The guide-RNA sequence dictates the slicing kinetics and conformational dynamics of the Argonaute silencing complex

Mol Cell. 2024 Aug 8;84(15):2918-2934.e11. doi: 10.1016/j.molcel.2024.06.026. Epub 2024 Jul 17.

Abstract

The RNA-induced silencing complex (RISC), which powers RNA interference (RNAi), consists of a guide RNA and an Argonaute protein that slices target RNAs complementary to the guide. We find that, for different guide-RNA sequences, slicing rates of perfectly complementary bound targets can be surprisingly different (>250-fold range), and that faster slicing confers better knockdown in cells. Nucleotide sequence identities at guide-RNA positions 7, 10, and 17 underlie much of this variation in slicing rates. Analysis of one of these determinants implicates a structural distortion at guide nucleotides 6-7 in promoting slicing. Moreover, slicing directed by different guide sequences has an unanticipated, 600-fold range in 3'-mismatch tolerance, attributable to guides with weak (AU-rich) central pairing requiring extensive 3' complementarity (pairing beyond position 16) to more fully populate the slicing-competent conformation. Together, our analyses identify sequence determinants of RISC activity and provide biochemical and conformational rationale for their action.

Keywords: AGO2; Argonaute; RISC; RNA-protein interactions; RNAi; kinetic analysis; microRNA; siRNA; slicing.

MeSH terms

  • Argonaute Proteins* / chemistry
  • Argonaute Proteins* / genetics
  • Argonaute Proteins* / metabolism
  • Base Sequence
  • HEK293 Cells
  • Humans
  • Kinetics
  • Nucleic Acid Conformation*
  • RNA Interference
  • RNA, Guide, CRISPR-Cas Systems* / genetics
  • RNA, Guide, CRISPR-Cas Systems* / metabolism
  • RNA-Induced Silencing Complex* / chemistry
  • RNA-Induced Silencing Complex* / genetics
  • RNA-Induced Silencing Complex* / metabolism

Substances

  • Argonaute Proteins
  • RNA-Induced Silencing Complex
  • RNA, Guide, CRISPR-Cas Systems
  • AGO2 protein, human