Identification via a Parallel Hit Progression Strategy of Improved Small Molecule Inhibitors of the Malaria Purine Uptake Transporter that Inhibit Plasmodium falciparum Parasite Proliferation

ACS Infect Dis. 2019 Oct 11;5(10):1738-1753. doi: 10.1021/acsinfecdis.9b00168. Epub 2019 Aug 14.

Abstract

Emerging resistance to current antimalarial medicines underscores the importance of identifying new drug targets and novel compounds. Malaria parasites are purine auxotrophic and import purines via the Plasmodium falciparum equilibrative nucleoside transporter type 1 (PfENT1). We previously showed that PfENT1 inhibitors block parasite proliferation in culture. Our goal was to identify additional, possibly more optimal chemical starting points for a drug discovery campaign. We performed a high throughput screen (HTS) of GlaxoSmithKline's 1.8 million compound library with a yeast-based assay to identify PfENT1 inhibitors. We used a parallel progression strategy for hit validation and expansion, with an emphasis on chemical properties in addition to potency. In one arm, the most active hits were tested for human cell toxicity; 201 had minimal toxicity. The second arm, hit expansion, used a scaffold-based substructure search with the HTS hits as templates to identify over 2000 compounds; 123 compounds had activity. Of these 324 compounds, 175 compounds inhibited proliferation of P. falciparum parasite strain 3D7 with IC50 values between 0.8 and ∼180 μM. One hundred forty-two compounds inhibited PfENT1 knockout (pfent1Δ) parasite growth, indicating they also hit secondary targets. Thirty-two hits inhibited growth of 3D7 but not pfent1Δ parasites. Thus, PfENT1 inhibition was sufficient to block parasite proliferation. Therefore, PfENT1 may be a viable target for antimalarial drug development. Six compounds with novel chemical scaffolds were extensively characterized in yeast-, parasite-, and human-erythrocyte-based assays. The inhibitors showed similar potencies against drug sensitive and resistant P. falciparum strains. They represent attractive starting points for development of novel antimalarial drugs.

Keywords: drug discovery; high throughput screen; malaria; purine; transporter.

Publication types

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

MeSH terms

  • Antimalarials / chemistry
  • Antimalarials / pharmacology*
  • Biological Transport / drug effects*
  • Cell Proliferation / drug effects*
  • Drug Discovery*
  • Erythrocytes / drug effects
  • Gene Knockout Techniques
  • Hep G2 Cells / drug effects
  • High-Throughput Screening Assays
  • Humans
  • Malaria / parasitology
  • Malaria, Falciparum / parasitology
  • Nucleobase, Nucleoside, Nucleotide, and Nucleic Acid Transport Proteins / drug effects
  • Nucleobase, Nucleoside, Nucleotide, and Nucleic Acid Transport Proteins / genetics
  • Plasmodium falciparum / drug effects*
  • Plasmodium falciparum / genetics
  • Plasmodium falciparum / growth & development
  • Plasmodium falciparum / metabolism
  • Protozoan Proteins / drug effects
  • Protozoan Proteins / genetics
  • Purines / metabolism*
  • Transcriptome
  • Yeasts / drug effects

Substances

  • Antimalarials
  • ENT1 protein, Plasmodium falciparum
  • Nucleobase, Nucleoside, Nucleotide, and Nucleic Acid Transport Proteins
  • Protozoan Proteins
  • Purines
  • purine