Sulfonylpiperazine compounds prevent Plasmodium falciparum invasion of red blood cells through interference with actin-1/profilin dynamics

PLoS Biol. 2023 Apr 13;21(4):e3002066. doi: 10.1371/journal.pbio.3002066. eCollection 2023 Apr.

Abstract

With emerging resistance to frontline treatments, it is vital that new antimalarial drugs are identified to target Plasmodium falciparum. We have recently described a compound, MMV020291, as a specific inhibitor of red blood cell (RBC) invasion, and have generated analogues with improved potency. Here, we generated resistance to MMV020291 and performed whole genome sequencing of 3 MMV020291-resistant populations. This revealed 3 nonsynonymous single nucleotide polymorphisms in 2 genes; 2 in profilin (N154Y, K124N) and a third one in actin-1 (M356L). Using CRISPR-Cas9, we engineered these mutations into wild-type parasites, which rendered them resistant to MMV020291. We demonstrate that MMV020291 reduces actin polymerisation that is required by the merozoite stage parasites to invade RBCs. Additionally, the series inhibits the actin-1-dependent process of apicoplast segregation, leading to a delayed death phenotype. In vitro cosedimentation experiments using recombinant P. falciparum proteins indicate that potent MMV020291 analogues disrupt the formation of filamentous actin in the presence of profilin. Altogether, this study identifies the first compound series interfering with the actin-1/profilin interaction in P. falciparum and paves the way for future antimalarial development against the highly dynamic process of actin polymerisation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / genetics
  • Actins / metabolism
  • Antimalarials* / pharmacology
  • Erythrocytes / parasitology
  • Humans
  • Malaria, Falciparum* / drug therapy
  • Malaria, Falciparum* / genetics
  • Malaria, Falciparum* / prevention & control
  • Plasmodium falciparum / metabolism
  • Profilins / genetics
  • Profilins / metabolism
  • Protozoan Proteins / genetics
  • Protozoan Proteins / metabolism

Substances

  • Actins
  • Profilins
  • Protozoan Proteins
  • Antimalarials

Grants and funding

This work was supported by the National Health and Medical Research Council (2001073 to P.R.G and W.N) and (119780521 to B.S.C), the Victoria Operational Infrastructure Support Programs received by the Burnet Institute and Walter and Eliza Hall Institute, the Academy of Finland (322917 to I.K and H.P), the Sigrid Jusélius Foundation (to I.K.) and the Hospital Research Foundation (to D.W.W). This work was also funded by an Australian Government Research Training Program Scholarship (to M.G.D), a University of Melbourne Research Scholarship (to T.K.J), an Ellen Corin Fellow (to B.E.S) and an National Health and Medical Research Council Senior Research Fellowship (1136300 to TdK-W). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.