Erythroid Progenitor Cells in Atlantic Salmon (<i>Salmo salar</i>) May Be Persistently and Productively Infected with Piscine Orthoreovirus (PRV)

Piscine orthoreovirus (PRV-1) can cause heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon (<i>Salmo salar</i>). The virus targets erythrocytes in the acute peak phase, followed by cardiomyocytes, before the infection subsides into persistence. The persistent phase i...

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Main Authors: Muhammad Salman Malik, Håvard Bjørgen, Kannimuthu Dhamotharan, Øystein Wessel, Erling Olaf Koppang, Emiliano Di Cicco, Elisabeth F. Hansen, Maria K. Dahle, Espen Rimstad
Format: Article
Language:English
Published: MDPI AG 2019-09-01
Series:Viruses
Subjects:
Online Access:https://www.mdpi.com/1999-4915/11/9/824
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spelling doaj-feb6fba1a9a94654bc25e08a6867bfed2020-11-25T01:20:33ZengMDPI AGViruses1999-49152019-09-0111982410.3390/v11090824v11090824Erythroid Progenitor Cells in Atlantic Salmon (<i>Salmo salar</i>) May Be Persistently and Productively Infected with Piscine Orthoreovirus (PRV)Muhammad Salman Malik0Håvard Bjørgen1Kannimuthu Dhamotharan2Øystein Wessel3Erling Olaf Koppang4Emiliano Di Cicco5Elisabeth F. Hansen6Maria K. Dahle7Espen Rimstad8Department of Food Safety and Infection Biology, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, 0454 Oslo, NorwayDepartment of Basic Science and Aquatic Medicine, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, 0454 Oslo, NorwayDepartment of Food Safety and Infection Biology, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, 0454 Oslo, NorwayDepartment of Food Safety and Infection Biology, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, 0454 Oslo, NorwayDepartment of Basic Science and Aquatic Medicine, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, 0454 Oslo, NorwayPacific Biological Station, Fisheries and Oceans Canada, Nanaimo, BC V9T 6N7, CanadaDepartment of Food Safety and Infection Biology, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, 0454 Oslo, NorwayDepartment of Fish Health, Norwegian Veterinary Institute, 0454 Oslo, NorwayDepartment of Food Safety and Infection Biology, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, 0454 Oslo, NorwayPiscine orthoreovirus (PRV-1) can cause heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon (<i>Salmo salar</i>). The virus targets erythrocytes in the acute peak phase, followed by cardiomyocytes, before the infection subsides into persistence. The persistent phase is characterized by high level of viral RNA, but low level of viral protein. The origin and nature of persistent PRV-1 are not clear. Here, we analyzed for viral persistence and activity in various tissues and cell types in experimentally infected Atlantic salmon. Plasma contained PRV-1 genomic dsRNA throughout an 18-week long infection trial, indicating that viral particles are continuously produced and released. The highest level of PRV-1 RNA in the persistent phase was found in kidney. The level of PRV-1 ssRNA transcripts in kidney was significantly higher than that of blood cells in the persistent phase. In-situ hybridization assays confirmed that PRV-1 RNA was present in erythroid progenitor cells, erythrocytes, macrophages, melano-macrophages and in some additional un-characterized cells in kidney. These results show that PRV-1 establishes a productive, persistent infection in Atlantic salmon and that erythrocyte progenitor cells are PRV target cells.https://www.mdpi.com/1999-4915/11/9/824PRV-1piscine orthoreoviruspersistenceerythroid progenitor cells
collection DOAJ
language English
format Article
sources DOAJ
author Muhammad Salman Malik
Håvard Bjørgen
Kannimuthu Dhamotharan
Øystein Wessel
Erling Olaf Koppang
Emiliano Di Cicco
Elisabeth F. Hansen
Maria K. Dahle
Espen Rimstad
spellingShingle Muhammad Salman Malik
Håvard Bjørgen
Kannimuthu Dhamotharan
Øystein Wessel
Erling Olaf Koppang
Emiliano Di Cicco
Elisabeth F. Hansen
Maria K. Dahle
Espen Rimstad
Erythroid Progenitor Cells in Atlantic Salmon (<i>Salmo salar</i>) May Be Persistently and Productively Infected with Piscine Orthoreovirus (PRV)
Viruses
PRV-1
piscine orthoreovirus
persistence
erythroid progenitor cells
author_facet Muhammad Salman Malik
Håvard Bjørgen
Kannimuthu Dhamotharan
Øystein Wessel
Erling Olaf Koppang
Emiliano Di Cicco
Elisabeth F. Hansen
Maria K. Dahle
Espen Rimstad
author_sort Muhammad Salman Malik
title Erythroid Progenitor Cells in Atlantic Salmon (<i>Salmo salar</i>) May Be Persistently and Productively Infected with Piscine Orthoreovirus (PRV)
title_short Erythroid Progenitor Cells in Atlantic Salmon (<i>Salmo salar</i>) May Be Persistently and Productively Infected with Piscine Orthoreovirus (PRV)
title_full Erythroid Progenitor Cells in Atlantic Salmon (<i>Salmo salar</i>) May Be Persistently and Productively Infected with Piscine Orthoreovirus (PRV)
title_fullStr Erythroid Progenitor Cells in Atlantic Salmon (<i>Salmo salar</i>) May Be Persistently and Productively Infected with Piscine Orthoreovirus (PRV)
title_full_unstemmed Erythroid Progenitor Cells in Atlantic Salmon (<i>Salmo salar</i>) May Be Persistently and Productively Infected with Piscine Orthoreovirus (PRV)
title_sort erythroid progenitor cells in atlantic salmon (<i>salmo salar</i>) may be persistently and productively infected with piscine orthoreovirus (prv)
publisher MDPI AG
series Viruses
issn 1999-4915
publishDate 2019-09-01
description Piscine orthoreovirus (PRV-1) can cause heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon (<i>Salmo salar</i>). The virus targets erythrocytes in the acute peak phase, followed by cardiomyocytes, before the infection subsides into persistence. The persistent phase is characterized by high level of viral RNA, but low level of viral protein. The origin and nature of persistent PRV-1 are not clear. Here, we analyzed for viral persistence and activity in various tissues and cell types in experimentally infected Atlantic salmon. Plasma contained PRV-1 genomic dsRNA throughout an 18-week long infection trial, indicating that viral particles are continuously produced and released. The highest level of PRV-1 RNA in the persistent phase was found in kidney. The level of PRV-1 ssRNA transcripts in kidney was significantly higher than that of blood cells in the persistent phase. In-situ hybridization assays confirmed that PRV-1 RNA was present in erythroid progenitor cells, erythrocytes, macrophages, melano-macrophages and in some additional un-characterized cells in kidney. These results show that PRV-1 establishes a productive, persistent infection in Atlantic salmon and that erythrocyte progenitor cells are PRV target cells.
topic PRV-1
piscine orthoreovirus
persistence
erythroid progenitor cells
url https://www.mdpi.com/1999-4915/11/9/824
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