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- Molecular and cellular changes in skin and muscle during metamorphosis of Atlantic halibut (Hippoglossus hippoglossus) are accompanied by changes in deiodinases expressionPublication . Campinho, Marco António; Galay-Burgos, M.; Silva, Nádia; Costa, R. A.; Alves, Ricardo N.; Sweeney, Glen E.; Power, DeborahFlatfish metamorphosis is the most dramatic postnatal developmental event in teleosts. Thyroid hormones (TH), thyroxine (T4) and 3,3′-5′-triiodothyronine (T3) are the necessary and sufficient factors that induce and regulate flatfish metamorphosis. Most of the cellular and molecular action of TH is directed through the binding of T3 to thyroid nuclear receptors bound to promoters with consequent changes in the expression of target genes. The conversion of T4 to T3 and nuclear availability of T3 depends on the expression and activity of a family of 3 selenocysteine deiodinases that activate T4 into T3 or degrade T4 and T3.
- The molecular and endocrine basis of flatfish metamorphosisPublication . Power, Deborah; Einarsdóttir, Ingibjörg E.; Pittman, Karin; Sweeney, Glen E.; Hildahl, Jon; Campinho, Marco António; Silva, Nadia; Saele, Oystein; Galay-Burgos, M.; Smaàradóttir, Heiddis; Björnsson, Björn ThrandurA significant component of aquaculture is the production of good quality larvae, and, in the case of flatfish, this is tied up with the change from a symmetric larva to an asymmetric juvenile. Despite the pioneering work carried out on the metamorphosis of the Japanese flounder (Paralichthys olivaceus) and summer flounder (Paralichthys dentatus), the underlying molecular basis of flatfish metamorphosis is still relatively poorly characterized. It is a thyroid hormone (TH) driven process, and the role of other hormones in the regulation of the process along with the interplay of abiotic factors are still relatively poorly characterized as is the extent of tissue and organ remodeling, which underlie the profound structural and functional modifications that accompany the larval/juvenile transition. The isolation of genes for hormones, receptors, binding proteins, and other accessory factors has provided powerful tools with which to pursue this question. The application of molecular methodologies such as candidate gene approaches and microarray analysis coupled to functional genomics has started to contribute to understanding the complexity of tissue and organ modifications that accompany flatfish metamorphosis. A better understanding of the biology of normal metamorphosis is essential to identify factors contributing to abnormal metamorphosis.
- The goitrogenic efficiency of thioamides in a marine teleost, sea bream (Sparus auratus)Publication . Campinho, Marco António; Morgado, Isabel; Pinto, Patricia IS; Silva, Nádia; Power, DeborahStudies on the role of thyroid hormones (THs) in teleost fish physiology have deployed the synthetic goitrogens, methimazol (MMI), propilthiouracil (PTU) and thiourea (TU) that are used to treat human hyperthyroidism. However, the action of the goitrogens, MMI, PTU and TU at different levels of the hypothalamic–pituitary–thyroid (HPT) axis in teleosts is largely unknown. The central importance of the hypothalamus and pituitary in a number of endocrine regulated systems and the cross-talk that occurs between different endocrine axes makes it pertinent to characterize the effects of MMI, PTU and TU, on several endpoints of the thyroid system. The marine teleost, sea bream (Sparus auratus) was exposed to MMI, PTU and TU (1 mg/kg wet weight per day), via the diet for 21 days. Radioimmunoassays (RIA) of plasma THs and ELISA of the TH carrier transthyretin (TTR) revealed that MMI was the only chemical that significantly reduced plasma TH levels (p < 0.05), although both MMI and PTU significantly (p < 0.05) reduced plasma levels of circulating TTR (p < 0.05). Histological analysis of the thyroid tissue revealed modifications in thyrocyte activity that explain the reduced circulating levels of THs. MMI also significantly (p < 0.05) up-regulated transcript abundance of liver deiodinase 1 and 2 while significantly (p < 0.05) decreasing TRb expression in the pituitary, all hallmarks of HPT axis action of goitrogens in vertebrates. The results indicate that in the sea bream MMI is the most effective goitrogen followed by PTU and that TU (1 mg/kg wet weight for 21 days) failed to have a goitrogenic effect. The study highlights the non-uniform effect of goitrogens on the thyroid axis of sea bream and provides the basis for future studies of thyroid disrupting pollutants.
- Regulation of troponin T expression during muscle development in sea bream Sparus auratus Linnaeus: the potential role of thyroid hormonesPublication . Campinho, Marco António; Sweeney, Glen E.; Power, DeborahIn the sea bream Sparus auratus three stage-specific fast troponin T (fTnT) isoforms have been cloned and correspond to embryonic-, larval- and adult-specific isoforms. Characterisation, using database searches, of the putative genomic organisation of Fugu rubripes and Tetraodon nigroviridis fTnT indicates that alternative exon splicing in the 59 region of the gene generates the different isoforms. Moreover, comparison of teleost fTnTs suggests that alternative splicing of fTnT appears to be common in teleosts. A different temporal expression pattern for each fTnT splice variant is found during sea bream development and probably relates to differing functional demands, as a highly acidic embryonic form (pI 5.16) is substituted by a basic larval form (pI 9.57). Thyroid hormones (THs), which play an important regulatory role in muscle development in flatfish and tetrapods, appear also to influence TnT gene expression in the sea bream. However, THs have a divergent action on different sea bream TnT genes and although the slow isoform (sTnT1) is TH-responsive, fTnT, sTnT2 and the itronless isoform (iTnT) are unaffected. The present results taken together with those published for flatfish seem to suggest differences may exist in the regulation of larval muscle development in teleosts.
- Teleost metamorphosis: the role of thyroid hormonePublication . Campinho, Marco AntónioIn most teleosts, metamorphosis encompasses a dramatic post-natal developmental process where the free-swimming larvae undergo a series of morphological, cellular and physiological changes that enable the larvae to become a fully formed, albeit sexually immature, juvenile fish. In all teleosts studied to date thyroid hormones (TH) drive metamorphosis, being the necessary and sufficient factors behind this developmental transition. During metamorphosis, negative regulation of thyrotropin by thyroxine (T4) is relaxed allowing higher whole-body levels of T4 that enable specific responses at the tissue/cellular level. Higher local thyroid cellular signaling leads to cell-specific responses that bring about localized developmental events. TH orchestrate in a spatial-temporal manner all local developmental changes so that in the end a fully functional organism arises. In bilateral teleost species, the most evident metamorphic morphological change underlies a transition to a more streamlined body. In the pleuronectiform lineage (flatfishes), these metamorphic morphological changes are more dramatic. The most evident is the migration of one eye to the opposite side of the head and the symmetric pelagic larva development into an asymmetric benthic juvenile. This transition encompasses a dramatic loss of the embryonic derived dorsal-ventral and left-right axis. The embryonic dorsal-ventral axis becomes the left-right axis, whereas the embryonic left-right axis becomes, irrespectively, the dorsal-ventral axis of the juvenile animal. This event is an unparalleled morphological change in vertebrate development and a remarkable display of the capacity of TH-signaling in shaping adaptation and evolution in teleosts. Notwithstanding all this knowledge, there are still fundamental questions in teleost metamorphosis left unanswered: how the central regulation of metamorphosis is achieved and the neuroendocrine network involved is unclear; the detailed cellular and molecular events that give rise to the developmental processes occurring during teleost metamorphosis are still mostly unknown. Also in flatfish, comparatively little is still known about the developmental processes behind asymmetric development. This review summarizes the current knowledge on teleost metamorphosis and explores the gaps that still need to be challenged.
- Molecular, cellular and histological changes in skin from a larval to an adult phenotype during bony fish metamorphosisPublication . Campinho, Marco António; Silva, Nadia; Sweeney, Glen E.; Power, DeborahDevelopmental models for skin exist in terrestrial and amphibious vertebrates but there is a lack of information in aquatic vertebrates. We have analysed skin epidermal development of a bony fish (teleost), the most successful group of extant vertebrates. A specific epidermal type I keratin cDNA (hhKer1), which may be a bony-fishspecific adaptation associated with the divergence of skin development (scale formation) compared with other vertebrates, has been cloned and characterized. The expression of hhKer1 and collagen 1α1 in skin taken together with the presence or absence of keratin bundle-like structures have made it possible to distinguish between larval and adult epidermal cells during skin development. The use of a flatfish with a well-defined larval to juvenile transition as a model of skin development has revealed that epidermal larval basal cells differentiate directly to epidermal adult basal cells at the climax of metamorphosis. Moreover,hhKer1 expression is downregulated at the climax of metamorphosis and is inversely correlated with increasing thyroxin levels. We suggest that, whereas early mechanisms of skin development between aquatic and terrestrial vertebrates are conserved, later mechanisms diverge.
- Coordination of deiodinase and thyroid hormone receptor expression during the larval to juvenile transition in sea bream (Sparus aurata, Linnaeus)Publication . Campinho, Marco António; Galay-Burgos, M.; Sweeney, Glen E.; Power, DeborahTo test the hypothesis that THs play an important role in the larval to juvenile transition in the marine teleost model, sea bream (Sparus auratus), key elements of the thyroid axis were analysed during development. Specific RT-PCR and Taqman quantitative RT-PCR were established and used to measure sea bream iodothyronine deiodinases and thyroid hormone receptor (TR) genes, respectively. Expression of deiodinases genes (D1 and D2) which encode enzymes producing T3, TRs and T4 levels start to increase at 20–30 days post-hatch (dph; beginning of metamorphosis), peak at about 45 dph (climax) and decline to early larval levels after 90–100 dph (end of metamorphosis) when fish are fully formed juveniles. The profile of these different TH elements during sea bream development is strikingly similar to that observed during the TH driven metamorphosis of flatfish and suggests that THs play an analogous role in the larval to juvenile transition in this species and probably also in other pelagic teleosts. However, the effect of T3 treatment on deiodinases and TR transcript abundance in sea bream is not as clear cut as in larval flatfish and tadpoles indicating divergence in the responsiveness of TH axis elements and highlighting the need for further studies of this axis during development of fish.
- Editorial: the role of thyroid hormones in vertebrate development, volume IIPublication . Campinho, Marco António; Sachs, Laurent M.The thyroid hormone is an important signaling molecule system involved in vertebrate development, acting at the embryonic and post-embryonic levels (1). Although this has long been established, a detailed understanding of the thyroid hormone’s developmental action still needs to be fully understood. The present Frontiers in Endocrinology Research Topic aims to close this knowledge gap by bringing together a collection of papers addressing what is known and the challenges ahead on the role of thyroid hormones in vertebrate development, from teleosts to humans. The published manuscripts highlight the pivotal action of thyroid hormones in vertebrate neurodevelopment (Lee at al.; Ng et al.; O’Shaughnessy et al.; Richard et al.; Silva and Campinho; Valcárcel-Hernández et al.), post natal development in amphibians (8–10) and how thyroid disorders can affect human development (Ru et al.; SeyedAlinaghi et al.).