Thiostrepton and derivatives exhibit antimalarial and gametocytocidal activity by dually targeting parasite proteasome and apicoplast

Antimicrob Agents Chemother. 2011 Apr;55(4):1338-48. doi: 10.1128/AAC.01096-10. Epub 2011 Jan 18.

Abstract

Ribosome-targeting antibiotics exert their antimalarial activity on the apicoplast of the malaria parasite, an organelle of prokaryote origin having essential metabolic functions. These antibiotics typically cause a delayed-death phenotype, which manifests in parasite killing during the second replication cycle following administration. As an exception, treatment with the antibiotic thiostrepton results in an immediate killing. We recently demonstrated that thiostrepton and its derivatives interfere with the eukaryotic proteasome, a multimeric protease complex that is important for the degradation of ubiquitinated proteins. Here, we report that the thiostrepton-based compounds are active against chloroquine-sensitive and -resistant Plasmodium falciparum, where they rapidly eliminate parasites before DNA replication. The minor parasite fraction that escapes the fast killing of the first replication cycle is arrested in the schizont stage of the following cycle, displaying a delayed-death phenotype. Thiostrepton further exhibits gametocytocidal activity by eliminating gametocytes, the sexual precursor cells that are crucial for parasite transmission to the mosquito. Compound treatment results in an accumulation of ubiquitinated proteins in the blood stages, indicating an effect on the parasite proteasome. In accordance with these findings, expression profiling revealed that the proteasome is present in the nucleus and cytoplasm of trophozoites, schizonts, and gametocytes. In conclusion, thiostrepton derivatives represent promising candidates for malaria therapy by dually acting on two independent targets, the parasite proteasome and the apicoplast, with the capacity to eliminate both intraerythrocytic asexual and transmission stages of the parasite.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antimalarials / pharmacology*
  • Blotting, Western
  • Chloroquine / pharmacology
  • Drug Resistance
  • Fluorescent Antibody Technique, Indirect
  • HeLa Cells
  • Humans
  • Microscopy, Immunoelectron
  • Plasmodium falciparum / drug effects*
  • Plasmodium falciparum / metabolism*
  • Plasmodium falciparum / pathogenicity
  • Proteasome Endopeptidase Complex / drug effects*
  • Proteasome Endopeptidase Complex / metabolism
  • Schizonts / drug effects
  • Schizonts / metabolism
  • Thiostrepton / pharmacology*
  • Trophozoites / drug effects
  • Trophozoites / metabolism

Substances

  • Antimalarials
  • Chloroquine
  • Proteasome Endopeptidase Complex
  • Thiostrepton