Dietary soyasaponin supplementation to pea protein concentrate reveals nutrigenomic interactions underlying enteropathy in Atlantic salmon (Salmo salar)

Abstract Background Use of plant ingredients in aquaculture feeds is impeded by high contents of antinutritional factors such as saponins, which may cause various pharmacological and biological effects. In this study, transcriptome changes were analyzed using a 21 k oligonucleotide microarray and qP...

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Main Authors: Kortner, Trond M, Skugor, Stanko, Penn, Michael H, Mydland, Liv, Djordjevic, Brankica, Hillestad, Marie, Krasnov, Aleksei, Krogdahl, Åshild
Format: Article in Journal/Newspaper
Language:English
Published: BioMed Central Ltd. 2012
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Online Access:http://www.biomedcentral.com/1746-6148/8/101
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spelling ftbiomed:oai:biomedcentral.com:1746-6148-8-101 2023-05-15T15:32:17+02:00 Dietary soyasaponin supplementation to pea protein concentrate reveals nutrigenomic interactions underlying enteropathy in Atlantic salmon (Salmo salar) Kortner, Trond M Skugor, Stanko Penn, Michael H Mydland, Liv Djordjevic, Brankica Hillestad, Marie Krasnov, Aleksei Krogdahl, Åshild 2012-07-02 http://www.biomedcentral.com/1746-6148/8/101 en eng BioMed Central Ltd. http://www.biomedcentral.com/1746-6148/8/101 Copyright 2012 Kortner et al.; licensee BioMed Central Ltd. Plant protein sources Fish feed Microarray Inflammation Digestion Saponin Research article 2012 ftbiomed 2012-08-25T23:52:34Z Abstract Background Use of plant ingredients in aquaculture feeds is impeded by high contents of antinutritional factors such as saponins, which may cause various pharmacological and biological effects. In this study, transcriptome changes were analyzed using a 21 k oligonucleotide microarray and qPCR in the distal intestine of Atlantic salmon fed diets based on five plant protein sources combined with soybean saponins. Results Diets with corn gluten, sunflower, rapeseed or horsebean produced minor effects while the combination of saponins with pea protein concentrate caused enteritis and major transcriptome changes. Acute inflammation was characterised by up-regulation of cytokines, NFkB and TNFalpha related genes and regulators of T-cell function, while the IFN-axis was suppressed. Induction of lectins, complement, metalloproteinases and the respiratory burst complex parallelled a down-regulation of genes for free radical scavengers and iron binding proteins. Marked down-regulation of xenobiotic metabolism was also observed, possibly increasing vulnerability of the intestinal tissue. A hallmark of metabolic changes was dramatic down-regulation of lipid, bile and steroid metabolism. Impairment of digestion was further suggested by expression changes of nutrient transporters and regulators of water balance (e.g. aquaporin, guanylin). On the other hand, microarray profiling revealed activation of multiple mucosal defence processes. Annexin-1, with important anti-inflammatory and gastroprotective properties, was markedly up-regulated. Furthermore, augmented synthesis of polyamines needed for cellular proliferation (up-regulation of arginase and ornithine decarboxylase) and increased mucus production (down-regulation of glycan turnover and goblet cell hyperplasia) could participate in mucosal healing and restoration of normal tissue function. Conclusion The current study promoted understanding of salmon intestinal pathology and establishment of a model for feed induced enteritis. Multiple gene expression profiling further characterised the inflammation and described the intestinal pathology at the molecular level. Ethical approval The present experiment was approved by the Norwegian Animal Research Authority and conducted according to prevailing animal welfare regulations: FOR-1996-01-15-23 (Norway), European Convention for the Protection of Vertebrate Animals used for Experimental and Other Scientific Purposes (Strasbourg, 18.III.1986) and COUNCIL DIRECTIVE of 24 November 1986 on the approximation of laws, regulations and administrative provisions of the Member States regarding the protection of animals used for experimental and other scientific purposes (86/609/EEC). Article in Journal/Newspaper Atlantic salmon Salmo salar BioMed Central Norway
institution Open Polar
collection BioMed Central
op_collection_id ftbiomed
language English
topic Plant protein sources
Fish feed
Microarray
Inflammation
Digestion
Saponin
spellingShingle Plant protein sources
Fish feed
Microarray
Inflammation
Digestion
Saponin
Kortner, Trond M
Skugor, Stanko
Penn, Michael H
Mydland, Liv
Djordjevic, Brankica
Hillestad, Marie
Krasnov, Aleksei
Krogdahl, Åshild
Dietary soyasaponin supplementation to pea protein concentrate reveals nutrigenomic interactions underlying enteropathy in Atlantic salmon (Salmo salar)
topic_facet Plant protein sources
Fish feed
Microarray
Inflammation
Digestion
Saponin
description Abstract Background Use of plant ingredients in aquaculture feeds is impeded by high contents of antinutritional factors such as saponins, which may cause various pharmacological and biological effects. In this study, transcriptome changes were analyzed using a 21 k oligonucleotide microarray and qPCR in the distal intestine of Atlantic salmon fed diets based on five plant protein sources combined with soybean saponins. Results Diets with corn gluten, sunflower, rapeseed or horsebean produced minor effects while the combination of saponins with pea protein concentrate caused enteritis and major transcriptome changes. Acute inflammation was characterised by up-regulation of cytokines, NFkB and TNFalpha related genes and regulators of T-cell function, while the IFN-axis was suppressed. Induction of lectins, complement, metalloproteinases and the respiratory burst complex parallelled a down-regulation of genes for free radical scavengers and iron binding proteins. Marked down-regulation of xenobiotic metabolism was also observed, possibly increasing vulnerability of the intestinal tissue. A hallmark of metabolic changes was dramatic down-regulation of lipid, bile and steroid metabolism. Impairment of digestion was further suggested by expression changes of nutrient transporters and regulators of water balance (e.g. aquaporin, guanylin). On the other hand, microarray profiling revealed activation of multiple mucosal defence processes. Annexin-1, with important anti-inflammatory and gastroprotective properties, was markedly up-regulated. Furthermore, augmented synthesis of polyamines needed for cellular proliferation (up-regulation of arginase and ornithine decarboxylase) and increased mucus production (down-regulation of glycan turnover and goblet cell hyperplasia) could participate in mucosal healing and restoration of normal tissue function. Conclusion The current study promoted understanding of salmon intestinal pathology and establishment of a model for feed induced enteritis. Multiple gene expression profiling further characterised the inflammation and described the intestinal pathology at the molecular level. Ethical approval The present experiment was approved by the Norwegian Animal Research Authority and conducted according to prevailing animal welfare regulations: FOR-1996-01-15-23 (Norway), European Convention for the Protection of Vertebrate Animals used for Experimental and Other Scientific Purposes (Strasbourg, 18.III.1986) and COUNCIL DIRECTIVE of 24 November 1986 on the approximation of laws, regulations and administrative provisions of the Member States regarding the protection of animals used for experimental and other scientific purposes (86/609/EEC).
format Article in Journal/Newspaper
author Kortner, Trond M
Skugor, Stanko
Penn, Michael H
Mydland, Liv
Djordjevic, Brankica
Hillestad, Marie
Krasnov, Aleksei
Krogdahl, Åshild
author_facet Kortner, Trond M
Skugor, Stanko
Penn, Michael H
Mydland, Liv
Djordjevic, Brankica
Hillestad, Marie
Krasnov, Aleksei
Krogdahl, Åshild
author_sort Kortner, Trond M
title Dietary soyasaponin supplementation to pea protein concentrate reveals nutrigenomic interactions underlying enteropathy in Atlantic salmon (Salmo salar)
title_short Dietary soyasaponin supplementation to pea protein concentrate reveals nutrigenomic interactions underlying enteropathy in Atlantic salmon (Salmo salar)
title_full Dietary soyasaponin supplementation to pea protein concentrate reveals nutrigenomic interactions underlying enteropathy in Atlantic salmon (Salmo salar)
title_fullStr Dietary soyasaponin supplementation to pea protein concentrate reveals nutrigenomic interactions underlying enteropathy in Atlantic salmon (Salmo salar)
title_full_unstemmed Dietary soyasaponin supplementation to pea protein concentrate reveals nutrigenomic interactions underlying enteropathy in Atlantic salmon (Salmo salar)
title_sort dietary soyasaponin supplementation to pea protein concentrate reveals nutrigenomic interactions underlying enteropathy in atlantic salmon (salmo salar)
publisher BioMed Central Ltd.
publishDate 2012
url http://www.biomedcentral.com/1746-6148/8/101
geographic Norway
geographic_facet Norway
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_relation http://www.biomedcentral.com/1746-6148/8/101
op_rights Copyright 2012 Kortner et al.; licensee BioMed Central Ltd.
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