Identification of a Natural T Cell Epitope Presented by Salmonella-Infected Macrophages and Recognized by T Cells from Orally Immunized Mice

Journal of Immunology

Volumn 158, Issue 9, 1997, Pages 4310-4319

  Cookson, Brad T ^a   Bevan, Michael J ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; BACTERIAL PROTEIN; FLAGELLIN;

AMINO ACID SEQUENCE; ANIMAL; ANIMAL SALMONELLOSIS; ANTIGEN PRESENTING CELL; ARTICLE; BAGG ALBINO MOUSE; C3H MOUSE; C57BL MOUSE; CD4+ T LYMPHOCYTE; EPITOPE MAPPING; FEMALE; IMMUNIZATION; IMMUNOLOGY; MACROPHAGE; MICROBIOLOGY; MOLECULAR GENETICS; MOUSE; ORAL DRUG ADMINISTRATION; SALMONELLA TYPHIMURIUM; T LYMPHOCYTE;

ADMINISTRATION, ORAL; AMINO ACID SEQUENCE; ANIMALS; ANTIGEN-PRESENTING CELLS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; CD4-POSITIVE T-LYMPHOCYTES; EPITOPE MAPPING; FEMALE; FLAGELLIN; IMMUNIZATION; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; T-LYMPHOCYTES;

EID: 0031134803     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (76)

1. Carter, P. B., and F. M. Collins. 1974. The route of enteric infection in normal mice. J. Exp. Med. 139:1189.
2. 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.
3. Collins, F. M. 1970. Immunity to enteric infection in mice. Infect. Immun. 1:243.
4. O'Callaghan, D., D. Maskell, F. Y. Liew, C. S. Easmon, and G. Dougan. 1988. Characterization of aromatic- and purine-dependent Salmonella typhimurium: attention, persistence, and ability to induce protective immunity in BALB/c mice. Infect. Immun. 56:419.
5. Hoiseth, S. K., and B. A. Stocker. 1981. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291:238.
6. Killar, L. M., and T. K. Eisenstein. 1985. Immunity to Salmonella typhimurium infection in C3H/HeJ and C3H/HeNCrlBR mice: studies with an aromatic-dependent live S. typhimurium strain as a vaccine. Infect. Immun. 47:605.
7. Wahdan, M. H., C. Serie, R. Germanier, A. Lackany, Y. Cerisier, N. Guerin, S. Sallam, P. Geoffroy, A. Sadek el Tantawi, and P. Guesry. 1980. A controlled field trial of liver oral typhoid vaccine Ty21a. Bull. World Health Organ. 58:469.
8. Levine, M. M., C. Ferreccio, R. E. Black, and R. Germanier. 1987. Large-scale field trial of Ty21a live oral typhoid vaccine in enteric-coated capsule formulation. Lancet 1:1049.
9. Chuttani, C. S., K. Prakash, A. Vergese, P. Gupta, R. K. Chawla, V. Grover, and D. S. Agarwal. 1973. Ineffectiveness of an oral killed typhoid vaccine in a field trial. Bull. World Health Organ. 48:754.
10. Chuttani, C. S., K. Prakash, P. Gupta, V. Grover, and A. Kumar. 1977. Controlled field trial of a high-dose oral killed typhoid vaccine in India. Bull. World Health Organ. 55:643.
11. Swanson, R. N., and A. D. O'Brien. 1983. Genetic control of the innate resistance of mice to Salmonella typhimurium: Ity gene is expressed in vivo by 24 hours after infection. J. Immunol. 131:3014.
12. Maskell, D. J., C. E. Hormaeche, K. A. Harrington, H. S. Joysey, and F. Y. Liew. 1987. The initial suppression of bacterial growth in a Salmonella infection is mediated by a localized rather than a systemic response. Microb. Pathog. 2:295.
13. Mastroeni, P., A. Arena, G. B. Costa, M. C. Liberto, L. Bonina, and C. E. Hormaeche. 1991. Serum TNF alpha in mouse typhoid and enhancement of a Salmonella infection by anti-TNF alpha antibodies. Microb. Pathog. 11:33.
14. Tite, J. P., G. Dougan, and S. N. Chatfield. 1991. The involvement of tumor necrosis factor in immunity to Salmonella infection. J. Immunol. 147:3161.
15. Nauciel, C., and M. F. Espinasse. 1992. Role of gamma interferon and tumor necrosis factor alpha in resistance to Salmonella typhimurium infection. Infect. Immun. 60:450.
16. Muotiala, A., and P. H. Makela. 1990. The role of IFN-gamma in murine Salmonella typhimurium infection. Microb. Pathog. 8:135.
17. Pie, S., B. P. Matsiota, B. P. Truffa, 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.
18. Ramarathinam, L., R. A. Shaban, D. W. Niesel, and G. R. Klimpel. 1991. Interferon gamma (IFN-gamma) production by gut-associated lymphoid tissue and spleen following oral Salmonella typhimurium challenge. Microb. Pathog. 11:347.
19. Chong, C. K. L. Bost, and J. D. Clements. 1996. Differential production of interleukin-12 mRNA by murine macrophages in response to viable or killed Salmonella spp. Infect. Immun. 64:1154.
20. Kincy-Cain, T., J. D. Clements, and K. L. Bost. 1996. Endogenous and exogenous interleukin-12 augment the protective immune response in mice orally challenged with Salmonella dublin. Infect. Immun. 64:1437.
21. Mastroeni, P., J. A. Harrison, J. A. Chabalgoity, and C. E. Hormaeche. 1996. Effect of interleukin 12 neutralization on host resistance and gamma interferon production in mouse typhoid. Infect. Immun. 64:189.
22. Schafer, R., and T. K. Eisenstein. 1992. Natural killer cells mediate protection induced by a Salmonella aroA mutant. Infect. Immun. 60:791.
23. 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.
24. Hobson, D. 1957. Resistance to reinfection in experimental mouse typhoid. J. Hyg. 55:334.
25. Ushiba, D. 1965. Two types of immunity in experimental typhoid; "cellular immunity" and "humoral immunity." Keio J. Med. 14:45.
26. Eisenstein, T. K., D. Huang, and M. G. Schwacha. 1996. Immunity to Salmonella. In Enteric Infections and Immunity. L. J. Paradise, M. Bendinelli, and H. Friedman, eds. Plenum Publishing Corp., New York, p. 57-78.
27. 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.
28. Collins, F. M., and G. B. Mackaness. 1968. Delayed hypersensitivity and arthus reactivity in relation to host resistance in Salmonella-infected mice. J. Immunol. 101:830.
29. Kotlarski, I., M. Pope, K. Doherty, and S. R. Attridge. 1989. The in vitro proliferative response of lymphoid cells of mice infected with Salmonella enteritidis 11RX. Immunol. Cell Biol. 67:19.
30. + T cells and T-independent mechanisms in acquired resistance to Salmonella typhimurium infection. J. Immunol. 145:1265.
31. Mastroeni, P., R. B. Villarreal, 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.
32. + T cells which can proliferate in vitro and mediate delayed-type hypersensitivity reactivity. Immunology 81:183.
33. Pope, M., I. Kotlarski, and K. Doherty. 1994. Induction of Lyt-2+ cytotoxic T lymphocytes following primary and secondary Salmonella infection. Immunology 81:177.
34. Davies, R., and I. Kotlarski. 1976. The role of thymus-derived cells in immunity to salmonella infection. Aust. J. Exp. Biol. Med. Sci. 54:221.
35. 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.
36. Mastroeni, P., R. B. Villarreal, 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.
37. + cytotoxic T cells. J. Exp. Med. 172:1083.
38. Flynn, J. L., W. R. Weiss, K. A. Norris, H. S. Seifert, S. Kumar, and M. So. 1990. Generation of a cytotoxic T-lymphocyte response using a Salmonella antigen-delivery system. Mol. Microbiol. 4:2111.
39. Verma, N. K., H. K. Ziegler, B. A. Stocker, and G. K. Schoolnik. 1995. Induction of a cellular immune response to a defined T-cell epitope as an insert in the flagellin of a live vaccine strain of Salmonella. Vaccine 13:235.
40. Verma, N. K., H. K. Ziegler, M. Wilson, M. Khan, S. Safley, B. A. Stocker, and G. K. Schoolnik. 1995. Delivery of class I and class II MHC-restricted T-cell epitopes of listeriolysin of Listeria monocytogenes by attenuated Salmonella. Vaccine 13:142.
41. Cardenas, L., and J. D. Clements. 1992. Oral immunization using live attenuated Salmonella spp. as carriers of foreign antigens. Clin. Microbiol. Rev. 5:328.
42. Curtiss, R., III, S. M. Kelly, S. A. Tinge, C. O. Tacket, M. M. Levine, J. Srinivasan, and M. Koopman. 1994. Recombinant Salmonella vectors in vaccine development. Dev. Biol. Stand. 82:23.
43. Chatfield, S., M. Roberts, J. Li, A. Starns, and G. Dougan. 1994. The use of live attenuated Salmonella for oral vaccination. Dev. Biol. Stand. 82:35.
44. White, J., M. Blackman, J. Bill, J. Kappler, P. Marrack, D. P. Gold, and W. Born. 1989. Two better cell lines for making hybridomas expressing specific T cell receptors. J. Immunol. 143:1822.
45. Glimcher, L. H., D. J. McKean, E. Choi, and J. G. Seidman. 1985. Complex regulation of class II gene expression: analysis with class II mutant cell lines. J. Immunol. 135:3542.
46. Coligan, J. E., A. M. Kruisbeek, D. H. Marguiles, E. M. Shevach, and W. Strober. 1994. Current Protocols in Immunology. John Wiley & Sons, Inc., New York.
47. Davis, R. W., D. Botstein, and J. R. Roth. 1980. Advanced Bacterial Genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
48. 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.
49. Kanto, S., H. Okino, S. Aizawa, and S. Yamaguchi. 1991. Amino acids responsible for flagellar shape are distributed in terminal regions of flagellin. J. Mol. Biol. 219:471.
50. Buchmeier, N. A., and F. Heffron. 1989. Intracellular survival of wild-type Salmonella typhimurium and macrophage-sensitive mutants in diverse populations of macrophages. Infect. Immun. 57:1.
51. Kappler, J. W., B. Skidmore, I. White, and P. Marrack. 1981. Antigen-inducible, H-2-restricted, interleukin-2-producing T cell hybridomas: lack of independent antigen and H-2 recognition. J. Exp. Med. 153:1198.
52. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl. 1995. Current Protocols in Molecular Biology. John Wiley & Sons, Inc., New York.
53. Gavin, M. A., M. J. Gilbert, S. R. Riddell, P. D. Greenberg, and M. J. Bevan. 1993. Alkali hydrolysis of recombinant proteins allows for the rapid identification of class I MHC-restricted CTL epitopes. J. Immunol. 151:3971.
54. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular Cloning. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
55. Wei, L. N., and T. M. Joys. 1985. Covalent structure of three phase-1 flagellar filament proteins of Salmonella. J. Mol. Biol. 186:791.
56. Rudensky, A. Y., H. P. Preston, S. C. Hong, A. Barlow, and C. A. J. Janeway. 1991. Sequence analysis of peptides bound to MHC class II molecules. Nature 353:622.
57. k. Proc. Natl. Acad. Sci. USA 89:7380.
58. Marrack, P., L. Ignatowicz, J. W. Kappler, J. Boymel, and J. H. Freed. 1993. Comparison of peptides bound to spleen and thymus class II. J. Exp. Med. 178:2173.
59. Starnbach, M. N., and M. J. Bevan. 1994. Cells infected with Yersinia present an epitope to class I MHC-restricted CTL. J. Immunol. 153:1603.
60. Allen, P. M., G. R. Matsueda, R. J. Evans, J. B. J. Dunbar, G. R. Marshall, and E. R. Unanue. 1987. Identification of the T-cell and Ia contact residues of a T-cell antigenic epitope. Nature 327:713.
61. Nelson, C. A., S. J. Petzold, and E. R. Unanue. 1994. Peptides determine the lifespan of MHC class II molecules in the antigen-presenting cell. Nature 371:250.
62. Vignali, D. A., and J. L. Strominger. 1994. Amino acid residues that flank core peptide epitopes and the extracellular domains of CD4 modulate differential signaling through the T cell receptor. J. Exp. Med. 179:1945.
63. Muller, C. P., W. Ammerlan, B. Fleckenstein, S. Krauss, H. Kalbacher, F. Schneider, G. Jung, and K.-H. Wiesmuller. 1996. Activation of T cells by the ragged tail of MHC class II-presented peptides of the measles virus fusion protein. Int. Immunol. 8:445.
64. Steeg, P. S., H. M. Johnson, and J. J. Oppenheim. 1982. Regulation of murine macrophage Ia antigen expression by an immune interferon-like lymphokine: inhibitory effect of endotoxin. J. Immunol. 129:2402.
65. King, D. P., and P. P. Jones. 1983. Induction of Ia and H-2 antigens on a macrophage cell line by immune interferon. J. Immunol. 131:315.
66. Hawrylowicz, C. M., and E. R. Unanue. 1988. Regulation of antigen-presentation-I. IFN-gamma induces antigen-presenting properties on B cells. J. Immunol. 141:4083.
67. Prina, E., C. Jouanne, S. L. S. de, A. Szabo, J. G. Guillet, and J. C. Antoine. 1993. Antigen presentation capacity of murine macrophages infected with Leishmania amazonensis amastigotes. J. Immunol. 151:2050.
68. Nadler, S. G., B. M. Rankin, D. P. Moran, J. S. Cleaveland, and P. A. Kiener. 1994. Effect of interferon-gamma on antigen processing in human monocytes. Eur. J. Immunol. 24:3124.
69. 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.
70. Wu, J. Y., S. Newton, A. Judd, B. Stocker, and W. S. Robinson. 1989. Expression of immunogenic epitopes of hepatitis B surface antigen with hybrid flagellin proteins by a vaccine strain of Salmonella. Proc. Natl. Acad. Sci. USA 86:4726.
71. Newton, S. M., C. O. Jacob, and B. A. Stocker. 1989. Immune response to cholera toxin epitope inserted in Salmonella flagellin. Science 244:70.
72. Ogunniyi, A. D., P. A. Manning, and I. Kotlarski. 1994. A Salmonella enteritidis 11RX pilin induces strong T-lymphocyte responses. Infect. Immun. 62:5376.
73. Ushiba, D., K. Saito, T. Akiyama, M. Nakano, T. Sugiyama, and S. Shirono. 1959. Studies on experimental typhoid: bacterial multiplication and host cell response after infection with Salmonella enteritidis in mice immunized with live and killed vaccines. Jpn. J. Microbiol. 3:231.
74. Thorns, C. J., M. G. Sojka, I. M. Mclaren, and F. M. Dibb. 1992. Characterisation of monoclonal antibodies against a fimbrial structure of Salmonella enteritidis and certain other serogroup D salmonellae and their application as serotyping reagents. Res. Vet. Sci. 53:300.
75. Turcotte, C., and M. J. Woodward. 1993. Cloning, DNA nucleotide sequence and distribution of the gene encoding the SHF14 fimbrial antigen of Salmonella enteritidis. J. Gen. Microbiol. 139:1477.
76. Collinson, S. K., S. L. Liu, S. C. Clouthier, P. A. Banser, J. L. Doran, K. E. Sanderson, and W. W. Kay. 1996. The location of four fimbrin-encoding genes, agfA, fimA, sefA and sefD, on the Salmonella enteritidis and/or S. typhimurium XbaI-BlnI genomic restriction maps. Gene 169:75.