Rational design of broad spectrum antibacterial activity based on a clinically relevant enoyl-acyl carrier protein (ACP) reductase inhibitor

J Biol Chem. 2014 Jun 6;289(23):15987-6005. doi: 10.1074/jbc.M113.532804. Epub 2014 Apr 16.

Abstract

Determining the molecular basis for target selectivity is of particular importance in drug discovery. The ideal antibiotic should be active against a broad spectrum of pathogenic organisms with a minimal effect on human targets. CG400549, a Staphylococcus-specific 2-pyridone compound that inhibits the enoyl-acyl carrier protein reductase (FabI), has recently been shown to possess human efficacy for the treatment of methicillin-resistant Staphylococcus aureus infections, which constitute a serious threat to human health. In this study, we solved the structures of three different FabI homologues in complex with several pyridone inhibitors, including CG400549. Based on these structures, we rationalize the 65-fold reduced affinity of CG400549 toward Escherichia coli versus S. aureus FabI and implement concepts to improve the spectrum of antibacterial activity. The identification of different conformational states along the reaction coordinate of the enzymatic hydride transfer provides an elegant visual depiction of the relationship between catalysis and inhibition, which facilitates rational inhibitor design. Ultimately, we developed the novel 4-pyridone-based FabI inhibitor PT166 that retained favorable pharmacokinetics and efficacy in a mouse model of S. aureus infection with extended activity against Gram-negative and mycobacterial organisms.

Keywords: CG400549; Drug Design; Enoyl-ACP Reductase; Enzyme Inhibitor; Enzyme Structure; FabI; Lipid Synthesis; Protein Drug Interaction; Staphylococcus aureus; Target Selectivity.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Bacterial Agents / chemistry
  • Anti-Bacterial Agents / pharmacokinetics
  • Anti-Bacterial Agents / pharmacology*
  • Base Sequence
  • Crystallography, X-Ray
  • DNA Primers
  • Drug Design*
  • Enoyl-(Acyl-Carrier-Protein) Reductase (NADH) / antagonists & inhibitors*
  • Enzyme Inhibitors / chemistry
  • Enzyme Inhibitors / pharmacokinetics
  • Enzyme Inhibitors / pharmacology*
  • Female
  • Mice
  • Mice, Inbred ICR
  • Microbial Sensitivity Tests
  • Molecular Structure
  • Polymerase Chain Reaction
  • Pyridones / chemistry
  • Pyridones / pharmacology*
  • Staphylococcus aureus / drug effects
  • Staphylococcus aureus / growth & development

Substances

  • Anti-Bacterial Agents
  • DNA Primers
  • Enzyme Inhibitors
  • Pyridones
  • Enoyl-(Acyl-Carrier-Protein) Reductase (NADH)

Associated data

  • PDB/4BKU
  • PDB/4CUZ
  • PDB/4CV0
  • PDB/4CV1
  • PDB/4CV2
  • PDB/4CV3