Potent antihematozoan activity of novel bisthiazolium drug T16: Evidence for inhibition of phosphatidylcholine metabolism in erythrocytes infected with Babesia and Plasmodium spp.

Antimicrobial Agents and Chemotherapy

Volumn 50, Issue 10, 2006, Pages 3381-3388

  Richier, Eric ^a   Biagini, Giancarlo A ^b   Wein, Sharon ^a   Boudou, Frederic ^a   Bray, Patrick G ^b   Ward, Steve A ^b   Precigout, Eric ^c   Calas, Michèle ^a   Dubremetz, Jean François ^a   Vial, Henri J ^a  

^a CNRS   (France)

^b LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^c UNIV MONTPELLIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

1,12 DODECANEMETHYLENE BIS(4 METHYL 5 ETHYLTHIAZOLIUM)IODIDE; ANTIPROTOZOAL AGENT; CHLOROQUINE; CHOLINE; HEMATIN; HEME; HEMOGLOBIN; IMIDOCARB; PENTAMIDINE; PHOSPHATIDYLCHOLINE; T 16; THIAZOLE DERIVATIVE; UNCLASSIFIED DRUG;

ANTIPROTOZOAL ACTIVITY; ARTICLE; BABESIA; BABESIA CANIS; BABESIA DIVERGENS; BIOACCUMULATION; CELL FRACTIONATION; CONTROLLED STUDY; DRUG POTENCY; DRUG TARGETING; ERYTHROCYTE; HUMAN; HUMAN CELL; IC 50; MALARIA; METABOLIC INHIBITION; NONHUMAN; PARASITE ISOLATION; PHOSPHOLIPID SYNTHESIS; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL;

ANIMALS; ANTIMALARIALS; ANTIPROTOZOAL AGENTS; BABESIA; BABESIOSIS; ERYTHROCYTES; HEMOLYSIS; HUMANS; MALARIA, FALCIPARUM; PHOSPHATIDYLCHOLINES; PLASMODIUM FALCIPARUM; THIAZOLES;

EID: 33749517035     PISSN: 00664804     EISSN: None     Source Type: Journal    
DOI: 10.1128/AAC.00443-06     Document Type: Article

References (48)

1. Ancelin, M. L., M. Calas, J. Bompart, G. Cordina, D. Martin, M. Ben Bari, T. Jei, P. Druilhe, and H. Vial. 1998. Antimalarial activity of 77 phospholipid head analogs: close correlation between inhibition of phospholipid metabolism and in vitro Plasmodium falciparum growth. Blood 91:1426-1437.
2. Ancelin, M. L., M. Calas, A. Bonhoure, S. Herbute, and H. Vial. 2003. In vivo antimalarial activities of mono- and bisquaternary ammonium salts interfering with Plasmodium phospholipid metabolism. Antimicrob. Agents Chemother. 47:2598-2605.
3. Ancelin, M. L., M. Calas, V. Vidal-Sailhan, S. Herbute, P. Ringwald, and H. Vial. 2003. Potent inhibitors of Plasmodium falciparum metabolism with a broad spectrum of in-vitro antimalarial activities. Antimicrob. Agents Chemother. 47:2590-2597.
4. Ancelin, M. L., M. Parant, M. J. Thuet, J. Philippot, and H. Vial. 1991. Increased permeability to choline in simian erythrocytes after Plasmodium knowlesi infection. Biochem. J. 273:701-709.
5. Ancelin, M. L., F. Vialettes, and H. Vial. 1991. An original method for rapid serial determination of phospholipid biosynthesis. Applications to mammalian lymphocytic cells and a lower eucaryote, Plasmodium falciparum. Anal. Biochem. 199:203-209.
6. Ansorge, I., J. Benting, S. Bhakdi, and K. Lingelbach. 1996. Protein sorting in Plasmodium falciparum-infected red blood cells permeabilized with the pore-forming protein streptolysin O. Biochem. J. 315:307-314.
7. Biagini, G., E. Richier, P. G. Bray, M. Calas, H. Vial, and S. Ward. 2003. Heme binding contributes to antimalarial activity of bis-quaternary ammoniums. Antimicrob. Agents Chemother. 47:2584-2589.
8. Biagini, G. A., E. M. Pasini, R. Hughes, H. P. De Koning, H. J. Vial, P. M. O'Neill, S. A. Ward, and P. G. Bray. 2004. Characterization of the choline carrier of Plasmodium falciparum: a route for the selective delivery of novel antimalarial drugs. Blood 105:3372-3377.
9. Biagini, G. A., S. A. Ward, and P. G. Bray. 2005. Malaria parasite transporters as a drug-delivery strategy. Trends Parasitol. 21:299-301.
10. Bray, P. G., O. Janneh, K. J. Raynes, M. Mungthin, H. Ginsburg, and S. Ward. 1999. Cellular uptake of chloroquine in dependant on binding to FPIX and is independent of NHE activity in Plasmodium falciparum. J. Cell Biol. 145:363-376.
11. Calas, M., M. L. Ancelin, G. Cordina, P. Portefaix, G. Piquet, V. Vidal-Sailhan, and H. Vial. 2000. Antimalarial activity of compounds interfering with Plasmodium falciparum phospholipid metabolism: comparison between mono- and bisquaternary ammonium salts. J. Med. Chem. 43:505-516.
12. Calas, M., G. Cordina, J. Bompart, M. Bari, T. Jei, M. L. Ancelin, and H. Vial. 1997. Antimalarial activity of molecules interfering with Plasmodium falciparum phospholipid metabolism. Structure-activity relationship analysis. J. Med. Chem. 40:3557-3566.
13. Desjardins, R. E., C. J. Canfield, J. D. Haynes, and J. D. Chulay. 1979. Quantitative assessment of antimalarial activity in vitro by a semiautomated microdilution technique. Antimicrob. Agents Chemother. 16:710-718.
14. Fast, N., L. Xue, S. Bingham, and P. Keeling. 2002. Re-examining alveolate evolution using multiple protein molecular phylogenies. J. Eukaryot. Microbiol. 49:30-37.
15. Fischer, A., and I. Hanin. 1980. Choline analogs as potential tools in developing selective animal models of central cholinergic hypofunction. Life Sci. 27:1615-1634.
16. Florin-Christensen, J., C. E. Suarez, M. Florin-Christensen, S. A. Hines, T. F. Mcelwain, and G. H. Palmer. 2000. Phosphatidylcholine formation is the predominant lipid biosynthetic event in the hemoparasites Babesia bovis. Mol. Biochem. Parasitol. 106:147-156.
17. Florin-Christensen, J., C. E. Suarez, M. Florin-Christensen, M. Wainszelbaum, W. C. Brown, T. F. Mcelwain, and G. H. Palmer. 2001. A unique phospholipid organization in bovine erythrocyte membranes. Proc. Natl. Acad. Sci. USA 98:7736-7741.
18. Gorenflot, A., P. Brasseur, E. Precigout, M. L'Hostis, A. Marchand, and J. Schrevel. 1991. Cytological and immunological responses to Babesia divergens in different hosts: ox, gerbils, man. Parasitol. Res. 77:3-12.
19. Gorenflot, A., K. Moubri, E. Precigout, B. Carcy, and P. Schetters. 1998. Human babesiosis. Ann. Trop. Med. Parasitol. 92:489-501.
20. Gray, J., L. V. Von Stedingk, and M. Grandstom. 2002. Zoonotic babesiosis. Int. J. Med. Microbiol. 291:108-111.
21. Gumila, C., M. L. Ancelin, G. Jeminet, A. M. Delort, G. Miquel, and H. Vial. 1996. Differentiel in-vitro activities of ionophore compounds against Plasmodium falciparum and mammalian cells. Antimicrob. Agents Chemother. 40:602-608.
22. Hamze, A., E. Rubi, P. Arnal, M. Boisbrun, C. Carcel, X. Salom-Roig, M. Maynadier, S. Wein, H. Vial, and M. Calas. 2005. Mono- and bis-thiazolium salts have potent antimalarial activity. J. Med. Chem. 48:3639-3643.
23. Healy, G. R., and T. K. Ruebusch. 1980. Morphology of Babesia microti in human blood smears. Am. J. Clin. Pathol. 73:107-109.
24. Homer, J. M., I. Aguilar-Delfin, S. R. Telford III, P. J. Krause, and D. H. Persing. 2000. Babesiosis. Clin. Microbiol. Rev. 13:451-469.
25. Jensen, J., and W. Trager. 1977. Plasmodium falciparum in culture: use of outdated erythrocytes and description of the candle jar method. J. Parsitol. 63:883-886.
26. Kjemtrup, A. M., and P. A. Conrad. 2000. Human babesiosis: an emerging tick-borne disease. Int. J. Parasitol. 30:1323-1337.
27. Krause, P. J. 2003. Babesiosis diagnosis and treatment. Vector Borne Zoonotic Dis. 3:45-51.
28. Lehane, A. M., K. J. Saliba, R. J. Allen, and K. Kirk. 2004. Choline uptake into the malaria parasite is energized by the membrane potential. Biochem. Biophys. Res. Commun. 320:311-317.
29. Morrissette, N. S., and D. Sibley. 2002. Cytoskeleton of apicomplexan parasites. Microbiol. Mol. Biol. Rev. 66:21-38.
30. Olliaro, P., and D. E. Goldberg. 1995. The Plasmodium digestive vacuole: metabolic headquarters and choice drug target. Parasitol. Today 11:294-297.
31. Rudzinska, M. A. 1976. Ultrastructure of intraerythrocytic Babesia microti with emphasis on the feeding mechanism. J. Protozool. 23:224-233.
32. Rudzinska, M. A., W. Trager, S. Lewengrub, and E. Gubert. 1976. An electron microscopic study of Babesia microti invading erythrocytes. Cell Tissue Res. 169:323-334.
33. Saliba, K. J., H. A. Horner, and K. Kirk. 1998. Transport and metabolism of the essential vitamin pantothenic acid in human erythrocytes infected with the malaria parasite Plasmodium falciparum. J. Biol. Chem. 273:10190-10195.
34. Salom-Roig, X. J., A. Hamze, M. Calas, and H. J. Vial. 2005. Dual molecules as new antimalarials. Comb. Chem. High Throughput Screen. 8:49-62.
35. Slater, A. F., and A. Cerami. 1992. Inhibition by chloroquine of a novel haem polymerase enzyme activity in malaria trophozoites. Nature 355:167-169.
36. Slomianny, C., P. Charet, and G. Prensier. 1983. Ultrastructural localization of enzymes involved in the feeding process in Plasmodium chabaudi and Babesia hylomysci. J. Protozool. 30:376-382.
37. Sullivan, D. J., I. Y. Gluzman, D. G. Russell, and D. E. Goldberg. 1996. On the molecular mechanism of chloroquine's antimalarial action. Proc. Natl. Acad. Sci. USA 93:11865-11870.
38. Trager, W., and J. Jensen. 1976. Human malaria parasites in continuous culture. Science 193:673-675.
39. Uilenberg, G., F. Franssen, N. Perie, and A. Spanjer. 1989. Three groups of Babesia canis distinguished and a proposal for nomenclature. Vet. Q. 11:33-40.
40. Valentin, A., D. Rigomier, E. Precigout, B. Carcy, A. Gorenflot, and J. Schrevel. 1991. Lipid trafficking between high density lipoproteins and Babesia divergens-infected human erythrocytes. Biol. Cell. 73:63-70.
41. Vial, H., M. L. Ancelin, J. Philippot, and M. J. Thuet. 1990. Biosynthesis and dynamics of lipids in Plasmodium-infected mature mammalian erythrocytes. Blood Cells 16:531-555.
42. Vial, H., P. Eldin, A. Tielens, and J. Hellemond. 2003. Phospholipids in parasitic protozoa. Mol. Biochem. Parasitol. 126:143-154.
43. Vial, H., and C. Mamoun. 2005. Plasmodium lipids: metabolism and function, p. 327-352. In I. Sherman (ed.), Molecular approach to malaria. ASM Press, Washington, D. C.
44. Vial, H. J., and M. Calas. 2001. Inhibitors of phospholipid metabolism, p. 347-365. In P. Rosenthal (ed.), Antimalarial chemotherapy, mechanisms of action, modes of resistance, and new directions in drug development. Humana Press, Totowa, N. J.
45. Vial, H. J., S. Wein, C. Farenc, C. Kocken, O. Nicolas, M. L. Ancelin, F. Bressolle, A. Thomas, and M. Calas. 2004. Prodrugs of bisthiazolium salts are orally potent antimalarials. Proc. Natl. Acad. Sci. USA 101:15458-15463.
46. Weiss, L. M. 2002. Babesiosis in humans: a treatment review. Exp. Opin. Pharmacother. 3:1109-1115.
47. Wengelnik, K., V. Vidal-Sailhan, M. L. Ancelin, A.-M. Cathiard, J.-L. Morgat, C. H. Kocken, M. Calas, S. Herrera, A. W. Thomas, and H. Vial. 2002. A class of potent antimalarials and their specific accumulation in infected erythrocytes. Science 295:1311-1314.
48. Zintl, A., G. Mulcahy, H. E. Skerett, S. M. Taylor, and J. S. Gray. 2003. Babesia divergens, a bovine blood parasite of veterinary and zoonotic importance. Clin. Microbiol. Rev. 16:622-636.