SQ109 targets MmpL3, a membrane transporter of trehalose monomycolate involved in mycolic acid donation to the cell wall core of Mycobacterium tuberculosis

Antimicrob Agents Chemother. 2012 Apr;56(4):1797-809. doi: 10.1128/AAC.05708-11. Epub 2012 Jan 17.

Abstract

SQ109, a 1,2-diamine related to ethambutol, is currently in clinical trials for the treatment of tuberculosis, but its mode of action remains unclear. Here, we demonstrate that SQ109 disrupts cell wall assembly, as evidenced by macromolecular incorporation assays and ultrastructural analyses. SQ109 interferes with the assembly of mycolic acids into the cell wall core of Mycobacterium tuberculosis, as bacilli exposed to SQ109 show immediate inhibition of trehalose dimycolate (TDM) production and fail to attach mycolates to the cell wall arabinogalactan. These effects were not due to inhibition of mycolate synthesis, since total mycolate levels were unaffected, but instead resulted in the accumulation of trehalose monomycolate (TMM), the precursor of TDM and cell wall mycolates. In vitro assays using purified enzymes showed that this was not due to inhibition of the secreted Ag85 mycolyltransferases. We were unable to achieve spontaneous generation of SQ109-resistant mutants; however, analogs of this compound that resulted in similar shutdown of TDM synthesis with concomitant TMM accumulation were used to spontaneously generate resistant mutants that were also cross-resistant to SQ109. Whole-genome sequencing of these mutants showed that these all had mutations in the essential mmpL3 gene, which encodes a transmembrane transporter. Our results suggest that MmpL3 is the target of SQ109 and that MmpL3 is a transporter of mycobacterial TMM.

Publication types

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

MeSH terms

  • Acyltransferases / metabolism
  • Adamantane / analogs & derivatives*
  • Adamantane / pharmacology
  • Aerobiosis
  • Antigens, Bacterial / metabolism
  • Antitubercular Agents / pharmacology*
  • Bacterial Proteins / drug effects*
  • Cell Wall / drug effects
  • Cell Wall / metabolism*
  • Chromatography, Thin Layer
  • Cord Factors / metabolism*
  • Drug Resistance, Bacterial / genetics
  • Ethylenediamines / pharmacology*
  • Lipid Metabolism
  • Membrane Transport Proteins / drug effects*
  • Microbial Sensitivity Tests
  • Microscopy, Electron
  • Mutation / genetics
  • Mycobacterium tuberculosis / drug effects
  • Mycobacterium tuberculosis / metabolism*
  • Mycobacterium tuberculosis / ultrastructure
  • Mycolic Acids / metabolism*

Substances

  • Antigens, Bacterial
  • Antitubercular Agents
  • Bacterial Proteins
  • Cord Factors
  • Ethylenediamines
  • Membrane Transport Proteins
  • MmpL7 protein, Mycobacterium tuberculosis H37Rv
  • Mycolic Acids
  • N-geranyl-N'-(2-adamantyl)ethane-1,2-diamine
  • trehalose monomycolate
  • Acyltransferases
  • antigen 85A, Mycobacterium tuberculosis
  • Adamantane