Coupled 5' nucleotide recognition and processivity in Xrn1-mediated mRNA decay

Mol Cell. 2011 Mar 4;41(5):600-8. doi: 10.1016/j.molcel.2011.02.004.

Abstract

Messenger RNA decay plays a central role in the regulation and surveillance of eukaryotic gene expression. The conserved multidomain exoribonuclease Xrn1 targets cytoplasmic RNA substrates marked by a 5' monophosphate for processive 5'-to-3' degradation by an unknown mechanism. Here, we report the crystal structure of an Xrn1-substrate complex. The single-stranded substrate is held in place by stacking of the 5'-terminal trinucleotide between aromatic side chains while a highly basic pocket specifically recognizes the 5' phosphate. Mutations of residues involved in binding the 5'-terminal nucleotide impair Xrn1 processivity. The substrate recognition mechanism allows Xrn1 to couple processive hydrolysis to duplex melting in RNA substrates with sufficiently long single-stranded 5' overhangs. The Xrn1-substrate complex structure thus rationalizes the exclusive specificity of Xrn1 for 5'-monophosphorylated substrates, ensuring fidelity of mRNA turnover, and posits a model for translocation-coupled unwinding of structured RNA substrates.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Catalysis
  • Drosophila Proteins / genetics*
  • Drosophila melanogaster
  • Exoribonucleases / genetics*
  • Hydrolysis
  • Magnesium / chemistry
  • Mutation
  • Nucleic Acid Conformation
  • Nucleotides / genetics*
  • Phosphates / chemistry
  • Phosphorylation
  • Protein Conformation
  • Protein Structure, Tertiary
  • RNA, Messenger / metabolism*

Substances

  • Drosophila Proteins
  • Nucleotides
  • Phosphates
  • RNA, Messenger
  • Exoribonucleases
  • pcm protein, Drosophila
  • Magnesium

Associated data

  • PDB/2Y35