The folate metabolic network of Falciparum malaria

Molecular and Biochemical Parasitology

Volumn 188, Issue 1, 2013, Pages 51-62

  Salcedo Sora, J Enrique ^a   Ward, Steve A ^a  

^a LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

Author keywords

Folate; Folate transport; One carbon metabolism; pABA; Plasmodium; Plasmodium cell cycle

Indexed keywords

4 AMINOBENZOIC ACID; AMODIAQUINE; ARTEMISININ; CARBON; FOLIC ACID; FOLIC ACID ANTAGONIST; FOLINIC ACID; LOMETREXOL; METHOTREXATE; PEMETREXED; PTERIN; PYRIMETHAMINE; SHIKIMIC ACID; SULFADOXINE; TRIMETREXATE;

ANOPHELES; BIOCHEMISTRY; BIOSYNTHESIS; CARBON METABOLISM; ERYTHROCYTE; FOLATE METABOLISM; GAMETOCYTE; HUMAN; LIFE CYCLE; LIVER CELL; MALARIA; MALARIA FALCIPARUM; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; REVIEW; THERMODYNAMICS;

ANTIMALARIALS; BIOLOGICAL TRANSPORT; DRUG RESISTANCE; FOLIC ACID; FOLIC ACID ANTAGONISTS; HUMANS; METABOLIC NETWORKS AND PATHWAYS; PLASMODIUM FALCIPARUM; PTERINS;

EID: 84876731079     PISSN: 01666851     EISSN: 18729428     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2013.02.003     Document Type: Review

References (152)

1. WHO World malaria report 2012 WHO Press Geneva
2. S.I. Hay, E.A. Okiro, and P.W. Gething Estimating the global clinical burden of Plasmodium falciparum malaria in 2007 PLoS Medicine 7 6 2010 e1000290
3. Walling J From methotrexate to pemetrexate and beyond. A review of the pharmacodynamic and clinical properties of antifolates Investigational New Drugs 24 2006 37 77
4. M.G. Feely, A. Erickson, and J.R. O'Dell Therapeutic options for rheumatoid arthritis Expert Opinion on Pharmacotherapy 10 13 2009 2095 2106
5. S. Said, E.W.B. Jeffes, and Weinstein GD Methotrexate Clinics in Dermatology 15 1997 781 797
6. P.A. Masters, T.A. O'Bryan, J. Zurlo, D.Q. Miller, and N. Joshi Trimethoprim-sulfamethoxazole revisited Archives of Internal Medicine 163 4 2003 402 410
7. S.L. Walker, and Lockwood DNJ Leprosy Clinics in Dermatology 25 2007 165 172
8. N.G. Guerina, H.-W. Hsu, and H.C. Meissner Neonatal serologic screening and early treatment for congenital Toxoplasma gondii infection New England Journal of Medicine 330 26 1994 1858 1863
9. A.A. Escalante, D.L. Smith, and Y. Kim The dynamics of mutations associated with anti-malarial drug resistance in Plasmodium falciparum Trends in Parasitology 25 12 2009 557 563
10. T. Mita, K. Tanabe, and K. Kita Spread and evolution of Plasmodium falciparum drug resistance Parasitology International 58 3 2009 201 209
11. WHO Guidelines for the treatment of malaria 2006 WHO Press Geneva
12. I.B. Müller, and J.E. Hyde Antimalarial drugs: modes of action and mechanisms of parasite resistance Future Microbiology 5 12 2010 1857 1873
13. A. Nzila Inhibitors of de novo folate enzymes in Plasmodium falciparum Drug Discovery Today 11 19-20 2006 939 944
14. Y.K.S. Yuthavong, and U.C.P. Leartsakulpanich Folate metabolism as a source of molecular targets for antimalarials Future Microbiology 1 2006 113 125
15. B. Shane Folate metabolism M.F. Picciano, E.L.R. Stokstad, J.F.J Gregory III Folic acid metabolism in health and disease 1990 Wiley-Liss New York 65 78
16. A. Bermingham, and J.P. Derrick The folic acid biosynthesis pathway in bacteria: evaluation of potential for antibacterial drug discovery BioEssays 24 7 2002 637 648
17. J.H. White, and Kilbey BJ DNA replication in the malaria parasite Parasitology Today 12 1996 151 155
18. N. Gerald, B. Mahajan, and S. Kumar Mitosis in the human malaria parasite Plasmodium falciparum Eukaryotic Cell 10 4 2011 474 482
19. J.E. Hyde Exploring the folate pathway in Plasmodium falciparum Acta Tropica 94 2005 191 206
20. J. Krungkrai, Y. Yuthavong, and H.K. Webster Guanosine triphosphate cyclohydrolase in Plasmodium falciparum and other Plasmodium species Molecular and Biochemical Parasitology 17 3 1985 265 276
21. C.S. Lee, E. Salcedo, Q. Wang, P. Wang, P.F. Sims, and J.E. Hyde Characterization of three genes encoding enzymes of the folate biosynthetic pathway in Plasmodium falciparum Parasitology 122 1 2001 1 13
22. S. Dittrich, S.L. Mitchell, and A.M. Blagborough An atypical orthologue of 6-pyruvoyltetrahydropterin synthase can provide the missing link in the folate biosynthesis pathway of malaria parasites Molecular Microbiology 67 3 2008 609 618
23. T. Triglia Primary structure and expression of the dihydropteroate synthetase gene of Plasmodium falciparum Proceedings of the National Academy of Sciences 91 15 1994 7149 7153
24. E. Salcedo, J.F. Cortese, C.V. Plowe, P.F. Sims, and J.E. Hyde A bifunctional dihydrofolate synthetasefolylpolyglutamate synthetase in Plasmodium falciparum identified by functional complementation in yeast and bacteria Molecular and Biochemical Parasitology 112 2 2001 239 252 10.1016/S0166-6851(00) 00370-4
25. S.J. Hall, P.F. Sims, and J.E. Hyde Functional expression of the dihydrofolate reductase and thymidylate synthetase activities of the human malaria parasite Plasmodium falciparum in Escherichia coli Molecular and Biochemical Parasitology 45 2 1991 317 330
26. F. Roberts, C.W. Roberts, and J.J. Johnson Evidence for the shikimate pathway in apicomplexan parasites Nature 393 6687 1998 801 805
27. C.W. Roberts, F. Roberts, and R.E. Lyons The shikimate pathway and its branches in apicomplexan parasites Journal of infectious diseases 185 Suppl. 1 2002 S25 36
28. S.O. Duke, and S.B. Powles Glyphosate: a once-in-a-century herbicide Pest Management Science 64 4 2008 319 325
29. G.A. McConkey Targeting the shikimate pathway in the malaria parasite Plasmodium falciparum Antimicrobial Agents and Chemotherapy 43 1 1999 175 177
30. L. McRobert, S. Jiang, A. Stead, and G.A. McConkey Plasmodium falciparum: interaction of shikimate analogues with antimalarial drugs Experimental Parasitology 111 3 2005 178 181
31. K.M. Herrmann, and L.M. Weaver The shikimate pathway Annual Review of Plant Physiology and Plant Molecular Biology 50 1 1999 473 503
32. A. Dieckmann, and A. Jung Mechanisms of sulfadoxine resistance in Plasmodium falciparum Molecular and Biochemical Parasitology 19 2 1986 143
33. G.A. McConkey, J.W. Pinney, and D.R. Westhead Annotating the Plasmodium genome and the enigma of the shikimate pathway Trends in Parasitology 20 2 2004 60 65
34. T. Fitzpatrick, S. Ricken, M. Lanzer, N. Amrhein, P. Macheroux, and B. Kappes Subcellular localization and characterization of chorismate synthase in the apicomplexan Plasmodium falciparum Molecular Microbiology 40 1 2001 65 75
35. B.P. Nichols, A.M. Seibold, and S.Z. Doktor Para-aminobenzoate synthesis from chorismate occurs in two steps Journal of Biological Chemistry 264 15 1989 8597 8601
36. G.J.C. Basset, E.P. Quinlivan, and S. Ravanel Folate synthesis in plants: the p-aminobenzoate branch is initiated by a bifunctional PabA-PabB protein that is targeted to plastids Proceedings of the National Academy of Sciences of the United States of America 101 6 2004 1496 1501
37. J.C. Edman, A.L. Goldstein, and J.G. Erbe Para-aminobenzoate synthase gene of Saccharomyces cerevisiae encodes a bifunctional enzyme Yeast 9 6 1993 669 675
38. C. Aurrecoechea, J. Brestelli, and B.P. Brunk PlasmoDB: a functional genomic database for malaria parasites Nucleic Acids Research 37 2009
39. T. Triglia, and A.F. Cowman Plasmodium falciparum: a homologue of p-aminobenzoic acid synthetase Experimental Parasitology 92 1999 154 158
40. G.J.C. Basset, S. Ravanel, and E.P. Quinlivan Folate synthesis in plants: the last step of the p-aminobenzoate branch is catalyzed by a plastidial aminodeoxychorismate lyase Plant Journal: for Cell and Molecular Biology 40 4 2004 453 461
41. J. Botet, L. Mateos, J.L. Revuelta, and M.A. Santos A chemogenomic screening of sulfanilamide-hypersensitive Saccharomyces cerevisiae mutants uncovers ABZ2 the gene encoding a fungal aminodeoxychorismate lyase Eukaryotic Cell 6 11 2007 2102 2111
42. J.M. Green, and B.P. Nichols p-Aminobenzoate biosynthesis in Escherichia coli. Purification of aminodeoxychorismate lyase and cloning of pabC Journal of Biological Chemistry 266 20 1991 12971 12975
43. Y. Zhang, L. Bai, and Z. Deng Functional characterization of the first two actinomycete 4-amino-4-deoxychorismate lyase genes Microbiology (Reading, England) 155 Pt 7 2009 2450 2459
44. S. Alfadhli, and P.K. Rathod Gene organization of a Plasmodium falciparum serine hydroxymethyltransferase and its functional expression in Escherichia coli Molecular and Biochemical Parasitology 110 2 2000 283 291
45. S. Maenpuen, K. Sopitthummakhun, Y. Yuthavong, P. Chaiyen, and U. Leartsakulpanich Characterization of Plasmodium falciparum serine hydroxymethyltransferase-a potential antimalarial target Molecular and Biochemical Parasitology 168 1 2009 63 73
46. W. Pornthanakasem, D. Kongkasuriyachai, C. Uthaipibull, Y. Yuthavong, and U. Leartsakulpanich Plasmodium serine hydroxymethyltransferase: indispensability and display of distinct localization Malaria Journal 11 1 2012 387
47. C.K.T. Pang, J.H. Hunter, and R. Gujjar Catalytic and ligand-binding characteristics of Plasmodium falciparum serine hydroxymethyltransferase Molecular and Biochemical Parasitology 168 1 2009 74 83
48. E. Salcedo, P.F.G. Sims, and J.E. Hyde A glycine-cleavage complex as part of the folate one-carbon metabolism of Plasmodium falciparum Trends in Parasitology 21 9 2005 406 411
49. M. Read, I.B. Müller, S.L. Mitchell, P.F.G. Sims, and J.E. Hyde Dynamic subcellular localization of isoforms of the folate pathway enzyme serine hydroxymethyltransferase (SHMT) through the erythrocytic cycle of Plasmodium falciparum Malaria Journal 9 1 2010 351
50. M.D. Spalding, M. Allary, J.R. Gallagher, and S.T. Prigge Validation of a modified method for Bxb1 mycobacteriophage integrase-mediated recombination in Plasmodium falciparum by localization of the H-protein of the glycine cleavage complex to the mitochondrion Molecular and Biochemical Parasitology 172 2 2010 156 160
51. J. Krungkrai, H.K. Webster, and Y. Yuthavong De novo and salvage biosynthesis of pteroylpentaglutamates in the human malaria parasite, Plasmodium falciparum Molecular and Biochemical Parasitology 32 1989 25 38
52. T. Rodrigues, M. Prudêncio, R. Moreira, M.M. Mota, and F. Lopes Targeting the liver stage of malaria parasites: a yet unmet goal Journal of Medicinal Chemistry 55 3 2012 995 1012
53. Y. Lin, S.R. Dueker, and J.R. Follett Quantitation of in vivo human folate metabolism American Journal of Clinical Nutrition 80 2004 680 691
54. J.E. Salcedo-Sora, E. Ochong, and S. Beveridge The molecular basis of folate salvage in Plasmodium falciparum: characterization of two folate transporters Journal of Biological Chemistry 286 52 2011 44659 44668
55. T.T. Wang, C.J. Chandler, and C.H. Halsted Intracellular pteroylpolyglutamate hydrolase from human jejunal mucosa. Isolation and characterization Journal of Biological Chemistry 261 29 1986 13551 13555
56. B. Eriksson, B. Courtier, A. Bjorkman, F. Miltgen, and D. Mazier Activity of dihydrofolate reductase inhibitors on the hepatic stages of Plasmodium yoelii yoelii in vitro Transactions of the Royal Society of Tropical Medicine and Hygiene 85 1991 725 726
57. P.J. Bagley, and J. Selhub A common mutation in the methylenetetrahydrofolate reductase gene is associated with an accumulation of formylated tetrahydrofolates in red blood cells Proceedings of the National Academy of Sciences of the United States of America 95 1998 13217 13220
58. M.J. Koury, and P. Ponka New insights into erythropoiesis: the roles of folate, vitamin B12 and Iron Annual Review of Nutrition 24 2004 105 131
59. R.E. Benesch, R. Benesch, S. Kwong, and C.M. Baugh A pteroylpolyglutamate binds to tetramers in deoxyhemoglobin but to dimers in oxyhemoglobin Proceedings of the National Academy of Sciences of the United States of America 80 20 1983 6202 6205
60. R. Benesch, S. Waxman, R. Benesch, and C. Baugh The binding of folyl polyglutamates by hemoglobin Biochemical and Biophysical Research Communications 106 4 1982 1359 1363
61. R. Ferone Folate metabolism in malaria Bulletin of the World Health Organization 55 2-3 1977 291 298
62. J. Krungkrai, Y. Yuthavong, and H.K. Webster High-performance liquid chromatographic assay for pteroylpolyglutamate hydrolase Journal of Chromatography 417 1987 47 56
63. A. Schapira, I.C. Bygbjerg, S. Jepsen, H. Flachs, and M.W. Bentzon The susceptibility of Plasmodium falciparum to sulfadoxine and pyrimethamine: correlation of in vivo and in vitro results American Journal of Tropical Medicine and Hygiene 35 2 1986 239 245
64. J.D. Chulay, W.M. Watkins, and D.G. Sixsmith Synergistic antimalarial activity of pyrimethamine and sulfadoxine against Plasmodium falciparum in vitro American Journal of Tropical Medicine and Hygiene 33 3 1984 325 330
65. F. Hawking Milk diet p-aminobenzoic acid and malaria (P. berghei) British Medical Journal 1953 1201 1202
66. B.G. Maegraith, T. Deegan, and E.S. Jones Suppression of malaria (P. Berghei) by milk British Medical Journal 2 4799 1952 1382 1384
67. S. Ramakrishnan, S. Prakash, S. Krishnaswami, and L. Singh Studies on P. berghei vincki and lipes, 1948. XIII. Effect of glucose, biotin, PABA and methionine on the course of blood induced infection in starving albino rats Indian Journal of Malariology 7 1953 225 228
68. S.P. Ramakrishnan, A.K. Krishnaswami, and C. Singh Studies on Plasmodium berghei n. sp. Vincke and Lips 1984. IX. Effect of milk diet on the course of blood-induced infection in albino rats Indian Journal of Malariology 7 1 1953 61 65
69. R.L. Jacobs Role of p-aminobenzoic acid in Plasmodium berghei infection in the mouse Experimental Parasitology 15 1964 213 225
70. R.S. Bray, and P.C. Garnham Effect of milk diet on P. cynomolgi infections in monkeys British Medical Journal 1 4821 1953 1200 1201
71. J. Greenberg, D.J. Taylor, and H.L. Trembley The effect of milk diets on the course of sporozoite-induced Plasmodium gallinaceum infections in chicks American Journal of Hygiene 60 2 1954 99 105
72. H. Keshavarz-Valian, N.E. Alger, and G.A. Boissonneault Effects of p-aminobenzoic acid methionine threonine and protein levels on susceptibility of mice to Plasmodium berghei Journal of Nutrition 115 12 1985 1613 1620
73. S. Ramakrishnan, V. Bhatnagar, S. Prakash, and B. Misra Effect of milk diet on Plasmodium gallinaceum infection in its vertebrate and invertebrate hosts Indian Journal of Malariology 7 1953 261 265
74. G.A. Kicska, L.-M. Ting, V.L. Schramm, and K. Kim Effect of dietary p-aminobenzoic acid on murine Plasmodium yoelii infection Journal of Infectious Diseases 188 11 2003 1776 1781
75. E.M. Al-Olayan, A.L. Beetsma, G.A. Butcher, R.E. Sinden, and H. Hurd Complete development of mosquito phases of the malaria parasite in vitro Science 295 5555 2002 677 679
76. W. Watkins, D. Sixsmith, J. Chulay, and H. Spencer Antagonism of sulfadoxine and pyrimethamine antimalarial activity in vitro by p-aminobenzoic acid, p-aminobenzoylglutamic acid and folic acid Molecular and Biochemical Parasitology 14 1 1985 55 61 10.1016/0166-6851(85)90105-7
77. P. Wang, N. Nirmalan, Q. Wang, P.F. Sims, and J.E. Hyde Genetic and metabolic analysis of folate salvage in the human malaria parasite Plasmodium falciparum Molecular and Biochemical Parasitology 135 1 2004 77 87 10.1016/j.molbiopara.2004.01.008
78. K.L. Olszewski, J.M. Morrisey, and D. Wilinski Host-parasite interactions revealed by Plasmodium falciparum metabolomics Cell Host & Microbe 5 2 2009 191 199
79. W. Asawamahasakda, and Y. Yuthavong The methionine synthesis cycle and salvage of methyltetrahydrofolate from host red cells in the malaria parasite (Plasmodium falciparum) Parasitology 107 1993 1 10
80. E. Nduati, A. Diriye, and S. Ommeh Effect of folate derivatives on the activity of antifolate drugs used against malaria and cancer Parasitology Research 102 6 2008 1227 1234
81. A.J.A. Wright, P.M. Finglas, and J.R. Dainty Differential kinetic behavior and distribution for pteroylglutamic acid and reduced folates: a revised hypothesis of the primary site of PteGlu metabolism in humans Journal of nutrition 135 3 2005 619 623
82. P. Wang, R.K. Brobey, T. Horii, P.F. Sims, and J.E. Hyde Utilization of exogenous folate in the human malaria parasite Plasmodium falciparum and its critical role in antifolate drug synergy Molecular Microbiology 32 6 1999 1254 1262
83. C.L. Krumdieck, K. Fukushima, T. Fukushima, T. Shiota, and J.C.E. Butterworth A long-term study of the excretion of folate and pterins in a human subject after ingestion of 14C folic acid with observations on the effect of diphenylhydantoin administration American Journal of Clinical Nutrition 31 1 1978 88 93
84. J.R. Suh, E.W. Oppenheim, S. Girgis, and P.J. Stover Purification and properties of a folate-catabolizing enzyme Journal of Biological Chemistry 275 45 2000 35646 35655
85. N.N. Odunukwe, L.A. Salako, C. Okany, and M.M. Ibrahim Serum ferritin and other haematological measurements in apparently healthy adults with malaria parasitaemia in Lagos Nigeria Tropical Medicine & International Health 5 8 2000 582 586
86. R.J. Stoltzfus, H.M. Chwaya, M. Albonico, K.J. Schulze, L. Savioli, and J.M. Tielsch Serum ferritin erythrocyte protoporphyrin and hemoglobin are valid indicators of iron status of school children in a malaria-holoendemic population Journal of Nutrition 127 2 1997 293 298
87. J.R. Suh, A.K. Herbig, and P.J. Stover New perspectives on folate catabolism Annual Review of Nutrition 21 2001 255 282
88. N. Lang-Unnasch, and A.D. Murphy Metabolic changes of the malaria parasite during the transition from the human to the mosquito host Annual Review of Microbiology 52 1998 562 590
89. M.S. Omar, W.E. Collins, and P.G. Contacos Gametocytocidal and sporontocidal effects of antimalarial drugs on malaria parasites Experimental Parasitology 36 1974 167 177
90. K.I. Barnes, F. Little, and A. Mabuza Increased gametocytemia after treatment: an early parasitological indicator of emerging sulfadoxine- pyrimethamine resistance in Falciparum malaria Journal of Infectious Diseases 197 11 2008 1605 1613
91. V.K. Bhasin, and W. Trager Gametocyte-forming and non-gametocyte-forming clones of Plasmodium falciparum American Journal of Tropical Medicine and Hygiene 33 4 1984 534 537
92. N.J. White The role of anti-malarial drugs in eliminating malaria Malaria Journal 7 Suppl. 1 2008 S8
93. C. Drakeley, C. Sutherland, J.T. Bousema, R.W. Sauerwein, and G.A.T. Targett The epidemiology of Plasmodium falciparum gametocytes: weapons of mass dispersion Trends in Parasitology 22 9 2006 424 430
94. A.H. Beavogui, A.A. Djimde, and A. Gregson Low infectivity of Plasmodium falciparum gametocytes to Anopheles gambiae following treatment with sulfadoxine-pyrimethamine in Mali International Journal for Parasitology 40 10 2010 1213 1220
95. A. Kone, M. van de Vegte-Bolmer, and R. Siebelink-Stoter Sulfadoxine-pyrimethamine impairs Plasmodium falciparum gametocyte infectivity and Anopheles mosquito survival International Journal for Parasitology 40 10 2010 1221 1228
96. R.H. Dadd Insect nutrition: current developments and metabolic implications Annual Review of Entomology 18 1973 381 420
97. S. Blatch, K.W. Meyer, and J.F. Harrison Effects of dietary folic acid level and symbiotic folate production on fitness and development in the fruit fly Drosophila melanogaster Fly 4 4 2010 312 319
98. K. Summers, A. Howells, and N. Pyliotis Biology of eye pigmentation in insects J. Treherne, Advances in insect physiology 1982 Academic Press London 119 166
99. D. Baker, T. Nolan, B. Fischer, A. Pinder, A. Crisanti, and S. Russell A comprehensive gene expression atlas of sex- and tissue-specificity in the malaria vector Anopheles gambiae BMC Genomics 12 1 2011 296
100. R.E. Sinden Molecular interactions between Plasmodium and its insect vectors Cellular Microbiology 4 11 2002 713 724
101. J.C. Beier Malaria parasite development in mosquitoes Annual Review of Entomology 43 1 1998 519 543
102. A.S. Perry, and S. Miller The essential role of folic acid and the effect of antimetabolites on growth and metamorphosis of housefly larvae Musca domestica L. Journal of Insect Physiology 11 1965 1277 1287
103. P. Wang, Q. Wang, P.F.G. Sims, and J.E. Hyde Characterisation of exogenous folate transport in Plasmodium falciparum Molecular and Biochemical Parasitology 154 1 2007 40 51
104. S.A. Desai, and R.L. Rosenberg Pore size of the malaria parasite's nutrient channel Proceedings of the National Academy of Sciences of the United States of America 94 5 1997 2045 2049
105. K.M. Massimine, L.T. Doan, and C.A. Atreya Toxoplasma gondii is capable of exogenous folate transport: a likely expansion of the BT1 family of transmembrane proteins Molecular and Biochemical Parasitology 144 1 2005 44 54
106. M.H. Saier A functional-phylogenetic classification system for transmembrane solute transporters Microbiology and Molecular Biology Reviews MMBR 64 2 2000 354 411
107. M. Ouellette, J. Drummelsmith, A. El Fadili, C. Kundig, D. Richard, and G. Roy Pterin transport and metabolism in Leishmania and related trypanosomatid parasites International Journal for Parasitology 32 4 2002 385 398
108. D. Richard, C. Kündig, and M. Ouellette A new type of high affinity folic acid transporter in the protozoan parasite Leishmania and deletion of its gene in methotrexate-resistant cells Journal of Biological Chemistry 277 33 2002 29460 29467
109. D. Richard, P. Leprohon, J. Drummelsmith, and M. Ouellette Growth phase regulation of the main folate transporter of Leishmania infantum and its role in methotrexate resistance Journal of Biological Chemistry 279 52 2004 54494 54501
110. Z. Bozdech, M. Llinas, B.L. Pulliam, E.D. Wong, J. Zhu, and J.L. DeRisi The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum PLoS Biology 1 1 2003 e5 10.1371/journal.pbio.0000005
111. E.P. Gianchandani, A.K. Chavali, and J.A. Papin The application of flux balance analysis in systems biology Wiley Interdisciplinary Reviews: Systems Biology and Medicine 2 3 2010 372 382 10.1002/wsbm.60
112. G. Plata, T.-L. Hsiao, K.L. Olszewski, M. Llinás, and D. Vitkup Reconstruction and flux-balance analysis of the Plasmodium falciparum metabolic network Molecular Systems Biology 6 2010 408
113. C. Huthmacher, A. Hoppe, S. Bulik, and H.-G. Holzhutter Antimalarial drug targets in Plasmodium falciparum predicted by stage-specific metabolic network analysis BMC Systems Biology 4 1 2010 120
114. R.A. Alberty, A. Cornish-Bowden, R.N. Goldberg, G.G. Hammes, K. Tipton, and H.V. Westerhoff Recommendations for terminology and databases for biochemical thermodynamics Biophysical Chemistry 155 23 2011 89 103
115. E. Noor, A. Bar-Even, A. Flamholz, Y. Lubling, D. Davidi, and R. Milo An integrated open framework for thermodynamics of reactions that combines accuracy and coverage Bioinformatics 28 15 2012 2037 2044
116. C.S. Henry, L.J. Broadbelt, and V. Hatzimanikatis Thermodynamics-based metabolic flux analysis Biophysical Journal 92 5 2007 1792 1805
117. T. Nakai, H. Mizutani, and I. Miyahara Three-dimensional structure of 4-amino-4-deoxychorismate lyase from Escherichia coli Journal of Biochemistry 128 1 2000 29 38
118. G. Spraggon, C. Kim, X. Nguyen-Huu, M.C. Yee, C. Yanofsky, and S.E. Mills The structures of anthranilate synthase of Serratia marcescens crystallized in the presence of (i) its substrates chorismate and glutamine and a product glutamate and (ii) its end-product inhibitor l-tryptophan Proceedings of the National Academy of Sciences of the United States of America 98 11 2001 6021 6026
119. S. Nair, B. Miller, and M. Barends Adaptive copy number evolution in malaria parasites PLoS Genetics 4 10 2008 e1000243
120. A. Heinberg, E. Siu, and C. Stern Direct evidence for the adaptive role of copy number variation on antifolate susceptibility in Plasmodium falciparum Molecular Microbiology 2013 10.1111/mmi.12162
121. G. Schoedon, U. Redweik, G. Frank, R.G. Cotton, and N. Blau Allosteric characteristics of GTP cyclohydrolase I from Escherichia coli European Journal of Biochemistry/FEBS 210 2 1992 561 568
122. P. Wang, Q. Wang, and Y. Yang Characterisation of the bifunctional dihydrofolate synthase-folylpolyglutamate synthase from Plasmodium falciparum; a potential novel target for antimalarial antifolate inhibition Molecular and Biochemical Parasitology 172 1 2010 41 51
123. I. Yeh, T. Hanekamp, S. Tsoka, P.D. Karp, and R.B. Altman Computational analysis of Plasmodium falciparum metabolism: organizing genomic information to facilitate drug discovery Genome Research 14 5 2004 917 924
124. D. Camara, C. Bisanz, and C. Barette Inhibition of p-aminobenzoate and folate syntheses in plants and apicomplexan parasites by natural product rubreserine Journal of Biological Chemistry 287 26 2012 22367 22376
125. K.T. Ziebart, S.M. Dixon, and B. Avila Targeting multiple chorismate-utilizing enzymes with a single inhibitor: validation of a three-stage design Journal of Medicinal Chemistry 53 9 2010 3718 3729
126. C. Kunding, A. Haimeur, D. Legare, B. Papadopoulou, and M. Ouellette Increased transport of pteridines compensates for mutations in the high affinity folate transporter and contributes to methotrexate resistance in the protozoan Leishmania tarentolae EMBO Journal 18 1999 2342 2351
127. K. Lanthaler, E. Bilsland, and P. Dobson Genome-wide assessment of the carriers involved in the cellular uptake of drugs: a model system in yeast BMC Biology 9 1 2011 70
128. A. Qiu, M. Jansen, and A. Sakaris Identification of an intestinal folate transporter and the molecular basis for hereditary folate malabsorption Cell 127 5 2006 917 928
129. R. Zhao, N. Diop-Bove, M. Visentin, and I.D. Goldman Mechanisms of membrane transport of folates into cells and across epithelia Annual Review of Nutrition 31 2011 177 201
130. O. Dar, M.S. Khan, and I. Adagu The potential use of methotrexate in the treatment of falciparum malaria: in vitro assays against sensitive and multidrug-resistan falciparum strains Japanese Journal of Infectious Diseases 61 2008 210 211
131. M. Imwong, B. Russell, and R. Suwanarusk Methotrexate is highly potent against pyrimethamine-resistant Plasmodium vivax Journal of Infectious Diseases 203 2 2011 207 210
132. A.C. Antony Folate receptors Annual Review of Nutrition 16 1996 501 521
133. A. Sowunmi, A.A. Adedeji, B.A. Fateye, and F.A. Fehintola Comparative effects of pyrimethamine-sulfadoxine with and without probenecid, on Plasmodium falciparum gametocytes in children with acute, uncomplicated malaria Annals of Tropical Medicine and Parasitology 98 8 2004 873 878
134. A. Sowunmi, F.A. Fehintola, and A.A. Adedeji Open randomized study of pyrimethamine-sulphadoxine vs. pyrimethamine-sulphadoxine plus probenecid for the treatment of uncomplicated Plasmodium falciparum malaria in children Tropical Medicine & International Health: TM & IH 9 5 2004 606 614
135. V. Masseno, S. Muriithi, and A. Nzila In vitro chemosensitization of Plasmodium falciparum to antimalarials by verapamil and probenecid Antimicrobial Agents and Chemotherapy 53 7 2009 3131 3134
136. A. Nzila, E. Mberu, and P. Bray Chemosensitization of Plasmodium falciparum by probenecid in vitro Antimicrobial Agents and Chemotherapy 47 2003 2108 2112
137. R. Tahar, and L.K. Basco Molecular epidemiology of malaria in Cameroon. XXVI. Twelve-year in vitro and molecular surveillance of pyrimethamine resistance and experimental studies to modulate pyrimethamine resistance American journal of Tropical Medicine and Hygiene 77 2 2007 221 227
138. J.L. Elliott, K.J. Saliba, and K. Kirk Transport of lactate and pyruvate in the intraerythrocytic malaria parasite Plasmodium falciparum Biochemical Journal 355 Pt 3 2001 733 739
139. W.G. Kuhr, C.J. van den Berg, and J. Korf In vivo identification and quantitative evaluation of carrier-mediated transport of lactate at the cellular level in the striatum of conscious, freely moving rats Journal of Cerebral Blood Flow and Metabolism 8 1988 848 856
140. K. Sopitthummakhun, C. Thongpanchang, T. Vilaivan, Y. Yuthavong, P. Chaiyen, and U. Leartsakulpanich Plasmodium serine hydroxymethyltransferase as a potential anti-malarial target: inhibition studies using improved methods for enzyme production and assay Malaria Journal 11 1 2012 194
141. B.D. Bennett, J. Yuan, E.H. Kimball, and J.D. Rabinowitz Absolute quantitation of intracellular metabolite concentrations by an isotope ratio-based approach Nature Protocols 3 8 2008 1299 1311
142. Y.K. Kwon, W. Lu, E. Melamud, N. Khanam, A. Bognar, and J.D. Rabinowitz A domino effect in antifolate drug action in Escherichia coli Nature Chemical Biology 4 10 2008 602 608
143. J. Yuan, B.D. Bennett, and J.D. Rabinowitz Kinetic flux profiling for quantitation of cellular metabolic fluxes Nature protocols 3 8 2008 1328 1340
144. C.B.N. IUPAC-IUB Nomenclature and symbols for folic acid and related compounds Pure and Applied Chemistry 59 6 1987 833 836
145. W. Kasekarn, R. Sirawaraporn, T. Chahomchuen, A.F. Cowman, and W. Sirawaraporn Molecular characterization of bifunctional hydroxymethyldihydropterin pyrophosphokinase-dihydropteroate synthase from Plasmodium falciparum Molecular and Biochemical Parasitology 137 1 2004 43 53
146. J. Krungkrai, Y. Yuthavong, and H.K. Webster High-performance liquid chromatographic assay for thymidylate synthase from the human malaria parasite, Plasmodium falciparum Journal of Chromatography 487 1989 51 59
147. W. Sirawaraporn, R. Sirawaraporn, A.F. Cowman, Y. Yuthavong, and D. Santi Heterologous expression of active thymidylate synthase-dihydrofolate reductase from Plasmodium falciparum Biochemistry 29 1990 10779 10785
148. M. Hekmat-Nejad, and P.K. Rathod Kinetics of Plasmodium falciparum thymidylate synthase: interactions with high-affinity metabolites of 5-fluoroorotate and D1694 Antimicrobial Agents and Chemotherapy 40 7 1996 1628 1632
149. J.M. Green, D.P. Ballou, and R.G. Matthews Examination of the role of methylenetetrahydrofolate reductase in incorporation of methyltetrahydrofolate into cellular metabolism FASEB Journal 2 1 1988 42 47
150. B.E. Maden Why methanopterin? Comparative bioenergetics of the reactions catalyzed by methylene tetrahydrofolate reductase and methylene tetrahydromethanopterin reductase Biochemical Society Transactions 24 1996 466S
151. J. Krungkrai, H.K. Webster, and Y. Yuthavong Characterization of cobalamin-dependent methionine synthase purified from the human malaria parasite, Plasmodium falciparum Parasitology Research 75 1989 512 517
152. A.S. Tibbetts, and D.R. Appling Compartmentalization of Mammalian folate-mediated one-carbon metabolism Annual Review of Nutrition 30 2010 57 81