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Mitochondrial function and bioenergetic trade‐offs during lactation in the house mouse (Mus musculus)

Energy allocation theory predicts that a lactating female should alter the energetic demands of its organ systems in a manner that maximizes nutrient allocation to reproduction while reducing nutrient use for tasks that are not vital to immediate survival. We posit that organ‐specific plasticity in...

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Autores principales: Mowry, Annelise V., Donoviel, Zachary S., Kavazis, Andreas N., Hood, Wendy R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5415517/
https://www.ncbi.nlm.nih.gov/pubmed/28479999
http://dx.doi.org/10.1002/ece3.2817
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author Mowry, Annelise V.
Donoviel, Zachary S.
Kavazis, Andreas N.
Hood, Wendy R.
author_facet Mowry, Annelise V.
Donoviel, Zachary S.
Kavazis, Andreas N.
Hood, Wendy R.
author_sort Mowry, Annelise V.
collection PubMed
description Energy allocation theory predicts that a lactating female should alter the energetic demands of its organ systems in a manner that maximizes nutrient allocation to reproduction while reducing nutrient use for tasks that are not vital to immediate survival. We posit that organ‐specific plasticity in the function of mitochondria plays a key role in mediating these energetic trade‐offs. The goal of this project was to evaluate mitochondrial changes that occur in response to lactation in two of the most energetically demanding organs in the body of a rodent, the liver and skeletal muscle. This work was conducted in wild‐derived house mice (Mus musculus) kept in seminatural enclosures that allow the mice to maintain a natural social structure and move within a home range size typical of wild mice. Tissues were collected from females at peak lactation and from age‐matched nonreproductive females. Mitochondrial respiration, oxidative damage, antioxidant, PGC‐1α, and uncoupling protein levels were compared between lactating and nonreproductive females. Our findings suggest that both liver and skeletal muscle downregulate specific antioxidant proteins during lactation. The liver, but not skeletal muscle, of lactating females displayed higher oxidative damage than nonreproductive females. The liver mass of lactating females increased, but the liver displayed no change in mitochondrial respiratory control ratio. Skeletal muscle mass and mitochondrial respiratory control ratio were not different between groups. However, the respiratory function of skeletal muscle did vary among lactating females as a function of stage of concurrent pregnancy, litter size, and mass of the mammary glands. The observed changes are predicted to increase the efficiency of skeletal muscle mitochondria, reducing the substrate demands of skeletal muscle during lactation. Differences between our results and prior studies highlight the role that an animals’ social and physical environment could play in how it adapts to the energetic demands of reproduction.
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spelling pubmed-54155172017-05-05 Mitochondrial function and bioenergetic trade‐offs during lactation in the house mouse (Mus musculus) Mowry, Annelise V. Donoviel, Zachary S. Kavazis, Andreas N. Hood, Wendy R. Ecol Evol Original Research Energy allocation theory predicts that a lactating female should alter the energetic demands of its organ systems in a manner that maximizes nutrient allocation to reproduction while reducing nutrient use for tasks that are not vital to immediate survival. We posit that organ‐specific plasticity in the function of mitochondria plays a key role in mediating these energetic trade‐offs. The goal of this project was to evaluate mitochondrial changes that occur in response to lactation in two of the most energetically demanding organs in the body of a rodent, the liver and skeletal muscle. This work was conducted in wild‐derived house mice (Mus musculus) kept in seminatural enclosures that allow the mice to maintain a natural social structure and move within a home range size typical of wild mice. Tissues were collected from females at peak lactation and from age‐matched nonreproductive females. Mitochondrial respiration, oxidative damage, antioxidant, PGC‐1α, and uncoupling protein levels were compared between lactating and nonreproductive females. Our findings suggest that both liver and skeletal muscle downregulate specific antioxidant proteins during lactation. The liver, but not skeletal muscle, of lactating females displayed higher oxidative damage than nonreproductive females. The liver mass of lactating females increased, but the liver displayed no change in mitochondrial respiratory control ratio. Skeletal muscle mass and mitochondrial respiratory control ratio were not different between groups. However, the respiratory function of skeletal muscle did vary among lactating females as a function of stage of concurrent pregnancy, litter size, and mass of the mammary glands. The observed changes are predicted to increase the efficiency of skeletal muscle mitochondria, reducing the substrate demands of skeletal muscle during lactation. Differences between our results and prior studies highlight the role that an animals’ social and physical environment could play in how it adapts to the energetic demands of reproduction. John Wiley and Sons Inc. 2017-03-23 /pmc/articles/PMC5415517/ /pubmed/28479999 http://dx.doi.org/10.1002/ece3.2817 Text en © 2017 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. This is an open access article under the terms of the Creative Commons Attribution (http://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Research
Mowry, Annelise V.
Donoviel, Zachary S.
Kavazis, Andreas N.
Hood, Wendy R.
Mitochondrial function and bioenergetic trade‐offs during lactation in the house mouse (Mus musculus)
title Mitochondrial function and bioenergetic trade‐offs during lactation in the house mouse (Mus musculus)
title_full Mitochondrial function and bioenergetic trade‐offs during lactation in the house mouse (Mus musculus)
title_fullStr Mitochondrial function and bioenergetic trade‐offs during lactation in the house mouse (Mus musculus)
title_full_unstemmed Mitochondrial function and bioenergetic trade‐offs during lactation in the house mouse (Mus musculus)
title_short Mitochondrial function and bioenergetic trade‐offs during lactation in the house mouse (Mus musculus)
title_sort mitochondrial function and bioenergetic trade‐offs during lactation in the house mouse (mus musculus)
topic Original Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5415517/
https://www.ncbi.nlm.nih.gov/pubmed/28479999
http://dx.doi.org/10.1002/ece3.2817
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