Anticodon-binding domain swapping in a nondiscriminating aspartyl-tRNA synthetase reveals contributions to tRNA specificity and catalytic activity

Proteins. 2020 Sep;88(9):1133-1142. doi: 10.1002/prot.25881. Epub 2020 Feb 24.

Abstract

The nondiscriminating aspartyl-tRNA synthetase (ND-AspRS), found in many archaea and bacteria, covalently attaches aspartic acid to tRNAAsp and tRNAAsn generating a correctly charged Asp-tRNAAsp and an erroneous Asp-tRNAAsn . This relaxed tRNA specificity is governed by interactions between the tRNA and the enzyme. In an effort to assess the contributions of the anticodon-binding domain to tRNA specificity, we constructed two chimeric enzymes, Chimera-D and Chimera-N, by replacing the native anticodon-binding domain in the Helicobacter pylori ND-AspRS with that of a discriminating AspRS (Chimera-D) and an asparaginyl-tRNA synthetase (AsnRS, Chimera-N), both from Escherichia coli. Both chimeric enzymes showed similar secondary structure compared to wild-type (WT) ND-AspRS and maintained the ability to form dimeric complexes in solution. Although less catalytically active than WT, Chimera-D was more discriminating as it aspartylated tRNAAsp over tRNAAsn with a specificity ratio of 7.0 compared to 2.9 for the WT enzyme. In contrast, Chimera-N exhibited low catalytic activity toward tRNAAsp and was unable to aspartylate tRNAAsn . The observed catalytic activities for the two chimeras correlate with their heterologous toxicity when expressed in E. coli. Molecular dynamics simulations show a reduced hydrogen bond network at the interface between the anticodon-binding domain and the catalytic domain in Chimera-N compared to Chimera-D or WT, explaining its lower stability and catalytic activity.

Keywords: Helicobacter pylori; ND-AspRS; anticodon-binding; chimeric enzyme; molecular dynamics; tRNA specificity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Anticodon*
  • Aspartate-tRNA Ligase / chemistry
  • Aspartate-tRNA Ligase / genetics
  • Aspartate-tRNA Ligase / metabolism*
  • Binding Sites
  • Biocatalysis
  • Cloning, Molecular
  • Crystallography, X-Ray
  • Escherichia coli / enzymology*
  • Escherichia coli / genetics
  • Gene Expression
  • Genetic Vectors / chemistry
  • Genetic Vectors / metabolism
  • Helicobacter pylori / enzymology*
  • Helicobacter pylori / genetics
  • Molecular Dynamics Simulation
  • Mutation
  • Protein Binding
  • Protein Conformation, alpha-Helical
  • Protein Conformation, beta-Strand
  • Protein Interaction Domains and Motifs
  • RNA, Transfer, Amino Acyl / chemistry
  • RNA, Transfer, Amino Acyl / genetics
  • RNA, Transfer, Amino Acyl / metabolism*
  • RNA, Transfer, Asn / chemistry
  • RNA, Transfer, Asn / metabolism*
  • RNA, Transfer, Asp / chemistry
  • RNA, Transfer, Asp / metabolism*
  • Recombinant Fusion Proteins / chemistry
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / metabolism
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism
  • Sequence Alignment
  • Sequence Homology, Amino Acid
  • Substrate Specificity

Substances

  • Anticodon
  • RNA, Transfer, Amino Acyl
  • RNA, Transfer, Asn
  • RNA, Transfer, Asp
  • Recombinant Fusion Proteins
  • Recombinant Proteins
  • Aspartate-tRNA Ligase
  • asparaginyl-tRNA synthetase