Transcriptome analyses of Atlantic salmon (Salmo salar L.) erythrocytes infected with piscine orthoreovirus (PRV)

Dahle, Maria K.; Wessel, Øystein; Timmerhaus, Gerrit; Nyman, Ingvild Berg; Jørgensen, Sven Martin; Rimstad, Espen; Krasnov, Aleksei

doi:10.1016/j.fsi.2015.05.049

Cited by 84 publications

(121 citation statements)

References 31 publications

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“…In our present study, we identified increased Mx expression in kidney tissues only once peak viral loads were reached, which in conjunction with the work of Dahle et al [9], suggests that an antiviral response against PRV is initiated late during the mature phase of PRV infection and can occur in both the presence and absence of inflammatory associated disease. However, without disease manifestations, we observed that Mx transcription was not maintained and returned to a comparable control level by 9 weeks post challenge (Fig.…”

Section: Discussionsupporting

confidence: 90%

“…Dahle et al [9] examined the transcriptional response of Atlantic salmon erythrocytes to infection with PRV using samples obtained from a cohabitation challenge conducted by Finstad et al [7] which resulted in a first detection of PRV at 4 wpc and histological signs of HSMI at 7 wpc when blood PRV loads were at their maximum. Microarray analysis conducted on peripheral erythrocyte samples collected at 5 and 7 wpc reported upregulation of a large number of viral responsive genes and down-regulation of non-immune related genes in PRV infected groups at both time points; however, qPCR validation of antiviral genes associated with the interferon response ( IFN-1α , IRF-1 , RIG-1 , Mx and PKR ) as well as the immuno-regulatory genes Interleukin-10 and Suppressor of Cytokine Signaling-1 did not identify significant responsiveness of these genes at 5 wpc relative to controls.…”

Section: Discussionmentioning

confidence: 99%

“…Microarray analysis conducted on peripheral erythrocyte samples collected at 5 and 7 wpc reported upregulation of a large number of viral responsive genes and down-regulation of non-immune related genes in PRV infected groups at both time points; however, qPCR validation of antiviral genes associated with the interferon response ( IFN-1α , IRF-1 , RIG-1 , Mx and PKR ) as well as the immuno-regulatory genes Interleukin-10 and Suppressor of Cytokine Signaling-1 did not identify significant responsiveness of these genes at 5 wpc relative to controls. At 7 wpc, when 4/6 fish sampled had histopathological signs of HSMI and PRV loads were highest, significant induction of these genes (except PKR) was observed although variability between individuals appeared high [9]. …”

Section: Discussionmentioning

confidence: 99%

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De novo assembly of Sockeye salmon kidney transcriptomes reveal a limited early response to piscine reovirus with or without infectious hematopoietic necrosis virus superinfection

et al. 2016

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BackgroundPiscine reovirus (PRV) has been associated with the serious disease known as Heart and Skeletal Muscle Inflammation (HSMI) in cultured Atlantic salmon Salmo salar in Norway. PRV is also prevalent in wild and farmed salmon without overt disease manifestations, suggesting multifactorial triggers or PRV variant-specific factors are required to initiate disease. In this study, we explore the head kidney transcriptome of Sockeye salmon Oncorhynchus nerka during early PRV infection to identify host responses in the absence of disease in hopes of elucidating mechanisms by which PRV may directly alter host functions and contribute to the development of a disease state. We further investigate the role of PRV as a coinfecting agent following superinfection with infectious hematopoietic necrosis virus (IHNV) – a highly pathogenic rhabdovirus endemic to the west coast of North America.ResultsChallenge of Sockeye salmon with PRV resulted in high quantities of viral transcripts to become present in the blood and kidney of infected fish without manifestations of disease. De novo transcriptome assembly of over 2.3 billion paired RNA-seq reads from the head kidneys of 36 fish identified more than 320,000 putative unigenes, of which less than 20 were suggested to be differentially expressed in response to PRV at either 2 or 3 weeks post challenge by DESeq2 and edgeR analysis. Of these, only one, Ependymin, was confirmed to be differentially expressed by qPCR in an expanded sample set. In contrast, IHNV induced substantial transcriptional changes (differential expression of > 20,000 unigenes) which included transcripts involved in antiviral and inflammatory response pathways. Prior infection with PRV had no significant effect on host responses to superinfecting IHNV, nor did host responses initiated by IHNV exposure influence increasing PRV loads.ConclusionsPRV does not substantially alter the head kidney transcriptome of Sockeye salmon during early (2 to 3 week) infection and dissemination in a period of significant increasing viral load, nor does the presence of PRV change the host transcriptional response to an IHNV superinfection. Further, concurrent infections of PRV and IHNV do not appear to significantly influence the infectivity or severity of IHNV associated disease, or conversely, PRV load.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3196-y) contains supplementary material, which is available to authorized users.

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Section: Discussionsupporting

confidence: 90%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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De novo assembly of Sockeye salmon kidney transcriptomes reveal a limited early response to piscine reovirus with or without infectious hematopoietic necrosis virus superinfection

et al. 2016

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“…Piscine erythrocytes are nucleated and contain the transcriptional and translational machinery necessary for expression of mRNA and proteins [17]. Erythrocytes are important target cells for PRV and the infection activates an innate antiviral immune response typical for RNA viruses in these cells [18]. During the peak phase of infection, more than 50% of all erythrocytes may be infected [19].…”

Section: Introductionmentioning

confidence: 99%

Viral Protein Kinetics of Piscine Orthoreovirus Infection in Atlantic Salmon Blood Cells

Haatveit

Wessel

Markussen

et al. 2017

Viruses

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Piscine orthoreovirus (PRV) is ubiquitous in farmed Atlantic salmon (Salmo salar) and the cause of heart and skeletal muscle inflammation. Erythrocytes are important target cells for PRV. We have investigated the kinetics of PRV infection in salmon blood cells. The findings indicate that PRV causes an acute infection of blood cells lasting 1–2 weeks, before it subsides into persistence. A high production of viral proteins occurred initially in the acute phase which significantly correlated with antiviral gene transcription. Globular viral factories organized by the non-structural protein µNS were also observed initially, but were not evident at later stages. Interactions between µNS and the PRV structural proteins λ1, µ1, σ1 and σ3 were demonstrated. Different size variants of µNS and the outer capsid protein µ1 appeared at specific time points during infection. Maximal viral protein load was observed five weeks post cohabitant challenge and was undetectable from seven weeks post challenge. In contrast, viral RNA at a high level could be detected throughout the eight-week trial. A proteolytic cleavage fragment of the µ1 protein was the only viral protein detectable after seven weeks post challenge, indicating that this µ1 fragment may be involved in the mechanisms of persistent infection.

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“…This is mainly because there has been a general lack of appropriate tools able to identify and characterize viruses collected from environmental samples. However, the emergence of high throughput next generation sequencing (NSG) in recent years has not only enhanced our understanding of host responses to viral infections (Chu et al, 2015; Dahle et al, 2015; Xu et al, 2015, 2016a,b; Liu et al, 2016), but it has opened a great avenue for identification of viruses found in different aquatic environments using metagenomics analyses (Suttle, 2005, 2007; Djikeng et al, 2009; Kim et al, 2015). Viral metagenomics is a culture independent sequencing tool able to identify a large number of viral genomes from the same sample at the same time without prior knowledge of genomic sequences of the viruses to be identified (Handelsman, 2004; Bibby, 2013).…”

Section: Introductionmentioning

confidence: 99%

Environmental Viral Metagenomics Analyses in Aquaculture: Applications in Epidemiology and Disease Control

Munang’andu

2016

Front. Microbiol.

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Studies on the epidemiology of viral diseases in aquaculture have for a long time depended on isolation of viruses from infected aquatic organisms. The role of aquatic environments in the epidemiology of viral diseases in aquaculture has not been extensively expounded mainly because of the lack of appropriate tools for environmental studies on aquatic viruses. However, the upcoming of metagenomics analyses opens great avenues in which environmental samples can be used to study the epidemiology of viral diseases outside their host species. Hence, in this review I have shown that epidemiological factors that influence the composition of viruses in different aquatic environments include ecological factors, anthropogenic activities and stocking densities of cultured organisms based on environmental metagenomics studies carried out this far. Ballast water transportation and global trade of aquatic organisms are the most common virus dispersal process identified this far. In terms of disease control for outdoor aquaculture systems, baseline data on viruses found in different environments intended for aquaculture use can be obtained to enable the design of effective disease control strategies. And as such, high-risk areas having a high specter of pathogenic viruses can be identified as an early warning system. As for the control of viral diseases for indoor recirculation aquaculture systems (RAS), the most effective disinfection methods able to eliminate pathogenic viruses from water used in RAS can be identified. Overall, the synopsis I have put forth in this review shows that environmental samples can be used to study the epidemiology of viral diseases in aquaculture using viral metagenomics analysis as an overture for the design of rational disease control strategies.

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Transcriptome analyses of Atlantic salmon (Salmo salar L.) erythrocytes infected with piscine orthoreovirus (PRV)

Cited by 84 publications

References 31 publications

De novo assembly of Sockeye salmon kidney transcriptomes reveal a limited early response to piscine reovirus with or without infectious hematopoietic necrosis virus superinfection

De novo assembly of Sockeye salmon kidney transcriptomes reveal a limited early response to piscine reovirus with or without infectious hematopoietic necrosis virus superinfection

Viral Protein Kinetics of Piscine Orthoreovirus Infection in Atlantic Salmon Blood Cells

Environmental Viral Metagenomics Analyses in Aquaculture: Applications in Epidemiology and Disease Control

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