Home LiteratureArticle Details
PMID: 10903134 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Vacuolar proton pyrophosphatase activity and pyrophosphate (PPi) in Toxoplasma gondii as possible chemotherapeutic targets.

The Biochemical journal ·Vol. 349 Pt 3 ·2000-08-01 ·Pages 737-45

Rodrigues CO, Scott DA, Bailey BN, De Souza W, Benchimol M, Moreno B, Urbina JA, Oldfield E, Moreno SN

Abstract

The addition of PP(i) promoted the acidification of a subcellular compartment in cell homogenates of Toxoplasma gondii tachyzoites, implying the presence of a proton-translocating pyrophosphatase. The proton gradient was collapsed by addition of the K(+)/H(+) antiporter nigericin, and was also inhibited by addition of the PP(i) analogue aminomethylenediphosphonate (AMDP). Both proton transport and PP(i) hydrolysis were dependent upon K(+), but Na(+) caused partial inhibition of these activities. PP(i) hydrolysis was sensitive in a dose-dependent manner to AMDP, imidodiphosphate, NaF and to the thiol reagent N-ethylmaleimide. This activity was unaffected by common inhibitors of phosphohydrolases, except that NaO(3)V (sodium orthovanadate) stimulated the activity by 87%. Immunofluorescence microscopy, using antisera raised against conserved peptide sequences of a plant vacuolar pyrophosphatase, suggested that the pyrophosphatase in T. gondii tachyzoites was located in the plasma membrane and intracellular vacuoles of the parasite. High-field (31)P-NMR spectroscopy showed that PP(i )was more abundant than ATP in tachyzoites. Bisphosphonates (PP(i) analogues), drugs that are used in the treatment of bone diseases, inhibited proton transport and PP(i) hydrolysis in tachyzoite homogenates, and also inhibited intracellular proliferation of tachyzoites in tissue culture cells.

MeSH Terms
Animals Antiprotozoal Agents/pharmacology Diphosphates/metabolism Enzyme Inhibitors/pharmacology Protons Pyrophosphatases/antagonists & inhibitors,metabolism Subcellular Fractions/metabolism Toxoplasma/drug effects,enzymology,metabolism Vacuoles/enzymology
Chemicals
Antiprotozoal Agents Diphosphates Enzyme Inhibitors Protons Pyrophosphatases
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Rodrigues C O
Laboratory of Molecular Parasitology, Department of Pathobiology, College of Veterinary Medicine, University of Illinois at Urbana-Champaign, 2001 South Lincoln Avenue, Urbana, IL 61802, USA.
Scott D A
Bailey B N
De Souza W
Benchimol M
Moreno B
Urbina J A
Oldfield E
Moreno S N
References (42)
42 references, click to expand
  1. Intracellular Ca2+ storage in acidocalcisomes of Trypanosoma cruzi.
    Biochem J. 1995 Sep 15;310 ( Pt 3):1005-12 PMID: 7575396
  2. Comparison of the phosphofructokinase and pyruvate kinase activities of Cryptosporidium parvum, Eimeria tenella and Toxoplasma gondii.
    Mol Biochem Parasitol. 1996 Feb-Mar;76(1-2):23-9 PMID: 8919992
  3. Comparative activity of macrolides against Toxoplasma gondii demonstrating utility of an in vitro microassay.
    Antimicrob Agents Chemother. 1991 May;35(5):903-9 PMID: 1854172
  4. NMR studies of metabolism.
    Annu Rev Biophys Biophys Chem. 1990;19:43-67 PMID: 2194483
  5. Pharmacokinetics of alendronate.
    Clin Pharmacokinet. 1999 May;36(5):315-28 PMID: 10384857
  6. The bisphosphonate tiludronate is a potent inhibitor of the osteoclast vacuolar H(+)-ATPase.
    J Bone Miner Res. 1996 Oct;11(10):1498-507 PMID: 8889850
  7. Characterization of a mitochondrial inorganic pyrophosphatase in Saccharomyces cerevisiae.
    Biochim Biophys Acta. 1992 Jan 16;1098(2):217-23 PMID: 1309654
  8. A pyrophosphate synthase gene: molecular cloning and sequencing of the cDNA encoding the inorganic pyrophosphate synthase from Rhodospirillum rubrum.
    Biochim Biophys Acta. 1998 May 27;1364(3):301-6 PMID: 9630689
  9. The vacuolar H+-ATPase: a universal proton pump of eukaryotes.
    Biochem J. 1997 Jun 15;324 ( Pt 3):697-712 PMID: 9210392
  10. Vacuolar-type H+-ATPase regulates cytoplasmic pH in Toxoplasma gondii tachyzoites.
    Biochem J. 1998 Mar 1;330 ( Pt 2):853-60 PMID: 9480901
  11. Accumulation of bisphosphonates in the aorta and some other tissues of healthy and atherosclerotic rabbits.
    J Lab Clin Med. 1996 Feb;127(2):200-6 PMID: 8636649
  12. Acidocalcisomes in Toxoplasma gondii tachyzoites.
    Biochem J. 1996 Jan 15;313 ( Pt 2):655-9 PMID: 8573106
  13. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.
    Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350-4 PMID: 388439
  14. Clodronate and liposome-encapsulated clodronate are metabolized to a toxic ATP analog, adenosine 5'-(beta, gamma-dichloromethylene) triphosphate, by mammalian cells in vitro.
    J Bone Miner Res. 1997 Sep;12(9):1358-67 PMID: 9286751
  15. Mechanisms of action of bisphosphonates.
    Annu Rev Pharmacol Toxicol. 1998;38:375-88 PMID: 9597160
  16. Electrogenic h-pumping pyrophosphatase in tonoplast vesicles of oat roots.
    Plant Physiol. 1986 Jun;81(2):497-502 PMID: 16664845
  17. Observation of tissue metabolites using 31P nuclear magnetic resonance.
    Nature. 1974 Nov 22;252(5481):285-7 PMID: 4431445
  18. Characterization of a vacuolar pyrophosphatase in Trypanosoma brucei and its localization to acidocalcisomes.
    Mol Cell Biol. 1999 Nov;19(11):7712-23 PMID: 10523660
  19. Farnesyl pyrophosphate synthase is the molecular target of nitrogen-containing bisphosphonates.
    Biochem Biophys Res Commun. 1999 Oct 14;264(1):108-11 PMID: 10527849
  20. Structural aspects of the effectiveness of bisphosphonates as competitive inhibitors of the plant vacuolar proton-pumping pyrophosphatase.
    Biochem J. 1999 Feb 1;337 ( Pt 3):373-7 PMID: 9895279
  21. Ca2+ content and expression of an acidocalcisomal calcium pump are elevated in intracellular forms of Trypanosoma cruzi.
    Mol Cell Biol. 1998 Apr;18(4):2309-23 PMID: 9528801
  22. Bisphosphonates promote apoptosis in murine osteoclasts in vitro and in vivo.
    J Bone Miner Res. 1995 Oct;10(10):1478-87 PMID: 8686503
  23. Aminomethylenediphosphonate: A Potent Type-Specific Inhibitor of Both Plant and Phototrophic Bacterial H+-Pyrophosphatases.
    Plant Physiol. 1994 Jan;104(1):153-159 PMID: 12232069
  24. Acidocalcisomes and a vacuolar H+-pyrophosphatase in malaria parasites.
    Biochem J. 2000 Apr 1;347 Pt 1:243-53 PMID: 10727425
  25. Lysosomes of Toxoplasma gondii and their possible relation to the host-cell penetration of toxoplasma parasites.
    J Bacteriol. 1968 Oct;96(4):916-9 PMID: 4176646
  26. Inorganic pyrophosphate in mitochondrial metabolism.
    Biochim Biophys Acta. 1989 Dec 7;977(3):237-47 PMID: 2556179
  27. Alendronate is a specific, nanomolar inhibitor of farnesyl diphosphate synthase.
    Arch Biochem Biophys. 2000 Jan 1;373(1):231-41 PMID: 10620343
  28. Intracellular Ca2+ pool content and signaling and expression of a calcium pump are linked to virulence in Leishmania mexicana amazonesis amastigotes.
    J Biol Chem. 1997 Apr 4;272(14):9464-73 PMID: 9083086
  29. Some phosphonic acid analogs as inhibitors of pyrophosphate-dependent phosphofructokinase, a novel target in Toxoplasma gondii.
    Biochem Pharmacol. 1995 Jan 6;49(1):105-13 PMID: 7840776
  30. A plant-like vacuolar H(+)-pyrophosphatase in Plasmodium falciparum.
    FEBS Lett. 1999 Oct 29;460(2):217-20 PMID: 10544238
  31. Protein prenyl transferase activities of Plasmodium falciparum.
    Mol Biochem Parasitol. 1998 Aug 1;94(2):175-84 PMID: 9747968
  32. Ca2+/H+ exchange in acidic vacuoles of Trypanosoma brucei.
    Biochem J. 1994 Nov 15;304 ( Pt 1):227-33 PMID: 7998937
  33. Acidic calcium pools in intraerythrocytic malaria parasites.
    Eur J Cell Biol. 1998 Jun;76(2):133-8 PMID: 9696353
  34. Acidic compartments and rhoptry formation in Toxoplasma gondii.
    Parasitology. 1998 Nov;117 ( Pt 5):435-43 PMID: 9836308
  35. Presence of a vacuolar H+-pyrophosphatase in promastigotes of Leishmania donovani and its localization to a different compartment from the vacuolar H+-ATPase.
    Biochem J. 1999 Jun 15;340 ( Pt 3):759-66 PMID: 10359662
  36. Alendronate mechanism of action: geranylgeraniol, an intermediate in the mevalonate pathway, prevents inhibition of osteoclast formation, bone resorption, and kinase activation in vitro.
    Proc Natl Acad Sci U S A. 1999 Jan 5;96(1):133-8 PMID: 9874784
  37. Nitrogen-containing bisphosphonates as carbocation transition state analogs for isoprenoid biosynthesis.
    Biochem Biophys Res Commun. 1999 Oct 5;263(3):754-8 PMID: 10512752
  38. Pharmacokinetics of pamidronate disodium in patients with cancer with normal or impaired renal function.
    J Clin Pharmacol. 1997 Apr;37(4):285-90 PMID: 9115053
  39. Trypanosoma cruzi contains major pyrophosphate stores, and its growth in vitro and in vivo is blocked by pyrophosphate analogs.
    J Biol Chem. 1999 Nov 19;274(47):33609-15 PMID: 10559249
  40. Molecular cloning and sequence of cDNA encoding the pyrophosphate-energized vacuolar membrane proton pump of Arabidopsis thaliana.
    Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1775-9 PMID: 1311852
  41. Purification and properties of a pyrophosphate-dependent phosphofructokinase from Toxoplasma gondii.
    Mol Biochem Parasitol. 1992 Sep;54(2):223-30 PMID: 1331784
  42. Presence of a plant-like proton-pumping pyrophosphatase in acidocalcisomes of Trypanosoma cruzi.
    J Biol Chem. 1998 Aug 21;273(34):22151-8 PMID: 9705361
Article Info
Journal
The Biochemical journal
Abbr.
Biochem J
ISSN
0264-6021
Published
2000-08-01
Pages
737-45
Language
English
Region
England
NLM ID
2984726R
PMCID
PMC1221200
Subset
IM
Grants
NIAID NIH HHS · AI43614 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]