Roles of mRNA fate modulators Dhh1 and Pat1 in TNRC6-dependent gene silencing recapitulated in yeast

J Biol Chem. 2015 Mar 27;290(13):8331-47. doi: 10.1074/jbc.M114.615088. Epub 2015 Feb 5.

Abstract

The CCR4-NOT complex, the major deadenylase in eukaryotes, plays crucial roles in gene expression at the levels of transcription, mRNA decay, and protein degradation. GW182/TNRC6 proteins, which are core components of the microRNA-induced silencing complex in animals, stimulate deadenylation and repress translation via recruitment of the CCR4-NOT complex. Here we report a heterologous experimental system that recapitulates the recruitment of CCR4-NOT complex by TNRC6 in S. cerevisiae. Using this system, we characterize conserved functions of the CCR4-NOT complex. The complex stimulates degradation of mRNA from the 5' end by Xrn1, in a manner independent of both translation and deadenylation. This degradation pathway is probably conserved in miRNA-mediated gene silencing in zebrafish. Furthermore, the mRNA fate modulators Dhh1 and Pat1 redundantly stimulate mRNA decay, but both factors are required for poly(A) tail-independent translation repression by tethered TNRC6A. Our tethering-based reconstitution system reveals that the conserved architecture of Not1/CNOT1 provides a binding surface for TNRC6, thereby connecting microRNA-induced silencing complex to the decapping machinery as well as the translation apparatus.

Keywords: Gene Silencing; Translation Regulation; Yeast; Zebrafish; mRNA Decay; miRNA Mechanism.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Autoantigens / physiology*
  • Cell Cycle Proteins / metabolism
  • DEAD-box RNA Helicases / physiology*
  • Embryo, Nonmammalian / metabolism
  • Gene Expression Regulation, Fungal
  • Polyadenylation
  • Protein Biosynthesis
  • RNA Interference
  • RNA Stability
  • RNA, Fungal / genetics
  • RNA, Fungal / metabolism
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • RNA-Binding Proteins / physiology*
  • Ribonucleases / metabolism
  • Saccharomyces cerevisiae / genetics*
  • Saccharomyces cerevisiae / metabolism
  • Saccharomyces cerevisiae Proteins / metabolism
  • Saccharomyces cerevisiae Proteins / physiology*
  • Transcription Factors / metabolism
  • Zebrafish / genetics
  • Zebrafish / metabolism
  • Zebrafish Proteins / physiology*

Substances

  • Autoantigens
  • CDC39 protein, S cerevisiae
  • Cell Cycle Proteins
  • PAT1 protein, S cerevisiae
  • RNA, Fungal
  • RNA, Messenger
  • RNA-Binding Proteins
  • Saccharomyces cerevisiae Proteins
  • TNRC6A protein, zebrafish
  • Transcription Factors
  • Zebrafish Proteins
  • CCR4 protein, S cerevisiae
  • Ribonucleases
  • DHH1 protein, S cerevisiae
  • DEAD-box RNA Helicases