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Four selenoprotein P genes exist in salmonids: Analysis of their origin and expression following Se supplementation and bacterial infection

The following research was conducted to elucidate the evolution and expression of salmonid selenoprotein P (SelP), a selenoprotein that is unique in having multiple selenocysteine (Sec) residues, following supranutritional selenium supplementation and infection in rainbow trout. We show that in salm...

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Autores principales: Pohl, Moritz A. N., Wang, Tiehui, Pohl, Thitiya, Sweetman, John, Martin, Samuel A. M., Secombes, Christopher J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6301783/
https://www.ncbi.nlm.nih.gov/pubmed/30571741
http://dx.doi.org/10.1371/journal.pone.0209381
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author Pohl, Moritz A. N.
Wang, Tiehui
Pohl, Thitiya
Sweetman, John
Martin, Samuel A. M.
Secombes, Christopher J.
author_facet Pohl, Moritz A. N.
Wang, Tiehui
Pohl, Thitiya
Sweetman, John
Martin, Samuel A. M.
Secombes, Christopher J.
author_sort Pohl, Moritz A. N.
collection PubMed
description The following research was conducted to elucidate the evolution and expression of salmonid selenoprotein P (SelP), a selenoprotein that is unique in having multiple selenocysteine (Sec) residues, following supranutritional selenium supplementation and infection in rainbow trout. We show that in salmonids SelP is present as four paralogues and that the diversification of SelP genes during vertebrate evolution relates to whole genome duplication events. With 17 and 16 selenocysteine residues for rainbow trout (Oncorhynchus mykiss)/Atlantic salmon (Salmo salar) SelPa1 and SelPa2 proteins respectively and 1 or 2 (trout or salmon) and 4 or 3 (trout or salmon) selenocysteine residues for salmonid SelPb1 and SelPb2 proteins respectively, this is the highest number of (predicted) multiple selenocysteine containing SelP proteins reported for any vertebrate species to date. To investigate the effects of selenium form on SelP expression we added different concentrations (1 nM– 10 μM) of organic or inorganic selenium to a trout cell line (RTG-2 cells) and analysed changes in mRNA abundance. We next studied the impact of supplementation on the potential modulation of these transcripts by PAMPs and proinflammatory cytokines in RTG-2 and RTS-11 cells. These experiments revealed that selenium type influenced the responses, and that SelP gene subfunctionalisation was apparent. To get an insight into the expression patterns in vivo we conducted a feeding trial with 2 diets differing in selenium content and 5 weeks later challenged the trout with a bacterial pathogen (Aeromonas salmonicida). Four tissues were analysed for SelP paralogue expression. The results show a significant induction of SelPa1 in gills and intestine following infection in selenium supplemented fish and for SelPa2 in gills. SelPb1 was significantly reduced in head kidney of both diet groups following infection, whilst SelPb2 was significantly upregulated in skin of both diet groups post infection. Overall these findings reveal differential expression profiles for the SelPa/SelPb paralogues in trout, influenced by selenium supply, cell type/tissue and stimulant. The increase of multiple Sec containing SelP proteins in salmonids could indicate an enhanced requirement for selenium in this lineage.
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spelling pubmed-63017832019-01-08 Four selenoprotein P genes exist in salmonids: Analysis of their origin and expression following Se supplementation and bacterial infection Pohl, Moritz A. N. Wang, Tiehui Pohl, Thitiya Sweetman, John Martin, Samuel A. M. Secombes, Christopher J. PLoS One Research Article The following research was conducted to elucidate the evolution and expression of salmonid selenoprotein P (SelP), a selenoprotein that is unique in having multiple selenocysteine (Sec) residues, following supranutritional selenium supplementation and infection in rainbow trout. We show that in salmonids SelP is present as four paralogues and that the diversification of SelP genes during vertebrate evolution relates to whole genome duplication events. With 17 and 16 selenocysteine residues for rainbow trout (Oncorhynchus mykiss)/Atlantic salmon (Salmo salar) SelPa1 and SelPa2 proteins respectively and 1 or 2 (trout or salmon) and 4 or 3 (trout or salmon) selenocysteine residues for salmonid SelPb1 and SelPb2 proteins respectively, this is the highest number of (predicted) multiple selenocysteine containing SelP proteins reported for any vertebrate species to date. To investigate the effects of selenium form on SelP expression we added different concentrations (1 nM– 10 μM) of organic or inorganic selenium to a trout cell line (RTG-2 cells) and analysed changes in mRNA abundance. We next studied the impact of supplementation on the potential modulation of these transcripts by PAMPs and proinflammatory cytokines in RTG-2 and RTS-11 cells. These experiments revealed that selenium type influenced the responses, and that SelP gene subfunctionalisation was apparent. To get an insight into the expression patterns in vivo we conducted a feeding trial with 2 diets differing in selenium content and 5 weeks later challenged the trout with a bacterial pathogen (Aeromonas salmonicida). Four tissues were analysed for SelP paralogue expression. The results show a significant induction of SelPa1 in gills and intestine following infection in selenium supplemented fish and for SelPa2 in gills. SelPb1 was significantly reduced in head kidney of both diet groups following infection, whilst SelPb2 was significantly upregulated in skin of both diet groups post infection. Overall these findings reveal differential expression profiles for the SelPa/SelPb paralogues in trout, influenced by selenium supply, cell type/tissue and stimulant. The increase of multiple Sec containing SelP proteins in salmonids could indicate an enhanced requirement for selenium in this lineage. Public Library of Science 2018-12-20 /pmc/articles/PMC6301783/ /pubmed/30571741 http://dx.doi.org/10.1371/journal.pone.0209381 Text en © 2018 Pohl et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Pohl, Moritz A. N.
Wang, Tiehui
Pohl, Thitiya
Sweetman, John
Martin, Samuel A. M.
Secombes, Christopher J.
Four selenoprotein P genes exist in salmonids: Analysis of their origin and expression following Se supplementation and bacterial infection
title Four selenoprotein P genes exist in salmonids: Analysis of their origin and expression following Se supplementation and bacterial infection
title_full Four selenoprotein P genes exist in salmonids: Analysis of their origin and expression following Se supplementation and bacterial infection
title_fullStr Four selenoprotein P genes exist in salmonids: Analysis of their origin and expression following Se supplementation and bacterial infection
title_full_unstemmed Four selenoprotein P genes exist in salmonids: Analysis of their origin and expression following Se supplementation and bacterial infection
title_short Four selenoprotein P genes exist in salmonids: Analysis of their origin and expression following Se supplementation and bacterial infection
title_sort four selenoprotein p genes exist in salmonids: analysis of their origin and expression following se supplementation and bacterial infection
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6301783/
https://www.ncbi.nlm.nih.gov/pubmed/30571741
http://dx.doi.org/10.1371/journal.pone.0209381
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