Cold-acclimation-induced non-shivering thermogenesis in birds is associated with upregulation of avian UCP but not with innate uncoupling or altered ATP efficiency
Abstract:) were obtained from a commercial stockbreeder (Eclosion Grimaud-lacorbière, Roussay, France). Birds were fed ad libitum with commercial mash (Moulin Guenard, 645000MI, Vonnas, France) and had free access to water. From the age of 10 days, ducklings were caged for Accepted 7 April 2010 SUMMARY Despite their lack of brown adipose tissue, some bird species develop regulatory non-shivering thermogenesis (NST) of skeletal muscle origin in response to cold acclimation. Mechanisms involved in avian NST are still unc… Show more
“…Altogether these data suggest that the sympathetic nervous system (norepinephrine) may modulate facultative thermogenesis in birds. This idea is also in line with recently published data suggesting that the beta-adrenergic system would be involved in regulating the expression of avian uncoupling protein (Joubert et al 2010(Joubert et al , 2011, a mitochondrial protein that has been linked to the intensity of regulatory thermogenesis in cold-acclimated ducklings (Teulier et al 2010). Whether guanethidine-treated ducklings displayed a lower expression of avian UCP is currently not known but deserves further study.…”
Abstract.Here we investigate the possible involvement of the sympathetic nervous system in the respiratory properties of intermyofibrillar and subsarcolemmal mitochondrial populations from heart and gastrocnemius muscles. Mitochondrial oxidative phosphorylation was assessed polarographically by using succinate (plus rotenone), and ascorbate plus N,N,N' ,N'-tetramethyl-p-phenyl-enediamine (plus antimycin) as respiratory substrates. We report that chronic chemical sympathectomy with guanethidine (150 mg/kg, daily for 3 weeks) induced a marked decrease in whole body metabolic and heart rates, in plasma metabolites (fatty acids and glucose) and norepinephrine levels. Guanethidine treatment decreased mainly the oxidative phosphorylation capacity of subsarcolemmal mitochondria in heart, irrespective of the substrate used. In contrast, both mitochondrial populations were affected by the treatment in skeletal muscle. This suggests that sympathetic nervous system activity can alter the energetic status of muscle cells, and to some extent play a thermogenic role in birds.
“…Altogether these data suggest that the sympathetic nervous system (norepinephrine) may modulate facultative thermogenesis in birds. This idea is also in line with recently published data suggesting that the beta-adrenergic system would be involved in regulating the expression of avian uncoupling protein (Joubert et al 2010(Joubert et al , 2011, a mitochondrial protein that has been linked to the intensity of regulatory thermogenesis in cold-acclimated ducklings (Teulier et al 2010). Whether guanethidine-treated ducklings displayed a lower expression of avian UCP is currently not known but deserves further study.…”
Abstract.Here we investigate the possible involvement of the sympathetic nervous system in the respiratory properties of intermyofibrillar and subsarcolemmal mitochondrial populations from heart and gastrocnemius muscles. Mitochondrial oxidative phosphorylation was assessed polarographically by using succinate (plus rotenone), and ascorbate plus N,N,N' ,N'-tetramethyl-p-phenyl-enediamine (plus antimycin) as respiratory substrates. We report that chronic chemical sympathectomy with guanethidine (150 mg/kg, daily for 3 weeks) induced a marked decrease in whole body metabolic and heart rates, in plasma metabolites (fatty acids and glucose) and norepinephrine levels. Guanethidine treatment decreased mainly the oxidative phosphorylation capacity of subsarcolemmal mitochondria in heart, irrespective of the substrate used. In contrast, both mitochondrial populations were affected by the treatment in skeletal muscle. This suggests that sympathetic nervous system activity can alter the energetic status of muscle cells, and to some extent play a thermogenic role in birds.
“…Six were assigned randomly to each of the two acclimation temperature groups. The ages of the ducklings at the beginning of the trial was five weeks and had been housed at their acclimation temperatures since 10 days of age: TN ducklings were housed at 258C and CA ducklings were housed at 58C following similar published protocols [30]. Ducklings varied in mass throughout the experiments, although at the outset of the measurement period the 12 ducklings chosen for the measurements were sizematched such that both acclimation groups had an average starting mass of approximately 1 kg.…”
Section: Materials and Methods (A) Animalsmentioning
confidence: 99%
“…The 0.5 value in the equation above is included to account for the fact that absolute temperature differences include both the decreases in T b as well as the increases over time, which would be symmetrical over a 24-h period in a homeothermic animal. These values were normalized to previously measured basal metabolic heat production (5 W kg 21 and 8 W kg 21 for 258C and 58C acclimated ducklings; [30,31]). …”
Section: (D) Incremental Cost Of Homeothermymentioning
confidence: 99%
“…The metabolic costs associated with the periodic rises in T b were typically higher in cold-acclimated ducklings, but declined more profoundly during fasting. The metabolic costs are not insubstantial; when expressed as a portion of basal metabolic rate [30] are between 7 and 11%.…”
This study aimed to examine thermoregulatory responses in birds facing two commonly experienced stressors, cold and fasting. Logging devices allowing long-term and precise access to internal body temperature were placed within the gizzards of ducklings acclimated to cold (CA) (58C) or thermoneutrality (TN) (258C). The animals were then examined under three equal 4-day periods: ad libitum feeding, fasting and re-feeding. Through the analysis of daily as well as short-term, or ultradian, variations of body temperature, we showed that while ducklings at TN show only a modest decline in daily thermoregulatory parameters when fasted, they exhibit reduced surface temperatures from key sites of vascular heat exchange during fasting. The CA birds, on the other hand, significantly reduced their short-term variations of body temperature while increasing long-term variability when fasting. This phenomenon would allow the CA birds to reduce the energetic cost of body temperature maintenance under fasting. By analysing ultradian regulation of body temperature, we describe a means by which an endotherm appears to lower thermoregulatory costs in response to the combined stressors of cold and fasting.
“…The mitochondrial oxidative phosphorylation efficiency was determined from the rate of ATP synthesis and oxygen consumption of isolated tadpole mitochondria (3mgml -1 ) respiring on succinate (5mmoll -1 plus 5mmoll -1 rotenone) in the respiratory medium supplemented with an ADP-regenerating system consisting of 1.5Uml -1 hexokinase, 20mmoll -1 glucose and two different concentrations of ) as previously described (Rigoulet et al, 1998;Nogueira et al, 2001;Clerc et al, 2007;Salin et al, 2010;Teulier et al, 2010).…”
Section: Mitochondrial Respiration and Oxidative Phosphorylation Effimentioning
SUMMARYMitochondria are known to play a central role in life history processes, being the main source of reactive oxygen species (ROS), which promote oxidative constraint. Surprisingly, although the main role of the mitochondria is to produce ATP, the plasticity of mitochondrial ATP generation has received little attention in life history studies. Yet, mitochondrial energy transduction represents the physiological link between environmental resources and energy allocated to animal performance. Studying both facets of mitochondrial functioning (ATP and ROS production) would allow better understanding of the proximate mechanisms underlying life history. We have experimentally modulated the mitochondrial capacity to generate ROS and ATP during larval development of Rana temporaria tadpoles, via chronic exposure (34days) to a mitochondrial uncoupler (2,4-dinitrophenol, dNP). The aim was to better understand the impact of mitochondrial uncoupling on both responses in terms of oxidative balance, energy input (oxygen and feeding consumption) and energy output (growth and development of the tadpole). Exposure to 2,4-dNP reduced mitochondrial ROS generation, total antioxidant defences and oxidative damage in treated tadpoles compared with controls. Despite the beneficial effect of dNP on oxidative status, development and growth rates of treated tadpoles were lower than those in the control group. Treatment of tadpoles with 2,4-dNP promoted a mild mitochondrial uncoupling and enhanced metabolic rate. These tadpoles did not increase their food consumption, and thus failed to compensate for the energy loss elicited by the decrease in the efficiency of ATP production. These data suggest that the cost of ATP production, rather than the oxidative balance, is the parameter that constrains growth/development of tadpoles, highlighting the central role of energy transduction in larval performance.
Supplementary material available online at
scite is a Brooklyn-based organization that helps researchers better discover and understand research articles through Smart Citations–citations that display the context of the citation and describe whether the article provides supporting or contrasting evidence. scite is used by students and researchers from around the world and is funded in part by the National Science Foundation and the National Institute on Drug Abuse of the National Institutes of Health.