Fatty acids from Plasmodium falciparum down-regulate the toxic activity of malaria glycosylphosphatidylinositols

Infection and Immunity

Volumn 74, Issue 10, 2006, Pages 5487-5496

  Debierre Grockiego, Françoise ^a   Schofield, Louis ^b   Azzouz, Nahid ^a,e   Schmidt, Jörg ^a   Santos De Macedo, Cristiana ^a,f   Ferguson, Michael A J ^c   Schwarz, Ralph T ^a,d  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

^d UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

^e ETH ZURICH   (Switzerland)

^f UNIVERSIDADE ANHANGUERA UNIDERP   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; FATTY ACID; GLYCOSYLPHOSPHATIDYLINOSITOL; MYRISTIC ACID; PALMITIC ACID; PALMITOLEIC ACID; PENTADECANOIC ACID; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ION EXCHANGE CHROMATOGRAPHY; MALARIA; MASS SPECTROMETRY; MOUSE; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; THIN LAYER CHROMATOGRAPHY;

ANIMALS; DOWN-REGULATION; FATTY ACIDS; FATTY ACIDS, MONOUNSATURATED; GLYCOSYLPHOSPHATIDYLINOSITOLS; MALARIA, FALCIPARUM; MASS SPECTROMETRY; MICE; MICROSCOPY, ELECTRON; MYRISTIC ACID; PALMITIC ACID; PLASMODIUM FALCIPARUM; TUMOR NECROSIS FACTOR-ALPHA; VIRULENCE FACTORS;

EID: 33749241164     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01934-05     Document Type: Article

References (44)

1. Ansorge, I., D. Jeckel, F. Wieland, and K. Lingelbach. 1995. Plasmodium falciparum-infected erythrocytes utilize a synthetic truncated ceramide precursor for synthesis and secretion of truncated sphingomyelin. Biochem. J. 308:335-341.
2. Azzouz, N., H. Shams-Eldin, and R. T. Schwarz. 2005. Removal of phospholipid contaminants through precipitation of glycosylphosphatidylinositols. Anal. Biochem. 343:152-158.
3. Bodennec, J., O. Koul, I. Aguado, G. Brichon, G. Zwingelstein, and J. Portoukalian. 2000. A procedure for fractionation of sphingolipid classes by solid-phase extraction on aminopropyl cartridges. J. Lipid Res. 41:1524-1531.
4. Debierre-Grockiego, F., N. Azzouz, J. Schmidt, J. F. Dubremetz, H. Geyer, R. Geyer, R. Weingart, R. R. Schmidt, and R. T. Schwarz. 2003. Roles of glycosylphosphatidylinositols of Toxoplasma gondii. Induction of tumor necrosis factor-alpha production in macrophages. J. Biol. Chem. 278:32987-32993.
5. Delorenzi, M., A. Sexton, H. Shams-Eldin, R. T. Schwarz, T. Speed, and L. Schofield. 2002. Genes for glycosylphosphatidylinositol toxin biosynthesis in Plasmodium falciparum. Infect. Immun. 70:4510-4522.
6. Dieckmann-Schuppert, A., S. Bender, M. Odenthal-Schnittler, E. Bause, and R. T. Schwarz. 1992. Apparent lack of N-glycosylation in the asexual intraerythrocytic stage of Plasmodium falciparum. Eur. J. Biochem. 205:815-825.
7. Elabbadi, N., M. L. Ancelin, and H. J. Vial. 1997. Phospholipid metabolism of serine in Plasmodium-infected erythrocytes involves phosphatidylserine and direct serine decarboxylation. Biochem. J. 324:435-445.
8. Elmendorf, H. G., and K. Haldar. 1994. Plasmodium falciparum exports the Golgi marker sphingomyelin synthase into a tubovesicular network in the cytoplasm of mature erythrocytes. J. Cell Biol. 124:449-462.
9. Folch, J., M. Lees, and G. H. Sloane Stanley. 1957. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226:497-509.
10. Gerold, P., A. Dieckmann-Schuppert, and R. T. Schwarz. 1994. Glycosylphosphatidylinositols synthesized by asexual erythrocytic stages of the malarial parasite, Plasmodium falciparum. Candidates for plasmodial glycosylphosphatidylinositol membrane anchor precursors and pathogenicity factors. J. Biol. Chem. 269:2597-2606.
11. Gerold, P., N. Jung, N. Azzouz, N. Freiberg, S. Kobe, and R. T. Schwarz. 1999. Biosynthesis of glycosylphosphatidylinositols of Plasmodium falciparum in a cell-free incubation system: inositol acylation is needed for mannosylation of glycosylphosphatidylinositols. Biochem. J. 344:731-738.
12. Gerold, P., L. Schofield, M. J. Blackman, A. A. Holder, and R. T. Schwarz. 1996. Structural analysis of the glycosyl-phosphatidylinositol membrane anchor of the merozoite surface proteins-1 and -2 of Plasmodium falciparum. Mol. Biochem. Parasitol. 75:131-143.
13. Gerold, P., and R. T. Schwarz. 2001. Biosynthesis of glycosphingolipids de-novo by the human malaria parasite Plasmodium falciparum. Mol. Biochem. Parasitol. 112:29-37.
14. Haldar, K., L. Uyetake, N. Ghori, H. G. Elmendorf, and W. L. Li. 1991. The accumulation and metabolism of a fluorescent ceramide derivative in Plasmodium falciparum-infected erythrocytes. Mol. Biochem. Parasitol. 49:143-156.
15. Hsiao, L. L., R. J. Howard, M. Aikawa, and T. F. Taraschi. 1991. Modification of host cell membrane lipid composition by the intra-erythrocytic human malaria parasite Plasmodium falciparum. Biochem. J. 274:121-132.
16. Krishnegowda, G., A. M. Hajjar, J. Zhu, E. J. Douglass, S. Uematsu, S. Akira, A. S. Woods, and D. C. Gowda. 2005. Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. J. Biol. Chem. 280:8606-8616.
17. Lauer, S. A., N. Ghori, and K. Haldar. 1995. Sphingolipid synthesis as a target for chemotherapy against malaria parasites. Proc. Natl. Acad. Sci. USA 92:9181-9185.
18. Lauer, S. A., P. K. Rathod, N. Ghori, and K. Haldar. 1997. A membrane network for nutrient import in red cells infected with the malaria parasite. Science 276:1122-1125.
19. Lee, J. Y., A. Plakidas, W. H. Lee, A. Heikkinen, P. Chanmugam, G. Bray, and D. H. Hwang. 2003. Differential modulation of Toll-like receptors by fatty acids: preferential inhibition by n-3 polyunsaturated fatty acids. J. Lipid Res. 44:479-486.
20. Levander, O. A., A. L. Ager, Jr., V. C. Morris, and R. G. May. 1990. Plasmodium yoelii: comparative antimalarial activities of dietary fish oils and fish oil concentrates in vitamin E-deficient mice. Exp. Parasitol. 70:323-329.
21. Martin, D., L. Gannoun-Zaki, S. Bonnefoy, P. Eldin, K. Wengelnik, and H. Vial. 2000. Characterization of Plasmodium falciparum CDP-diacylglycerol synthase, a proteolytically cleaved enzyme. Mol. Biochem. Parasitol. 110:93-105.
22. McGilvray, I. D., L. Serghides, A. Kapus, O. D. Rotstein, and K. C. Kain. 2000. Nonopsonic monocyte/macrophage phagocytosis of Plasmodium falcipuram-parasitized erythrocytes: a role for CD36 in malarial clearance. Blood 96:3231-3240.
23. Mishra, A., A. Chaudhary, and S. Sethi. 2004. Oxidized omega-3 fatty acids inhibit NF-kappaB activation via a PPARalpha-dependent pathway. Arterioscler. Thromb. Vasc. Biol. 24:1621-1627.
24. Mitamura, T., K. Hanada, E. P. Ko-Mitamura, M. Nishijinia, and T. Horii. 2000. Serum factors governing intraerythrocytic development and cell cycle progression of Plasmodium falciparum. Parasitol. Int. 49:219-229.
25. Moya-Camarena, S. Y., J. P. Vanden Heuvel, S. G. Blanchard, L. A. Leesnitzer, and M. A. Belury. 1999. Conjugated linoleic acid is a potent naturally occurring ligand and activator of PPARalpha. J. Lipid Res. 40:1426-1433.
26. Nawabi, P., A. Lykidis, D. Ji, and K. Haldar. 2003. Neutral-lipid analysis reveals elevation of acylglycerols and lack of cholesterol esters in Plasmodium falciparum-infected erythrocytes. Eukaryot. Cell. 2:1128-1131.
27. Nebl, T., D. E. V. MJ, and L. Schofield. 2005. Stimulation of innate immune responses by malarial glycosylphosphatidylinositol via pattern recognition receptors. Parasitology. 130(Suppl. 1):S45-S62.
28. Palacpac, N. M., Y. Hiramine, F. Mi-ichi, M. Torii, K. Kita, R. Hiramatsu, T. Horii, and T. Mitamura. 2004. Developmental-stage-specific triacylglycerol biosynthesis, degradation and trafficking as lipid bodies in Plasmodium falciparum-infected erythrocytes. J. Cell Sci. 117:1469-1480.
29. Schmidt, A., R. T. Schwarz, and P. Gerold. 1998. Plasmodium falciparum: asexual erythrocytic stages synthesize two structurally distinct free and protein-bound glycosylphosphatidylinositols in a maturation-dependent manner. Exp. Parasitol. 88:95-102.
30. Schmitz, F., J. Mages, A. Heit, R. Lang, and H. Wagner. 2004. Transcriptional activation induced in macrophages by Toll-like receptor (TLR) ligands: from expression profiling to a model of TLR signaling. Eur. J. Immunol. 34:2863-2873.
31. Schofield, L. 2002. Antidisease vaccines. Chem. Immunol. 80:322-342.
32. Schofield, L., and G. E. Grau. 2005. Immunological processes in malaria pathogenesis. Nat. Rev. Immunol. 5:722-735.
33. Schofield, L., and F. Hackett. 1993. Signal transduction in host cells by a glycosylphosphatidylinositol toxin of malaria parasites. J. Exp. Med. 177:145-153.
34. Schofield, L., M. C. Hewitt, K. Evans, M. A. Siomos, and P. H. Seeberger. 2002. Synthetic GPI as a candidate anti-toxic vaccine in a model of malaria. Nature 418:785-789.
35. Schofield, L., S. Novakovic, P. Gerold, R. T. Schwarz, M. J. McConville, and S. D. Tachado. 1996. Glycosylphosphatidylinositol toxin of Plasmodium upregulates intercellular adhesion molecule-1, vascular cell adhesion molecule-1, and E-selectin expression in vascular endothelial cells and increases leukocyte and parasite cytoadherence via tyrosine kinase-dependent signal transduction. J. Immunol. 156:1886-1896.
36. Schwarzer, E., H. Kuhn, E. Valente, and P. Arese. 2003. Malaria-parasitized erythrocytes and hemozoin nonenzymatically generate large amounts of hydroxy fatty acids that inhibit monocyte functions. Blood 101:722-728.
37. Serghides, L., and K. C. Kain. 2001. Peroxisome proliferator-activated receptor gamma-retinoid X receptor agonists increase CD36-dependent phagocytosis of Plasmodium falcipuram-parasitized erythrocytes and decrease malaria-induced TNF-alpha secretion by monocytes/macrophages. J. Immunol. 166:6742-6748.
38. Sheikh, N. A., H. N. Caro, J. Taverne, J. H. Playfair, and T. W. Rademacher. 1996. Malaria: a tumour necrosis factor inhibitor from parasitized erythrocytes. Immunology 87:461-466.
39. Tachado, S. D., P. Gerold, M. J. McConville, T. Baldwin, D. Quilici, R. T. Schwarz, and L. Schofield. 1996. Glycosylphosphatidylinositol toxin of Plasmodium induces nitric oxide synthase expression in macrophages and vascular endothelial cells by a protein tyrosine kinase-dependent and protein kinase C-dependent signaling pathway. J. Immunol. 156:1897-1907.
40. Tachado, S. D., P. Gerold, R. Schwarz, S. Novakovic, M. McConville, and L. Schofield. 1997. Signal transduction in macrophages by glycosylphosphatidylinositols of Plasmodium, Trypanosoma, and Leishmania: activation of protein tyrosine kinases and protein kinase C by inositolglycan and diacyl-glycerol moieties. Proc. Natl. Acad. Sci. USA 94:4022-4027.
41. Vial, H. J., M. L. Ancelin, J. R. Philippot, and M. J. Thuet. 1990. Biosynthesis and dynamics of lipids in Plasmodium-infected mature mammalian erythrocytes. Blood Cells 16:531-555. (Discussion, 16:556-561.)
42. Vielemeyer, O., M. T. McIntosh, K. A. Joiner, and I. Coppens. 2004. Neutral lipid synthesis and storage in the intraerythrocytic stages of Plasmodium falciparum. Mol. Biochem. Parasitol. 135:197-209.
43. Yang, M., and M. E. Cook. 2003. Dietary conjugated linoleic acid decreased cachexia, macrophage tumor necrosis factor-alpha production, and modifies splenocyte cytokines production. Exp. Biol. Med. 228:51-58.
44. Yeo, H. J., J. Sri Widada, O. Mercereau-Puijalon, and H. J. Vial. 1995. Molecular cloning of CTP:phosphocholine cytidylyltransferase from Plasmodium falciparum. Eur. J. Biochem. 233:62-72.