Molecular Cell
Volume 74, Issue 5, 6 June 2019, Pages 982-995.e6
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Article
The RNA-Binding ATPase, Armitage, Couples piRNA Amplification in Nuage to Phased piRNA Production on Mitochondria

https://doi.org/10.1016/j.molcel.2019.04.006Get rights and content
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Highlights

  • The ping-pong and phased piRNA biogenesis pathways are physically separate

  • Armi couples piRNA biogenesis in nuage to phased piRNA production on mitochondria

  • Armi binds piRNA precursors during both ping-pong and phased piRNA production

  • Armi ATPase mutants inappropriately bind mRNA and fail to support piRNA production

Summary

PIWI-interacting RNAs (piRNAs) silence transposons in Drosophila ovaries, ensuring female fertility. Two coupled pathways generate germline piRNAs: the ping-pong cycle, in which the PIWI proteins Aubergine and Ago3 increase the abundance of pre-existing piRNAs, and the phased piRNA pathway, which generates strings of tail-to-head piRNAs, one after another. Proteins acting in the ping-pong cycle localize to nuage, whereas phased piRNA production requires Zucchini, an endonuclease on the mitochondrial surface. Here, we report that Armitage (Armi), an RNA-binding ATPase localized to both nuage and mitochondria, links the ping-pong cycle to the phased piRNA pathway. Mutations that block phased piRNA production deplete Armi from nuage. Armi ATPase mutants cannot support phased piRNA production and inappropriately bind mRNA instead of piRNA precursors. We propose that Armi shuttles between nuage and mitochondria, feeding precursor piRNAs generated by Ago3 cleavage into the Zucchini-dependent production of Aubergine- and Piwi-bound piRNAs on the mitochondrial surface.

Keywords

small RNA
argonaute
microscopy
immunoprecipitation
mass spectrometry
RNA-seq
DTME
helicase
ATP
mitochondrion

Cited by (0)

3

Present address: Amgen Inc., 1120 Veterans Boulevard, South San Francisco, CA 94080, USA

4

Present address: Voyager Therapeutics Inc., 75 Sidney Street, Cambridge, MA 02139, USA

5

Lead Contact