Bioluminescent Reporters for Rapid Mechanism of Action Assessment in Tuberculosis Drug Discovery

Antimicrob Agents Chemother. 2016 Oct 21;60(11):6748-6757. doi: 10.1128/AAC.01178-16. Print 2016 Nov.

Abstract

The tuberculosis (TB) drug discovery pipeline is fueled by compounds identified in whole-cell screens against the causative agent, Mycobacterium tuberculosis Phenotypic screening enables the selection of molecules that inhibit essential cellular functions in live, intact bacilli grown under a chosen in vitro condition. However, deducing the mechanism of action (MOA), which is important to avoid promiscuous targets, often requires significant biological resources in a lengthy process that risks decoupling medicinal chemistry and biology efforts. Therefore, there is a need to develop methods enabling rapid MOA assessment of putative "actives" for triage decisions. Here, we describe a modified version of a bioluminescence reporter assay that allows nondestructive detection of compounds targeting either of two macromolecular processes in M. tuberculosis: cell wall biosynthesis or maintenance of DNA integrity. Coupling the luxCDABE operon from Photorhabdus luminescens to mycobacterial promoters driving expression of the iniBAC operon (PiniB-LUX) or the DNA damage-inducible genes, recA (PrecA-LUX) or radA (PradA-LUX), provided quantitative detection in real time of compounds triggering expression of any of these promoters over an extended 10- to 12-day incubation. Testing against known anti-TB agents confirmed the specificity of each reporter in registering the MOA of the applied antibiotic in M. tuberculosis, independent of bactericidal or bacteriostatic activity. Moreover, profiles obtained for experimental compounds indicated the potential to infer complex MOAs in which multiple cellular processes are disrupted. These results demonstrate the utility of the reporters for early triage of compounds based on the provisional MOA and suggest their application to investigate polypharmacology in known and experimental anti-TB agents.

Publication types

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

MeSH terms

  • Antitubercular Agents / chemistry
  • Antitubercular Agents / pharmacology*
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Cell Wall / drug effects*
  • Cell Wall / genetics
  • Cell Wall / metabolism
  • DNA, Bacterial / genetics*
  • DNA, Bacterial / metabolism
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Drug Discovery*
  • Genes, Reporter*
  • High-Throughput Screening Assays*
  • Luciferases / genetics
  • Luciferases / metabolism
  • Luminescent Measurements
  • Mycobacterium tuberculosis / drug effects
  • Mycobacterium tuberculosis / genetics
  • Mycobacterium tuberculosis / growth & development
  • Mycobacterium tuberculosis / metabolism
  • Operon
  • Photorhabdus / chemistry
  • Photorhabdus / genetics
  • Photorhabdus / metabolism
  • Promoter Regions, Genetic
  • Rec A Recombinases / genetics
  • Rec A Recombinases / metabolism

Substances

  • Antitubercular Agents
  • Bacterial Proteins
  • DNA, Bacterial
  • DNA-Binding Proteins
  • RadA protein, bacteria
  • Luciferases
  • Rec A Recombinases