Spindle-E cycling between nuage and cytoplasm is controlled by Qin and PIWI proteins

J Cell Biol. 2016 Apr 25;213(2):201-11. doi: 10.1083/jcb.201411076. Epub 2016 Apr 18.

Abstract

Transposable elements (TEs) are silenced in germ cells by a mechanism in which PIWI proteins generate and use PIWI-interacting ribonucleic acid (piRNA) to repress expression of TE genes. piRNA biogenesis occurs by an amplification cycle in microscopic organelles called nuage granules, which are localized to the outer face of the nuclear envelope. One cofactor required for amplification is the helicase Spindle-E (Spn-E). We found that the Spn-E protein physically associates with the Tudor domain protein Qin and the PIWI proteins Aubergine (Aub) and Argonaute3 (Ago3). Spn-E and Qin proteins are mutually dependent for their exit from nuage granules, whereas Spn-E and both Aub and Ago3 are mutually dependent for their entry or retention in nuage. The result is a dynamic cycling of Spn-E and its associated factors in and out of nuage granules. This implies that nuage granules can be considered to be hubs for active, mobile, and transient complexes. We suggest that this is in some way coupled with the execution of the piRNA amplification cycle.

MeSH terms

  • Adenosine Triphosphatases / metabolism
  • Animals
  • Argonaute Proteins / genetics
  • Argonaute Proteins / metabolism
  • Argonaute Proteins / physiology*
  • Biological Transport
  • DNA Transposable Elements / physiology
  • Drosophila / metabolism*
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism
  • Drosophila Proteins / physiology*
  • Models, Biological
  • Nonlinear Dynamics
  • Peptide Initiation Factors / metabolism
  • RNA, Small Interfering / metabolism*
  • Regression Analysis
  • Ubiquitin-Protein Ligases / genetics
  • Ubiquitin-Protein Ligases / metabolism
  • Ubiquitin-Protein Ligases / physiology*

Substances

  • AGO3 protein, Drosophila
  • Argonaute Proteins
  • DNA Transposable Elements
  • Drosophila Proteins
  • Peptide Initiation Factors
  • RNA, Small Interfering
  • aub protein, Drosophila
  • Qin protein, Drosophila
  • Ubiquitin-Protein Ligases
  • Adenosine Triphosphatases
  • spn-E protein, Drosophila