A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, Crassostrea gigas
International audience 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...
Published in: | mBio |
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Main Authors: | , , , , , , , , , , , , |
Other Authors: | , , , , , , , , , , , , |
Format: | Article in Journal/Newspaper |
Language: | English |
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HAL CCSD
2020
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Subjects: | |
Online Access: | https://hal.archives-ouvertes.fr/hal-02527469 https://hal.archives-ouvertes.fr/hal-02527469/document https://hal.archives-ouvertes.fr/hal-02527469/file/Lafont-2020-MBio.pdf https://doi.org/10.1128/mBio.02777-19 |
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Open Polar |
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Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe) |
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ftccsdartic |
language |
English |
topic |
immune memory antiviral response transcriptomic POMS poly(I·C) interferon oyster innate immunity priming OsHV-1 [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE] [SDE.BE]Environmental Sciences/Biodiversity and Ecology |
spellingShingle |
immune memory antiviral response transcriptomic POMS poly(I·C) interferon oyster innate immunity priming OsHV-1 [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE] [SDE.BE]Environmental Sciences/Biodiversity and Ecology Lafont, Maxime Vergnes, Agnès Vidal-Dupiol, Jeremie De Lorgeril, Julien Guéguen, Yannick Haffner, Philippe Petton, Bruno Chaparro, Cristian Barrachina, Célia Destoumieux-Garzón, 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 |
immune memory antiviral response transcriptomic POMS poly(I·C) interferon oyster innate immunity priming OsHV-1 [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE] [SDE.BE]Environmental Sciences/Biodiversity and Ecology |
description |
International audience 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 Cras-sostrea 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 anti-viral 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. IMPORTANCE In the last decade, important discoveries have shown that resistance to reinfection can be achieved without a functional adaptive immune system, introducing the concept of innate immune memory in invertebrates. However, this field has been constrained by the limited number of molecular mechanisms evidenced to support these phenomena. Taking advantage of an invertebrate species, the Pacific oyster (Crassostrea gigas), in which we evidenced one of the longest and most effective periods of protection against viral infection observed in an invertebrate, we provide the first comprehensive transcriptomic analysis of antiviral innate immune priming. We show that priming with poly(I·C) induced a massive upregulation of immune-related ... |
author2 |
Interactions Hôtes-Pathogènes-Environnements (IHPE) Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Perpignan Via Domitia (UPVD) Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR) Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM) Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS) Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER) Institut de Génomique Fonctionnelle - Montpellier GenomiX (IGF MGX) Institut de Génomique Fonctionnelle (IGF) Université de Montpellier (UM)-Université Montpellier 1 (UM1)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Université Montpellier 1 (UM1)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Centre National de la Recherche Scientifique (CNRS) ANR-14-CE19-0023,DECIPHER,Déchiffrage des maladies multifactorielles: cas des mortalités de l'huître(2014) ANR-13-JSV7-0009,INVIMORY,Immunité mémoire chez les invertébrés : spécificité et mécanismes de l'immunité mémoire chez le mollusque Lophotrochozoaire Biomphalaria glabrata.(2013) ANR-11-IDEX-0002,UNITI,Université Fédérale de Toulouse(2011) European Project: 678589,H2020,H2020-SFS-2015-2,VIVALDI(2016) |
format |
Article in Journal/Newspaper |
author |
Lafont, Maxime Vergnes, Agnès Vidal-Dupiol, Jeremie De Lorgeril, Julien Guéguen, Yannick Haffner, Philippe Petton, Bruno Chaparro, Cristian Barrachina, Célia Destoumieux-Garzón, Delphine Mitta, Guillaume Gourbal, Benjamin Montagnani, Caroline |
author_facet |
Lafont, Maxime Vergnes, Agnès Vidal-Dupiol, Jeremie De Lorgeril, Julien Guéguen, Yannick Haffner, Philippe Petton, Bruno Chaparro, Cristian Barrachina, Célia Destoumieux-Garzón, 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 |
HAL CCSD |
publishDate |
2020 |
url |
https://hal.archives-ouvertes.fr/hal-02527469 https://hal.archives-ouvertes.fr/hal-02527469/document https://hal.archives-ouvertes.fr/hal-02527469/file/Lafont-2020-MBio.pdf https://doi.org/10.1128/mBio.02777-19 |
geographic |
Pacific |
geographic_facet |
Pacific |
genre |
Crassostrea gigas Pacific oyster |
genre_facet |
Crassostrea gigas Pacific oyster |
op_source |
ISSN: 2161-2129 EISSN: 2150-7511 mBio https://hal.archives-ouvertes.fr/hal-02527469 mBio, American Society for Microbiology, 2020, ⟨10.1128/mBio.02777-19⟩ |
op_relation |
info:eu-repo/semantics/altIdentifier/doi/10.1128/mBio.02777-19 info:eu-repo/grantAgreement//678589/EU/Preventing and mitigating farmed bivalve diseases/VIVALDI hal-02527469 https://hal.archives-ouvertes.fr/hal-02527469 https://hal.archives-ouvertes.fr/hal-02527469/document https://hal.archives-ouvertes.fr/hal-02527469/file/Lafont-2020-MBio.pdf doi:10.1128/mBio.02777-19 |
op_rights |
info:eu-repo/semantics/OpenAccess |
op_doi |
https://doi.org/10.1128/mBio.02777-19 |
container_title |
mBio |
container_volume |
11 |
container_issue |
2 |
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1766394153595305984 |
spelling |
ftccsdartic:oai:HAL:hal-02527469v1 2023-05-15T15:58:25+02:00 A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, Crassostrea gigas Lafont, Maxime Vergnes, Agnès Vidal-Dupiol, Jeremie De Lorgeril, Julien Guéguen, Yannick Haffner, Philippe Petton, Bruno Chaparro, Cristian Barrachina, Célia Destoumieux-Garzón, Delphine Mitta, Guillaume Gourbal, Benjamin Montagnani, Caroline Interactions Hôtes-Pathogènes-Environnements (IHPE) Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Perpignan Via Domitia (UPVD) Laboratoire des Sciences de l'Environnement Marin (LEMAR) (LEMAR) Institut de Recherche pour le Développement (IRD)-Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER)-Université de Brest (UBO)-Institut Universitaire Européen de la Mer (IUEM) Institut de Recherche pour le Développement (IRD)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Institut national des sciences de l'Univers (INSU - CNRS)-Université de Brest (UBO)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS) Institut Français de Recherche pour l'Exploitation de la Mer (IFREMER) Institut de Génomique Fonctionnelle - Montpellier GenomiX (IGF MGX) Institut de Génomique Fonctionnelle (IGF) Université de Montpellier (UM)-Université Montpellier 1 (UM1)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Université Montpellier 1 (UM1)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Centre National de la Recherche Scientifique (CNRS) ANR-14-CE19-0023,DECIPHER,Déchiffrage des maladies multifactorielles: cas des mortalités de l'huître(2014) ANR-13-JSV7-0009,INVIMORY,Immunité mémoire chez les invertébrés : spécificité et mécanismes de l'immunité mémoire chez le mollusque Lophotrochozoaire Biomphalaria glabrata.(2013) ANR-11-IDEX-0002,UNITI,Université Fédérale de Toulouse(2011) European Project: 678589,H2020,H2020-SFS-2015-2,VIVALDI(2016) 2020-03-10 https://hal.archives-ouvertes.fr/hal-02527469 https://hal.archives-ouvertes.fr/hal-02527469/document https://hal.archives-ouvertes.fr/hal-02527469/file/Lafont-2020-MBio.pdf https://doi.org/10.1128/mBio.02777-19 en eng HAL CCSD American Society for Microbiology info:eu-repo/semantics/altIdentifier/doi/10.1128/mBio.02777-19 info:eu-repo/grantAgreement//678589/EU/Preventing and mitigating farmed bivalve diseases/VIVALDI hal-02527469 https://hal.archives-ouvertes.fr/hal-02527469 https://hal.archives-ouvertes.fr/hal-02527469/document https://hal.archives-ouvertes.fr/hal-02527469/file/Lafont-2020-MBio.pdf doi:10.1128/mBio.02777-19 info:eu-repo/semantics/OpenAccess ISSN: 2161-2129 EISSN: 2150-7511 mBio https://hal.archives-ouvertes.fr/hal-02527469 mBio, American Society for Microbiology, 2020, ⟨10.1128/mBio.02777-19⟩ immune memory antiviral response transcriptomic POMS poly(I·C) interferon oyster innate immunity priming OsHV-1 [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE] [SDE.BE]Environmental Sciences/Biodiversity and Ecology info:eu-repo/semantics/article Journal articles 2020 ftccsdartic https://doi.org/10.1128/mBio.02777-19 2021-12-19T01:24:56Z International audience 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 Cras-sostrea 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 anti-viral 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. IMPORTANCE In the last decade, important discoveries have shown that resistance to reinfection can be achieved without a functional adaptive immune system, introducing the concept of innate immune memory in invertebrates. However, this field has been constrained by the limited number of molecular mechanisms evidenced to support these phenomena. Taking advantage of an invertebrate species, the Pacific oyster (Crassostrea gigas), in which we evidenced one of the longest and most effective periods of protection against viral infection observed in an invertebrate, we provide the first comprehensive transcriptomic analysis of antiviral innate immune priming. We show that priming with poly(I·C) induced a massive upregulation of immune-related ... Article in Journal/Newspaper Crassostrea gigas Pacific oyster Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe) Pacific mBio 11 2 |