Insufficient TLR activation contributes to the slow development of CD8 + T cell responses in Trypanosoma cruzi infection

Journal of Immunology

Volumn 183, Issue 2, 2009, Pages 1245-1252

  Padilla, Angel M ^a   Simpson, Laura J ^a   Tarleton, Rick L ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; EPITOPE; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 9; CYTOKINE; T LYMPHOCYTE RECEPTOR; TLR2 PROTEIN, MOUSE; TLR9 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ANTIGEN RECOGNITION; ARTICLE; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELLULAR IMMUNITY; CHAGAS DISEASE; CONTROLLED STUDY; EFFECTOR CELL; IMMUNOSUPPRESSIVE TREATMENT; IN VIVO STUDY; INNATE IMMUNITY; LYMPH NODE; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRYPANOSOMA CRUZI; ANIMAL; BLOOD; C57BL MOUSE; CELL PROLIFERATION; CYTOTOXICITY; DENDRITIC CELL; DRUG POTENTIATION; IMMUNITY; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; NEUTROPHIL CHEMOTAXIS; PARASITOLOGY; PATHOLOGY; TIME;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CHAGAS DISEASE; CHEMOTAXIS, LEUKOCYTE; CYTOKINES; CYTOTOXICITY, IMMUNOLOGIC; DENDRITIC CELLS; IMMUNITY; LYMPH NODES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; T-CELL ANTIGEN RECEPTOR SPECIFICITY; TIME FACTORS; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 9;

EID: 68149158996     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0901178     Document Type: Article

References (37)

1. Schuster, J. P., and G. A. Schaub. 2000. Trypanosoma cruzi: skin-penetration kinetics of vector-derived metacyclic trypomastigotes. Int. J. Parasitol. 30: 1475-1479.
2. 2-microglobulin-deficient mice to Trypanosoma cruzi infection. Nature 356: 338-340.
3. Tarleton, R. L., J. Sun, L. Zhang, and M. Postan. 1994. Depletion of T-cell subpopulations results in exacerbation of myocarditis and parasitism in experimental Chagas' disease. Infect. Immun. 62: 1820-1829.
4. + T-cell responses to Trypanosoma cruzi are highly focused on strain-variant trans-sialidase epitopes. PLoS Pathog. 2: e77.
5. El-Sayed, N. M., P. J. Myler, D. C. Bartholomeu, D. Nilsson, G. Aggarwal, A. N. Tran, E. Ghedin, E. A. Worthey, A. L. Delcher, G. Blandin, et al. 2005. The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309: 409-415.
6. Pope, C., S. K. Kim, A. Marzo, D. Masopust, K. Williams, J. Jiang, H. Shen, and L. Lefrancois. 2001. Organ-specific regulation of the CD8 T cell response to Listeria monocytogenes infection. J. Immunol. 166: 3402-3409. (Pubitemid 33117342)
7. Lorenzi, H. A., M. P. Vazquez, and M. J. Levin. 2003. Integration of expression vectors into the ribosomal locus of Trypanosoma cruzi. Gene 310: 91-99.
8. Martin, D. L., and R. L. Tarleton. 2005. Antigen-specific T cells maintain an effector memory phenotype during persistent Trypanosoma cruzi infection. J. Immunol. 174: 1594-1601.
9. Cummings, K. L., and R. L. Tarleton. 2003. Rapid quantitation of Trypanosoma cruzi in host tissue by real-time PCR. Mol. Biochem. Parasitol. 129: 53-59.
10. + T lymphocytes protective against malaria liver stages are primed in skin-draining lymph nodes. Nat. Med. 13: 1035-1041.
11. + T cells against malaria liver stages. J. Exp. Med. 194: 173-180.
12. + T cells undergoing primary and secondary responses to infection in the same host. J. Immunol. 170: 4933-4942.
13. + T central memory response in chronic Chagas disease. Nat. Med. 14: 542-550.
14. + cytotoxic T cells after infection with Trypanosoma cruzi in naive or vaccinated mice. Infect. Immun. 74: 2477-2481.
15. Minoprio, P. 2001. Parasite polyclonal activators: new targets for vaccination approaches? Int. J. Parasitol. 31: 588-591.
16. Poncini, C. V., C. D. Alba Soto, E. Batalla, M. E. Solana, and S. M. Gonzalez Cappa. 2008. Trypanosoma cruzi induces regulatory dendritic cells in vitro. Infect. Immun. 76: 2633-2641.
17. Michelin, M. A., J. S. Silva, and F. Q. Cunha. 2005. Inducible cyclooxygenase released prostaglandin mediates immunosuppression in acute phase of experimental Trypanosoma cruzi infection. Exp. Parasitol. 111: 71-79.
18. Borges, M., A. C. Da Silva, D. Sereno, and A. Ouaissi. 2003. Peptide-based analysis of the amino acid sequence important to the immunoregulatory function of Trypanosoma cruzi Tc52 virulence factor. Immunology 109: 147-155.
19. Warger, T., P. Osterloh, G. Rechtsteiner, M. Fassbender, V. Heib, B. Schmid, E. Schmitt, H. Schild, and M. P. Radsak. 2006. Synergistic activation of dendritic cells by combined Toll-like receptor ligation induces superior CTL responses in vivo. Blood 108: 544-550.
20. Zhu, Q., C. Egelston, A. Vivekanandhan, S. Uematsu, S. Akira, D. M. Klinman, I. M. Belyakov, and J. A. Berzofsky. 2008. Toll-like receptor ligands synergize through distinct dendritic cell pathways to induce T cell responses: implications for vaccines. Proc. Natl. Acad. Sci. USA 105: 16260-16265.
21. + T cell expansion, memory, and protective immunity after immunization with peptide-coated dendritic cells. J. Immunol. 169: 4936-4944.
22. + T cells differentiation and proliferation by the timing of increase in the pathogen load. PLoS ONE 2: e393.
23. Davenport, M. P., G. T. Belz, and R. M. Ribeiro. 2009. The race between infection and immunity: how do pathogens set the pace? Trends Immunol. 30: 61-66.
24. Giddings, O. K., C. S. Eickhoff, T. J. Smith, L. A. Bryant, and D. F. Hoft. 2006. Anatomical route of invasion and protective mucosal immunity in Trypanosoma cruzi conjunctival infection. Infect. Immun. 74: 5549-5560.
25. Bubonja, M., B. Wraber, G. Brumini, I. Gobin, D. Veljkovic, and M. Abram. 2006. Systemic and local CC chemokines production in a murine model of Listeria monocytogenes infection. Mediators Inflamm. 2006: 54202.
26. Dorner, B. G., A. Scheffold, M. S. Rolph, M. B. Huser, S. H. Kaufmann, A. Radbruch, I. E. Flesch, and R. A. Kroczek. 2002. MIP-1alpha, MIP-1β, RANTES, and ATAC/lymphotactin function together with IFN-γ as type 1 cytokines. Proc. Natl. Acad. Sci. USA 99: 6181-6186.
27. Griffith, J. W., C. O'Connor, K. Bernard, T. Town, D. R. Goldstein, and R. Bucala. 2007. Toll-like receptor modulation of murine cerebral malaria is dependent on the genetic background of the host. J. Infect. Dis. 196: 1553-1564.
28. Sarfo, B. Y., H. B. Armah, I. Irune, A. A. Adjei, C. S. Olver, S. Singh, J. W. Lillard, Jr., and J. K. Stiles. 2005. Plasmodium yoelii 17XL infection upregulates RANTES, CCR1, CCR3 and CCR5 expression, and induces ultrastructural changes in the cerebellum. Malar. J. 4: 63.
29. Bafica, A., H. C. Santiago, R. Goldszmid, C. Ropert, R. T. Gazzinelli, and A. Sher. 2006. Cutting edge: TLR9 and TLR2 signaling together account for MyD88-dependent control of parasitemia in Trypanosoma cruzi infection. J. Immunol. 177: 3515-3519.
30. 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.
31. Engel, J. C., P. S. Doyle, and J. A. Dvorak. 1985. Trypanosoma cruzi: biological characterization of clones derived from chronic chagasic patients. II. Quantitative analysis of the intracellular cycle. J. Protozool. 32: 80-83.
32. Jeannin, P., S. Jaillon, and Y. Delneste. 2008. Pattern recognition receptors in the immune response against dying cells. Curr. Opin. Immunol. 20: 530-537.
33. Vaena de Avalos, S., I. J. Blader, M. Fisher, J. C. Boothroyd, and B. A. Burleigh. 2002. Immediate/early response to Trypanosoma cruzi infection involves minimal modulation of host cell transcription. J. Biol. Chem. 277: 639-644.
34. Bartholomeu, D. C., C. Ropert, M. B. Melo, P. Parroche, C. F. Junqueira, S. M. Teixeira, C. Sirois, P. Kasperkovitz, C. F. Knetter, E. Lien, et al. 2008. Recruitment and endo-lysosomal activation of TLR9 in dendritic cells infected with Trypanosoma cruzi. J. Immunol. 181: 1333-1344.
35. Koga, R., S. Hamano, H. Kuwata, K. Atarashi, M. Ogawa, H. Hisaeda, M. Yamamoto, S. Akira, K. Himeno, M. Matsumoto, and K. Takeda. 2006. TLR-dependent induction of IFN-β mediates host defense against Trypanosoma cruzi. J. Immunol. 177: 7059-7066.
36. + T cells reside in nonlymphoid tissues during chronic Trypanosoma cruzi infection. J. Immunol. 170: 2264-2268.
37. Combs, T. P., F. Nagajyothi, S. Mukherjee, C. J. de Almeida, L. A. Jelicks, W. Schubert, Y. Lin, D. S. Jayabalan, D. Zhao, V. L. Braunstein, et al. 2005. The adipocyte as an important target cell for Trypanosoma cruzi infection. J. Biol. Chem. 280: 24085-24094.