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

Journal article
Authors R. N. Alves
Kristina Sundell
L. Anjos
Henrik Sundh
T. Harboe
B. Norberg
D. M. Power
Published in Cell and Tissue Research
Volume 372
Issue 3
Pages 469-492
ISSN 0302-766X
Publication year 2018
Published at Department of Biological and Environmental Sciences
Pages 469-492
Language en
Links doi.org/10.1007/s00441-018-2794-1
Keywords Metamorphosis, Skin development, Asymmetry, Mucins, Na+,K+-ATPase, mitochondria-rich cells, pleuronectes-platessa-l, seabream, sparus-aurata, gilthead sea bream, early-life stages, chloride cells, solea-senegalensis, epidermal mucus, eye migration, developmental, sequence
Subject categories Cell Biology

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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