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

Heart and skeletal muscle inflammation (HSMI), caused by infection with Piscine orthoreovirus-1 (PRV-1), is a common disease in farmed Atlantic salmon ( Salmo salar ). Both an inactivated whole virus vaccine and a DNA vaccine have previously been tested experimentally against HSMI and demonstrated t...

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Published in:Vaccines
Main Authors: Muhammad Salman Malik, Lena H. Teige, Stine Braaen, Anne Berit Olsen, Monica Nordberg, Marit M. Amundsen, Kannimuthu Dhamotharan, Steingrim Svenning, Eva Stina Edholm, Tomokazu Takano, Jorunn B. Jørgensen, Øystein Wessel, Espen Rimstad, Maria K. Dahle
Format: Article in Journal/Newspaper
Language:English
Published: MDPI AG 2021
Subjects:
R
Online Access:https://doi.org/10.3390/vaccines9030230
https://doaj.org/article/3e749278f3c64f52a269a40398c0de5c
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spelling ftdoajarticles:oai:doaj.org/article:3e749278f3c64f52a269a40398c0de5c 2024-01-07T09:42:11+01:00 Piscine Orthoreovirus (PRV)-3, but Not PRV-2, Cross-Protects against PRV-1 and Heart and Skeletal Muscle Inflammation in Atlantic Salmon Muhammad Salman Malik Lena H. Teige Stine Braaen Anne Berit Olsen Monica Nordberg Marit M. Amundsen Kannimuthu Dhamotharan Steingrim Svenning Eva Stina Edholm Tomokazu Takano Jorunn B. Jørgensen Øystein Wessel Espen Rimstad Maria K. Dahle 2021-03-01T00:00:00Z https://doi.org/10.3390/vaccines9030230 https://doaj.org/article/3e749278f3c64f52a269a40398c0de5c EN eng MDPI AG https://www.mdpi.com/2076-393X/9/3/230 https://doaj.org/toc/2076-393X doi:10.3390/vaccines9030230 2076-393X https://doaj.org/article/3e749278f3c64f52a269a40398c0de5c Vaccines, Vol 9, Iss 3, p 230 (2021) heart and skeletal muscle inflammation Piscine orthoreovirus vaccine atlantic salmon antibodies immune response Medicine R article 2021 ftdoajarticles https://doi.org/10.3390/vaccines9030230 2023-12-10T01:46:52Z Heart and skeletal muscle inflammation (HSMI), caused by infection with Piscine orthoreovirus-1 (PRV-1), is a common disease in farmed Atlantic salmon ( Salmo salar ). Both an inactivated whole virus vaccine and a DNA vaccine have previously been tested experimentally against HSMI and demonstrated to give partial but not full protection. To understand the mechanisms involved in protection against HSMI and evaluate the potential of live attenuated vaccine strategies, we set up a cross-protection experiment using PRV genotypes not associated with disease development in Atlantic salmon. The three known genotypes of PRV differ in their preference of salmonid host species. The main target species for PRV-1 is Atlantic salmon. Coho salmon ( Oncorhynchus kisutch ) is the target species for PRV-2, where the infection may induce erythrocytic inclusion body syndrome (EIBS). PRV-3 is associated with heart pathology and anemia in rainbow trout, but brown trout ( S. trutta ) is the likely natural main host species. Here, we tested if primary infection with PRV-2 or PRV-3 in Atlantic salmon could induce protection against secondary PRV-1 infection, in comparison with an adjuvanted, inactivated PRV-1 vaccine. Viral kinetics, production of cross-reactive antibodies, and protection against HSMI were studied. PRV-3, and to a low extent PRV-2, induced antibodies cross-reacting with the PRV-1 σ1 protein, whereas no specific antibodies were detected after vaccination with inactivated PRV-1. Ten weeks after immunization, the fish were challenged through cohabitation with PRV-1-infected shedder fish. A primary PRV-3 infection completely blocked PRV-1 infection, while PRV-2 only reduced PRV-1 infection levels and the severity of HSMI pathology in a few individuals. This study indicates that infection with non-pathogenic, replicating PRV could be a future strategy to protect farmed salmon from HSMI. Article in Journal/Newspaper Atlantic salmon Salmo salar Directory of Open Access Journals: DOAJ Articles Vaccines 9 3 230
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic heart and skeletal muscle inflammation
Piscine orthoreovirus
vaccine
atlantic salmon
antibodies
immune response
Medicine
R
spellingShingle heart and skeletal muscle inflammation
Piscine orthoreovirus
vaccine
atlantic salmon
antibodies
immune response
Medicine
R
Muhammad Salman Malik
Lena H. Teige
Stine Braaen
Anne Berit Olsen
Monica Nordberg
Marit M. Amundsen
Kannimuthu Dhamotharan
Steingrim Svenning
Eva Stina Edholm
Tomokazu Takano
Jorunn B. Jørgensen
Øystein Wessel
Espen Rimstad
Maria K. Dahle
Piscine Orthoreovirus (PRV)-3, but Not PRV-2, Cross-Protects against PRV-1 and Heart and Skeletal Muscle Inflammation in Atlantic Salmon
topic_facet heart and skeletal muscle inflammation
Piscine orthoreovirus
vaccine
atlantic salmon
antibodies
immune response
Medicine
R
description Heart and skeletal muscle inflammation (HSMI), caused by infection with Piscine orthoreovirus-1 (PRV-1), is a common disease in farmed Atlantic salmon ( Salmo salar ). Both an inactivated whole virus vaccine and a DNA vaccine have previously been tested experimentally against HSMI and demonstrated to give partial but not full protection. To understand the mechanisms involved in protection against HSMI and evaluate the potential of live attenuated vaccine strategies, we set up a cross-protection experiment using PRV genotypes not associated with disease development in Atlantic salmon. The three known genotypes of PRV differ in their preference of salmonid host species. The main target species for PRV-1 is Atlantic salmon. Coho salmon ( Oncorhynchus kisutch ) is the target species for PRV-2, where the infection may induce erythrocytic inclusion body syndrome (EIBS). PRV-3 is associated with heart pathology and anemia in rainbow trout, but brown trout ( S. trutta ) is the likely natural main host species. Here, we tested if primary infection with PRV-2 or PRV-3 in Atlantic salmon could induce protection against secondary PRV-1 infection, in comparison with an adjuvanted, inactivated PRV-1 vaccine. Viral kinetics, production of cross-reactive antibodies, and protection against HSMI were studied. PRV-3, and to a low extent PRV-2, induced antibodies cross-reacting with the PRV-1 σ1 protein, whereas no specific antibodies were detected after vaccination with inactivated PRV-1. Ten weeks after immunization, the fish were challenged through cohabitation with PRV-1-infected shedder fish. A primary PRV-3 infection completely blocked PRV-1 infection, while PRV-2 only reduced PRV-1 infection levels and the severity of HSMI pathology in a few individuals. This study indicates that infection with non-pathogenic, replicating PRV could be a future strategy to protect farmed salmon from HSMI.
format Article in Journal/Newspaper
author Muhammad Salman Malik
Lena H. Teige
Stine Braaen
Anne Berit Olsen
Monica Nordberg
Marit M. Amundsen
Kannimuthu Dhamotharan
Steingrim Svenning
Eva Stina Edholm
Tomokazu Takano
Jorunn B. Jørgensen
Øystein Wessel
Espen Rimstad
Maria K. Dahle
author_facet Muhammad Salman Malik
Lena H. Teige
Stine Braaen
Anne Berit Olsen
Monica Nordberg
Marit M. Amundsen
Kannimuthu Dhamotharan
Steingrim Svenning
Eva Stina Edholm
Tomokazu Takano
Jorunn B. Jørgensen
Øystein Wessel
Espen Rimstad
Maria K. Dahle
author_sort Muhammad Salman Malik
title Piscine Orthoreovirus (PRV)-3, but Not PRV-2, Cross-Protects against PRV-1 and Heart and Skeletal Muscle Inflammation in Atlantic Salmon
title_short Piscine Orthoreovirus (PRV)-3, but Not PRV-2, Cross-Protects against PRV-1 and Heart and Skeletal Muscle Inflammation in Atlantic Salmon
title_full Piscine Orthoreovirus (PRV)-3, but Not PRV-2, Cross-Protects against PRV-1 and Heart and Skeletal Muscle Inflammation in Atlantic Salmon
title_fullStr Piscine Orthoreovirus (PRV)-3, but Not PRV-2, Cross-Protects against PRV-1 and Heart and Skeletal Muscle Inflammation in Atlantic Salmon
title_full_unstemmed Piscine Orthoreovirus (PRV)-3, but Not PRV-2, Cross-Protects against PRV-1 and Heart and Skeletal Muscle Inflammation in Atlantic Salmon
title_sort piscine orthoreovirus (prv)-3, but not prv-2, cross-protects against prv-1 and heart and skeletal muscle inflammation in atlantic salmon
publisher MDPI AG
publishDate 2021
url https://doi.org/10.3390/vaccines9030230
https://doaj.org/article/3e749278f3c64f52a269a40398c0de5c
genre Atlantic salmon
Salmo salar
genre_facet Atlantic salmon
Salmo salar
op_source Vaccines, Vol 9, Iss 3, p 230 (2021)
op_relation https://www.mdpi.com/2076-393X/9/3/230
https://doaj.org/toc/2076-393X
doi:10.3390/vaccines9030230
2076-393X
https://doaj.org/article/3e749278f3c64f52a269a40398c0de5c
op_doi https://doi.org/10.3390/vaccines9030230
container_title Vaccines
container_volume 9
container_issue 3
container_start_page 230
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