Pterostilbene restores carbapenem susceptibility in New Delhi metallo-β-lactamase-producing isolates by inhibiting the activity of New Delhi metallo-β-lactamases

Br J Pharmacol. 2019 Dec;176(23):4548-4557. doi: 10.1111/bph.14818. Epub 2019 Dec 9.

Abstract

Background and purpose: Bacteria producing New Delhi metallo-β-lactamase-1 (NDM-1) are an increasing clinical threat. NDM-1 can inactivate almost all β-lactams and is not sensitive to any existing β-lactamase inhibitors. To identify effective inhibitors of the NDM-1 enzyme and clarify the mechanism of action, a "lead compound" for developing more potent NDM-1 inhibitors needs to be provided.

Experimental approach: Natural compounds were tested by enzyme inhibition screening to find potential inhibitors. MIC assays, growth curve assays, and time-kill assays were conducted to evaluate the in vitro antibacterial activity of pterostilbene and the combination of pterostilbene and meropenem. A murine thigh model and a mouse pneumonia model were used to evaluate the in vivo efficacy of combined therapy. Molecular modelling and a mutational analysis were used to clarify the mechanism of action.

Key results: Pterostilbene significantly inhibited NDM-1 hydrolysis activity in enzyme inhibition screening assays and effectively restored the effectiveness of meropenem in vitro with NDM-expressing isolates in antibacterial activity assays. In addition, the combined therapy effectively reduced the bacterial burden in a murine thigh model and protected mice from pneumonia caused by Klebsiella pneumoniae. By means of molecular dynamics simulation, we observed that pterostilbene localized to the catalytic pocket of NDM-1, hindering substrate binding to NDM-1 and reducing NDM-1 activity.

Conclusions and implications: These findings indicated that pterostilbene combined with meropenem may offer a new safe and potential "lead compound" for the further development of NDM-1 inhibitors.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Bacterial Agents / chemistry
  • Anti-Bacterial Agents / pharmacology*
  • Carbapenems / chemistry
  • Carbapenems / pharmacology*
  • Enzyme Inhibitors / chemistry
  • Enzyme Inhibitors / pharmacology*
  • Escherichia coli / drug effects
  • Escherichia coli / enzymology
  • Escherichia coli / growth & development
  • Female
  • Klebsiella pneumoniae / drug effects
  • Klebsiella pneumoniae / enzymology
  • Klebsiella pneumoniae / growth & development
  • Mice
  • Mice, Inbred BALB C
  • Microbial Sensitivity Tests
  • Models, Molecular
  • Molecular Structure
  • Stilbenes / chemistry
  • Stilbenes / pharmacology*
  • beta-Lactamases / isolation & purification
  • beta-Lactamases / metabolism*

Substances

  • Anti-Bacterial Agents
  • Carbapenems
  • Enzyme Inhibitors
  • Stilbenes
  • pterostilbene
  • beta-Lactamases
  • beta-lactamase NDM-1