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The Journal of Immunology, 2001, 167: 416-423.
Copyright © 2001 by The American Association of Immunologists

Activation of Toll-Like Receptor-2 by Glycosylphosphatidylinositol Anchors from a Protozoan Parasite1

Marco A. S. Campos*, Igor C. Almeida{dagger}, Osamu Takeuchi{ddagger}, Shizuo Akira{ddagger}, Eneida P. Valente*, Daniela O. Procópio*, Luiz R. Travassos§, Jason A. Smith, Douglas T. Golenbock and Ricardo T. Gazzinelli2,*

* Department of Biochemistry and Immunology, Biological Sciences Institute, Federal University of Minas Gerais and Centro de Pesquisas René Rachou, Oswaldo Cruz Foundation, Belo Horizonte, Brazil; {dagger} Department of Parasitology, University of Sao Paulo, Sao Paulo, Brazil; {ddagger} Department of Host Defense, Research Institute for Microbial Diseases, Osaka University, Osaka, Japan; § Unit for Experimental Oncology, Federal University of Sao Paulo, Sao Paulo, Brazil; and Boston University School of Medicine, Boston, MA 02118

Glycosylphosphatidylinositol (GPI) anchors and glycoinositolphospholipids (GIPLs) from parasitic protozoa have been shown to exert a wide variety of effects on cells of the host innate immune system. However, the receptor(s) that are triggered by these protozoan glycolipids has not been identified. Here we present evidence that Trypanosoma cruzi-derived GPI anchors and GIPLs trigger CD25 expression on Chinese hamster ovary-K1 cells transfected with CD14 and Toll-like receptor-2 (TLR-2), but not wild-type (TLR-2-deficient) Chinese hamster ovary cells. The protozoan-derived GPI anchors and GIPLs containing alkylacylglycerol and saturated fatty acid chains or ceramide were found to be active in a concentration range of 100 nM to 1 µM. More importantly, the GPI anchors purified from T. cruzi trypomastigotes, which contain a longer glycan core and unsaturated fatty acids in the sn-2 position of the alkylacylglycerolipid component, triggered TLR-2 at subnanomolar concentrations. We performed experiments with macrophages from TLR-2 knockout and TLR-4 knockout mice, and found that TLR-2 expression appears to be essential for induction of IL-12, TNF-{alpha}, and NO by GPI anchors derived from T. cruzi trypomastigotes. Thus, highly purified GPI anchors from T. cruzi parasites are potent activators of TLR-2 from both mouse and human origin. The activation of TLR-2 may initiate host innate defense mechanisms and inflammatory response during protozoan infection, and may provide new strategies for immune intervention during protozoan infections.




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M. Skold and S. M. Behar
Role of CD1d-Restricted NKT Cells in Microbial Immunity
Infect. Immun., October 1, 2003; 71(10): 5447 - 5455.
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Infect. Immun.Home page
C. S. Eickhoff, L. Eckmann, and D. F. Hoft
Differential Interleukin-8 and Nitric Oxide Production in Epithelial Cells Induced by Mucosally Invasive and Noninvasive Trypanosoma cruzi Trypomastigotes
Infect. Immun., September 1, 2003; 71(9): 5394 - 5397.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
F. Debierre-Grockiego, N. Azzouz, J. Schmidt, J.-F. Dubremetz, H. Geyer, R. Geyer, R. Weingart, R. R. Schmidt, and R. T. Schwarz
Roles of Glycosylphosphatidylinositols of Toxoplasma gondii: INDUCTION OF TUMOR NECROSIS FACTOR-{alpha} PRODUCTION IN MACROPHAGES
J. Biol. Chem., August 29, 2003; 278(35): 32987 - 32993.
[Abstract] [Full Text] [PDF]


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Infect. Immun.Home page
C. A. Petersen and B. A. Burleigh
Role for Interleukin-1{beta} in Trypanosoma cruzi-Induced Cardiomyocyte Hypertrophy
Infect. Immun., August 1, 2003; 71(8): 4441 - 4447.
[Abstract] [Full Text] [PDF]


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Innate ImmunityHome page
R. I. Tapping and P. S. Tobias
Mycobacterial lipoarabinomannan mediates physical interactions between TLR1 and TLR2 to induce signaling
Innate Immunity, August 1, 2003; 9(4): 264 - 268.
[Abstract] [PDF]


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J. Immunol.Home page
C. Ropert, M. Closel, A. C. L. Chaves, and R. T. Gazzinelli
Inhibition of a p38/Stress-Activated Protein Kinase-2-Dependent Phosphatase Restores Function of IL-1 Receptor-Associated Kinase-1 and Reverses Toll-Like Receptor 2- and 4-Dependent Tolerance of Macrophages
J. Immunol., August 1, 2003; 171(3): 1456 - 1465.
[Abstract] [Full Text] [PDF]


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Infect. Immun.Home page
C. S. Boutlis, E. Tjitra, H. Maniboey, M. A. Misukonis, J. R. Saunders, S. Suprianto, J. B. Weinberg, and N. M. Anstey
Nitric Oxide Production and Mononuclear Cell Nitric Oxide Synthase Activity in Malaria-Tolerant Papuan Adults
Infect. Immun., July 1, 2003; 71(7): 3682 - 3689.
[Abstract] [Full Text] [PDF]


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Infect. Immun.Home page
N. Delgado, J. Xue, J.-J. Yu, C.-Y. Hung, and G. T. Cole
A Recombinant {beta}-1,3-Glucanosyltransferase Homolog of Coccidioides posadasii Protects Mice against Coccidioidomycosis
Infect. Immun., June 1, 2003; 71(6): 3010 - 3019.
[Abstract] [Full Text] [PDF]


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BloodHome page
N. L. Bernasconi, N. Onai, and A. Lanzavecchia
A role for Toll-like receptors in acquired immunity: up-regulation of TLR9 by BCR triggering in naive B cells and constitutive expression in memory B cells
Blood, June 1, 2003; 101(11): 4500 - 4504.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
T. K. Means, F. Hayashi, K. D. Smith, A. Aderem, and A. D. Luster
The Toll-Like Receptor 5 Stimulus Bacterial Flagellin Induces Maturation and Chemokine Production in Human Dendritic Cells
J. Immunol., May 15, 2003; 170(10): 5165 - 5175.
[Abstract] [Full Text] [PDF]


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Sci SignalHome page
A. Dunne and L. A. J. O'Neill
The Interleukin-1 Receptor/Toll-Like Receptor Superfamily: Signal Transduction During Inflammation and Host Defense
Sci. Signal., February 25, 2003; 2003(171): re3 - re3.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
L. R. P. Ferreira, E. F. Abrantes, C. V. Rodrigues, B. Caetano, G. C. Cerqueira, A. C. Salim, L. F. L. Reis, and R. T. Gazzinelli
Identification and characterization of a novel mouse gene encoding a Ras-associated guanine nucleotide exchange factor: expression in macrophages and myocarditis elicited by Trypanosoma cruzi parasites
J. Leukoc. Biol., December 1, 2002; 72(6): 1215 - 1227.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
D. O. Procopio, I. C. Almeida, A. C. T. Torrecilhas, J. E. Cardoso, L. Teyton, L. R. Travassos, A. Bendelac, and R. T. Gazzinelli
Glycosylphosphatidylinositol-Anchored Mucin-Like Glycoproteins from Trypanosoma cruzi Bind to CD1d but Do Not Elicit Dominant Innate or Adaptive Immune Responses Via the CD1d/NKT Cell Pathway
J. Immunol., October 1, 2002; 169(7): 3926 - 3933.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
K. Artavanis-Tsakonas and E. M. Riley
Innate Immune Response to Malaria: Rapid Induction of IFN-{gamma} from Human NK Cells by Live Plasmodium falciparum-Infected Erythrocytes
J. Immunol., September 15, 2002; 169(6): 2956 - 2963.
[Abstract] [Full Text] [PDF]


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Infect. Immun.Home page
J. B. de Souza, J. Todd, G. Krishegowda, D. C. Gowda, D. Kwiatkowski, and E. M. Riley
Prevalence and Boosting of Antibodies to Plasmodium falciparum Glycosylphosphatidylinositols and Evaluation of Their Association with Protection from Mild and Severe Clinical Malaria
Infect. Immun., September 1, 2002; 70(9): 5045 - 5051.
[Abstract] [Full Text] [PDF]


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Int ImmunolHome page
S. E. Applequist, R. P. A. Wallin, and H.-G. Ljunggren
Variable expression of Toll-like receptor in murine innate and adaptive immune cell lines
Int. Immunol., September 1, 2002; 14(9): 1065 - 1074.
[Abstract] [Full Text] [PDF]


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Clin. Microbiol. Rev.Home page
J. Caamano and C. A. Hunter
NF-{kappa}B Family of Transcription Factors: Central Regulators of Innate and Adaptive Immune Functions
Clin. Microbiol. Rev., July 1, 2002; 15(3): 414 - 429.
[Abstract] [Full Text] [PDF]


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Infect. Immun.Home page
C. Brodskyn, J. Patricio, R. Oliveira, L. Lobo, A. Arnholdt, L. Mendonca-Previato, A. Barral, and M. Barral-Netto
Glycoinositolphospholipids from Trypanosoma cruzi Interfere with Macrophages and Dendritic Cell Responses
Infect. Immun., July 1, 2002; 70(7): 3736 - 3743.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
O. Takeuchi, S. Sato, T. Horiuchi, K. Hoshino, K. Takeda, Z. Dong, R. L. Modlin, and S. Akira
Cutting Edge: Role of Toll-Like Receptor 1 in Mediating Immune Response to Microbial Lipoproteins
J. Immunol., July 1, 2002; 169(1): 10 - 14.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
C. A. Scanga, J. Aliberti, D. Jankovic, F. Tilloy, S. Bennouna, E. Y. Denkers, R. Medzhitov, and A. Sher
Cutting Edge: MyD88 Is Required for Resistance to Toxoplasma gondii Infection and Regulates Parasite-Induced IL-12 Production by Dendritic Cells
J. Immunol., June 15, 2002; 168(12): 5997 - 6001.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
A. Ouaissi, E. Guilvard, Y. Delneste, G. Caron, G. Magistrelli, N. Herbault, N. Thieblemont, and P. Jeannin
The Trypanosoma cruzi Tc52-Released Protein Induces Human Dendritic Cell Maturation, Signals Via Toll-Like Receptor 2, and Confers Protection Against Lethal Infection
J. Immunol., June 15, 2002; 168(12): 6366 - 6374.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
P. S. Coelho, A. Klein, A. Talvani, S. F. Coutinho, O. Takeuchi, S. Akira, J. S. Silva, H. Canizzaro, R. T. Gazzinelli, and M. M. Teixeira
Glycosylphosphatidylinositol-anchored mucin-like glycoproteins isolated from Trypanosoma cruzi trypomastigotes induce in vivo leukocyte recruitment dependent on MCP-1 production by IFN-{gamma}-primed-macrophages
J. Leukoc. Biol., May 1, 2002; 71(5): 837 - 844.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
A. Fox-Marsh and L. C. Harrison
Emerging evidence that molecules expressed by mammalian tissue grafts are recognized by the innate immune system
J. Leukoc. Biol., March 1, 2002; 71(3): 401 - 409.
[Abstract] [Full Text] [PDF]


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J. Immunol.Home page
K. Adachi, H. Tsutsui, S.-I. Kashiwamura, E. Seki, H. Nakano, O. Takeuchi, K. Takeda, K. Okumura, L. Van Kaer, H. Okamura, et al.
Plasmodiumberghei Infection in Mice Induces Liver Injury by an IL-12- and Toll-Like Receptor/Myeloid Differentiation Factor 88-Dependent Mechanism
J. Immunol., November 15, 2001; 167(10): 5928 - 5934.
[Abstract] [Full Text] [PDF]


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J. Leukoc. Biol.Home page
I. C. Almeida and R. T. Gazzinelli
Proinflammatory activity of glycosylphosphatidylinositol anchors derived from Trypanosoma cruzi: structural and functional analyses
J. Leukoc. Biol., October 1, 2001; 70(4): 467 - 477.
[Abstract] [Full Text] [PDF]




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