Discovery of Small-Molecule Antibiotics against a Unique tRNA-Mediated Regulation of Transcription in Gram-Positive Bacteria

ChemMedChem. 2019 Apr 3;14(7):758-769. doi: 10.1002/cmdc.201800744. Epub 2019 Mar 1.

Abstract

The emergence of multidrug-resistant bacteria necessitates the identification of unique targets of intervention and compounds that inhibit their function. Gram-positive bacteria use a well-conserved tRNA-responsive transcriptional regulatory element in mRNAs, known as the T-box, to regulate the transcription of multiple operons that control amino acid metabolism. T-box regulatory elements are found only in the 5'-untranslated region (UTR) of mRNAs of Gram-positive bacteria, not Gram-negative bacteria or the human host. Using the structure of the 5'UTR sequence of the Bacillus subtilis tyrosyl-tRNA synthetase mRNA T-box as a model, in silico docking of 305 000 small compounds initially yielded 700 as potential binders that could inhibit the binding of the tRNA ligand. A single family of compounds inhibited the growth of Gram-positive bacteria, but not Gram-negative bacteria, including drug-resistant clinical isolates at minimum inhibitory concentrations (MIC 16-64 μg mL-1 ). Resistance developed at an extremely low mutational frequency (1.21×10-10 ). At 4 μg mL-1 , the parent compound PKZ18 significantly inhibited in vivo transcription of glycyl-tRNA synthetase mRNA. PKZ18 also inhibited in vivo translation of the S. aureus threonyl-tRNA synthetase protein. PKZ18 bound to the Specifier Loop in vitro (Kd ≈24 μm). Its core chemistry necessary for antibacterial activity has been identified. These findings support the T-box regulatory mechanism as a new target for antibiotic discovery that may impede the emergence of resistance.

Keywords: Gram-positive bacteria; antibiotic resistance; drug discovery; gene expression; tRNA.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anti-Bacterial Agents / chemistry
  • Anti-Bacterial Agents / pharmacology*
  • Drug Discovery*
  • Gene Expression Regulation, Bacterial / drug effects*
  • Gram-Positive Bacteria / drug effects*
  • Gram-Positive Bacteria / genetics
  • Magnetic Resonance Spectroscopy
  • Microbial Sensitivity Tests
  • Molecular Docking Simulation
  • RNA, Messenger / genetics
  • RNA, Transfer / metabolism*
  • Small Molecule Libraries / chemistry
  • Small Molecule Libraries / pharmacology*
  • Structure-Activity Relationship
  • Transcription, Genetic / drug effects*

Substances

  • Anti-Bacterial Agents
  • RNA, Messenger
  • Small Molecule Libraries
  • RNA, Transfer