scholarly journals Faculty Opinions recommendation of A Sustained Immune Response Supports Long-Term Antiviral Immune Priming in the Pacific Oyster, Crassostrea gigas.

Author(s):  
Jean-Luc Imler
mBio ◽  
2020 ◽  
Vol 11 (2) ◽  
Author(s):  
Maxime Lafont ◽  
Agnès Vergnes ◽  
Jeremie Vidal-Dupiol ◽  
Julien de Lorgeril ◽  
Yannick Gueguen ◽  
...  

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 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.


mBio ◽  
2020 ◽  
Vol 11 (2) ◽  
Author(s):  
Nelson E. Martins

ABSTRACT Viral diseases cause significant losses in aquaculture. Prophylactic measures, such as immune priming, are promising control strategies. Treatment of the Pacific oyster (Crassostrea gigas) with the double-stranded RNA analog poly(I·C) confers long-term protection against infection with ostreid herpesvirus 1, the causative agent of Pacific oyster mortality syndrome. In a recent article in mBio, Lafont and coauthors (M. Lafont, A. Vergnes, J. Vidal-Dupiol, J. de Lorgeril, et al., mBio 11:e02777-19, 2020, https://doi.org/10.1128/mBio.02777-19) characterized the transcriptome of oysters treated with poly(I·C). This immune stimulator induced genes related to the interferon and apoptosis pathways. This response overlaps the response to viral infection, and high expression levels of potential effector genes are maintained for up to 4 months. This work opens the door to characterization of the phenomena of immune priming in a poorly studied invertebrate model. It also highlights the importance of interferon-like responses for invertebrate antiviral immunity.


2016 ◽  
Vol 58 ◽  
pp. 449-461 ◽  
Author(s):  
Courtney E. Hart ◽  
Michael J. Lauth ◽  
Cassidy S. Hunter ◽  
Brennan R. Krasny ◽  
Kristin M. Hardy

2020 ◽  
Author(s):  
Jing Fang ◽  
Xiaohui Cai ◽  
Fengyi Mao ◽  
Hongyu Li ◽  
Honglin Chen ◽  
...  

Abstract Background: Marine molluscs living in intertidal and estuarine areas, such as oysters, face numerous pathogen challenges during their development. Infection from bacteria such as Vibrio alginolyticus, represents a major factor affecting larval development and frequently leads to high mortality of the pacific oyster, Crassostrea gigas. The oyster immune response is known to play an important role in protecting the animal during development by mitigating the consequences of infection. Results: In this study, we undertook a comprehensive analysis of the immune response of C. gigas to V. alginolyticus challenge. We sequenced the transcriptome of C. gigas at 0, 6, 12, 24, 48 and 72 hours post infection. After RNA-seq, the raw reads are available through the NCBI Sequence Read Archive under accession number PRJNA623063. After filtering, a total of 58.24 Gb clean reads were produced and assembled using the reference genome of C. gigas. The distribution of quality Q30 was higher than 90.88% for each sample and the GC content ranged from 41.27% to 42.91%. When compared with sequences in the COG, GO, KEGG, Swiss-Prot, and NR databases, there were 1267, 1112, 2187, 682, 1133 differentially expressed genes annotated at 6, 12, 24, 48, 72 hours post infection respectively. Numerous immune-related genes displayed differential expression that varied over time: toll-like receptors, tripartite motif proteins, Lectin-like factors, scavenger receptors, signaling pathway components such as Myeloid differentiation factor 88, and stress proteins such as Heat shock 70 kDa protein were all found to be higher in abundance following V. alginolyticus challenge compared to control. For analysis, these genes were divided into several categories such as pattern recognition receptors, fibrinogen-like proteins, damage associated molecular patterns, complement factors, etc. These general categories allowed us to generate an immune response profile for C. gigas over the first 72 hours of infection. These results indicate that bacterial infection induce a complex pattern of immune gene expression in C. gigas larvae. Conclusion: Our study will facilitate targeted investigation into the function of specific immune factors that may explain the diversity and evolution of invertebrate immune molecules and lead to the development of effective measures to improve the performance of oyster culture.


2019 ◽  
Vol 91 ◽  
pp. 108-114 ◽  
Author(s):  
Jiejie Sun ◽  
Lingling Wang ◽  
Zhaojun Wu ◽  
Shuo Han ◽  
Liyan Wang ◽  
...  

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