Fatty acids isolated from Toxoplasma gondii reduce glycosylphosphatidylinositol-induced tumor necrosis factor alpha production through inhibition of the NF-κB signaling pathway

Infection and Immunity

Volumn 75, Issue 6, 2007, Pages 2886-2893

  Debierre Grockiego, Françoise ^a   Rabi, Khamran ^a   Schmidt, Jörg ^a   Geyer, Hildegard ^b   Geyer, Rudolf ^b   Schwarz, Ralph T ^a,c  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b Institut fur Biochemie   (Germany)

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

Author keywords

[No Author keywords available]

Indexed keywords

CYTOPLASM PROTEIN; FATTY ACID; GLYCOSYLPHOSPHATIDYLINOSITOL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MYRISTIC ACID; PALMITIC ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; IMMUNE RESPONSE; MACROPHAGE; MOUSE; NONHUMAN; PARASITOSIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; TACHYZOITE; THIN LAYER CHROMATOGRAPHY; TOXOPLASMA GONDII;

ANIMALS; FATTY ACIDS; GLYCOSYLPHOSPHATIDYLINOSITOLS; MACROPHAGES; NF-KAPPA B; SIGNAL TRANSDUCTION; TOXOPLASMA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 34249912631     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01431-06     Document Type: Article

References (44)

1. Appel, S., V. Mirakaj, A. Bringmann, M. M. Weck, F. Grunebach, and P. Brossart. 2005. PPAR-γ agonists inhibit Toll-like receptor-mediated activation of dendritic cells via the MAP kinase and NF-κ pathways. Blood 106:3888-3894.
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. Banner, C. D., M. Gottlicher, E. Widmark, J. Sjovall, J. J. Rafter, and J. A. Gustafsson. 1993. A systematic analytical chemistry/cell assay approach to isolate activators of orphan nuclear receptors from biological extracts: characterization of peroxisome proliferator-activated receptor activators in plasma. J. Lipid Res. 34:1583-1591.
4. Bisanz, C., O. Bastien, D. Grando, J. Jouhet, E. Marechal, and M. F. Cesbron-Delauw. 2006. Toxoplasma gondii acyl-lipid metabolism: de novo synthesis from apicoplast-generated fatty acids versus scavenging of host cell precursors. Biochem. J. 394:197-205.
5. Black, T. H. 1983. The preparation and reactions of diazomethane. Aldrichimica Acta 16:3-10.
6. Bodennec, J., C. Famy, G. Brichon, G. Zwingelstein, and J. Portoukalian. 2000. Purification of free sphingoid bases by solid-phase extraction on weak cation exchanger cartridges. Anal. Biochem. 279:245-248.
7. Campos, M. A., I. C. Almeida, O. Takeuchi, S. Akira, E. P. Valente, D. O. Procopio, L. R. Travassos, J. A. Smith, D. T. Golenbock, and R. T. Gazzinelli. 2001. Activation of Toll-like receptor-2 by glycosylphosphatidylinositol anchors from a protozoan parasite. J. Immunol. 167:416-423.
8. Charron, A. J., and L. D. Sibley. 2002. Host cells: mobilizable lipid resources for the intracellular parasite Toxoplasma gondii. J. Cell Sci. 115:3049-3059.
9. Chawla, A., Y. Barak, L. Nagy, D. Liao, P. Tontonoz, and R. M. Evans. 2001. PPAR-γ dependent and independent effects on macrophage-gene expression in lipid metabolism and inflammation. Nat. Med. 7:48-52.
10. 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.
11. Debierre-Grockiego, F., L. Schofield, N. Azzouz, J. Schmidt, C. S. de Macedo, M. A. J. Ferguson, and R. T. Schwarz. 2006. Fatty acids from Plasmodium falciparum down-regulate the toxic activity of malaria glycosylphosphatidylinositols. Infect. Immun. 74:5487-5496.
12. Forman, B. M., J. Chen, and R. M. Evans. 1997. Hypolipidemic drugs, polyunsaturated fatty acids, and eicosanoids are ligands for peroxisome proliferator-activated receptors α and δ. Proc. Natl. Acad. Sci. USA 94:4312-4317.
13. Gaver, R. C., and C. C. Sweeley. 1965. Methods for methanolysis of sphingolipids and direct determination of long-chain bases by gas chromatography. J. Am. Oil Chem. Soc. 42:294-298.
14. Grimwood, B. G., K. Hechemy, and R. W. Stevens. 1979. Toxoplasma gondii: purification of trophozoites propagated in cell culture. Exp. Parasitol 48: 282-286.
15. Ibrahimi, A., Z. Sfeir, H. Magharaie, E. Z. Amri, P. Grimaldi, and N. A. Abumrad. 1996. Expression of the CD36 homolog (FAT) in fibroblast cells: effects on fatty acid transport. Proc. Natl. Acad. Sci. USA 93:2646-2651.
16. Kamp, F., D. Zakim, F. Zhang, N. Noy, and J. A. Hamilton. 1995. Fatty acid flip-flop in phospholipid bilayers is extremely fast. Biochemistry 34:11928-11937.
17. Kim, F., K. A. Tysseling, J. Rice, M. Pham, L. Haji, B. M. Gallis, A. S. Baas, P. Paramsothy, C. M. Giachelli, M. A. Corson, and E. W. Raines. 2005. Free fatty acid impairment of nitric oxide production in endothelial cells is mediated by IKKβ. Arterioscler. Thromb. Vasc. Biol. 25:989-994.
18. Kliewer, S. A., S. S. Sundseth, S. A. Jones, P. J. Brown, G. B. Wisely, C. S. Koble, P. Devchand, W. Wahli, T. M. Willson, J. M. Lenhard, and J. M. Lehmann. 1997. Fatty acids and eicosanoids regulate gene expression through direct interactions with peroxisome proliferator-activated receptors α and γ. Proc. Natl. Acad. Sci. USA 94:4318-4323.
19. Krey, G., O. Braissant, F. L'Horset, E. Kalkhoven, M. Perroud, M. G. Parker, and W. Wahli. 1997. Fatty acids, eicosanoids, and hypolipidemic agents identified as ligands of peroxisome proliferator-activated receptors by coactivator-dependent receptor ligand assay. Mol. Endocrinol. 11:779-791.
20. 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.
21. 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.
22. Lee, J. Y., K. H. Sohn, S. H. Rhee, and D. Hwang. 2001. Saturated fatty acids, but not unsaturated fatty acids, induce the expression of cyclooxygenase-2 mediated through Toll-like receptor 4. J. Biol. Chem. 276:16683-16689.
23. Lee, J. Y., J. Ye, Z. Gao, H. S. Youn, W. H. Lee, L. Zhao, N. Sizemore, and D. H. Hwang. 2003. Reciprocal modulation of Toll-like receptor-4 signaling pathways involving MyD88 and phosphatidylinositol 3-kinase/AKT by saturated and polyunsaturated fatty acids. J. Biol. Chem. 278:37041-37051.
24. Lee, J. Y., L. Zhao, H. S. Youn, A. R. Weatherill, R. Tapping, L. Feng, W. H. Lee, K. A. Fitzgerald, and D. H. Hwang. 2004. Saturated fatty acid activates but polyunsaturated fatty acid inhibits Toll-like receptor 2 dimerized with Toll-like receptor 6 or 1. J. Biol. Chem. 279:16971-16979.
25. Leesnitzer, L. M., D. J. Parks, R. K. Bledsoe, J. E. Cobb, J. L. Collins, T. G. Consler, R. G. Davis, E. A. Hull-Ryde, J. M. Lenhard, L. Patel, K. D. Plunket, J. L. Shenk, J. B. Stimmel, C. Therapontos, T. M. Willson, and S. G. Blanchard. 2002. Functional consequences of cysteine modification in the ligand binding sites of peroxisome proliferator activated receptors by GW9662. Biochemistry 41:6640-6650.
26. Lin, Q., S. E. Ruuska, N. S. Shaw, D. Dong, and N. Noy. 1999. Ligand selectivity of the peroxisome proliferator-activated receptor α. Biochemistry 38:185-190.
27. Menon, A. K., R. T. Schwarz, S. Mayor, and G. A. Cross. 1990. Cell-free synthesis of glycosyl-phosphatidylinositol precursors for the glycolipid membrane anchor of Trypanosoma brucei variant surface glycoproteins. Structural characterization of putative biosynthetic intermediates. J. Biol. Chem. 265: 9033-9042.
28. Mishra, A., A. Chaudhary, and S. Sethi. 2004. Oxidized omega-3 fatty acids inhibit NF-κ activation via a PPARα-dependent pathway. Arterioscler. Thromb. Vasc. Biol. 24:1621-1627.
29. Murakami, A., T. Nishizawa, K. Egawa, T. Kawada, Y. Nishikawa, K. Uenakai, and H. Ohigashi. 2005. New class of linoleic acid metabolites biosynthesized by corn and rice lipoxygenases: suppression of proinflammatory mediator expression via attenuation of MAPK- and Akt-, but not PPARγ-, dependent pathways in stimulated macrophages. Biochem. Pharmacol. 70:1330-1342.
30. Nishikawa, Y., F. Quittnat, T. T. Stedman, D. R. Voelker, J. Y. Choi, M. Zahn, M. Yang, M. Pypaert, K. A. Joiner, and I. Coppens. 2005. Host cell lipids control cholesteryl ester synthesis and storage in intracellular Toxoplasma. Cell Microbiol 7:849-867.
31. Ricote, M., A. C. Li, T. M. Willson, C. J. Kelly, and C. K. Glass. 1998. The peroxisome proliferator-activated receptor-γ is a negative regulator of macrophage activation. Nature 391:79-82.
32. Rossi, A., P. Kapahi, G. Natoli, T. Takahashi, Y. Chen, M. Karin, and M. G. Santoro. 2000. Anti-inflammatory cyclopentenone prostaglandins are direct inhibitors of IκB kinase. Nature 403:103-108.
33. Schaffer, J. E., and H. F. Lodish. 1994. Expression cloning and characterization of a novel adipocyte long chain fatty acid transport protein. Cell 79:427-436.
34. Schofield, L., and F. Hackett. 1993. Signal transduction in host cells by a glycosylphosphatidylinositol toxin of malaria parasites. J. Exp. Med. 177: 145-153.
35. Schofield, L., L. Vivas, F. Hackett, P. Gerold, R. T. Schwarz, and S. Tachado. 1993. Neutralizing monoclonal antibodies to glycosylphosphatidylinositol, the dominant TNF-α-inducing toxin of Plasmodium falciparum: prospects for the immunotherapy of severe malaria. Ann. Trop. Med. Parasitol. 87:617-626.
36. Sinai, A. P., P. Webster, and K. A. Joiner. 1997. Association of host cell endoplasmic reticulum and mitochondria with the Toxoplasma gondii parasitophorous vacuole membrane: a high-affinity interaction. J. Cell Sci. 110(Pt. 17):2117-2128.
37. Straus, D. S., G. Pascual, M. Li, J. S. Welch, M. Ricote, C. H. Hsiang, L. L. Sengchanthalangsy, G. Ghosh, and C. K. Glass. 2000. 15-deoxy-δ12,14-prostaglandin J2 inhibits multiple steps in the NF-κ signaling pathway. Proc. Natl. Acad. Sci. USA 97:4844-4849.
38. Stremmel, W., G. Lotz, G. Strohmeyer, and P. D. Berk. 1985. Identification, isolation, and partial characterization of a fatty acid binding protein from rat jejunal microvillous membranes. J. Clin. Investig. 75:1068-1076.
39. Striepen, B., C. F. Zinecker, J. B. Damm, P. A. Melgers, G. J. Gerwig, M. Koolen, J. F. Vliegenthart, J. F. Dubremetz, and R. T. Schwarz. 1997. Molecular structure of the "low molecular weight antigen" of Toxoplasma gondii: a glucose α1-4 N-acetylgalactosamine makes free glycosyl-phosphatidylinositols highly immunogenic. J. Mol. Biol. 266:797-813.
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 diacylglycerol moieties. Proc. Natl. Acad. Sci. USA 94:4022-4027.
41. Tachado, S. D., and L. Schofield. 1994. Glycosylphosphatidylinositol toxin of Trypanosoma brucei regulates IL-I α and TNF-α expression in macrophages by protein tyrosine kinase mediated signal transduction. Biochem. Biophys. Res. Commun. 205:984-991.
42. Thardin, J. F., C. M'Rini, M. Beraud, J. Vandaele, M. F. Frisach, M. H. Bessieres, J. P. Seguela, and B. Pipy. 1993. Eicosanoid production by mouse peritoneal macrophages during Toxoplasma gondii penetration: role of parasite and host cell phospholipases. Infect. Immun. 61:1432-1441.
43. Weatherill, A. R., J. Y. Lee, L. Zhao, D. G. Lemay, H. S. Youn, and D. H. Hwang. 2005. Saturated and polyunsaturated fatty acids reciprocally modulate dendritic cell functions mediated through TLR4. J. Immunol. 174:5390-5397.
44. Zhang, H., N. E. Buckley, K. Gibson, and S. Spiegel. 1990. Sphingosine stimulates cellular proliferation via a protein kinase C-independent pathway. J. Biol. Chem. 265:76-81.