The mechanism of discriminative aminoacylation by isoleucyl-tRNA synthetase based on wobble nucleotide recognition

Nat Commun. 2024 Dec 30;15(1):10817. doi: 10.1038/s41467-024-55183-0.

Abstract

The faithful charging of amino acids to cognate tRNAs by aminoacyl-tRNA synthetases (AARSs) determines the fidelity of protein translation. Isoleucyl-tRNA synthetase (IleRS) distinguishes tRNAIle from tRNAMet solely based on the nucleotide at wobble position (N34), and a single substitution at N34 could exchange the aminoacylation specificity between two tRNAs. Here, we report the structural and biochemical mechanism of N34 recognition-based tRNA discrimination by Saccharomyces cerevisiae IleRS (ScIleRS). ScIleRS utilizes a eukaryotic/archaeal-specific arginine as the H-bond donor to recognize the common carbonyl group (H-bond acceptor) of various N34s of tRNAIle, which induces mutual structural adaptations between ScIleRS and tRNAIle to achieve a preferable editing state. C34 of unmodified tRNAIle(CAU) (behaves like tRNAMet) lacks a relevant H-bond acceptor, which disrupts key H-bonding interactions and structural adaptations and suspends the ScIleRS·tRNAIle(CAU) complex in an initial non-reactive state. This wobble nucleotide recognition-based structural adaptation provides mechanistic insights into selective tRNA aminoacylation by AARSs.

MeSH terms

  • Aminoacylation*
  • Arginine / chemistry
  • Arginine / metabolism
  • Crystallography, X-Ray
  • Hydrogen Bonding
  • Isoleucine-tRNA Ligase* / chemistry
  • Isoleucine-tRNA Ligase* / genetics
  • Isoleucine-tRNA Ligase* / metabolism
  • Models, Molecular
  • Nucleotides / metabolism
  • RNA, Transfer, Ile / chemistry
  • RNA, Transfer, Ile / genetics
  • RNA, Transfer, Ile / metabolism
  • Saccharomyces cerevisiae Proteins / chemistry
  • Saccharomyces cerevisiae Proteins / genetics
  • Saccharomyces cerevisiae Proteins / metabolism
  • Saccharomyces cerevisiae* / genetics
  • Saccharomyces cerevisiae* / metabolism
  • Substrate Specificity
  • Transfer RNA Aminoacylation

Substances

  • Isoleucine-tRNA Ligase
  • Saccharomyces cerevisiae Proteins
  • RNA, Transfer, Ile
  • Nucleotides
  • Arginine