A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, <named-content content-type="genus-species">Crassostrea gigas</named-content>
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...
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American Society for Microbiology
2020
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ftdoajarticles:oai:doaj.org/article:6dc73d86aaa944dc8615214914c93433 2023-05-15T15:57:55+02:00 A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, <named-content content-type="genus-species">Crassostrea gigas</named-content> Maxime Lafont Agnès Vergnes Jeremie Vidal-Dupiol Julien de Lorgeril Yannick Gueguen Philippe Haffner Bruno Petton Cristian Chaparro Celia Barrachina Delphine Destoumieux-Garzon Guillaume Mitta Benjamin Gourbal Caroline Montagnani 2020-04-01T00:00:00Z https://doi.org/10.1128/mBio.02777-19 https://doaj.org/article/6dc73d86aaa944dc8615214914c93433 EN eng American Society for Microbiology https://journals.asm.org/doi/10.1128/mBio.02777-19 https://doaj.org/toc/2150-7511 doi:10.1128/mBio.02777-19 2150-7511 https://doaj.org/article/6dc73d86aaa944dc8615214914c93433 mBio, Vol 11, Iss 2 (2020) innate immunity priming OsHV-1 antiviral response immune memory oyster Microbiology QR1-502 article 2020 ftdoajarticles https://doi.org/10.1128/mBio.02777-19 2022-12-31T05:07:53Z 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. 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 ... Article in Journal/Newspaper Crassostrea gigas Pacific oyster Directory of Open Access Journals: DOAJ Articles Pacific mBio 11 2 |
institution |
Open Polar |
collection |
Directory of Open Access Journals: DOAJ Articles |
op_collection_id |
ftdoajarticles |
language |
English |
topic |
innate immunity priming OsHV-1 antiviral response immune memory oyster Microbiology QR1-502 |
spellingShingle |
innate immunity priming OsHV-1 antiviral response immune memory oyster Microbiology QR1-502 Maxime Lafont Agnès Vergnes Jeremie Vidal-Dupiol Julien de Lorgeril Yannick Gueguen Philippe Haffner Bruno Petton Cristian Chaparro Celia Barrachina Delphine Destoumieux-Garzon Guillaume Mitta Benjamin Gourbal Caroline Montagnani A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, <named-content content-type="genus-species">Crassostrea gigas</named-content> |
topic_facet |
innate immunity priming OsHV-1 antiviral response immune memory oyster Microbiology QR1-502 |
description |
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. 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 ... |
format |
Article in Journal/Newspaper |
author |
Maxime Lafont Agnès Vergnes Jeremie Vidal-Dupiol Julien de Lorgeril Yannick Gueguen Philippe Haffner Bruno Petton Cristian Chaparro Celia Barrachina Delphine Destoumieux-Garzon Guillaume Mitta Benjamin Gourbal Caroline Montagnani |
author_facet |
Maxime Lafont Agnès Vergnes Jeremie Vidal-Dupiol Julien de Lorgeril Yannick Gueguen Philippe Haffner Bruno Petton Cristian Chaparro Celia Barrachina Delphine Destoumieux-Garzon Guillaume Mitta Benjamin Gourbal Caroline Montagnani |
author_sort |
Maxime Lafont |
title |
A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, <named-content content-type="genus-species">Crassostrea gigas</named-content> |
title_short |
A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, <named-content content-type="genus-species">Crassostrea gigas</named-content> |
title_full |
A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, <named-content content-type="genus-species">Crassostrea gigas</named-content> |
title_fullStr |
A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, <named-content content-type="genus-species">Crassostrea gigas</named-content> |
title_full_unstemmed |
A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, <named-content content-type="genus-species">Crassostrea gigas</named-content> |
title_sort |
sustained immune response supports long-term antiviral immune priming in the pacific oyster, <named-content content-type="genus-species">crassostrea gigas</named-content> |
publisher |
American Society for Microbiology |
publishDate |
2020 |
url |
https://doi.org/10.1128/mBio.02777-19 https://doaj.org/article/6dc73d86aaa944dc8615214914c93433 |
geographic |
Pacific |
geographic_facet |
Pacific |
genre |
Crassostrea gigas Pacific oyster |
genre_facet |
Crassostrea gigas Pacific oyster |
op_source |
mBio, Vol 11, Iss 2 (2020) |
op_relation |
https://journals.asm.org/doi/10.1128/mBio.02777-19 https://doaj.org/toc/2150-7511 doi:10.1128/mBio.02777-19 2150-7511 https://doaj.org/article/6dc73d86aaa944dc8615214914c93433 |
op_doi |
https://doi.org/10.1128/mBio.02777-19 |
container_title |
mBio |
container_volume |
11 |
container_issue |
2 |
_version_ |
1766393635826302976 |