Abstract
Recent developments on extracellular vesicles (EVs) containing multiple virus particles challenge the rigid definition of non-enveloped viruses. However, how non-enveloped viruses hijack cell machinery to promote non-lytic release in EVs, and their functional roles, remain to be clarified. Here we used Bluetongue virus (BTV) as a model of a non-enveloped arthropod-borne virus and discovered that the majority of viruses are released in EVs. Based on the cellular proteins detected in these EVs, and use of inhibitors targeting the cellular degradation process, we demonstrated that these extracellular vesicles are derived from secretory lysosomes, in which the acidic pH is neutralized upon the infection. Moreover, we report that secreted EVs are more efficient than free-viruses for initiating infections, but that they trigger super-infection exclusion that only free-viruses can overcome.
Highlights
Lipid envelopes surrounding viruses are likely the results of a convergent evolution, potentially acquired during the adaptation of non-enveloped virus to animals [1]
Since Bluetongue virus (BTV) particles were shown to be associated with MVBs components during trafficking [16] and the purified virus particles are associated with NS3 [15], a membrane protein, it is possible that multiple BTV particles are released within extracellular vesicles (EVs)
Western blot analysis of the structural protein content, both in the pellet and the supernatant revealed that VP2, VP5 and VP7 were at higher levels in the pellet (Fig 1C), consistent with the virus titres
Summary
Lipid envelopes surrounding viruses are likely the results of a convergent evolution, potentially acquired during the adaptation of non-enveloped virus to animals [1]. Non-enveloped viruses developed alternative mechanisms, such as cell entry by membrane penetration [2] and exit by cell lysis. In both cases, free virus particles remain the canonical unit of virus infection, with a single virus particle entering a cell to replicate and amplify its genome. It was observed that EVs could contain multiple virus particles, allowing infection of a unique cell with many virus particles at a time [7,10] This new transmission mechanism, reported as en block transmission, allows viral genome complementation during the infection and could be a regulator of fitness evolution for a virus population [11,12]
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