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

Type Article
Date 2020-03
Language English
Author(s) Lafont Maxime1, 2, Vergnes Agnes1, Vidal-Dupiol Jeremie1, De Lorgeril Julien1, Gueguen Yannick1, Haffner Philippe1, Petton Bruno3, Chaparro Cristian2, Barrachina Celia5, Destoumieux-Garzon Delphine1, Mitta Guillaume2, Gourbal Benjamin2, Montagnani Caroline1
Affiliation(s) 1 : IHPE, University of Montpellier, CNRS, Ifremer, University of Perpignan Via Domitia, Montpellier, France
2 : IHPE, University of Montpellier, CNRS, Ifremer, University of Perpignan Via Domitia, Perpignan, France
3 : Ifremer, LEMAR UMR6539, Argenton-en-Landunvez, France
4 : MGX, Biocampus Montpellier, CNRS, INSERM, University of Montpellier, Montpellier, France
5 : IHPE, University of Montpellier, CNRS, Ifremer, University of Perpignan Via Domitia, Montpellier, France
Source Mbio (2150-7511) (American Society for Microbiology), 2020-03 , Vol. 11 , N. 2 , P. e02777-19 (17p.)
DOI 10.1128/mBio.02777-19
WOS© Times Cited 1
Keyword(s) innate immunity, priming, OsHV-1, antiviral response, immune memory, oyster, POMS, poly(I-C), interferon, transcriptomic
Abstract

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.

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Publisher's official version 17 3 MB Open access
TABLE S1 Library and mapped reads on the C. gigas genome or OsHV-1 genome used for RNA-seq analyses. 13 KB Open access
FIG S1 Technical validation of the RNA-seq data by RT-qPCR. Twenty genes with contrasting expression levels were selected... 1 MB Open access
FIG S2 Distribution of differentially expressed genes postpriming. Numbers of DEG following poly(I·C) injection upregulated (red) or downregulated (green) are plotted following their fold change leve 1 MB Open access
TABLE S2 Primers used for RNA-seq validation and RT-qPCR analyses. 16 KB Open access
TABLE S3 (A) List of differentially expressed genes postpriming with poly(I·C); (B) DEG identification in primed oysters postchallenge. 2 MB Open access
FIG S3 Hierarchical clustering trees of Gene ontology categories affected by poly(I·C) priming. Hierarchical clustering trees of significant GO categories belonging to biological processes ... 830 KB Open access
TABLE S4 List of enriched categories identified by RBGOA 29 KB Open access
TABLE S5 (A) List of the 1,587 DEG regulated postpriming and their respective genome identifier, annotation, GO correspondence and FC, and RPKM in postpriming and postchallenge ... 667 KB Open access
FIG S4 Comparative analysis of the poly(I·C) sustained expression pattern and the FSW-specific challenge. (A) Venn diagram representing the genes common to the two patterns. (B) Comparison of the... 1 MB Open access
FIG S5 Experimental design used to identify the long-term molecular basis underlying poly(I·C) priming. (A) Specific-pathogen-free (SPF) oysters, highly susceptible to juvenile oyster syndrome, ... 75 KB Open access
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How to cite 

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). A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, Crassostrea gigas. Mbio, 11(2), e02777-19 (17p.). Publisher's official version : https://doi.org/10.1128/mBio.02777-19 , Open Access version : https://archimer.ifremer.fr/doc/00614/72580/