Phosphoenolpyruvate Carboxylase Identified as a Key Enzyme in Erythrocytic Plasmodium falciparum Carbon Metabolism

PLoS Pathogens

Volumn 10, Issue 1, 2014, Pages

  Storm, Janet ^a,e   Sethia, Sonal ^a   Blackburn, Gavin J ^b   Chokkathukalam, Achuthanunni ^c   Watson, David G ^b   Breitling, Rainer ^d   Coombs, Graham H ^b   Müller, Sylke ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF STRATHCLYDE   (United Kingdom)

^c UNIVERSITY OF GLASGOW   (United Kingdom)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

^e LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYLIC ACID; PHOSPHOENOLPYRUVATE CARBOXYLASE; PROTOZOAL PROTEIN;

ANTAGONISTS AND INHIBITORS; CITRIC ACID CYCLE; ENZYMOLOGY; ERYTHROCYTE; GENETICS; GENOME; HUMAN; MALARIA, FALCIPARUM; METABOLISM; MITOCHONDRION; PENTOSE PHOSPHATE CYCLE; PHYSIOLOGY; PLASMODIUM FALCIPARUM; RADIOGRAPHY;

ACIDS, ACYCLIC; CITRIC ACID CYCLE; ERYTHROCYTES; GENOME, PROTOZOAN; HUMANS; MALARIA, FALCIPARUM; MITOCHONDRIA; PENTOSE PHOSPHATE PATHWAY; PHOSPHOENOLPYRUVATE CARBOXYLASE; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS;

EID: 84893809802     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003876     Document Type: Article

References (63)

1. WHO, (2012) World Malaria Report 2012, World Health Organisation, Geneva, Switzerland, 59.
2. Hay SI, Guerra CA, Gething PW, Patil AP, Tatem AJ, et al. (2009) A world malaria map: Plasmodium falciparum endemicity in 2007. PLoS Med 6: e1000048.
3. MacRae JI, Dixon MW, Dearnley MK, Chua HH, Chambers JM, et al. (2013) Mitochondrial metabolism of sexual and asexual blood stages of the malaria parasite Plasmodium falciparum. BMC Biol 11: 67.
4. Foth BJ, Stimmler LM, Handman E, Crabb BS, Hodder AN, et al. (2005) The malaria parasite Plasmodium falciparum has only one pyruvate dehydrogenase complex, which is located in the apicoplast. Mol Microbiol 55: 39-53.
5. Pei Y, Tarun AS, Vaughan AM, Herman RW, Soliman JM, et al. (2010) Plasmodium pyruvate dehydrogenase activity is only essential for the parasite's progression from liver infection to blood infection. Mol Microbiol 75: 957-971.
6. Cobbold SA, Vaughan AM, Lewis IA, Painter HJ, Camargo N, et al. (2013) Kinetic flux profiling elucidates two independent acetyl-CoA biosynthetic pathways in Plasmodium falciparum. J Biol Chem Oct 25[Epub ahead of print].
7. MacRae JI, Sheiner L, Nahid A, Tonkin C, Striepen B, et al. (2012) Mitochondrial metabolism of glucose and glutamine is required for intracellular growth of Toxoplasma gondii. Cell Host Microbe 12: 682-692.
8. Olszewski KL, Mather MW, Morrisey JM, Garcia BA, Vaidya AB, et al. (2010) Branched tricarboxylic acid metabolism in Plasmodium falciparum. Nature 466: 774-778.
9. Olszewski KL, Mather MW, Morrisey JM, Garcia BA, Vaidya AB, et al. (2013) Retraction: Branched tricarboxylic acid metabolism in Plasmodium falciparum. Nature 497: 652.
10. Sherman IW, Ting IP, (1966) Carbon dioxide fixation in malaria (Plasmodium lophurae). Nature 212: 1387-1388.
11. Sherman IW, Ting IP, (1968) Carbon dioxide fixation in malaria. II. Plasmodium knowlesi (monkey malaria). Comp Biochem Physiol 24: 639-642.
12. Nagarajan K, (1968) Metabolism of Plasmodium berghei. 3. Carbon dioxide fixation and role of pyruvate and dicarboxylic acids. Exp Parasitol 22: 33-42.
13. Trager W, Jensen JB, (1976) Human malaria parasites in continuous culture. Science 193: 673-675.
14. McDaniel HG, Siu PM, (1972) Purification and characterization of phosphoenolpyruvate carboxylase from Plasmodium berghei. J Bacteriol 109: 385-390.
15. Blum JJ, Ginsburg H, (1984) Absence of alpha-ketoglutarate dehydrogenase activity and presence of CO2-fixing activity in Plasmodium falciparum grown in vitro in human erythrocytes. J Protozool 31: 167-169.
16. Hayward RE, (2000) Plasmodium falciparum phosphoenolpyruvate carboxykinase is developmentally regulated in gametocytes. Mol Biochem Parasitol 107: 227-240.
17. Krungkrai SR, Suraveratum N, Rochanakij S, Krungkrai J, (2001) Characterisation of carbonic anhydrase in Plasmodium falciparum. Int J Parasitol 31: 661-668.
18. Izui K, Matsumura H, Furumoto T, Kai Y, (2004) Phosphoenolpyruvate carboxylase: a new era of structural biology. Annu Rev Plant Biol 55: 69-84.
19. O'Leary B, Park J, Plaxton WC, (2011) The remarkable diversity of plant PEPC (phosphoenolpyruvate carboxylase): recent insights into the physiological functions and post-translational controls of non-photosynthetic PEPCs. Biochem J 436: 15-34.
20. West-Eberhard MJ, Smith JA, Winter K, (2011) Plant science. Photosynthesis, reorganized. Science 332: 311-312.
21. Maier AG, Braks JA, Waters AP, Cowman AF, (2006) Negative selection using yeast cytosine deaminase/uracil phosphoribosyl transferase in Plasmodium falciparum for targeted gene deletion by double crossover recombination. Mol Biochem Parasitol 150: 118-121.
22. Peng Y, Cai J, Wang W, Su B, (2012) Multiple inter-kingdom horizontal gene transfers in the evolution of the phosphoenolpyruvate carboxylase gene family. PLoS One 7: e51159.
23. Svensson P, Bläsing OE, Westhoff P, (2003) Evolution of C4 phosphoenolpyruvate carboxylase. Arch Biochem Biophys 414: 180-188.
24. Westhoff P, Gowik U, (2004) Evolution of c4 phosphoenolpyruvate carboxylase. Genes and proteins: a case study with the genus Flaveria. Ann Bot 93: 13-23.
25. Treeck M, Sanders JL, Elias JE, Boothroyd JC, (2011) The phosphoproteomes of Plasmodium falciparum and Toxoplasma gondii reveal unusual adaptations within and beyond the parasites' boundaries. Cell Host Microbe 10: 410-419.
26. Janski AM, Cornell NW, (1981) Inhibition by cycloserine of mitochondrial and cytosolic aspartate aminotransferase in isolated rat hepatocytes. Biochem J 194: 1027-1030.
27. Gujjar R, El Mazouni F, White KL, White J, Creason S, et al. (2011) Lead optimization of aryl and aralkyl amine-based triazolopyrimidine inhibitors of Plasmodium falciparum dihydroorotate dehydrogenase with antimalarial activity in mice. J Med Chem 54: 3935-3949.
28. Vaidya AB, Mather MW, (2009) Mitochondrial evolution and functions in malaria parasites. Annu Rev Microbiol 63: 249-267.
29. Esser L, Quinn B, Li YF, Zhang M, Elberry M, et al. (2004) Crystallographic studies of quinol oxidation site inhibitors: a modified classification of inhibitors for the cytochrome bc(1) complex. J Mol Biol 341: 281-302.
30. Barton V, Fisher N, Biagini GA, Ward SA, O'Neill PM, (2010) Inhibiting Plasmodium cytochrome bc1: a complex issue. Curr Opin Chem Biol 14: 440-446.
31. Ribaut C, Berry A, Chevalley S, Reybier K, Morlais I, et al. (2008) Concentration and purification by magnetic separation of the erythrocytic stages of all human Plasmodium species. Malar J 7: 45.
32. Jenkins CL, (1989) Effects of the phosphoenolpyruvate carboxylase inhibitor 3,3-dichloro-2-(dihydroxyphosphinoylmethyl)propenoate on photosynthesis: C(4) selectivity and studies on C(4) photosynthesis. Plant Physiol 89: 1231-1237.
33. Gardner MJ, Hall N, Fung E, White O, Berriman M, et al. (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498-511.
34. Gibala MJ, Young ME, Taegtmeyer H, (2000) Anaplerosis of the citric acid cycle: role in energy metabolism of heart and skeletal muscle. Acta Physiol Scand 168: 657-665.
35. Jitrapakdee S, Vidal-Puig A, Wallace JC, (2006) Anaplerotic roles of pyruvate carboxylase in mammalian tissues. Cell Mol Life Sci 63: 843-854.
36. Olszewski KL, Llinás M, (2011) Central carbon metabolism of Plasmodium parasites. Mol Biochem Parasitol 175: 95-103.
37. García-Alles LF, Erni B, (2002) Synthesis of phosphoenol pyruvate (PEP) analogues and evaluation as inhibitors of PEP-utilizing enzymes. Eur J Biochem 269: 3226-3236.
38. Izui K, Matsuda Y, Kameshita I, Katsuki H, Woods AE, (1983) Phosphoenolpyruvate carboxylase of Escherichia coli. Inhibition by various analogs and homologs of phosphoenolpyruvate. J Biochem 94: 1789-1795.
39. Bulusu V, Jayaraman V, Balaram H, (2011) Metabolic fate of fumarate, a side product of the purine salvage pathway in the intraerythrocytic stages of Plasmodium falciparum. J Biol Chem 286: 9236-9245.
40. Tanaka KR, Valentine WN, (1961) Fumarase activity of human leukocytes and erythrocytes. Blood 17: 328-333.
41. Simpson RJ, Brindle KM, Campbell ID, (1982) Spin ECHO proton NMR studies of the metabolism of malate and fumarate in human erythrocytes. Dependence on free NAD levels. Biochim Biophys Acta 721: 191-200.
42. Tripathi AK, Desai PV, Pradhan A, Khan SI, Avery MA, et al. (2004) An alpha-proteobacterial type malate dehydrogenase may complement LDH function in Plasmodium falciparum. Cloning and biochemical characterization of the enzyme. Eur J Biochem 271: 3488-3502.
43. Nozawa A, Fujimoto R, Matsuoka H, Tsuboi T, Tozawa Y, (2011) Cell-free synthesis, reconstitution, and characterization of a mitochondrial dicarboxylate-tricarboxylate carrier of Plasmodium falciparum. Biochem Biophys Res Commun 414: 612-617.
44. van Dooren GG, Stimmler LM, McFadden GI, (2006) Metabolic maps and functions of the Plasmodium mitochondrion. FEMS Microbiol Rev 30: 596-630.
45. Wrenger C, Müller S, (2003) Isocitrate dehydrogenase of Plasmodium falciparum. Eur J Biochem 270: 1775-1783.
46. Lambros C, Vanderberg JP, (1979) Synchronization of Plasmodium falciparum erythrocytic stages in culture. J Parasitol 65: 418-420.
47. Umlas J, Fallon JN, (1971) New thick-film technique for malaria diagnosis. Use of saponin stromatolytic solution for lysis. Am J Trop Med Hyg 20: 527-529.
48. Wu Y, Sifri CD, Lei HH, Su XZ, Wellems TE, (1995) Transfection of Plasmodium falciparum within human red blood cells. Proc Natl Acad Sci USA 92: 973-977.
49. Kirkman LA, Su XZ, Wellems TE, (1996) Plasmodium falciparum: isolation of large numbers of parasite clones from infected blood samples. Exp Parasitol 83: 147-149.
50. Günther S, Wallace L, Patzewitz EM, McMillan PJ, Storm J, et al. (2007) Apicoplast lipoic acid protein ligase B is not essential for Plasmodium falciparum. PLoS Pathog 3: e189.
51. Desjardins RE, Canfield CJ, Haynes JD, Chulay JD, (1979) Quantitative assessment of antimalarial activity in vitro by a semiautomated microdilution technique. Antimicrob Agents Chemother 16: 710-718.
52. De Souza DP, Saunders EC, McConville MJ, Likić VA, (2006) Progressive peak clustering in GC-MS metabolomic experiments applied to Leishmania parasites. Bioinformatics 22: 1391-1396.
53. Trang DT, Huy NT, Kariu T, Tajima K, Kamei K, (2004) One-step concentration of malarial parasite-infected red blood cells and removal of contaminating white blood cells. Malar J 3: 7.
54. Ahn SY, Shin MY, Kim YA, Yoo JA, Kwak DH, et al. (2008) Magnetic separation: a highly effective method for synchronization of cultured erythrocytic Plasmodium falciparum. Parasitol Res 102: 1195-1200.
55. Tautenhahn R, Böttcher C, Neumann S, (2008) Highly sensitive feature detection for high resolution LC/MS. BMC Bioinformatics 9: 504.
56. Scheltema RA, Jankevics A, Jansen RC, Swertz MA, Breitling R, (2011) PeakML/mzMatch: a file format, Java library, R library, and tool-chain for mass spectrometry data analysis. Anal Chem 83: 2786-2793.
57. Jankevics A, Merlo ME, De Vries M, Vonk RJ, Takano E, et al. (2012) Separating the wheat from the chaff: a prioritisation pipeline for the analysis of metabolomics datasets. Metabolomics 8: 29-36.
58. Chokkathukalam A, Jankevics A, Creek DJ, Achcar F, Barrett MP, et al. (2013) mzMatch-ISO: an R tool for the annotation and relative quantification of isotope-labelled mass spectrometry data. Bioinformatics Oxford England 29: 281-283.
59. Zhang Y, (2008) I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 23 9: 40.
60. Roy A, Kucukural A, Zhang Y, (2010) I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 5: 725-738.
61. Matsumura H, Xie Y, Shirakata S, Inoue T, Yoshinaga T, et al. (2002) Crystal structures of C4 form maize and quaternary complex of E. coli phosphoenolpyruvate carboxylases. Structure 10: 1721-1730.
62. Dharmarajan L, Kraszewski JL, Mukhopadhyay B, Dunten PW, (2011) Structure of an archaeal-type phosphoenolpyruvate carboxylase sensitive to inhibition by aspartate. Proteins 79: 1820-1829.
63. Guex N, Peitsch MC, (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18: 2714-2723.