Purine salvage pathways in the intraerythrocytic malaria parasite Plasmodium falciparum

Eukaryotic Cell

Volumn 7, Issue 8, 2008, Pages 1231-1237

  Downie, Megan J ^a,b   Kirk, Kiaran ^b   Mamoun, Choukri Ben ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE PHOSPHORIBOSYLTRANSFERASE; ADENOSINE DEAMINASE; GLYCOSYLTRANSFERASE; NUCLEOSIDE PHOSPHORYLASE; NUCLEOSIDE TRANSPORTER; PURINE DERIVATIVE;

ANIMAL; CELL MEMBRANE; CELL VACUOLE; ERYTHROCYTE; METABOLISM; PARASITOLOGY; PLASMODIUM FALCIPARUM; SHORT SURVEY; ULTRASTRUCTURE;

ADENINE PHOSPHORIBOSYLTRANSFERASE; ADENOSINE DEAMINASE; ANIMALS; CELL MEMBRANE; ERYTHROCYTES; NUCLEOSIDE TRANSPORT PROTEINS; PENTOSYLTRANSFERASES; PLASMODIUM FALCIPARUM; PURINES; VACUOLES;

PLASMODIUM FALCIPARUM;

EID: 48949098886     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00159-08     Document Type: Short Survey

References (71)

1. Asahi, H., T. Kanazawa, Y. Kajihara, K. Takahashi, and T. Takahashi. 1996. Hypoxanthine: a low molecular weight factor essential for growth of erythrocytic Plasmodium falciparum in a serum-free medium. Parasitology 113:19-23.
2. Baldwin, S. A., G. A. McConkey, C. E. Cass, and J. D. Young. 2007. Nucleoside transport as a potential target for chemotherapy in malaria. Curr. Pharm. Des. 13:569-580.
3. Bhat, J. Y., B. G. Shastri, and H. Balaram. 2008. Kinetic and biochemical characterization of Plasmodium falciparum GMP synthetase. Biochem. J. 409:263-273.
4. Booden, T., and R. W. Hull. 1973. Nucleic acid precursor synthesis by Plasmodium lophurae parasitizing chicken erythrocytes. Exp. Parasitol. 34:220-228.
5. Bozdech, Z., M. Llinas, B. L. Pulliam, E. D. Wong, J. Zhu, and J. L. DeRisi. 2003. The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol. 1:E5.
6. Brown, D. M., A. G. Netting, B. K. Chun, Y. Choi, C. K. Chu, and A. M. Gero. 1999. L-nucleoside analogues as potential antimalarials that selectively target Plasmodium falciparum adenosine deaminase. Nucleosides Nucleotides 18:2521-2532.
7. Bungener, W., and G. Nielsen. 1967. Nucleic acid metabolism in experimental malaria. 1. Studies on the incorporation of thymidine, uridine, and adenosine in the malaria parasite (Plasmodium berghei and Plasmodium vinckei). Z. Tropenmed. Parasitol. 18:456-462. (In German.)
8. Bungener, W., and G. Nielsen. 1968. Nucleic acid metabolism in experimental malaria. 2. Incorporation of adenosine and hypoxanthine into the nucleic acids of malaria parasites (Plasmodium berghei and Plasmodium vinckei). Z Tropenmed Parasitol. 19:185-197. (In German.)
9. Bzowska, A., E. Kulikowska, and D. Shugar. 2000. Purine nucleoside phosphorylases: properties, functions, and clinical aspects. Pharmacol. Ther. 88: 349-425.
10. Carter, N. S., C. Ben Mamoun, W. Liu, E. O. Silva, S. M. Landfear, D. E. Goldberg, and B. Ullman. 2000. Isolation and functional characterization of the PfNT1 nucleoside transporter gene from Plasmodium falciparum. J. Biol. Chem. 275:10683-10691.
11. Carter, N. S., P. Yates, C. S. Arendt, J. M. Boitz, and B. Ullman. 2008. Purine and pyrimidine metabolism in Leishmania. Adv. Exp. Med. Biol. 625:141-154.
12. Chaudhary, K., J. A. Darling, L. M. Fohl, W. J. Sullivan, Jr., R. G. Donald, E. R. Pfefferkorn, B. Ullman, and D. S. Roos. 2004. Purine salvage pathways in the apicomplexan parasite Toxoplasma gondii. J. Biol. Chem. 279:31221-31227.
13. Chaudhary, K., L. M. Ting, K. Kim, and D. S. Roos. 2006. Toxoplasma gondii purine nucleoside phosphorylase biochemical characterization, inhibitor profiles, and comparison with the Plasmodium falciparum ortholog. J. Biol. Chem. 281:25652-25658.
14. Craig, S. P., III, and A. E. Eakin. 2000. Purine phosphoribosyltransferases. J. Biol. Chem. 275:20231-20234.
15. Daddona, P. E., W. P. Wiesmann, C. Lambros, W. N. Kelley, and H. K. Webster. 1984. Human malaria parasite adenosine deaminase. Characterization in host enzyme-deficient erythrocyte culture. J. Biol. Chem. 259:1472-1475.
16. Daddona, P. E., W. P. Wiesmann, W. Milhouse, J. W. Chern, L. B. Townsend, M. S. Hershfield, and H. K. Webster. 1986. Expression of human malaria parasite purine nucleoside phosphorylase in host enzyme-deficient erythrocyte culture. Enzyme characterization and identification of novel inhibitors. J. Biol. Chem. 261:11667-11673.
17. de Koning, H. P., D. J. Bridges, and R. J. Burchmore. 2005. Purine and pyrimidine transport in pathogenic protozoa: from biology to therapy. FEMS Microbiol. Rev. 29:987-1020.
18. Desai, S. A., D. J. Krogstad, and E. W. McCleskey. 1993. A nutrient-permeable channel on the intraerythrocytic malaria parasite. Nature 362:643-646.
19. Downie, M. J., K. J. Saliba, S. Broer, S. M. Howitt, and K. Kirk. 2008. Purine nucleobase transport in the intraerythrocytic malaria parasite. Int. J. Parasitol. 38:203-209.
20. Downie, M. J., K. J. Saliba, S. M. Howitt, S. Bröer, and K. Kirk. 2006. Transport of nucleosides across the Plasmodium falciparum parasite plasma membrane has characteristics of PfENT1. Mol. Microbiol. 60:738-748.
21. El Bissati, K., R. Zufferey, W. H. Witola, N. S. Carter, B. Ullman, and C. Ben Mamoun. 2006. The plasma membrane permease PfNT1 is essential for purine salvage in the human malaria parasite Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 103:9286-9291.
22. El Bissati, K., M. J. Downie, S.-K. Kim, M. Horowitz, N. Carter, B. Ullman, and C. Ben Mamoun. 3 July 2008. Genetic evidence for the essential role of PfNT1 in the transport and utilization of xanthine, guanine, guanosine and adenine by Plasmodium falciparum. Mol. Biochem. Parasitol. doi:10.1016/j.molbiopara.2008.06.012.
23. Engelhardt, B. E., M. I. Jordan, K. E. Muratore, and S. E. Brenner. 2005. Protein molecular function prediction by bayesian phylogenomics. PLoS Comput. Biol. 1:e45.
24. Gandhi, V., J. M. Kilpatrick, W. Plunkett, M. Ayres, L. Harman, M. Du, S. Bantia, J. Davisson, W. G. Wierda, S. Faderl, H. Kantarjian, and D. Thomas. 2005. A proof-of-principle pharmacokinetic, pharmacodynamic, and clinical study with purine nucleoside phosphorylase inhibitor immucillin-H (BCX-1777, forodesine). Blood 106:4253-4260.
25. Gardner, M. J., N. Hall, E. Fung, O. White, M. Berriman, R. W. Hyman, J. M. Carlton, A. Pain, K. E. Nelson, S. Bowman, I. T. Paulsen, K. James, J. A. Eisen, K. Rutherford, S. L. Salzberg, A. Craig, S. Kyes, M. S. Chan, V. Nene, S. J. Shallom, B. Suh, J. Peterson, S. Angiuoli, M. Pertea, J. Allen, J. Selengut, D. Haft, M. W. Mather, A. B. Vaidya, D. M. Martin, A. H. Fairlamb, M. J. Fraunholz, D. S. Roos, S. A. Ralph, G. I. McFadden, L. M. Cummings, G. M. Subramanian, C. Mungall, J. C. Venter, D. J. Carucci, S. L. Hoffman, C. Newbold, R. W. Davis, C. M. Fraser, and B. Barrell. 2002. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498-511.
26. Gati, W. P., A. N. Lin, T. I. Wang, J. D. Young, and A. R. Paterson. 1990. Parasite-induced processes for adenosine permeation in mouse erythrocytes infected with the malarial parasite Plasmodium yoelii. Biochem. J. 272:277-280.
27. Gero, A. M., E. M. Bugledich, A. R. Paterson, and G. P. Jamieson. 1988. Stage-specific alteration of nucleoside membrane permeability and nitrobenzylthioinosine insensitivity in Plasmodium falciparum infected erythrocytes. Mol. Biochem. Parasitol. 27:159-170.
28. Gero, A. M., and S. T. Hall. 1997. Plasmodium falciparum: transport of enantiomers of nucleosides into Sendai-treated trophozoites. Exp. Parasitol. 86:228-231.
29. Gutteridge, W. E., and P. I. Trigg. 1970. Incorporation of radioactive precursors into DNA and RNA of Plasmodium knowlesi in vitro. J. Protozool. 17:89-96.
30. Hyde, J. E. 2007. Targeting purine and pyrimidine metabolism in human apicomplexan parasites. Curr. Drug Targets 8:31-47.
31. Jayalakshmi, R., K. Sumathy, and H. Balaram. 2002. Purification and characterization of recombinant Plasmodium falciparum adenylosuccinate synthetase expressed in Escherichia coli. Protein Expr. Purif. 25:65-72.
32. Keough, D. T., A. L. Ng, D. J. Winzor, B. T. Emmerson, and J. de Jersey. 1999. Purification and characterization of Plasmodium falciparum hypoxanthine-guanine-xanthine phosphoribosyltransferase and comparison with the human enzyme. Mol. Biochem. Parasitol. 98:29-41.
33. Keough, D. T., T. Skinner-Adams, M. K. Jones, A. L. Ng, I. M. Brereton, L. W. Guddat, and J. de Jersey. 2006. Lead compounds for antimalarial chemotherapy: purine base analogs discriminate between human and P. falciparum 6-oxopurine phosphoribosyltransferases. J. Med. Chem. 49:7479-7486.
34. Kicska, G. A., P. C. Tyler, G. B. Evans, R. H. Furneaux, K. Kim, and V. L. Schramm. 2002. Transition state analogue inhibitors of purine nucleoside phosphorylase from Plasmodium falciparum. J. Biol. Chem. 277:3219-3225.
35. Kicska, G. A., P. C. Tyler, G. B. Evans, R. H. Furneaux, V. L. Schramm, and K. Kim. 2002. Purine-less death in Plasmodium falciparum induced by immucillin-H, a transition state analogue of purine nucleoside phosphorylase. J. Biol. Chem. 277:3226-3231.
36. King, A., and D. W. Melton. 1987. Characterisation of cDNA clones for hypoxanthine-guanine phosphoribosyltransferase from the human malarial parasite, Plasmodium falciparum: comparisons to the mammalian gene and protein. Nucleic Acids Res. 15:10469-10481.
37. Kirk, K., H. A. Horner, B. C. Elford, J. C. Ellory, and C. I. Newbold. 1994. Transport of diverse substrates into malaria-infected erythrocytes via a pathway showing functional characteristics of a chloride channel. J. Biol. Chem. 269:3339-3347.
38. Lauer, S. A., P. K. Rathod, N. Ghori, and K. Haldar. 1997. A membrane network for nutrient import in red cells infected with the malaria parasite. Science 276:1122-1125.
39. Li, C. M., P. C. Tyler, R. H. Furneaux, G. Kicska, Y. Xu, C. Grubmeyer, M. E. Girvin, and V. L. Schramm. 1999. Transition-state analogs as inhibitors of human and malarial hypoxanthine-guanine phosphoribosyltransferases. Nat. Struct. Biol. 6:582-587.
40. Marshall, V. M., and R. L. Coppel. 1997. Characterisation of the gene encoding adenylosuccinate lyase of Plasmodium falciparum. Mol. Biochem. Parasitol. 88:237-241.
41. Martin, R. E., R. I. Henry, J. L. Abbey, J. D. Clements, and K. Kirk. 2005. The 'permeome' of the malaria parasite: an overview of the membrane transport proteins of Plasmodium falciparum. Genome Biol. 6:R26.
42. McConkey, G. A. 2000. Plasmodium falciparum: isolation and characterisation of a gene encoding protozoan GMP synthase. Exp. Parasitol. 94:23-32.
43. Murray, A. W. 1971. The biological significance of purine salvage. Annu. Rev. Biochem. 40:811-826.
44. Ofulla, A. V., V. C. Okoye, B. Khan, J. I. Githure, C. R. Roberts, A. J. Johnson, and S. K. Martin. 1993. Cultivation of Plasmodium falciparum parasites in a serum-free medium. Am. J. Trop. Med. Hyg. 49:335-340.
45. Parker, M. D., R. J. Hyde, S. Y. Yao, L. McRobert, C. E. Cass, J. D. Young, G. A. McConkey, and S. A. Baldwin. 2000. Identification of a nucleoside/nucleobase transporter from Plasmodium falciparum, a novel target for antimalarial chemotherapy. Biochem. J. 349:67-75.
46. Penny, J. I., S. T. Hall, C. J. Woodrow, G. M. Cowan, A. M. Gero, and S. Krishna. 1998. Expression of substrate-specific transporters encoded by Plasmodium falciparum in Xenopus laevis oocytes. Mol. Biochem. Parasitol. 93:81-89.
47. Polet, H., and C. F. Barr. 1968. DNA, RNA, and protein synthesis in erythrocytic forms of Plasmodium knowlesi. Am. J. Trop. Med. Hyg. 17:672-679.
48. Pollack, Y., R. Shemer, S. Metzger, D. T. Spira, and J. Golenser. 1985. Plasmodium falciparum: expression of the adenine phosphoribosyltransferase gene in mouse L cells. Exp. Parasitol. 60:270-275.
49. Quashie, N. B., D. Dorin-Semblat, P. G. Bray, G. A. Biagini, C. Doerig, L. C. Ranford-Cartwright, and H. P. De Koning. 2008. A comprehensive model of purine uptake by the malaria parasite Plasmodium falciparum: identification of four purine transport activities in intraerythrocytic parasites. Biochem. J. 411:287-295.
50. Queen, S. A., D. Vander Jagt, and P. Reyes. 1988. Properties and substrate specificity of a purine phosphoribosyltransferase from the human malaria parasite, Plasmodium falciparum. Mol. Biochem. Parasitol. 30:123-133.
51. Queen, S. A., D. L. Vander Jagt, and P. Reyes. 1989. Characterization of adenine phosphoribosyltransferase from the human malaria parasite, Plasmodium falciparum. Biochim. Biophys. Acta 996:160-165.
52. Rager, N., C. B. Mamoun, N. S. Carter, D. E. Goldberg, and B. Ullman. 2001. Localization of the Plasmodium falciparum PfNT1 nucleoside transporter to the parasite plasma membrane. J. Biol. Chem. 276:41095-41099.
53. Reyes, P., P. K. Rathod, D. J. Sanchez, J. E. Mrema, K. H. Rieckmann, and H. G. Heidrich. 1982. Enzymes of purine and pyrimidine metabolism from the human malaria parasite, Plasmodium falciparum. Mol. Biochem. Parasitol. 5:275-290.
54. Roth, E., Jr., N. Ogasawara, and S. Schulman. 1989. The deamination of adenosine and adenosine monophosphate in Plasmodium falciparum-infected human erythrocytes: in vitro use of 2-deoxycoformycin and AMP deaminase-deficient red cells. Blood 74:1121-1125.
55. Schramm, V. L. 2004. Immucillins as antibiotics for T-cell proliferation and malaria. Nucleosides Nucleotides Nucleic Acids 23:1305-1311.
56. Sherman, I. W. 1998. Purine and pyrimidine metabolism of asexual stages, p. 177-184. In I. W. Sherman (ed.), Malaria: parasite biology, pathogenesis and protection. ASM Press, Washington, DC.
57. Shi, W., C. M. Li, P. C. Tyler, R. H. Furneaux, S. M. Cahill, M. E. Girvin, C. Grubmeyer, V. L. Schramm, and S. C. Almo. 1999. The 2.0 A structure of malarial purine phosphoribosyltransferase in complex with a transition-state analogue inhibitor. Biochemistry 38:9872-9880.
58. Shi, W., C. M. Li, P. C. Tyler, R. H. Furneaux, C. Grubmeyer, V. L. Schramm, and S. C. Almo. 1999. The 2.0 A structure of human hypoxanthine-guanine phosphoribosyltransferase in complex with a transition-state analog inhibitor. Nat. Struct. Biol. 6:588-593.
59. Shi, W., L. M. Ting, G. A. Kicska, A. Lewandowicz, P. C. Tyler, G. B. Evans, R. H. Furneaux, K. Kim, S. C. Almo, and V. L. Schramm. 2004. Plasmodium falciparum purine nucleoside phosphorylase: crystal structures, immucillin inhibitors, and dual catalytic function. J. Biol. Chem. 279:18103-18106.
60. Snow, R. W., C. A. Guerra, A. M. Noor, H. Y. Myint, and S. I. Hay. 2005. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434:214-217.
61. Ting, L. M., W. Shi, A. Lewandowicz, V. Singh, A. Mwakingwe, M. R. Birck, E. A. Ringia, G. Bench, D. C. Madrid, P. C. Tyler, G. B. Evans, R. H. Furneaux, V. L. Schramm, and K. Kim. 2005. Targeting a novel Plasmodium falciparum purine recycling pathway with specific immucillins. J. Biol. Chem. 280:9547-9554.
62. Tracy, S. M., and I. W. Sherman. 1972. Purine uptake and utilization by the avian malaria parasite Plasmodium lophurae. J. Protozool. 19:541-549.
63. Traut, T. W. 1994. Physiological concentrations of purines and pyrimidines. Mol. Cell. Biochem. 140:1-22.
64. Tyler, P. C., E. A. Taylor, R. F. Frohlich, and V. L. Schramm. 2007. Synthesis of 5-methylthio coformycins: specific inhibitors for malarial adenosine deaminase. J. Am. Chem. Soc. 129:6872-6879.
65. Upston, J. M., and A. M. Gero. 1995. Parasite-induced permeation of nucleosides in Plasmodium falciparum malaria. Biochim. Biophys. Acta 1236:249-258.
66. Van Dyke, K., G. C. Tremblay, C. H. Lantz, and C. Szustkiewicz. 1970. The source of purines and pyrimidines in Plasmodium berghei. Am. J. Trop. Med. Hyg. 19:202-208.
67. Walsh, J. C., and I. W. Sherman. 1968. Purine and pyrimidine synthesis by the avian malaria parasite Plasmodium lophurae. J. Protozool. 15:763-770.
68. Webster, H. K., W. P. Wiesman, and C. S. Pavia. 1984. Adenosine deaminase in malaria infection: effect of 2-deoxycoformycin in vivo. Adv. Exp. Med. Biol. 165:225-229.
69. World Health Organization. 2007. A safer future: global public health security in the 21st century. World Health Report 2007. World Health Organization, Geneva, Switzerland.
70. Yamada, K. A., and I. W. Sherman. 1981. Purine metabolizing enzymes of Plasmodium lophurae and its host cell, the duckling (Anas domesticus) erythrocyte. Mol. Biochem. Parasitol. 2:349-358.
71. Young, J. A., Q. L. Fivelman, P. L. Blair, P. de la Vega, K. G. Le Roch, Y. Zhou, D. J. Carucci, D. A. Baker, and E. A. Winzeler. 2005. The Plasmodium falciparum sexual development transcriptome: a microarray analysis using ontology-based pattern identification. Mol. Biochem. Parasitol. 143:67-79.