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2. Metabolomics and Multi-Omics Determination of Potential Plasma Biomarkers in PRV-1-Infected Atlantic Salmon.

Author

Ivanova, Lada, Rangel-Huerta, Oscar D., Tartor, Haitham, Dahle, Maria K., Uhlig, Silvio, and Fæste, Christiane Kruse

Subjects
ATLANTIC salmon, MULTIOMICS, MYOSITIS, MYOCARDIUM, LIPID metabolism
Abstract

Metabolomic analysis has been explored to search for disease biomarkers in humans for some time. The application to animal species, including fish, however, is still at the beginning. In the present study, we have used targeted and untargeted metabolomics to identify metabolites in the plasma of Atlantic salmon (Salmo salar) challenged with Piscine orthoreovirus (PRV-1), aiming to find metabolites associated with the progression of PRV-1 infection into heart and skeletal muscle inflammation (HSMI). The metabolomes of control and PRV-1-infected salmon were compared at three time points during disease development by employing different biostatistical approaches. Targeted metabolomics resulted in the determination of affected metabolites and metabolic pathways, revealing a substantial impact of PRV-1 infection on lipid homeostasis, especially on several (lyso)phosphatidylcholines, ceramides, and triglycerides. Untargeted metabolomics showed a clear separation of the treatment groups at later study time points, mainly due to effects on lipid metabolism pathways. In a subsequent multi-omics approach, we combined both metabolomics datasets with previously reported proteomics data generated from the same salmon plasma samples. Data processing with DIABLO software resulted in the identification of significant metabolites and proteins that were representative of the HSMI development in the salmon. [ABSTRACT FROM AUTHOR]

Published
2024
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5. Transcriptomics of early responses to purified Piscine orthoreovirus-1 in Atlantic salmon (Salmo salar L.) red blood cells compared to nonsusceptible cell lines.

Author

Tsoulia, Thomais, Sundaram, Arvind Y. M., Braaen, Stine, Jørgensen, Jorunn B., Rimstad, Espen, Wessel, Øystein, and Dahle, Maria K.

Subjects
ATLANTIC salmon, ERYTHROCYTES, TRANSCRIPTOMES, CELL lines, PATTERN perception receptors
Abstract

Piscine red blood cells (RBC) are nucleated and have been characterized as mediators of immune responses in addition to their role in gas exchange. Salmonid RBC are major target cells of Piscine orthoreovirus-1 (PRV-1), the etiological agent of heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon (Salmo salar). PRV-1 replicates in RBC ex vivo, but no viral amplification has been possible in available A. salmon cell lines. To compare RBC basal transcripts and transcriptional responses to PRV-1 in the early phase of infection with non-susceptible cells, we exposed A. salmon RBC, Atlantic salmon kidney cells (ASK) and Salmon head kidney cells (SHK-1) to PRV-1 for 24 h. The RNAseq analysis of RBC supported their previous characterization as pluripotent cells, as they expressed a wide repertoire of genes encoding pattern recognition receptors (PRRs), cytokine receptors, and genes implicated in antiviral activities. The comparison of RBC to ASK and SHK-1 revealed immune cell features exclusively expressed in RBC, such as genes involved in chemotactic activity in response to inflammation. Differential expression analysis of RBC exposed to PRV-1 showed 46 significantly induced genes (≥ 2-fold upregulation) linked to the antiviral response pathway, including RNA-specific PRRs and interferon (IFN) response factors. In SHK1, PRV induced a more potent or faster antiviral response (213 genes induced). ASK cells showed a differential response pattern (12 genes induced, 18 suppressed) less characterized by the dsRNA-induced antiviral pathway. Despite these differences, the RIG-I-like receptor 3 (RLR3) in the family of cytosolic dsRNA receptors was significantly induced in all PRV-1 exposed cells. IFN regulatory factor 1 (IRF1) was significantly induced in RBC only, in contrast to IRF3/IRF7 induced in SHK-1. Differences in IRF expression and activity may potentially affect viral propagation. [ABSTRACT FROM AUTHOR]

Published
2024
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6. Experimental transmission of piscine orthoreovirus-1 (PRV-1) in different life stages of Atlantic salmon (Salmo salar) and brown trout (Salmo trutta)

Author

Kannimuthu, Dhamotharan, primary, Roh, HyeongJin, additional, Morton, H Craig, additional, Peñaranda, Ma Michelle D., additional, Vossgård, Anne, additional, Hansen, Tom, additional, Fjelldal, Per Gunnar, additional, Karlsbakk, Egil, additional, Fiksdal, Ingrid, additional, Dahle, Maria K., additional, Berg-Rolness, Håkon, additional, Mæhle, Stig, additional, Berhe, Ghebretnsae Dawit, additional, Nordbø, Joachim, additional, Patel, Sonal, additional, Madhun, Abdullah, additional, Grove, Søren, additional, and Kvamme, Bjørn Olav, additional

Published
2023
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14. Piscine Orthoreovirus (PRV)-3, but Not PRV-2, Cross-Protects against PRV-1 and Heart and Skeletal Muscle Inflammation in Atlantic Salmon

Author

Malik, Muhammad Salman, primary, Teige, Lena H., additional, Braaen, Stine, additional, Olsen, Anne Berit, additional, Nordberg, Monica, additional, Amundsen, Marit M., additional, Dhamotharan, Kannimuthu, additional, Svenning, Steingrim, additional, Edholm, Eva Stina, additional, Takano, Tomokazu, additional, Jørgensen, Jorunn B., additional, Wessel, Øystein, additional, Rimstad, Espen, additional, and Dahle, Maria K., additional

Published
2021
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15. Piscine Orthoreovirus-1 Isolates Differ in Their Ability to Induce Heart and Skeletal Muscle Inflammation in Atlantic Salmon (Salmo salar)

Author

Wessel, Øystein, primary, Hansen, Elisabeth F., additional, Dahle, Maria K., additional, Alarcon, Marta, additional, Vatne, Nina A., additional, Nyman, Ingvild B., additional, Soleim, Karen B., additional, Dhamotharan, Kannimuthu, additional, Timmerhaus, Gerrit, additional, Markussen, Turhan, additional, Lund, Morten, additional, Aanes, Håvard, additional, Devold, Magnus, additional, Inami, Makoto, additional, Løvoll, Marie, additional, and Rimstad, Espen, additional

Published
2020
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18. Inactivation of Piscine orthoreovirus

Author

Wessel, Øystein, primary, Hansen, Elisabeth F., additional, Løvoll, Marie, additional, Inami, Makoto, additional, Husby, Asbjørn, additional, Kruse, Gesa, additional, Dahle, Maria K., additional, and Rimstad, Espen, additional

Published
2020
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19. Genotyping of Salmon Gill Poxvirus Reveals One Main Predominant Lineage in Europe, Featuring Fjord- and Fish Farm-Specific Sub-Lineages

Author

Gulla, Snorre, primary, Tengs, Torstein, additional, Mohammad, Saima Nasrin, additional, Gjessing, Mona, additional, Garseth, Åse Helen, additional, Sveinsson, Karoline, additional, Moldal, Torfinn, additional, Petersen, Petra E., additional, Tørud, Brit, additional, Dale, Ole Bendik, additional, and Dahle, Maria K., additional

Published
2020
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21. Detection of Salmonid IgM Specific to the Piscine Orthoreovirus Outer Capsid Spike Protein Sigma 1 Using Lipid-Modified Antigens in a Bead-Based Antibody Detection Assay

Author

Teige, Lena Hammerlund, Kumar, Subramani, Johansen, Grethe M, Wessel, Øystein, Vendramin, Niccolò, Lund, Morten, Rimstad, Espen, Boysen, Preben, Dahle, Maria K, Teige, Lena Hammerlund, Kumar, Subramani, Johansen, Grethe M, Wessel, Øystein, Vendramin, Niccolò, Lund, Morten, Rimstad, Espen, Boysen, Preben, and Dahle, Maria K

Abstract

Bead-based multiplex immunoassays are promising tools for determination of the specific humoral immune response. In this study, we developed a multiplexed bead-based immunoassay for the detection of Atlantic salmon (Salmo salar) antibodies against Piscine orthoreovirus (PRV). Three different genotypes of PRV (PRV-1, PRV-2, and PRV-3) cause disease in farmed salmonids. The PRV outer capsid spike protein σ1 is predicted to be a host receptor binding protein and a target for neutralizing and protective antibodies. While recombinant σ1 performed poorly as an antigen to detect specific antibodies, N-terminal lipid modification of recombinant PRV-1 σ1 enabled sensitive detection of specific IgM in the bead-based assay. The specificity of anti-PRV-1 σ1 antibodies was confirmed by western blotting and pre-adsorption of plasma. Binding of non-specific IgM to beads coated with control antigens also increased after PRV infection, indicating a release of polyreactive antibodies. This non-specific binding was reduced by heat treatment of plasma. The same immunoassay also detected anti-PRV-3 σ1 antibodies from infected rainbow trout. In summary, a refined bead based immunoassay created by N-terminal lipid-modification of the PRV-1 σ1 antigen allowed sensitive detection of anti-PRV-1 and anti-PRV-3 antibodies from salmonids.

Published
2019

22. Dynamics of Polarized Macrophages and Activated CD8+ Cells in Heart Tissue of Atlantic Salmon Infected With Piscine Orthoreovirus-1.

Author

Malik, Muhammad Salman, Nyman, Ingvild Berg, Wessel, Øystein, Dahle, Maria K., and Rimstad, Espen

Subjects
HEART cells, ATLANTIC salmon, MYOCARDIUM, FLUORESCENCE in situ hybridization, MACROPHAGES
Abstract

Piscine orthoreovirus (PRV-1) infection causes heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon (Salmo salar). The virus is also associated with focal melanized changes in white skeletal muscle where PRV-1 infection of macrophages appears to be important. In this study, we studied the macrophage polarization into M1 (pro-inflammatory) and M2 (anti-inflammatory) phenotypes during experimentally induced HSMI. The immune response in heart with HSMI lesions was characterized by CD8+ and MHC-I expressing cells and not by polarized macrophages. Fluorescent in situ hybridization (FISH) assays revealed localization of PRV-1 in a few M1 macrophages in both heart and skeletal muscle. M2 type macrophages were widely scattered in the heart and were more abundant in heart compared to the skeletal muscle. However, the M2 macrophages did not co-stain for PRV-1. There was a strong cellular immune response to the infection in the heart compared to that of the skeletal muscle, seen as increased MHC-I expression, partly in cells also containing PRV-1 RNA, and a high number of cytotoxic CD8+ granzyme producing cells that targeted PRV-1. In skeletal muscle, MHC-I expressing cells and CD8+ cells were dispersed between myocytes, but these cells did not stain for PRV-1. Gene expression analysis by RT-qPCR complied with the FISH results and confirmed a drop in level of PRV-1 following the cell mediated immune response. Overall, the results indicated that M1 macrophages do not contribute to the initial development of HSMI. However, large numbers of M2 macrophages reside in the heart and may contribute to the subsequent fast recovery following clearance of PRV-1 infection. [ABSTRACT FROM AUTHOR]

Published
2021
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27. Evolution of the Piscine orthoreovirus Genome Linked to Emergence of Heart and Skeletal Muscle Inflammation in Farmed Atlantic Salmon (Salmo salar)

Author

Dhamotharan, Kannimuthu, primary, Tengs, Torstein, additional, Wessel, Øystein, additional, Braaen, Stine, additional, Nyman, Ingvild B., additional, Hansen, Elisabeth F., additional, Christiansen, Debes H., additional, Dahle, Maria K., additional, Rimstad, Espen, additional, and Markussen, Turhan, additional

Published
2019
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30. DNA vaccine expressing the non-structural proteins of Piscine orthoreovirus delay the kinetics of PRV infection and induces moderate protection against heart -and skeletal muscle inflammation in Atlantic salmon (Salmo salar)

Author

Haatveit, Hanne M., primary, Hodneland, Kjartan, additional, Braaen, Stine, additional, Hansen, Elisabeth F., additional, Nyman, Ingvild B., additional, Dahle, Maria K., additional, Frost, Petter, additional, and Rimstad, Espen, additional

Published
2018
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34. 9-cis Retinoic Acid Inhibits Inflammatory Responses of Adherent Monocytes and Increases Their Ability to Induce Classical Monocyte Migration

Author

Kolseth, Ingrid B.M., Ågren, Joanna, Sundvold-Gjerstad, Vibeke, Lyngstadaas, Staale P., Wang, Jacob E., and Dahle, Maria K.

Abstract

Patients with vitamin A/retinol deficiency are shown to be prone to infections and to suffer from increased inflammation, effects which can be remedied by vitamin A supplements. We aimed to study how human monocytes from the peripheral venous blood of healthy donors acted within the initial hours after adherence and exposure to bacterial endotoxin in the presence or absence of the 9-cis-isomer of retinoic acid (9cisRA). We found that adherent human monocytes were dominated by the CD14dimCD16+ subtype. Pretreatment with 9cisRA for 1 h significantly decreased lipopolysaccharide (LPS)-induced mRNA expression and protein release of tumor necrosis factor (TNF)α, interleukin (IL)-6 and chemokine ligands (CCL)3 and CCL4. In contrast, treatment with 9cisRA rapidly enhanced the production of monocyte chemoattractive protein/CCL2. 9cisRA treatment also led to enhanced migration of classical CD14high monocytes in a transwell in vitro system. We conclude that 9cisRA treatment of human adherent monocytes attenuates the inflammatory responses to LPS and induces the attraction of classical monocytes, a feature which may help explain why supplements administered to vitamin A-deficient patients counteract inflammation and increases the ability to fight infections.

Published
2024
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36. USF2 inhibits C/EBP-mediated transcriptional regulation of the RIIβ subunit of cAMP-dependent protein kinase

Author

Dahle, Maria K, Taskén, Kjetil, and Taskén, Austlid K

Subjects
endocrine system
Abstract

Background Cyclic AMP-dependent protein kinase (PKA) plays a central role in regulation of energy metabolism. Upon stimulation of testicular Sertoli cells by follicle stimulating hormone (FSH), glycolysis is activated to increase the production of nutrients for the germ cells, and a new regulatory subunit of cAMP-dependent protein kinase, RIIβ, is induced. We have previously shown that production of the transcription factor C/EBPβ is rapidly increased by FSH and cAMP in primary Sertoli cell cultures, and that C/EBPβ induces the RIIβ promoter. Results In this work we show that USF1, USF2 and truncated USF isoforms bind to a conserved E-box in the RIIβ gene. Interestingly, overexpression of USF2, but not USF1, led to inhibition of both cAMP- and C/EBPβ-mediated induction of RIIβ. Furthermore, Western blots show that a novel USF1 isoform is induced by cAMP in Sertoli cells. Conclusions These results indicate that the expression of various USF isoforms may be regulated by cAMP, and that the interplay between USF and C/EBPβ is important for cAMP-mediated regulation of RIIβ expression. The counteracting effects of USF2 and C/EBPβ observed on the RIIβ promoter is in accordance with the hypothesis that C/EBP and USF play opposite roles in regulation of glucose metabolism.

Published
2002

37. Correction: Sequence Analysis of the Genome of Piscine Orthoreovirus (PRV) Associated with Heart and Skeletal Muscle Inflammation (HSMI) in Atlantic Salmon (Salmo salar)

Author

Markussen, Turhan, primary, Dahle, Maria K., additional, Tengs, Torstein, additional, Løvoll, Marie, additional, Finstad, Øystein W., additional, Wiik-Nielsen, Christer R., additional, Grove, Søren, additional, Lauksund, Silje, additional, Robertsen, Børre, additional, and Rimstad, Espen, additional

Published
2013
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38. Sequence Analysis of the Genome of Piscine Orthoreovirus (PRV) Associated with Heart and Skeletal Muscle Inflammation (HSMI) in Atlantic Salmon (Salmo salar)

Author

Markussen, Turhan, primary, Dahle, Maria K., additional, Tengs, Torstein, additional, Løvoll, Marie, additional, Finstad, Øystein W., additional, Wiik-Nielsen, Christer R., additional, Grove, Søren, additional, Lauksund, Silje, additional, Robertsen, Børre, additional, and Rimstad, Espen, additional

Published
2013
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43. Liver X Receptor Protects against Liver Injury in Sepsis Caused by Rodent Cecal Ligation and Puncture

Author

Wang, Yun Yong, primary, Ryg, Una, additional, Dahle, Maria K., additional, Steffensen, Knut R., additional, Thiemermann, Christoph, additional, Chaudry, Irshad H., additional, Reinholt, Finn P., additional, Collins, Jon L., additional, Nebb, Hilde I., additional, Aasen, Ansgar O., additional, Gustafsson, Jan-Åke, additional, and Wang, Jacob E., additional

Published
2011
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44. LIVER X RECEPTOR AGONIST GW3965 DOSE-DEPENDENTLY REGULATES LPS-MEDIATED LIVER INJURY AND MODULATES POSTTRANSCRIPTIONAL TNF-α PRODUCTION AND P38 MITOGEN-ACTIVATED PROTEIN KINASE ACTIVATION IN LIVER MACROPHAGES

Author

Wang, Yun Yong, primary, Dahle, Maria K., additional, Steffensen, Knut R., additional, Reinholt, Finn P., additional, Collins, Jon L., additional, Thiemermann, Christoph, additional, Aasen, Ansgar O., additional, Gustafsson, Jan-Åke, additional, and Wang, Jacob E., additional

Published
2009
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