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The potential of mass spectrometry for the global profiling of parasite metabolomes

Published online by Cambridge University Press:  22 December 2009

D. G. WATSON
D. G. WATSON*
Affiliation:
Strathclyde Institute of Pharmacy and Biomedical Sciences, 27, Taylor Street, Glasgow G4 0NR, UK
*
*Tel: +441415482651. Fax: +441415522562. E-mail: d.g.watson@strath.ac.uk
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Summary

The strengths and limitations of existing mass spectrometry methods for metabolite detection and identification are discussed. A brief review is made of the methods available for quenching and extraction of cells or organisms prior to instrumental analysis. The techniques available for carrying out mass spectrometry-based profiling of metabolomes are discussed using the analysis of extracts from trypanosomes to illustrate various points regarding methods of separation and mass spectrometric analysis. The advantages of hydrophilic interaction chromatography (HILIC) for the analysis of polar metabolites are discussed. The challenges of data processing are outlined and illustrated using the example of ThermoFisher's Sieve software. The existing literature on applications of mass spectrometry to the profiling of parasite metabolomes is reviewed.

Keywords

TrypanosomesmetabolomicsOrbitraphydrophilic interaction chromatographyextractionGC-MS
Type
Research Article
Information
Parasitology , Volume 137 , Special Issue 9: Insights into the metabolomes of parasites , August 2010 , pp. 1409 - 1423
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Amantonico, A., Urban, P. L. and Zenobi, R. (2009). Facile analysis of metabolites by capillary electrophoresis coupled to matrix-assisted laser desorption/ionization mass spectrometry using target plates with polysilazane nanocoating and grooves. Analyst 134, 1536–1540.Google Scholar
Ariyanayagam, M. R., Oza, S. L., Mehlert, A. and Fairlamb, A. H. (2003). Bis(glutathionyl) spermine and other novel trypanothione analogues in Trypanosoma cruzi. Journal of Biological Chemistry 278, 27612–27619.Google Scholar
Baidoo, E. E. K., Benket, P. I., Neususs, C., Pelzing, M., Kruppa, G., Leary, J. A. and Keasling, J. D. (2008). Capillary electrophoresis-Fourier transform ion cyclotron resonance mass spectrometry for the identification of cationic metabolites via a pH-mediated stacking-transient isotachophoretic method. Analytical Chemistry 80, 3112–3122.Google Scholar
Boibessot, I., Turner, C. M. R., Watson, D. G., Goldie, E., Connel, G., Mcintosh, A., Grant, M. H. and Skellern, G. G. (2002). Metabolism and distribution of phenanthridine trypanocides in Trypanosoma brucei. Acta Tropica 84, 219–228.Google Scholar
Breitling, R., Ritchie, S., Goodenowe, D., Stewart, M. L. and Barrett, M. P. (2006). Ab initio prediction of metabolic networks using Fourier transform mass spectrometry data. Metabolomics 2, 155–164.Google Scholar
Bruce, S. J., Tavazzi, I., Parisod, V., Rezzi, S., Kochhar, S. and Guy, P. A. (2009). Investigation of human blood plasma sample preparation for performing metabolomics using ultrahigh performance liquid chromatography/mass spectrometry. Analytical Chemistry 81, 3285–3296.Google Scholar
Callahan, D. L., Souza, D., Bacic, A. and Roessner, U. (2009). Profiling of polar metabolites in biological extracts using diamond hydride-based aqueous normal phase chromatography. Journal of Separation Science 32, 2273–2280.Google Scholar
Chace, D. H., Kalas, T. A. and Naylor, E. W. (2003). Use of tandem mass spectrometry for multianalyte screening of dried blood specimens from newborns. Clinical Chemistry 49, 1797–1817.Google Scholar
Couto, A. S., Caffaro, C., Uhrig, M. L., Kimura, E., Peres, V. J., Merino, E. F., Katzin, A. M., Nishioka, M., Nonami, H. and Erra-Balsells, R. (2004). Glycosphingolipids in Plasmodium falciparum – presence of an active glucosylceramide synthase. European Journal of Biochemistry 271, 2204–2214.Google Scholar
De Souza, D. P., Saunders, E. C., McConville, M. J. and Likic, V. A. (2006). Progressive peak clustering in GC-MS metabolomic experiments applied to Leishmania parasites. Bioinformatics 22, 1391–1396.CrossRefGoogle ScholarPubMed
Demirev, P. A., Feldman, A. B., Kongkasuriyachai, D., Scholl, P., Sullivan, D. and Kumar, N. (2002). Detection of malaria parasites in blood by laser desorption mass spectrometry. Analytical Chemistry 74, 3262–3266.Google Scholar
Desmet, G. (2008). Comparison techniques for HPLC column performance. LC-GC Europe 21, 310–320.Google Scholar
Dunn, W. B., Broadhurst, D., Brown, M., Baker, P. N., Redman, C. W. G., Kenny, L. C. and Kell, D. B. (2008). Metabolic profiling of serum using Ultra Performance Liquid Chromatography and the LTQ-Orbitrap mass spectrometry system. Journal of Chromatography B-Analytical Technologies in the Biomedical and Life Sciences 871, 288–298.Google Scholar
Ewald, J. C., Heux, S. and Zamboni, N. (2009). High-throughput quantitative metabolomics: workflow for cultivation, quenching, and analysis of yeast in a multiwell format. Analytical Chemistry 81, 3623–3629.Google Scholar
Frank, R. and Hargreaves, R. (2003). Clinical biomarkers in drug discovery and development. Nature Reviews Drug Discovery 2, 566–580.Google Scholar
Gika, H. G., Theodoridis, G., Extance, J., Edge, A. M. and Wilson, I. D. (2008 a). High temperature-ultra performance liquid chromatography-mass spectrometry for the metabonomic analysis of Zucker rat urine. Journal of Chromatography B-Analytical Technologies in the Biomedical and Life Sciences 871, 279–287.Google Scholar
Gika, H. G., Theodoridis, G. A. and Wilson, I. D. (2008 b). Hydrophilic interaction and reversed-phase ultra-performance liquid chromatography TOF-MS for metabonomic analysis of Zucker rat urine. Journal of Separation Science 31, 1598–1608.Google Scholar
Guler, J. L., Kriegova, E., Smith, T. K., Lukes, J. and Englund, P. T. (2008). Mitochondrial fatty acid synthesis is required for normal mitochondrial morphology and function in Trypanosoma brucei. Molecular Microbiology 67, 1125–1142.Google Scholar
Hänscheid, T., Egan, T. J. & Grobusch, M. P. (2007). Haemozoin: from melatonin pigment to drug target, diagnostic tool, and immune modulator Lancet Infectious Diseases 7, 675–685.Google Scholar
Houston, K. M. and Harnett, W. (2004). Structure and synthesis of nematode phosphorylcholine-containing glycoconjugates. Parasitology 129, 655–661.Google Scholar
Hu, Q. Z., Noll, R. J., Li, H. Y., Makarov, A., Hardman, M. and Cooks, R. G. (2005). The Orbitrap: a new mass spectrometer. Journal of Mass Spectrometry 40, 430–443.Google Scholar
Kaiser, A., Gottwald, A., Wiersch, C., Lindenthal, B., Maier, W. and Seitz, H. M. (2001). Effect of drugs inhibiting spermidine biosynthesis and metabolism on the in vitro development of Plasmodium falciparum. Parasitology Research 87, 963–972.Google Scholar
Kamleh, A., Barrett, M. P., Wildridge, D., Burchmore, R. J. S., Scheltema, R. A. and Watson, D. G. (2008). Metabolomic profiling using Orbitrap Fourier transform mass spectrometry with hydrophilic interaction chromatography: a method with wide applicability to analysis of biomolecules. Rapid Communications in Mass Spectrometry 22, 1912–1918.Google Scholar
Kamleh, M. A., Dow, J. A. T. and Watson, D. G. (2009). Applications of mass spectrometry in metabolomic studies of animal model and invertebrate systems. Briefings in Functional Genomics and Proteomics 8, 28–48.Google Scholar
Landoni, M., Duschak, V. G., Peres, V. J., Nonami, H., Erra-Balsells, R., Katzin, A. M. and Couto, A. S. (2007). Plasmodium falciparum biosynthesizes sulfoglycosphingolipids. Molecular and Biochemical Parasitology 154, 22–29.Google Scholar
Lapainis, T., Rubakhin, S. S. and Sweedler, J. V. (2009). Capillary electrophoresis with Electrospray Ionization Mass Spectrometric Detection for single-cell metabolomics. Analytical Chemistry 81, 5858–5864.Google Scholar
Link, H., Anselment, B. and Weuster-Botz, D. (2008). Leakage of adenylates during cold methanol/glycerol quenching of Escherichia coli. Metabolomics 4, 240–247.Google Scholar
Makarov, A. (1999). ‘Mass Spectrometer’, in U.S.Patent Ed. 5, p. 346.Google Scholar
Makarov, A., Denisov, E., Lange, O. and Horning, S. (2006). Dynamic range of mass accuracy in LTQ Orbitrap hybrid mass spectrometer. Journal of the American Society for Mass Spectrometry 17, 977–982.CrossRefGoogle ScholarPubMed
Michopoulos, F., Lai, L., Gika, H., Theodoridis, G. and Wilson, I. (2009). UPLC-MS-based analysis of human plasma for metabonomics using solvent precipitation or solid phase extraction. Journal of Proteome Research 8, 2114–2121.Google Scholar
Morelle, K. C., Chirat, F., Faid, V. and Michalski, J.-C. (2006). The use of mass spectrometry for the proteomic analysis of glycosylation. Proteomics 6, 3993–4015.Google Scholar
Musilova, J., Sedlacek, V., Kucera, I. and Glatz, Z. (2009). Capillary zone electrophoresis with field enhanced sample stacking as a tool for targeted metabolome analysis of adenine nucleotides and coenzymes in Paracoccus denitrificans. Journal of Separation Science 32, 2416–2420.Google Scholar
Olszewski, K. L., Morrisey, J. M., Wilinski, D., Burns, J. M., Vaidya, A. B., Rabinowitz, J. D. and Linas, M. (2009). Host-parasite interactions revealed by Plasmodium falciparum metabolomics. Cell Host and Microbe 5, 191–199.Google Scholar
Pesek, J. J., Matyska, M. T., Fischer, S. M. and Sana, T. R. (2008). Analysis of hydrophilic metabolites by high-performance liquid chromatography-mass spectrometry using a silica hydride-based stationary phase. Journal of Chromatography A 1204, 48–55.Google Scholar
Pesek, J. J., Matyska, M. T., Loo, J. A., Fischer, S. M. and Sana, T. R. (2009). Analysis of hydrophilic metabolites in physiological fluids by HPLC-MS using a silica hydride-based stationary phase. Journal of Separation Science 32, 2200–2208.Google Scholar
Plumb, R. S., Granger, J. H., Stumpf, C. L., Johnson, K. A., Smith, B. W., Gaulitz, S., Wilson, I. D. and Castro-Perez, J. (2005). A rapid screening approach to metabonomics using UPLC and oa-TOF mass spectrometry: application to age, gender and diurnal variation in normal/Zucker obese rats and black, white and nude mice. Analyst 130, 844–849.Google Scholar
Ralton, J. E., Naderer, T., Piraino, H. L., Bashtannyk, T. A., Callaghan, J. M. and McConville, M. J. (2003). Evidence that intracellular beta 1–2 mannan is a virulence factor in Leishmania parasites. Journal of Biological Chemistry 278, 40757–40763.Google Scholar
Ritter, J. B., Genzel, Y. and Reichl, U. (2008). Simultaneous extraction of several metabolites of energy metabolism and related substances in mammalian cells: Optimization using experimental design. Analytical Biochemistry 373, 349–369.Google Scholar
Robinson, M. D., De Souza, D. P., Keen, W. W., Saunders, E. C., McConville, M. J., Speed, T. P. and Likic, V. A. (2007). A dynamic programming approach for the alignment of signal peaks in multiple gas chromatography-mass spectrometry experiments. Bmc Bioinformatics 8, 419.CrossRefGoogle ScholarPubMed
Robijn, M. L. M., Planken, J., Kornelis, D., Hokke, C. H. and Deelder, A. M. (2008). Mass spectrometric detection of urinary oligosaccharides as markers of Schistosoma mansoni infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 102, 79–83.Google Scholar
Sellick, C. A., Hansen, R., Maqsood, A. R., Dunn, W. B., Stephens, G. M., Goodacre, R. and Dickson, A. J. (2009). Effective quenching processes for physiologically valid metabolite profiling of suspension cultured mammalian cells. Analytical Chemistry 81, 174–183.Google Scholar
Scheltema, R. A., Kamleh, A., Wildridge, D., Ebikeme, C., Watson, D. G., Barrett, M. R., Jansen, R. C. and Breitling, R. (2008). Increasing the mass accuracy of high-resolution LC-MS data using background ions – a case study on the LTQ-Orbitrap. Proteomics 8, 4647–4656.Google Scholar
Teng, R., Junankar, P. R., Bubb, W. A., Rae, C., Mercier, P. and Kirk, K. (2009). Metabolite profiling of the intraerythrocytic malaria parasite Plasmodium falciparum by (1)H NMR spectroscopy. NMR Biomedicine, 22, 292–302.Google Scholar
Ting, L. M., Shi, W. X., Lewandowicz, A., Singh, V., Mwakingwe, A., Birck, M. R., Ringia, E. A. T., Bench, G., Madrid, D. C., Tyler, P. C., Evans, G. B., Furneaux, R. H., Schramm, V. L. and Kim, K. (2005). Targeting a novel Plasmodium falciparum purine recycling pathway with specific immucillins. Journal of Biological Chemistry 280, 9547–9554.Google Scholar
Tonhosolo, R., D'alexandri, F. L., De Rosso, V. V., Gazarini, M. L., Matsumura, M. Y., Peres, V. J., Merino, E. F., Carlton, J. M., Wunderlich, G., Mercadante, A. Z., Kimura, E. A. and Katzin, A. M. (2009). Carotenoid biosynthesis in intraerythrocytic stages of Plasmodium falciparum. Journal of Biological Chemistry 284, 9974–9985.Google Scholar
Torres-Santos, E. C., Sampaio-Santos, M. I., Buckner, F. S., Yokoyama, K., Gelb, M., Urbina, J. A. and Rossi-Bergmann, B. (2009). Altered sterol profile induced in Leishmania amazonensis by a natural dihydroxymethoxylated chalcone. Journal of Antimicrobial Chemotherapy 63, 469–472.Google Scholar
Trivedi, V., Chand, P., Srivastava, K., Puri, S. K., Maulik, P. R. and Bandyopadhyay, U. (2005). Clotrimazole inhibits hemoperoxidase of Plasmodium falciparum and induces oxidative stress – proposed antimalarial mechanism of clotrimazole. Journal of Biological Chemistry 280, 41129–41136.Google Scholar
Turnock, D. C. and Ferguson, M. A. J. (2007). Sugar nucleotide pools of Trypanosoma brucei, Trypanosoma cruzi, and Leishmania major. Eukaryotic Cell 6, 1450–1463.CrossRefGoogle ScholarPubMed
van der Werf, M. J., Overkamp, K. M., Muilwijk, B., Coulier, L. and Hankemeier, T. (2007). Microbial metabolomics: toward a platform with full metabolome coverage. Analytical Biochemistry 370, 17–25.CrossRefGoogle Scholar
Wang, T. J., Gona, P., Larson, M. G., Tofler, G. H., Levy, D., Newton-Cheh, C., Jacques, P. F., Rifai, N., Selhub, J., Robins, S. J., Benjamin, E. J., D'agostino, R. B. and Vasan, R. S. (2006). Multiple biomarkers for the prediction of first major cardiovascular events and death. New England Journal of Medicine 355, 2631–2639.CrossRefGoogle ScholarPubMed
Watson, A. D. (2006). Thematic review series: Systems Biology approaches to metabolic and cardiovascular disorders. Lipidomics: a global approach to lipid analysis in biological systems, Journal of Lipid Research 47, 2101–2111.Google Scholar
Weisenberg, S. A., Butterfield, T. R., Fischer, S. M. and Rhee, K. Y. (2009). Suitability of silica hydride stationary phase, aqueous normal phase chromatography for untargeted metabolomic profiling of Enterococcus faecium and Staphylococcus aureus. Journal of Separation Science 32, 2262–2265.Google Scholar
Welti, R., Mui, E., Sparks, A., Wernimont, S., Isaac, G., Kirisits, M., Roth, M., Roberts, C. W., Botte, C., Marechal, E. and Mcleod, R. (2007). Lipidomic analysis of Toxoplasma gondii reveals unusual polar lipids. Biochemistry 46, 13882–13890.CrossRefGoogle ScholarPubMed
Winder, C. L., Dunn, W. B., Schuler, S., Broadhurst, D., Jarvis, R., Stephens, G. M. and Goodacre, R. (2008). Global metabolic profiling of Escherichia coli cultures: An evaluation of methods for quenching and extraction of intracellular metabolites. Analytical Chemistry 80, 2939–2948.Google Scholar
Woods, W. G., Tuchman, M., Robison, L. L., Bernstein, M., Leclerc, J. M., Brisson, L. C., Brossard, J., Hill, G., Shuster, J., Luepker, R., Byrne, T., Weitzman, S., Bunin, G. and Lemieux, B. (1996). A population-based study of the usefulness of screening for neuroblastoma. Lancet 348, 1682–1687.CrossRefGoogle ScholarPubMed
Wuhrer, M., Dennis, R. D., Doenhoff, M. J. and Geyer, R. (2000). Stage-associated expression of ceramide structures in glycosphingolipids from the human trematode parasite Schistosoma mansoni. Biochimica et Biophysica Acta – General Subjects 1524, 155–161.Google Scholar
Wuhrer, M., Kantelhardt, S. R., Dennis, R. D., Doenhoff, M. J., Lochnit, G. and Geyer, R. (2002). Characterization of glycosphingolipids from Schistosoma mansoni eggs carrying Fuc(alpha 1-3)GalNAc-, GalNAc(beta 1-4)[Fuc(alpha 1-3)]GlcNAc- and Gal(beta 1-4)[Fuc(alpha 1-3)]GlcNAc- (Lewis X) terminal structures. European Journal of Biochemistry 269, 481–493.Google Scholar
Xu, Y., Shen, Z. Z., Wiper, D. W., Wu, M. Z., Morton, R. E., Elson, P., Kennedy, A. W., Belinson, J., Markman, M. and Casey, G. (1998). Lysophosphatidic acid as a potential biomarker for ovarian and other gynecologic cancers. Journal of the American Medical Association 280, 719–723.CrossRefGoogle ScholarPubMed
Yan, S. C., Li, F., Ding, K. Y. and Sun, H. Z. (2003). Reduction of pentavalent antimony by trypanothione and formation of a binary and ternary complex of antimony(III) and trypanothione. Journal of Biological Inorganic Chemistry 8, 689–697.Google Scholar
Zelena, E., Dunn, W. B., Broadhurst, D., Francis-McIntyre, S., Carroll, K. M., Begley, P., O'Hagan, S., Knowles, J. D., Halsall, A., Wilson, I. D., Kell, D. B. and Consortium, H. (2009). Development of a robust and repeatable UPLC-MS method for the long-term metabolomic study of human serum. Analytical Chemistry 81, 1357–1364.Google Scholar
Zhang, Y., Jiye, A., Wang, G. J., Huang, Q., Yan, B., Zha, W. B., Gu, S. H., Liu, L. S., Ren, H. C., Ren, M. T. and Sheng, L. S. (2009). Organic solvent extraction and metabonomic profiling of the metabolites in erythrocytes. Journal of Chromatography B – Analytical Technologies in the Biomedical and Life Sciences 877, 1751–1757.Google Scholar
Zhang, K., Hsu, F. F., Scott, D. A., Docampo, R., Turk, J. and Beverley, S. M. (2005). Leishmania salvage and remodelling of host sphingolipids in amastigote survival and acidocalcisome biogenesis. Molecular Microbiology 55, 1566–1578.Google Scholar
Zytkovicz, T. H., Fitzgerald, E. F., Marsden, D., Larson, C. A., Shih, V. E., Johnson, D. M., Strauss, A. W., Comeau, A. M., Eaton, R. B. and Grady, G. F. (2001). Tandem mass spectrometric analysis for amino, organic, and fatty acid disorders in newborn dried blood spots: A two-year summary from the New England newborn screening program. Clinical Chemistry 47, 1945–1955.Google Scholar