Thyroid status, but not insulin status, affects expression of avian uncoupling protein mRNA in chicken

Abstract

Decuypere. Thyroid status, but not insulin status, affects expression of avian uncoupling protein mRNA in chicken. Am J Physiol Endocrinol Metab 284: E771-E777, 2003. First published December 10, 2002 10.1152/ajpendo.00478.2002The aim of this study was to investigate the hormonal regulation of the avian homolog of mammalian uncoupling protein (avUCP) by studying the impact of thyroid hormones and insulin on avUCP mRNA expression in chickens (Gallus gallus). For 3 wk, chicks received either a standard diet (control group), or a standard diet supplemented with triiodothyronine (T 3; T3 group) or with the thyroid gland inhibitor methimazole (MMI group). A fourth group received injections of the deiodinase inhibitor iopanoic acid (IOP group). During the 4th wk of age, all animals received two daily injections of either human insulin or saline solution. The results indicate a twofold overexpression of avUCP mRNA in gastrocnemius muscle of T3 birds and a clear downregulation (Ϫ74%) in MMI chickens compared with control chickens. Insulin injections had no significant effect on avUCP mRNA expression in chickens. This study describes for the first time induction of avUCP mRNA expression by the thermogenic hormone T 3 in chickens and supports a possible involvement of avUCP in avian thermogenesis. thyroid hormones; thermogenesis; muscle IN MAMMALS, mitochondrial uncoupling proteins (UCPs) are known to uncouple phosphorylation from oxidation and, hence, to be involved in energy metabolism. Brown fat UCP1 has also been reported to be involved in heat production (for review see Ref. 32). The impact of thyroid hormones on UCP expression is well documented (16,23,25), and UCP3 could be one mediator of the thermogenic effect of triiodothyronine (T 3 ) in mammalian skeletal muscle (10). However, the implication of UCP3 in thermogenesis in mammals is controversial (17, 33).As in mammals, T 3 has been reported to have a role in thermoregulatory mechanisms in birds by stimulating heat production (9, 34). However, the involvement of uncoupling mechanisms in such regulation is still unclear. A recent study (31) showed that a UCP homolog called avian (av)UCP is expressed in chicken and duckling muscle. The authors suggest that avUCP is structurally close to mammalian UCP2 and UCP3 but that its function could be nearer to that of UCP1 (expressed exclusively in brown adipose tissue) in mammals. Indeed, the avUCP messenger is overexpressed in cases of cold acclimatization in ducklings and in cockerels from the Rϩ line presenting a high diet-induced thermogenesis (31). Recent results obtained in our laboratory (6) also suggest that the induction of avUCP mRNA expression in cold-exposed chicks is associated with increased plasma T 3 concentrations and heat production. Moreover, avUCP mRNA expression has been shown to be inhibited in chickens early conditioned to heat (37), characterized by low plasma T 3 concentrations (39). However, the influence of thyroid hormones on avUCP expression in chickens has not previously been clearly demonstr...

Acute cold‐ and chronic heat‐exposure upregulate hepatic leptin and muscle uncoupling protein (UCP) gene expression in broiler chickens

“…Cold exposure also increases the expression of UCP in chicken muscle corroborating previous studies in mammals (Boss et al,'97a;Carmona et al,'98) and in birds (Raimbault et al, 2001;Collin et al, 2003a;Talbot et al, 2004;Ueda et al, 2005). This latter observation, in combination with previous findings based on the predominant distribution of UCP in skeletal muscle (Raimbault et al, 2001), and its induction by thyroid hormones (Collin et al, 2003b) and glucagon (the thermogenic hormone in birds) (Raimbault et al, 2001) suggest that UCP may play a pivotal role in non-shivering thermogenesis. The rapidity of leptin and UCP response to cold reported here can appear surprising, but is similar to that due to isoproterenol (non selective b-adrenergic agonist) infusion in humans (Ricci and Fried,'99) supporting a possible shortterm control of leptin and UCP gene expression in chickens.…”

Cold-acclimation-induced non-shivering thermogenesis in birds is associated with upregulation of avian UCP but not with innate uncoupling or altered ATP efficiency

“…By increasing membrane proton conductance, avUCP should decrease the efficiency of the oxidative phosphorylation process, thereby diverting the energy from ATP synthesis to thermogenesis. In line with this idea, avUCP level increased in a situation where energy efficiency is decreased such as in triiodothyronine-treated chickens (Collin et al, 2003b) whereas it was reported to be decreased in hypothyroid chickens (Collin et al, 2003b) or in long-term fasted penguins (Rey et al, 2008) when energy efficiency would increase. Interestingly, a chicken line selected for its low efficiency of food utilization for growth displayed a higher level of avUCP mRNA in their skeletal muscle than a chicken line divergently selected for its high food efficiency (Raimbault et al, 2001;Ojano-Dirain et al, 2007).…”

Endothermy in birds: underlying molecular mechanisms

“…Unlike in muscle, however, reduced thyroid levels did not influence PGC1α gene expression in liver, where it may be induced instead by cAMP and glucocorticoids to controls gluconeogenesis (Yoon et al, 2001). In addition to stimulating PGC1α expression and thereby mitochondrial capacity, thyroid hormones can also control the activity of ANT and UCP (Collin et al, 2003). The downregulation of ANT in liver after induced hypothyroidism indicates a regulatory effect of thyroid hormones on ANT.…”