Abstract
BackgroundExposure of the American bullfrog Lithobates catesbeianus tadpoles to low temperature affects many biological processes including lipid metabolism and the thyroid hormone (TH) signaling pathway, resulting in arrest of TH-induced metamorphosis. To clarify what molecular events occur in this phenomenon, we investigated the glycerophospholipid and fatty acid (FA) compositions, the activities of mitochondrial enzymes and the transcript levels of related genes in the liver of control (26 °C) and cold-treated (4 °C) tadpoles with or without 5 nM 3,3′,5-triiodothyronine (T3).ResultsExposure to T3 decreased the tail height and polyunsaturation of FAs in the glycerophospholipids, and increased plasma glucose levels and transcript levels of primary TH-response genes including TH receptor, and some energy metabolic (cox4, srebp1 and fas) and FA chain elongase genes (elovl3 and elovl5). However, these T3-induced responses were abolished at 4 °C. Exposure to cold temperature enhanced plasma glucose, triglyceride and free FA levels, monounsaturation of FAs, mitochondrial enzymes activities (cytochrome c oxidase and carnitine palmitoyltransferase; U/g liver), with the upregulation of the genes involved in glycogenolysis (pygl), gluconeogenesis (pck1 and g6pc2), FA β-oxidation (acadl), and cholesterol uptake and synthesis (hmgcr, srebp2 and ldlr1), glycerophospholipids synthesis (pcyt1, pcyt2, pemt, and pparg), and FA monounsaturation (scd1) and chain elongation (elovl1 and elovl2). T3 had little effect on the cold-induced changes.ConclusionsOur study demonstrated that exposures to T3 and cold temperature exert different effects on lipid metabolism, resulting in changes in the FA composition in glycerophospholipids, and suggests that a cold-induced signal may block TH-signaling pathway around primary TH-response genes.Electronic supplementary materialThe online version of this article (doi:10.1186/s13578-016-0087-5) contains supplementary material, which is available to authorized users.
Highlights
Exposure of the American bullfrog Lithobates catesbeianus tadpoles to low temperature affects many biological processes including lipid metabolism and the thyroid hormone (TH) signaling pathway, resulting in arrest of TH-induced metamorphosis
In tadpoles that were not exposed to T3, exposure to cold temperature did not affect these morphological parameters at day 3 or 7 (Additional file 1: Table S1)
The present study demonstrates that exposures to T3 and cold temperature for up to 7 days have different effects on components of membrane lipids with dynamic changes in transcript levels for energy/carbohydrate/ lipid metabolism (Table 2)
Summary
Exposure of the American bullfrog Lithobates catesbeianus tadpoles to low temperature affects many biological processes including lipid metabolism and the thyroid hormone (TH) signaling pathway, resulting in arrest of TH-induced metamorphosis. Findings from recent in vivo and in vitro studies revealed that transcription of the TH-response genes TRβ (a primary TH-response gene) and ornithine transcarbamylase (a secondary THresponse gene) remains at basal levels when L. catesbeianus tadpoles and cells are exposed to cold temperature (4 °C) in the presence of T3 for 3‒6 days [3, 5]. Findings from a recent report demonstrated that T3 and its metabolite 3,5-diiodothyronine affected swimming performance, metabolic rate, and tissue-specific regulatory enzyme activities, depending on the actual temperature and thermal history of the zebrafish [6]. Whether TH signaling is completely blocked when tadpole metamorphosis is arrested by exposure to cold temperature is not known
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