An uncoupling protein homologue putatively involved in facultative muscle thermogenesis in birds

RAIMBAULT, Serge; Dridi, Sami; DENJEAN, Frédérique; LACHUER, Joël; COUPLAN, Elodie; Bouillaud, Frédéric; Bordas, A.; Duchamp, Claude; Taouis, Mohammed; Ricquier, Daniel

doi:10.1042/bj3530441

Cited by 143 publications

(70 citation statements)

References 25 publications

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“…3B). Previous studies have shown that exposure to cold stress increased expression of avUCP [18,30,31] and avANT [18] gene transcripts in the skeletal muscle of birds. These results led to the hypothesis that expression of avUCP and avANT influence thermogenesis.…”

Section: Discussionmentioning

confidence: 94%

Sequential changes in superoxide production, anion carriers and substrate oxidation in skeletal muscle mitochondria of heat‐stressed chickens

et al. 2007

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We have shown that heat-stressed birds exhibit increased superoxide production in skeletal muscle mitochondria.To determine the precise mechanism for this effect, here we studied not only progressive, but also sequential changes in superoxide production, anion carriers and substrate oxidation in mitochondria of heat-stressed chickens. Exposure to acute heat stress (34°C for 6, 12 and 18 h) stimulated pectoralis muscle mitochondrial superoxide production. Heat stress-induced downregulations of avUCP gene transcripts and mitochondrial avUCP protein content were time-dependent: avUCP gene transcript was decreased after 6 h, while avUCP protein content was only downregulated after 12 h of heat stress. Avian adenine nucleotide translocator (avANT) gene transcripts were not changed on exposure to heat stress, suggesting that avANT may not be involved in the regulation of superoxide production in the muscle mitochondria of heat-stressed chickens. During the initial stage of acute heat stress b-oxidation enzymes gene transcripts and activity were upregulated, with elevated plasma non-esterified fatty acid levels and increased expression of mitochondrial fatty acid transport genes. This sudden surge in mitochondrial substrate oxidation resulted in higher superoxide production: the avUCP expression at 6 h after heat stress might have not been large enough to alleviate the overproduction of reactive oxygen species (ROS) even though a small amount of endogenous FFA, a potential uncoupler, might have been present in the mitochondria. Thereafter, avUCP content was downregulated while substrate oxidation returned to control levels. This downregulation of avUCP may have caused increased mitochondrial superoxide production, keeping the superoxide production high in the later stages of heat stress. These results suggest that overproduction of mitochondrial ROS in chicken skeletal muscle under the heat stress might result from enhanced substrate oxidation and downregulation of avUCP in a time-dependent manner.

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Section: Discussionmentioning

confidence: 94%

Sequential changes in superoxide production, anion carriers and substrate oxidation in skeletal muscle mitochondria of heat‐stressed chickens

et al. 2007

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“…Even so, no bird species thus far studied have been shown to possess distinct stores of BAT or a related type of thermogenic tissue [4,5]. However, the relatively increased expression of avUCP in cold-acclimated ducklings has been demonstrated [38], along with an increase of avANT and avUCP mRNA levels in the skeletal muscle of cold-acclimated chickens (4-6°C for 10-12 days) [11]. The present data demonstrate that avUCP expression in the skeletal muscle of cold-exposed chickens initially increased significantly and then decreased slightly, but, unlike UCP3 in rodent skeletal muscle, remained above basal levels ( Fig.…”

Section: Discussionmentioning

confidence: 99%

Possible role for avPGC‐1α in the control of expression of fiber type, along with avUCP and avANT mRNAs in the skeletal muscles of cold‐exposed chickens

et al. 2004

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Peroxisome proliferator-activated receptor c coactivator-1a ( PGC-1a), a transcriptional coactivator, plays a role in mitochondrial biogenesis, muscle fiber specialization, and adaptive thermogenesis. Because of an absence of brown adipose tissue, the skeletal muscle tissue in chickens serves as an important source of thermogenesis to counter the cold. The present experiments were conducted (i) to clone the cDNA of PGC-1a homologs from chicken skeletal muscle and to examine alterations to PGC-1a mRNA expression in the skeletal muscles of cold-exposed chickens, (ii) to study the effect of cold-acclimation on the metabolic fiber phenotype of typically fast-glycolytic (type IIB) pectoralis muscles, and (iii) to compare avANT and avUCP mRNA expression in control and cold-exposed chickens. Results show that the cloned avPGC-1a cDNA encodes a 796 aminoacid protein (GenBank Accession No. AB170013) showing 84% identity with rodent PGC-1a cDNA. Exposure of chickens to a cold environment resulted in the prompt upregulation of avPGC-1a expression, which preceded increments in avUCP and avANT expression in skeletal muscle mitochondria. Consistent with the morphological appearance of muscles, an increase in the number of fast-oxidative-glycolytic (type IIA) fibers in the pectoralis muscle, which contains exclusively type IIB fibers in control chickens, was observed in cold-acclimated chickens. These findings provide novel information about possible regulatory pathways in avian skeletal muscle during thermogenesis.

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“…Increased expression of avUCP in cold-acclimated ducklings [24], chickens [25] and king penguins [26] has been demonstrated. Moreover, we also reported the negative correlation between avUCP content and mitochondrial superoxide production in chicken skeletal muscle during acute heat stress [27].…”

Section: Introductionmentioning

confidence: 96%

“…Although bird species have no distinct stores of BAT or a related type of thermogenic tissue [22,23], a new protein, named avian UCP (avUCP), which shares a 71-73% amino acid identity with both UCP2 and UCP3, was identified in chicken skeletal muscle [24,25]. Increased expression of avUCP in cold-acclimated ducklings [24], chickens [25] and king penguins [26] has been demonstrated.…”

Section: Introductionmentioning

confidence: 99%

Possible role of avian uncoupling protein in down‐regulating mitochondrial superoxide production in skeletal muscle of fasted chickens

et al. 2006

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Little is known about the precise physiological roles of uncoupling protein 1 (UCP1) homologs (UCP2, UCP3, avian UCP) whose levels are up-regulated during fasting. UCPs in skeletal muscle are thought to play a role in the regulation of lipids as fuel substrates, and/or in controlling the production of reactive oxygen species (ROS). The aim of this investigation, using skeletal muscle from fasted chickens, was to examine alterations in the expression of genes encoding for avian UCP and key enzymes relevant to lipid flux across the mitochondrial b-oxidation pathway. We also clarified whether an increase in avUCP content could be associated with altered ROS production by mitochondria. Transcription levels of avUCP and CPT-I genes were increased 7.7-and 9.5-fold after a 24 h fast and slightly diminished but remained about 5.0-and 7.7-fold higher than baseline levels, respectively, after 48 h of fasting. In contrast, members of the b-oxidation pathway, LCAD and 3HADH, were gradually up-regulated from 12 to 48 h of fasting. This suggests that processes involved in the transfer and oxidation of fatty acids are up-regulated differently during the initial stage of fasting. Analysis of ROS production by lucigenin-derived chemiluminescence showed that the FFA-sensitive portion of carboxyatractyloside-upregulated ROS production was greater in skeletal muscle mitochondria from 24 h-fasted chickens compared with control, which leads us to postulate that ROS production is potentially down-regulated by UCP. The possible involvement of a backlog of fatty acid for oxidation, observed in chickens after a 24 h fast, in a transmembrane gradient of free non-oxidized fatty acids is also discussed.

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An uncoupling protein homologue putatively involved in facultative muscle thermogenesis in birds

Cited by 143 publications

References 25 publications

Sequential changes in superoxide production, anion carriers and substrate oxidation in skeletal muscle mitochondria of heat‐stressed chickens

Sequential changes in superoxide production, anion carriers and substrate oxidation in skeletal muscle mitochondria of heat‐stressed chickens

Possible role for avPGC‐1α in the control of expression of fiber type, along with avUCP and avANT mRNAs in the skeletal muscles of cold‐exposed chickens

Possible role of avian uncoupling protein in down‐regulating mitochondrial superoxide production in skeletal muscle of fasted chickens

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