Thyroid hormone actions are temperature-specific and regulate thermal acclimation in zebrafish (Danio rerio)

Abstract

BackgroundThyroid hormone (TH) is best known for its role in development in animals, and for its control of metabolic heat production (thermogenesis) during cold acclimation in mammals. It is unknown whether the regulatory role of TH in thermogenesis is derived in mammals, or whether TH also mediates thermal responses in earlier vertebrates. Ectothermic vertebrates show complex responses to temperature variation, but the mechanisms mediating these are poorly understood. The molecular mechanisms underpinning TH action are very similar across vertebrates, suggesting that TH may also regulate thermal responses in ectotherms. We therefore aimed to determine whether TH regulates thermal acclimation in the zebrafish (Danio rerio). We induced hypothyroidism, followed by supplementation with 3,5-diiodothyronine (T2) or 3,5,3′-triiodothyronine (T3) in zebrafish exposed to different chronic temperatures. We measured whole-animal responses (swimming performance and metabolic rates), tissue-specific regulatory enzyme activities, gene expression, and free levels of T2 and T3.ResultsWe found that both T3 and the lesser-known T2, regulate thermal acclimation in an ectotherm. To our knowledge, this is the first such study to show this. Hypothyroid treatment impaired performance measures in cold-acclimated but not warm-acclimated individuals, whereas supplementation with both TH metabolites restored performance. TH could either induce or repress responses, depending on the actual temperature and thermal history of the animal.ConclusionsThe low sensitivity to TH at warm temperatures could mean that increasing temperatures (that is, global warming) will reduce the capacity of animals to regulate their physiologies to match demands. We suggest that the properties that underlie the role of TH in thermal acclimation (temperature sensitivity and metabolic control) may have predisposed this hormone for a regulatory role in the evolution of endothermy.

3,5-di-iodothyronine stimulates tilapia growth through an alternate isoform of thyroid hormone receptor β1

“…A major finding in this study consists in the demonstration that, through interacting with a specific and distinct TRb1 isoform, T 2 effectively triggers an outburst of body growth in tilapia fingerlings, with an efficiency comparable to that of T 3 . These results confirm and extend previous reports from our laboratory and others suggesting that T 2 is also an important transcriptional regulator, at least in teleosts (García-G et al 2004, 2007, Little et al 2013, Mendoza et al 2013. The lack of available data on circulating or intratissular T 2 concentrations has masked the importance of this TH.…”

“…The lack of available data on circulating or intratissular T 2 concentrations has masked the importance of this TH. However, very recent studies have shown that zebrafish intramuscular T 2 concentrations closely resemble those of T 3 (Little et al 2013). These data together with our previous findings that T 2 preferentially binds to and activates the L-TRb1, an isoform that is expressed in vivo at 10 6 -fold higher levels than S-TRb1, support the notion that, at least in teleosts, T 2 is physiologically relevant ( Mendoza et al 2013).…”

“…Furthermore, the administration protocol had a positive effect on fish growth and no negative effects on fish survival, while it induced a burst in growth of w30% in both T 3 -and T 2 -treated fish (Table 2). Most importantly, the low TH concentrations used did not alter the thyroidal homeostasis of the fish, as judged by the intrahepatic T 3 levels, which were similar to those recently reported for intramuscular zebrafish T 3 and T 2 (1.8G0.2 and 2.8G0.4 ng/g respectively; Little et al 2013). Indeed, despite the fact that intrahepatic T 3 concentrations remained within the euthyroid range in all tilapia treated with the different THs, only fish treated with 1 nM T 3 or T 2 presented a four fold body weight gain compared with the control group (P!0.001; Fig.…”

The Behavior-Physiology Nexus: Behavioral and Physiological Compensation Are Relied on to Different Extents between Seasons

“…Although the thermal quality of the habitat is low in winter, warm days are scattered throughout the season, and these recurring opportunities, albeit unpredictable, may form part of the information acquired by these organisms. Increased metabolism (perhaps regulated via thyroid hormone; Little et al 2013) may enable rapid cellular responses to enhance performance in changing environmental conditions (Clarke and Fraser 2004). Indeed, metabolic cold compensation has been reported for other temperate species that remain active in winter (Roberts 1968;Dutton and Fitzpatrick 1974;Davies et al 1981;Tsuji 1988b).…”

Oxygen- and capacity-limited thermal tolerance: bridging ecology and physiology

“…For example, hypoxia-inducible factor 1 (HIF-1) contributes to improving anaerobic capacity as well as oxygen supply through erythropoesis and may, thereby, enhance the capacity for heat and cold endurance. Cold adaptation may be supported by thyroid hormones (Little et al, 2013). Depending on the animal phylum, these changes contribute to adjustments of oxygen-transport capacity by both ventilation and circulation (invertebrates) or mainly circulation (fishes), as well as to adjustments in mitochondrial density, capacity, oxygen demand and energy budget (all tissues).…”