Dataset Information

Gene expression analysis of Atlantic salmon gills reveals mucin 5 and interleukin 4/13 as key molecules during amoebic gill disease.

ABSTRACT: Amoebic gill disease (AGD) is one of the main diseases affecting Atlantic salmon (Salmo salar L.) mariculture. Hallmarks of AGD are hyperplasia of the lamellar epithelium and increased production of gill mucus. This study investigated the expression of genes involved in mucus secretion, cell cycle regulation, immunity and oxidative stress in gills using a targeted 21-gene PCR array. Gill samples were obtained from experimental and natural Neoparamoeba perurans infections, and sampling points included progressive infection stages and post-freshwater treatment. Up-regulation of genes related to mucin secretion and cell proliferation, and down-regulation of pro-inflammatory and pro-apoptotic genes were associated with AGD severity, while partial restoration of the gill homeostasis was detected post-treatment. Mucins and Th2 cytokines accoun ted for most of the variability observed between groups highlighting their key role in AGD. Two mucins (muc5, muc18) showed differential regulation upon disease. Substantial up-regulation of the secreted muc5 was detected in clinical AGD, and the membrane bound muc18 showed an opposite pattern. Th2 cytokines, il4/13a and il4/13b2, were significantly up-regulated from 2 days post-infection onwards, and changes were lesion-specific. Despite the differences between experimental and natural infections, both yielded comparable results that underline the importance of the studied genes in the respiratory organs of fish, and during AGD progression.

SUBMITTER: Marcos-Lopez M

PROVIDER: S-EPMC6135806 | biostudies-literature | 2018 Sep

REPOSITORIES: biostudies-literature

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Gene expression analysis of Atlantic salmon gills reveals mucin 5 and interleukin 4/13 as key molecules during amoebic gill disease.

Marcos-López Mar M Calduch-Giner Josep A JA Mirimin Luca L MacCarthy Eugene E Rodger Hamish D HD O'Connor Ian I Sitjà-Bobadilla Ariadna A Pérez-Sánchez Jaume J Piazzon M Carla MC

Scientific reports 20180912 1

Amoebic gill disease (AGD) is one of the main diseases affecting Atlantic salmon (Salmo salar L.) mariculture. Hallmarks of AGD are hyperplasia of the lamellar epithelium and increased production of gill mucus. This study investigated the expression of genes involved in mucus secretion, cell cycle regulation, immunity and oxidative stress in gills using a targeted 21-gene PCR array. Gill samples were obtained from experimental and natural Neoparamoeba perurans infections, and sampling points inc ...[more]

PMID: 30209326

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Project description:BackgroundGill health is one of the main concerns for Atlantic salmon aquaculture, and Amoebic Gill Disease (AGD), attributable to infection by the amoeba Neoparamoeba perurans, is a frequent cause of morbidity. In the absence of preventive measures, increasing genetic resistance of salmon to AGD via selective breeding can reduce the incidence of the disease and mitigate gill damage. Understanding the mechanisms leading to AGD resistance and the underlying causative genomic features can aid in this effort, while also providing critical information for the development of other control strategies. AGD resistance is considered to be moderately heritable, and several putative QTL have been identified. The aim of the current study was to improve understanding of the mechanisms underlying AGD resistance, and to identify putative causative genomic factors underlying the QTL. To achieve this, RNA was extracted from the gill and head kidney of AGD resistant and susceptible animals following a challenge with N. perurans, and sequenced.ResultsComparison between resistant and susceptible animals primarily highlighted differences mainly in the local immune response in the gill, involving red blood cell genes and genes related to immune function and cell adhesion. Differentially expressed immune genes pointed to a contrast in Th2 and Th17 responses, which is consistent with the increased heritability observed after successive challenges with the amoeba. Five QTL-region candidate genes showed differential expression, including a gene connected to interferon responses (GVINP1), a gene involved in systemic inflammation (MAP4K4), and a positive regulator of apoptosis (TRIM39). Analyses of allele-specific expression highlighted a gene in the QTL region on chromosome 17, cellular repressor of E1A-stimulated genes 1 (CREG1), showing allelic differential expression suggestive of a cis-acting regulatory variant.ConclusionsIn summary, this study provides new insights into the mechanisms of resistance to AGD in Atlantic salmon, and highlights candidate genes for further functional studies that can further elucidate the genomic mechanisms leading to resistance and contribute to enhancing salmon health via improved genomic selection.

Project description:Amoebic gill disease (AGD) is one of the most important parasitic diseases of farmed Atlantic salmon. It is a source of major economic loss to the industry and poses significant threats to animal welfare. Previous studies have shown that resistance against this disease has a moderate, heritable genetic component, although the genes and the genetic pathways that contribute to this process have yet to be elucidated. In this study, to identify the genetic mechanisms of AGD resistance, we first investigated the molecular signatures of AGD infection in Atlantic salmon through a challenge model, where we compared the transcriptome profiles of the naïve and infected animals. We then conducted a genome-wide association analysis with 1,333 challenged tested fish to map the AGD resistance genomic regions, supported by the results from the transcriptomic data. Further, we investigated the potential of incorporating gene expression analysis results in genomic prediction to improve prediction accuracy. Our data suggest thousands of genes have modified their expression following infection, with a significant increase in the transcription of genes with functional properties in cell adhesion and a sharp decline in the abundance of various components of the immune system genes. From the genome-wide association analysis, QTL regions on chromosomes ssa04, ssa09, and ssa13 were detected to be linked with AGD resistance. In particular, we found that QTL region on ssa04 harbors members of the cadherin gene family. These genes play a critical role in target recognition and cell adhesion. The QTL region on ssa09 also is associated with another member of the cadherin gene family, protocadherin Fat 4. The associated genetic markers on ssa13 span a large genomic region that includes interleukin-18-binding protein, a gene with function essential in inhibiting the proinflammatory effect of cytokine IL18. Incorporating gene expression information through a weighted genomic relationship matrix approach decreased genomic prediction accuracy and increased bias of prediction. Together, these findings help to improve our breeding programs and animal welfare against AGD and advance our knowledge of the genetic basis of host-pathogen interactions.

Dataset Information

Gene expression analysis of Atlantic salmon gills reveals mucin 5 and interleukin 4/13 as key molecules during amoebic gill disease.

Publications

Gene expression analysis of Atlantic salmon gills reveals mucin 5 and interleukin 4/13 as key molecules during amoebic gill disease.

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