Immunity to salmonellosis

Immunological Reviews

Volumn 240, Issue 1, 2011, Pages 196-210

  Dougan, Gordon ^a   John, Victoria ^a   Palmer, Sophie ^a   Mastroeni, Pietro ^b  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Immunity; Intracellular; Macrophage; Pathogen; Salmonella; Vaccine

Indexed keywords

SALMONELLOSIS VACCINE;

CELLULAR IMMUNITY; HUMAN; HUMORAL IMMUNITY; IMMUNE RESPONSE; IMMUNITY; NONHUMAN; PATHOGENICITY; PRIORITY JOURNAL; REVIEW; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SALMONELLOSIS;

ANIMALS; HUMANS; IMMUNITY; MICE; SALMONELLA ENTERICA; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM;

EID: 79951939319     PISSN: 01052896     EISSN: 1600065X     Source Type: Journal    
DOI: 10.1111/j.1600-065X.2010.00999.x     Document Type: Review

References (172)

1. Euzeby JP Revised Salmonella nomenclature: designation of Salmonella enterica (ex Kauffmann and Edwards 1952) Le Minor and Popoff 1987 sp. nov., nom. rev. as the neotype species of the genus Salmonella Lignieres 1900 (approved lists 1980), rejection of the name Salmonella choleraesuis (Smith 1894) Weldin 1927 (approved lists 1980), and conservation of the name Salmonella typhi (Schroeter 1886) Warren and Scott 1930 (approved lists 1980). Request for an opinion. Int J Syst Bacteriol 1999;49 (Pt 2):927-930.
2. Kauffmann F. The classification and nomenclature of salmonella-species. Zentralbl Bakteriol Orig A 1973;223:508-512.
3. Glaser JB, et al. Recurrent Salmonella typhimurium bacteremia associated with the acquired immunodeficiency syndrome. Ann Intern Med 1985;102:189-193.
4. Gordon MA. Salmonella infections in immunocompromised adults. J Infect 2008;56:413-422.
5. Kingsley RA, et al. Epidemic multiple drug resistant Salmonella typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. Genome Res 2009;19:2279-2287.
6. Libby SJ, et al. Humanized nonobese diabetic-scid IL2rgammanull mice are susceptible to lethal Salmonella Typhi infection. Proc Natl Acad Sci USA 2010;107:15589-15594.
7. Paulin SM, et al. Analysis of Salmonella enterica serotype-host specificity in calves: avirulence of S. enterica serotype gallinarum correlates with bacterial dissemination from mesenteric lymph nodes and persistence in vivo. Infect Immun 2002;70:6788-6797.
8. Hormaeche CE. Natural resistance to Salmonella typhimurium in different inbred mouse strains. Immunology 1979;37:311-318.
9. Rescigno M, Borrow P. The host-pathogen interaction: new themes from dendritic cell biology. Cell 2001;106:267-270.
10. Richter-Dahlfors A, Buchan AM, Finlay BB. Murine salmonellosis studied by confocal microscopy: Salmonella typhimurium resides intracellularly inside macrophages and exerts a cytotoxic effect on phagocytes in vivo. J Exp Med 1997;186:569-580.
11. Fields PI, et al. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci USA 1986;83:5189-5193.
12. Parkhill J, et al. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 2001;413:848-852.
13. McClelland M, et al. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 2001;413:852-856.
14. Hensel M, et al. Simultaneous identification of bacterial virulence genes by negative selection. Science 1995;269:400-403.
15. Galan JE, Curtiss R 3rd. Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc Natl Acad Sci USA 1989;86:6383-6387.
16. Hindle Z, et al. Characterization of Salmonella enterica derivatives harboring defined aroC and Salmonella pathogenicity island 2 type III secretion system (ssaV) mutations by immunization of healthy volunteers. Infect Immun 2002;70:3457-3467.
17. Hoiseth SK, Stocker BA. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 1981;291:238-239.
18. Miller I, et al. Isolation of orally attenuated Salmonella typhimurium following TnphoA mutagenesis. Infect Immun 1989;57:2758-2763.
19. Miller SI, Kukral AM, Mekalanos JJ. A two-component regulatory system (phoP phoQ) controls Salmonella typhimurium virulence. Proc Natl Acad Sci USA 1989;86:5054-5058.
20. O'Callaghan D, et al. Characterization of aromatic- and purine-dependent Salmonella typhimurium: attention, persistence, and ability to induce protective immunity in BALB/c mice. Infect Immun 1988;56:419-423.
21. Villarreal-Ramos B, et al. Susceptibility of calves to challenge with Salmonella typhimurium 4/74 and derivatives harbouring mutations in htrA or purE. Microbiology 2000;146:2775-2783.
22. Pullinger GD, et al. Systemic translocation of Salmonella enterica serovar Dublin in cattle occurs predominantly via efferent lymphatics in a cell-free niche and requires type III secretion system 1 (T3SS-1) but not T3SS-2. Infect Immun 2007;75:5191-5199.
23. Hornick RB, et al. Typhoid fever: pathogenesis and immunologic control. N Engl J Med 1970;283:686-691.
24. Muller C, et al. Acid stress activation of the sigma(E) stress response in Salmonella enterica serovar Typhimurium. Mol Microbiol 2009;71:1228-1238.
25. Kingsley RA, et al. Molecular and phenotypic analysis of the CS54 island of Salmonella enterica serotype typhimurium: identification of intestinal colonization and persistence determinants. Infect Immun 2003;71:629-640.
26. Michetti P, et al. Monoclonal immunoglobulin A prevents adherence and invasion of polarized epithelial cell monolayers by Salmonella typhimurium. Gastroenterology 1994;107:915-923.
27. Bishop A, et al. Interaction of Salmonella enterica serovar Typhi with cultured epithelial cells: roles of surface structures in adhesion and invasion. Microbiology 2008;154:1914-1926.
28. Jensen VB, Harty JT, Jones BD. Interactions of the invasive pathogens Salmonella typhimurium, Listeria monocytogenes, and Shigella flexneri with M cells and murine Peyer's patches. Infect Immun 1998;66:3758-3766.
29. Halle S, et al. Solitary intestinal lymphoid tissue provides a productive port of entry for Salmonella enterica serovar Typhimurium. Infect Immun 2007;75:1577-1585.
30. Jepson MA, Clark MA. The role of M cells in Salmonella infection. Microbes Infect 2001;3:1183-1190.
31. Hernandez LD, et al. A Salmonella protein causes macrophage cell death by inducing autophagy. J Cell Biol 2003;163:1123-1131.
32. Jones BD, Ghori N, Falkow S. Salmonella typhimurium initiates murine infection by penetrating and destroying the specialized epithelial M cells of the Peyer's patches. J Exp Med 1994;180:15-23.
33. Penheiter KL, et al. Non-invasive Salmonella typhimurium mutants are avirulent because of an inability to enter and destroy M cells of ileal Peyer's patches. Mol Microbiol 1997;24:697-709.
34. Hopkins SA, et al. A recombinant Salmonella typhimurium vaccine strain is taken up and survives within murine Peyer's patch dendritic cells. Cell Microbiol 2000;2:59-68.
35. Johansson C, Wick MJ. Liver dendritic cells present bacterial antigens and produce cytokines upon Salmonella encounter. J Immunol 2004;172:2496-2503.
36. Kirby AC, et al. Differential involvement of dendritic cell subsets during acute Salmonella infection. J Immunol 2001;166:6802-6811.
37. Petrovska L, et al. Salmonella enterica serovar Typhimurium interaction with dendritic cells: impact of the sifA gene. Cell Microbiol 2004;6:1071-1084.
38. Sundquist M, Wick MJ. TNF-alpha-dependent and -independent maturation of dendritic cells and recruited CD11c(int)CD11b+ Cells during oral Salmonella infection. J Immunol 2005;175:3287-3298.
39. Tam MA, et al. Early cellular responses to Salmonella infection: dendritic cells, monocytes, and more. Immunol Rev 2008;225:140-162.
40. Tam MA, Sundquist M, Wick MJ. MyD88 and IFN-alphabeta differentially control maturation of bystander but not Salmonella-associated dendritic cells or CD11cintCD11b+ cells during infection. Cell Microbiol 2008;10:1517-1529.
41. van der Velden AW, Velasquez M, Starnbach MN. Salmonella rapidly kill dendritic cells via a caspase-1-dependent mechanism. J Immunol 2003;171:6742-6749.
42. Wick MJ. The role of dendritic cells during Salmonella infection. Curr Opin Immunol 2002;14:437-443.
43. Yrlid U, et al. In vivo activation of dendritic cells and T cells during Salmonella enterica serovar Typhimurium infection. Infect Immun 2001;69:5726-5735.
44. Yrlid U, Wick MJ. Antigen presentation capacity and cytokine production by murine splenic dendritic cell subsets upon Salmonella encounter. J Immunol 2002;169:108-116.
45. Vazquez-Torres A, et al. Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature 1999;401:804-808.
46. Rescigno M, et al. Dendritic cells shuttle microbes across gut epithelial monolayers. Immunobiology 2001;204:572-581.
47. Rescigno M, et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol 2001;2:361-367.
48. Hapfelmeier S, et al. The Salmonella pathogenicity island (SPI)-2 and SPI-1 type III secretion systems allow Salmonella serovar typhimurium to trigger colitis via MyD88-dependent and MyD88-independent mechanisms. J Immunol 2005;174:1675-1685.
49. Gordon MA, et al. Non-typhoidal salmonella bacteraemia among HIV-infected Malawian adults: high mortality and frequent recrudescence. AIDS 2002;16:1633-1641.
50. Graham SM, et al. Malaria and Salmonella infections: cause or coincidence? Trans R Soc Trop Med Hyg 2000;94:227.
51. MacLennan C, et al. Interleukin (IL)-12 and IL-23 are key cytokines for immunity against Salmonella in humans. J Infect Dis 2004;190:1755-1757.
52. Raffatellu M, et al. The Vi capsular antigen of Salmonella enterica serotype Typhi reduces Toll-like receptor-dependent interleukin-8 expression in the intestinal mucosa. Infect Immun 2005;73:367-374.
53. Sharma A, Qadri A. Vi polysaccharide of Salmonella typhi targets the prohibitin family of molecules in intestinal epithelial cells and suppresses early inflammatory responses. Proc Natl Acad Sci USA 2004;101:17492-17497.
54. Holt KE, et al. High-throughput sequencing provides insights into genome variation and evolution in Salmonella Typhi. Nat Genet 2008;40:987-993.
55. Wilson RP, et al. The Vi-capsule prevents Toll-like receptor 4 recognition of Salmonella. Cell Microbiol 2008;10:876-890.
56. Uematsu S, et al. Detection of pathogenic intestinal bacteria by Toll-like receptor 5 on intestinal CD11c+ lamina propria cells. Nat Immunol 2006;7:868-874.
57. Johansson C, Ingman M, Wick MJ. Elevated neutrophil, macrophage and dendritic cell numbers characterize immune cell populations in mice chronically infected with Salmonella. Microb Pathog 2006;41:49-58.
58. Rydstrom A, Wick MJ. Monocyte recruitment, activation, and function in the gut-associated lymphoid tissue during oral Salmonella infection. J Immunol 2007;178:5789-5801.
59. Salcedo SP, et al. Intracellular replication of Salmonella typhimurium strains in specific subsets of splenic macrophages in vivo. Cell Microbiol 2001;3:587-597.
60. Chakravortty D, Hansen-Wester I, Hensel M. Salmonella pathogenicity island 2 mediates protection of intracellular Salmonella from reactive nitrogen intermediates. J Exp Med 2002;195:1155-1166.
61. Schwan WR, et al. Differential bacterial survival, replication, and apoptosis-inducing ability of Salmonella serovars within human and murine macrophages. Infect Immun 2000;68:1005-1013.
62. Watson PR, et al. Salmonella enterica serovars Typhimurium and Dublin can lyse macrophages by a mechanism distinct from apoptosis. Infect Immun 2000;68:3744-3747.
63. Mastroeni P, et al. Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. II. Effects on microbial proliferation and host survival in vivo. J Exp Med 2000;192:237-248.
64. Blanden RV, Mackaness GB, Collins FM. Mechanisms of acquired resistance in mouse typhoid. J Exp Med 1966;124:585-600.
65. Monack DM, Bouley DM, Falkow S. Salmonella typhimurium persists within macrophages in the mesenteric lymph nodes of chronically infected Nramp1+/+ mice and can be reactivated by IFNgamma neutralization. J Exp Med 2004;199:231-241.
66. Mittrucker HW, et al. Cutting edge: role of B lymphocytes in protective immunity against Salmonella typhimurium infection. J Immunol 2000;164:1648-1652.
67. Dunstan SJ, et al. Genes of the class II and class III major histocompatibility complex are associated with typhoid fever in Vietnam. J Infect Dis 2001;183:261-268.
68. Mastroeni P, Sheppard M. Salmonella infections in the mouse model: host resistance factors and in vivo dynamics of bacterial spread and distribution in the tissues. Microbes Infect 2004;6:398-405.
69. Sheppard M, et al. Dynamics of bacterial growth and distribution within the liver during Salmonella infection. Cell Microbiol 2003;5:593-600.
70. Brown SP, et al. Intracellular demography and the dynamics of Salmonella enterica infections. PLoS Biol 2006;4:e349.
71. Grant AJ, et al. Modelling within-host spatiotemporal dynamics of invasive bacterial disease. PLoS Biol 2008;6:e74.
72. Maskell DJ, Hormaeche CE. Genes within the major histocompatibility complex influence the response to ampicillin therapy and severity of relapse in H-2 congenic, susceptible Itys mice infected with virulent Salmonella typhimurium. J Immunogenet 1986;13:451-457.
73. Nauciel C. Role of CD4+ T cells and T-independent mechanisms in acquired resistance to Salmonella typhimurium infection. J Immunol 1990;145:1265-1269.
74. Hormaeche CE, Maskell DJ. Influence of the Ity gene on salmonella infections. Res Immunol 1989;140:791-793.
75. Hormaeche CE, Harrington KA, Joysey HS. Natural resistance to salmonellae in mice: control by genes within the major histocompatibility complex. J Infect Dis 1985;152:1050-1056.
76. Fernandez-Beros ME, et al. Immune response to the iron-deprivation-induced proteins of Salmonella typhi in typhoid fever. Infect Immun 1989;57:1271-1275.
77. Gil-Cruz C, et al. The porin OmpD from nontyphoidal Salmonella is a key target for a protective B1b cell antibody response. Proc Natl Acad Sci USA 2009;106:9803-9808.
78. Harada H, et al. Development of a mucosal complex vaccine against oral Salmonella infection in mice. Microbiol Immunol 2002;46:891-905.
79. VanCott JL, et al. Regulation of host immune responses by modification of Salmonella virulence genes. Nat Med 1998;4:1247-1252.
80. Lawley TD, et al. Host transmission of Salmonella enterica serovar Typhimurium is controlled by virulence factors and indigenous intestinal microbiota. Infect Immun 2008;76:403-416.
81. Barman M, et al. Enteric salmonellosis disrupts the microbial ecology of the murine gastrointestinal tract. Infect Immun 2008;76:907-915.
82. Bohnhoff M, Miller CP. Enhanced susceptibility to Salmonella infection in streptomycin-treated mice. J Infect Dis 1962;111:117-127.
83. Miller CP, Bohnhoff M. Changes in the mouse's enteric microflora associated with enhanced susceptibility to Salmonella infection following streptomycin treatment. J Infect Dis 1963;113:59-66.
84. Stecher B, et al. Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol 2007;5:2177-2189.
85. Jones BD. Host responses to pathogenic Salmonella infection. Genes Dev 1997;11:679-687.
86. Mastroeni P, et al. Interleukin-12 is required for control of the growth of attenuated aromatic-compound-dependent salmonellae in BALB/c mice: role of gamma interferon and macrophage activation. Infect Immun 1998;66:4767-4776.
87. Mastroeni P, et al. Igh-6(-/-) (B-cell-deficient) mice fail to mount solid acquired 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.
88. Mittrucker HW, Kaufmann SH. Immune response to infection with Salmonella typhimurium in mice. J Leukoc Biol 2000;67:457-463.
89. Monack DM, Detweiler CS, Falkow S. Salmonella pathogenicity island 2-dependent macrophage death is mediated in part by the host cysteine protease caspase-1. Cell Microbiol 2001;3:825-837.
90. Lara-Tejero M, et al. Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis. J Exp Med 2006;203:1407-1412.
91. Bergsbaken T, Fink SL, Cookson BT. Pyroptosis: host cell death and inflammation. Nat Rev Microbiol 2009;7:99-109.
92. Franchi L, et al. The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat Immunol 2009;10:241-247.
93. Wijburg OL, et al. Innate secretory antibodies protect against natural Salmonella typhimurium infection. J Exp Med 2006;203:21-26.
94. Crouch ML, et al. The alternative sigma factor sigma is required for resistance of Salmonella enterica serovar Typhimurium to anti-microbial peptides. Mol Microbiol 2005;56:789-799.
95. Robbins JD, Robbins JB. Reexamination of the protective role of the capsular polysaccharide (Vi antigen) of Salmonella typhi. J Infect Dis 1984;150:436-449.
96. Acharya IL, et al. Prevention of typhoid fever in Nepal with the Vi capsular polysaccharide of Salmonella typhi. A preliminary report. N Engl J Med 1987;317:1101-1104.
97. Klugman KP, et al. Protective activity of Vi capsular polysaccharide vaccine against typhoid fever. Lancet 1987;2:1165-1169.
98. Parry CM, et al. Typhoid fever. N Engl J Med 2002;347:1770-1782.
99. Mai NL, et al. Persistent efficacy of Vi conjugate vaccine against typhoid fever in young children. N Engl J Med 2003;349:1390-1391.
100. Hormaeche CE. The in vivo division and death rates of Salmonella typhimurium in the spleens of naturally resistant and susceptible mice measured by the superinfecting phage technique of Meynell. Immunology 1980;41:973-979.
101. Mastroeni P, Villarreal-Ramos B, Hormaeche CE. 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 1992;13:477-491.
102. Tite JP, Dougan G, Chatfield SN. The involvement of tumor necrosis factor in immunity to Salmonella infection. J Immunol 1991;147:3161-3164.
103. Mastroeni P, et al. Serum TNF alpha inhibitor in mouse typhoid. Microb Pathog 1992;12:343-349.
104. Mastroeni P, Villarreal-Ramos B, Hormaeche CE. Effect of late administration of anti-TNF alpha antibodies on a Salmonella infection in the mouse model. Microb Pathog 1993;14:473-480.
105. Everest P, et al. The molecular mechanisms of severe typhoid fever. Trends Microbiol 2001;9:316-320.
106. Everest P, Roberts M, Dougan G. Susceptibility to Salmonella typhimurium infection and effectiveness of vaccination in mice deficient in the tumor necrosis factor alpha p55 receptor. Infect Immun 1998;66:3355-3364.
107. Khan SA, et al. Early responses to Salmonella typhimurium infection in mice occur at focal lesions in infected organs. Microb Pathog 2001;30:29-38.
108. Mastroeni P, et al. Interleukin 18 contributes to host resistance and gamma interferon production in mice infected with virulent Salmonella typhimurium. Infect Immun 1999;67:478-483.
109. 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;66:5862-5866.
110. Young D, Hussell T, Dougan G. Chronic bacterial infections: living with unwanted guests. Nat Immunol 2002;3:1026-1032.
111. Muotiala A, Makela PH. The role of IFN-gamma in murine Salmonella typhimurium infection. Microb Pathog 1990;8:135-141.
112. Gaspal F, et al. Critical synergy of CD30 and OX40 signals in CD4 T cell homeostasis and Th1 immunity to Salmonella. J Immunol 2008;180:2824-2829.
113. Martinoli C, Chiavelli A, Rescigno M. Entry route of Salmonella typhimurium directs the type of induced immune response. Immunity 2007;27:975-984.
114. Pie S, et al. Th1 response in Salmonella typhimurium-infected mice with a high or low rate of bacterial clearance. Infect Immun 1997;65:4509-4514.
115. Hess J, et al. 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 1996;156:3321-3326.
116. Ugrinovic S, et al. Characterization and development of T-Cell immune responses in B-cell-deficient (Igh-6(-/-)) mice with Salmonella enterica serovar Typhimurium infection. Infect Immun 2003;71:6808-6819.
117. Salazar-Gonzalez RM, et al. CCR6-mediated dendritic cell activation of pathogen-specific T cells in Peyer's patches. Immunity 2006;24:623-632.
118. Sinha K, et al. Salmonella typhimurium aroA, htrA, and aroD htrA mutants cause progressive infections in athymic (nu/nu) BALB/c mice. Infect Immun 1997;65:1566-1569.
119. Mastroeni P, Villarreal-Ramos B, Hormaeche CE. 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 1993;61:3981-3984.
120. 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;172:6884-6893.
121. Srinivasan A, et al. Low-dose Salmonella infection evades activation of flagellin-specific CD4 T cells. J Immunol 2004;173:4091-4099.
122. Srinivasan A, et al. Innate immune activation of CD4 T cells in salmonella-infected mice is dependent on IL-18. J Immunol 2007;178:6342-6459.
123. Raffatellu M, et al. Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nat Med 2008;14:421-428.
124. Godinez I, et al. Interleukin-23 orchestrates mucosal responses to Salmonella enterica serotype Typhimurium in the intestine. Infect Immun 2009;77:387-398.
125. Liu JZ, Pezeshki M, Raffatellu M. Th17 cytokines and host-pathogen interactions at the mucosa: dichotomies of help and harm. Cytokine 2009;48:156-160.
126. Mackenzie G, et al. A decline in the incidence of invasive non-typhoidal Salmonella infection in The Gambia temporally associated with a decline in malaria infection. PLoS ONE 2010;5:e10568.
127. Raffatellu M, et al. Lipocalin-2 resistance confers an advantage to Salmonella enterica serotype Typhimurium for growth and survival in the inflamed intestine. Cell Host Microbe 2009;5:476-486.
128. Bergman MA, et al. CD4+-T-cell responses generated during murine Salmonella enterica serovar Typhimurium infection are directed towards multiple epitopes within the natural antigen FliC. Infect Immun 2005;73:7226-7235.
129. Cunningham AF, et al. Responses to the soluble flagellar protein FliC are Th2, while those to FliC on Salmonella are Th1. Eur J Immunol 2004;34:2986-2995.
130. Salazar-Gonzalez RM, McSorley SJ. Salmonella flagellin, a microbial target of the innate and adaptive immune system. Immunol Lett 2005;101:117-122.
131. Alaniz RC, et al. Salmonella typhimurium coordinately regulates FliC location and reduces dendritic cell activation and antigen presentation to CD4+ T cells. J Immunol 2006;177:3983-3993.
132. Cummings LA, et al. FliC-specific CD4+ T cell responses are restricted by bacterial regulation of antigen expression. J Immunol 2005;174:7929-7938.
133. Akeda H, et al. The synergistic contribution of macrophages and antibody to protection against Salmonella typhimurium during the early phase of infection. J Gen Microbiol 1981;123:209-214.
134. Angerman CR, Eisenstein TK. Correlation of the duration and magnitude of protection against Salmonella infection afforded by various vaccines with antibody titers. Infect Immun 1980;27:435-443.
135. MacLennan CA, et al. The neglected role of antibody in protection against bacteremia caused by nontyphoidal strains of Salmonella in African children. J Clin Invest 2008;118:1553-1562.
136. Collins FM. Vaccines and cell-mediated immunity. Bacteriol Rev 1974;38:371-402.
137. Uppington H, et al. Effect of immune serum and role of individual Fcgamma receptors on the intracellular distribution and survival of Salmonella enterica serovar Typhimurium in murine macrophages. Immunology 2006;119:147-158.
138. Menager N, et al. Fcgamma receptors are crucial for the expression of acquired resistance to virulent Salmonella enterica serovar Typhimurium in vivo but are not required for the induction of humoral or T-cell-mediated immunity. Immunology 2007;120:424-432.
139. Rodriguez A, et al. Requirement of bic/microRNA-155 for normal immune function. Science 2007;316:608-611.
140. Barr TA, et al. TLR and B cell receptor signals to B cells differentially program primary and memory Th1 responses to Salmonella enterica. J Immunol 2010;185:2783-2789.
141. Vazquez-Torres A, et al. Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. Science 2000;287:1655-1658.
142. Giannella RA, Broitman SA, Zamcheck N. Salmonella enteritis. I. Role of reduced gastric secretion in pathogenesis. Am J Dig Dis 1971;16:1000-1006.
143. Salzman NH, et al. Protection against enteric salmonellosis in transgenic mice expressing a human intestinal defensin. Nature 2003;422:522-526.
144. Zasloff M. Trypsin, for the defense. Nat Immunol 2002;3:508-510.
145. Lazarus GM, Neu HC. Agents responsible for infection in chronic granulomatous disease of childhood. J Pediatr 1975;86:415-417.
146. Landesman SH, Rao SP, Ahonkhai VI. Infections in children with sickle cell anemia. Special reference to pneumococcal and salmonella infections. Am J Pediatr Hematol Oncol 1982;4:407-418.
147. Hermaszewski RA, Webster AD. Primary hypogammaglobulinaemia: a survey of clinical manifestations and complications. Q J Med 1993;86:31-42.
148. Leen CL, et al. Salmonellosis in patients with primary hypogammaglobulinaemia. J Infect 1986;12:241-245.
149. Tarr PE, et al. Infections in patients with immunodeficiency with thymoma (Good syndrome). Report of 5 cases and review of the literature. Medicine 2001;80:123-133.
150. Kelleher P, Misbah SA. What is Good's syndrome? Immunological abnormalities in patients with thymoma. J Clin Pathol 2003;56:12-16.
151. Levy J, et al. Clinical spectrum of X-linked hyper-IgM syndrome. J Pediatr 1997;131:47-54.
152. Dunstan SJ, et al. A TNF region haplotype offers protection from typhoid fever in Vietnamese patients. Hum Genet 2007;122:51-61.
153. Lammas DA, Casanova JL, Kumararatne DS. Clinical consequences of defects in the IL-12-dependent interferon-gamma (IFN-gamma) pathway. Clin Exp Immunol 2000;121:417-425.
154. Remus N, et al. Impaired interferon gamma-mediated immunity and susceptibility to mycobacterial infection in childhood. Pediatr Res 2001;50:8-13.
155. Picard C, et al. Inherited interleukin-12 deficiency: IL12B genotype and clinical phenotype of 13 patients from six kindreds. Am J Hum Genet 2002;70:336-348.
156. Fieschi C, et al. Low penetrance, broad resistance, and favorable outcome of interleukin 12 receptor beta1 deficiency: medical and immunological implications. J Exp Med 2003;197:527-535.
157. Doffinger R, et al. Inherited disorders of IL-12- and IFNgamma-mediated immunity: a molecular genetics update. Mol Immunol 2002;38:903-909.
158. Doffinger R, et al. X-linked anhidrotic ectodermal dysplasia with immunodeficiency is caused by impaired NF-kappaB signaling. Nat Genet 2001;27:277-285.
159. Hart CA, et al. Infections in AIDS. J Med Microbiol 2000;49:947-967.
160. Celum CL, et al. Incidence of salmonellosis in patients with AIDS. J Infect Dis 1987;156:998-1002.
161. MacLennan CA, et al. Dysregulated humoral immunity to nontyphoidal Salmonella in HIV-infected African adults. Science 2010;328:508-512.
162. Klein C, et al. Major histocompatibility complex class II deficiency: clinical manifestations, immunologic features, and outcome. J Pediatr 1993;123:921-928.
163. Nguyen QC, et al. A clinical, microbiological, and pathological study of intestinal perforation associated with typhoid fever. Clin Infect Dis 2004;39:61-67.
164. Marmion DE, Naylor GR, Stewart IO. Second attacks of typhoid fever. J Hyg 1953;51:260-267.
165. Wain J, et al. Molecular typing of multiple-antibiotic-resistant Salmonella enterica serovar Typhi from Vietnam: application to acute and relapse cases of typhoid fever. J Clin Microbiol 1999;37:2466-2472.
166. Kantele A, et al. Differences in immune responses induced by oral and rectal immunizations with Salmonella typhi Ty21a: evidence for compartmentalization within the common mucosal immune system in humans. Infect Immun 1998;66:5630-5635.
167. Kilhamn J, et al. T- and B-cell immune responses of patients who had undergone colectomies to oral administration of Salmonella enterica serovar Typhi Ty21a vaccine. Clin Diagn Lab Immunol 2003;10:426-430.
168. Sztein MB, et al. Cytokine production patterns and lymphoproliferative responses in volunteers orally immunized with attenuated vaccine strains of Salmonella typhi. J Infect Dis 1994;170:1508-1517.
169. Salerno-Goncalves R, et al. Identification of a human HLA-E-restricted CD8+ T cell subset in volunteers immunized with Salmonella enterica serovar Typhi strain Ty21a typhoid vaccine. J Immunol 2004;173:5852-5862.
170. Salerno-Goncalves R, et al. Generation of heterogeneous memory T cells by live attenuated tularemia vaccine in humans. Vaccine 2009;28:195-206.
171. Salerno-Goncalves R, Sztein MB. Priming of Salmonella enterica serovar typhi-specific CD8(+) T cells by suicide dendritic cell cross-presentation in humans. PLoS ONE 2009;4:e5879.
172. Sztein MB. Cell-mediated immunity and antibody responses elicited by attenuated Salmonella enterica Serovar Typhi strains used as live oral vaccines in humans. Clin Infect Dis 2007;45(Suppl):S15-S19.