A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, Crassostrea gigas

Over the last decade, innate immune priming has been evidenced in many invertebrate phyla. If mechanistic models have been proposed, molecular studies aiming to substantiate these models have remained scarce. We reveal here the transcriptional signature associated with immune priming in the oyster C...

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Published in:mBio
Main Authors: Lafont, Maxime, Vergnes, Agnes, Vidal-dupiol, Jeremie, De Lorgeril, Julien, Gueguen, Yannick, Haffner, Philippe, Petton, Bruno, Chaparro, Cristian, Barrachina, Celia, Destoumieux-garzon, Delphine, Mitta, Guillaume, Gourbal, Benjamin, Montagnani, Caroline
Format: Article in Journal/Newspaper
Language:English
Published: American Society for Microbiology 2020
Subjects:
Online Access:https://archimer.ifremer.fr/doc/00614/72580/71541.pdf
https://archimer.ifremer.fr/doc/00614/72580/71542.xlsx
https://archimer.ifremer.fr/doc/00614/72580/71543.tif
https://archimer.ifremer.fr/doc/00614/72580/71544.tif
https://archimer.ifremer.fr/doc/00614/72580/71545.xlsx
https://archimer.ifremer.fr/doc/00614/72580/71546.xlsx
https://archimer.ifremer.fr/doc/00614/72580/71547.eps
https://archimer.ifremer.fr/doc/00614/72580/71548.xlsx
https://archimer.ifremer.fr/doc/00614/72580/71549.xlsx
https://archimer.ifremer.fr/doc/00614/72580/71550.tif
https://archimer.ifremer.fr/doc/00614/72580/71551.tif
https://doi.org/10.1128/mBio.02777-19
https://archimer.ifremer.fr/doc/00614/72580/
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spelling ftarchimer:oai:archimer.ifremer.fr:72580 2023-11-12T04:16:08+01:00 A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, Crassostrea gigas Lafont, Maxime Vergnes, Agnes Vidal-dupiol, Jeremie De Lorgeril, Julien Gueguen, Yannick Haffner, Philippe Petton, Bruno Chaparro, Cristian Barrachina, Celia Destoumieux-garzon, Delphine Mitta, Guillaume Gourbal, Benjamin Montagnani, Caroline 2020-03 application/pdf https://archimer.ifremer.fr/doc/00614/72580/71541.pdf https://archimer.ifremer.fr/doc/00614/72580/71542.xlsx https://archimer.ifremer.fr/doc/00614/72580/71543.tif https://archimer.ifremer.fr/doc/00614/72580/71544.tif https://archimer.ifremer.fr/doc/00614/72580/71545.xlsx https://archimer.ifremer.fr/doc/00614/72580/71546.xlsx https://archimer.ifremer.fr/doc/00614/72580/71547.eps https://archimer.ifremer.fr/doc/00614/72580/71548.xlsx https://archimer.ifremer.fr/doc/00614/72580/71549.xlsx https://archimer.ifremer.fr/doc/00614/72580/71550.tif https://archimer.ifremer.fr/doc/00614/72580/71551.tif https://doi.org/10.1128/mBio.02777-19 https://archimer.ifremer.fr/doc/00614/72580/ eng eng American Society for Microbiology info:eu-repo/grantAgreement/EC/FP7/678589/EU//VIVALDI https://archimer.ifremer.fr/doc/00614/72580/71541.pdf https://archimer.ifremer.fr/doc/00614/72580/71542.xlsx https://archimer.ifremer.fr/doc/00614/72580/71543.tif https://archimer.ifremer.fr/doc/00614/72580/71544.tif https://archimer.ifremer.fr/doc/00614/72580/71545.xlsx https://archimer.ifremer.fr/doc/00614/72580/71546.xlsx https://archimer.ifremer.fr/doc/00614/72580/71547.eps https://archimer.ifremer.fr/doc/00614/72580/71548.xlsx https://archimer.ifremer.fr/doc/00614/72580/71549.xlsx https://archimer.ifremer.fr/doc/00614/72580/71550.tif https://archimer.ifremer.fr/doc/00614/72580/71551.tif doi:10.1128/mBio.02777-19 https://archimer.ifremer.fr/doc/00614/72580/ info:eu-repo/semantics/openAccess restricted use Mbio (2150-7511) (American Society for Microbiology), 2020-03 , Vol. 11 , N. 2 , P. e02777-19 (17p.) innate immunity priming OsHV-1 antiviral response immune memory oyster POMS poly(I-C) interferon transcriptomic text Article info:eu-repo/semantics/article 2020 ftarchimer https://doi.org/10.1128/mBio.02777-19 2023-10-17T22:51:11Z Over the last decade, innate immune priming has been evidenced in many invertebrate phyla. If mechanistic models have been proposed, molecular studies aiming to substantiate these models have remained scarce. We reveal here the transcriptional signature associated with immune priming in the oyster Crassostrea gigas. Oysters were fully protected against Ostreid herpesvirus 1 (OsHV-1), a major oyster pathogen, after priming with poly(I·C), which mimics viral double-stranded RNA. Global analysis through RNA sequencing of oyster and viral genes after immune priming and viral infection revealed that poly(I·C) induces a strong antiviral response that impairs OsHV-1 replication. Protection is based on a sustained upregulation of immune genes, notably genes involved in the interferon pathway and apoptosis, which control subsequent viral infection. This persistent antiviral alert state remains active over 4 months and supports antiviral protection in the long term. This acquired resistance mechanism reinforces the molecular foundations of the sustained response model of immune priming. It further opens the way to applications (pseudovaccination) to cope with a recurrent disease that causes dramatic economic losses in the shellfish farming industry worldwide. Article in Journal/Newspaper Crassostrea gigas Pacific oyster Archimer (Archive Institutionnelle de l'Ifremer - Institut français de recherche pour l'exploitation de la mer) Pacific mBio 11 2
institution Open Polar
collection Archimer (Archive Institutionnelle de l'Ifremer - Institut français de recherche pour l'exploitation de la mer)
op_collection_id ftarchimer
language English
topic innate immunity
priming
OsHV-1
antiviral response
immune memory
oyster
POMS
poly(I-C)
interferon
transcriptomic
spellingShingle innate immunity
priming
OsHV-1
antiviral response
immune memory
oyster
POMS
poly(I-C)
interferon
transcriptomic
Lafont, Maxime
Vergnes, Agnes
Vidal-dupiol, Jeremie
De Lorgeril, Julien
Gueguen, Yannick
Haffner, Philippe
Petton, Bruno
Chaparro, Cristian
Barrachina, Celia
Destoumieux-garzon, Delphine
Mitta, Guillaume
Gourbal, Benjamin
Montagnani, Caroline
A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, Crassostrea gigas
topic_facet innate immunity
priming
OsHV-1
antiviral response
immune memory
oyster
POMS
poly(I-C)
interferon
transcriptomic
description Over the last decade, innate immune priming has been evidenced in many invertebrate phyla. If mechanistic models have been proposed, molecular studies aiming to substantiate these models have remained scarce. We reveal here the transcriptional signature associated with immune priming in the oyster Crassostrea gigas. Oysters were fully protected against Ostreid herpesvirus 1 (OsHV-1), a major oyster pathogen, after priming with poly(I·C), which mimics viral double-stranded RNA. Global analysis through RNA sequencing of oyster and viral genes after immune priming and viral infection revealed that poly(I·C) induces a strong antiviral response that impairs OsHV-1 replication. Protection is based on a sustained upregulation of immune genes, notably genes involved in the interferon pathway and apoptosis, which control subsequent viral infection. This persistent antiviral alert state remains active over 4 months and supports antiviral protection in the long term. This acquired resistance mechanism reinforces the molecular foundations of the sustained response model of immune priming. It further opens the way to applications (pseudovaccination) to cope with a recurrent disease that causes dramatic economic losses in the shellfish farming industry worldwide.
format Article in Journal/Newspaper
author Lafont, Maxime
Vergnes, Agnes
Vidal-dupiol, Jeremie
De Lorgeril, Julien
Gueguen, Yannick
Haffner, Philippe
Petton, Bruno
Chaparro, Cristian
Barrachina, Celia
Destoumieux-garzon, Delphine
Mitta, Guillaume
Gourbal, Benjamin
Montagnani, Caroline
author_facet Lafont, Maxime
Vergnes, Agnes
Vidal-dupiol, Jeremie
De Lorgeril, Julien
Gueguen, Yannick
Haffner, Philippe
Petton, Bruno
Chaparro, Cristian
Barrachina, Celia
Destoumieux-garzon, Delphine
Mitta, Guillaume
Gourbal, Benjamin
Montagnani, Caroline
author_sort Lafont, Maxime
title A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, Crassostrea gigas
title_short A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, Crassostrea gigas
title_full A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, Crassostrea gigas
title_fullStr A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, Crassostrea gigas
title_full_unstemmed A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, Crassostrea gigas
title_sort sustained immune response supports long-term antiviral immune priming in the pacific oyster, crassostrea gigas
publisher American Society for Microbiology
publishDate 2020
url https://archimer.ifremer.fr/doc/00614/72580/71541.pdf
https://archimer.ifremer.fr/doc/00614/72580/71542.xlsx
https://archimer.ifremer.fr/doc/00614/72580/71543.tif
https://archimer.ifremer.fr/doc/00614/72580/71544.tif
https://archimer.ifremer.fr/doc/00614/72580/71545.xlsx
https://archimer.ifremer.fr/doc/00614/72580/71546.xlsx
https://archimer.ifremer.fr/doc/00614/72580/71547.eps
https://archimer.ifremer.fr/doc/00614/72580/71548.xlsx
https://archimer.ifremer.fr/doc/00614/72580/71549.xlsx
https://archimer.ifremer.fr/doc/00614/72580/71550.tif
https://archimer.ifremer.fr/doc/00614/72580/71551.tif
https://doi.org/10.1128/mBio.02777-19
https://archimer.ifremer.fr/doc/00614/72580/
geographic Pacific
geographic_facet Pacific
genre Crassostrea gigas
Pacific oyster
genre_facet Crassostrea gigas
Pacific oyster
op_source Mbio (2150-7511) (American Society for Microbiology), 2020-03 , Vol. 11 , N. 2 , P. e02777-19 (17p.)
op_relation info:eu-repo/grantAgreement/EC/FP7/678589/EU//VIVALDI
https://archimer.ifremer.fr/doc/00614/72580/71541.pdf
https://archimer.ifremer.fr/doc/00614/72580/71542.xlsx
https://archimer.ifremer.fr/doc/00614/72580/71543.tif
https://archimer.ifremer.fr/doc/00614/72580/71544.tif
https://archimer.ifremer.fr/doc/00614/72580/71545.xlsx
https://archimer.ifremer.fr/doc/00614/72580/71546.xlsx
https://archimer.ifremer.fr/doc/00614/72580/71547.eps
https://archimer.ifremer.fr/doc/00614/72580/71548.xlsx
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https://archimer.ifremer.fr/doc/00614/72580/71550.tif
https://archimer.ifremer.fr/doc/00614/72580/71551.tif
doi:10.1128/mBio.02777-19
https://archimer.ifremer.fr/doc/00614/72580/
op_rights info:eu-repo/semantics/openAccess
restricted use
op_doi https://doi.org/10.1128/mBio.02777-19
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