Drosophila cells use nanotube-like structures to transfer dsRNA and RNAi machinery between cells

Sci Rep. 2016 Jun 3;6:27085. doi: 10.1038/srep27085.

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.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / genetics
  • Actins / metabolism
  • Animals
  • Argonaute Proteins / genetics*
  • Argonaute Proteins / metabolism
  • Biological Transport
  • Cell Communication
  • Cell Line
  • Dicistroviridae / genetics
  • Dicistroviridae / growth & development
  • Drosophila Proteins / genetics*
  • Drosophila Proteins / metabolism
  • Drosophila melanogaster / metabolism*
  • Drosophila melanogaster / microbiology
  • Drosophila melanogaster / ultrastructure
  • Drosophila melanogaster / virology
  • Gene Expression Regulation
  • Genes, Reporter
  • Green Fluorescent Proteins / genetics
  • Green Fluorescent Proteins / metabolism
  • Luminescent Proteins / genetics
  • Luminescent Proteins / metabolism
  • Organelles / metabolism*
  • Organelles / microbiology
  • Organelles / ultrastructure
  • Organelles / virology
  • Pectobacterium carotovorum / genetics
  • Pectobacterium carotovorum / growth & development
  • RNA Interference
  • RNA, Double-Stranded / genetics*
  • RNA, Double-Stranded / metabolism
  • Tubulin / genetics
  • Tubulin / metabolism
  • Viral Proteins / antagonists & inhibitors*
  • Viral Proteins / genetics
  • Viral Proteins / metabolism
  • rab GTP-Binding Proteins / genetics
  • rab GTP-Binding Proteins / metabolism

Substances

  • AGO2 protein, Drosophila
  • Actins
  • Argonaute Proteins
  • Drosophila Proteins
  • Luminescent Proteins
  • RNA, Double-Stranded
  • Tubulin
  • Viral Proteins
  • enhanced green fluorescent protein
  • fluorescent protein 583
  • Green Fluorescent Proteins
  • rab7 protein
  • rab GTP-Binding Proteins