Uncoupling protein and ATP/ADP carrier increase mitochondrial proton conductance after cold adaptation of king penguins

Abstract

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).

Herba Cistanches stimulates cellular glutathione redox cycling by reactive oxygen species generated from mitochondrial respiration in H9c2 cardiomyocytes

“…The ability of HCF1 pretreatment to partially reverse the mitochondrial GSH depletion induced by I/R challenge likely involved the upregulation of cellular glutathione redox cycling through the intermediacy of mitochondrial ROS production, as was the case in H9c2 cardiomyocytes (Yim & Ko, 1999;Ramires & Ji, 2001). While the reduction of tissue ATP level by long-term, low-dose HCF1 pretreatment in non-I/R rat hearts might be due to the induction of a sustained mitochondrial uncoupling, the significant reduction of tissue ATP level in ischemic/reperfused rat hearts was likely due to the impaired mitochondrial electron transport and oxidative phosphorylation (Talbot et al, 2004;Brennan et al, 2006). The reduced extent of I/Rinduced myocardial ATP depletion in HCF1-pretreated rat hearts, as observed in the present study, was likely related to the increased ATP-GC that compensated the enhanced ATP consumption for cellular homeostasis during reperfusion (Plaschke et al, 1998;Young, 2008).…”

Oxidative phosphorylation efficiency, proton conductance and reactive oxygen species production of liver mitochondria correlates with body mass in frogs

“…However, the loss of the phylogenetic and allometric differences in proton conductance found with liposomes made from the mitochondrial membrane (Brookes et al, 1997) further highlights that the presence of mitochondrial membrane proteins plays an important role in determining proton permeability (Stuart et al, 2001). For example, this has been suggested for the content of adenine nucleotide translocase (Talbot et al, 2004;Brand et al, 2005;Shabalina et al, 2006). In amphibians, some studies have shown that the mitochondrial inner membrane surface area might be greater in the mitochondria of liver and muscle from smaller species (Brookes et al, 1998;Hulbert et al, 2006;Berner et al, 2009).…”

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

“…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].…”