Characterization of DprE1-Mediated Benzothiazinone Resistance in Mycobacterium tuberculosis

Antimicrob Agents Chemother. 2016 Oct 21;60(11):6451-6459. doi: 10.1128/AAC.01523-16. Print 2016 Nov.

Abstract

Benzothiazinones (BTZs) are a class of compounds found to be extremely potent against both drug-susceptible and drug-resistant Mycobacterium tuberculosis strains. The potency of BTZs is explained by their specificity for their target decaprenylphosphoryl-d-ribose oxidase (DprE1), in particular by covalent binding of the activated form of the compound to the critical cysteine 387 residue of the enzyme. To probe the role of C387, we used promiscuous site-directed mutagenesis to introduce other codons at this position into dprE1 of M. tuberculosis The resultant viable BTZ-resistant mutants were characterized in vitro, ex vivo, and biochemically to gain insight into the effects of these mutations on DprE1 function and on M. tuberculosis Five different mutations (C387G, C387A, C387S, C387N, and C387T) conferred various levels of resistance to BTZ and exhibited different phenotypes. The C387G and C387N mutations resulted in a lower growth rate of the mycobacterium on solid medium, which could be attributed to the significant decrease in the catalytic efficiency of the DprE1 enzyme. All five mutations rendered the mycobacterium less cytotoxic to macrophages. Finally, differences in the potencies of covalent and noncovalent DprE1 inhibitors in the presence of C387 mutations were revealed by enzymatic assays. As expected from the mechanism of action, the covalent inhibitor PBTZ169 only partially inhibited the mutant DprE1 enzymes compared to the near-complete inhibition with a noncovalent DprE1 inhibitor, Ty38c. This study emphasizes the importance of the C387 residue for DprE1 activity and for the killing action of covalent inhibitors such as BTZs and other recently identified nitroaromatic inhibitors.

MeSH terms

  • Alcohol Oxidoreductases / antagonists & inhibitors*
  • Alcohol Oxidoreductases / chemistry
  • Alcohol Oxidoreductases / genetics
  • Alcohol Oxidoreductases / metabolism
  • Amino Acid Substitution
  • Antitubercular Agents / chemistry
  • Antitubercular Agents / pharmacology*
  • Bacterial Proteins / antagonists & inhibitors*
  • Bacterial Proteins / chemistry
  • Bacterial Proteins / genetics
  • Bacterial Proteins / metabolism
  • Cell Line
  • Cysteine / chemistry
  • Cysteine / metabolism
  • Drug Resistance, Multiple, Bacterial / genetics*
  • Enzyme Inhibitors / chemistry
  • Enzyme Inhibitors / pharmacology
  • Gene Expression
  • Humans
  • Macrophages / microbiology
  • Molecular Docking Simulation
  • Mutagenesis, Site-Directed
  • Mutation*
  • Mycobacterium smegmatis / drug effects
  • Mycobacterium smegmatis / enzymology
  • Mycobacterium smegmatis / genetics
  • Mycobacterium smegmatis / growth & development
  • Mycobacterium tuberculosis / drug effects*
  • Mycobacterium tuberculosis / enzymology
  • Mycobacterium tuberculosis / genetics
  • Mycobacterium tuberculosis / growth & development
  • Phenotype
  • Piperazines / chemistry
  • Piperazines / pharmacology
  • Structure-Activity Relationship
  • Thiazines / chemistry
  • Thiazines / pharmacology
  • Tuberculosis, Multidrug-Resistant / microbiology

Substances

  • Antitubercular Agents
  • Bacterial Proteins
  • Enzyme Inhibitors
  • Piperazines
  • Thiazines
  • macozinone
  • Alcohol Oxidoreductases
  • DprE1 protein, Mycobacterium tuberculosis
  • Cysteine

Grants and funding

This work was supported by the European Community's Seventh Framework Program FP7/2007-2013 under grant agreement 260872. Benoit Lechartier was a recipient of a grant from the Fondation Jacqueline Beytout. João Neres was awarded a Marie Curie fellowship.