Structural basis for the Nanos-mediated recruitment of the CCR4-NOT complex and translational repression

Genes Dev. 2014 Apr 15;28(8):888-901. doi: 10.1101/gad.237289.113.

Abstract

The RNA-binding proteins of the Nanos family play an essential role in germ cell development and survival in a wide range of metazoan species. They function by suppressing the expression of target mRNAs through the recruitment of effector complexes, which include the CCR4-NOT deadenylase complex. Here, we show that the three human Nanos paralogs (Nanos1-3) interact with the CNOT1 C-terminal domain and determine the structural basis for the specific molecular recognition. Nanos1-3 bind CNOT1 through a short CNOT1-interacting motif (NIM) that is conserved in all vertebrates and some invertebrate species. The crystal structure of the human Nanos1 NIM peptide bound to CNOT1 reveals that the peptide opens a conserved hydrophobic pocket on the CNOT1 surface by inserting conserved aromatic residues. The substitutions of these aromatic residues in the Nanos1-3 NIMs abolish binding to CNOT1 and abrogate the ability of the proteins to repress translation. Our findings provide the structural basis for the recruitment of the CCR4-NOT complex by vertebrate Nanos, indicate that the NIMs are the major determinants of the translational repression mediated by Nanos, and identify the CCR4-NOT complex as the main effector complex for Nanos function.

Keywords: SLiM; deadenylation; decapping; mRNA decay; translational repression.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Motifs
  • Conserved Sequence
  • Gene Expression Regulation*
  • HEK293 Cells
  • Humans
  • Models, Molecular*
  • Multiprotein Complexes / chemistry
  • Nuclear Receptor Subfamily 4, Group A, Member 2 / chemistry*
  • Nuclear Receptor Subfamily 4, Group A, Member 2 / metabolism*
  • Peptides / chemistry
  • Peptides / metabolism
  • Protein Binding
  • Protein Structure, Quaternary
  • RNA Stability / genetics
  • RNA, Messenger / metabolism
  • RNA-Binding Proteins / genetics
  • RNA-Binding Proteins / metabolism*
  • Receptors, CCR4 / chemistry*
  • Receptors, CCR4 / metabolism*
  • Reproducibility of Results

Substances

  • CCR4 protein, human
  • Multiprotein Complexes
  • NR4A2 protein, human
  • Nuclear Receptor Subfamily 4, Group A, Member 2
  • Peptides
  • RNA, Messenger
  • RNA-Binding Proteins
  • Receptors, CCR4

Associated data

  • PDB/4CQO