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...

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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: Public Library of Science 2016
Subjects:
Online Access:http://hdl.handle.net/11250/2398321
https://doi.org/10.1371/journal.pone.0154592
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spelling ftimr:oai:imr.brage.unit.no:11250/2398321 2023-05-15T15:32:44+02:00 Auto-Adhesion Potential of Extraocular Aqp0 during Teleost Development Chauvigné, Francois Fjelldal, Per Gunnar Cerdà, Joan Finn, Roderick Nigel 2016-08-03T13:16:08Z application/octet-stream http://hdl.handle.net/11250/2398321 https://doi.org/10.1371/journal.pone.0154592 eng eng Public Library of Science Chauvigné F, Fjelldal PG, Cerdà J, Finn RN (2016) Auto-Adhesion Potential of Extraocular Aqp0 during Teleost Development. PLoS ONE 11(5): e0154592. doi:10.1371/journal.pone.0154592 urn:issn:1932-6203 http://hdl.handle.net/11250/2398321 https://doi.org/10.1371/journal.pone.0154592 cristin:1354505 Navngivelse 3.0 Norge http://creativecommons.org/licenses/by/3.0/no/ CC-BY 21 s. 11 PLoS ONE 5 VDP::Matematikk og naturvitenskap: 400::Basale biofag: 470::Cellebiologi: 471 VDP::Mathematics and natural scienses: 400::Basic biosciences: 470::Cell biology: 471 Journal article Peer reviewed 2016 ftimr https://doi.org/10.1371/journal.pone.0154592 2021-09-23T20:14:30Z - 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. Article in Journal/Newspaper Atlantic salmon Institute for Marine Research: Brage IMR PLOS ONE 11 5 e0154592
institution Open Polar
collection Institute for Marine Research: Brage IMR
op_collection_id ftimr
language English
topic VDP::Matematikk og naturvitenskap: 400::Basale biofag: 470::Cellebiologi: 471
VDP::Mathematics and natural scienses: 400::Basic biosciences: 470::Cell biology: 471
spellingShingle 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
topic_facet VDP::Matematikk og naturvitenskap: 400::Basale biofag: 470::Cellebiologi: 471
VDP::Mathematics and natural scienses: 400::Basic biosciences: 470::Cell biology: 471
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.
format Article in Journal/Newspaper
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
title Auto-Adhesion Potential of Extraocular Aqp0 during Teleost Development
title_short 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_sort auto-adhesion potential of extraocular aqp0 during teleost development
publisher Public Library of Science
publishDate 2016
url http://hdl.handle.net/11250/2398321
https://doi.org/10.1371/journal.pone.0154592
genre Atlantic salmon
genre_facet Atlantic salmon
op_source 21 s.
11
PLoS ONE
5
op_relation Chauvigné F, Fjelldal PG, Cerdà J, Finn RN (2016) Auto-Adhesion Potential of Extraocular Aqp0 during Teleost Development. PLoS ONE 11(5): e0154592. doi:10.1371/journal.pone.0154592
urn:issn:1932-6203
http://hdl.handle.net/11250/2398321
https://doi.org/10.1371/journal.pone.0154592
cristin:1354505
op_rights Navngivelse 3.0 Norge
http://creativecommons.org/licenses/by/3.0/no/
op_rightsnorm CC-BY
op_doi https://doi.org/10.1371/journal.pone.0154592
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