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A Heterochromatin-Specific RNA Export Pathway Facilitates piRNA Production

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  • Mostafa F ElMaghraby, Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna Biocenter (VBC), Dr. Bohrgasse 3, 1030 Vienna, Austria.
  • ,
  • Peter Refsing Andersen
  • Florian Pühringer, Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna Biocenter (VBC), Dr. Bohrgasse 3, 1030 Vienna, Austria.
  • ,
  • Ulrich Hohmann, Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna Biocenter (VBC), Dr. Bohrgasse 3, 1030 Vienna, Austria.
  • ,
  • Katharina Meixner, Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna Biocenter (VBC), Dr. Bohrgasse 3, 1030 Vienna, Austria.
  • ,
  • Thomas Lendl, Institute of Molecular Pathology (IMP), Vienna BioCenter (VBC), Campus-Vienna-Biocenter 1, 1030 Vienna, Austria.
  • ,
  • Laszlo Tirian, Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna Biocenter (VBC), Dr. Bohrgasse 3, 1030 Vienna, Austria.
  • ,
  • Julius Brennecke, Institute of Molecular Biotechnology of the Austrian Academy of Sciences (IMBA), Vienna Biocenter (VBC), Dr. Bohrgasse 3, 1030 Vienna, Austria.

PIWI-interacting RNAs (piRNAs) guide transposon silencing in animals. The 22-30 nt piRNAs are processed in the cytoplasm from long non-coding RNAs that often lack RNA processing hallmarks of export-competent transcripts. By studying how these transcripts achieve nuclear export, we uncover an RNA export pathway specific for piRNA precursors in the Drosophila germline. This pathway requires Nxf3-Nxt1, a variant of the hetero-dimeric mRNA export receptor Nxf1-Nxt1. Nxf3 interacts with UAP56, a nuclear RNA helicase essential for mRNA export, and CG13741/Bootlegger, which recruits Nxf3-Nxt1 and UAP56 to heterochromatic piRNA source loci. Upon RNA cargo binding, Nxf3 achieves nuclear export via the exportin Crm1 and accumulates together with Bootlegger in peri-nuclear nuage, suggesting that after export, Nxf3-Bootlegger delivers precursor transcripts to the piRNA processing sites. These findings indicate that the piRNA pathway bypasses nuclear RNA surveillance systems to export unprocessed transcripts to the cytoplasm, a strategy also exploited by retroviruses.

Original languageEnglish
JournalCell
Volume178
Issue4
Pages (from-to)964-979
ISSN0092-8674
DOIs
Publication statusPublished - Aug 2019
Externally publishedYes

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