Peptide nucleic acids can form hairpins and bind RNA-binding proteins

PLoS One. 2024 Sep 16;19(9):e0310565. doi: 10.1371/journal.pone.0310565. eCollection 2024.

Abstract

RNA-binding proteins (RBPs) are a major class of proteins that interact with RNAs to change their fate or function. RBPs and the ribonucleoprotein complexes they constitute are involved in many essential cellular processes. In many cases, the molecular details of RBP:RNA interactions differ between viruses, prokaryotes and eukaryotes, making prokaryotic and viral RBPs good potential drug targets. However, targeting RBPs with small molecules has so far been met with limited success as RNA-binding sites tend to be extended, shallow and dynamic with a mixture of charged, polar and hydrophobic interactions. Here, we show that peptide nucleic acids (PNAs) with nucleic acid-like binding properties and a highly stable peptide-like backbone can be used to target some RBPs. We have designed PNAs to mimic the short RNA stem-loop sequence required for the initiation of prokaryotic signal recognition particle (SRP) assembly, a target for antibiotics development. Using a range of biophysical and biochemical assays, the designed PNAs were demonstrated to fold into a hairpin structure, bind the targeted protein and compete with the native RNA hairpin to inhibit SRP formation. To show the applicability of PNAs against other RBPs, a PNA was also shown to bind Nsp9 from SARS-CoV-2, a protein that exhibits non-sequence-specific RNA binding but preferentially binds hairpin structures. Taken together, our results support that PNAs can be a promising class of compounds for targeting RNA-binding activities in RBPs.

MeSH terms

  • Binding Sites
  • Nucleic Acid Conformation
  • Peptide Nucleic Acids* / chemistry
  • Peptide Nucleic Acids* / metabolism
  • Protein Binding*
  • RNA / chemistry
  • RNA / metabolism
  • RNA-Binding Proteins* / chemistry
  • RNA-Binding Proteins* / metabolism
  • SARS-CoV-2 / metabolism
  • Signal Recognition Particle / chemistry
  • Signal Recognition Particle / metabolism

Substances

  • Peptide Nucleic Acids
  • RNA-Binding Proteins
  • RNA
  • Signal Recognition Particle

Grants and funding

The University of Sydney Drug Discovery Initiative (DDI) seed funding The production of 2H13C15N FtsYNG was supported by grant NDF9615 from the National Deuteration Facility, which is partly supported by the National Collaborative Research Infrastructure Strategy – an initiative of the Australian Government. The funders of Drug Discovery Initiative Seed Grant and ANSTO National Dueteration Facility (NDF) Grant had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. NDF staff scientist, Dr Anthony Duff, is a co-author and led the production of isotopically labelled FtsY and proofread the manuscript.