Tracking the dynamics of T-cell activation in response to Salmonella infection

Immunology

Volumn 114, Issue 4, 2005, Pages 450-458

  Ravindran, Rajesh ^a   McSorley, Stephen J ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

Author keywords

Bacteria; Memory; Salmonella; T cell; Vaccination

Indexed keywords

SALMONELLOSIS VACCINE;

ANIMAL CELL; ANIMAL MODEL; ANTIGEN SPECIFICITY; DEVELOPING COUNTRY; EFFECTOR CELL; IMMUNE RESPONSE; IMMUNOLOGICAL MEMORY; INFECTION PREVENTION; MEMORY CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVIEW; SALMONELLA; SALMONELLOSIS; T LYMPHOCYTE ACTIVATION; TYPHOID FEVER; VACCINATION;

ANIMALS; B-LYMPHOCYTES; DEVELOPING COUNTRIES; HUMANS; IMMUNOLOGIC MEMORY; LYMPHOCYTE ACTIVATION; MICE; MICE, MUTANT STRAINS; MODELS, ANIMAL; SALMONELLA TYPHIMURIUM; T-LYMPHOCYTES; TYPHOID FEVER; TYPHOID-PARATYPHOID VACCINES;

EID: 16444375178     PISSN: 00192805     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2005.02140.x     Document Type: Review

References (89)

1. Jones BD, Falkow S. Salmonellosis: host immune responses and bacterial virulence determinants. Annu Rev Immunol 1996; 14:533-61.
2. Santos RL, Zhang S, Tsolis RM, Kingsley RA, Adams LG, Baumler AJ. Animal models of Salmonella infections: enteritis versus typhoid fever. Microbes Infect 2001; 3:1335-44.
3. Mittrucker HW, Kaufmann SH. Immune response to infection with Salmonella typhimurium in mice. J Leukoc Biol 2000; 67:457-63.
4. Wick MJ. Living in the danger zone: innate immunity to Salmonella. Curr Opin Microbiol 2004; 7:51-7.
5. Gewirtz AT, Simon PO, Schmitt CK, Taylor LJ, Hagedorn CH, O'Brien AD, Neish AS, Madara JL. Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response. J Clin Invest 2001; 107:99-109.
6. Tapping RI, Akashi S, Miyake K, Godowski PJ, Tobias PS. Toll-like receptor 4, but not toll-like receptor 2, is a signaling receptor for Escherichia and Salmonella lipopolysaccharides. J Immunol 2000; 165:5780-7.
7. Sha J, Fadl AA, Klimpel GR, Niesel DW, Popov VL, Chopra AK. The two murein lipoproteins of Salmonella enterica serovar Typhimurium contribute to the virulence of the organism. Infect Immun 2004; 72:3987-4003.
8. Sinha K, Mastroeni P, Harrison J, de Hormaeche RD, Hormaeche CE. Salmonella typhimurium aroA, htrA, and AroD htrA mutants cause progressive infections in athymic (nu/nu) BALB/c mice. Infect Immun 1997; 65:1566-9.
9. + TCR-alpha beta cells and IFN-gamma in bacterial clearance independent of intracellular location. J Immunol 1996; 156:3321-6.
10. Weintraub BC, Eckmann L, Okamoto S, Hense M, Hedrick SM, Fierer J. Role of alphabeta and gammadelta T cells in the host response to Salmonella infection as demonstrated in T-cell-receptor-deficient mice of defined Ity genotypes. Infect Immun 1997; 65:2306-12.
11. + T cells in immunity to Salmonella infection and the involvement of MHC class Ib molecules. J Immunol 1999; 162:5398-406.
12. Mastroeni P, Simmons C, Fowler R, Hormaeche CE, Dougan G. Igh-6 (-/-) (B-cell-deficient) mice fail to mount solid aquired resistance to oral challenge with virulent Salmonella enterica serovar typhimurium and show impaired Th1 T-cell responses to Salmonella antigens. Infect Immun 2000; 68:46-53.
13. McSorley SJ, Jenkins MK. Antibody is required for protection against virulent but not attenuated Salmonella enterica serovar typhimurium. Infect Immun 2000; 68:3344-8.
14. Mittrucker HW, Raupach B, Kohler A, Kaufmann SH. Cutting edge, role of B lymphocytes in protective immunity against Salmonella typhimurium infection. J Immunol 2000; 164:1648-52.
15. Hoiseth SK, Stocker BAD. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 1981; 291:238-9.
16. Mastroeni P, Villarreal-Ramos B, Hormaeche CE. Adoptive transfer of immunity to oral challenge with virulent Salmonella in innately susceptible BALB/c mice requires both immune serum and T cells. Infect Immun 1993; 61:3981-4.
17. Sztein MB, Tanner MK, Polotsky Y, Orenstein JM, Levine MM. Cytotoxic T lymphocytes after oral immunization with attenuated vaccine strains of Salmonella typhi in humans. J Immunol 1995; 155:3987-93.
18. Salerno-Goncalves R, Pasetti MF, Sztein MB. Characterization of CD8 (+) effector T cell responses in volunteers immunized with Salmonella enterica serovar Typhi strain Ty21a typhoid vaccine. J Immunol 2002; 169:2196-203.
19. Lundin BS, Johansson C, Svennerholm AM. Oral immunization with a Salmonella enterica serovar typhi vaccine induces specific circulating mucosa-homing CD4 (+) and CD8 (+) T cells in humans. Infect Immun 2002; 70:5622-7.
20. + T cell responses in volunteers immunized with Salmonella enterica serovar typhi strain CVD 908-htrA. J Immunol 2003; 170:2734-41.
21. + T cell subset in volunteers immunized with Salmonella enterica serovar Typhi strain Ty21a typhoid vaccine. J Immunol 2004; 173:5852-62.
22. Srinivasan A, McSorley SJ. Visualizing the immune response to pathogens. Curr Opin Immunol 2004; 16:494-8.
23. Bumann D. T cell receptor-transgenic mouse models for studying cellular immune responses to Salmonella in vivo. FEMS Immunol Med Microbiol 2003; 37:105-9.
24. Jenkins MK, Khoruts A, Ingulli E, Mueller DL, McSorley SJ, Reinhardt RL, Itano A, Pape KA. In vivo activation of antigen-specific CD4 T cells. Annu Rev Immunol 2001; 19:23-45.
25. Chen ZM, Jenkins MK. Clonal expansion of antigen-specific CD4 T cells following infection with Salmonella typhimurium is similar in susceptible (Itys) and resistant (Ityr) BALB/c mice. Infect Immun 1999; 67:2025-9.
26. Bumann D. In vivo visualization of bacterial colonization, antigen expression and specific T-cell induction following oral administration of live recombinant Salmonella enterica serovar typhimurium. Infect Immun 2001; 69:4618-26.
27. Iwasaki A, Kelsall BL. Mucosal immunity and inflammation. I. Mucosal dendritic cells: their specialized role in initiating T cell responses. Am J Physiol 1999; 276:G1074-8.
28. McSorley SJ, Asch S, Costalonga M, Rieinhardt RL, Jenkins MK. Tracking Salmonella-specific CD4 T cells in vivo reveals a local mucosal response to a disseminated infection. Immunity 2002; 16:365-77.
29. Yrlid U, Wick MJ. Salmonella-induced apoptosis of infected macrophages results in presentation of a bacteria-encoded antigen after uptake by bystander dendritic cells. J Exp Med 2000; 191:613-23.
30. Kelsall BL, Strober W. Distinct populations of dendritic cells are present in the subepithelial dome and T cell regions of the murine Peyer's patch. J Exp Med 1996; 183:237-47.
31. Kelsall BL, Strober W Gut-associated lymphoid tissue. In: Ogra PL, Mestecky J, Lamm ME, Strober W, Bienenstock J, McGhee JR, eds. Mucosal Immunology. London: Academic Press; 1999: 293-318.
32. + T cell responses during natural infection with Salmonella typhimurium. J Immunol 2000; 164:986-93.
33. Shreedhar VK, Kelsall BL, Neutra MR. Cholera toxin induces migration of dendritic cells from the subepithelial dome region to T- and B-cell areas of Peyer's patches. Infect Immun 2003; 71:504-9.
34. Wyant TL, Tanner MK, Sztein MB. Salmonella typhi flagella are potent inducers of proinflammatory cytokine secretion by human monocytes. Infect Immun 1999; 67:3619-24.
35. Gewirtz AT, Nava TA, Lyons S, Godowski PJ, Madera JL. Cutting Edge: Bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol 2001; 167:1882-5.
36. Hayashi F, Smith KD, Ozinsky A et al. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 2001; 410:1099-103.
37. McSorley SJ, Ehst BD, Yu Y, Gewirtz AT. Bacterial flagellin is an effective adjuvant for CD4 T cells in vivo. J Immunol 2002; 169:3914.
38. Sierro F, Dubois B, Coste A, Kaiserlian D, Kraehenbuhl JP, Sirard JC. Flagellin stimulation of intestinal epithelial cells triggers CCL20-mediated migration of dendritic cells. Proc Natl Acad Sci USA 2001; 98:13722-7.
39. Macnab RM. Genetics and biogenesis of bacterial flagella. Annu Rev Genet 1992; 26:131-58.
40. Carter PB, Collins FM. The route of enteric infection in normal mice. J Exp Med 1974; 139:1189-203.
41. Mittrucker H, Kohler A, Kaufmann SH. Characterization of the murine T-lymphocyte response to Salmonella enterica serovar typhimurium infection. Infect Immun 2002; 70:199-203.
42. Dutton RW, Bradley LM, Swain SL. T cell memory. Annu Rev Immunol 1998; 16:201-23.
43. Yrlid U, Svensson M, Hakansson A, Chambers BJ, Ljunggren HG, Wick MJ. In vivo activation of dendritic cells and T cells during Salmonella enterica serovar Typhimurium infection. Infect Immun 2001; 69:5726-35.
44. Srinivasan A, Foley J, McSorley SJ. Massive number of antigen-specific CD4 T cells during vaccination with live attenuated salmonella causes interclonal competition. J Immunol 2004; 172:6884-93.
45. Kirby AC, Sundquist M, Wick MJ. In vivo compartmentalization of functionally distinct, rapidly responsive antigen-specific T-cell populations in DNA-immunized or Salmonella enterica serovar Typhimurium-infected mice. Infect Immun 2004; 72:6390-400.
46. Murali-Krishna K, Altman JD, Suresh M, Sourdive DJD, Zajac AJ, Miller JD, Slansky J, Ahmed R. Counting antigen-specific CD8 T cells: a reevaluation of bystander activation during viral infection. Immunity 1998; 8:177-87.
47. + T cells during an acute virus infection. Immunity 1998; 8: 167-75.
48. + T cell frequencies from acute infection into long term memory. J Immunol 1998; 161:367-74.
49. Whitmire JK, Murali-Krishna K, Altman J, Ahmed R. Antiviral CD4 and CD8 T-cell memory: differences in the size of the response and activation requirements. Philos Trans R Soc Lond B Biol Sci 2000; 355:373-9.
50. + T-cell memory. Nat Med 2001; 7:913-9.
51. Foulds KE, Zenewicz LA, Shedlock DJ, Jiang J, Troy AE, Shen H. Cutting edge. CD4 and CD8 T cells are intrinsically different in their proliferative responses. J Immunol 2002; 168:1528-32.
52. Kaufmann SH. Immunity to intracellular bacteria. Annu Rev Immunol 1993; 11:129-63.
53. Mastroeni P. Immunity to systemic Salmonella infections. Curr Mol Med 2002; 2:393-406.
54. Cookson BT, Bevan MJ. Identification of a natural T cell epitope presented by Salmonella-infected macrophages and recognised by T cells from orally immunised mice. J Immunol 1997; 158:4310-9.
55. Musson JA, Hayward RD, Delvig AA, Hormaeche CE, Koronakis V, Robinson JH. Processing of viable Salmonella typhimurium for presentation of a CD4 T cell epitope from the Salmonella invasion protein C (SipC). Eur J Immunol 2002; 32:2664-71.
56. +-T-cell recognition. Infect Immun 2004; 72:3059-62.
57. Lo WF, Woods AS, DeCloux A, Cotter RJ, Metcalf ES, Soloski MJ. Molecular mimicry mediated by MHC class Ib molecules after infection with gram-negative pathogens. Nat Med 2000; 6:215-8.
58. Brown A, Hormaeche CE. The antibody response to salmonellae in mice and humans studied by immunoblots and ELISA. Microb Pathog 1989; 6:445-54.
59. Sztein MB, Wasserman SS, Tacket CO, Edelman R, Hone D, Lindberg AA, Levine MM. Cytokine production patterns and lymphoproliferative responses in volunteers orally immunised with attenuated vaccine strains of Salmonella typhi. J Infect Dis 1994; 170:1508-17.
60. Strindelius L, Degling Wikingsson L, Sjoholm I. Extracellular antigens from Salmonella enteritidis induce effective immune response in mice after oral vaccination. Infect Immun 2002; 70:1434-42.
61. Rollenhagen C, Sorensen M, Rizos K, Hurvitz R, Bumann D. Antigen selection based on expression levels during infection facilitates vaccine development for an intracellular pathogen. Proc Natl Acad Sci USA 2004; 101:8739-44.
62. Ugrinovic S, Menager N, Goh N, Mastroeni P. Characterization and development of T-Cell immune responses in B-cell-deficient (Igh-6 (-/-) mice with Salmonella enterica serovar Typhimurium infection. Infect Immun 2003; 71:6808-19.
63. Ahmed R, Gray D. Immunological memory and protective immunity: understanding their relation. Science 1996; 272:54-60.
64. Levine MM, Ferreccio C, Black RE, Germanier R. Large-scale field trial of Ty21a live oral typhoid vaccine in enteric-coated capsule formulation. Lancet 1987; 1:1049-52.
65. Blattman JN, Anita R, Sourdive DJD, Wang X, Kaech SM, Murali-Krishna K, Altman JD, Ahmed R. Estimating the precursor frequency of naive antigen-specific CD8 T cells. J Exp Med 2002; 195:657-64.
66. Kaech SM, Tan JT, Wherry EJ, Konieczny BT, Surh CD, Ahmed R. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat Immunol 2003; 4:1191-8.
67. + memory T cell subsets. Proc Natl Acad Sci USA 2004; 101:5610-5.
68. Eriksson S, Lucchini S, Thompson A, Rhen M, Hinton JC. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol Microbiol 2003; 47:103-18.
69. Typhoid immunization. Recommendations of the Immunization Practices Advisory Committee (ACIP). MMWR Recomm Rep 1990; 39:1-5.
70. ACIP Updates. Recommendations for the use of antiviral agents in influenza. Advisory Committee on Immunization Practices. Am Fam Physician 1995; 52 (659-660):663.
71. Pryjma J, Baran J, Ernst M, Woloszyn M, Flad HD. Altered antigen-presenting capacity of human monocytes after phagocytosis of bacteria. Infect Immun 1994; 62:1961-7.
72. Mitchell EK, Mastroeni P, Kelly AP, Trowsdale J. Inhibition of cell surface MHC class II expression by Salmonella. Eur J Immunol 2004; 34:2559-67.
73. Qimron U, Madar N, Mittrucker HW et al. Identification of Salmonella typhimurium genes responsible for interference with peptide presentation on MHC class I molecules: Deltayej Salmonella mutants induce superior CD8 T-cell responses. Cell Microbiol 2004; 6:1057-70.
74. Tobar JA, Gonzalez PA, Kalergis AM. Salmonella escape from antigen presentation can be overcome by targeting bacteria to Fcgamma receptors on dendritic cells. J Immunol 2004; 173:4058-65.
75. Chen LM, Kaniga K, Galan JE. Salmonella spp. are cytotoxic for cultured macrophages. Mol Microbiol 1996; 21:1101-15.
76. Monack DM, Raupach B, Hromockyj AE, Falkow S. Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc Natl Acad Sci USA 1996; 93:9833-8.
77. Hersh D, Monack DM, Smith MR, Ghori N, Falkow S, Zychlinsky A. The Salmonella invasin SipB induces macrophage apoptosis by binding to caspase-1. Proc Natl Acad Sci USA 1999; 96: 2396-401.
78. Brennan MA, Cookson BT. Salmonella induces macrophage death by caspase-1-dependent necrosis. Mol Microbiol 2000; 38:31-40.
79. van der Velden AVV, Velasquez M, Starnbach MN. Salmonella rapidly kill dendritic cells via a caspase-1-dependent mechanism. J Immunol 2003; 171:6742-9.
80. al-Ramadi BK, Chen YW, Meissler JJ Jr, Eisenstein TK. Immunosuppression induced by attenuated Salmonella. Reversal by JL-4. J Immunol 1991; 147:1954-61.
81. al-Ramadi BK, Meissler JJ Jr, Huang D, Eisenstein TK. Immunosuppression induced by nitric oxide and its inhibition by interleukin-4. Eur J Immunol 1992; 22:2249-54.
82. Schwacha MG, Meissler JJ Jr, Eisenstein TK. Salmonella typhimurium infection in mice induces nitric oxide-mediated immunosuppression through a natural killer cell-dependent pathway. Infect Immun 1998; 66:5862-6.
83. Hopkins SA, Niedergang F, Corthesy-Theulaz IE, Kraehenbuhl JP. A recombinant Salmonella typhimurium vaccine strain is taken up and survives within murine Peyer's patch dendritic cells. Cell Microbiol 2000; 2:59-68.
84. Yrlid U, Wick MJ. Antigen presentation capacity and cytokine production by murine splenic dendritic cell subsets upon Salmonella encounter. J Immunol 2002; 169:108-16.
85. Jantsch J, Cheminay C, Chakravortty D, Lindig T, Hein J, Hensel M. Intracellular activities of Salmonella enterica in murine dendritic cells. Cell Microbiol 2003; 5:933-45.
86. Johansson C, Wick MJ. Liver dendritic cells present bacterial antigens and produce cytokines upon Salmonella encounter. J Immunol 2004; 172:2496-503.
87. Hsu HS. Pathogenesis and immunity in murine salmonellosis. Microbiol Rev 1989; 53:390-409.
88. Srinivasan A, Foley J, Ravindran R, McSorley SJ. Low-dose salmonella infection evades activation of flagellin-specific CD4 T cells. J Immunol 2004; 173:4091-9.
89. Ferreccio C, Levine MM, Rodriguez H, Contreras R. Comparative efficacy of two, three, or four doses of TY21a live oral typhoid vaccine in enteric-coated capsules: a field trial in an endemic area. J Infect Dis 1989; 159:766-9.