CD4+-T-cell responses generated during murine Salmonella enterica serovar typhimurium infection are directed towards multiple epitopes within the natural antigen FliC

Infection and Immunity

Volumn 73, Issue 11, 2005, Pages 7226-7235

  Bergman, Molly A ^a,c   Cummings, Lisa A ^a   Alaniz, Robert C ^a   Mayeda, Laura ^a   Fellnerova, Ivana ^a   Cookson, Brad T ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF WASHINGTON MEDICAL CENTER   (United States)

^c TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; CD4 ANTIGEN; CYTOKINE; EPITOPE; FLIC PROTEIN; GAMMA INTERFERON; HYBRID PROTEIN; RECOMBINANT PROTEIN; TOLL LIKE RECEPTOR 5; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN RECOGNITION; ANTIGEN SPECIFICITY; ANTIGENICITY; ARTICLE; BACTERIAL FLAGELLUM; BACTERIAL VIRULENCE; CYTOKINE PRODUCTION; DENDRITIC CELL; EFFECTOR CELL; FEMALE; GRAM NEGATIVE BACTERIUM; IMMUNE RESPONSE; LYMPHOCYTE CLONE; MACROPHAGE; MOUSE; NONHUMAN; PHAGOCYTE; PRIORITY JOURNAL; SALMONELLA ENTERICA; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TYPHOID FEVER;

AMINO ACID SEQUENCE; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; EPITOPES; FEMALE; FLAGELLIN; INTERFERON TYPE II; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHAGOCYTES; PROTEIN STRUCTURE, TERTIARY; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 27744434894     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.73.11.7226-7235.2005     Document Type: Article

References (58)

1. + T cells and Toll-like receptors recognize Salmonella antigens expressed in bacterial surface organelles. Infect. Immun. 73:1350-1356.
2. Bhardwaj, V., O. Kanagawa, P. E. Swanson, and E. R. Unanue. 1998. Chronic Listeria infection in SCID mice: requirements for the carrier state and the dual role of T cells in transferring protection or suppression. J. Immunol. 160:376-384.
3. Bierer, B., J. E. Coligan, D. H. Margulies, E. M. Shevach, W. Strober, and A. Kruisbeek. 1991. Current protocols in immunology. John Wiley & Sons. Inc., New York, N.Y.
4. Brown, A., and C. E. Hormaeche. 1989. The antibody response to salmonellae in mice and humans studied by immunoblots and ELISA. Microb. Pathog. 6:445-454.
5. Buchmeier, N. A., and R. D. Schreiber. 1985. Requirement of endogenous interferon-gamma production for resolution of Listeria monocytogenes infection. Proc. Natl. Acad. Sci. USA 82:7404-7408.
6. Carter, P. B., and F. M. Collins. 1974. The route of enteric infection in normal mice. J. Exp. Med. 139:1189-1203.
7. Cookson, B. T., and M. J. Bevan. 1997. Identification of a natural T cell epitope presented by Salmonella-infected macrophages and recognized by T cells from orally immunized mice. J. Immunol. 158:4310-4319.
8. Cookson, B. T., L. A. Cummings, and S. L. R. Barrett. 2001. Bacterial antigens elicit T cell responses via adaptive and transitional immune recognition. Curr. Opin. Microbiol. 4:267-273.
9. Cummings, L. A., S. L. Barrett, W. D. Wilkerson, I. Fellnerova, and B. T. Cookson. 2005. FliC-specific CD4+ T cell responses are restricted by bacterial regulation of antigen expression. J. Immunol. 174:7929-7938.
10. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. USA 97:6640-6645.
11. Dembic, Z., P. A. Singer, and J. Klein. 1984. Eo: a history of a mutation. EMBO J. 3:1647-1654.
12. Eisenstein, T. K., L. M. Killar, and B. M. Sultzer. 1984. Immunity to infection with Salmonella typhimurium: mouse strain differences in vaccine- and serum-mediated protection. J. Infect. Dis. 150:425-435.
13. Feldman, M., R. Bryan, S. Rajan, L. Scheffler, S. Brunnert, H. Tang, and A. Prince. 1998. Role of flagella in pathogenesis of Pseudomonas aeruginosa pulmonary infection. Infect. Immun. 66:43-51.
14. Fields, P. I., E. A. Groisman, and F. Heffron. 1989. A Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells. Science 243:1059-1062.
15. Fields, P. I., R. V. Swanson, C. G. Haidaris, and F. Heffron. 1986. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc. Natl. Acad. Sci. USA 83:5189-5193.
16. Friedman, R. L., and R. J. Moon. 1977. Hepatic clearance of Salmonella typhimurium in silica-treated mice. Infect. Immun. 16:1005-1012.
17. d encodes a dominant surface epitope and a stabilizing factor for functional flagella. J. Bacteriol. 176:2406-2414.
18. Hess, J., C. Ladel, D. Miko, and S. H. Kaufmann. 1996. Salmonella typhimurium aroA-infection in gene-targeted immunodeficient mice: major role of CD4+ TCR-alpha beta cells and IFN-gamma in bacterial clearance independent of intracellular location. J. Immunol. 156:3321-3326.
19. Hoiseth, S. K., and B. A. Stocker. 1981. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291: 238-239.
20. Homma, M., H. Fujita, S. Yamaguchi, and T. Iino. 1987. Regions of Salmonella typhimurium flagellin essential for its polymerization and excretion. J. Bacteriol. 169:291-296.
21. Honko, A. N., and S. B. Mizel. 2004. Mucosal administration of flagellin induces innate immunity in the mouse lung. Infect. Immun. 72:6676-6679.
22. Jones, B. D., N. Ghori, and S. Falkow. 1994. Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. J. Exp. Med. 180:15-23.
23. Joys, T. M., and F. Schodel. 1991. Epitope mapping of the d flagellar antigen of Salmonella muenchen. Infect. Immun. 59:3330-3332.
24. Joys, T. M., and N. E. Street. 1993. Mapping of T-cell epitopes of flagellar antigen d of Salmonella muenchen. Infect. Immun. 61:1146-1148.
25. Korbsrisate, S., A. Thanomsakyuth, N. Banchuin, S. McKay, M. Hossain, and S. Sarasombath. 1999. Characterization of a phase 1-d epitope on Salmonella typhi flagellin and its role in the serodiagnosis of typhoid fever. Asian Pac. J. Allergy Immunol. 17:31-39.
26. Kwang, J., R. Wilson, S. Yang, and Y. He. 1996. Mapping of the H7-serospecific domain of Escherichia coli flagellin. Clin. Diagn. Lab. Immunol. 3:523-526.
27. Liaudet, L., C. Szabo, O. V. Evgenov, K. G. Murthy, P. Pacher, L. Virag, J. G. Mabley, A. Marton, F. G. Soriano, M. Y. Kirov, L. J. Bjertnaes, and A. L. Salzman. 2003. Flagellin from gram-negative bacteria is a potent mediator of acute pulmonary inflammation in sepsis. Shock 19:131-137.
28. Liu, X., S. Dai, F. Crawford, R. Fruge, P. Marrack, and J. Kappler. 2002. Alternate interactions define the binding of peptides to the MHC molecule IA(D). Proc. Natl. Acad. Sci. USA 99:8820-8825.
29. Lodes, M. J., Y. Cong, C. O. Elson, R. Mohamath, C. J. Landers, S. R. Targan, M. Fort, and R. M. Hershberg. 2004. Bacterial flagellin is a dominant antigen in Crohn disease. J. Clin. Investig. 113:1296-1306.
30. Manca, F., D. Fenoglio, A. Kunkl, C. Cambiaggi, M. Sasso, and F. Celada. 1988. Differential activation of T cell clones stimulated by macrophages exposed to antigen complexed with monoclonal antibodies. A possible influence of paratope specificity on the mode of antigen processing. J. Immunol. 140:2893-2898.
31. Manca, F., D. Fenoglio, G. Li Pira, A. Kunkl, and F. Celada. 1991. Effect of antigen/antibody ratio on macrophage uptake, processing, and presentation to T cells of antigen complexed with polyclonal antibodies. J. Exp. Med. 173:37-48.
32. Mastroeni, P., B. Villarreal-Ramos, and C. E. Hormaeche. 1993. Adoptive transfer of immunity to oral challenge with virulent salmonellae in innately susceptible BALB/c mice requires both immune serum and T cells. Infect. Immun. 61:3981-3984.
33. Mastroeni, P., B. Villarreal-Ramos, and C. E. Hormaeche. 1992. Role of T cells, TNF alpha and IFN gamma in recall of immunity to oral challenge with virulent salmonellae in mice vaccinated with live attenuated aro-Salmonella vaccines. Microb. Pathog. 13:477-491.
34. McSorley, S. J., S. Asch, M. Costalonga, R. L. Reinhardt, and M. K. Jenkins. 2002. Tracking salmonella-specific CD4 T cells in vivo reveals a local mucosal response to a disseminated infection. Immunity 16:365-377.
35. McSorley, S. J., B. T. Cookson, and M. K. Jenkins. 2000. Characterization of CD4+ T cell responses during natural infection with Salmonella typhimurium. J. Immunol. 164:986-993.
36. McSorley, S. J., B. D. Ehst, Y. Yu, and A. T. Gewirtz. 2002. Bacterial flagellin is an effective adjuvant for CD4+ T cells in vivo. J. Immunol. 169:3914-3919.
37. McSorley, S. J., and M. K. Jenkins. 2000. Antibody is required for protection against virulent but not attenuated Salmonella enterica serovar Typhimurium. Infect. Immun. 68:3344-3348.
38. Mempel, T. R., S. E. Henrickson, and U. H. Von Andrian. 2004. T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 427:154-159.
39. Mittrucker, H. W., and S. H. Kaufmann. 2000. Immune response to infection with Salmonella typhimurium in mice. J. Leukoc. Biol. 67:457-463.
40. Mittrucker, H. W., B. Raupach, A. Kohler, and S. H. Kaufmann. 2000. Cutting edge: role of B lymphocytes in protective immunity against Salmonella typhimurium infection. J. Immunol. 164:1648-1652.
41. Nauciel, C. 1990. Role of CD4+ T cells and T-independent mechanisms in acquired resistance to Salmonella typhimurium infection. J. Immunol. 145: 1265-1269.
42. Nauciel, C., and F. Espinasse-Maes. 1992. Role of gamma interferon and tumor necrosis factor alpha in resistance to Salmonella typhimurium infection. Infect. Immun. 60:450-454.
43. O'Brien, A. D., I. Scher, and S. B. Formal. 1979. Effect of silica on the innate resistance of inbred mice to Salmonella typhimurium infection. Infect. Immun. 25:513-520.
44. Pie, S., P. Matsiota-Bernard, P. Truffa-Bachi, and C. Nauciel. 1996. Gamma interferon and interleukin-10 gene expression in innately susceptible and resistant mice during the early phase of Salmonella typhimurium infection. Infect. Immun. 64:849-854.
45. Ramarathinam, L., D. W. Niesel, and G. R. Klimpel. 1993. Salmonella typhimurium induces IFN-gamma production in murine splenocytes. Role of natural killer cells and macrophages. J. Immunol. 150:3973-3981.
46. Rammensee, H., J. Bachmann, N. P. Emmerich, O. A. Bachor, and S. Stevanovic. 1999. SYFPEITHI: database for MHC ligands and peptide motifs. Immunogenetics 50:213-219.
47. Ramos, H. C., M. Rumbo, and J. C. Sirard. 2004. Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa. Trends Microbiol. 12:509-517.
48. Richter-Dahlfors, A., A. M. J. Buchan, and B. B. Finlay. 1997. Murine salmonellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J. Exp. Med. 186:569-580.
49. Samatey, F. A., K. Imada, S. Nagashima, F. Vonderviszt, T. Kumasaka, M. Yamamoto, and K. Namba. 2001. Structure of the bacterial flagellar protofilament and implications for a switch for supercoiling. Nature 410:331-337.
50. Schafer, R., and T. K. Eisenstein. 1992. Natural killer cells mediate protection induced by a Salmonella aroA mutant. Infect. Immun. 60:791-797.
51. Seah, J. N., and J. Kwang. 2002. Production of a monoclonal antibody specific to Escherichia coli H33 flagellin by using predetermined polypeptides. Arch. Microbiol. 177:192-196.
52. Simitsek, P. D., D. G. Campbell, A. Lanzavecchia, N. Fairweather, and C. Watts. 1995. Modulation of antigen processing by bound antibodies can boost or suppress class II major histocompatibility complex presentation of different T cell determinants. J. Exp. Med. 181:1957-1963.
53. Smith, K. D., E. Andersen-Nissen, F. Hayashi, K. Strobe, M. A. Bergman, S. L. Barrett, B. T. Cookson, and A. Aderem. 2003. Toll-like receptor 5 recognizes a conserved site on flagellin required for protofilament formation and bacterial motility. Nat. Immunol. 4:1247-1253.
54. Srinivasan, A., J. Foley, and S. J. McSorley. 2004. Massive number of antigen-specific CD4 T cells during vaccination with live attenuated Salmonella causes interclonal competition. J. Immunol. 172:6884-6893.
55. Srinivasan, A., J. Foley, R. Ravindran, and S. J. McSorley. 2004. Low-dose Salmonella infection evades activation of flagellin-specific CD4 T cells. J. Immunol. 173:4091-4099.
56. Stocker, B. A. D., and J. C. Campbell. 1959. The effect of non-lethal deflagellation on bacterial motility and observations on flagellar regeneration. J. Gen. Microbiol. 20:670.
57. Sztein, M. B., S. S. Wasserman, C. O. Tacket, R. Edelman, D. Hone, A. A. Lindberg, and M. M. Levine. 1994. Cytokine production patterns and lymphoproliferative responses in volunteers orally immunized with attenuated vaccine strains of Salmonella typhi. J. Infect. Dis. 170:1508-1517.
58. Weintraub, B. C., L. Eckmann, S. Okamoto, M. Hense, S. M. Hedrick, and J. Fierer. 1997. Role of αβ and γδ T cells in the host response to Salmonella infection as demonstrated in T-cell-receptor-deficient mice of defined Ity genotypes. Infect. Immun. 65:2306-2312. (Erratum, 66:882.)