Virus-Induced Tubule: a Vehicle for Rapid Spread of Virions through Basal Lamina from Midgut Epithelium in the Insect Vector

Virus-Induced Tubule: a Vehicle for Rapid Spread of Virions through Basal Lamina from Midgut Epithelium in the Insect Vector
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病毒诱导的小管:病毒粒子通过昆虫载体中肠上皮基底层快速传播的载体

DOI:
10.1128/jvi.01261-14
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发表时间:
2014-09-01
影响因子:
5.4
通讯作者:
Wei, Taiyun
Wei, Taiyun
中科院分区:
医学2区
文献类型:
--
作者:
Jia, Dongsheng;Mao, Qianzhuo;Wei, Taiyun

文献摘要

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摘要植物呼肠孤病毒、植物弹状病毒、冠状病毒和细小病毒通过昆虫媒介以持续繁殖的方式传播。这些病毒诱导病毒包涵体的形成,以促进病毒在昆虫载体中的传播。昆虫媒介的肠道是由位于非细胞基板上的上皮细胞形成的,基板周围环绕着内脏肌肉组织。在这里,我们证明了最近发现的一种植物呼肠孤病毒,南方水稻黑条矮缩病毒(SRBSDV),它利用由病毒编码的非结构蛋白P7-1组成的含病毒小管,从最初感染的上皮细胞直接穿过基膜,到达其媒介白背飞虱(Sogatella Furcifera)肠道内的内脏肌肉组织。此外,这些小管通过P7-1和肌动蛋白的直接相互作用沿着内脏肌肉组织扩散。针对P7-1基因的合成双链RNA通过RNA干扰破坏小管组装,在体内外抑制了病毒在昆虫载体中的传播。所有这些结果首次表明,病毒利用病毒诱导的小管作为载体,从最初感染的中肠上皮通过基膜传播病毒,促进病毒从昆虫媒介的肠道快速传播。重要性许多植物病毒通过吸液昆虫持续传播,包括蓟马、蚜虫、稻飞虱和叶蝉。这些病毒被昆虫摄取,在昆虫媒介的肠道上皮中确立了它们的原始感染。随后,入侵的病毒设法横穿基膜,这是肠道内的一层非细胞层,从理论上讲,这是一个可能阻止病毒传播的屏障。植物病毒穿过基膜的机制尚不清楚。在这里,我们报告了一种植物病毒已经进化到利用病毒诱导的小管从昆虫媒介的最初感染的中肠上皮穿过基膜,从而揭示了病毒适应的先前未描述的从昆虫媒介的肠道快速传播病毒粒子的途径。
ABSTRACT The plant reoviruses, plant rhabdoviruses, tospoviruses, and tenuiviruses are transmitted by insect vectors in a persistent propagative manner. These viruses induce the formation of viral inclusions to facilitate viral propagation in insect vectors. The intestines of insect vectors are formed by epithelial cells that lie on the noncellular basal lamina surrounded by visceral muscle tissue. Here, we demonstrate that a recently identified plant reovirus, southern rice black-streaked dwarf virus (SRBSDV), exploits virus-containing tubules composed of virus-encoded nonstructural protein P7-1 to directly cross the basal lamina from the initially infected epithelium toward visceral muscle tissues in the intestine of its vector, the white-backed planthopper (Sogatella furcifera). Furthermore, such tubules spread along visceral muscle tissues through a direct interaction of P7-1 and actin. The destruction of tubule assembly by RNA interference with synthesized double-stranded RNA targeting the P7-1 gene inhibited viral spread in the insect vector in vitro and in vivo. All these results show for the first time that a virus employs virus-induced tubule as a vehicle for viral spread from the initially infected midgut epithelium through the basal lamina, facilitating the rapid dissemination of virus from the intestine of the insect vector. IMPORTANCE Numerous plant viruses are transmitted in a persistent manner by sap-sucking insects, including thrips, aphids, planthoppers, and leafhoppers. These viruses, ingested by the insects, establish their primary infection in the intestinal epithelium of the insect vector. Subsequently, the invading virus manages to transverse the basal lamina, a noncellular layer lining the intestine, a barrier that may theoretically hinder viral spread. The mechanism by which plant viruses cross the basal lamina is unknown. Here, we report that a plant virus has evolved to exploit virus-induced tubules to pass through the basal lamina from the initially infected midgut epithelium of the insect vector, thus revealing the previously undescribed pathway adapted by the virus for rapid dissemination of virions from the intestine of the insect vector.