National Research Center for the Control and Prevention of Infectious Diseases, Nagasaki University, Nagasaki, Japan.
Central Laboratory, Institute of Tropical Medicine (NEKKEN), Nagasaki University, Nagasaki, Japan.
Microbiol Spectr. 2024 Sep 3;12(9):e0026924. doi: 10.1128/spectrum.00269-24. Epub 2024 Jul 30.
Filoviruses produce viral particles with characteristic filamentous morphology. The major viral matrix protein, VP40, is trafficked to the plasma membrane and promotes viral particle formation and subsequent viral egress. In the present study, we assessed the role of the small GTPase Rab11-mediated endocytic pathway in Marburg virus (MARV) particle formation and budding. Although Rab11 was predominantly localized in the perinuclear region, it exhibited a more diffuse distribution in the cytoplasm of cells transiently expressing MARV VP40. Rab11 was incorporated into MARV-like particles. Expression of the dominant-negative form of Rab11 and knockdown of Rab11 decreased the amount of VP40 fractions in the cell periphery. Moreover, downregulation of Rab11 moderately reduced the release of MARV-like particles and authentic MARV. We further demonstrated that VP40 induces the distribution of the microtubule network toward the cell periphery, which was partly associated with Rab11. Depolymerization of microtubules reduced the accumulation of VP40 in the cell periphery along with viral particle formation. VP40 physically interacted with α-tubulin, a major component of microtubules, but not with Rab11. Taken together, these results suggested that VP40 partly interacts with microtubules and facilitates their distribution toward the cell periphery, leading to the trafficking of transiently tethering Rab11-positive vesicles toward the cell surface. As we previously demonstrated the role of Rab11 in the formation of Ebola virus particles, the results here suggest that filoviruses in general exploit the vesicle-trafficking machinery for proper virus-particle formation and subsequent egress. These pathways may be a potential target for the development of pan-filovirus therapeutics.IMPORTANCEFiloviruses, including Marburg and Ebola viruses, produce distinct filamentous viral particles. Although it is well known that the major viral matrix protein of these viruses, VP40, is trafficked to the cell surface and promotes viral particle production, details regarding the associated molecular mechanisms remain unclear. To address this knowledge gap, we investigated the role of the small GTPase Rab11-mediated endocytic pathway in this process. Our findings revealed that Marburg virus exploits the Rab11-mediated vesicle-trafficking pathway for the release of virus-like particles and authentic virions in a microtubule network-dependent manner. Previous findings demonstrated that Rab11 is also involved in Ebola virus-particle production. Taken together, these data suggest that filoviruses, in general, may hijack the microtubule-dependent vesicle-trafficking machinery for productive replication. Therefore, this pathway presents as a potential target for the development of pan-filovirus therapeutics.
丝状病毒产生具有特征性丝状形态的病毒颗粒。主要的病毒基质蛋白 VP40 被转运到质膜,并促进病毒颗粒的形成和随后的病毒逸出。在本研究中,我们评估了小 GTPase Rab11 介导的内吞途径在马尔堡病毒(MARV)颗粒形成和出芽中的作用。尽管 Rab11 主要定位于核周区域,但在瞬时表达 MARV VP40 的细胞中,它表现出更弥散的细胞质分布。Rab11 被纳入 MARV 样颗粒中。表达显性负形式的 Rab11 和敲低 Rab11 减少了细胞周围 VP40 分数的量。此外,下调 Rab11 适度减少了 MARV 样颗粒和真正的 MARV 的释放。我们进一步证明 VP40 诱导微管网络向细胞外周的分布,这部分与 Rab11 有关。微管的去聚合减少了 VP40 在细胞周围的积累,同时也减少了病毒颗粒的形成。VP40 与微管的主要成分 α-微管蛋白发生物理相互作用,但不与 Rab11 相互作用。总之,这些结果表明 VP40 部分与微管相互作用,并促进其向细胞外周的分布,从而将瞬时连接的 Rab11 阳性囊泡转运到细胞表面。正如我们之前证明 Rab11 在埃博拉病毒颗粒形成中的作用一样,这里的结果表明丝状病毒总体上利用囊泡运输机制来正确形成病毒颗粒并随后逸出。这些途径可能是开发泛丝状病毒治疗药物的潜在靶点。
重要性
丝状病毒,包括马尔堡病毒和埃博拉病毒,产生独特的丝状病毒颗粒。尽管众所周知,这些病毒的主要病毒基质蛋白 VP40 被转运到细胞表面并促进病毒颗粒的产生,但有关相关分子机制的详细信息仍不清楚。为了解决这一知识空白,我们研究了小 GTPase Rab11 介导的内吞途径在这一过程中的作用。我们的发现表明,马尔堡病毒以微管网络依赖的方式利用 Rab11 介导的囊泡运输途径释放病毒样颗粒和真正的病毒粒子。先前的研究表明,Rab11 也参与了埃博拉病毒颗粒的产生。总之,这些数据表明,丝状病毒通常可能劫持微管依赖性囊泡运输机制进行有效的复制。因此,该途径是开发泛丝状病毒治疗药物的潜在靶点。