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Stimulation of innate immune responses by malarial glycosylphosphatidylinositol via pattern recognition receptors

Published online by Cambridge University Press:  11 November 2005

T. NEBL
Affiliation:
The Walter and Eliza Hall Institute of Medical Research, 1G Royal Parade, Victoria, 3050, Australia
M. J. DE VEER
Affiliation:
The Walter and Eliza Hall Institute of Medical Research, 1G Royal Parade, Victoria, 3050, Australia
L. SCHOFIELD
Affiliation:
The Walter and Eliza Hall Institute of Medical Research, 1G Royal Parade, Victoria, 3050, Australia

Abstract

The glycosylphosphatidylinositol (GPI) anchor of Plasmodium falciparum is thought to function as a critical toxin that contributes to severe malarial pathogenesis by eliciting the production of proinflammatory responses by the innate immune system of mammalian hosts. Analysis of the fine structure of P. falciparum GPI suggests a requirement for the presence of both core glycan and lipid moieties in the recognition and signalling of parasite glycolipids by host immune cells. It has been demonstrated that GPI anchors of various parasitic protozoa can mediate cellular immune responses via members of the Toll-like family of pattern recognition receptors (TLRs). Recent studies indicate that GPI anchors of P. falciparum and other protozoa are preferentially recognized by TLR-2, involving the MyD88-dependent activation of specific signalling pathways that mediate the production of proinflammatory cytokines and nitric oxide from host macrophages in vitro. However, the contribution of malaria GPI toxin to severe disease syndromes and the role of specific TLRs or other pattern recognition receptors in innate immunity in vivo is only just beginning to be characterized. A better understanding of the molecular mechanisms underlying severe malarial pathogenesis may yet lead to substantial new insights with important implications for the development of novel therapeutics for malaria treatment.

Type
Research Article
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

ADACHI, K., TSUTSUI, H., KASHIWAMURA, S., SEKI, E., NAKANO, H., TAKEUCHI, O., TAKEDA, K., OKUMURA, K., VAN KAER, L., OKAMURA, H., AKIRA, S. & NAKANISHI, K. ( 2001). Plasmodium berghei infection in mice induces liver injury by an IL-12- and toll-like receptor/myeloid differentiation factor 88-dependent mechanism. Journal of Immunlogy 167, 59285934.CrossRefGoogle Scholar
AKIRA, S. & TAKEDA, K. ( 2004). Toll-like receptor signalling. Nature Reviews Immunology 4, 499511.CrossRefGoogle Scholar
AL YAMAN, F. M., MOKELA, D., GENTON, B., ROCKETT, K. A., ALPERS, M. P. & CLARK, I. A. ( 1996). Association between serum levels of reactive nitrogen intermediates and coma in children with cerebral malaria in Papua New Guinea. Transaction of the Royal Society of Tropical Medicine and Hygiene 90, 270273.CrossRefGoogle Scholar
ALMEIDA, I. C., CAMARGO, M. M., PROCOPIO, D. O., SILVA, L. S., MEHLERT, A., TRAVASSOS, L. R., GAZZINELLI, R. T. & FERGUSON, M. A. ( 2000). Highly purified glycosylphosphatidylinositols from Trypanosoma cruzi are potent proinflammatory agents. EMBO Journal 19, 14761485.CrossRefGoogle Scholar
ALMEIDA, I. C. & GAZZINELLI, R. T. ( 2001). Proinflammatory activity of glycosylphosphatidylinositol anchors derived from Trypanosoma cruzi: structural and functional analyses. Journal of Leukocyte Biology 70, 467477.Google Scholar
AMANI, V., VIGARIO, A. M., BELNOUE, E., MARUSSIG, M., FONSECA, L., MAZIER, D. & RENIA, L. ( 2000). Involvement of IFN-gamma receptor-medicated signaling in pathology and anti-malarial immunity induced by Plasmodium berghei infection. European Journal of Immunology 30, 16461655.3.0.CO;2-0>CrossRefGoogle Scholar
ANDERSON, R. G. & JACOBSON, K. ( 2002). A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. Science 296, 18211825.CrossRefGoogle Scholar
BELLAMY, R., RUWENDE, C., MCADAM, K. P., THURSZ, M., SUMIYA, M., SUMMERFIELD, J., GILBERT, S. C., CORRAH, T., KWIATKOWSKI, D., WHITTLE, H. C. & HILL, A. V. ( 1998). Mannose binding protein deficiency is not associated with malaria, hepatitis B carriage nor tuberculosis in Africans. Quarterly Journal of Medicine 91, 1318.CrossRefGoogle Scholar
BENTING, J., RIETVELD, A., ANSORGE, I. & SIMONS, K. ( 1999). Acyl and alkyl chain length of GPI-anchors is critical for raft association in vitro. FEBS Letters 462, 4750.CrossRefGoogle Scholar
BERENDT, A. R., SIMMONS, D. L., TANSEY, J., NEWBOLD, C. I. & MARSH, K. ( 1989). Intercellular adhesion molecule-1 is an endothelial cell adhesion molecule for Plasmodium falciparum. Nature 341, 5759.CrossRefGoogle Scholar
BOUTLIS, C. S., GOWDA, D. C., NAIK, R. S., MAGUIRE, G. P., MGONE, C. S., BOCKARIE, M. J., LAGOG, M., IBAM, E., LORRY, K. & ANSTEY, N. M. ( 2002). Antibodies to Plasmodium falciparum glycosylphosphatidylinositols: inverse association with tolerance of parasitemia in Papua New Guinean children and adults. Infection and Immunity 70, 50525057.CrossRefGoogle Scholar
BROWN, D. A. & LONDON, E. ( 2000). Structure and function of sphingolipid- and cholesterol-rich membrane rafts. Journal of Biological Chemistry 275, 1722117224.CrossRefGoogle Scholar
CAMARGO, M. M., ALMEIDA, I. C., PEREIRA, M. E., FERGUSON, M. A., TRAVASSOS, L. R. & GAZZINELLI, R. T. ( 1997 a). Glycosylphosphatidylinositol-anchored mucin-like glycoproteins isolated from Trypanosoma cruzi trypomastigotes initiate the synthesis of proinflammatory cytokines by macrophages. Journal of Immunology 158, 58905901.Google Scholar
CAMARGO, M. M., ANDRADE, A. C., ALMEIDA, I. C., TRAVASSOS, L. R. & GAZZINELLI, R. T. ( 1997 b). Glycoconjugates isolated from Trypanosoma cruzi but not from Leishmania species membranes trigger nitric oxide synthesis as well as microbicidal activity in IFN-gamma-primed macrophages. Journal of Immunology 159, 61316139.Google Scholar
CAMBI, A. & FIGDOR, C. G. ( 2003). Dual function of C-type lectin-like receptors in the immune system. Current Opinion in Cell Biology 15, 539546.CrossRefGoogle Scholar
CAMBI, A., GIJZEN, K., DE VRIES, J. M., TORENSMA, R., JOOSTEN, B., ADEMA, G. J., NETEA, M. G., KULLBERG, B. J., ROMANI, L. & FIGDOR, C. G. ( 2003). The C-type lectin DC-SIGN (CD209) is an antigen-uptake receptor for Candida albicans on dendritic cells. European Journal of Immunology 33, 532538.CrossRefGoogle Scholar
CAMPOS, M. A., ALMEIDA, I. C., TAKEUCHI, O., AKIRA, S., VALENTE, E. P., PROCOPIO, D. O., TRAVASSOS, L. R., SMITH, J. A., GOLENBOCK, D. T. & GAZZINELLI, R. T. ( 2001). Activation of Toll-like receptor-2 by glycosylphosphatidylinositol anchors from a protozoan parasite. Journal of Immunology 167, 416423.CrossRefGoogle Scholar
CAMPOS, M. A., CLOSEL, M., VALENTE, E. P., CARDOSO, J. E., AKIRA, S., ALVAREZ-LEITE, J. I., ROPERT, C. & GAZZINELLI, R. T. ( 2004). Impaired production of proinflammatory cytokines and host resistance to acute infection with Trypanosoma cruzi in mice lacking functional myeloid differentiation factor 88. Journal of Immunology 172, 17111718.CrossRefGoogle Scholar
CHANG, W. L., JONES, S. P., LEFER, D. J., WELBOURNE, T., SUN, G., YIN, L., SUZUKI, H., HUANG, J., GRANGER, D. N. & VAN DER HEYDE, H. C. ( 2001). CD8(+)-T-cell depletion ameliorates circulatory shock in Plasmodium berghei-infected mice. Infection and Immunity 69, 73417348.CrossRefGoogle Scholar
CHEN, M., AOSAI, F., NOROSE, K., MUN, H. S., TAKEUCHI, O., AKIRA, S. & YANO, A. ( 2002). Involvement of MyD88 in host defense and the down-regulation of anti-heat shock protein 70 autoantibody formation by MyD88 in Toxoplasma gondii-infected mice. Journal of Parasitology 88, 10171019.Google Scholar
CHEN, Q., SCHLICHTHERLE, M. & WAHLGREN, M. ( 2000). Molecular aspects of severe malaria. Clinical Microbiology Reviews 13, 439450.CrossRefGoogle Scholar
COBAN, C., ISHII, K. J., KAWAI, T., HEMMI, H., SATO, S., UEMATSU, S., YAMAMOTO, M., TAKEUCHI, O., ITAGAKI, S., KUMAR, N., HORII, T. & AKIRA, S. ( 2005). Toll-like receptor 9 mediates innate immune activation by the malaria pigment hemozoin. Journal of Experimental Medicine 201, 1925.CrossRefGoogle Scholar
CUSCHIERI, J., UMANSKIY, K. & SOLOMKIN, J. ( 2004). PKC-zeta is essential for endotoxin-induced macrophage activation. Journal of Surgical Research 121, 7683.CrossRefGoogle Scholar
DAVIDSON, E. A. & GOWDA, D. C. ( 2001). Glycobiology of Plasmodium falciparum. Biochimie 83, 601604.CrossRefGoogle Scholar
DE SOUZA, J. B. & RILEY, E. M. ( 2002). Cerebral malaria: the contribution of studies in animal models to our understanding of immunopathogenesis. Microbes and Infection 4, 291300.CrossRefGoogle Scholar
DE VEER, M. J., CURTIS, J. M., BALDWIN, T. M., DIDONATO, J. A., SEXTON, A., MCCONVILLE, M. J., HANDMAN, E. & SCHOFIELD, L. ( 2003). MyD88 is essential for clearance of Leishmania major: possible role for lipophosphoglycan and Toll-like receptor 2 signalling. European Journal of Immunology 33, 28222831.CrossRefGoogle Scholar
DEBIERRE-GROCKIEGO, F., AZZOUZ, N., SCHMIDT, J., DUBREMETZ, J. F., GEYER, H., GEYER, R., WEINGART, R., SCHMIDT, R. R. & SCHWARZ, R. T. ( 2003). Roles of glycosylphosphatidylinositols of Toxoplasma gondii. Induction of tumor necrosis factor-alpha production in macrophages. Journal of Biological Chemistry 278, 3298732993.Google Scholar
DELORENZI, M., SEXTON, A., SHAMS-ELDIN, H., SCHWARZ, R. T., SPEED, T. & SCHOFIELD, L. ( 2002). Genes for glycosylphosphatidylinositol toxin biosynthesis in Plasmodium falciparum. Infection and Immunity 70, 45104522.CrossRefGoogle Scholar
EISENHABER, B., BORK, P. & EISENHABER, F. ( 2001). Post-translational GPI lipid anchor modification of proteins in kingdoms of life: analysis of protein sequence data from complete genomes. Protein Engineering 14, 1725.CrossRefGoogle Scholar
EZEKOWITZ, R. A., SASTRY, K., BAILLY, P. & WARNER, A. ( 1990). Molecular characterization of the human macrophage mannose receptor: demonstration of multiple carbohydrate recognition-like domains and phagocytosis of yeasts in Cos-1 cells. Journal of Experimental Medicine 172, 17851794.CrossRefGoogle Scholar
FERGUSON, M. A., BRIMACOMBE, J. S., COTTAZ, S., FIELD, R. A., GUTHER, L. S., HOMANS, S. W., MCCONVILLE, M. J., MEHLERT, A., MILNE, K. G., RALTON, J. E. & et al. ( 1994). Glycosyl-phosphatidylinositol molecules of the parasite and the host. Parasitology 108 (Suppl.) S45S54.CrossRefGoogle Scholar
FRIEDRICHSON, T. & KURZCHALIA, T. V. ( 1998). Microdomains of GPI-anchored proteins in living cells revealed by crosslinking. Nature 394, 802805.Google Scholar
GADJEVA, M., TAKAHASHI, K. & THIEL, S. ( 2004). Mannan-binding lectin–a soluble pattern recognition molecule. Molecular Immunology 41, 113121.CrossRefGoogle Scholar
GARRED, P., NIELSEN, M. A., KURTZHALS, J. A., MALHOTRA, R., MADSEN, H. O., GOKA, B. Q., AKANMORI, B. D., SIM, R. B. & HVIID, L. ( 2003). Mannose-binding lectin is a disease modifier in clinical malaria and may function as opsonin for Plasmodium falciparum-infected erythrocytes. Infection and Immunity 71, 52455253.CrossRefGoogle Scholar
GEROLD, P., DIECKMANN-SCHUPPERT, A. & SCHWARZ, R. T. ( 1994). Glycosylphosphatidylinositols synthesized by asexual erythrocytic stages of the malarial parasite, Plasmodium falciparum. Candidates for plasmodial glycosylphosphatidylinositol membrane anchor precursors and pathogenicity factors. Journal of Biological Chemistry 269, 25972606.Google Scholar
GOWDA, D. C., GUPTA, P. & DAVIDSON, E. A. ( 1997). Glycosylphosphatidylinositol anchors represent the major carbohydrate modification in proteins of intraerythrocytic stage Plasmodium falciparum. Journal of Biological Chemistry 272, 64286439.CrossRefGoogle Scholar
GRAU, G. E., FAJARDO, L. F., PIGUET, P. F., ALLET, B., LAMBERT, .H. & VASSALLI, P. ( 1987). Tumor necrosis factor (cachectin) as an essential mediator in murine cerebral malaria. Science 237, 12101212.CrossRefGoogle Scholar
GRAU, G. E., HEREMANS, H., PIGUET, P. F., POINTAIRE, P., LAMBERT, P. H., BILLIAU, A. & VASSALLI, P. ( 1989 a). Monoclonal antibody against interferon gamma can prevent experimental cerebral malaria and its associated overproduction of tumor necrosis factor. Proceedings of the National Academy of Sciences, USA 86, 55725574.Google Scholar
GRAU, G. E., POINTAIRE, P., PIGUET, P. F., VESIN, C., ROSEN, H., STAMENKOVIC, I., TAKEI, F. & VASSALLI, P. ( 1991). Late administration of monoclonal antibody to leukocyte function-antigen 1 abrogates incipient murine cerebral malaria. European Journal of Immunology 21, 22652267.CrossRefGoogle Scholar
GRAU, G. E., TAYLOR, T. E., MOLYNEUX, M. E., WIRIMA, J. J., VASSALLI, P., HOMMEL, M. & LAMBERT, P. H. ( 1989 b). Tumor necrosis factor and disease severity in children with falciparum malaria. New England Journal of Medicine 320, 15861591.Google Scholar
GREEN, P. J., FEIZI, T., STOLL, M. S., THIEL, S., PRESCOTT, A. & MCCONVILLE, M. J. ( 1994). Recognition of the major cell surface glycoconjugates of Leishmania parasites by the human serum mannan-binding protein. Molecular and Biochemical Parasitology 66, 319328.CrossRefGoogle Scholar
HANSEN, D. S., SIOMOS, M. A., BUCKINGHAM, L., SCALZO, A. A. & SCHOFIELD, L. ( 2003). Regulation of murine cerebral malaria pathogenesis by CD1d-restricted NKT cells and the natural killer complex. Immunity 18, 391402.CrossRefGoogle Scholar
HAWN, T. R., OZINSKY, A., UNDERHILL, D. M., BUCKNER, F. S., AKIRA, S. & ADEREM, A. ( 2002). Leishmania major activates IL-1 alpha expression in macrophages through a MyD88-dependent pathway. Microbes and Infection 4, 763771.CrossRefGoogle Scholar
HENNEKE, P., TAKEUCHI, O., VAN STRIJP, J. A., GUTTORMSEN, H. K., SMITH, J. A., SCHROMM, A. B., ESPEVIK, T. A., AKIRA, S., NIZET, V., KASPER, D. L. & GOLENBOCK, D. T. ( 2001). Novel engagement of CD14 and multiple toll-like receptors by group B streptococci. Journal of Immunology 167, 70697076.CrossRefGoogle Scholar
HOREJSI, V., CEBECAUER, M., CERNY, J., BRDICKA, T., ANGELISOVA, P. & DRBAL, K. ( 1998). Signal transduction in leucocytes via GPI-anchored proteins: an experimental artefact or an aspect of immunoreceptor function? Immunology Letters 63, 6373.Google Scholar
HORNG, T., BARTON, G. M., FLAVELL, R. A. & MEDZHITOV, R. ( 2002). The adaptor molecule TIRAP provides signalling specificity for Toll-like receptors. Nature 420, 329333.CrossRefGoogle Scholar
JACOBSON, K. & DIETRICH, C. ( 1999). Looking at lipid rafts? Trends in Cell Biology 9, 8791.Google Scholar
JENNINGS, V. M., ACTOR, J. K., LAL, A. A. & HUNTER, R. L. ( 1997). Cytokine profile suggesting that murine cerebral malaria is an encephalitis. Infection and Immunity 65, 48834887.Google Scholar
KANZAKI, M., MORA, S., HWANG, J. B., SALTIEL, A. R. & PESSIN, J. E. ( 2004). Atypical protein kinase C (PKCzeta/lambda) is a convergent downstream target of the insulin-stimulated phosphatidylinositol 3-kinase and TC10 signaling pathways. Journal of Cell Biology 164, 279290.CrossRefGoogle Scholar
KASAHARA, K. & SANAI, Y. ( 2000). Functional roles of glycosphingolipids in signal transduction via lipid rafts. Glycoconjugates Journal 17, 153162.CrossRefGoogle Scholar
KLABUNDE, J., UHLEMANN, A. C., TEBO, A. E., KIMMEL, J., SCHWARZ, R. T., KREMSNER, P. G. & KUN, J. F. ( 2002). Recognition of Plasmodium falciparum proteins by mannan-binding lectin, a component of the human innate immune system. Parasitology Research 88, 113117.CrossRefGoogle Scholar
KOCH, O., AWOMOYI, A., USEN, S., JALLOW, M., RICHARDSON, A., HULL, J., PINDER, M., NEWPORT, M. & KWIATKOWSKI, D. ( 2002). IFNGR1 gene promoter polymorphisms and susceptibility to cerebral malaria. Journal of Infectious Diseases 185, 16841687.CrossRefGoogle Scholar
KRISHNEGOWDA, G. & GOWDA, D. C. ( 2003). Intraerythrocytic Plasmodium falciparum incorporates extraneous fatty acids into its lipids without any structural modification. Molecular and Biochemical Parasitology 132, 5558.CrossRefGoogle Scholar
KRISHNEGOWDA, G., HAJJAR, A. M., ZHU, J., DOUGLASS, E. J., UEMATSU, S., AKIRA, S., WOODS, A. S. & GOWDA, D. C. ( 2005). Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: cell signalling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. Journal of Biological Chemistry 280, 86068616.CrossRefGoogle Scholar
LATZ, E., SCHOENEMEYER, A., VISINTIN, A., FITZGERALD, K. A., MONKS, B. G., KNETTER, C. F., LIEN, E., NILSEN, N. J., ESPEVIK, T. & GOLENBOCK, D. T. ( 2004). TLR9 signals after translocating from the ER to CpG DNA in the lysosome. Nature Immunology 5, 190198.CrossRefGoogle Scholar
LUCAS, R., JUILLARD, P., DECOSTER, E., REDARD, M., BURGER, D., DONATI, Y., GIROUD, C., MONSO-HINARD, C., DE KESEL, T., BUURMAN, W. A., MOORE, M. W., DAYER, J. M., FIERS, W., BLUETHMANN, H. & GRAU, G. E. ( 1997). Crucial role of tumor necrosis factor (TNF) receptor 2 and membrane-bound TNF in experimental cerebral malaria. European Journal of Immunology 27, 17191725.CrossRefGoogle Scholar
LUND, J. M., ALEXOPOULOU, L., SATO, A., KAROW, M., ADAMS, N. C., GALE, N. W., IWASAKI, A. & FLAVELL, R. A. ( 2004). Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proceedings of the National Academy Sciences, USA, 101, 55985603.CrossRefGoogle Scholar
LYKE, K. E., BURGES, R., CISSOKO, Y., SANGARE, L., DAO, M., DIARRA, I., KONE, A., HARLEY, R., PLOWE, C. V., DOUMBO, O. K. & SZTEIN, M. B. ( 2004). Serum levels of the proinflammatory cytokines interleukin-1 beta (IL-1beta), IL-6, IL-8, IL-10, tumor necrosis factor alpha, and IL-12(p70) in Malian children with severe Plasmodium falciparum malaria and matched uncomplicated malaria or healthy controls. Infection and Immunity 72, 56305637.CrossRefGoogle Scholar
MAGEZ, S., STIJLEMANS, B., RADWANSKA, M., PAYS, E., FERGUSON, M. A. & DE BAETSELIER, P. ( 1998). The glycosyl-inositol-phosphate and dimyristoylglycerol moieties of the glycosylphosphatidylinositol anchor of the trypanosome variant-specific surface glycoprotein are distinct macrophage-activating factors. Journal of Immunology 160, 19491956.Google Scholar
MAYOR, S. & RIEZMAN, H. ( 2004). Sorting GPI-anchored proteins. Nature Reviews: Molecular Cell Biology 5, 110120.CrossRefGoogle Scholar
MCCONVILLE, M. J. & FERGUSON, M. A. ( 1993). The structure, biosynthesis and function of glycosylated phosphatidylinositols in the parasitic protozoa and higher eukaryotes. Biochemical Journal 294, 305324.CrossRefGoogle Scholar
MCCONVILLE, M. J. & MENON, A. K. ( 2000). Recent developments in the cell biology and biochemistry of glycosylphosphatidylinositol lipids (review). Molecular Membrane Biology 17, 116.CrossRefGoogle Scholar
MCGETTRICK, A. F. & O'NEILL, L. A. ( 2004). The expanding family of MyD88-like adaptors in Toll-like receptor signal transduction. Molecular Immunology 41, 577582.CrossRefGoogle Scholar
MCGUIRE, W., HILL, A. V., ALLSOPP, C. E., GREENWOOD, B. M. & KWIATKOWSKI, D. ( 1994). Variation in the TNF-alpha promoter region associated with susceptibility to cerebral malaria. Nature 371, 508510.CrossRefGoogle Scholar
MILLER, L. H., BARUCH, D. I., MARSH, K. & DOUMBO, O. K. ( 2002). The pathogenic basis of malaria. Nature 415, 673679.CrossRefGoogle Scholar
MITAMURA, T., HANADA, K., KO-MITAMURA, E. P., NISHIJIMA, M. & HORII, T. ( 2000). Serum factors governing intraerythrocytic development and cell cycle progression of Plasmodium falciparum. Parasitology International 49, 219229.CrossRefGoogle Scholar
MURAILLE, E., DE TREZ, C., BRAIT, M., DE BAETSELIER, P., LEO, O. & CARLIER, Y. ( 2003). Genetically resistant mice lacking MyD88-adapter protein display a high susceptibility to Leishmania major infection associated with a polarized Th2 response. Journal of Immunology 170, 42374241.CrossRefGoogle Scholar
NAGAI, Y., SHIMAZU, R., OGATA, H., AKASHI, S., SUDO, K., YAMASAKI, H., HAYASHI, S., IWAKURA, Y., KIMOTO, M. & MIYAKE, K. ( 2002). Requirement for MD-1 in cell surface expression of RP105/CD180 and B-cell responsiveness to lipopolysaccharide. Blood 99, 16991705.CrossRefGoogle Scholar
NAIK, R. S., BRANCH, O. H., WOODS, A. S., VIJAYKUMAR, M., PERKINS, D. J., NAHLEN, B. L., LAL, A. A., COTTER, R. J., COSTELLO, C. E., OCKENHOUSE, C. F., DAVIDSON, E. A. & GOWDA, D. C. ( 2000). Glycosylphosphatidylinositol anchors of Plasmodium falciparum: molecular characterization and naturally elicited antibody response that may provide immunity to malaria pathogenesis. Journal of Experimental Medicine 192, 15631576.CrossRefGoogle Scholar
O'NEILL, L. A. ( 2003). The role of MyD88-like adapters in Toll-like receptor signal transduction. Biochemical Society Transactions 31, 643647.CrossRefGoogle Scholar
PFEIFFER, A., BOTTCHER, A., ORSO, E., KAPINSKY, M., NAGY, P., BODNAR, A., SPREITZER, I., LIEBISCH, G., DROBNIK, W., GEMPEL, K., HORN, M., HOLMER, S., HARTUNG, T., MULTHOFF, G., SCHUTZ, G., SCHINDLER, H., ULMER, A. J., HEINE, H., STELTER, F., SCHUTT, C., ROTHE, G., SZOLLOSI, J., DAMJANOVICH, S. & SCHMITZ, G. ( 2001). Lipopolysaccharide and ceramide docking to CD14 provokes ligand-specific receptor clustering in rafts. European Journal of Immunology 31, 31533164.3.0.CO;2-0>CrossRefGoogle Scholar
PICHYANGKUL, S., YONGVANITCHIT, K., KUM-ARB, U., HEMMI, H., AKIRA, S., KRIEG, A. M., HEPPNER, D. G., STEWART, V. A., HASEGAWA, H., LOOAREESUWAN, S., SHANKS, G. D. & MILLER, R. S. ( 2004). Malaria blood stage parasites activate human plasmacytoid dendritic cells and murine dendritic cells through a Toll-like receptor 9-dependent pathway. Journal of Immunology 172, 49264933.CrossRefGoogle Scholar
POLTORAK, A., HE, X., SMIRNOVA, I., LIU, M. Y., VAN HUFFEL, C., DU, X., BIRDWELL, D., ALEJOS, E., SILVA, M., GALANOS, C., FREUDENBERG, M., RICCIARDI-CASTAGNOLI, P., LAYTON, B. & BEUTLER, B. ( 1998). Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282, 20852088.CrossRefGoogle Scholar
RINGWALD, P., PEYRON, F., VUILLEZ, J. P., TOUZE, J. E., LE BRAS, J. & DELORON, P. ( 1991). Levels of cytokines in plasma during Plasmodium falciparum malaria attacks. Journal of Clinical Microbiology 29, 20762078.Google Scholar
ROPERT, C., ALMEIDA, I. C., CLOSEL, M., TRAVASSOS, L. R., FERGUSON, M. A., COHEN, P. & GAZZINELLI, R. T. ( 2001). Requirement of mitogen-activated protein kinases and I kappa B phosphorylation for induction of proinflammatory cytokines synthesis by macrophages indicates functional similarity of receptors triggered by glycosylphosphatidylinositol anchors from parasitic protozoa and bacterial lipopolysaccharide. Journal of Immunology 166, 34233431.CrossRefGoogle Scholar
ROPERT, C., FERREIRA, L. R., CAMPOS, M. A., PROCOPIO, D. O., TRAVASSOS, L. R., FERGUSON, M. A., REIS, L. F., TEIXEIRA, M. M., ALMEIDA, I. C. & GAZZINELLI, R. T. ( 2002). Macrophage signaling by glycosylphosphatidylinositol-anchored mucin-like glycoproteins derived from Trypanosoma cruzi trypomastigotes. Microbes and Infection 4, 10151025.CrossRefGoogle Scholar
SCANGA, C. A., ALIBERTI, J., JANKOVIC, D., TILLOY, F., BENNOUNA, S., DENKERS, E. Y., MEDZHITOV, R. & SHER, A. ( 2002). Cutting edge: MyD88 is required for resistance to Toxoplasma gondii infection and regulates parasite-induced IL-12 production by dendritic cells. Journal of Immunology 168, 59976001.CrossRefGoogle Scholar
SCHOFIELD, L., GEROLD, P., SCHWARZ, R. T. & TACHADO, S. ( 1994). Signal transduction in host cells mediated by glycosylphosphatidylinositols of the parasitic protozoa, or why do the parasitic protozoa have so many GPI molecules? Brazilian Journal of Medical and Biological Research 27, 249254.Google Scholar
SCHOFIELD, L. & HACKETT, F. ( 1993). Signal transduction in host cells by a glycosylphosphatidylinositol toxin of malaria parasites. Journal of Experimental Medicine 177, 145153.CrossRefGoogle Scholar
SCHOFIELD, L., HEWITT, M. C., EVANS, K., SIOMOS, M. A. & SEEBERGER, P. H. ( 2002). Synthetic GPI as a candidate anti-toxic vaccine in a model of malaria. Nature 418, 785789.CrossRefGoogle Scholar
SCHOFIELD, L., NOVAKOVIC, S., GEROLD, P., SCHWARZ, R. T., MCCONVILLE, M. J. & TACHADO, S. D. ( 1996). Glycosylphosphatidylinositol toxin of Plasmodium up-regulates 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. Journal of Immunology 156, 18861896.Google Scholar
SCHOFIELD, L., VILLAQUIRAN, J., FERREIRA, A., SCHELLEKENS, H., NUSSENZWEIG, R. & NUSSENZWEIG, V. ( 1987). Gamma interferon, CD8+ T cells and antibodies required for immunity to malaria sporozoites. Nature 330, 664666.CrossRefGoogle Scholar
SCHOFIELD, L., VIVAS, L., HACKETT, F., GEROLD, P., SCHWARZ, R. T. & TACHADO, S. ( 1993). Neutralizing monoclonal antibodies to glycosylphosphatidylinositol, the dominant TNF-alpha-inducing toxin of Plasmodium falciparum: prospects for the immunotherapy of severe malaria. Annals of Tropical Medicine and Parasitology 87, 617626.CrossRefGoogle Scholar
SCHROEDER, R. J., AHMED, S. N., ZHU, Y., LONDON, E. & BROWN, D. A. ( 1998). Cholesterol and sphingolipid enhance the Triton X-100 insolubility of glycosylphosphatidylinositol-anchored proteins by promoting the formation of detergent-insoluble ordered membrane domains. Journal of Biological Chemistry 273, 11501157.CrossRefGoogle Scholar
SHARMA, P., VARMA, R., SARASIJ, R. C., IRA, gousset, K., KRISHNAMOORTHY, G., RAO, M. & MAYOR, S. ( 2004). Nanoscale organization of multiple GPI-anchored proteins in living cell membranes. Cell 116, 577589.CrossRefGoogle Scholar
SILEGHEM, M., SAYA, R., GRAB, D. J. & NAESSENS, J. ( 2001). An accessory role for the diacylglycerol moiety of variable surface glycoprotein of African trypanosomes in the stimulation of bovine monocytes. Veterinary Immunology Immunopathology 78, 325339.CrossRefGoogle Scholar
SIMONS, K. & TOOMRE, D. ( 2000). Lipid rafts and signal transduction. Nature Reviews: Molecular Cell Biology 1, 3139.CrossRefGoogle Scholar
SUGUITAN, A. L., GOWDA, D. C., FOUDA, G., THUITA, L., ZHOU, A., DJOKAM, R., METENOU, S., LEKE, R. G. & TAYLOR, D. W. ( 2004). Lack of association between antibodies to Plasmodium falciparum glycosylphosphatidylinositols and malaria-associdated placental changes in Cameroonian women with preterm and full-term deliveries. Infection and Immunity 72, 52675273.CrossRefGoogle Scholar
STEVENSON, M. M. & RILEY, E. M. ( 2004). Innate immunity to malaria. Nature Reviews Immunology 4, 169180.CrossRefGoogle Scholar
TACHADO, S. D., GEROLD, P., MCCONVILLE, M. J., BALDWIN, T., QUILICI, D., SCHWARZ, R. T. & SCHOFIELD, L. ( 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. Journal of Immunology 156, 18971907.Google Scholar
TACHADO, S. D., GEROLD, P., SCHWARZ, R., NOVAKOVIC, S., MCCONVILLE, M. & SCHOFIELD, L. ( 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. Proceedings of the National Academy Sciences, USA 94, 40224027.CrossRefGoogle Scholar
TACHADO, S. D. & SCHOFIELD, L. ( 1994). Glycosylphosphatidylinositol toxin of Trypanosoma brucei regulates IL-1 alpha and TNF-alpha expression in macrophages by protein tyrosine kinase mediated signal transduction. Biochemistry and Biophysics Research Communications 205, 984991.CrossRefGoogle Scholar
TAKEDA, K., KAISHO, T. & AKIRA, S. ( 2003). Toll-like receptors. Annual Review of Immunology 21, 335376.CrossRefGoogle Scholar
TAKEDA, K., TAKEUCHI, O. & AKIRA, S. ( 2002). Recognition of lipopeptides by Toll-like receptors. Journal of Endotoxin Research 8, 459463.CrossRefGoogle Scholar
TRIANTAFILOU, K., TRIANTAFILOU, M. & DEDRICK, R. L. ( 2001 a). A CD14-independent LPS receptor cluster. Nature Immunology 2, 338345.Google Scholar
TRIANTAFILOU, K., TRIANTAFILOU, M., LADHA, S., MACKIE, A., DEDRICK, R. L., FERNANDEZ, N. & CHERRY, R. ( 2001 b). Fluorescence recovery after photobleaching reveals that LPS rapidly transfers from CD14 to hsp70 and hsp90 on the cell membrane. Journal of Cell Science 114, 25352545.Google Scholar
TRIANTAFILOU, M., MIYAKE, K., GOLENBOCK, D. T. & TRIANTAFILOU, K. ( 2002). Mediators of innate immune recognition of bacteria concentrate in lipid rafts and facilitate lipopolysaccharide-induced cell activation. Journal of Cell Science 115, 26032611.Google Scholar
TRIANTAFILOU, M. & TRIANTAFILOU, K. ( 2002). Lipopolysaccharide recognition: CD14, TLRs and the LPS-activation cluster. Trends in Immunology 23, 301304.CrossRefGoogle Scholar
VARMA, R. & MAYOR, S. ( 1998). GPI-anchored proteins are organized in submicron domains at the cell surface. Nature 394, 798801.Google Scholar
VIJAYKUMAR, M., NAIK, R. S. & GOWDA, D. C. ( 2001). Plasmodium falciparum glycosylphosphatidylinositol-induced TNF-alpha secretion by macrophages is mediated without membrane insertion or endocytosis. Journal of Biological Chemistry 276, 69096912.CrossRefGoogle Scholar
WHITE, N. J. & HO, M. ( 1992). The pathophysiology of malaria. Advances in Parasitology. 31, 83173.CrossRefGoogle Scholar
WRIGHT, S. D., RAMOS, R. A., TOBIAS, P. S., ULEVITCH, R. J. & MATHISON, J. C. ( 1990). CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science 249, 14311433.CrossRefGoogle Scholar
YAMAMOTO, M., SATO, S., HEMMI, H., HOSHINO, K., KAISHO, T., SANJO, H., TAKEUCHI, O., SUGIYAMA, M., OKABE, M., TAKEDA, K. & AKIRA, S. ( 2003 a). Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 301, 640643.Google Scholar
YAMAMOTO, M., SATO, S., HEMMI, H., SANJO, H., UEMATSU, S., KAISHO, T., HOSHINO, K., TAKEUCHI, O., KOBAYASHI, M., FUJITA, T., TAKEDA, K. & AKIRA, S. ( 2002). Essential role for TIRAP in activation of the signalling cascade shared by TLR2 and TLR4. Nature 420, 324329.CrossRefGoogle Scholar
YAMAMOTO, M., SATO, S., HEMMI, H., UEMATSU, S., HOSHINO, K., KAISHO, T., TAKEUCHI, O., TAKEDA, K. & AKIRA, S. ( 2003 b). TRAM is specifically involved in the Toll-like receptor 4-mediated MyD88-independent signaling pathway. Nature Immunology 4, 11441150.Google Scholar
ZHU, J., KRISHNEGOWDA, G. & GOWDA, D. C. ( 2005). Induction of proinflammatory responses in macrophages by the glycophosphatidylinositols (GPIs) of Plasmodium falciparum. Journal of Biological Chemistry 280, 86178627.CrossRefGoogle Scholar