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Tissue-specific reductions in mitochondrial efficiency and increased ROS release rates during ageing in zebra finches, Taeniopygia guttata

Mitochondrial dysfunction and oxidative damage have long been suggested as critically important mechanisms underlying the ageing process in animals. However, conflicting data exist on whether this involves increased production of mitochondrial reactive oxygen species (ROS) during ageing. We employed...

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Autores principales: Salmón, Pablo, Millet, Caroline, Selman, Colin, Monaghan, Pat, Dawson, Neal J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer International Publishing 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9886749/
https://www.ncbi.nlm.nih.gov/pubmed/35986126
http://dx.doi.org/10.1007/s11357-022-00624-1
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author Salmón, Pablo
Millet, Caroline
Selman, Colin
Monaghan, Pat
Dawson, Neal J.
author_facet Salmón, Pablo
Millet, Caroline
Selman, Colin
Monaghan, Pat
Dawson, Neal J.
author_sort Salmón, Pablo
collection PubMed
description Mitochondrial dysfunction and oxidative damage have long been suggested as critically important mechanisms underlying the ageing process in animals. However, conflicting data exist on whether this involves increased production of mitochondrial reactive oxygen species (ROS) during ageing. We employed high‐resolution respirometry and fluorometry on flight muscle (pectoralis major) and liver mitochondria to simultaneously examine mitochondrial function and ROS (H(2)O(2)) release rates in young (3 months) and old (4 years) zebra finches (Taeniopygia guttata). Respiratory capacities for oxidative phosphorylation did not differ between the two age groups in either tissue. Respiratory control ratios (RCR) of liver mitochondria also did not differ between the age classes. However, RCR in muscle mitochondria was 55% lower in old relative to young birds, suggesting that muscle mitochondria in older individuals are less efficient. Interestingly, this observed reduction in muscle RCR was driven almost entirely by higher mitochondrial LEAK-state respiration. Maximum mitochondrial ROS release rates were found to be greater in both flight muscle (1.3-fold) and the liver (1.9-fold) of old birds. However, while maximum ROS (H(2)O(2)) release rates from mitochondria increased with age across both liver and muscle tissues, the liver demonstrated a proportionally greater age-related increase in ROS release than muscle. This difference in age-related increases in ROS release rates between muscle and liver tissues may be due to increased mitochondrial leakiness in the muscle, but not the liver, of older birds. This suggests that age-related changes in cellular function seem to occur in a tissue-specific manner in zebra finches, with flight muscle exhibiting signs of minimising age-related increase in ROS release, potentially to reduce damage to this crucial tissue in older individuals. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s11357-022-00624-1.
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spelling pubmed-98867492023-02-01 Tissue-specific reductions in mitochondrial efficiency and increased ROS release rates during ageing in zebra finches, Taeniopygia guttata Salmón, Pablo Millet, Caroline Selman, Colin Monaghan, Pat Dawson, Neal J. GeroScience Original Article Mitochondrial dysfunction and oxidative damage have long been suggested as critically important mechanisms underlying the ageing process in animals. However, conflicting data exist on whether this involves increased production of mitochondrial reactive oxygen species (ROS) during ageing. We employed high‐resolution respirometry and fluorometry on flight muscle (pectoralis major) and liver mitochondria to simultaneously examine mitochondrial function and ROS (H(2)O(2)) release rates in young (3 months) and old (4 years) zebra finches (Taeniopygia guttata). Respiratory capacities for oxidative phosphorylation did not differ between the two age groups in either tissue. Respiratory control ratios (RCR) of liver mitochondria also did not differ between the age classes. However, RCR in muscle mitochondria was 55% lower in old relative to young birds, suggesting that muscle mitochondria in older individuals are less efficient. Interestingly, this observed reduction in muscle RCR was driven almost entirely by higher mitochondrial LEAK-state respiration. Maximum mitochondrial ROS release rates were found to be greater in both flight muscle (1.3-fold) and the liver (1.9-fold) of old birds. However, while maximum ROS (H(2)O(2)) release rates from mitochondria increased with age across both liver and muscle tissues, the liver demonstrated a proportionally greater age-related increase in ROS release than muscle. This difference in age-related increases in ROS release rates between muscle and liver tissues may be due to increased mitochondrial leakiness in the muscle, but not the liver, of older birds. This suggests that age-related changes in cellular function seem to occur in a tissue-specific manner in zebra finches, with flight muscle exhibiting signs of minimising age-related increase in ROS release, potentially to reduce damage to this crucial tissue in older individuals. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s11357-022-00624-1. Springer International Publishing 2022-08-19 /pmc/articles/PMC9886749/ /pubmed/35986126 http://dx.doi.org/10.1007/s11357-022-00624-1 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Original Article
Salmón, Pablo
Millet, Caroline
Selman, Colin
Monaghan, Pat
Dawson, Neal J.
Tissue-specific reductions in mitochondrial efficiency and increased ROS release rates during ageing in zebra finches, Taeniopygia guttata
title Tissue-specific reductions in mitochondrial efficiency and increased ROS release rates during ageing in zebra finches, Taeniopygia guttata
title_full Tissue-specific reductions in mitochondrial efficiency and increased ROS release rates during ageing in zebra finches, Taeniopygia guttata
title_fullStr Tissue-specific reductions in mitochondrial efficiency and increased ROS release rates during ageing in zebra finches, Taeniopygia guttata
title_full_unstemmed Tissue-specific reductions in mitochondrial efficiency and increased ROS release rates during ageing in zebra finches, Taeniopygia guttata
title_short Tissue-specific reductions in mitochondrial efficiency and increased ROS release rates during ageing in zebra finches, Taeniopygia guttata
title_sort tissue-specific reductions in mitochondrial efficiency and increased ros release rates during ageing in zebra finches, taeniopygia guttata
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9886749/
https://www.ncbi.nlm.nih.gov/pubmed/35986126
http://dx.doi.org/10.1007/s11357-022-00624-1
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