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1 Medical Research Council Dunn Human Nutrition Unit, Hills Road, Cambridge CB2 2XY, UK2 Laboratoire Physiologie Intégrative, Cellulaire et Moléculaire, Centre National de la Recherche Scientifique-Université Cl. Bernard Lyon 1, 43 Bld 11 Novembre 1918, F-69622 Villeurbanne Cedex, France
Juvenile king penguins develop adaptive thermogenesis after repeated immersion in cold water. However, the mechanisms of such metabolic adaptation in birds are unknown, as they lack brown adipose tissue and uncoupling protein-1 (UCP1), which mediate adaptive non-shivering thermogenesis in mammals. We used three different groups of juvenile king penguins to investigate the mitochondrial basis of avian adaptive thermogenesis in vitro. Skeletal muscle mitochondria isolated from penguins that had never been immersed in cold water showed no superoxide-stimulated proton conductance, indicating no functional avian UCP. Skeletal muscle mitochondria from penguins that had been either experimentally immersed or naturally adapted to cold water did possess functional avian UCP, demonstrated by a superoxide-stimulated, GDP-inhibitable proton conductance across their inner membrane. This was associated with a markedly greater abundance of avian UCP mRNA. In the presence (but not the absence) of fatty acids, these mitochondria also showed a greater adenine nucleotide translocase-catalysed proton conductance than those from never-immersed penguins. This was due to an increase in the amount of adenine nucleotide translocase. Therefore, adaptive thermogenesis in juvenile king penguins is linked to two separate mechanisms of uncoupling of oxidative phosphorylation in skeletal muscle mitochondria: increased proton transport activity of avian UCP (dependent on superoxide and inhibited by GDP) and increased proton transport activity of the adenine nucleotide translocase (dependent on fatty acids and inhibited by carboxyatractylate).
(Received 3 March 2004;
accepted after revision 7 May 2004;
first published online 14 May 2004)
Corresponding author M. D. Brand: Medical Research Council Dunn Human Nutrition Unit, Hills Road, Cambridge CB2 2XY, UK. Email: martin.brand{at}mrc-dunn.cam.ac.uk
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