Dis3l2-Mediated Decay Is a Quality Control Pathway for Noncoding RNAs

Cell Rep. 2016 Aug 16;16(7):1861-73. doi: 10.1016/j.celrep.2016.07.025. Epub 2016 Aug 4.

Abstract

Mutations in the 3'-5' exonuclease DIS3L2 are associated with Perlman syndrome and hypersusceptibility to Wilms tumorigenesis. Previously, we found that Dis3l2 specifically recognizes and degrades uridylated pre-let-7 microRNA. However, the widespread relevance of Dis3l2-mediated decay of uridylated substrates remains unknown. Here, we applied an unbiased RNA immunoprecipitation strategy to identify Dis3l2 targets in mouse embryonic stem cells. The disease-associated long noncoding RNA (lncRNA) Rmrp, 7SL, as well as several other Pol III-transcribed noncoding RNAs (ncRNAs) were among the most highly enriched Dis3l2-bound RNAs. 3'-Uridylated Rmrp, 7SL, and small nuclear RNA (snRNA) species were highly stabilized in the cytoplasm of Dis3l2-depleted cells. Deep sequencing analysis of Rmrp 3' ends revealed extensive oligouridylation mainly on transcripts with imprecise ends. We implicate the terminal uridylyl transferases (TUTases) Zcchc6/11 in the uridylation of these ncRNAs, and biochemical reconstitution assays demonstrate the sufficiency of TUTase-Dis3l2 for Rmrp decay. This establishes Dis3l2-mediated decay (DMD) as a quality-control pathway that eliminates aberrant ncRNAs.

Keywords: 7SL; Dis3l2; Rmrp; TUTase; Zcchc11; Zcchc6; lncRNA; snRNA; uridylation.

MeSH terms

  • Animals
  • CRISPR-Cas Systems
  • Cells, Cultured
  • Exoribonucleases / deficiency
  • Exoribonucleases / genetics*
  • Gene Editing
  • Gene Expression Regulation
  • Humans
  • Immunoprecipitation
  • Mice
  • MicroRNAs / genetics*
  • MicroRNAs / metabolism
  • Mouse Embryonic Stem Cells / cytology
  • Mouse Embryonic Stem Cells / metabolism
  • Protein Binding
  • RNA Cleavage*
  • RNA Nucleotidyltransferases / genetics
  • RNA Nucleotidyltransferases / metabolism
  • RNA Stability
  • RNA, Small Cytoplasmic / genetics*
  • RNA, Small Cytoplasmic / metabolism
  • RNA, Untranslated / genetics*
  • RNA, Untranslated / metabolism
  • Signal Recognition Particle / genetics*
  • Signal Recognition Particle / metabolism
  • Signal Transduction
  • Uridine / metabolism

Substances

  • 7SL RNA
  • MicroRNAs
  • RNA, Small Cytoplasmic
  • RNA, Untranslated
  • Signal Recognition Particle
  • RNA Nucleotidyltransferases
  • Dis3l2 protein, mouse
  • Exoribonucleases
  • Uridine