Iodothyronine deiodinases and thyroid hormone receptors regulation during flatfish (Solea senegalensis) metamorphosis

Abstract

Thyroid hormone-induced metamorphosis seems to represent an ancestral feature of chrordates (urochordates, cephalochordates and vertebrates), but also of nonchordate animals. Although thyroid hormones and thyroid hormone receptor profiles during metamorphosis have been analyzed in different vertebrate taxa, including fish, developmental expression and activity of type 2 (dio2, D2) and type 3 (dio3, D3) iodothyronine deiodinases, two key enzymes in anuran metamorphosis, remain unknown in any fish species. The aim of this work was to investigate the development of thyroid hormone system during the metamorphosis of a flatfish species, the Senegalese sole, focusing on the deiodinases developmental profile. We have cloned sole D2 and D3 and analyzed several parameters of thyroid hormones system in pre-, early-, middle-, and late-metamorphic larvae. Both deiodinases contain in their catalytic centers an UGA triplet encoding for a selenocystein (Sec) residue as expected. Left eye migration and rotation in body position were associated with a significant increase in both thyroid hormones and thyroid hormone receptors at the middle-late metamorphic stages. Although dio2 expression slightly increased during metamorphosis, D2 activity augmentation was much more significant. Sole dio3 expression declined only slightly, whereas the D3 activity clearly decreased at mid-late metamorphic period. This developmental profile of deiodinases sustained the rise of thyroid hormones levels observed during sole metamorphosis. No clear cut daily rhythms were observed in the parameters analyzed although it seemed that thyroid hormone system was more active during daytime, in particular at late metamorphic stages. These developmental changes point out the importance not only of thyroid hormones and their receptors but also of dio2 and dio3 in mediating flatfish metamorphosis, as it has been described in amphibians.

Iodothyronine deiodinases: a functional and evolutionary perspective

“…Another conspicuous functional distinction between D1/D3 and D2 is the fact that the latter exhibits a remarkable circadian rhythm entrained by the light/dark cycle. This rhythmicity has been documented in teleosts (García-G et al 2004, Isorna et al 2009), birds (Yoshimura et al 2003), and mammals (Luna et al 1995, reviewed in Gereben et al (2008) in several neuroendocrine structures, such as the hypothalamus, pituitary, pineal, and adrenal glands, as well as in brown adipose tissue, liver, Harderian gland, and cerebral cortex. Furthermore, recent studies support the notion that D2 expression in hypothalamic tanycytes is an important factor in regulation of seasonal reproduction both in mammals and birds (Williams & Duncan Bassett 2011, Ikegami & Yoshimura 2012.…”

Expression patterns of type II and III iodothyronine deiodinase genes in the liver of the goldlined spinefoot, Siganus guttatus

“…The difficulty in obtaining such a fragment may be partially attributable to the occurrence of long introns; it has been reported in mammals that the 3 0 UTR of D2 has long introns (8.1-8.5 kb) within two exons [36]. Similar incomplete sequences have been reported for D2 of the Senegalese sole [37] and mummichog [38] and considered to be due to either the lack of an extended 3 0 UTR (up to 7.5 kb in length) including the SECIS structure [39] or the fragment being a splice variant [37]. The full sequence of mummichog D2 cDNA was later cloned and a SECIS element was found within the 4652 bp region with an intron divided by a 4.8 kb exon [40].…”

“…To the best of our knowledge, daily variations of iodothyronine deiodinase transcript levels have only been reported in the late metamorphic stages of the Senegalese sole [37]; D3 transcript levels in larval homogenates were measured using qPCR and found to significantly increase from Zeitgeber time (ZT) 7 to ZT12 and then decrease from ZT12 to ZT24. The results of our study clearly show that the abundance of SgD2 and SgD3 mRNA in several tissues was higher at 1200 hours than at 2400 hours, suggesting that TH levels fluctuate daily.…”

Thyroid hormone deiodinase type 2 mRNA levels in sea lamprey (Petromyzon marinus) are regulated during metamorphosis and in response to a thyroid challenge

“…Sequence ( [20]), sea bream (Sparus aurata; [10]) and rabbitfish (Siganus guttatus; [39]). The characteristic hairpin secondary structure of the SECIS element, the prevalence of repeating sequences, and the overall length of the 3 0 UTR sequence have all been suggested as reasons for the many difficulties experienced in cloning D2.…”

“…Likewise, distinct temporal and spatial patterns of deiodinase gene expression or activity are observed during the development of a variety of fishes including zebrafish, Atlantic salmon, rainbow trout, and Senegalese sole [20,30]. Tissue-specific regulation of TH levels by deiodinases has been suggested as a mechanism to account for the differences in lamprey serum TH profiles compared to other metamorphosing vertebrates [12,13].…”