The minor groove-binding agent ELB-21 forms multiple interstrand and intrastrand covalent cross-links with duplex DNA and displays potent bactericidal activity against methicillin-resistant Staphylococcus aureus

J Antimicrob Chemother. 2011 May;66(5):985-96. doi: 10.1093/jac/dkr044. Epub 2011 Mar 3.

Abstract

Objectives: The antistaphylococcal pyrrolobenzodiazepine dimer ELB-21 forms multiple adducts with duplex DNA through covalent interactions with appropriately spaced guanine residues; it is now known to form interstrand and intrastrand adducts with oligonucleotide sequences of variable length. We determined the DNA sequence preferences of ELB-21 in relation to its capacity to exert a bactericidal effect by damaging DNA.

Methods: Formation of adducts by ELB-21 and 12- to 14-mer DNA duplexes was investigated using ion-pair reversed phase liquid chromatography and mass spectrometry. Drug-induced changes in gene expression were measured in prophage-free Staphylococcus aureus RN4220 by microarray analysis.

Results: ELB-21 preferentially formed intrastrand adducts with guanines separated by three nucleotide base pairs. Interstrand and intrastrand adducts were formed with duplexes both longer and shorter than the preferred target sequences. ELB-21 elicited rapid bactericidal effects against prophage-carrying and prophage-free S. aureus strains; cell lysis occurred following activation and release of resident prophages. Killing appeared to be due to irreparable damage to bacterial DNA and susceptibility to ELB-21 was governed by the capacity of staphylococci to repair DNA lesions through induction of the SOS DNA damage response mediated by the RecA-LexA pathway.

Conclusions: The data support the contention that ELB-21 arrests DNA replication, eliciting formation of ssDNA-RecA filaments that inactivate LexA, the SOS repressor, and phage repressors such as Cl, resulting in activation of the DNA damage response and de-repression of resident prophages. Above the MIC threshold, DNA repair is ineffective.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anti-Bacterial Agents / metabolism*
  • Anti-Bacterial Agents / pharmacology*
  • Benzodiazepines / metabolism*
  • Benzodiazepines / pharmacology*
  • Binding Sites
  • DNA / metabolism*
  • DNA Adducts / metabolism
  • DNA Adducts / pharmacology
  • DNA Repair / drug effects
  • Gene Expression Profiling
  • Gene Expression Regulation, Bacterial / drug effects
  • Methicillin-Resistant Staphylococcus aureus / drug effects*
  • Microarray Analysis
  • Microbial Viability / drug effects*
  • Protein Binding
  • Pyrroles / metabolism*
  • Pyrroles / pharmacology*

Substances

  • Anti-Bacterial Agents
  • DNA Adducts
  • Pyrroles
  • pyrrolo(2,1-c)(1,4)benzodiazepine
  • Benzodiazepines
  • DNA