Structural basis of DNA gyrase inhibition by antibacterial QPT-1, anticancer drug etoposide and moxifloxacin

Nat Commun. 2015 Dec 7:6:10048. doi: 10.1038/ncomms10048.

Abstract

New antibacterials are needed to tackle antibiotic-resistant bacteria. Type IIA topoisomerases (topo2As), the targets of fluoroquinolones, regulate DNA topology by creating transient double-strand DNA breaks. Here we report the first co-crystal structures of the antibacterial QPT-1 and the anticancer drug etoposide with Staphylococcus aureus DNA gyrase, showing binding at the same sites in the cleaved DNA as the fluoroquinolone moxifloxacin. Unlike moxifloxacin, QPT-1 and etoposide interact with conserved GyrB TOPRIM residues rationalizing why QPT-1 can overcome fluoroquinolone resistance. Our data show etoposide's antibacterial activity is due to DNA gyrase inhibition and suggests other anticancer agents act similarly. Analysis of multiple DNA gyrase co-crystal structures, including asymmetric cleavage complexes, led to a 'pair of swing-doors' hypothesis in which the movement of one DNA segment regulates cleavage and religation of the second DNA duplex. This mechanism can explain QPT-1's bacterial specificity. Structure-based strategies for developing topo2A antibacterials are suggested.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anti-Bacterial Agents / chemistry*
  • Anti-Bacterial Agents / pharmacology
  • Antineoplastic Agents / chemistry*
  • Antineoplastic Agents / pharmacology
  • DNA Gyrase / chemistry*
  • DNA Gyrase / genetics
  • DNA Gyrase / metabolism
  • DNA, Bacterial / chemistry
  • DNA, Bacterial / genetics
  • DNA, Bacterial / metabolism
  • Drug Resistance, Bacterial
  • Etoposide / chemistry*
  • Etoposide / pharmacology
  • Fluoroquinolones / chemistry*
  • Fluoroquinolones / pharmacology
  • Models, Molecular
  • Molecular Structure
  • Moxifloxacin
  • Staphylococcus aureus / chemistry
  • Staphylococcus aureus / drug effects
  • Staphylococcus aureus / enzymology*
  • Topoisomerase II Inhibitors / chemistry*
  • Topoisomerase II Inhibitors / pharmacology

Substances

  • Anti-Bacterial Agents
  • Antineoplastic Agents
  • DNA, Bacterial
  • Fluoroquinolones
  • Topoisomerase II Inhibitors
  • Etoposide
  • DNA Gyrase
  • Moxifloxacin