Proinflammatory responses by glycosylphosphatidylinositols (GPIs) of Plasmodium falciparum are mainly mediated through the recognition of TLR2/TLR1

Experimental Parasitology

Volumn 128, Issue 3, 2011, Pages 205-211

  Zhu, Jianzhong ^a   Krishnegowda, Gowdahalli ^a   Li, Guangfu ^a   Channe Gowda, D ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

Author keywords

Glycosylphosphatidylinositol anchors; Plasmodium falciparum; Proinflammatory responses; Recognition specificity; TLR2 TLR1 TLR6; Toll like receptors

Indexed keywords

GLYCOSYLPHOSPHATIDYLINOSITOL; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 6;

ACYLATION; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME SPECIFICITY; GENETIC POLYMORPHISM; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; MACROPHAGE; MOUSE; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; ANTIBODIES, MONOCLONAL; CYTOKINES; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION REGULATION; GLYCOSYLPHOSPHATIDYLINOSITOLS; HUMANS; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MONOCYTES; NITRIC OXIDE; PLASMODIUM FALCIPARUM; RNA, MESSENGER; SIGNAL TRANSDUCTION; SPECIFIC PATHOGEN-FREE ORGANISMS; TOLL-LIKE RECEPTOR 1; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 6;

BACTERIA (MICROORGANISMS); PLASMODIUM FALCIPARUM;

EID: 79956110876     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2011.03.010     Document Type: Article

References (42)

1. 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. Plasmodium berghei infection in mice induces liver injury by an IL-12- and toll-like receptor/myeloid differentiation factor 88-dependent mechanism. Journal of Immunology 2001, 167:5928-5934.
2. Akira S. Innate immunity to pathogens: diversity in receptors for microbial recognition. Immunological Reviews 2009, 227:5-8.
3. Butikofer P., Greganova E., Liu Y.C., Edwards I.J., Lehane M.J., Acosta-Serrano A. Lipid remodelling of glycosylphosphatidylinositol (GPI) glycoconjugates in procyclic-form trypanosomes: biosynthesis and processing of GPIs revisited. Biochemical Journal 2010, 428:409-418.
4. Chandra S., Ruhela D., Deb A., Vishwakarma R.A. Glycobiology of the Leishmania parasite and emerging targets for antileishmanial drug discovery. Expert Opinion on Therapeutic Targets 2010, 14:739-757.
5. Channe Gowda D. Structure and activity of glycosylphosphatidylinositol anchors of Plasmodium falciparum. Microbes and Infection 2002, 4:983-990.
6. Coban C., Ishii K.J., Akira S. Immune interventions of human diseases through toll-like receptors. Advances in Experimental Medicine and Biology 2009, 655:63-80.
7. Coban C., Ishii K.J., Uematsu S., Arisue N., Sato S., Yamamoto M., Kawai T., Takeuchi O., Hisaeda H., Horii T., Akira S. Pathological role of Toll-like receptor signaling in cerebral malaria. Intinonal Immunology 2007, 19:67-79.
8. Couper K.N., Barnes T., Hafalla J.C., Combes V., Ryffel B., Secher T., Grau G.E., Riley E.M., de Souza J.B. Parasite-derived plasma microparticles contribute significantly to malaria infection-induced inflammation through potent macrophage stimulation. PLoS Pathogens 2010, 6:e1000744.
9. de Veer M.J., Curtis J.M., Baldwin T.M., DiDonato J.A., Sexton A., McConville M.J., Handman E., Schofield L. MyD88 is essential for clearance of Leishmania major: possible role for lipophosphoglycan and Toll-like receptor 2 signaling. European Journal of Immunology 2003, 33:2822-2831.
10. Debierre-Grockiego F., Campos M.A., Azzouz N., Schmidt J., Bieker U., Resende M.G., Mansur D.S., Weingart R., Schmidt R.R., Golenbock D.T., Gazzinelli R.T., Schwarz R.T. Activation of TLR2 and TLR4 by glycosylphosphatidylinositols derived from Toxoplasma gondii. Journal of Immunology 2007, 179:1129-1137.
11. Debierre-Grockiego F., Schwarz R.T. Immunological reactions in response to apicomplexan glycosylphosphatidylinositols. Glycobiology 2010, 20:801-811.
12. Drage M.G., Pecora N.D., Hise A.G., Febbraio M., Silverstein R.L., Golenbock D.T., Boom W.H., Harding C.V. TLR2 and its co-receptors determine responses of macrophages and dendritic cells to lipoproteins of Mycobacterium tuberculosis. Cellular Immunology 2009, 258:29-37.
13. Ferguson M.A. The structure, biosynthesis and functions of glycosylphosphatidylinositol anchors, and the contributions of trypanosome research. Journal of Cell Science 1999, 112(Pt 17):2799-2809.
14. Figueiredo R.T., Fernandez P.L., Mourao-Sa D.S., Porto B.N., Dutra F.F., Alves L.S., Oliveira M.F., Oliveira P.L., Graca-Souza A.V., Bozza M.T. Characterization of heme as activator of Toll-like receptor 4. Journal of Biological Chemistry 2007, 282:20221-20229.
15. Franklin B.S., Rodrigues S.O., Antonelli L.R., Oliveira R.V., Goncalves A.M., Sales-Junior P.A., Valente E.P., Alvarez-Leite J.I., Ropert C., Golenbock D.T., Gazzinelli R.T. MyD88-dependent activation of dendritic cells and CD4(+) T lymphocytes mediates symptoms, but is not required for the immunological control of parasites during rodent malaria. Microbes and Infection 2007, 9:881-890.
16. Gowda D.C. TLR-mediated cell signaling by malaria GPIs. Trends in Parasitology 2007, 23:596-604.
17. Hamann L., Bedu-Addo G., Eggelte T.A., Schumann R.R., Mockenhaupt F.P. The toll-like receptor 1 variant S248N influences placental malaria. Infection, Genetics and Evolution 2010, 10:785-789.
18. Khor C.C., Chapman S.J., Vannberg F.O., Dunne A., Murphy C., Ling E.Y., Frodsham A.J., Walley A.J., Kyrieleis O., Khan A., Aucan C., Segal S., Moore C.E., Knox K., Campbell S.J., Lienhardt C., Scott A., Aaby P., Sow O.Y., Grignani R.T., Sillah J., Sirugo G., Peshu N., Williams T.N., Maitland K., Davies R.J., Kwiatkowski D.P., Day N.P., Yala D., Crook D.W., Marsh K., Berkley J.A., O'Neill L.A., Hill A.V. A Mal functional variant is associated with protection against invasive pneumococcal disease, bacteremia, malaria and tuberculosis. Nature Genetics 2007, 39:523-528.
19. Krishnegowda G., Hajjar A.M., Zhu J., Douglass E.J., Uematsu S., Akira S., Woods A.S., Gowda D.C. Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. Journal of Biological Chemistry 2005, 280:8606-8616.
20. Lepenies B., Cramer J.P., Burchard G.D., Wagner H., Kirschning C.J., Jacobs T. Induction of experimental cerebral malaria is independent of TLR2/4/9. Medical Microbiology and Immunology 2008, 197:39-44.
21. Mockenhaupt F.P., Cramer J.P., Hamann L., Stegemann M.S., Eckert J., Oh N.R., Otchwemah R.N., Dietz E., Ehrhardt S., Schroder N.W., Bienzle U., Schumann R.R. Toll-like receptor (TLR) polymorphisms in African children: Common TLR-4 variants predispose to severe malaria. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:177-182.
22. Mockenhaupt F.P., Hamann L., von Gaertner C., Bedu-Addo G., von Kleinsorgen C., Schumann R.R., Bienzle U. Common polymorphisms of toll-like receptors 4 and 9 are associated with the clinical manifestation of malaria during pregnancy. Journal of Infectious Diseases 2006, 194:184-188.
23. 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. Glycosylphosphatidylinositol anchors of Plasmodium falciparum: molecular characterization and naturally elicited antibody response that may provide immunity to malaria pathogenesis. Journal of Experimental Medicine 2000, 192:1563-1576.
24. Nakao Y., Funami K., Kikkawa S., Taniguchi M., Nishiguchi M., Fukumori Y., Seya T., Matsumoto M. Surface-expressed TLR6 participates in the recognition of diacylated lipopeptide and peptidoglycan in human cells. Journal of Immunology 2005, 174:1566-1573.
25. Parroche P., Lauw F.N., Goutagny N., Latz E., Monks B.G., Visintin A., Halmen K.A., Lamphier M., Olivier M., Bartholomeu D.C., Gazzinelli R.T., Golenbock D.T. Malaria hemozoin is immunologically inert but radically enhances innate responses by presenting malaria DNA to Toll-like receptor 9. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:1919-1924.
26. Paulick M.G., Bertozzi C.R. The glycosylphosphatidylinositol anchor: a complex membrane-anchoring structure for proteins. Biochemistry 2008, 47:6991-7000.
27. 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. Malaria blood stage parasites activate human plasmacytoid dendritic cells and murine dendritic cells through a Toll-like receptor 9-dependent pathway. Journal of Immunology 2004, 172:4926-4933.
28. Riley E.M., Wahl S., Perkins D.J., Schofield L. Regulating immunity to malaria. Parasite Immunology 2006, 28:35-49.
29. Ropert C., Gazzinelli R.T. Regulatory role of Toll-like receptor 2 during infection with Trypanosoma cruzi. Journal of Endotoxin Research 2004, 10:425-430.
30. Schofield L., Grau G.E. Immunological processes in malaria pathogenesis. Nature Reviews Immunology 2005, 5:722-735.
31. Schofield L., Hackett F. Signal transduction in host cells by a glycosylphosphatidylinositol toxin of malaria parasites. Journal of Experimental Medicine 1993, 177:145-153.
32. Stevenson M.M., Riley E.M. Innate immunity to malaria. Nature Reviews Immunology 2004, 4:169-180.
33. Takeda K., Takeuchi O., Akira S. Recognition of lipopeptides by Toll-like receptors. Journal of Endotoxin Research 2002, 8:459-463.
34. Takeuchi O., Kawai T., Muhlradt P.F., Morr M., Radolf J.D., Zychlinsky A., Takeda K., Akira S. Discrimination of bacterial lipoproteins by Toll-like receptor 6. International Immunology 2001, 13:933-940.
35. Takeuchi O., Sato S., Horiuchi T., Hoshino K., Takeda K., Dong Z., Modlin R.L., Akira S. Cutting edge: role of Toll-like receptor 1 in mediating immune response to microbial lipoproteins. Journal of Immunology 2002, 169:10-14.
36. Tapping R.I., Tobias P.S. Mycobacterial lipoarabinomannan mediates physical interactions between TLR1 and TLR2 to induce signaling. Journal of Endotoxin Research 2003, 9:264-268.
37. Torre D., Speranza F., Martegani R. Role of proinflammatory and anti-inflammatory cytokines in the immune response to Plasmodium falciparum malaria. Lancet Infectious Diseases 2002, 2:719-720.
38. Vijaykumar M., Naik R.S., Gowda D.C. Plasmodium falciparum glycosylphosphatidylinositol-induced TNF-alpha secretion by macrophages is mediated without membrane insertion or endocytosis. Journal of Biological Chemistry 2001, 276:6909-6912.
39. Wieland C.W., Knapp S., Florquin S., de Vos A.F., Takeda K., Akira S., Golenbock D.T., Verbon A., van der Poll T. Non-mannose-capped lipoarabinomannan induces lung inflammation via toll-like receptor 2. American Journal of Respiratory and Critical Care Medicine 2004, 170:1367-1374.
40. Wu X., Gowda N.M., Kumar S., Gowda D.C. Protein-DNA complex is the exclusive malaria parasite component that activates dendritic cells and triggers innate immune responses. Journal of Immunology 2010, 184:4338-4348.
41. Wurfel M.M., Gordon A.C., Holden T.D., Radella F., Strout J., Kajikawa O., Ruzinski J.T., Rona G., Black R.A., Stratton S., Jarvik G.P., Hajjar A.M., Nickerson D.A., Rieder M., Sevransky J., Maloney J.P., Moss M., Martin G., Shanholtz C., Garcia J.G., Gao L., Brower R., Barnes K.C., Walley K.R., Russell J.A., Martin T.R. Toll-like receptor 1 polymorphisms affect innate immune responses and outcomes in sepsis. American Journal of Respiratory and Critical Care Medicine 2008, 178:710-720.
42. Zhu J., Krishnegowda G., Gowda D.C. Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: the requirement of extracellular signal-regulated kinase, p38, c-Jun N-terminal kinase and NF-kappaB pathways for the expression of proinflammatory cytokines and nitric oxide. Journal of Biological Chemistry 2005, 280:8617-8627.