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Structural and functional maturation of skin during metamorphosis in the Atlantic halibut (Hippoglossus hippoglossus)

Abstract

To establish if the developmental changes in the primary barrier and osmoregulatory capacity of Atlantic halibut skin are modified during metamorphosis, histological, histochemical, gene expression and electrophysiological measurements were made. The morphology of the ocular and abocular skin started to diverge during the metamorphic climax and ocular skin appeared thicker and more stratified. Neutral mucins were the main glycoproteins produced by the goblet cells in skin during metamorphosis. Moreover, the number of goblet cells producing neutral mucins increased during metamorphosis and asymmetry in their abundance was observed between ocular and abocular skin. The increase in goblet cell number and their asymmetric abundance in skin was concomitant with the period that thyroid hormones (THs) increase and suggests that they may be under the control of these hormones. Several mucin transcripts were identified in metamorphosing halibut transcriptomes and Muc18 and Muc5AC were characteristic of the body skin. Na+, K+-ATPase positive (NKA) cells were observed in skin of all metamorphic stages but their number significantly decreased with the onset of metamorphosis. No asymmetry was observed between ocular and abocular skin in NKA cells. The morphological changes observed were linked to modified skin barrier function as revealed by modifications in its electrophysiological properties. However, the maturation of the skin functional characteristics preceded structural maturation and occurred at stage 8 prior to the metamorphic climax. Treatment of Atlantic halibut with the THs disrupter methimazole (MMI) affected the number of goblet cells producing neutral mucins and the NKA cells. The present study reveals that the asymmetric development of the skin in Atlantic halibut is TH sensitive and is associated with metamorphosis and that this barrier’s functional properties mature earlier and are independent of metamorphosis.

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This research study was funded by the European Community FP7 project LIFECYCLE (FP7 222719, http://www.lifecycle.gu.se/, 17.08.2012) and the European Regional Development Fund (ERDF) COMPETE—Operational Competitiveness Programme and Portuguese funds through the Foundation for Science and Technology (FCT), Portugal (project Pest-C/MAR/LA0015/2013). RNA and LA were funded by FCT Portugal (SFRH/BD/69209/2010 and SFRH/BPD/79105/2011, respectively).

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Contributions

DMP, KSS and BN designed the study. TH ran the halibut experiments and sampling. RNA carried out the analyses, KSS and HS ran the electrophysiology and LA assisted in the immunohistochemistry. RNA, DMP, KSS, HS and LA contributed to the critical interpretation of the data. RNA, DMP and KSS drafted the MS. All authors contributed to the writing of the manuscript and critically read and approved the final version.

Corresponding author

Correspondence to Deborah M. Power.

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The authors declare that they have no competing interests.

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Alves, R.N., Sundell, K.S., Anjos, L. et al. Structural and functional maturation of skin during metamorphosis in the Atlantic halibut (Hippoglossus hippoglossus). Cell Tissue Res 372, 469–492 (2018). https://doi.org/10.1007/s00441-018-2794-1

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Keywords

  • Metamorphosis
  • Skin development
  • Asymmetry
  • Mucins
  • Na+,K+-ATPase