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First published online April 18, 2008
Journal of Experimental Biology 211, 1456-1462 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.012328

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Reptilian uncoupling protein: functionality and expression in sub-zero temperatures

Benjamin Rey¹, Brigitte Sibille¹, Caroline Romestaing¹, Maud Belouze¹, Dominique Letexier¹, Stéphane Servais¹, Hervé Barré¹, Claude Duchamp¹ and Yann Voituron^2,*

¹ Laboratoire de Physiologie Intégrative, cellulaire et moléculaire, Centre National de la Recherche Scientifique (CNRS) – Université Claude Bernard Lyon 1, 43 Bvd 11 Novembre 1918, F-69622 Villeurbanne Cedex, France
² Station d'Ecologie Expérimentale du CNRS à Moulis, Laboratoire Evolution et Diversité du Vivant, Moulis, F-09200 Saint-Girons, France

^* Author for correspondence at present address: Université Claude Bernard Lyon 1, UMR CNRS 5023 – Ecologie des Hydrosystèmes Fluviaux, Bât. Darwin C, F-69622 Villeurbanne Cedex, France (e-mail: yann.voituron{at}univ-lyon1.fr)

Accepted 3 March 2008

Here we report the partial nucleotide sequence of a reptilian uncoupling protein (repUCP) gene from the European common lizard (Lacerta vivipara). Overlapping sequence analysis reveals that the protein shows 55%, 72% and 77% sequence homology with rat UCP1, UCP2 and UCP3, respectively, and 73% with bird and fish UCPs. RepUCP gene expression was ubiquitously detected in 4°C cold-acclimated lizard tissues and upregulated in muscle tissues by a 20 h exposure to sub-zero temperatures in a supercooling state or after thawing. In parallel, we show an increase in the co-activators, peroxisome proliferator-activated receptor coactivator-1 (PGC-1) and peroxisome proliferator-activated receptors (PPAR), mRNA expression, suggesting that the mechanisms regulating UCP expression may be conserved between mammals (endotherms) and reptiles (ectotherms). Furthermore, mitochondria extracted from lizard skeletal muscle showed a guanosine diphosphate (GDP)-sensitive non phosphorylating respiration. This last result indicates an inhibition of extra proton leakage mediated by an uncoupling protein, providing arguments that repUCP is functional in lizard tissues. This result is associated with a remarkable GDP-dependent increase in mitochondrial endogenous H₂O₂ production. All together, these data support a physiological role of the repUCP in superoxide limitation by lizard mitochondria in situations of stressful oxidative reperfusion following a re-warming period in winter.

Key words: Lacerta, cold hardiness, mitochondria, superoxide, supercooling, freezing