Signatures of Nucleotide Analog Incorporation by an RNA-Dependent RNA Polymerase Revealed Using High-Throughput Magnetic Tweezers

Cell Rep. 2017 Oct 24;21(4):1063-1076. doi: 10.1016/j.celrep.2017.10.005.

Abstract

RNA viruses pose a threat to public health that is exacerbated by the dearth of antiviral therapeutics. The RNA-dependent RNA polymerase (RdRp) holds promise as a broad-spectrum, therapeutic target because of the conserved nature of the nucleotide-substrate-binding and catalytic sites. Conventional, quantitative, kinetic analysis of antiviral ribonucleotides monitors one or a few incorporation events. Here, we use a high-throughput magnetic tweezers platform to monitor the elongation dynamics of a prototypical RdRp over thousands of nucleotide-addition cycles in the absence and presence of a suite of nucleotide analog inhibitors. We observe multiple RdRp-RNA elongation complexes; only a subset of which are competent for analog utilization. Incorporation of a pyrazine-carboxamide nucleotide analog, T-1106, leads to RdRp backtracking. This analysis reveals a mechanism of action for this antiviral ribonucleotide that is corroborated by cellular studies. We propose that induced backtracking represents a distinct mechanistic class of antiviral ribonucleotides.

Keywords: RNA polymerase; RNA virus; T-1106; T-705; backtracking; inhibitor; magnetic tweezers; nucleoside analog; pyrazine carboxamide.

MeSH terms

  • Antiviral Agents / chemistry
  • Antiviral Agents / pharmacology*
  • HeLa Cells
  • Humans
  • Imaging, Three-Dimensional
  • Magnetic Fields
  • Nucleosides / chemistry
  • Nucleosides / pharmacology*
  • Pyrazines / chemistry
  • Pyrazines / pharmacology*
  • RNA-Dependent RNA Polymerase / antagonists & inhibitors
  • RNA-Dependent RNA Polymerase / chemistry
  • RNA-Dependent RNA Polymerase / metabolism*
  • Ribonucleotides / chemistry
  • Ribonucleotides / metabolism
  • Viral Proteins / antagonists & inhibitors
  • Viral Proteins / chemistry
  • Viral Proteins / metabolism*

Substances

  • Antiviral Agents
  • Nucleosides
  • Pyrazines
  • Ribonucleotides
  • T 1106
  • Viral Proteins
  • RNA-Dependent RNA Polymerase