The anti-tubercular callyaerins target the Mycobacterium tuberculosis-specific non-essential membrane protein Rv2113

Cell Chem Biol. 2024 Oct 17;31(10):1755-1771.e73. doi: 10.1016/j.chembiol.2024.06.002. Epub 2024 Jul 8.

Abstract

Spread of antimicrobial resistances urges a need for new drugs against Mycobacterium tuberculosis (Mtb) with mechanisms differing from current antibiotics. Previously, callyaerins were identified as promising anti-tubercular agents, representing a class of hydrophobic cyclopeptides with an unusual (Z)-2,3-di-aminoacrylamide unit. Here, we investigated the molecular mechanisms underlying their antimycobacterial properties. Structure-activity relationship studies enabled the identification of structural determinants relevant for antibacterial activity. Callyaerins are bacteriostatics selectively active against Mtb, including extensively drug-resistant strains, with minimal cytotoxicity against human cells and promising intracellular activity. By combining mutant screens and various chemical proteomics approaches, we showed that callyaerins target the non-essential, Mtb-specific membrane protein Rv2113, triggering a complex dysregulation of the proteome, characterized by global downregulation of lipid biosynthesis, cell division, DNA repair, and replication. Our study thus identifies Rv2113 as a previously undescribed Mtb-specific drug target and demonstrates that also non-essential proteins may represent efficacious targets for antimycobacterial drugs.

Keywords: Mycobacterium tuberculosis; anti-TB drug development; antibiotic action; callyaerin; cyclopeptide; natural product; photoaffinity labeling.

MeSH terms

  • Antitubercular Agents* / chemistry
  • Antitubercular Agents* / pharmacology
  • Bacterial Proteins* / antagonists & inhibitors
  • Bacterial Proteins* / genetics
  • Bacterial Proteins* / metabolism
  • Humans
  • Membrane Proteins / antagonists & inhibitors
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Microbial Sensitivity Tests*
  • Mycobacterium tuberculosis* / drug effects
  • Mycobacterium tuberculosis* / metabolism
  • Peptides, Cyclic / chemistry
  • Peptides, Cyclic / pharmacology
  • Structure-Activity Relationship

Substances

  • Bacterial Proteins
  • Antitubercular Agents
  • Membrane Proteins
  • Peptides, Cyclic