Chemical and genetic validation of thiamine utilization as an antimalarial drug target

Nature Communications

Volumn 4, Issue , 2013, Pages

  Chan, Xie Wah Audrey ^a   Wrenger, Carsten ^b,c   Stahl, Katharina ^b   Bergmann, Bärbel ^b   Winterberg, Markus ^a   Müller, Ingrid B ^b   Saliba, Kevin J ^a  

^a AUSTRALIAN NATIONAL UNIVERSITY   (Australia)

^b BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CHLOROQUINE; COCARBOXYLASE; GREEN FLUORESCENT PROTEIN; OXOGLUTARATE DEHYDROGENASE; OXYTHIAMINE; PYRUVATE DEHYDROGENASE; THIAMINE; THIAMINE PYROPHOSPHOKINASE; ANTIMALARIAL AGENT; MESSENGER RNA; PYRUVATE DEHYDROGENASE COMPLEX; RECOMBINANT PROTEIN;

ANTIMALARIAL AGENT; CHEMICAL ANALYSIS; ENZYME ACTIVITY; MALARIA; METABOLITE; MODEL VALIDATION; PARASITE; PROTOZOAN; SUBSTRATE; VITAMIN;

AFFINITY CHROMATOGRAPHY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIMALARIAL ACTIVITY; ARTICLE; BODY WEIGHT; CHEMICAL ANALYSIS; CONTROLLED STUDY; ENZYME SUBUNIT; FEMALE; GENETIC ANALYSIS; GROWTH INHIBITION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IC 50; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PARASITE SURVIVAL; PARASITE VIABILITY; PARASITEMIA; PLASMODIUM FALCIPARUM; PLASMODIUM VINCKEI INFECTION; PROTEIN EXPRESSION; SURVIVAL TIME; TREATMENT DURATION; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; BIOLOGICAL MODEL; CHEMISTRY; DRUG EFFECT; ENZYMOLOGY; ERYTHROCYTE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PARASITE; PARASITOLOGY; PHOSPHORYLATION; REPRODUCIBILITY; TRANSGENIC ANIMAL; DRUG EFFECTS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIMALARIALS; BLOTTING, WESTERN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ERYTHROCYTES; FEMALE; GENE EXPRESSION REGULATION; KETOGLUTARATE DEHYDROGENASE COMPLEX; MICE; MICE, INBRED BALB C; MODELS, BIOLOGICAL; OXYTHIAMINE; PARASITEMIA; PARASITES; PHOSPHORYLATION; PLASMODIUM FALCIPARUM; PYRUVATE DEHYDROGENASE COMPLEX; RECOMBINANT PROTEINS; REPRODUCIBILITY OF RESULTS; RNA, MESSENGER; THIAMIN PYROPHOSPHOKINASE; THIAMINE; THIAMINE PYROPHOSPHATE;

EID: 84885869433     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3060     Document Type: Article

References (57)

1. Divo, A. A., Geary, T. G., Davis, N. L. & Jensen, J. B. Nutritional requirements of Plasmodium falciparum in culture. I. Exogenously supplied dialyzable components necessary for continuous growth. J. Protozool. 32, 59-64 (1985).
2. Saliba, K. J. & Kirk, K. Nutrient acquisition by intracellular apicomplexan parasites: staying in for dinner. Int. J. Parasitol. 31, 1321-1330 (2001).
3. Bozdech, Z. & Ginsburg, H. Data mining of the transcriptome of Plasmodium falciparum: the pentose phosphate pathway and ancillary processes. Malar. J. 4, 17 (2005).
4. Ralph, S. A. et al. Tropical infectious diseases: metabolic maps and functions of the Plasmodium falciparum apicoplast. Nat. Rev. Microbiol. 2, 203-216 (2004).
5. Wrenger, C. et al. Vitamin B1 de novo synthesis in the human malaria parasite Plasmodium falciparum depends on external provision of 4-amino-5-hydroxymethyl-2-methylpyrimidine. Biol. Chem. 387, 41-51 (2006).
6. 6 in the malaria parasite: requisite or dispensable? Braz. J. Med. Biol. Res. 41, 82-88 (2008).
7. Muller, I. B., Hyde, J. E. & Wrenger, C. Vitamin B metabolism in Plasmodium falciparum as a source of drug targets. Trends. Parasitol. 26, 35-43 (2010).
8. Eschbach, M. L., Muller, I. B., Gilberger, T. W., Walter, R. D. & Wrenger, C. The human malaria parasite Plasmodium falciparum expresses an atypical N-terminally extended pyrophosphokinase with specificity for thiamine. Biol. Chem. 387, 1583-1591 (2006).
9. Friedrich, W. Vitamins (W. de Gruyter, 1988).
10. Lonsdale, D. Thiamine. J. Orthomol. Med. 13, 197-209 (1984).
11. Pohl, M., Sprenger, G. A. & Muller, M. A new perspective on thiamine catalysis. Curr. Opin. Biotechnol. 15, 335-342 (2004).
12. Foth, B. J. et al. The malaria parasite Plasmodium falciparum has only one pyruvate dehydrogenase complex, which is located in the apicoplast. Mol. Microbiol. 55, 39-53 (2005).
13. McMillan, P. J., Stimmler, L. M., Foth, B. J., McFadden, G. I. & Muller, S. The human malaria parasite Plasmodium falciparum possesses two distinct dihydrolipoamide dehydrogenases. Mol. Microbiol. 55, 27-38 (2005).
14. Joshi, S. et al. Molecular cloning and characterization of Plasmodium falciparum transketolase. Mol. Biochem. Parasitol. 160, 32-41 (2008).
15. Pei, Y. et al. Plasmodium pyruvate dehydrogenase activity is only essential for the parasite's progression from liver infection to blood infection. Mol. Microbiol. 75, 957-971 (2010).
16. Weber, W. & Kewitz, H. Determination of thiamine in human plasma and its pharmacokinetics. Eur. J. Clin. Pharmacol. 28, 213-219 (1985).
17. Knockel, J. et al. The antioxidative effect of de novo generated vitamin B6 in Plasmodium falciparum validated by protein interference. Biochem. J. 443, 397-405 (2012).
18. Rug, M., Wickham, M. E., Foley, M., Cowman, A. F. & Tilley, L. Correct promoter control is needed for trafficking of the ring-infected erythrocyte surface antigen to the host cytosol in transfected malaria parasites. Infect. Immun. 72, 6095-6105 (2004).
19. Geary, T. G., Divo, A. A. & Jensen, J. B. Nutritional requirements of Plasmodium falciparum in culture. II. Effects of antimetabolites in a semi-defined medium. J. Protozool. 32, 65-69 (1985).
20. Vogl, C., Klein, C. M., Batke, A. F., Schweingruber, M. E. & Stolz, J. Characterization of Thi9, a novel thiamine (vitamin B1) transporter from Schizosaccharomyces pombe. J Biol. Chem. 283, 7379-7389 (2008).
21. Tylicki, A. et al. Modification of thiamine pyrophosphate dependent enzyme activity by oxythiamine in Saccharomyces cerevisiae cells. Can. J. Microbiol. 51, 833-839 (2005).
22. Thomas, A. A. et al. Synthesis, in vitro and in vivo activity of thiamine antagonist transketolase inhibitors. Bioorg. Med. Chem. Lett. 18, 2206-2210 (2008).
23. Boros, L. G. et al. Oxythiamine and dehydroepiandrosterone inhibit the nonoxidative synthesis of ribose and tumor cell proliferation. Cancer. Res. 57, 4242-4248 (1997).
24. Rais, B. et al. Oxythiamine and dehydroepiandrosterone induce a G1 phase cycle arrest in Ehrlich's tumor cells through inhibition of the pentose cycle. FEBS Lett. 456, 113-118 (1999).
25. Yang, C. M., Liu, Y. Z., Liao, J. W. & Hu, M. L. The in vitro and in vivo anti-metastatic efficacy of oxythiamine and the possible mechanisms of action. Clin. Exp. Metastasis 27, 341-349 (2010).
26. Smithline, H. A., Donnino, M. & Greenblatt, D. J. Pharmacokinetics of high-dose oral thiamine hydrochloride in healthy subjects. BMC. Clin. Pharmacol. 12, 4 (2012).
27. Krishna, S. et al. Thiamine deficiency and malaria in adults from southeast Asia. Lancet 353, 546-549 (1999).
28. Mayxay, M. et al. Thiamin deficiency and uncomplicated falciparum malaria in Laos. Trop. Med. Int. Health. 12, 363-369 (2007).
29. Muller, I. B. et al. Poisoning pyridoxal 5-phosphate-dependent enzymes: a new strategy to target the malaria parasite Plasmodium falciparum . PLoS One 4, e4406 (2009).
30. Gardiner, D. L., Trenholme, K. R., Skinner-Adams, T. S., Stack, C. M. & Dalton, J. P. Overexpression of leucyl aminopeptidase in Plasmodium falciparum parasites. Target for the antimalarial activity of bestatin. J. Biol. Chem. 281, 1741-1745 (2006).
31. Slavic, K. et al. Life cycle studies of the hexose transporter of Plasmodium species and genetic validation of their essentiality. Mol. Microbiol. 75, 1402-1413 (2010).
32. Joshi, S. et al. Identification of potential P. falciparum transketolase inhibitors: pharmacophore design, in silico screening and docking studies. J. Biophys. Chem. 1, 96-104 (2010).
33. Yeh, E. & DeRisi, J. L. Chemical rescue of malaria parasites lacking an apicoplast defines organelle function in blood-stage Plasmodium falciparum. PLoS Biol. 9, e1001138 (2011).
34. Rao, A., Yeleswarapu, S. J., Srinivasan, R. & Bulusu, G. Localization of haem biosynthesis pathway enzymes in Plasmodium falciparum . Indian. J. Biochem. Biophys. 45, 365-373 (2008).
35. Hopkins, J. et al. The plastid in Plasmodium falciparum asexual blood stages: a three-dimensional ultrastructural analysis. Protist 150, 283-295 (1999).
36. Sato, S., Clough, B., Coates, L. & Wilson, R. J. Enzymes for haem biosynthesis are found in both the mitochondrion and plastid of the malaria parasite Plasmodium falciparum . Protist 155, 117-125 (2004).
37. van Dooren, G. G. et al. Development of the endoplasmic reticulum, mitochondrion and apicoplast during the asexual life cycle of Plasmodium falciparum. Mol. Microbiol. 57, 405-419 (2005).
38. vanDooren,G.G., Stimmler, L. M.&McFadden, G. I. Metabolic maps and functions of the Plasmodium mitochondrion. FEMS. Microbiol. Rev. 30, 596-630 (2006).
39. Mather, M. W., Henry, K. W. & Vaidya, A. B. Mitochondrial drug targets in apicomplexan parasites. Curr. Drug. Targets 8, 49-60 (2007).
40. Painter, H. J., Morrisey, J. M. & Vaidya, A. B. Mitochondrial electron transport inhibition and viability of intraerythrocytic Plasmodium falciparum. Antimicrob. Agents. Chemother. 54, 5281-5287 (2010).
41. Pradel, G. & Schlitzer, M. Antibiotics in malaria therapy and their effect on the parasite apicoplast. Curr. Mol. Med. 10, 335-349 (2010).
42. Vaidya, A. B. Mitochondrial and plastid functions as antimalarial drug targets. Curr. Drug. Targets. Infect. Disord. 4, 11-23 (2004).
43. Trager, W. & Jensen, J. B. Human malaria parasites in continuous culture. Science 193, 673-675 (1976).
44. Allen, R. J. & Kirk, K. Plasmodium falciparum culture: the benefits of shaking. Mol. Biochem. Parasitol. 169, 63-65 (2010).
45. Das Gupta, R. et al. 3-Aminooxy-1-aminopropane and derivatives have an antiproliferative effect on cultured Plasmodium falciparum by decreasing intracellular polyamine concentrations. Antimicrob. Agents. Chemother. 49, 2857-2864 (2005).
46. Muller, I. B. et al. The assembly of the plasmodial PLP synthase complex follows a defined course. PLoS One 3, e1815 (2008).
47. Crabb, B. S. et al. Transfection of the human malaria parasite Plasmodium falciparum. Methods. Mol. Biol. 270, 263-276 (2004).
48. Muller, I. B. et al. Secretion of an acid phosphatase provides a possible mechanism to acquire host nutrients by Plasmodium falciparum. Cell. Microbiol. 12, 677-691 (2010).
49. Biller, L. et al. Comparison of two genetically related Entamoeba histolytica cell lines derived from the same isolate with different pathogenic properties. Proteomics 9, 4107-4120 (2009).
50. Rozen, S. & Skaletsky, H. Primer3 on the WWW for general users and for biologist programmers. Methods. Mol. Biol. 132, 365-386 (2000).
51. Salanti, A. et al. Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria. Mol. Microbiol. 49, 179-191 (2003).
52. Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25, 402-408 (2001).
53. Butzloff, S., Groves, M. R., Wrenger, C. & Muller, I. B. Cytometric quantification of singlet oxygen in the human malaria parasite Plasmodium falciparum. Cytometry. A 81, 698-703 (2012).
54. Muller, I. B. et al. The vitamin B1 metabolism of Staphylococcus aureus is controlled at enzymatic and transcriptional levels. PLoS One 4, e7656 (2009).
55. Fang, R., Nixon, P. F. & Duggleby, R. G. Identification of the catalytic glutamate in the E1 component of human pyruvate dehydrogenase. FEBS Lett. 437, 273-277 (1998).
56. 5 (pantothenol) inhibits growth of the intraerythrocytic malaria parasite. Antimicrob. Agents Chemother. 49, 632-637 (2005).
57. van Schalkwyk, D. A., Priebe, W. & Saliba, K. J. The inhibitory effect of 2-halo derivatives of D-glucose on glycolysis and on the proliferation of the human malaria parasite Plasmodium falciparum. J. Pharmacol. Exp. Ther. 327, 511-517 (2008).