A potent and selective reaction hijacking inhibitor of Plasmodium falciparum tyrosine tRNA synthetase exhibits single dose oral efficacy in vivo

PLoS Pathog. 2024 Dec 9;20(12):e1012429. doi: 10.1371/journal.ppat.1012429. eCollection 2024 Dec.

Abstract

The Plasmodium falciparum cytoplasmic tyrosine tRNA synthetase (PfTyrRS) is an attractive drug target that is susceptible to reaction-hijacking by AMP-mimicking nucleoside sulfamates. We previously identified an exemplar pyrazolopyrimidine ribose sulfamate, ML901, as a potent reaction hijacking inhibitor of PfTyrRS. Here we examined the stage specificity of action of ML901, showing very good activity against the schizont stage, but lower trophozoite stage activity. We explored a series of ML901 analogues and identified ML471, which exhibits improved potency against trophozoites and enhanced selectivity against a human cell line. Additionally, it has no inhibitory activity against human ubiquitin-activating enzyme (UAE) in vitro. ML471 exhibits low nanomolar activity against asexual blood stage P. falciparum and potent activity against liver stage parasites, gametocytes and transmissible gametes. It is fast-acting and exhibits a long in vivo half-life. ML471 is well-tolerated and shows single dose oral efficacy in the SCID mouse model of P. falciparum malaria. We confirm that ML471 is a reaction hijacking inhibitor that is converted into a tight binding Tyr-ML471 conjugate by the PfTyrRS enzyme. A crystal structure of the PfTyrRS/ Tyr-ML471 complex offers insights into improved potency, while molecular docking into UAE provides a rationale for improved selectivity.

MeSH terms

  • Administration, Oral
  • Animals
  • Antimalarials* / pharmacology
  • Enzyme Inhibitors / pharmacology
  • Humans
  • Malaria, Falciparum* / drug therapy
  • Malaria, Falciparum* / parasitology
  • Mice
  • Mice, SCID*
  • Plasmodium falciparum* / drug effects
  • Plasmodium falciparum* / enzymology
  • Protozoan Proteins / antagonists & inhibitors
  • Protozoan Proteins / metabolism
  • Pyrimidines / pharmacology
  • Tyrosine-tRNA Ligase* / antagonists & inhibitors
  • Tyrosine-tRNA Ligase* / metabolism

Substances

  • Antimalarials
  • Tyrosine-tRNA Ligase
  • Protozoan Proteins
  • Enzyme Inhibitors
  • Pyrimidines

Grants and funding

Funding was provided by the Global Health Innovative Technology Fund, Japan (H2019-104 to LT, LRD, SL, AEG), the Australian National Health and Medical Research Council (APP2022075 to LT), the Australian Research Council (DE230101173 to SCX), the Medicines for Malaria Venture (RD-19-001 to LMB; RD-08-0015 to DAF; RD-21-1003 to MJD), the Foundation for Research Support of the State of São Paulo (FAPESP; 2019/19708-0 and 2013/07600-3 to RVCG and ACCA), the South African Medical Research Council and the Department of Science and Innovation South African Research Chairs Initiative Grant managed by the National Research Foundation (UID 84627 to LMB), a Medical Research Council Career Development Award (MR/V010034/1 to MJD), the Bill & Melinda Gates Foundation (INV-033538 to DAF), and Millennium Pharmaceuticals, a wholly owned subsidiary of Takeda Pharmaceuticals Company Limited (LRD, SL, AEG). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.