Potent 1,2,4-Triazino[5,6 b]indole-3-thioether Inhibitors of the Kanamycin Resistance Enzyme Eis from Mycobacterium tuberculosis

ACS Infect Dis. 2018 Jun 8;4(6):1030-1040. doi: 10.1021/acsinfecdis.8b00074. Epub 2018 Mar 30.

Abstract

A common cause of resistance to kanamycin (KAN) in tuberculosis is overexpression of the enhanced intracellular survival (Eis) protein. Eis is an acetyltransferase that multiacetylates KAN and other aminoglycosides, rendering them unable to bind the bacterial ribosome. By high-throughput screening, a series of substituted 1,2,4-triazino[5,6 b]indole-3-thioether molecules were identified as effective Eis inhibitors. Herein, we purchased 17 and synthesized 22 new compounds, evaluated their potency, and characterized their steady-state kinetics. Four inhibitors were found not only to inhibit Eis in vitro, but also to act as adjuvants of KAN and partially restore KAN sensitivity in a Mycobacterium tuberculosis KAN-resistant strain in which Eis is upregulated. A crystal structure of Eis in complex with a potent inhibitor and CoA shows that the inhibitors bind in the aminoglycoside binding site snugly inserted into a hydrophobic cavity. These inhibitors will undergo preclinical development as novel KAN adjuvant therapies to treat KAN-resistant tuberculosis.

Keywords: aminoglycoside resistance; antitubercular agent; combination therapy; high-throughput screen; structure-activity relationship (SAR).

Publication types

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

MeSH terms

  • A549 Cells
  • Acetyltransferases / antagonists & inhibitors*
  • Acetyltransferases / chemistry*
  • Acetyltransferases / metabolism
  • Antitubercular Agents / pharmacology
  • Bacterial Proteins / antagonists & inhibitors*
  • Bacterial Proteins / chemistry*
  • Bacterial Proteins / metabolism
  • Binding Sites
  • HEK293 Cells
  • Humans
  • Indoles / chemical synthesis
  • Indoles / chemistry*
  • Indoles / pharmacology*
  • Kanamycin / pharmacology
  • Kanamycin Resistance / drug effects*
  • Microbial Sensitivity Tests
  • Mycobacterium tuberculosis / drug effects
  • Mycobacterium tuberculosis / enzymology*
  • Protein Binding
  • Protein Structure, Secondary
  • Regression Analysis
  • Sulfides / chemistry
  • Triazines / chemistry

Substances

  • Antitubercular Agents
  • Bacterial Proteins
  • Indoles
  • Sulfides
  • Triazines
  • Kanamycin
  • Acetyltransferases
  • Eis protein, Mycobacterium tuberculosis