Tsoulia Thomais, Sundaram Arvind Ym, Amundsen Marit M, Rimstad Espen, Wessel Øystein, Jørgensen Jorunn B, Dahle Maria K
Departments of Aquatic Animal Health and Analysis and Diagnostics, Norwegian Veterinary Institute, Ås, Norway; Department of Biotechnology, Fisheries and Economy, UiT Arctic University of Norway, Tromsø, Norway.
Departments of Aquatic Animal Health and Analysis and Diagnostics, Norwegian Veterinary Institute, Ås, Norway; Department of Medical Genetics, Oslo University Hospital, Oslo, Norway.
Fish Shellfish Immunol. 2025 Feb;157:110088. doi: 10.1016/j.fsi.2024.110088. Epub 2024 Dec 9.
Piscine orthoreovirus (PRV) infection is common in aquaculture of salmonids. The three known PRV genotypes (PRV-1-3) have host species specificity and cause different diseases, but all infect and replicate in red blood cells (RBCs) in early infection phase. PRV-1 is the causative agent of heart and skeletal muscle inflammation (HSMI) in farmed Atlantic salmon (Salmo salar), PRV-2 causes erythrocytic inclusion body syndrome (EIBS) in coho salmon (Oncorhynchus kisutch), while PRV-3 induces HSMI-like disease in farmed rainbow trout (Oncorhynchus mykiss). PRV-3 can also infect A. salmon without causing clinical disease and has been shown to cross-protect against PRV-1 infection and HSMI, while PRV-2 or inactivated adjuvanted PRV-1 vaccine only partially reduced HSMI pathologic changes. In the present work, we studied the transcriptional responses in blood cells of A. salmon two- and five-weeks post infection with PRV-1, PRV-2, PRV-3, or post injection with inactivated PRV-1 vaccine. PRV-1 and PRV-3 replicated well in A. salmon blood cells, and both induced the typical innate antiviral responses triggered by dsRNA viruses. Two weeks post infection, PRV-3 triggered stronger antiviral responses than PRV-1, despite their similar viral RNA replication levels, but after five weeks the induced responses were close to equal. PRV-2 and the InPRV-1 vaccine did not trigger the same typical antiviral responses as the replicating PRV-1 and PRV-3 genotypes, but induced genes involved in membrane trafficking and signaling pathways that may regulate physiological functions. These findings propose that the protection mediated by PRV-3 against a secondary infection by PRV-1 occur due to a potent and early activation of the same type of innate immune responses. The difference in the timing of antiviral responses may give PRV-1 an evolutionary edge, facilitating its dissemination to A. salmon heart, a critical step for HSMI development.
鱼类正呼肠孤病毒(PRV)感染在鲑科鱼类养殖中很常见。已知的三种PRV基因型(PRV-1至3)具有宿主物种特异性,并会引发不同疾病,但在感染早期均能感染红细胞(RBC)并在其中复制。PRV-1是养殖大西洋鲑(Salmo salar)心脏和骨骼肌炎症(HSMI)的病原体,PRV-2会导致银大麻哈鱼(Oncorhynchus kisutch)出现红细胞包涵体综合征(EIBS),而PRV-3会在养殖虹鳟(Oncorhynchus mykiss)中诱发类似HSMI的疾病。PRV-3也能感染大西洋鲑但不引发临床疾病,并且已证明其能交叉保护抵抗PRV-1感染和HSMI,而PRV-2或灭活佐剂PRV-1疫苗只能部分减轻HSMI的病理变化。在本研究中,我们研究了感染PRV-1、PRV-2、PRV-3两周和五周后或注射灭活PRV-1疫苗后,大西洋鲑血细胞中的转录反应。PRV-1和PRV-3在大西洋鲑血细胞中复制良好,二者均能诱导由双链RNA病毒引发的典型先天性抗病毒反应。感染两周后,尽管PRV-3和PRV-1的病毒RNA复制水平相似,但PRV-3引发的抗病毒反应比PRV-1更强,但五周后诱导的反应接近相等。PRV-2和InPRV-1疫苗并未引发与复制型PRV-1和PRV-3基因型相同的典型抗病毒反应,但诱导了参与膜运输和信号通路的基因,这些基因可能调节生理功能。这些发现表明,PRV-3介导的针对PRV-1二次感染的保护作用是由于同一类型先天性免疫反应的强力早期激活。抗病毒反应时间的差异可能使PRV-1具有进化优势,有助于其传播至大西洋鲑心脏,这是HSMI发展的关键步骤。