Sialylated ligands on pathogenic Trypanosoma cruzi interact with Siglec-E (sialic acid-binding Ig-like lectin-E)

Cellular Microbiology

Volumn 11, Issue 11, 2009, Pages 1600-1611

  Erdmann, Hanna ^a   Steeg, Christiane ^a   Koch Nolte, Friedrich ^b   Fleischer, Bernhard ^a,b   Jacobs, Thomas ^a  

^a BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 12; LECTIN; SIALIC ACID BINDING IMMUNOGLOBULIN LIKE LECTIN E; SIALIDASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW; CELL FUNCTION; CHAGAS DISEASE; CHO CELL; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; ENZYME ACTIVITY; HOST PATHOGEN INTERACTION; IMMUNOMODULATION; IN VITRO STUDY; LIGAND BINDING; MALE; MOUSE; NONHUMAN; PARASITE VIRULENCE; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN SYNTHESIS INHIBITION; SIALYLATION; STRAIN DIFFERENCE; T LYMPHOCYTE ACTIVATION; TRYPANOSOMA CRUZI;

ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, B-LYMPHOCYTE; DENDRITIC CELLS; GLYCOPROTEINS; INTERLEUKIN-12; LIGANDS; LYMPHOCYTE ACTIVATION; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEURAMINIDASE; PROTEIN BINDING; SIALIC ACIDS; TRYPANOSOMA CRUZI; VIRULENCE FACTORS;

MUS; TRYPANOSOMA CRUZI;

EID: 72749104617     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2009.01350.x     Document Type: Article

References (52)

1. Abrahamsohn, I.A. (1998) Cytokines in innate and acquired immunity to Trypanosoma cruzi infection. Braz J Med Biol Res 31: 117-121
2. Aliberti, J.C., Cardoso, M.A., Martins, G.A., Gazzinelli, R.T., Vieira, L.Q., and Silva, J.S. (1996) Interleukin-12 mediates resistance to Trypanosoma cruzi in mice and is produced by murine macrophages in response to live trypomastigotes. Infect Immun 64: 1961-1967.
3. Ando, M., Tu, W., Nishijima, K., and Iijima, S. (2008) Siglec-9 enhances IL-10 production in macrophages via tyrosinebased motifs. Biochem Biophys Res Commun 369: 878- 883
4. Argibay, P.F., Di Noia, J.M., Hidalgo, A., Mocetti, E., Barbich, M., Lorenti, A.S., et al. (2002) Trypanosoma cruzi surface mucin TcMuc-e2 expressed on higher eukaryotic cells induces human T cell anergy, which is reversible. Glycobiology 12: 25-32
5. Barrett, M.P., Burchmore, R.J., Stich, A., Lazzari, J.O., Frasch, A.C., Cazzulo, J.J., and Krishna, S. (2003) The trypanosomiases. Lancet 362: 1469-1480.
6. Blasius, A.L., Cella, M., Maldonado, J., Takai, T., and Colonna, M. (2006) Siglec-H is an IPC-specific receptor that modulates type I IFN secretion through DAP12. Blood 107: 2474-2476.
7. Blixt, O., Head, S., Mondala, T., Scanlan, C., Huflejt, M.E., Alvarez, R., et al. (2004) Printed covalent glycan array for ligand profiling of diverse glycan binding proteins. Proc Natl Acad Sci USA 101: 17033-17038.
8. Burleigh, B.A., and Andrews, N.W. (1995) A 120 kDa alkaline peptidase from Trypanosoma cruzi is involved in the generation of a novel Ca2+ signaling factor for mammalian cells. J Biol Chem 270: 5172-5180.
9. Buscaglia, C.A., Campo, V.A., Frasch, A.C., and Di Noia, J.M. (2006) Trypanosoma cruzi surface mucins: hostdependent coat diversity. Nat Rev Microbiol 4: 229-236.
10. Buschiazzo, A., Amaya, M.F., Cremona, M.L., Frasch, A.C., and Alzari, P.M. (2002) The crystal structure and mode of action of trans-sialidase, a key enzyme in Trypanosoma cruzi pathogenesis. Mol Cell 10: 757-768
11. Carlin, A.F., Lewis, A.L., Varki, A., and Nizet, V. (2007) Group B streptococcal capsular sialic acids interact with Siglecs (immunoglobulin-like lectins) on human leukocytes. J Bacteriol 189: 1231-1237.
12. Carlin, A.F., Uchiyama, S., Chang, Y.C., Lewis, A.L., Nizet, V., and Varki, A. (2009) Molecular mimicry of host sialylated glycans allows a bacterial pathogen to engage neutrophil Siglec-9 and dampen the innate immune response. Blood 113: 3333-3336
13. Colli, W. (1993) Trans-sialidase: a unique enzyme activity discovered in the protozoan Trypanosoma cruzi. FASEB J 7: 1257-1264.
14. Crocker, P.R., Paulson, J.C., and Varki, A. (2007) Siglecs and their roles in the immune system. Nat Rev Immunol 7: 255-266.
15. DosReis, G.A., Freire-de-Lima, C.G., Nunes, M.P., and Lopez, M.F. (2005) The importance of aberrant T-cell responses in Chagas' disease. Trends Parasitol 21: 237- 243.
16. Dvorak, J.A. (1984) The natural heterogeneity of Trypanosoma cruzi biological and medical implication. J Cell Biochem 24: 357-371.
17. Frasch, A.C. (2000) Functional diversity in the trans-sialidase and mucin families in Trypanosoma cruzi. Parasitol Today 16: 282-286.
18. Frosch, S., Kraus, S., and Fleischer, B. (1996) Trypanosoma cruzi is a potent inducer of interleukin-12 production in macrophages. Med Microbiol Immunol 185: 189-193.
19. Golden, M.J., and Tarleton, R.L. (1991) Trypanosoma cruzi: cytokine effects on macrophage trypanocidal activity. Exp Parasitol 72: 391-402.
20. Hoelscher, C., Kohler, G., Muller, U., Mossmann, H., Schaub, G.A., and Brombacher, F. (1998) Defective nitric oxide effector functions lead to extreme susceptibility of Trypanosoma cruzi-infected mice deficient in gamma interferon receptor or inducible nitric oxide synthase. Infect Immun 66: 1208-1215.
21. Hunter, C.A., Ellis-Neyes, L.A., Slifer, T., Canaly, S., Grunig, G., Fort, M., et al. (1997) IL-10 is required to prevent immune hyperactivity during infection with Trypanosoma cruzi. J Immunol 158: 3311-3316.
22. Joiner, K., Sher, A., Gaither, T., and Hammer, C. (1986) Evasion of alternative complement pathway by Trypanosoma cruzi results from inefficient binding of factor B. Proc Natl Acad Sci USA 83: 6593-6597.
23. Kaye, P.M., Rogers, N.J., Curry, A.J., and Scott, J.C. (1994) Deficient expression of co-stimulatory molecules on Leishmania-infected macrophages. Eur J Immunol 24: 2850-2854.
24. Kierszenbaum, F. (1982) Immunologic deficiency during experimental Chagas' disease (Trypanosoma cruzi infection): role of adherent, non-specific esterase-positive splenic cells. J Immunol 129: 2202-2205.
25. Kumar, S., and Tarleton, R.L. (2001) Antigen-specific Th1 but not Th2 cells provide protection from lethal Trypanosoma cruzi infection in mice. J Immunol 166: 4596-4603.
26. Lieke, T., Graefe, S.E., Klauenberg, U., Fleischer, B., and Jacobs, T. (2004) NK cells contribute to the control of Trypanosoma cruzi infection by killing free parasites by perforin-independent mechanisms. Infect Immun 72: 6817-6825.
27. Lutz, M.B., Kukutsch, N., Ogilvie, A.L., Rossner, S., Koch, F., Romani, N., and Schuler, G. (1999) An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods 223: 77-92.
28. Meyer zum Bueschenfelde, C., Cramer, S., Trumpfheller, C., Fleischer, B., and Frosch, S. (1997) Trypanosoma cruzi induces strong IL-12 and IL-18 gene expression in vivo: correlation with interferon-gamma (IFN-gamma) production. Clin Exp Immunol 110: 378-385.
29. Monteiro, V.G., Lobato, C.S.S., Silva, A.R., Medina, D.V., de Oliveira, M.A., Seabra, S.H., et al. (2005) Increased association of Trypanosoma cruzi with sialoadhesin positive mice macrophages. Parasitol Res 97: 380-385.
30. Pereira-Chioccola, V.L., Acosta-Serrano, A., Correira de Almeida, I., Ferguson, M.A., Souto-Padron, T., Rodrigues, M.M., et al. (2000) Mucin-like molecules from a negatively charged coat that protects Trypanosoma cruzi trypomastigotes from killing by human anti-a-galactosyl antibodies. J Cell Sci 113: 1299-1307.
31. Poncini, C.V., Alba Soto, C.D., Batalla, E., Solana, M.E., and Gonzalez Cappa, S.M. (2008) Trypanosoma cruzi induces regulatory dendritic cells in vitro. Infect Immun 76: 2633- 2641.
32. Ravetch, J.V., and Lanier, L.L. (2000) Immune inhibitory receptors. Science 290: 84-89.
33. Reed, S.G., Brownell, C.E., Russo, D.M., Silva, J.S., Grabstein, K.H., and Morrissey, P.J. (1994) IL-10 mediates susceptibility to Trypanosoma cruzi infection. J Immunol 153: 3135-3140.
34. Rempel, H., Calosing, C., Sun, B., and Pulliam, L. (2008). Sialoadhesin expressed on IFN-induced monocytes binds HIV-1 and enhances infectivity. PloS ONE 3: e1967.
35. Risso, M.G., Garbarino, G.B., Mocetti, E., Campetella, O., González Cappa, S.M., Buscaglia, C.A., and Leguizamón, M.S. 2004 Differential expression of a virulence factor, the trans-sialidase, by the main Trypanosoma cruzi phylogenetic lineages. J Infect Dis 189: 2250-2259.
36. Saeftel, M., Fleischer, B., and Hoerauf, A. (2001) Stagedependent role of nitric oxide in control of Trypanosoma cruzi infection. Infect Immun 69: 2252-2259.
37. Saha, B., Das, G., Vohra, H., Ganguly, N.K., and Mishra, G.C. (1994) Macrophage-T cell interaction in experimental mycobacterial infection. Selective regulation of co-stimulatory molecules on Mycobacterium-infected macrophages and its implication in the suppression of cellmediated immune response. Eur J Immunol 24: 2618- 2624.
38. Saha, B., Das, G., Vohra, H., Ganguly, N.K., and Mishra, G.C. (1995) Macrophage-T cell interaction in experimental visceral leishmaniasis: failure to express costimulatory molecules on Leishmania-infected macrophages and its implication in the suppression of cell-mediated immunity. Eur J Immunol 25: 2492-2498.
39. Schenkman, S., Eichinger, D., Pereira, M.E., and Nussenzweig, V. (1994) Structural and functional properties of Trypanosoma trans-sialidase. Annu Rev Microbiol 48: 299-323.
40. Souto, R.P., Fernandes, O., Macedo, A.M., Campbell, D.A., and Zingales, B. (1996) DNA markers define two major phylogenetic lineages of Trypanosoma cruzi. Mol Biochem Parasitol 83: 141-152.
41. Tarleton, R.L. (2001) Parasite persistence in the aetiology of Chagas' disease. Int J Parasitol 21: 550-554. Tarleton, R.L. (2003) Chagas' disease: a role for autoimmunity? Trends Parasitol 19: 447-451.
42. Tarleton, R.L., and Zhang, L. (1999) Chagas' disease etiology: autoimmunity or parasite persistence? Parasitol Today 15: 94-99.
43. Tibayrenc, M. (1998) Genetic epidemiology of parasitic protozoa and other infectious agents: the need for an integrated approach. Int J Parasitol 28: 85-104.
44. Tomlinson, S., Pontes de Carvalho, L.C., Vandekerckhove, F., and Nussenzweig, V. (1994) Role of sialic acid in the resistance of Trypanosoma cruzi trypomastigotes to complement. J Immunol 153: 3141-3147.
45. Van Overtvelt, L., Andrieu, M., Verhasselt, V., Connan, F., Choppin, J., Vercruysse, V., et al. (2002) Trypanosoma cruzi down-regulates lipopolysaccharide-induced MHC class I on human dendritic cells and impairs antigen presentation to specific CD8(+) T lymphocytes. Int Immunol 14: 1135-1144.
46. Vandekerckhove, F., Schenkman, S., Pontes de Carvalho, L., Tomlinson, S., Kiso, M., Yoshida, M., et al. (1992) Substrate specificity of the Trypanosoma cruzi trans-sialidase. Glycobiology 2: 541-548.
47. Varki, A., and Angata, T. (2006) Siglecs - the major subfamily of I-type lectins. Glycobiology 16: 1R-27R.
48. Williams-Blangero, S., VandeBerg, J.L., Blangero, J., and Correa-Oliveira, R. (2003) Genetic epidemiology of Trypanosoma cruzi infection and Chagas' disease. Front Biosci 8: e337-e345.
49. Wilson, J.C., Kiefel, M.J., Albouz-Abo, S., and von Itzstein, M. (2000) Preliminary 1H NMR investigation of sialic acid transfer by the trans-sialidase from Trypanosoma cruzi. Bioorg Med Chem Lett 10: 2791-2794.
50. Zhang, J., Raper, A., Sugita, N., Hingorani, R., Salio, M., Palmowski, M.J., et al. (2006) Characterization of Siglec-H as a novel endocytic receptor expressed on murine plasmacytoid dendritic cell precursors. Blood 107: 3600- 3608.
51. Zhang, J.Q., Biedermann, B., Nitschke, L., and Crocker, P.R. (2004) The murine inhibitory receptor mSiglec-E is expressed broadly on cells of the innate immune system whereas mSiglec-F is restricted to eosinophils. Eur J Immunol 34: 1175-1184.
52. Zingales, B., Stolf, B., Souto, R., Fernandes, O., and Briones, M. 1999 Epidemiology, biochemistry and evolution of Trypanosoma cruzi lineages based on ribosomal RNA sequences. Mem Inst Oswaldo Cruz 94: 159-164.