PMID- 32156821 OWN - NLM STAT- MEDLINE DCOM- 20210311 LR - 20210311 IS - 2150-7511 (Electronic) VI - 11 IP - 2 DP - 2020 Mar 10 TI - A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, Crassostrea gigas. LID - 10.1128/mBio.02777-19 [doi] LID - e02777-19 AB - 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.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 genes, which control subsequent viral infection, and it was maintained for over 4 months after priming. This acquired resistant mechanism reinforces the molecular foundations of the sustained response model of immune priming. It opens the way to pseudovaccination to prevent the recurrent diseases that currently afflict economically or ecologically important invertebrates. CI - Copyright (c) 2020 Lafont et al. FAU - Lafont, Maxime AU - Lafont M AD - IHPE, University of Montpellier, CNRS, Ifremer, University of Perpignan Via Domitia, Montpellier, France. AD - IHPE, University of Montpellier, CNRS, Ifremer, University of Perpignan Via Domitia, Perpignan, France. FAU - Vergnes, Agnes AU - Vergnes A AD - IHPE, University of Montpellier, CNRS, Ifremer, University of Perpignan Via Domitia, Montpellier, France. FAU - Vidal-Dupiol, Jeremie AU - Vidal-Dupiol J AUID- ORCID: 0000-0002-0577-2953 AD - IHPE, University of Montpellier, CNRS, Ifremer, University of Perpignan Via Domitia, Montpellier, France. FAU - de Lorgeril, Julien AU - de Lorgeril J AUID- ORCID: 0000-0002-6400-5455 AD - IHPE, University of Montpellier, CNRS, Ifremer, University of Perpignan Via Domitia, Montpellier, France. FAU - Gueguen, Yannick AU - Gueguen Y AUID- ORCID: 0000-0002-8749-9582 AD - IHPE, University of Montpellier, CNRS, Ifremer, University of Perpignan Via Domitia, Montpellier, France. FAU - Haffner, Philippe AU - Haffner P AD - IHPE, University of Montpellier, CNRS, Ifremer, University of Perpignan Via Domitia, Montpellier, France. FAU - Petton, Bruno AU - Petton B AD - Ifremer, LEMAR UMR6539, Argenton-en-Landunvez, France. FAU - Chaparro, Cristian AU - Chaparro C AUID- ORCID: 0000-0002-5162-349X AD - IHPE, University of Montpellier, CNRS, Ifremer, University of Perpignan Via Domitia, Perpignan, France. FAU - Barrachina, Celia AU - Barrachina C AD - MGX, Biocampus Montpellier, CNRS, INSERM, University of Montpellier, Montpellier, France. FAU - Destoumieux-Garzon, Delphine AU - Destoumieux-Garzon D AUID- ORCID: 0000-0002-8793-9138 AD - IHPE, University of Montpellier, CNRS, Ifremer, University of Perpignan Via Domitia, Montpellier, France. FAU - Mitta, Guillaume AU - Mitta G AUID- ORCID: 0000-0003-1188-1467 AD - IHPE, University of Montpellier, CNRS, Ifremer, University of Perpignan Via Domitia, Perpignan, France. FAU - Gourbal, Benjamin AU - Gourbal B AUID- ORCID: 0000-0003-2097-2563 AD - IHPE, University of Montpellier, CNRS, Ifremer, University of Perpignan Via Domitia, Perpignan, France. FAU - Montagnani, Caroline AU - Montagnani C AUID- ORCID: 0000-0002-0861-7967 AD - IHPE, University of Montpellier, CNRS, Ifremer, University of Perpignan Via Domitia, Montpellier, France cmontagn@ifremer.fr. LA - eng PT - Journal Article PT - Research Support, Non-U.S. Gov't DEP - 20200310 PL - United States TA - mBio JT - mBio JID - 101519231 RN - O84C90HH2L (Poly I-C) RN - Ostreid herpesvirus 1 SB - IM CIN - mBio. 2020 Mar 24;11(2):. PMID: 32209685 MH - Animals MH - Crassostrea/*genetics/*immunology MH - DNA Virus Infections/genetics/*immunology MH - DNA Viruses/*immunology/pathogenicity MH - Gene Expression Profiling MH - *Immunity, Innate MH - Poly I-C/immunology MH - Up-Regulation PMC - PMC7064767 OTO - NOTNLM OT - OsHV-1 OT - POMS OT - antiviral response OT - immune memory OT - innate immunity OT - interferon OT - oyster OT - poly(I.C) OT - priming OT - transcriptomic EDAT- 2020/03/12 06:00 MHDA- 2021/03/12 06:00 PMCR- 2020/03/10 CRDT- 2020/03/12 06:00 PHST- 2020/03/12 06:00 [entrez] PHST- 2020/03/12 06:00 [pubmed] PHST- 2021/03/12 06:00 [medline] PHST- 2020/03/10 00:00 [pmc-release] AID - mBio.02777-19 [pii] AID - mBio02777-19 [pii] AID - 10.1128/mBio.02777-19 [doi] PST - epublish SO - mBio. 2020 Mar 10;11(2):e02777-19. doi: 10.1128/mBio.02777-19.