Metabolomics-Based Screening of the Malaria Box Reveals both Novel and Established Mechanisms of Action

Antimicrob Agents Chemother. 2016 Oct 21;60(11):6650-6663. doi: 10.1128/AAC.01226-16. Print 2016 Nov.

Abstract

High-throughput phenotypic screening of chemical libraries has resulted in the identification of thousands of compounds with potent antimalarial activity, although in most cases, the mechanism(s) of action of these compounds remains unknown. Here we have investigated the mode of action of 90 antimalarial compounds derived from the Malaria Box collection using high-coverage, untargeted metabolomics analysis. Approximately half of the tested compounds induced significant metabolic perturbations in in vitro cultures of Plasmodium falciparum In most cases, the metabolic profiles were highly correlated with known antimalarials, in particular artemisinin, the 4-aminoquinolines, or atovaquone. Select Malaria Box compounds also induced changes in intermediates in essential metabolic pathways, such as isoprenoid biosynthesis (i.e., 2-C-methyl-d-erythritol 2,4-cyclodiphosphate) and linolenic acid metabolism (i.e., traumatic acid). This study provides a comprehensive database of the metabolic perturbations induced by chemically diverse inhibitors and highlights the utility of metabolomics for triaging new lead compounds and defining specific modes of action, which will assist with the development and optimization of new antimalarial drugs.

MeSH terms

  • Aminoquinolines / pharmacology
  • Antimalarials / chemistry
  • Antimalarials / pharmacology*
  • Artemisinins / pharmacology
  • Atovaquone / pharmacology
  • Cells, Cultured
  • Chromatography, Liquid / methods
  • Cluster Analysis
  • Databases, Chemical
  • Dicarboxylic Acids / antagonists & inhibitors
  • Dicarboxylic Acids / metabolism
  • Drug Resistance / drug effects
  • Erythrocytes / drug effects
  • Erythrocytes / parasitology
  • Humans
  • Metabolic Networks and Pathways / drug effects*
  • Metabolomics / methods
  • Molecular Targeted Therapy / methods*
  • Plasmodium falciparum / drug effects*
  • Plasmodium falciparum / growth & development
  • Plasmodium falciparum / metabolism
  • Small Molecule Libraries / chemistry
  • Small Molecule Libraries / pharmacology*
  • Tandem Mass Spectrometry
  • Terpenes / antagonists & inhibitors
  • Terpenes / metabolism

Substances

  • Aminoquinolines
  • Antimalarials
  • Artemisinins
  • Dicarboxylic Acids
  • Small Molecule Libraries
  • Terpenes
  • artemisinin
  • traumatic acid
  • Atovaquone

Grants and funding

This work was funded by Australian National Health and Medical Research Council grants to Malcolm J. McConville and Stuart A. Ralph (APP106024), Darren J. Creek (APP1088855; APP), and Stuart A. Ralph (APP1062504).