Naphthoquinone derivatives exert their antitrypanosomal activity via a multi-target mechanism

PLoS Negl Trop Dis. 2013;7(1):e2012. doi: 10.1371/journal.pntd.0002012. Epub 2013 Jan 17.

Abstract

Background and methodology: Recently, we reported on a new class of naphthoquinone derivatives showing a promising anti-trypanosomatid profile in cell-based experiments. The lead of this series (B6, 2-phenoxy-1,4-naphthoquinone) showed an ED(50) of 80 nM against Trypanosoma brucei rhodesiense, and a selectivity index of 74 with respect to mammalian cells. A multitarget profile for this compound is easily conceivable, because quinones, as natural products, serve plants as potent defense chemicals with an intrinsic multifunctional mechanism of action. To disclose such a multitarget profile of B6, we exploited a chemical proteomics approach.

Principal findings: A functionalized congener of B6 was immobilized on a solid matrix and used to isolate target proteins from Trypanosoma brucei lysates. Mass analysis delivered two enzymes, i.e. glycosomal glycerol kinase and glycosomal glyceraldehyde-3-phosphate dehydrogenase, as potential molecular targets for B6. Both enzymes were recombinantly expressed and purified, and used for chemical validation. Indeed, B6 was able to inhibit both enzymes with IC(50) values in the micromolar range. The multifunctional profile was further characterized in experiments using permeabilized Trypanosoma brucei cells and mitochondrial cell fractions. It turned out that B6 was also able to generate oxygen radicals, a mechanism that may additionally contribute to its observed potent trypanocidal activity.

Conclusions and significance: Overall, B6 showed a multitarget mechanism of action, which provides a molecular explanation of its promising anti-trypanosomatid activity. Furthermore, the forward chemical genetics approach here applied may be viable in the molecular characterization of novel multitarget ligands.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antiprotozoal Agents / pharmacology*
  • Enzyme Inhibitors / pharmacology
  • Glyceraldehyde-3-Phosphate Dehydrogenases / antagonists & inhibitors
  • Glyceraldehyde-3-Phosphate Dehydrogenases / isolation & purification
  • Glycerol Kinase / antagonists & inhibitors
  • Glycerol Kinase / isolation & purification
  • Inhibitory Concentration 50
  • Mass Spectrometry
  • Naphthoquinones / pharmacology*
  • Proteome / analysis
  • Protozoan Proteins / analysis
  • Reactive Oxygen Species / metabolism
  • Reactive Oxygen Species / toxicity
  • Trypanosoma brucei rhodesiense / chemistry
  • Trypanosoma brucei rhodesiense / drug effects*

Substances

  • Antiprotozoal Agents
  • Enzyme Inhibitors
  • Naphthoquinones
  • Proteome
  • Protozoan Proteins
  • Reactive Oxygen Species
  • Glyceraldehyde-3-Phosphate Dehydrogenases
  • Glycerol Kinase

Grants and funding

The following sources have provided funding for this work: the University of Bologna, the University of Geneva, and in part the Swiss National Science Foundation grant no. 3100A0-120566/1. JRH and BMB were supported by an NWO Vernieuwingsimpuls grant to BMB and by SysMO project SilicoTryp. BMB has a Rosalind Franklin Fellowship from the University of Groningen, The Netherlands. SP thanks the COST Action CM-0801 “New Drugs for Neglected Diseases” of the EC for a grant that enabled him to work for three months in the ‘de Duve Institute’ in Brussels. MM acknowledges a postdoctoral fellowship from the F.R.S.-FNRS (Belgium). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.