Norwegian Veterinary Institute, Ås, Norway.
Marine Laboratory, Aberdeen, Scotland, United Kingdom.
PLoS Pathog. 2022 Oct 14;18(10):e1010905. doi: 10.1371/journal.ppat.1010905. eCollection 2022 Oct.
Viral interference is a process where infection with one virus prevents a subsequent infection with the same or a different virus. This is believed to limit superinfection, promote viral genome stability, and protect the host from overwhelming infection. Mechanisms of viral interference have been extensively studied in plants, but remain poorly understood in vertebrates. We demonstrate that infection with infectious salmon anaemia virus (ISAV) strongly reduces homologous viral attachment to the Atlantic salmon, Salmo salar L. vascular surface. A generalised loss of ISAV binding was observed after infection with both high-virulent and low-virulent ISAV isolates, but with different kinetics. The loss of ISAV binding was accompanied by an increased susceptibility to sialidase, suggesting a loss of the vascular 4-O-sialyl-acetylation that mediates ISAV attachment and simultaneously protects the sialic acid from cleavage. Moreover, the ISAV binding capacity of cultured cells dramatically declined 3 days after ISAV infection, accompanied by reduced cellular permissiveness to infection with a second antigenically distinct isolate. In contrast, neither infection with infectious haematopoietic necrosis virus nor stimulation with the viral mimetic poly I:C restricted subsequent cellular ISAV attachment, revealing an ISAV-specific mechanism rather than a general cellular antiviral response. Our study demonstrates homologous ISAV attachment interference by de-acetylation of sialic acids on the vascular surface. This is the first time the kinetics of viral receptor destruction have been mapped throughout the full course of an infection, and the first report of homologous attachment interference by the loss of a vascular viral receptor. Little is known about the biological functions of vascular O-sialyl-acetylation. Our findings raise the question of whether this vascular surface modulation could be linked to the breakdown of central vascular functions that characterises infectious salmon anaemia.
病毒干扰是一种过程,即感染一种病毒会阻止随后感染同一种或不同种病毒。这种现象被认为可以限制病毒的超感染,促进病毒基因组的稳定性,并保护宿主免受过度感染。病毒干扰的机制在植物中得到了广泛的研究,但在脊椎动物中仍知之甚少。我们证明,传染性鲑鱼贫血病毒(ISAV)的感染强烈降低了鲑鱼血管表面对同源病毒的附着。在感染高毒力和低毒力 ISAV 分离株后,均观察到 ISAV 结合的普遍丧失,但动力学不同。ISAV 结合的丧失伴随着对神经氨酸酶的易感性增加,表明介导 ISAV 附着的血管 4-O-唾液酰化的丧失,同时保护唾液酸免受裂解。此外,ISAV 感染后 3 天,培养细胞的 ISAV 结合能力显著下降,同时对第二种抗原上不同的分离株的感染性也降低。相比之下,感染传染性造血坏死病毒或用病毒模拟物 poly I:C 刺激均不会限制随后细胞 ISAV 的附着,这表明存在一种 ISAV 特异性机制,而不是普遍的细胞抗病毒反应。我们的研究表明,通过血管表面唾液酸的去乙酰化来实现同源 ISAV 附着的干扰。这是首次在整个感染过程中绘制病毒受体破坏的动力学,也是首次报道通过血管病毒受体的丧失来实现同源附着干扰。关于血管 O-唾液酰化的生物学功能知之甚少。我们的发现提出了一个问题,即这种血管表面的调节是否与传染性鲑鱼贫血症特征性的中心血管功能的崩溃有关。