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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 expression

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Abstract

Flatfish metamorphosis is the most dramatic post-natal 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. We have investigated the role of deiodinases in skin and muscle metamorphic changes in halibut. We show that, both at the whole body level and at the cellular level in muscle and skin of the Atlantic halibut (Hippoglossus hippoglossus) during metamorphosis, the coordination between activating (D2) and deactivating (D3) deiodinases expression is strongly correlated with the developmental TH-driven changes. The expression pattern of D2 and D3 in cells of both skin and muscle indicate that TH are necessary for the maintenance of larval metamorphic development and juvenile cell types in these tissues. No break in symmetry occurs in the expression of deiodinases and in metamorphic developmental changes occurring both in trunk skin and muscle. The findings that two of the major tissues in both larvae and juveniles maintain their symmetry throughout metamorphosis suggest that the asymmetric changes occurring during flatfish metamorphosis are restricted to the eye and head region.

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Acknowledgement

We thank Heiddis Smáradóttir of Fiskeldi Eyjafjarðar, IS-600 Akureyri, Iceland, for providing the halibut samples.

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Authors and Affiliations

  1. Comparative and Molecular Endocrinology Group, Centre for Marine Sciences (CCMAR), Universidade do Algarve, Campus de Gambelas, 8005-139, Faro, Portugal

    M. A. Campinho, N. Silva, R. A. Costa, R. N. Alves & D. M. Power

  2. ECETOC, European Centre for Ecotoxicology and Toxicology of Chemicals, 4 avenue E. Van Nieuwenhuyse, B-1160, Brussels, Belgium

    M. Galay-Burgos

  3. School of Biosciences, Cardiff University, Cardiff, Wales, UK

    G. E. Sweeney

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  1. M. A. Campinho
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  2. M. Galay-Burgos
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  3. N. Silva
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  5. R. N. Alves
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Correspondence to M. A. Campinho.

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This project was supported by the European Community project, LIFECYCLE (222719-2) and the Portuguese Ministry of Science (FCT; project PDCT/MAR/115005/2009). M.A.C. was sponsored by the Portuguese Ministry of Science (grant no. SFRH/BPD/66808/2009).

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Figure S1

Halibut D1 (a) and D3 (b) cDNA sequences and predicted protein sequences. Double-underlining in a represents the TGA Sec insertion codon. In a, b, single underlining represents the putative polyadenylation signal; sequences in bold represent the SECISearch-predicted SECIS element (star termination codon). SECISearch predicted hhD1 (a’) and hhD3 (b’) SECIS element. Boxed regions in a’ and b’ represent the SECIS core, while bold letters represent conserved SECIS nucleotides. Halibut D2 RT-PCR isolated nucleotide and predicted peptide sequences (c). Double underlining in c represents the TGA Sec insertion codon and boxed amino acids represent characteristic conserved vertebrate D2 amino acids. (JPEG 480 kb)

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Figure S2

In situ hybridization experiments on halibut larvae sections from stages 5 (a), 7 (b), 9 (c) and 10 (d) hybridized with hhD2 (c, d) or hhD3 (a, b) sense probes. Bar 10 μm. (JPEG 1105 kb)

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Campinho, M.A., Galay-Burgos, M., Silva, N. et al. Molecular and cellular changes in skin and muscle during metamorphosis of Atlantic halibut (Hippoglossus hippoglossus) are accompanied by changes in deiodinases expression. Cell Tissue Res 350, 333–346 (2012). https://doi.org/10.1007/s00441-012-1473-x

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  • DOI: https://doi.org/10.1007/s00441-012-1473-x

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