Target repurposing unravels avermectins and derivatives as novel antibiotics inhibiting energy-coupling factor transporters (ECFTs)

Arch Pharm (Weinheim). 2024 Sep;357(9):e2400267. doi: 10.1002/ardp.202400267. Epub 2024 Jun 19.

Abstract

Energy-coupling factor transporters (ECFTs) are membrane-bound ATP-binding cassette (ABC) transporters in prokaryotes that are found in pathogens against which novel antibiotics are urgently needed. To date, just 54 inhibitors of three molecular-structural classes with mostly weak inhibitory activity are known. Target repurposing is a strategy that transfers knowledge gained from a well-studied protein family to under-studied targets of phylogenetic relation. Forty-eight human ABC transporters are known that may harbor structural motifs similar to ECFTs to which particularly multitarget compounds may bind. We assessed 31 multitarget compounds which together target the entire druggable human ABC transporter proteome against ECFTs, of which nine showed inhibitory activity (hit rate 29.0%) and four demonstrated moderate to strong inhibition of an ECFT (IC50 values between 4.28 and 50.2 µM) as well as antibacterial activity against ECFT-expressing Streptococcus pneumoniae. Here, ivermectin was the most potent candidate (MIC95: 22.8 µM), and analysis of five ivermectin derivatives revealed moxidectin as one of the most potent ECFT-targeting antibacterial agents (IC50: 2.23 µM; MIC95: 2.91 µM). Distinct molecular-structural features of avermectins and derivatives as well as the differential biological response of the hit compounds in general provided first indications with respect to the structure-activity relationships and mode of action, respectively.

Keywords: ABC transporter; ECF transporter; avermectin; drug repurposing; milbemycin.

MeSH terms

  • ATP-Binding Cassette Transporters / antagonists & inhibitors
  • ATP-Binding Cassette Transporters / metabolism
  • Anti-Bacterial Agents* / chemical synthesis
  • Anti-Bacterial Agents* / chemistry
  • Anti-Bacterial Agents* / pharmacology
  • Dose-Response Relationship, Drug
  • Drug Repositioning*
  • Humans
  • Ivermectin* / analogs & derivatives
  • Ivermectin* / chemical synthesis
  • Ivermectin* / chemistry
  • Ivermectin* / pharmacology
  • Microbial Sensitivity Tests*
  • Molecular Structure
  • Streptococcus pneumoniae / drug effects
  • Structure-Activity Relationship

Substances

  • Anti-Bacterial Agents
  • Ivermectin
  • avermectin
  • ATP-Binding Cassette Transporters