Gnaiger 2000 Proc Natl Acad Sci U S A: Difference between revisions

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{{Publication
{{Publication
|title=Gnaiger E, MΓ©ndez G, Hand SC (2000) High phosphorylation efficiency and depression of uncoupled respiration in mitochondria under hypoxia. Proc Natl Acad Sci U S A 97:11080-5.
|title=Gnaiger E, MΓ©ndez G, Hand SC (2000) High phosphorylation efficiency and depression of uncoupled respiration in mitochondria under hypoxia. Proc Natl Acad Sci U S A 97:11080-5. https://doi.org/10.1073/pnas.97.20.11080
|info=[http://www.ncbi.nlm.nih.gov/pubmed/11005877 PMID: 11005877 Open Access]
|info=[http://www.ncbi.nlm.nih.gov/pubmed/11005877 PMID: 11005877 Open Access]
|authors=Gnaiger E, Mendez G, Hand SC
|authors=Gnaiger Erich, Mendez Gabriela, Hand Steven C
|year=2000
|year=2000
|journal=Proc Natl Acad Sci U S A
|journal=Proc Natl Acad Sci U S A
|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.
|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.
|mipnetlab=AT Innsbruck Gnaiger E, US LA Baton Rouge Hand SC
|mipnetlab=AT Innsbruck Oroboros, AT Innsbruck Gnaiger E, US LA Baton Rouge Hand SC
|discipline=Mitochondrial Physiology
}}
}}
== Selected quotes ==
::::* Atmospheric oxygen levels were probably 0.1 % of the present when mitochondria became associated with cells early during evolution (1-4). Such low-oxygen conditions persist in extreme environments (5-8), and oxygen pessures as low as 0.3-0.4 kPa (2-3 mmHg) are observed in the intracellular microenvironment of mitochondria in tissues under [[normoxic |normoxia]] (9-13). Even so, in typical studies with isolated mitochondria, these organelles are artificially exposed to the high partial pressure of oxygen at air saturation (c. 20 kPa), despite the fact that this condition is effectively [[hyperoxic]], rarely physiological and increases oxidative stress (14, 15).
::::* From the present study, it can be inferred that air-saturation as a reference condition is questionable for evaluating mitochondrial efficiency. If representative measures of performance are to be obtained for mitochondria and even cultured cells (42, 44), then oxygen tension should be shifted away from these non-physiological levels to minimize the risk of oxidative stress.
::::* Furthermore, the high efficiency of oxidative phosphorylation at low oxygen emphasizes that even trace amounts of oxygen can make a vital energetic contribution when ATP limitation threatens cellular survival under severe hypoxia encountered at high altitude, in aquatic habitats, and during pathological states of ischemia.
== Further details ==
:::* Gnaiger E (2001) Bioenergetics at low oxygen: dependence of respiration and phosphorylation on oxygen and adenosine diphosphate supply. Respir Physiol 128:277-97. - [[Gnaiger 2001 Respir Physiol |Β»Bioblast linkΒ«]]
::::Β» [[OXPHOS-coupling efficiency]]
::::Β» [[ETS coupling efficiency]]
{{Template:Keywords: hypoxia, normoxia, hyperoxia}}
:::* [http://www.ncbi.nlm.nih.gov/pubmed?db=pubmed&cmd=link&linkname=pubmed_pubmed_citedin&uid=11005877 Citations]
== Cited by ==
::* 60 articles in PubMed (2021-12-27) https://pubmed.ncbi.nlm.nih.gov/11005877/
{{Template:Cited by Cardoso 2021 MitoFit MgG}}
{{Template:Cited by Gnaiger 2020 BEC MitoPathways}}
{{Template:Cited by Gnaiger 2020 BEC MitoPhysiology}}
{{Labeling
{{Labeling
|area=Respiration, Comparative MiP;environmental MiP, Developmental biology
|area=Respiration, mt-Biogenesis;mt-density, mt-Structure;fission;fusion, Comparative MiP;environmental MiP, Developmental biology
|organism=Rat, Artemia
|organism=Rat, Artemia, Crustaceans
|taxonomic group=Crustaceans
|tissues=Liver
|tissues=Liver
|preparations=Isolated mitochondria
|preparations=Isolated mitochondria
|topics=ADP, ATP, Coupling efficiency;uncoupling, Oxygen kinetics
|topics=ADP, ATP, Coupling efficiency;uncoupling, Oxygen kinetics
|couplingstates=LEAK, OXPHOS
|couplingstates=LEAK, OXPHOS
|substratestates=CII
|pathways=S
|instruments=Oxygraph-2k, TIP2k
|instruments=Oxygraph-2k, TIP2k
|discipline=Mitochondrial Physiology
|additional=Ambiguity crisis, Tissue normoxia, ATP, Steady state,
BEC 2020.1, BEC 2020.2, MitoFit 2021 MgG, MitoFit2022rTCA, MitoFit2022Hypoxia
}}
}}
== Further details ==
:::* Gnaiger E (2001) Bioenergetics at low oxygen: dependence of respiration and phosphorylation on oxygen and adenosine diphosphate supply. Respir Physiol 128:277-97. [[Gnaiger 2001 Respir Physiol |Β»Bioblast linkΒ«]]
:::* Gnaiger E (2014) Mitochondrial pathways and respiratory control. An introduction to OXPHOS analysis. 4th ed. Mitochondr Physiol Network 19.12. OROBOROS MiPNet Publications, Innsbruck:80 pp. - [[Gnaiger 2014 MitoPathways |Β»Bioblast linkΒ«]] with update on terminology and biochemical efficiency.
:::* [http://www.ncbi.nlm.nih.gov/pubmed?db=pubmed&cmd=link&linkname=pubmed_pubmed_citedin&uid=11005877 Citations]

Revision as of 09:47, 11 March 2024

Publications in the MiPMap
Has title::Gnaiger E, MΓ©ndez G, Hand SC (2000) High phosphorylation efficiency and depression of uncoupled respiration in mitochondria under hypoxia. Proc Natl Acad Sci U S A 97:11080-5. https://doi.org/10.1073/pnas.97.20.11080

Β» [[Has info::PMID: 11005877 Open Access]]

Was written by::Gnaiger Erich, Was written by::Mendez Gabriela, Was written by::Hand Steven C (Was published in year::2000) Was published in journal::Proc Natl Acad Sci U S A

Abstract: [[has 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.]]


β€’ O2k-Network Lab: Was published by MiPNetLab::AT Innsbruck Oroboros, Was published by MiPNetLab::AT Innsbruck Gnaiger E, Was published by MiPNetLab::US LA Baton Rouge Hand SC

Selected quotes

  • Atmospheric oxygen levels were probably 0.1 % of the present when mitochondria became associated with cells early during evolution (1-4). Such low-oxygen conditions persist in extreme environments (5-8), and oxygen pessures as low as 0.3-0.4 kPa (2-3 mmHg) are observed in the intracellular microenvironment of mitochondria in tissues under normoxia (9-13). Even so, in typical studies with isolated mitochondria, these organelles are artificially exposed to the high partial pressure of oxygen at air saturation (c. 20 kPa), despite the fact that this condition is effectively hyperoxic, rarely physiological and increases oxidative stress (14, 15).
  • From the present study, it can be inferred that air-saturation as a reference condition is questionable for evaluating mitochondrial efficiency. If representative measures of performance are to be obtained for mitochondria and even cultured cells (42, 44), then oxygen tension should be shifted away from these non-physiological levels to minimize the risk of oxidative stress.
  • Furthermore, the high efficiency of oxidative phosphorylation at low oxygen emphasizes that even trace amounts of oxygen can make a vital energetic contribution when ATP limitation threatens cellular survival under severe hypoxia encountered at high altitude, in aquatic habitats, and during pathological states of ischemia.


Further details

  • Gnaiger E (2001) Bioenergetics at low oxygen: dependence of respiration and phosphorylation on oxygen and adenosine diphosphate supply. Respir Physiol 128:277-97. - Β»Bioblast linkΒ«
Β» OXPHOS-coupling efficiency
Β» ETS coupling efficiency


Keywords: Oxia terms

Questions.jpg


Click to expand or collaps
Bioblast links: Hypoxia, normoxia, hyperoxia - >>>>>>> - Click on [Expand] or [Collapse] - >>>>>>>

{{#ask:Additional label::MitoPedia:Normoxia | mainlabel=Term |?Has abbr=Abbreviation |?Description=Description |format=broadtable |limit=5000 |order=ascending }}

General
Β» Oxygen, dioxygen, O2
Β» Intracellular oxygen
Β» Oxygen pressure
Β» Oxygen solubility
Β» Gas pressure
Β» pascal
Β» Pressure
Β» Barometric pressure
Β» Concentration
Related keyword lists
Β» Keywords: Oxygen signal
Β» Keywords: Concentration and pressure

Publications: Tissue normoxia

{{#ask:Additional label::Tissue normoxia |?Was published in year=Year |?Has title=Reference |?Mammal and model=Organism |?Tissue and cell=Tissue;cell |?Preparation=Preparations |?Stress |?Diseases |format=broadtable |limit=5000 |offset=0 |sort=Was published in year |order=descending }}

Abstracts: Tissue normoxia

{{#ask: Additional label::Tissue normoxia |?Was submitted in year=Year |?Has title=Reference |?Mammal and model=Organism |?Tissue and cell=Tissue;cell |?Preparation=Preparations |?Stress |?Diseases |format=broadtable |limit=5000 |offset=0 |sort=Was submitted in year |order=descending }}


Cited by

  • Cardoso et al (2021) Magnesium Green for fluorometric measurement of ATP production does not interfere with mitochondrial respiration. Bioenerg Commun 2021.1. doi:10.26124/bec:2021-0001
Gnaiger 2020 BEC MitoPathways
Gnaiger E (2020) Mitochondrial pathways and respiratory control. An introduction to OXPHOS analysis. 5th ed. Bioenerg Commun 2020.2. https://doi.org/10.26124/bec:2020-0002


Gnaiger Erich et al ― MitoEAGLE Task Group (2020) Mitochondrial physiology. Bioenerg Commun 2020.1.
Gnaiger E et al ― MitoEAGLE Task Group (2020) Mitochondrial physiology. Bioenerg Commun 2020.1. doi:10.26124/bec:2020-0001.v1.



Labels: MiParea: MiP area::Respiration, MiP area::mt-Biogenesis;mt-density, MiP area::mt-Structure;fission;fusion, MiP area::Comparative MiP;environmental MiP, MiP area::Developmental biology 


Organism: Organism::Rat, Organism::Artemia, Organism::Crustaceans  Tissue;cell: tissue and cell::Liver  Preparation: Preparation::Isolated mitochondria 

Regulation: Topic::ADP, Topic::ATP, Topic::Coupling efficiency;uncoupling, Topic::Oxygen kinetics  Coupling state: Coupling states::LEAK, Coupling states::OXPHOS  Pathway: Pathways::S  HRR: Instrument and method::Oxygraph-2k, Instrument and method::TIP2k 

additional label::Ambiguity crisis, additional label::Tissue normoxia, additional label::ATP, additional label::Steady state, additional label::BEC 2020.1, additional label::BEC 2020.2, additional label::MitoFit 2021 MgG, additional label::MitoFit2022rTCA, additional label::MitoFit2022Hypoxia