Global Mass Spectrometry Based Metabolomics Profiling of Erythrocytes Infected with Plasmodium falciparum

PLoS ONE

Volumn 8, Issue 4, 2013, Pages

  Sana, Theodore R ^a   Gordon, D Benjamin ^a   Fischer, Steven M ^a   Tichy, Shane E ^a   Kitagawa, Norton ^a   Lai, Cindy ^a   Gosnell, William L ^b   Chang, Sandra P ^b  

^a AGILENT TECHNOLOGIES   (United States)

^b UNIVERSITY OF HAWAII   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHORISMIC ACID; SPHINGOLIPID;

AMINO ACID METABOLISM; ANALYTIC METHOD; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL DIFFERENTIATION; CITRIC ACID CYCLE; CONTROLLED STUDY; DATA ANALYSIS SOFTWARE; DATA MINING; ERYTHROCYTE; FATTY ACID METABOLISM; GLYCOLYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; MALARIA FALCIPARUM; METABOLOMICS; MULTIPLE REACTION MONITORING; NONHUMAN; NUCLEOTIDE METABOLISM; PROCESS OPTIMIZATION; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; UREA CYCLE; VALIDATION PROCESS;

ARGININE; CYCLIC ADP-RIBOSE; DATA MINING; DATABASES, FACTUAL; ERYTHROCYTES; GLYCOLYSIS; HUMANS; HYDROLYSIS; MALARIA, FALCIPARUM; MASS SPECTROMETRY; METABOLIC NETWORKS AND PATHWAYS; METABOLOME; METABOLOMICS; PHOSPHORYLATION; PLASMODIUM FALCIPARUM;

HOMO SAPIENS; PLASMODIUM FALCIPARUM;

EID: 84876060343     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0060840     Document Type: Article

References (57)

1. Programme WGM (2010) World Malaria Report 2010. Geneva: World Health Organization.
2. Phyo AP, Nkhoma S, Stepniewska K, Ashley EA, Nair S, et al. (2012) Emergence of artemisinin-resistant malaria on the western border of Thailand: a longitudinal study. Lancet.
3. Bloland PB (2001) Drug resistance in malaria. World Health Organization. WHO/CDS/CSR/DRS/2001.4 WHO/CDS/CSR/DRS/2001.4. 1-27 p.
4. Oliver SG, (1996) From DNA sequence to biological function. Nature 379: 597-600.
5. Fiehn O, Kopka J, Dormann P, Altmann T, Trethewey RN, et al. (2000) Metabolite profiling for plant functional genomics. Nat Biotechnol 18: 1157-1161.
6. Goodacre R, (2007) Metabolomics of a superorganism. J Nutr 137: 259S-266S.
7. Sana TR, Roark JC, Li X, Waddell K, Fischer SM, (2008) Molecular formula and METLIN Personal Metabolite Database matching applied to the identification of compounds generated by LC/TOF-MS. J Biomol Tech 19: 258-266.
8. Gardner M, Hall N, Fung E, White O, Berriman M, et al. (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498-511.
9. Hall N, Karras M, Raine J, Carlton J, Kooij T, et al. (2005) A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 307: 82-86.
10. Bozdech Z, Llinás M, Pulliam B, Wong E, Zhu J, et al. (2003) The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol 1: E5.
11. Foth B, Zhang N, Mok S, Preiser P, Bozdech Z, (2008) Quantitative protein expression profiling reveals extensive post-transcriptional regulation and post-translational modifications in schizont-stage malaria parasites. Genome Biol 9: R177.
12. Ginsburg H, (2006) Progress in in silico functional genomics: the malaria Metabolic Pathways database. Trends Parasitol 22: 238-240.
13. Kanehisa M, Goto S, (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28: 27-30.
14. Venter JC, Adams MD, Myers EW, Li PW, Mural RJ, et al. (2001) The sequence of the human genome. Science 291: 1304-1351.
15. Aurrecoechea C, Brestelli J, Brunk BP, Dommer J, Fischer S, et al. (2009) PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res 37: D539-543.
16. Sana TR, Waddell K, Fischer SM, (2008) A sample extraction and chromatographic strategy for increasing LC/MS detection coverage of the erythrocyte metabolome. J Chromatogr B Analyt Technol Biomed Life Sci 871: 314-321.
17. Pesek JJ, Matyska MT, Fischer SM, Sana TR, (2008) Analysis of hydrophilic metabolites by high-performance liquid chromatography-mass spectrometry using a silica hydride-based stationary phase. J Chromatogr A 1204: 48-55.
18. Pesek JJ, Matyska MT, Loo JA, Fischer SM, Sana TR, (2009) Analysis of hydrophilic metabolites in physiological fluids by HPLC-MS using a silica hydride-based stationary phase. J Sep Sci 32: 2200-2208.
19. Technologies A (2008) Agilent Fiehn GC/MS Metabolomics RTL Library.
20. Sana TR, Fischer S, Wohlgemuth G, Katrekar A, Jung KH, et al. (2010) Metabolomic and transcriptomic analysis of the rice response to the bacterial blight pathogen Xanthomonas oryzae pv. oryzae. Metabolomics 6: 451-465.
21. Trager W, Jensen JB, (1976) Human malaria parasites in continuous culture. Science 193: 673-675.
22. Palmer KL, Hui GS, Siddiqui WA, Palmer EL, (1982) A large-scale in vitro production system for Plasmodium falciparum. J Parasitol 68: 1180-1183.
23. Foth BJ, Zhang N, Chaal BK, Sze SK, Preiser PR, et al. (2011) Quantitative time-course profiling of parasite and host cell proteins in the human malaria parasite Plasmodium falciparum. Mol Cell Proteomics.
24. Jackson KE, Spielmann T, Hanssen E, Adisa A, Separovic F, et al. (2007) Selective permeabilization of the host cell membrane of Plasmodium falciparum-infected red blood cells with streptolysin O and equinatoxin II. Biochem J 403: 167-175.
25. Canales J, Fernández A, Rodrigues J, Ferreira R, Ribeiro J, et al. (2009) Hydrolysis of the phosphoanhydride linkage of cyclic ADP-ribose by the Mn(2+)-dependent ADP-ribose/CDP-alcohol pyrophosphatase. FEBS Lett 583: 1593-1598.
26. Fiehn O, Kopka J, Trethewey RN, Willmitzer L, (2000) Identification of uncommon plant metabolites based on calculation of elemental compositions using gas chromatography and quadrupole mass spectrometry. Anal Chem 72: 3573-3580.
27. Kind T, Wohlgemuth G, Lee dY, Lu Y, Palazoglu M, et al. (2009) FiehnLib: mass spectral and retention index libraries for metabolomics based on quadrupole and time-of-flight gas chromatography/mass spectrometry. Anal Chem 81: 10038-10048.
28. Hochberg Y, Benjamini Y, (1990) More powerful procedures for multiple significance testing. Stat Med 9: 811-818.
29. Tukey JW, (1949) Comparing individual means in the analysis of variance. Biometrics 5: 99-114.
30. Kind T, Fiehn O, (2006) Metabolomic database annotations via query of elemental compositions: mass accuracy is insufficient even at less than 1 ppm. BMC Bioinformatics 7: 234.
31. van Iersel MP, Pico AR, Kelder T, Gao J, Ho I, et al. (2010) The BridgeDb framework: standardized access to gene, protein and metabolite identifier mapping services. BMC Bioinformatics 11: 5.
32. Teng R, Junankar PR, Bubb WA, Rae C, Mercier P, et al. (2009) Metabolite profiling of the intraerythrocytic malaria parasite Plasmodium falciparum by (1)H NMR spectroscopy. NMR Biomed 22: 292-302.
33. Olszewski KL, Morrisey JM, Wilinski D, Burns JM, Vaidya AB, et al. (2009) Host-parasite interactions revealed by Plasmodium falciparum metabolomics. Cell Host Microbe 5: 191-199.
34. Wishart DS, Knox C, Guo AC, Eisner R, Young N, et al. (2009) HMDB: a knowledgebase for the human metabolome. Nucleic Acids Res 37: D603-610.
35. Guse AH, (2000) Cyclic ADP-ribose. J Mol Med 78: 26-35.
36. Jones ML, Cottingham C, Rayner JC, (2009) Effects of calcium signaling on Plasmodium falciparum erythrocyte invasion and post-translational modification of gliding-associated protein 45 (PfGAP45). Mol Biochem Parasitol 168: 55-62.
37. Olszewski KL, Morrisey JM, Wilinski D, Burns JM, Vaidya AB, et al. (2009) Host-parasite interactions revealed by Plasmodium falciparum metabolomics. Cell Host Microbe 5: 191-199.
38. Sana T, Fischer S, Tichy S (2010) An LC/MS Metabolomics Discovery Workflow for Malaria-Infected Red Blood Cells Using Mass Profiler Professional Software and LC-Triple Quadrupole MRM Confirmation. Santa Clara, CA: Agilent Technologies, Inc.
39. Olszewski KL, Mather MW, Morrisey JM, Garcia BA, Vaidya AB, et al. (2010) Branched tricarboxylic acid metabolism in Plasmodium falciparum. Nature 466: 774-778.
40. Olszewski KL, Llinás M (2010) Central carbon metabolism of Plasmodium parasites. Mol Biochem Parasitol.
41. Roth E (1990) Plasmodium falciparum carbohydrate metabolism: a connection between host cell and parasite. Blood Cells 16: 453-460; discussion 461-456.
42. Kanaani J, Ginsburg H, (1991) Transport of lactate in Plasmodium falciparum-infected human erythrocytes. J Cell Physiol 149: 469-476.
43. Huang da W, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
44. Friend SH, Dai H, (2006) Accelerating drug discovery: Open source cancer cell biology? Cancer Cell 10: 349-351.
45. Bowen BP, Fischer CR, Baran R, Banfield JF, Northen T, (2011) Improved genome annotation through untargeted detection of pathway-specific metabolites. BMC Genomics 12Suppl 1: S6.
46. Yeh I, Hanekamp T, Tsoka S, Karp PD, Altman RB, (2004) Computational analysis of Plasmodium falciparum metabolism: organizing genomic information to facilitate drug discovery. Genome Res 14: 917-924.
47. Roberts CW, Roberts F, Lyons RE, Kirisits MJ, Mui EJ, et al. (2002) The shikimate pathway and its branches in apicomplexan parasites. J Infect Dis 185Suppl 1: S25-36.
48. Elford BC, Haynes JD, Chulay JD, Wilson RJ, (1985) Selective stage-specific changes in the permeability to small hydrophilic solutes of human erythrocytes infected with Plasmodium falciparum. Mol Biochem Parasitol 16: 43-60.
49. Downie MJ, Kirk K, Mamoun CB, (2008) Purine salvage pathways in the intraerythrocytic malaria parasite Plasmodium falciparum. Eukaryot Cell 7: 1231-1237.
50. Gowda DC, Davidson EA, (1999) Protein glycosylation in the malaria parasite. Parasitol Today 15: 147-152.
51. Takasawa S, Tohgo A, Noguchi N, Koguma T, Nata K, et al. (1993) Synthesis and hydrolysis of cyclic ADP-ribose by human leukocyte antigen CD38 and inhibition of the hydrolysis by ATP. J Biol Chem 268: 26052-26054.
52. Currie KP, Swann K, Galione A, Scott RH, (1992) Activation of Ca(2+)-dependent currents in cultured rat dorsal root ganglion neurones by a sperm factor and cyclic ADP-ribose. Mol Biol Cell 3: 1415-1425.
53. Bailey VC, Sethi JK, Fortt SM, Galione A, Potter BV, (1997) 7-Deaza cyclic adenosine 5′-diphosphate ribose: first example of a Ca(2+)-mobilizing partial agonist related to cyclic adenosine 5′-diphosphate ribose. Chem Biol 4: 51-61.
54. Jones M, Cottingham C, Rayner J, (2009) Effects of calcium signaling on Plasmodium falciparum erythrocyte invasion and post-translational modification of gliding-associated protein 45 (PfGAP45). Mol Biochem Parasitol 168: 55-62.
55. Galione A, (1992) Ca(2+)-induced Ca2+ release and its modulation by cyclic ADP-ribose. Trends Pharmacol Sci 13: 304-306.
56. Lakshmanan V, Rhee KY, Wang W, Yu Y, Khafizov K, et al. (2012) Metabolomic analysis of patient plasma yields evidence of plant-like α-linolenic acid metabolism in Plasmodium falciparum. J Infect Dis 206: 238-248.
57. de Carvalho LP, Zhao H, Dickinson CE, Arango NM, Lima CD, et al. (2010) Activity-based metabolomic profiling of enzymatic function: identification of Rv1248c as a mycobacterial 2-hydroxy-3-oxoadipate synthase. Chem Biol 17: 323-332.