Auto-Adhesion Potential of Extraocular Aqp0 during Teleost Development

AQP0 water channels are the most abundant proteins expressed in the mammalian lens fiber membranes where they are essential for lens development and transparency. Unlike other aquaporin paralogs, mammalian AQP0 has a low intrinsic water permeability, but can form cell-to-cell junctions between the l...

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Published in:PLOS ONE
Main Authors: Chauvigné, Francois, Fjelldal, Per Gunnar, Cerdà, Joan, Finn, Roderick Nigel
Format: Article in Journal/Newspaper
Language:English
Published: PLoS 2016
Subjects:
Online Access:https://hdl.handle.net/1956/12874
https://doi.org/10.1371/journal.pone.0154592
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author Chauvigné, Francois
Fjelldal, Per Gunnar
Cerdà, Joan
Finn, Roderick Nigel
author_facet Chauvigné, Francois
Fjelldal, Per Gunnar
Cerdà, Joan
Finn, Roderick Nigel
author_sort Chauvigné, Francois
collection University of Bergen: Bergen Open Research Archive (BORA-UiB)
container_issue 5
container_start_page e0154592
container_title PLOS ONE
container_volume 11
description AQP0 water channels are the most abundant proteins expressed in the mammalian lens fiber membranes where they are essential for lens development and transparency. Unlike other aquaporin paralogs, mammalian AQP0 has a low intrinsic water permeability, but can form cell-to-cell junctions between the lens fibers. It is not known whether the adhesive properties of AQP0 is a derived feature found only in mammals, or exists as a conserved ancestral trait in non-mammalian vertebrates. Here we show that a tetraploid teleost, the Atlantic salmon, expresses four Aqp0 paralogs in the developing lens, but also expresses significant levels of aqp0 mRNAs and proteins in the epithelia of the pronephros, presumptive enterocytes, gill filament and epidermis. Quantitative PCR reveals that aqp0 mRNA titres increase by three orders of magnitude between the onset of somitogenesis and pigmentation of the eye. Using in situ hybridization and specific antisera, we show that at least two of the channels (Aqp0a1, -0b1 and/or -0b2) are localized in the extraocular basolateral and apical membranes, while Aqp0a2 is lens-specific. Heterologous expression of the Aqp0 paralogs in adhesion-deficient mouse fibolast L-cells reveals that, as for human AQP0, each intact salmon channel retains cell-to-cell adhesive properties. The strongest Aqp0 interactions are auto-adhesion, suggesting that homo-octamers likely form the intercellular junctions of the developing lens and epithelial tissues. The present data are thus the first to show the adhesion potential of Aqp0 channels in a non-mammalian vertebrate, and further uncover a novel extraocular role of the channels during vertebrate development. publishedVersion
format Article in Journal/Newspaper
genre Atlantic salmon
genre_facet Atlantic salmon
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institution Open Polar
language English
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op_doi https://doi.org/10.1371/journal.pone.0154592
op_relation Norges forskningsråd: 224816
Norges forskningsråd: 254872
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https://hdl.handle.net/1956/12874
https://doi.org/10.1371/journal.pone.0154592
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op_rights Attribution CC BY
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publisher PLoS
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spelling ftunivbergen:oai:bora.uib.no:1956/12874 2025-01-16T21:04:45+00:00 Auto-Adhesion Potential of Extraocular Aqp0 during Teleost Development Chauvigné, Francois Fjelldal, Per Gunnar Cerdà, Joan Finn, Roderick Nigel 2016-08-03T13:16:30Z application/pdf https://hdl.handle.net/1956/12874 https://doi.org/10.1371/journal.pone.0154592 eng eng PLoS Norges forskningsråd: 224816 Norges forskningsråd: 254872 urn:issn:1932-6203 https://hdl.handle.net/1956/12874 https://doi.org/10.1371/journal.pone.0154592 cristin:1354505 Attribution CC BY https://creativecommons.org/licenses/by/4.0/ Copyright 2016 the authors Embryos Fishes immune serum VDP::Matematikk og naturvitenskap: 400::Basale biofag: 470::Cellebiologi: 471 VDP::Mathematics and natural scienses: 400::Basic biosciences: 470::Cell biology: 471 Peer reviewed Journal article 2016 ftunivbergen https://doi.org/10.1371/journal.pone.0154592 2023-03-14T17:44:07Z AQP0 water channels are the most abundant proteins expressed in the mammalian lens fiber membranes where they are essential for lens development and transparency. Unlike other aquaporin paralogs, mammalian AQP0 has a low intrinsic water permeability, but can form cell-to-cell junctions between the lens fibers. It is not known whether the adhesive properties of AQP0 is a derived feature found only in mammals, or exists as a conserved ancestral trait in non-mammalian vertebrates. Here we show that a tetraploid teleost, the Atlantic salmon, expresses four Aqp0 paralogs in the developing lens, but also expresses significant levels of aqp0 mRNAs and proteins in the epithelia of the pronephros, presumptive enterocytes, gill filament and epidermis. Quantitative PCR reveals that aqp0 mRNA titres increase by three orders of magnitude between the onset of somitogenesis and pigmentation of the eye. Using in situ hybridization and specific antisera, we show that at least two of the channels (Aqp0a1, -0b1 and/or -0b2) are localized in the extraocular basolateral and apical membranes, while Aqp0a2 is lens-specific. Heterologous expression of the Aqp0 paralogs in adhesion-deficient mouse fibolast L-cells reveals that, as for human AQP0, each intact salmon channel retains cell-to-cell adhesive properties. The strongest Aqp0 interactions are auto-adhesion, suggesting that homo-octamers likely form the intercellular junctions of the developing lens and epithelial tissues. The present data are thus the first to show the adhesion potential of Aqp0 channels in a non-mammalian vertebrate, and further uncover a novel extraocular role of the channels during vertebrate development. publishedVersion Article in Journal/Newspaper Atlantic salmon University of Bergen: Bergen Open Research Archive (BORA-UiB) PLOS ONE 11 5 e0154592
spellingShingle Embryos
Fishes
immune serum
VDP::Matematikk og naturvitenskap: 400::Basale biofag: 470::Cellebiologi: 471
VDP::Mathematics and natural scienses: 400::Basic biosciences: 470::Cell biology: 471
Chauvigné, Francois
Fjelldal, Per Gunnar
Cerdà, Joan
Finn, Roderick Nigel
Auto-Adhesion Potential of Extraocular Aqp0 during Teleost Development
title Auto-Adhesion Potential of Extraocular Aqp0 during Teleost Development
title_full Auto-Adhesion Potential of Extraocular Aqp0 during Teleost Development
title_fullStr Auto-Adhesion Potential of Extraocular Aqp0 during Teleost Development
title_full_unstemmed Auto-Adhesion Potential of Extraocular Aqp0 during Teleost Development
title_short Auto-Adhesion Potential of Extraocular Aqp0 during Teleost Development
title_sort auto-adhesion potential of extraocular aqp0 during teleost development
topic Embryos
Fishes
immune serum
VDP::Matematikk og naturvitenskap: 400::Basale biofag: 470::Cellebiologi: 471
VDP::Mathematics and natural scienses: 400::Basic biosciences: 470::Cell biology: 471
topic_facet Embryos
Fishes
immune serum
VDP::Matematikk og naturvitenskap: 400::Basale biofag: 470::Cellebiologi: 471
VDP::Mathematics and natural scienses: 400::Basic biosciences: 470::Cell biology: 471
url https://hdl.handle.net/1956/12874
https://doi.org/10.1371/journal.pone.0154592