
Mitochondria are confronted with low oxygen levels in the microenvironment within tissues; yet, isolated mitochondria are routinely studied under air-saturated conditions that are effectively hyperoxic, increase oxidative stress, and may impair mitochondrial function. Under hypoxia, on the other han...
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| Published in | Proceedings of the National Academy of Sciences - PNAS Vol. 97; no. 20; pp. 11080 - 11085 |
|---|---|
| Main Authors | , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
National Academy of Sciences of the United States of America
26.09.2000
National Acad Sciences National Academy of Sciences The National Academy of Sciences |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Mitochondria are confronted with low oxygen levels in the microenvironment within tissues; yet, isolated mitochondria are routinely studied under air-saturated conditions that are effectively hyperoxic, increase oxidative stress, and may impair mitochondrial function. Under hypoxia, on the other hand, respiration and ATP supply are restricted. Under these conditions of oxygen limitation, any compromise in the coupling of oxidative phosphorylation to oxygen consumption could accentuate ATP depletion, leading to metabolic failure. To address this issue, we have developed the approach of oxygen-injection microcalorimetry and ADP-injection respirometry for evaluating mitochondrial function at limiting oxygen supply. Whereas phosphorylation efficiency drops during ADP limitation at high oxygen levels, we show here that oxidative phosphorylation is more efficient at low oxygen than at air saturation, as indicated by higher ratios of ADP flux to total oxygen flux at identical submaximal rates of ATP synthesis. At low oxygen, the proton leak and uncoupled respiration are depressed, thus reducing maintenance energy expenditure. This indicates the importance of low intracellular oxygen levels in avoiding oxidative stress and protecting bioenergetic efficiency. |
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| AbstractList | Mitochondria are confronted with low oxygen levels in the
microenvironment within tissues; yet, isolated mitochondria are
routinely studied under air-saturated conditions that are effectively
hyperoxic, increase oxidative stress, and may impair mitochondrial
function. Under hypoxia, on the other hand, respiration and ATP supply
are restricted. Under these conditions of oxygen limitation,
any compromise in the coupling of oxidative phosphorylation to
oxygen consumption could accentuate ATP depletion, leading to
metabolic failure. To address this issue, we have developed the
approach of oxygen-injection microcalorimetry and ADP-injection
respirometry for evaluating mitochondrial function at limiting oxygen
supply. Whereas phosphorylation efficiency drops during ADP limitation
at high oxygen levels, we show here that oxidative phosphorylation is
more efficient at low oxygen than at air saturation, as indicated by
higher ratios of ADP flux to total oxygen flux at identical submaximal
rates of ATP synthesis. At low oxygen, the proton leak and uncoupled
respiration are depressed, thus reducing maintenance energy
expenditure. This indicates the importance of low intracellular oxygen
levels in avoiding oxidative stress and protecting bioenergetic
efficiency. Mitochondria are confronted with low oxygen levels in the microenvironment within tissues; yet, isolated mitochondria are routinely studied under air-saturated conditions that are effectively hyperoxic, increase oxidative stress, and may impair mitochondrial function. Under hypoxia, on the other hand, respiration and ATP supply are restricted. Under these conditions of oxygen limitation, any compromise in the coupling of oxidative phosphorylation to oxygen consumption could accentuate ATP depletion, leading to metabolic failure. To address this issue, we have developed the approach of oxygen-injection microcalorimetry and ADP-injection respirometry for evaluating mitochondrial function at limiting oxygen supply. Whereas phosphorylation efficiency drops during ADP limitation at high oxygen levels, we show here that oxidative phosphorylation is more efficient at low oxygen than at air saturation, as indicated by higher ratios of ADP flux to total oxygen flux at identical submaximal rates of ATP synthesis. At low oxygen, the proton leak and uncoupled respiration are depressed, thus reducing maintenance energy expenditure. This indicates the importance of low intracellular oxygen levels in avoiding oxidative stress and protecting bioenergetic efficiency. Mitochondria are confronted with low oxygen levels in the microenvironment within tissues; yet, isolated mitochondria are routinely studied under air-saturated conditions that are effectively hyperoxic, increase oxidative stress, and may impair mitochondrial function. |
| Author | Gnaiger, Erich Hand, Steven C. Mendez, Gabriela |
| AuthorAffiliation | Department of Transplant Surgery, D. Swarovski Research Laboratory, University Hospital Innsbruck, Anichstrasse 35, A-6020 Innsbruck, Austria; and ‡ Department of Environmental, Population, and Organismic Biology, University of Colorado, Boulder, CO 80309-0334 |
| AuthorAffiliation_xml | – name: Department of Transplant Surgery, D. Swarovski Research Laboratory, University Hospital Innsbruck, Anichstrasse 35, A-6020 Innsbruck, Austria; and ‡ Department of Environmental, Population, and Organismic Biology, University of Colorado, Boulder, CO 80309-0334 |
| Author_xml | – sequence: 1 givenname: Erich surname: Gnaiger fullname: Gnaiger, Erich – sequence: 2 givenname: Gabriela surname: Mendez fullname: Mendez, Gabriela – sequence: 3 givenname: Steven C. surname: Hand fullname: Hand, Steven C. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/11005877$$D View this record in MEDLINE/PubMed |
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| Copyright | Copyright 1993-2000 National Academy of Sciences of the United States of America Copyright National Academy of Sciences Sep 26, 2000 Copyright © 2000, The National Academy of Sciences 2000 |
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| Snippet | Mitochondria are confronted with low oxygen levels in the microenvironment within tissues; yet, isolated mitochondria are routinely studied under air-saturated... Mitochondria are confronted with low oxygen levels in the microenvironment within tissues; yet, isolated mitochondria are routinely studied under air-saturated... |
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| SubjectTerms | Adenosine Triphosphate - metabolism Air Animals Artemia Biological Sciences Electron Transport Hypoxia Liver Mitochondria Mitochondria, Liver - metabolism Oxidative stress Oxygen Phosphorylation Ratios Rats Rats, Sprague-Dawley Respiration Respiratory system |
| Title | High Phosphorylation Efficiency and Depression of Uncoupled Respiration in Mitochondria under Hypoxia |
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