Trypanosoma brucei CYP51: Essentiality and Targeting Therapy in an Experimental Model

PLoS Negl Trop Dis. 2016 Nov 17;10(11):e0005125. doi: 10.1371/journal.pntd.0005125. eCollection 2016 Nov.

Abstract

Trypanosoma brucei gambiense is the main causative agent of Human African Trypanosomiasis (HAT), also known as sleeping sickness. Because of limited alternatives and treatment toxicities, new therapeutic options are urgently needed for patients with HAT. Sterol 14alpha-demethylase (CYP51) is a potential drug target but its essentiality has not been determined in T. brucei. We used a tetracycline-inducible RNAi system to assess the essentiality of CYP51 in T. brucei bloodstream form (BSF) cells and we evaluated the effect of posaconazole, a well-tolerated triazole drug, within a panel of virulent strains in vitro and in a murine model. Expression of CYP51 in several T. brucei cell lines was demonstrated by western blot and its essentiality was demonstrated by RNA interference (CYP51RNAi) in vitro. Following reduction of TbCYP51 expression by RNAi, cell growth was reduced and eventually stopped compared to WT or non-induced cells, showing the requirement of CYP51 in T. brucei. These phenotypes were rescued by addition of ergosterol. Additionally, CYP51RNAi induction caused morphological defects with multiflagellated cells (p<0.05), suggesting cytokinesis dysfunction. The survival of CYP51RNAi Doxycycline-treated mice (p = 0.053) and of CYP51RNAi 5-day pre-induced Doxycycline-treated mice (p = 0.008) were improved compared to WT showing a CYP51 RNAi effect on trypanosomal virulence in mice. The posaconazole concentrations that inhibited parasite growth by 50% (IC50) were 8.5, 2.7, 1.6 and 0.12 μM for T. b. brucei 427 90-13, T. b. brucei Antat 1.1, T. b. gambiense Feo (Feo/ITMAP/1893) and T. b. gambiense Biyamina (MHOM/SD/82), respectively. During infection with these last three virulent strains, posaconazole-eflornithine and nifurtimox-eflornithine combinations showed similar improvement in mice survival (p≤0.001). Our results provide support for a CYP51 targeting based treatment in HAT. Thus posaconazole used in combination may represent a therapeutic alternative for trypanosomiasis.

MeSH terms

  • 14-alpha Demethylase Inhibitors / pharmacology*
  • Animals
  • Anti-Bacterial Agents / therapeutic use
  • Cytokinesis
  • Disease Models, Animal
  • Doxycycline / therapeutic use
  • Eflornithine / therapeutic use
  • Ergosterol / pharmacology
  • Humans
  • Mice
  • Nifurtimox / therapeutic use*
  • Phenotype
  • RNA Interference
  • Sterol 14-Demethylase / genetics
  • Sterol 14-Demethylase / metabolism*
  • Triazoles / pharmacology
  • Triazoles / therapeutic use
  • Trypanocidal Agents / therapeutic use*
  • Trypanosoma brucei brucei / drug effects*
  • Trypanosoma brucei brucei / enzymology*
  • Trypanosoma brucei brucei / growth & development
  • Trypanosoma brucei brucei / pathogenicity
  • Trypanosomiasis, African / drug therapy*
  • Trypanosomiasis, African / parasitology

Substances

  • 14-alpha Demethylase Inhibitors
  • Anti-Bacterial Agents
  • Triazoles
  • Trypanocidal Agents
  • posaconazole
  • Sterol 14-Demethylase
  • Nifurtimox
  • Doxycycline
  • Ergosterol
  • Eflornithine

Grants and funding

This research was supported by internal funding and support from the ANR, LABEX ParaFrap, ANR-11-LABX-0024 and from the Association pour le développement de la recherche en parasitologie et médecine tropicale. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.