Transfection studies to explore essential folate metabolism and antifolate drug synergy in the human malaria parasite Plasmodium falciparum

Molecular Microbiology

Volumn 51, Issue 5, 2004, Pages 1425-1438

  Wang, Ping ^a   Wang, Qi ^a   Aspinall, Tanya V ^a   Sims, Paul F G ^a   Hyde, John E ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIMALARIAL AGENT; BACTERIAL ENZYME; DIHYDROPTEROATE SYNTHASE; FOLIC ACID; FOLIC ACID ANTAGONIST; POLYGLUTAMIC ACID;

ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; DRUG MECHANISM; DRUG POTENTIATION; DRUG TARGETING; ENZYME ACTIVATION; ENZYME ACTIVITY; FOLATE METABOLISM; GENETIC TRANSFECTION; IN VIVO STUDY; NONHUMAN; PLASMODIUM FALCIPARUM; PRECURSOR; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTOZOAL GENETICS;

ANIMALS; ANTIMALARIALS; DIHYDROPTEROATE SYNTHASE; DRUG RESISTANCE; DRUG SYNERGISM; ERYTHROCYTES; FOLIC ACID; FOLIC ACID ANTAGONISTS; HUMANS; PLASMIDS; PLASMODIUM FALCIPARUM; PYRIMETHAMINE; SULFADOXINE; TRANSFECTION;

BACTERIA (MICROORGANISMS); PLASMODIUM FALCIPARUM; PROTOZOA;

EID: 1542721577     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2003.03915.x     Document Type: Article

References (40)

1. Achari, A., Somers, D.O., Champness, J.N., Bryant, P.K., Rosemond, J., and Stammers, D.K. (1997) Crystal structure of the anti-bacterial sulfonamide drug target dihydropteroate synthase. Nature Struct Biol 4: 490-497.
2. Alfadhli, S., and Rathod, P.K. (2000) Gene organization of a Plasmodium falciparum serine hydroxymethyltransferase and its functional expression in Escherichia coli. Mol Biochem Parasitol 110: 283-291.
3. Asawamahasakda, W., and Yuthavong, Y. (1993) The methionine synthesis cycle and salvage of methyltetrahydrofolate from host red cells in the malaria parasite (Plasmodium falciparum) Parasitology 107: 1-10.
4. Aspinall, T.V., Joynson, D.H.M., Guy, E., Hyde, J.E., and Sims, P.F.G. (2002) The molecular basis of sulfonamide resistance in Toxoplasma gondii and implications for the clinical management of toxoplasmosis. J Inf Dis 185: 1637-1643.
5. Baca, A.M., Sirawaraporn, R., Turley, S., Sirawaraporn, W., and Hol, W.G.J. (2000) Crystal structure of Mycobacterium tuberculosis 6-hydroxymethyl-7,8-dihydropteroate synthase in complex with pterin monophosphate: new insight into the enzymatic mechanism and sulfa-drug action. J Mol Biol 302: 1193-1212.
6. Baker, H., Tenhove, W., Baker, E., and Frank, O. (1994) Vitamin activities in human portal, hepatic and femoral blood after vitamin ingestion. Int J Vit Nutr Res 64: 60-67.
7. Braganca, B.M., Aravindakshan, I.A., and Ghanekar, D.S. (1957) Enzymic cleavage of folic acid by extracts from human blood cells. 1. Preparation and cofactor requirements of the enzyme system. Biochim Biophys Acta 25: 623-634.
8. Brooks, D.R., Wang, P., Read, M., Watkins, W.M., Sims, P.F.G., and Hyde, J.E. (1994) Sequence variation of the hydroxymethyldihydropterin pyrophosphokinase - dihydropteroate synthase gene in lines of the human malaria parasite, Plasmodium falciparum, with differing resistance to sulfadoxine. Eur J Biochem 224: 397-405.
9. Bzik, D.J., Li, W.B., Horii, T., and Inselburg, J. (1987) Molecular cloning and sequence analysis of the Plasmodium falciparum dihydrofolate reductase-thymidylate synthase gene. Proc Natl Acad Sci USA 84: 8360-8364.
10. Chulay, J.D., Watkins, W.M., and Sixsmith, D.G. (1984) Synergistic antimalarial activity of pyrimethamine and sulfadoxine against Plasmodium falciparum in vitro. Am J Trop Med Hyg 33: 325-330.
11. Crabb, B.S., Triglia, T., Waterkeyn, J.G., and Cowman, A.F. (1997) Stable transgene expression in Plasmodium falciparum. Mol Biochem Parasitol 90: 131-144.
12. Deitsch, K.W., Driskill, C.L., and Wellems, T.E. (2001) Transformation of malaria parasites by the spontaneous uptake and expression of DNA from human erythrocytes. Nucleic Acids Res 29: 850-853.
13. DeSouza, L., Shen, Y., and Bognar, A.L. (2000) Disruption of cytoplasmic and mitochondrial folylpolyglutamate synthetase activity in Saccharomyces cerevisiae. Arch Biochem Biophys 376: 299-312.
14. Ferone, R. (1973) The enzymatic synthesis of dihydropteroate and dihydrofolate by Plasmodium berghei. J Protozool 20: 459-464.
15. Fidock, D.A., Nomura, T., and Wellems, T.E. (1998) Cycloguanil and its parent compound proguanil demonstrate distinct activities against Plasmodium falciparum malaria parasites transformed with human dihydrofolate reductase. Mol Pharmacol 54: 1140-1147.
16. Krumdieck, C.L., Eto, I., and Baggott, J.E. (1992) Regulatory role of oxidized and reduced pteroylpolyglutamates. Ann New York Acad Sci 669: 44-58.
17. Krungkrai, J., Webster, H.K., and Yuthavong, Y. (1989) De novo and salvage biosynthesis of pteroylpentaglutamates in the human malaria parasite, Plasmodium falciparum. Mol Biochem Parasitol 32: 25-37.
18. Lee, C.S., Salcedo, E., Wang, Q., Wang, P., Sims, P.F.G., and Hyde, J.E. (2001) Characterization of three genes encoding enzymes of the folate biosynthetic pathway in Plasmodium falciparum. Parasitology 122: 1-13.
19. Nelson, B.C., Pfeiffer, C.M., Margolis, S.A., and Nelson, C.P. (2003) Affinity extraction combined with stable isotope dilution LC/MS for the determination of 5-methyltetrahydrofolate in human plasma. Anal Biochem 313: 117-127.
20. Nzila, A., Mberu, E., Bray, P., Kokwaro, G., Winstanley, P., Marsh, K., and Ward, S. (2003) Chemosensitization of Plasmodium falciparum by probenecid in vitro. Antimicrob Agents Chemoth 47: 2108-2112.
21. Nzila, A.M., Mberu, E.K., Sulo, J., Dayo, H., Winstanley, P.A., Sibley, C.H., and Watkins, W.M. (2000) Towards an understanding of the mechanism of pyrimethamine-sulfadoxine resistance in Plasmodium falciparum: Genotyping of dihydrofolate reductase and dihydropteroate synthase of Kenyan parasites. Antimicrob Agents Chemoth 44: 991-996.
22. C'Donnell, R.A., Preiser, P.R., Williamson, D.H., Moore, P.W., Cowman, A.F., and Crabb, B.S. (2001) An alteration in concatameric structure is associated with efficient segregation of plasmids in transfected Plasmodium falciparum parasites. Nucleic Acids Res 29: 716-724.
23. Pashley, T.V., Volpe, F., Pudney, M., Hyde, J.E., Sims, P.F.G., and Delves, C.J. (1997) Isolation and molecular characterization of the bifunctional hydroxymethyldihydropterin pyrophosphokinase-dihydropteroate synthase gene from Toxoplasma gondii. Mol Biochem Parasitol 86: 37-47.
24. Plowe, C.V., Kublin, J.G., and Doumbo, O.K. (1998) P. falciparum dihydrofolate reductase and dihydropteroate synthase mutations: epidemiology and role in clinical resistance to antifolates. Drug Resist Updates 1: 389-396.
25. Ravanel, S., Cherest, H., Jabrin, S., Grunwald, D., Surdin-Kerjan, Y., Douce, R., and Rebeille, F. (2001) Tetrahydrofolate biosynthesis in plants: Molecular and functional characterization of dihydrofolate synthetase and three isoforms of folylpolyglutamate synthetase in Arabidopsis thaliana. Proc Natl Acad Sci USA 98: 15360-15365.
26. Read, M., Sherwin, T., Holloway, S.P., Gull, K., and Hyde, J.E. (1993) Microtubular organization visualized by immunofluorescence microscopy during erythrocytic schizogony in Plasmodium falciparum and investigation of posttranslational modifications of parasite tubulin. Parasitology 106: 223-232.
27. Richey, D.P., and Brown, G.M. (1970) A comparison of the effectiveness with which p-aminobenzoic acid and p-aminobenzoylglutamic acid are used as substrate by dihydropteroate synthetase from Escherichia coli. Biochim Biophys Acta 222: 237-239.
28. Roberts, F., Roberts, C.W., Johnson, J.J., Kyle, D.E., Krell, T., Coggins, J.R., et al. (1998) Evidence for the shikimate pathway in apicomplexan parasites. Nature 393: 801-805.
29. Salcedo, E., Cortese, J.F., Plowe, C.V., Sims, P.F.G., and Hyde, J.E. (2001) A bifunctional dihydrofolate synthetase-folylpolyglutamate synthetase in Plasmodium falciparum identified by functional complementation in yeast and bacteria. Mol Biochem Parasitol 112: 241-254.
30. Selhub, J. (1989) Determination of tissue folate composition by affinity-chromatography followed by high-pressure ion-pair liquid- chromatography. Anal Biochem 182: 84-93.
31. Sibley, C.H., Hyde, J.E., Sims, P.F.G., Plowe, C.V., Kublin, J.G., Mberu, E.K., et al. (2001) Pyrimethamine-sulfadoxine resistance in Plasmodium falciparum: what next? Trends Parasitol 17: 582-588.
32. Sims, P., Wang, P., and Hyde, J.E. (1999) Selection and synergy in Plasmodium falciparum. Parasitol Today 15: 132-134.
33. Triglia, T., and Cowman, A.F. (1994) Primary structure and expression of the dihydropteroate synthetase gene of Plasmodium falciparum. Proc Natl Acad Sci USA 91: 7149-7153.
34. Triglia, T., Menting, J.G.T., Wilson, C., and Cowman, A.F. (1997) Mutations in dihydropteroate synthase are responsible for sulfone and sulfonamide resistance in Plasmodium falciparum. Proc Natl Acad Sci USA 94: 13944-13949.
35. Wang, P., Lee, C.S., Bayoumi, R., Djimde, A., Doumbo, O., Swedberg, G., et al. (1997a) Resistance to antifolates in Plasmodium falciparum monitored by sequence analysis of dihydropteroate synthetase and dihydrofolate reductase alleles in a large number of field samples of diverse origins. Mol Biochem Parasitol 89: 161-177.
36. Wang, P., Read, M., Sims, P.F.G., and Hyde, J.E. (1997b) Sulfadoxine resistance in the human malaria parasite Plasmodium falciparum is determined by mutations in dihydropteroate synthetase and an additional factor associated with folate utilization. Mol Microbiol 23: 979-986.
37. Wang, P., Sims, P.F.G., and Hyde, J.E. (1997c) A modified in vitro sulfadoxine susceptibility assay for Plasmodium falciparum suitable for investigating Fansidar resistance. Parasitology 115: 223-230.
38. Wang, P., Brobey, R.K.B., Horii, T., Sims, P.F.G., and Hyde, J.E. (1999) Utilization of exogenous folate in the human malaria parasite Plasmodium falciparum and its critical role in antifolate drug synergy. Mol Microbiol 32: 1254-1262.
39. Wang, P., Wang, Q., Sims, P.F.G., and Hyde, J.E. (2002) Rapid positive selection of stable integrants following transfection of Plasmodium falciparum. Mol Biochem Parasitol 123: 1-10.
40. Watkins, W.M., Mberu, E.K., Winstanley, P.A., and Plowe, C.V. (1997) The efficacy of antifolate antimalarial combinations in Africa: a predictive model based on pharmacodynamic and pharmacokinetic analyses. Parasitol Today 13: 459-464.