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Research Article
Mitochondrial uncoupling prevents cold-induced oxidative stress: a case study using UCP1 knockout mice
Antoine Stier, Pierre Bize, Caroline Habold, Frederic Bouillaud, Sylvie Massemin, François Criscuolo
Journal of Experimental Biology 2014 217: 624-630; doi: 10.1242/jeb.092700
Antoine Stier
1University of Strasbourg, Institut Pluridisciplinaire Hubert Curien, Strasbourg 67037, France
2Département d'Ecologie, Physiologie et Ethologie (DEPE), CNRS UMR7178, 23 Rue Becquerel, 67087 Strasbourg Cedex 2, France
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  • For correspondence: antoine.stier@gmail.com
Pierre Bize
3Department of Ecology and Evolution, University of Lausanne, Biophore Building 1015, Lausanne-Dorigny, Switzerland
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Caroline Habold
1University of Strasbourg, Institut Pluridisciplinaire Hubert Curien, Strasbourg 67037, France
2Département d'Ecologie, Physiologie et Ethologie (DEPE), CNRS UMR7178, 23 Rue Becquerel, 67087 Strasbourg Cedex 2, France
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Frederic Bouillaud
4Institut Cochin, Inserm UMRS 1016, CNRS UMR 8104, Université Paris Descartes, 75014 Paris, France
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Sylvie Massemin
1University of Strasbourg, Institut Pluridisciplinaire Hubert Curien, Strasbourg 67037, France
2Département d'Ecologie, Physiologie et Ethologie (DEPE), CNRS UMR7178, 23 Rue Becquerel, 67087 Strasbourg Cedex 2, France
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François Criscuolo
1University of Strasbourg, Institut Pluridisciplinaire Hubert Curien, Strasbourg 67037, France
2Département d'Ecologie, Physiologie et Ethologie (DEPE), CNRS UMR7178, 23 Rue Becquerel, 67087 Strasbourg Cedex 2, France
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Abstract

The relationship between metabolism and reactive oxygen species (ROS) production by the mitochondria has often been (wrongly) viewed as straightforward, with increased metabolism leading to higher generation of pro-oxidants. Insights into mitochondrial functioning show that oxygen consumption is principally coupled with either energy conversion as ATP or as heat, depending on whether the ATP-synthase or the mitochondrial uncoupling protein 1 (UCP1) is driving respiration. However, these two processes might greatly differ in terms of oxidative costs. We used a cold challenge to investigate the oxidative stress consequences of an increased metabolism achieved either by the activation of an uncoupled mechanism (i.e. UCP1 activity) in the brown adipose tissue (BAT) of wild-type mice or by ATP-dependent muscular shivering thermogenesis in mice deficient for UCP1. Although both mouse strains increased their metabolism by more than twofold when acclimatised for 4 weeks to moderate cold (12°C), only mice deficient for UCP1 suffered from elevated levels of oxidative stress. When exposed to cold, mice deficient for UCP1 showed an increase of 20.2% in plasmatic reactive oxygen metabolites, 81.8% in muscular oxidized glutathione and 47.1% in muscular protein carbonyls. In contrast, there was no evidence of elevated levels of oxidative stress in the plasma, muscles or BAT of wild-type mice exposed to cold despite a drastic increase in BAT activity. Our study demonstrates differing oxidative costs linked to the functioning of two highly metabolically active organs during thermogenesis, and advises careful consideration of mitochondrial functioning when investigating the links between metabolism and oxidative stress.

FOOTNOTES

  • ↵‡ Present address: Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen AB24 2TZ, UK.

  • Author contributions

    A.S. designed the study. A.S. and C.H. collected the data. A.S., F.C., P.B., S.M. and F.B. took part in data analyses and interpretations. A.S., P.B. and F.C. wrote the paper. All authors have read and approved the final version of the manuscript.

  • Competing interests

    The authors declare no competing financial interests.

  • Funding

    This work was supported by the CNRS (PICS, grant no. 5296 to F.C.), the French Ministry of Research and the University of Strasbourg. P.B. is funded by the Swiss National Research Foundation (grant no. 31003A_124988).

  • Supplementary material

    Supplementary material available online at http://jeb.biologists.org/lookup/suppl/doi:10.1242/jeb.092700/-/DC1

  • © 2014. Published by The Company of Biologists Ltd
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Keywords

  • Uncoupling protein
  • Oxidative stress
  • Reactive Oxygen Species
  • Cold
  • nonshivering thermogenesis
  • Mitochondria

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Research Article
Mitochondrial uncoupling prevents cold-induced oxidative stress: a case study using UCP1 knockout mice
Antoine Stier, Pierre Bize, Caroline Habold, Frederic Bouillaud, Sylvie Massemin, François Criscuolo
Journal of Experimental Biology 2014 217: 624-630; doi: 10.1242/jeb.092700
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Research Article
Mitochondrial uncoupling prevents cold-induced oxidative stress: a case study using UCP1 knockout mice
Antoine Stier, Pierre Bize, Caroline Habold, Frederic Bouillaud, Sylvie Massemin, François Criscuolo
Journal of Experimental Biology 2014 217: 624-630; doi: 10.1242/jeb.092700

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