Lipophilic analogs of zoledronate and risedronate inhibit Plasmodium geranylgeranyl diphosphate synthase (GGPPS) and exhibit potent antimalarial activity

Proc Natl Acad Sci U S A. 2012 Mar 13;109(11):4058-63. doi: 10.1073/pnas.1118215109. Epub 2012 Mar 5.

Abstract

We report the results of an in vitro screening assay targeting the intraerythrocytic form of the malaria parasite Plasmodium falciparum using a library of 560 prenyl-synthase inhibitors. Based on "growth-rescue" and enzyme-inhibition experiments, geranylgeranyl diphosphate synthase (GGPPS) is shown to be a major target for the most potent leads, BPH-703 and BPH-811, lipophilic analogs of the bone-resorption drugs zoledronate and risedronate. We determined the crystal structures of these inhibitors bound to a Plasmodium GGPPS finding that their head groups bind to the [Mg(2+)](3) cluster in the active site in a similar manner to that found with their more hydrophilic parents, whereas their hydrophobic tails occupy a long-hydrophobic tunnel spanning both molecules in the dimer. The results of isothermal-titration-calorimetric experiments show that both lipophilic bisphosphonates bind to GGPPS with, on average, a ΔG of -9 kcal mol(-1), only 0.5 kcal mol(-1) worse than the parent bisphosphonates, consistent with the observation that conversion to the lipophilic species has only a minor effect on enzyme activity. However, only the lipophilic species are active in cells. We also tested both compounds in mice, finding major decreases in parasitemia and 100% survival. These results are of broad general interest because they indicate that it may be possible to overcome barriers to cell penetration of existing bisphosphonate drugs in this and other systems by simple covalent modification to form lipophilic analogs that retain their enzyme-inhibition activity and are also effective in vitro and in vivo.

Publication types

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

MeSH terms

  • Animals
  • Antimalarials / chemistry
  • Antimalarials / pharmacology*
  • Antimalarials / therapeutic use
  • Calorimetry
  • Crystallography, X-Ray
  • Diphosphonates / chemistry
  • Diphosphonates / pharmacology*
  • Diphosphonates / therapeutic use
  • Enzyme Inhibitors / chemistry
  • Enzyme Inhibitors / pharmacology
  • Erythrocytes / drug effects
  • Erythrocytes / parasitology
  • Etidronic Acid / analogs & derivatives*
  • Etidronic Acid / chemistry
  • Etidronic Acid / pharmacology
  • Etidronic Acid / therapeutic use
  • Farnesyltranstransferase / antagonists & inhibitors*
  • Farnesyltranstransferase / chemistry
  • Farnesyltranstransferase / metabolism
  • High-Throughput Screening Assays
  • Humans
  • Imidazoles / chemistry
  • Imidazoles / pharmacology*
  • Imidazoles / therapeutic use
  • Lipids / chemistry*
  • Mice
  • Models, Molecular
  • Parasitemia / drug therapy
  • Parasitemia / parasitology
  • Plasmodium / drug effects*
  • Plasmodium / enzymology*
  • Plasmodium falciparum / drug effects
  • Plasmodium falciparum / enzymology
  • Plasmodium vivax / drug effects
  • Plasmodium vivax / enzymology
  • Protein Binding / drug effects
  • Risedronic Acid
  • Survival Analysis
  • Terpenes / chemistry
  • Terpenes / metabolism
  • Zoledronic Acid

Substances

  • Antimalarials
  • Diphosphonates
  • Enzyme Inhibitors
  • Imidazoles
  • Lipids
  • Terpenes
  • Zoledronic Acid
  • Farnesyltranstransferase
  • Risedronic Acid
  • Etidronic Acid