A comprehensive model of purine uptake by the malaria parasite Plasmodium falciparum: Identification of four purine transport activities in intraerythrocytic parasites

Biochemical Journal

Volumn 411, Issue 2, 2008, Pages 287-295

  Quashie, Neils B ^a   Dorin Semblat, Dominique ^b   Bray, Patrick G ^c   Biagini, Giancarlo A ^c   Doerig, Christian ^b   Ranford Cartwright, Lisa C ^a   De Koning, Harry P ^a  

^a Institute of Biomedical and Life Sciences   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

Author keywords

Drug target; Equilibrative nucleoside transporter family; Nucleobase transporter; PfNT1; Plasmodium falciparum; Purine salvage

Indexed keywords

DRUG TARGET; EQUILIBRATIVE NUCLEOSIDE TRANSPORTER FAMILY; NUCLEOBASE TRANSPORTER; PLASMODIUM FALCIPARUM; PURINE SALVAGE;

BIOSYNTHESIS; PROTEINS; TRANSPORT PROPERTIES;

PHYSIOLOGICAL MODELS;

ADENINE; ADENOSINE; HYPOXANTHINE; NUCLEOSIDE TRANSPORTER; NUCLEOSIDE TRANSPORTER 1; PURINE; UNCLASSIFIED DRUG; PURINE DERIVATIVE;

ARTICLE; CONTROLLED STUDY; ERYTHROCYTE; GENE LOCUS; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOSIDE TRANSPORT; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; TROPHOZOITE; ANIMAL; BIOLOGICAL MODEL; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PARASITOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

PLASMODIUM FALCIPARUM;

ANIMALS; BIOLOGICAL TRANSPORT; ERYTHROCYTES; MODELS, BIOLOGICAL; MOLECULAR STRUCTURE; NUCLEOSIDE TRANSPORT PROTEINS; PLASMODIUM FALCIPARUM; PURINES; TROPHOZOITES;

EID: 42449112152     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20071460     Document Type: Article

References (45)

1. De Koning, H. P., Bridges, D. J. and Burchmore, R. (2005) Purine and pyrimidine transport in pathogenic protozoa: from biology to therapy. FEMS Microbiol. Rev. 29, 987-1020
2. Tracy, S. M. and Sherman, I. W. (1972) Purine uptake and utilization by the avian malaria parasite Plasmodium lophurae. J. Protozool. 19, 541-549
3. Hansen, B. D., Sleeman, H. and Pappas, P. W. (1980) Purine base and nucleoside uptake in Plasmodium berghei and host erythrocytes. J. Parasitol. 66, 205-212
4. Reyes, P., Rathod, P. K., Sanchez, D. J., Mrema, J. E. K., Rieckmann, K. H. and Heidrich, H. G. (1982) Enzymes of purine and pyrimidine metabolism from the human malaria parasite Plasmodium falciparum. Mol. Biochem. Parasitol. 5, 275-290
5. Manandhar, M. S. P. and Van Dyke, K. (1975) Detailed purine salvage metabolism in and outside the free malarial parasite. Exp. Parasitol. 37, 138-146
6. Berman, P. A., Human, L. and Freese, J. A. (1991) Xanthine oxidase inhibits growth of Plasmodium falciparum in human erythrocytes in vitro. J. Clin. Invest. 88, 1848-1855
7. Penny, J. I., Hall, S. T., Woodrow, C. J., Cowan, G. M., Gero, A. M. and Krishna, S. (1998) Expression of substrate-specific transporters encoded by Plasmodium falciparum in Xenopus laevis oocytes. Mol. Biochem. Parasitol. 93, 81-89
8. Parker, M. D., Hyde, R. J., Yao, S. Y. M., McRobert, L., Cass, C. E., Young, J. D., McConkey, G. A. and Baldwin, S. A. (2000) Identification of a nucleoside/nucleobase transporter from Plasmodium falciparum, a novel target for antimalarial chemotherapy. Biochem. J. 349, 67-75
9. Carter, N. S., Ben Mamoun, C., Liu, W., Silva, E. O., Landfear, S. M., Goldberg, D. E. and Ullman, B. (2000) Isolation and functional characterization of the PfNT1 nucleoside transporter gene from Plasmodium falciparum. J. Biol. Chem. 275, 10683-10691
10. Rager, N., Ben Mamoun, C., Carter, N. S., Goldberg, D. E. and Ullman, B. (2001) Localization of the Plasmodium falciparum PfNT1 nucleoside transporter to the parasite plasma membrane. J. Biol. Chem. 276, 41095-41099
11. Downie, M. J., Saliba, K. J., Howitt, S. M., Bröer, S. and Kirk, K. (2006) Transport of nucleosides across the Plasmodium falciparum parasite plasma membrane has characteristics of PfENT1 Mol. Microbiol. 60, 738-748
12. Ghosh, M. and Mukherjee, T. (2000) Stage-specific development of a novel adenosine transporter in Leishmania donovani amastigotes. Mol. Biochem. Parasitol. 108, 93-99
13. De Koning, H. P., Al-Salabi, M. I., Cohen, A., Coombs, G. and Washing, J. M. (2003) Identification and characterization of high affinity purine nucleoside and nucleobase transporters in Toxoplasma gondii. Int. J. Parasitol. 33, 821-831
14. Al-Salabi, M. I. and De Koning, H. P. (2005) Purine nucleobase transport in amastigotes of Leishmania mexicana: involvement in allopurinol uptake. Antimicrob. Ag. Chemother. 49, 3682-3689
15. Carter, N. S. and Fairlamb, A. H. (1993) Arsenical-resistant trypanosomes lack an unusual adenosine transporter. Nature 361, 173-176
16. De Koning, H. P. and Jarvis, S. M. (1997) Purine nucleobase transport in bloodstream forms of Trypanosoma brucei is mediated by two novel transporters. Mol. Biochem. Parasitol. 89, 245-258
17. El Bissati, K., Zufferey, R., Wittola, W. H., Carter, N. S., Ullman, B. and Ben Mamoun, C. (2006) The plasma membrane permease PfNT1 is essential for purine salvage in the human malaria parasite Plasmodium falciparum. Proc. Natl. Acad. Sci. U.S.A. 103, 9286-9291
18. Martin, R. E., Henry, R. I., Abbey, J. L., Clements, J. D. and Kirk, K. (2005) The 'permeome' of the malaria parasite: an overview of the membrane transport proteins of Plasmodium falciparum. Genome Biol. 6, R26
19. Trager, W. and Jensen, J. B. (1976) Human malaria parasites in continuous culture. Science 193, 673-675
20. Lambros, C. and Vanderberg, J. P. (1979) Synchronization of Plasmodium falciparum erythrocytic stages in culture. J. Parasitol. 65, 418-420
21. Stead, A. M. W., Bray, P. G., De Koning, H. P., Elford, B. C., Stocks, P. A. and Ward, S. A. (2001) Diamidine compounds: selective uptake and targeting in Plasmodium falciparum. Mol. Pharmacol. 59, 1298-1306
22. Beaumelle, B. D., Vial, H. J. and Phillippot, J. R. (1987) Reevaluation, using marker enzymes, of the ability of saponin and ammonium chloride to free Plasmodium from infected erythrocytes. J. Parasitol. 73, 743-748.
23. +-ATPase. J. Biol. Chem. 274, 33213-33219
24. Allen, R. J. W. and Kirk, K. (2004) The membrane potential of the intraerythrocytic malaria parasite Plasmodium falciparum. J. Biol. Chem. 279, 11264-11272
25. De Koning, H. P., Watson, C. J. and Jarvis, S. M. (1998) Characterisation of a nucleoside/proton symporter in procyclic Trypanosoma brucei brucei. J. Biol. Chem. 273, 9486-9494
26. Al-Salabi, M. I., Wallace, L. J. M. and De Koning, H. P. (2003) A Leishmania major nucleobase transporter responsible for allopurinol uptake is a functional homologue of the Trypanosoma brucei H2 transporter. Mol. Pharmacol. 63, 814-820
27. Wallace, L. J. M., Candlish, D. and De Koning, H. P. (2002) Different substrate recognition motifs of human and trypanosome nucleobase transporters: selective uptake of purine antimetabolites. J. Biol. Chem. 277, 26149-26156
28. Saliba, K. J., Horner, H. A. and Kirk, K. (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
29. Sidhu, A. B., Valderramos, S. G. and Fidock, D. A. (2005) Pfmdr1 mutations contribute to guinine resistance and enhance mefloguine and artemisinin sensitivity in Plasmodium falciparum. Mol. Microbiol. 57, 913-926
30. Desai, S. A., Krogstad, D. J. and McCleskey, E. W. (1993) A nutrient-permeable channel on the intraerythrocytic malaria parasite. Nature 362, 643-646
31. Stein, A., Vaseduvan, G., Carter, N. S., Ullman, B., Landtear, S. M. and Kavanaugh, M. P. (2003) Equilibrative nucleoside transporter family members from Leishmania. J. Biol. Chem. 278, 35127-35134
32. Gutteridge, W. E. and Trigg, P. I. (1970) Incorporation of radioactive precursors into DNA and RNA of Plasmodium knowlesi in vitro. J. Protozool. 17, 89-96
33. Too, K., Brown, D. M., Bongard, E., Yardley, V., Vivas, L. and Loakes, D. (2007) Anti-malarial activity of N6-modified purine analogs. Bioorg. Med. Chem. 15, 5551-5562
34. Goudela, S., Karatza, P., Koukaki, M., Frilingos, S. and Diallinas, G. (2005) Comparative substrate recognition by bacterial and fungal purine transporters of the NAT/NCS2 family. Mol. Membr. Biol. 22, 263-275
35. Ting, L. M., Shi, W., Lewandowicz, A., Singh, V., Mwakingwe, A., Birck, M. R., Ringia, E. A., Bench, G., Madrid, D. C., Tyler, P. C. et al. (2005) Targeting a novel Plasmodium falciparum purine recycling pathway with specific immucillins. J. Biol. Chem. 280, 9547-9554
36. Chaudhary, K., Darling, J. A., Fohl, L. M., Sullivan, W. J., Donald, R. G., Pfefferkorn, E. R., Ullman, B. and Roos, D. S. (2004) Purine salvage pathways in the apicomplexan parasite Toxoplasma gondii. J. Biol. Chem. 279, 31221-31227
37. Walter, R. D. and Königk, E. (1974) Hypoxanthine-guanine phosphoribosyltransferase and adenine phosphoribosyltransferase from Plasmodium chabaudi; purification and properties. Tropenmed. Parasitol. 25, 227-235
38. Queen, S. A., Vander Jagt, D. L. and Reyes, P. (1989) Characterisation of adenine phosphoribosyltransferase from the human malaria parasite, Plasmodium falciparum. Biochim. Biophys. Acta 996, 160-165
39. Geary, T. G., Divo, A. A., Bonanni, L. C. and Jensen, J. B. (1985) Nutritional requirements of Plasmodium falciparum in culture. III. Further observations on essential nutrients and antimetabolites. J. Protozool. 32, 608-613
40. Van Dyke, K. (1975) Comparison of tritiated hypoxanthine, adenine and adenosine for purine salvage incorporation into nucleic acids of the malarial parasite, Plasmodium falciparum. Tropenmed. Parasitol. 26, 232-238
41. Gardner, M. J., Hall, N., Fung, E., White, C., Berriman, M., Hyman, R. W., Carlton, J. M., Pain, A., Nelson, K. E., Bowman, S. et al. (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419, 498-511
42. Berens, R. L., Krug, E. C. and Marr, J. J. (1995) Purine and pyrimidine metabolism. In Biochemistry and Molecular Biology of Parasites (Marr, J. J. and Müller, M., eds.), pp. 89-117, New York, Academic Press
43. Plagemann, P. G. W., Wohlhueter, R. M. and Woffendin, C. (1988) Nucleoside and nucleobase transport in animal cells. Biochim. Biophys. Acta 947, 405-443
44. Schwab, J. C., Afifi Afifi, M., Pizzorno, C., Handschumacher, R. E. and Joiner, K. A. (1995) Toxoplasma gondii tachyzoites possess an unusual plasma membrane adenosine transporter. Mol. Biochem. Parasitol. 70, 59-69
45. Chiang, C.-W., Carter, N., Sullivan, W. J., Donald, R. G., Roos, D. S., Naguib, F. N., El Kouni, M. H., Ullman, B. and Wilson, C. M. (1999) The adenosine transporter of Toxoplasma gondii; identification by insertional mutagenesis, cloning, and recombinant expression. J. Biol. Chem. 274, 35255-35261