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Crystal structure of A. aeolicus argonaute, a site-specific DNA-guided endoribonuclease, provides insights into RISC-mediated mRNA cleavage

Mol Cell. 2005 Aug 5;19(3):405-19. doi: 10.1016/j.molcel.2005.07.011.

Abstract

Argonaute (Ago) proteins constitute a key component of the RNA-induced silencing complex (RISC). We report the crystal structure of Aquifex aeolicus Ago (Aa-Ago) together with binding and cleavage studies, which establish this eubacterial Ago as a bona fide guide DNA strand-mediated site-specific RNA endonuclease. We have generated a stereochemically robust model of the complex, where the guide DNA-mRNA duplex is positioned within a basic channel spanning the bilobal interface, such that the 5' phosphate of the guide strand can be anchored in a basic pocket, and the mRNA can be positioned for site-specific cleavage by RNase H-type divalent cation-coordinated catalytic Asp residues of the PIWI domain. Domain swap experiments involving chimeras of human Ago (hAgo1) and cleavage-competent hAgo2 reinforce the role of the PIWI domain in "slicer" activity. We propose a four-step Ago-mediated catalytic cleavage cycle model, which provides distinct perspectives into the mechanism of guide strand-mediated mRNA cleavage within the RISC.

Publication types

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

MeSH terms

  • Amino Acid Sequence
  • Argonaute Proteins
  • Bacteria / enzymology*
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Binding Sites / genetics
  • Catalytic Domain / genetics
  • Cations, Divalent / chemistry
  • Crystallography, X-Ray
  • DNA, Single-Stranded / metabolism
  • Endoribonucleases / chemistry*
  • Endoribonucleases / genetics
  • Endoribonucleases / metabolism
  • Eukaryotic Initiation Factor-2
  • Eukaryotic Initiation Factors / genetics
  • Eukaryotic Initiation Factors / metabolism
  • Humans
  • Models, Chemical
  • Models, Molecular
  • Molecular Sequence Data
  • Oligonucleotides / metabolism
  • Peptide Initiation Factors / genetics
  • Peptide Initiation Factors / metabolism
  • Protein Binding
  • Protein Conformation
  • Protein Structure, Tertiary
  • RNA, Double-Stranded / metabolism
  • RNA, Messenger / metabolism*
  • RNA-Induced Silencing Complex / metabolism*
  • Recombinant Fusion Proteins / metabolism
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Sequence Homology, Amino Acid
  • Static Electricity

Substances

  • AGO1 protein, human
  • AGO2 protein, human
  • Argonaute Proteins
  • Bacterial Proteins
  • Cations, Divalent
  • DNA, Single-Stranded
  • Eukaryotic Initiation Factor-2
  • Eukaryotic Initiation Factors
  • Oligonucleotides
  • Peptide Initiation Factors
  • RNA, Double-Stranded
  • RNA, Messenger
  • RNA-Induced Silencing Complex
  • Recombinant Fusion Proteins
  • Recombinant Proteins
  • Endoribonucleases
  • argonaute protein, Aquiflex aeolicus