Sugar nucleotide quantification by liquid chromatography tandem mass spectrometry reveals a distinct profile in Plasmodium falciparum sexual stage parasites

Biochemical Journal

Volumn 474, Issue 6, 2017, Pages 897-905

  López Gutiérrez, Borja ^a   Dinglasan, Rhoel R ^b   Izquierdo, Luis ^a  

^a CENTRE FOR RESEARCH IN ENVIRONMENTAL EPIDEMIOLOGY CREAL   (Spain)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARBON; POROUS GRAPHITIC CARBON; SUGAR NUCLEOTIDE; UNCLASSIFIED DRUG; GUANOSINE DIPHOSPHATE FUCOSE; GUANOSINE DIPHOSPHATE GLUCOSE; GUANOSINE DIPHOSPHATE MANNOSE; GUANOSINE DIPHOSPHATE SUGAR; URIDINE DIPHOSPHATE GALACTOSE; URIDINE DIPHOSPHATE GLUCOSE; URIDINE DIPHOSPHATE N ACETYLGALACTOSAMINE;

ARTICLE; ASEXUAL REPRODUCTION; CONTROLLED STUDY; ERYTHROCYTE; GAMETOCYTE; GLYCOSYLATION; HUMAN; HUMAN CELL; LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY; NONHUMAN; PARASITE DEVELOPMENT; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; SCHIZONT; TROPHOZOITE; VALIDATION PROCESS; GAMETOGENESIS; GROWTH, DEVELOPMENT AND AGING; LIFE CYCLE STAGE; LIQUID CHROMATOGRAPHY; METABOLISM; PARASITOLOGY; PHYSIOLOGY; TANDEM MASS SPECTROMETRY;

CHROMATOGRAPHY, LIQUID; ERYTHROCYTES; GAMETOGENESIS; GUANOSINE DIPHOSPHATE FUCOSE; GUANOSINE DIPHOSPHATE MANNOSE; GUANOSINE DIPHOSPHATE SUGARS; HUMANS; LIFE CYCLE STAGES; PLASMODIUM FALCIPARUM; TANDEM MASS SPECTROMETRY; URIDINE DIPHOSPHATE GALACTOSE; URIDINE DIPHOSPHATE GLUCOSE; URIDINE DIPHOSPHATE N-ACETYLGALACTOSAMINE;

EID: 85016155897     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BCJ20161030     Document Type: Article

References (43)

1. WHO. (2016) WHO | World Malaria Report 2015. WHO, World Health Organization
2. Fairhurst, R.M. and Dondorp, A.M. (2016) Artemisinin-Resistant Plasmodium falciparum malaria. Microbiol. Spectr. 4, doi:10.1128/microbiolspec. EI10-0013-2016
3. The malERA Consultative Group on Basic Science and Enabling Technologies. (2011) A research agenda for malaria eradication: basic science and enabling technologies. PLoS Med. 8, e1000399
4. Cova, M., Rodrigues, J.A., Smith, T.K. and Izquierdo, L. (2015) Sugar activation and glycosylation in Plasmodium. Malar. J. 14, 427
5. Von Itzstein, M., Plebanski, M., Cooke, B.M. and Coppel, R.L. (2008) Hot, sweet and sticky: the glycobiology of Plasmodium falciparum. Trends Parasitol. 24, 210-218
6. Naik, R.S., Branch, O.H., Woods, A.S., Vijaykumar, M., Perkins, D.J., Nahlen, B.L. et al. (2000) Glycosylphosphatidylinositol anchors of Plasmodium falciparum: molecular characterization and naturally elicited antibody response that may provide immunity to malaria pathogenesis. J. Exp. Med. 192, 1563-1576
7. Sanders, P.R., Kats, L.M., Drew, D.R., O'Donnell, R.A., O'Neill, M., Maier, A.G. et al. (2006) A set of glycosylphosphatidyl inositol-anchored membrane proteins of Plasmodium falciparum is refractory to genetic deletion. Infect. Immun. 74, 4330-4338
8. Schofield, L. and Hackett, F. (1993) Signal transduction in host cells by a glycosylphosphatidylinositol toxin of malaria parasites. J. Exp. Med. 177, 145-153
9. Bushkin, G.G., Ratner, D.M., Cui, J., Banerjee, S., Duraisingh, M.T., Jennings, C.V. et al. (2010) Suggestive evidence for Darwinian selection against asparagine-linked glycans of Plasmodium falciparum and Toxoplasma gondii. Eukaryot. Cell 9, 228-241
10. Swearingen, K.E., Lindner, S.E., Shi, L., Shears, M.J., Harupa, A., Hopp, C.S. et al. (2016) Interrogating the Plasmodium sporozoite surface: identification of surface-exposed proteins and demonstration of glycosylation on CSP and TRAP by mass spectrometry-based proteomics. PLoS Pathog. 12, e1005606
11. Sanz, S., Bandini, G., Ospina, D., Bernabeu, M., Marino, K., Fernandez-Becerra, C. et al. (2013) Biosynthesis of GDP-fucose and other sugar nucleotides in the blood stages of Plasmodium falciparum. J. Biol. Chem. 288, 16506-16517
12. Varki, A., Cummings, R.D., Esko, J.D., Freeze, H.H., Stanley, P., Bertozzi, C.R. et al. (2009) Essentials of Glycobiology, Cold Spring Harbor Laboratory Press
13. Takeda, J. and Kinoshita, T. (1995) GPI-anchor biosynthesis. Trends Biochem. Sci. 20, 367-371
14. Ferguson, M.A. (1999) The structure, biosynthesis and functions of glycosylphosphatidylinositol anchors, and the contributions of trypanosome research. J. Cell Sci. 112, 2799-2809
15. Samuelson, J., Banerjee, S., Magnelli, P., Cui, J., Kelleher, D.J., Gilmore, R. et al. (2005) The diversity of dolichol-linked precursors to Asn-linked glycans likely results from secondary loss of sets of glycosyltransferases. Proc. Natl Acad. Sci. U.S.A. 102, 1548-1553
16. Turnock, D.C. and Ferguson, M.A.J. (2007) Sugar nucleotide pools of Trypanosoma brucei, Trypanosoma cruzi, and Leishmania major. Eukaryot. Cell 6, 1450-1463
17. Turnock, D.C., Izquierdo, L. and Ferguson, M.A.J. (2007) The de novo synthesis of GDP-fucose is essential for flagellar adhesion and cell growth in Trypanosoma brucei. J. Biol. Chem. 282, 28853-28863
18. Marino, K., Guther, M.L.S., Wernimont, A.K., Qiu, W., Hui, R. and Ferguson, M.A.J. (2011) Characterization, localization, essentiality, and high-resolution crystal structure of glucosamine 6-phosphate N-acetyltransferase from Trypanosoma brucei. Eukaryot. Cell 10, 985-997
19. Sanz, S., López-Gutiérrez, B., Bandini, G., Damerow, S., Absalon, S., Dinglasan, R.R. et al. (2016) The disruption of GDP-fucose de novo biosynthesis suggests the presence of a novel fucose-containing glycoconjugate in Plasmodium asexual blood stages. Sci. Rep. 6, 37230
20. Pabst, M., Grass, J., Fischl, R., Léonard, R., Jin, C., Hinterkörner, G. et al. (2010) Nucleotide and nucleotide sugar analysis by liquid chromatography-electrospray ionization-mass spectrometry on surface-conditioned porous graphitic carbon. Anal. Chem. 82, 9782-9788
21. Antignac, J.-P., de Wasch, K., Monteau, F., De Brabander, H., Andre, F. and Le Bizec, B. (2005) The ion suppression phenomenon in liquid chromatography-mass spectrometry and its consequences in the field of residue analysis. Anal. Chim. Acta 529, 129-136
22. Jessome, L. and Volmer, D.A. (2006) Ion suppression: a major concern in mass spectrometry. LC-GC North Am. 24, 498-510
23. Antonio, C., Larson, T., Gilday, A., Graham, I., Bergström, E. and Thomas-Oates, J. (2007) Quantification of sugars and sugar phosphates in Arabidopsis thaliana tissues using porous graphitic carbon liquid chromatography-electrospray ionization mass spectrometry. J. Chromatogr. A 1172, 170-178
24. West, C., Elfakir, C. and Lafosse, M. (2010) Porous graphitic carbon: a versatile stationary phase for liquid chromatography. J. Chromatogr. A 1217, 3201-3216
25. Joice, R., Nilsson, S.K., Montgomery, J., Dankwa, S., Egan, E., Morahan, B. et al. (2014) Plasmodium falciparum transmission stages accumulate in the human bone marrow. Sci. Transl. Med. 6, 244re5
26. Alano, P. (2007) Plasmodium falciparum gametocytes: still many secrets of a hidden life. Mol. Microbiol. 66, 291-302
27. Adjalley, S.H., Johnston, G.L., Li, T., Eastman, R.T., Ekland, E.H., Eappen, A.G. et al. (2011) Quantitative assessment of Plasmodium falciparum sexual development reveals potent transmission-blocking activity by methylene blue. Proc. Natl Acad. Sci. U.S.A. 108, E1214-E1223
28. MacRae, J.I., Dixon, M.W., Dearnley, M.K., Chua, H.H., Chambers, J.M., Kenny, S. et al. (2013) Mitochondrial metabolism of sexual and asexual blood stages of the malaria parasite Plasmodium falciparum. BMC Biol. 11, 67
29. Rivadeneira, E.M., Wasserman, M. and Espinal, C.T. (1983) Separation and concentration of schizonts of Plasmodium falciparum by Percoll gradients. J. Protozool. 30, 367-370
30. Lambros, C. and Vanderberg, J.P. (1979) Synchronization of Plasmodium falciparum erythrocytic stages in culture. J. Parasitol. 65, 418-420
31. Kafsack, B.F.C., Rovira-Graells, N., Clark, T.G., Bancells, C., Crowley, V.M., Campino, S.G. et al. (2014) A transcriptional switch underlies commitment to sexual development in malaria parasites. Nature 507, 248-252
32. Ribaut, C., Berry, A., Chevalley, S., Reybier, K., Morlais, I., Parzy, D. et al. (2008) Concentration and purification by magnetic separation of the erythrocytic stages of all human Plasmodium species. Malar. J. 7, 45
33. Di Girolamo, F., Raggi, C., Birago, C., Pizzi, E., Lalle, M., Picci, L. et al. (2008) Plasmodium lipid rafts contain proteins implicated in vesicular trafficking and signalling as well as members of the PIR superfamily, potentially implicated in host immune system interactions. Proteomics 8, 2500-2513
34. Räbinä, J., Mäki, M., Savilahti, E.M., Järvinen, N., Penttilä, L. and Renkonen, R. (2001) Analysis of nucleotide sugars from cell lysates by ion-pair solid-phase extraction and reversed-phase high-performance liquid chromatography. Glycoconj. J. 18, 799-805
35. Radfar, A., Méndez, D., Moneriz, C., Linares, M., Marín-García, P., Puyet, A. et al. (2009) Synchronous culture of Plasmodium falciparum at high parasitemia levels. Nat. Protoc. 4, 1828-1844
36. Sinden, R.E. (1983) Sexual development of malarial parasites. Adv. Parasitol. 22, 153-216
37. Martinez, A.P., Margos, G., Barker, G. and Sinden, R.E. (2000) The roles of the glycosylphosphatidylinositol anchor on the production and immunogenicity of recombinant ookinete surface antigen Pbs21 of Plasmodium berghei when prepared in a baculovirus expression system. Parasite Immunol. 22, 493-500
38. Hanssen, E., Knoechel, C., Dearnley, M., Dixon, M.W.A.A., Le Gros, M., Larabell, C. et al. (2012) Soft X-ray microscopy analysis of cell volume and hemoglobin content in erythrocytes infected with asexual and sexual stages of Plasmodium falciparum. J. Struct. Biol. 177, 224-232
39. Gilson, P.R., Nebl, T., Vukcevic, D., Moritz, R.L., Sargeant, T., Speed, T.P. et al. (2006) Identification and stoichiometry of glycosylphosphatidylinositol-anchored membrane proteins of the human malaria parasite Plasmodium falciparum. Mol. Cell. Proteomics 5, 1286-1299
40. McConville, M.J. and Ferguson, M.A. (1993) The structure, biosynthesis and function of glycosylated phosphatidylinositols in the parasitic protozoa and higher eukaryotes. Biochem. J. 294, 305-324
41. Rovira-Graells, N., Gupta, A.P., Planet, E., Crowley, V.M., Mok, S., Ribas de Pouplana, L. et al. (2012) Transcriptional variation in the malaria parasite Plasmodium falciparum. Genome Res. 22, 925-938
42. Luo, Y., Koles, K., Vorndam, W., Haltiwanger, R.S. and Panin, V.M. (2006) Protein O-fucosyltransferase 2 adds O-fucose to thrombospondin type 1 repeats. J. Biol. Chem. 281, 9393-9399
43. Rodrigues, J.A., Acosta-Serrano, A., Aebi, M., Ferguson, M.A.J., Routier, F.H., Schiller, I. et al. (2015) Parasite glycobiology: a bittersweet symphony. PLOS Pathog. 11, e1005169