Abstract
Tunnelling nanotubes and cytonemes function as highways for the transport of organelles, cytosolic and membrane-bound molecules, and pathogens between cells. During viral infection in the model organism Drosophila melanogaster, a systemic RNAi antiviral response is established presumably through the transport of a silencing signal from one cell to another via an unknown mechanism. Because of their role in cell-cell communication, we investigated whether nanotube-like structures could be a mediator of the silencing signal. Here, we describe for the first time in the context of a viral infection the presence of nanotube-like structures in different Drosophila cell types. These tubules, made of actin and tubulin, were associated with components of the RNAi machinery, including Argonaute 2, double-stranded RNA, and CG4572. Moreover, they were more abundant during viral, but not bacterial, infection. Super resolution structured illumination microscopy showed that Argonaute 2 and tubulin reside inside the tubules. We propose that nanotube-like structures are one of the mechanisms by which Argonaute 2, as part of the antiviral RNAi machinery, is transported between infected and non-infected cells to trigger systemic antiviral immunity in Drosophila.
Highlights
To establish systemic immunity and protect both the site of initial infection and the entire organism, all multicellular species have developed sophisticated ways to communicate immune signals
Because of their role in cell-cell communication, we investigated whether membrane-nanotubes could be one of the mediators that connect Drosophila cells in order to establish a systemic RNA interference (RNAi)-mediated antiviral immune response
We identify nanotube-like structures in Drosophila cells in the context of a viral infection, and we provide evidence that they may function in cell-cell communication in response to infection
Summary
To establish systemic immunity and protect both the site of initial infection and the entire organism, all multicellular species have developed sophisticated ways to communicate immune signals. Inaba et al.[22] described for the first time microtubule-based nanotubes in Drosophila testis that resemble TNTs previously described in mammalian cells, that are neither filopodia nor cytonemes They proposed that these structures contribute to short-range signalling in Drosophila niche-stem-cell. Non-cell-autonomous RNAi presumes that a silencing signal is transported from one cell to another via an unknown mechanism to establish antiviral systemic immunity[38,39]. Because of their role in cell-cell communication, we investigated whether membrane-nanotubes could be one of the mediators that connect Drosophila cells in order to establish a systemic RNAi-mediated antiviral immune response. We postulate that the spread of the silencing signal in insects could rely, among other cellular mechanisms, on nanotube-like structures forming intercellular connections
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