Long-lasting antiviral innate immune priming in the Lophotrochozoan Pacific oyster, Crassostrea gigas

International audience In the last decade, a paradigm shift has emerged in comparative immunology. Invertebrates can no longer be considered to be devoid of specific recognition and immune memory. However, we still lack a comprehensive view of these phenomena and their molecular mechanisms across ph...

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Published in:Scientific Reports
Main Authors: Lafont, Maxime, Petton, Bruno, Vergnes, Agnès, Pauletto, Marianna, Segarra, Amélie, Gourbal, Benjamin, Montagnani, Caroline
Other Authors: 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), Universita degli Studi di Padova, ANR-14-CE19-0023,DECIPHER,Déchiffrage des maladies multifactorielles: cas des mortalités de l'huître(2014)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2017
Subjects:
ACL
Online Access:https://hal.archives-ouvertes.fr/hal-01632346
https://hal.archives-ouvertes.fr/hal-01632346/document
https://hal.archives-ouvertes.fr/hal-01632346/file/Lafont-2017-SciRep.LongLasting.pdf
https://doi.org/10.1038/s41598-017-13564-0
id ftccsdartic:oai:HAL:hal-01632346v1
record_format openpolar
institution Open Polar
collection Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe)
op_collection_id ftccsdartic
language English
topic SECONDARY CHALLENGE
OSTREID HERPESVIRUS-1
SPOT SYNDROME VIRUS
DOUBLE-STRANDED-RNA
VIBRIO-SPLENDIDUS
INVERTEBRATE IMMUNITY
IN-VIVO
INFECTION
MEMORY
RESPONSES
ACL
[SDV.IMM.II]Life Sciences [q-bio]/Immunology/Innate immunity
[SDV.BA.ZI]Life Sciences [q-bio]/Animal biology/Invertebrate Zoology
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
spellingShingle SECONDARY CHALLENGE
OSTREID HERPESVIRUS-1
SPOT SYNDROME VIRUS
DOUBLE-STRANDED-RNA
VIBRIO-SPLENDIDUS
INVERTEBRATE IMMUNITY
IN-VIVO
INFECTION
MEMORY
RESPONSES
ACL
[SDV.IMM.II]Life Sciences [q-bio]/Immunology/Innate immunity
[SDV.BA.ZI]Life Sciences [q-bio]/Animal biology/Invertebrate Zoology
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
Lafont, Maxime
Petton, Bruno
Vergnes, Agnès
Pauletto, Marianna
Segarra, Amélie
Gourbal, Benjamin
Montagnani, Caroline
Long-lasting antiviral innate immune priming in the Lophotrochozoan Pacific oyster, Crassostrea gigas
topic_facet SECONDARY CHALLENGE
OSTREID HERPESVIRUS-1
SPOT SYNDROME VIRUS
DOUBLE-STRANDED-RNA
VIBRIO-SPLENDIDUS
INVERTEBRATE IMMUNITY
IN-VIVO
INFECTION
MEMORY
RESPONSES
ACL
[SDV.IMM.II]Life Sciences [q-bio]/Immunology/Innate immunity
[SDV.BA.ZI]Life Sciences [q-bio]/Animal biology/Invertebrate Zoology
[SDE.BE]Environmental Sciences/Biodiversity and Ecology
description International audience In the last decade, a paradigm shift has emerged in comparative immunology. Invertebrates can no longer be considered to be devoid of specific recognition and immune memory. However, we still lack a comprehensive view of these phenomena and their molecular mechanisms across phyla, especially in terms of duration, specificity, and efficiency in a natural context. In this study, we focused on a Lophotrochozoan/virus interaction, as antiviral priming is mostly overlooked in molluscs. Juvenile Crassostrea gigas oysters experience reoccurring mass mortalities events from Ostreid herpes virus 1 with no existing therapeutic treatment. Our results showed that various nucleic acid injections can prime oysters to trigger an antiviral state ultimately protecting them against a subsequent viral infection. Focusing on poly(I:C) as elicitor, we evidenced that it protected from an environmental infection, by mitigating viral replication. That protection seemed to induce a specific antiviral response as poly(I:C) fails to protect against a pathogenic bacteria. Finally, we showed that this phenomenon was long-lasting, persisting for at least 5 months thus suggesting for the first time the existence of innate immune memory in this invertebrate species. This study strengthens the emerging hypotheses about the broad conservation of innate immune priming and memory mechanisms in Lophotrochozoans.
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)
Universita degli Studi di Padova
ANR-14-CE19-0023,DECIPHER,Déchiffrage des maladies multifactorielles: cas des mortalités de l'huître(2014)
format Article in Journal/Newspaper
author Lafont, Maxime
Petton, Bruno
Vergnes, Agnès
Pauletto, Marianna
Segarra, Amélie
Gourbal, Benjamin
Montagnani, Caroline
author_facet Lafont, Maxime
Petton, Bruno
Vergnes, Agnès
Pauletto, Marianna
Segarra, Amélie
Gourbal, Benjamin
Montagnani, Caroline
author_sort Lafont, Maxime
title Long-lasting antiviral innate immune priming in the Lophotrochozoan Pacific oyster, Crassostrea gigas
title_short Long-lasting antiviral innate immune priming in the Lophotrochozoan Pacific oyster, Crassostrea gigas
title_full Long-lasting antiviral innate immune priming in the Lophotrochozoan Pacific oyster, Crassostrea gigas
title_fullStr Long-lasting antiviral innate immune priming in the Lophotrochozoan Pacific oyster, Crassostrea gigas
title_full_unstemmed Long-lasting antiviral innate immune priming in the Lophotrochozoan Pacific oyster, Crassostrea gigas
title_sort long-lasting antiviral innate immune priming in the lophotrochozoan pacific oyster, crassostrea gigas
publisher HAL CCSD
publishDate 2017
url https://hal.archives-ouvertes.fr/hal-01632346
https://hal.archives-ouvertes.fr/hal-01632346/document
https://hal.archives-ouvertes.fr/hal-01632346/file/Lafont-2017-SciRep.LongLasting.pdf
https://doi.org/10.1038/s41598-017-13564-0
geographic Pacific
geographic_facet Pacific
genre Crassostrea gigas
Pacific oyster
genre_facet Crassostrea gigas
Pacific oyster
op_source ISSN: 2045-2322
EISSN: 2045-2322
Scientific Reports
https://hal.archives-ouvertes.fr/hal-01632346
Scientific Reports, Nature Publishing Group, 2017, 7, pp.13143. ⟨10.1038/s41598-017-13564-0⟩
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1038/s41598-017-13564-0
hal-01632346
https://hal.archives-ouvertes.fr/hal-01632346
https://hal.archives-ouvertes.fr/hal-01632346/document
https://hal.archives-ouvertes.fr/hal-01632346/file/Lafont-2017-SciRep.LongLasting.pdf
doi:10.1038/s41598-017-13564-0
op_rights info:eu-repo/semantics/OpenAccess
op_doi https://doi.org/10.1038/s41598-017-13564-0
container_title Scientific Reports
container_volume 7
container_issue 1
_version_ 1766393931996594176
spelling ftccsdartic:oai:HAL:hal-01632346v1 2023-05-15T15:58:12+02:00 Long-lasting antiviral innate immune priming in the Lophotrochozoan Pacific oyster, Crassostrea gigas Lafont, Maxime Petton, Bruno Vergnes, Agnès Pauletto, Marianna Segarra, Amélie 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) Universita degli Studi di Padova ANR-14-CE19-0023,DECIPHER,Déchiffrage des maladies multifactorielles: cas des mortalités de l'huître(2014) 2017-10-13 https://hal.archives-ouvertes.fr/hal-01632346 https://hal.archives-ouvertes.fr/hal-01632346/document https://hal.archives-ouvertes.fr/hal-01632346/file/Lafont-2017-SciRep.LongLasting.pdf https://doi.org/10.1038/s41598-017-13564-0 en eng HAL CCSD Nature Publishing Group info:eu-repo/semantics/altIdentifier/doi/10.1038/s41598-017-13564-0 hal-01632346 https://hal.archives-ouvertes.fr/hal-01632346 https://hal.archives-ouvertes.fr/hal-01632346/document https://hal.archives-ouvertes.fr/hal-01632346/file/Lafont-2017-SciRep.LongLasting.pdf doi:10.1038/s41598-017-13564-0 info:eu-repo/semantics/OpenAccess ISSN: 2045-2322 EISSN: 2045-2322 Scientific Reports https://hal.archives-ouvertes.fr/hal-01632346 Scientific Reports, Nature Publishing Group, 2017, 7, pp.13143. ⟨10.1038/s41598-017-13564-0⟩ SECONDARY CHALLENGE OSTREID HERPESVIRUS-1 SPOT SYNDROME VIRUS DOUBLE-STRANDED-RNA VIBRIO-SPLENDIDUS INVERTEBRATE IMMUNITY IN-VIVO INFECTION MEMORY RESPONSES ACL [SDV.IMM.II]Life Sciences [q-bio]/Immunology/Innate immunity [SDV.BA.ZI]Life Sciences [q-bio]/Animal biology/Invertebrate Zoology [SDE.BE]Environmental Sciences/Biodiversity and Ecology info:eu-repo/semantics/article Journal articles 2017 ftccsdartic https://doi.org/10.1038/s41598-017-13564-0 2021-12-19T02:29:44Z International audience In the last decade, a paradigm shift has emerged in comparative immunology. Invertebrates can no longer be considered to be devoid of specific recognition and immune memory. However, we still lack a comprehensive view of these phenomena and their molecular mechanisms across phyla, especially in terms of duration, specificity, and efficiency in a natural context. In this study, we focused on a Lophotrochozoan/virus interaction, as antiviral priming is mostly overlooked in molluscs. Juvenile Crassostrea gigas oysters experience reoccurring mass mortalities events from Ostreid herpes virus 1 with no existing therapeutic treatment. Our results showed that various nucleic acid injections can prime oysters to trigger an antiviral state ultimately protecting them against a subsequent viral infection. Focusing on poly(I:C) as elicitor, we evidenced that it protected from an environmental infection, by mitigating viral replication. That protection seemed to induce a specific antiviral response as poly(I:C) fails to protect against a pathogenic bacteria. Finally, we showed that this phenomenon was long-lasting, persisting for at least 5 months thus suggesting for the first time the existence of innate immune memory in this invertebrate species. This study strengthens the emerging hypotheses about the broad conservation of innate immune priming and memory mechanisms in Lophotrochozoans. Article in Journal/Newspaper Crassostrea gigas Pacific oyster Archive ouverte HAL (Hyper Article en Ligne, CCSD - Centre pour la Communication Scientifique Directe) Pacific Scientific Reports 7 1