Salmonella, the host and disease: A brief review

Immunology and Cell Biology

Volumn 85, Issue 2, 2007, Pages 112-118

  Coburn, Bryan ^a,b   Grassl, Guntram A ^a   Finlay, B B ^a,b  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Enterocolitis; PAMP; Salmonella; SPI; Typhoid; Virulence

Indexed keywords

ANTIINFECTIVE AGENT; CYTOKINE; FLAGELLIN; GAMMA INTERFERON ANTIBODY; GENE PRODUCT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 12; INTERLEUKIN 18 ANTIBODY; LIPOPOLYSACCHARIDE; NALIDIXIC ACID; QUINOLINE DERIVED ANTIINFECTIVE AGENT; SALMONELLA PATHOGENICITY ISLAND 1 PROTEIN; SALMONELLA PATHOGENICITY ISLAND 2 PROTEIN; SALMONELLOSIS VACCINE; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG;

DIARRHEA; ENTEROCOLITIS; HOST; HUMAN; INFECTION CONTROL; INFLAMMATION; INNATE IMMUNITY; NEUTROPHIL; NONHUMAN; PATHOGENESIS; REVIEW; SALMONELLA; SALMONELLA ENTERICA; SALMONELLOSIS; TYPHOID FEVER; VIRULENCE;

ANIMALS; BACTERIAL PROTEINS; CYTOKINES; DIARRHEA; DISEASE SUSCEPTIBILITY; ENTEROCOLITIS; HOST-PARASITE RELATIONS; HUMANS; IMMUNITY, NATURAL; INFLAMMATION; NEUTROPHIL INFILTRATION; NF-KAPPA B; SALMONELLA; SALMONELLA INFECTIONS; TOLL-LIKE RECEPTOR 4; VIRULENCE FACTORS;

SALMONELLA; SALMONELLA ENTERICA;

EID: 33947129778     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/sj.icb.7100007     Document Type: Review

References (115)

1. Ochman H, Groisman EA. The origin and evolution of species differences in Escherichia coli and Salmonella typhimurium. EXS 1994; 69: 479-493.
2. Fierer J, Guiney DG. Diverse virulence traits underlying different clinical outcomes of Salmonella infection. J Clin Invest 2001; 107: 775-780.
3. Baumler AJ, Tsolis RM, Ficht TA, Adams LG. Evolution of host adaptation in Salmonella enterica. Infect Immun 1998; 66: 4579-4587.
4. Hornick RB. Pathogenesis of typhoid fever. J Egypt Public Health Assoc 1970; 45: 247-259.
5. Bonhoff M, Drake BL, Miller CP. Effect of streptomycin on susceptibility of intestinal tract to experimental Salmonella infection. Proc Soc Exp Biol Med 1954; 86: 132-137.
6. Stecher B, Macpherson AJ, Hapfelmeier S, Kremer M, Stallmach T, Hardt WD. Comparison of Salmonella enterica serovar Typhimurium colitis in germfree mice and mice pretreated with streptomycin. Infect Immun 2005; 73: 3228-3241.
7. 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.
8. Rescigno M, Urbano M, Valzasina B, Francolini M, Rotta G, Bonasio R et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol 2001; 2: 361-367.
9. Vazquez-Torres A, Jones-Carson J, Baumler AJ, Falkow S, Valdivia R, Brown W et al. Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature 1999; 401: 804-808.
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. 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: 5726-5735.
12. Nakoneczna I, Hsu HS. The comparative histopathology of primary and secondary lesions in murine salmonellosis. Br J Exp Pathol 1980; 61: 76-84.
13. Fields PI, Swanson RV, Haidaris CG, Heffron F. Mutants of Salmonella typhimurium that cannot survive within the macrophage are avirulent. Proc Natl Acad Sci USA 1986; 83: 5189-5193.
14. Gorvel JP, Meresse S. Maturation steps of the Salmonella- containing vacuole. Microbes Infect 2001; 3: 1299-1303.
15. Meresse S, Steele-Mortimer O, Finlay BB, Gorvel JP. The rab7 GTPase controls the maturation of Salmonella typhimurium-containing vacuoles in HeLa cells. EMBO J 1999; 18: 4394-4403.
16. Steele-Mortimer O, Meresse S, Gorvel JP, Toh BH, Finlay BB. Biogenesis of Salmonella typhimurium-containing vacuoles in epithelial cells involves interactions with the early endocytic pathway. Cell Microbiol 1999; 1: 33-49.
17. Vazquez-Torres A, Xu YS, Jones-Carson J, Holden DW, Lucia SM, Dinauer MC et al. Salmonella pathogenicity island 2-dependent evasion of the phagocyte NADPH oxidase. Science 2000; 287: 1655-1658.
18. Parry CM, Hien TT, Dougan G, White NJ, Farrar JJ. Typhoid fever. N Engl J Med 2002; 347: 1770-1782.
19. World Health Organization Drug-Resistant Salmonella. http://www.who.int/mediacentre/factsheets/fs139/en/print.html. 2005. WHO website.
20. Barthel M, Hapfelmeier S, Quintanilla-Martinez L, Kremer M, Rohde M, Hogardt M et al. Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect Immun 2003; 71: 2839-2858.
21. Mcgovern VJ, Slavutin LJ. Pathology of Salmonella Colitis. Am J Surg Pathol 1979; 3: 483-490.
22. Giannella RA, Formal SB, Dammin GJ, Collins H. Pathogenesis of salmonellosis. Studies of fluid secretion, mucosal invasion, and morphologic reaction in the rabbit ileum. J Clin Invest 1973; 52: 441-453.
23. Clarke RC, Gyles CL. Virulence of wild and mutant strains of Salmonella typhimurium in ligated intestinal segments of calves, pigs, and rabbits. Am J Vet Res 1987; 48: 504-510.
24. Finlay BB, Heffron F, Falkow S. Epithelial cell surfaces induce Salmonella proteins required for bacterial adherence and invasion. Science 1989; 243: 940-943.
25. McCormick BA, Colgan SP, Delp-Archer C, Miller SI, Madara JL. Salmonella typhimurium attachment to human intestinal epithelial monolayers: transcellular signalling to subepithelial neutrophils. J Cell Biol 1993; 123: 895-907.
26. McCormick BA, Miller SI, Carnes D, Madara JL. Transepithelial signaling to neutrophils by salmonellae - a novel virulence mechanism for gastroenteritis. Infect Immun 1995; 63: 2302-2309.
27. Tsolis RM, Adams LG, Ficht TA, Baumler AJ. Contribution of Salmonella typhimurium virulence factors to diarrheal disease in calves. Infect Immun 1999; 67: 4879-4885.
28. Wray C, Sojka WJ. Experimental Salmonella typhimurium infection in calves. Res Vet Sci 1978; 25: 139-143.
29. Wallis TS, Hawker RJ, Candy DC, Qi GM, Clarke GJ, Worton KJ et al. Quantification of the leucocyte influx into rabbit ileal loops induced by strains of Salmonella typhimurium of different virulence. J Med Microbiol 1989; 30: 149-156.
30. Boyd JF. Pathology of the alimentary tract in Salmonella typhimurium food poisoning. Gut 1985; 26: 935-944.
31. Galan JE, Curtiss III R. 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.
32. Mills DM, Bajaj V, Lee CA. A 40 kb chromosomal fragment encoding Salmonella typhimurium invasion genes is absent from the corresponding region of the Escherichia coli K-12 chromosome. Mol Microbiol 1995; 15: 749-759.
33. McCormick BA, Parkos CA, Colgan SP, Carnes DK, Madara JL. Apical secretion of a pathogen-elicited epithelial chemoattractant activity in response to surface colonization of intestinal epithelia by Salmonella typhimurium. J Immunol 1998; 160: 455-466.
34. Gewirtz AT, Siber AM, Madara JL, McCormick BA. Orchestration of neutrophil movement by intestinal epithelial cells in response to Salmonella typhimurium can be uncoupled from bacterial internalization. Infect Immun 1999; 67: 608-617.
35. Lee CA, Silva M, Siber AM, Kelly AJ, Galyov E, McCormick BA. A secreted Salmonella protein induces a proinflammatory response in epithelial cells, which promotes neutrophil migration. Proc Natl Acad Sci USA 2000; 97: 12283-12288.
36. Zhang SP, Santos RL, Tsolis RM, Stender S, Hardt WD, Baumler AJ et al. The Salmonella enterica serotype typhimurium effector proteins SipA, SopA, SopB, SopD, and SopE2 act in concert to induce diarrhea in calves. Infect Immun 2002; 70: 3843-3855.
37. 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: 2396-2401.
38. Monack DM, Hersh D, Ghori N, Bouley D, Zychlinsky A, Falkow S. Salmonella exploits caspase-1 to colonize Peyer's patches in a murine typhoid model. J Exp Med 2000; 192: 249-258.
39. Lara-Tejero M, Sutterwala FS, Ogura Y, Grant EP, Bertin J, Coyle AJ et al. Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis. J Exp Med 2006; 203: 1407-1412.
40. Chen LM, Hobbie S, Galan JE. Requirement of CDC42 for Salmonella-induced cytoskeletal and nuclear responses. Science 1996; 274: 2115-2118.
41. Hobbie S, Chen LM, Davis RJ, Galan JE. Involvement of mitogen-activated protein kinase pathways in the nuclear responses and cytokine production induced by Salmonella typhimurium in cultured intestinal epithelial cells. J Immunol 1997; 159: 5550-5559.
42. Hardt WD, Chen LM, Schuebel KE, Bustelo XR, Galan JE. S. typhimurium encodes an activator of Rho GTPases that induces membrane ruffling and nuclear responses in host cells. Cell 1998; 93: 815-826.
43. Fu Y, Galan JE. A salmonella protein antagonizes Rac-1 and Cdc42 to mediate host-cell recovery after bacterial invasion. Nature 1999; 401: 293-297.
44. Watson PR, Paulin SM, Bland AP, Jones PW, Wallis TS. Characterization of intestinal invasion by Salmonella typhimurium and Salmonella dublin and effect of a mutation in the invH gene. Infect Immun 1995; 63: 2743-2754.
45. Lodge J, Douce GR, Amin II, Bolton AJ, Martin GD, Chatfield S et al. Biological and genetic characterization of TnphoA mutants of Salmonella typhimurium TML in the context of gastroenteritis. Infect Immun 1995; 63: 762-769.
46. Watson PR, Galyov EE, Paulin SM, Jones PW, Wallis TS. Mutation of invH, but not stn, reduces Salmonella-induced enteritis in cattle. Infect Immun 1998; 66: 1432-1438.
47. Galyov EE, Wood MW, Rosqvist R, Mullan PB, Watson PR, Hedges S et al. A secreted effector protein of Salmonella dublin is translocated into eukaryotic cells and mediates inflammation and fluid secretion in infected ileal mucosa. Mol Microbiol 1997; 25: 903-912.
48. Jones MA, Wood MW, Mullan PB, Watson PR, Wallis TS, Galyov EE. Secreted effector proteins of Salmonella dublin act in concert to induce enteritis. Infect Immun 1998; 66: 5799-5804.
49. Wallis TS, Wood M, Watson P, Paulin S, Jones M, Galyov E. Sips, Sops, and SPIs but not STN influence Salmonella enteropathogenesis. Mech Pathogen Enteric Dis 2 1999; 473: 275-280.
50. Wood MW, Jones MA, Watson PR, Hedges S, Wallis TS, Galyov EE. Identification of a pathogenicity island required for Salmonella enteropathogenicity. Mol Microbiol 1998; 29: 883-891.
51. Wood MW, Jones MA, Watson PR, Siber AM, McCormick BA, Hedges S et al. The secreted effector protein of Salmonella dublin, SopA, is translocated into eukaryotic cells and influences the induction of enteritis. Cell Microbiol 2000; 2: 293-303.
52. Zhang S, Santos RL, Tsolis RM, Mirold S, Hardt WD, Adams LG et al. Phage mediated horizontal transfer of the sopE1 gene increases enteropathogenicity of Salmonella enterica serotype Typhimurium for calves. FEMS Microbiol Lett 2002; 217: 243-247.
53. Raffatellu M, Wilson RP, Chessa D, Andrews-Polymenis H, Tran QT, Lawhon S et al. SipA, SopA, SopB, SopD, and SopE2 contribute to Salmonella enterica serotype typhimurium invasion of epithelial cells. Infect Immun 2005; 73: 146-154.
54. Zhang S, Kingsley RA, Santos RL, Andrews-Polymenis H, Raffatellu M, Figueiredo J et al. Molecular pathogenesis of Salmonella enterica serotype typhimurium-induced diarrhea. Infect Immun 2003; 71: 1-12.
55. Santos RL, Tsolis RM, Baumler AJ, Adams LG. Pathogenesis of Salmonella-induced enteritis. Braz J Med Biol Res 2003; 36: 3-12.
56. Hapfelmeier S, Ehrbar K, Stecher B, Barthel M, Kremer M, Hardt WD. Role of the Salmonella pathogenicity island 1 effector proteins SipA, SopB, SopE, and SopE2 in Salmonella enterica subspecies 1 serovar typhimurium colitis in streptomycin-pretreated mice. Infect Immun 2004; 72: 795-809.
57. Coombes BK, Coburn BA, Potter AA, Gomis S, Mirakhur K, Li Y et al. Analysis of the contribution of Salmonella pathogenicity islands 1 and 2 to enteric disease progression using a novel bovine ileal loop model and a murine model of infectious enterocolitis. Infect Immun 2005; 73: 7161-7169.
58. Hapfelmeier S, Stecher B, Barthel M, Kremer M, Muller AJ, Heikenwalder M 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.
59. Zeng H, Carlson AQ, Guo YW, Yu YM, Collier-Hyams LS, Madara JL et al. Flagellin is the major proinflammatory determinant of enteropathogenic Salmonella. J Immunol 2003; 171: 3668-3674.
60. Hensel M, Shea JE, Gleeson C, Jones MD, Dalton E, Holden DW. Simultaneous identification of bacterial virulence genes by negative selection. Science 1995; 269: 400-403.
61. Shea JE, Hensel M, Gleeson C, Holden DW. Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc Natl Acad Sci USA 1996; 93: 2593-2597.
62. Ochman H, Soncini FC, Solomon F, Groisman EA. Identification of a pathogenicity island required for Salmonella survival in host cells. Proc Natl Acad Sci USA 1996; 93: 7800-7804.
63. Coburn B, Li Y, Owen D, Vallance BA, Finlay BB. Salmonella enterica serovar Typhimurium pathogenicity island 2 is necessary for complete virulence in a mouse model of infectious enterocolitis. Infect Immun 2005; 73: 3219-3227.
64. Hapfelmeier S, Stecher B, Barthel M, Kremer M, Muller AJ, Heikenwalder M 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.
65. Bispham J, Tripathi BN, Watson PR, Wallis TS. Salmonella pathogenicity island 2 influences both systemic salmonellosis and Salmonella-induced enteritis in calves. Infect Immun 2001; 69: 367-377.
66. Hapfelmeier S, Hardt WD. A mouse model for S. typhimurium-induced enterocolitis. Trends Microbiol 2005; 13: 497-503.
67. Uchiya K, Groisman EA, Nikai T. Involvement of Salmonella pathogenicity island 2 in the up-regulation of interleukin-10 expression in macrophages: Role of protein kinase a signal pathway. Infect Immun 2004; 72: 1964-1973.
68. Uchiya K, Nikai T. Salmonella pathogenicity island 2-dependent expression of suppressor of cytokine signaling 3 in macrophages. Infect Immun 2005; 73: 5587-5594.
69. Uchiya K, Nikai T. Salmonella enterica serovar Typhimurium infection induces cyclooxygenase 2 expression in macrophages: involvement of Salmonella pathogenicity island 2. Infect Immun 2004; 72: 6860-6869.
70. MacVittie TJ, O'Brien AD, Walker RI, Weinberg SR. Inflammatory response of LPS-hyporesponsive and LPS-responsive mice to challenge with Gram-negative bacteria Salmonella typhimurium and Klebsiella pneumoniae. Adv Exp Med Biol 1982; 155: 325-334.
71. O'Brien AD, Weinstein DA, Soliman MY, Rosenstreich DL. Additional evidence that the Lps gene locus regulates natural resistance to S. typhimurium in mice. J Immunol 1985; 134: 2820-2823.
72. O'Brien AD, Rosenstreich DL, Scher I, Campbell GH, MacDermott RP, Formal SB. Genetic control of susceptibility to Salmonella typhimurium in mice: role of the LPS gene. J Immunol 1980; 124: 20-24.
73. Weinstein DL, Lissner CR, Swanson RN, O'Brien AD. Macrophage defect and inflammatory cell recruitment dysfunction in Salmonella susceptible C3H/HeJ mice. Cell Immunol 1986; 102: 68-77.
74. Vazquez-Torres A, Vallance BA, Bergman MA, Finlay BB, Cookson BT, Jones-Carson J et al. Toll-like receptor 4 dependence of innate and adaptive immunity to Salmonella: importance of the Kupffer cell network. J Immunol 2004; 172: 6202-6208.
75. Rosenberger CM, Scott MG, Gold MR, Hancock RE, Finlay BB. Salmonella typhimurium infection and lipopolysaccharide stimulation induce similar changes in macrophage gene expression. J Immunol 2000; 164: 5894-5904.
76. Royle MC, Totemeyer S, Alldridge LC, Maskell DJ, Bryant CE. Stimulation of Toll-like receptor 4 by lipopolysaccharide during cellular invasion by live Salmonella typhimurium is a critical but not exclusive event leading to macrophage responses. J Immunol 2003; 170: 5445-5454.
77. O'Brien GC, Wang JH, Redmond HP. Bacterial lipoprotein induces resistance to Gram-negative sepsis in TLR4-deficient mice via enhanced bacterial clearance. J Immunol 2005; 174: 1020-1026.
78. Gewirtz AT, Simon Jr PO, Schmitt CK, Taylor LJ, Hagedorn CH, O'Brien AD et al. Salmonella typhimurium translocates flagellin across intestinal epithelia, inducing a proinflammatory response. J Clin Invest 2001; 107: 99-109.
79. Yu Y, Zeng H, Lyons S, Carlson A, Merlin D, Neish AS et al. TLR5-mediated activation of p38 MAPK regulates epithelial IL-8 expression via posttranscriptional mechanism. Am J Physiol Gastrointest Liver Physiol 2003; 285: G282-G290.
80. Gewirtz AT, Rao AS, Simon Jr PO, Merlin D, Carnes D, Madara JL et al. Salmonella typhimurium induces epithelial IL-8 expression via Ca(2+)-mediated activation of the NF-kappaB pathway. J Clin Invest 2000; 105: 79-92.
81. Zeng H, Wu H, Sloane V, Jones R, Yu Y, Lin P et al. Flagellin/TLR5 responses in epithelia reveal intertwined activation of inflammatory and apoptotic pathways. Am J Physiol Gastrointest Liver Physiol 2006; 290: G96-G108.
82. Franchi L, Amer A, Body-Malapel M, Kanneganti TD, Ozoren N, Jagirdar R et al. Cytosolic flagellin requires Ipaf for activation of caspase-1 and interleukin 1beta in salmonella-infected macrophages. Nat Immunol 2006; 7: 576-582.
83. Miao EA, Alpuche-Aranda CM, Dors M, Clark AE, Bader MW, Miller SI et al. Cytoplasmic flagellin activates caspase-1 and secretion of interleukin 1beta via Ipaf. Nat Immunol 2006; 7: 569-575.
84. Subramanian N, Qadri A. Lysophospholipid sensing triggers secretion of flagellin from pathogenic salmonella. Nat Immunol 2006; 7: 583-589.
85. Stecher B, Hapfelmeier S, Muller C, Kremer M, Stallmach T, Hardt WD. Flagella and chemotaxis are required for efficient induction of Salmonella enterica serovar typhimurium colitis in streptomycin-pretreated mice. Infect Immun 2004; 72: 4138-4150.
86. Lyons S, Wang L, Casanova JE, Sitaraman SV, Merlin D, Gewirtz AT. Salmonella typhimurium transcytoses flagellin via an SPI2-mediated vesicular transport pathway. J Cell Sci 2004; 117: 5771-5780.
87. Hapfelmeier S, Stecher B, Barthel M, Kremer M, Muller AJ, Heikenwalder M 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.
88. Jung HC, Eckmann L, Yang SK, Panja A, Fierer J, Morzycka-Wroblewska E et al. A distinct array of proinflammatory cytokines is expressed in human colon epithelial cells in response to bacterial invasion. J Clin Invest 1995; 95: 55-65.
89. Rosenberger CM, Pollard AJ, Finlay BB. Gene array technology to determine host responses to Salmonella. Microb Infect 2001; 3: 1353-1360.
90. Svensson M, Johansson C, Wick MJ. Salmonella typhimurium-induced cytokine production and surface molecule expression by murine macrophages. Microb Pathog 2001; 31: 91-102.
91. 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.
92. Pietila TE, Veckman V, Kyllonen P, Lahteenmaki K, Korhonen TK, Julkunen I. Activation, cytokine production, and intracellular survival of bacteria in Salmonella-infected human monocyte-derived macrophages and dendritic cells. J Leukoc Biol 2005; 78: 909-920.
93. Yrlid U, Svensson M, Johansson C, Wick MJ. Salmonella infection of bone marrow-derived macrophages and dendritic cells: influence on antigen presentation and initiating an immune response. FEMS Immunol Med Microbiol 2000; 27: 313-320.
94. Eckmann L, Kagnoff MF. Cytokines in host defense against Salmonella. Microb Infect 2001; 3: 1191-1200.
95. Ottenhoff TH, Verreck FA, Lichtenauer-Kaligis EG, Hoeve MA, Sanal O, van Dissel JT. Genetics, cytokines and human infectious disease: lessons from weakly pathogenic mycobacteria and salmonellae. Nat Genet 2002; 32: 97-105.
96. van d V, Hoeve MA, Ottenhoff TH. Human genetics of intracellular infectious diseases: molecular and cellular immunity against mycobacteria and salmonellae. Lancet Infect Dis 2004; 4: 739-749.
97. de Jong R, Altare F, Haagen IA, Elferink DG, Boer T, Breda Vriesman PJ et al. Severe mycobacterial and Salmonella infections in interleukin-12 receptor-deficient patients. Science 1998; 280: 1435-1438.
98. Doffinger R, Patel S, Kumararatne DS. Human immunodeficiencies that predispose to intracellular bacterial infections. Curr Opin Rheumatol 2005; 17: 440-446.
99. Sanal O, Turul T, De Boer T, van d V, Yalcin I, Tezcan I et al. Presentation of interleukin-12/-23 receptor beta1 deficiency with various clinical symptoms of Salmonella infections. J Clin Immunol 2006; 26: 1-6.
100. Ottenhoff TH, Kumararatne D, Casanova JL. Novel human immunodeficiencies reveal the essential role of type-I cytokines in immunity to intracellular bacteria. Immunol Today 1998; 19: 491-494.
101. MacLennan C, Fieschi C, Lammas DA, Picard C, Dorman SE, Sanal O et al. Interleukin (IL)-12 and IL-23 are key cytokines for immunity against Salmonella in humans. J Infect Dis 2004; 190: 1755-1757.
102. Muotiala A, Makela PH. The role of IFN-gamma in murine Salmonella typhimurium infection. Microb Pathog 1990; 8: 135-141.
103. Muotiala A, Makela PH. Role of gamma interferon in late stages of murine salmonellosis. Infect Immun 1993; 61: 4248-4253.
104. Tite JP, Dougan G, Chatfield SN. The involvement of tumor necrosis factor in immunity to Salmonella infection. J Immunol 1991; 147: 3161-3164.
105. Gulig PA, Doyle TJ, Clare-Salzler MJ, Maiese RL, Matsui H. Systemic infection of mice by wild-type but not Spv- Salmonella typhimurium is enhanced by neutralization of gamma interferon and tumor necrosis factor alpha. Infect Immun 1997; 65: 5191-5197.
106. Nauciel C, Espinasse-Maes F. Role of gamma interferon and tumor necrosis factor alpha in resistance to Salmonella typhimurium infection. Infect Immun 1992; 60: 450-454.
107. Ramarathinam L, Niesel DW, Klimpel GR. Salmonella typhimurium induces IFN-gamma production in murine splenocytes. Role of natural killer cells and macrophages. J Immunol 1993; 150: 3973-3981.
108. Kirby AC, Yrlid U, Wick MJ. The innate immune response differs in primary and secondary Salmonella infection. J Immunol 2002; 169: 4450-4459.
109. Brigl M, Bry L, Kent SC, Gumperz JE, Brenner MB. Mechanism of CD1d-restricted natural killer T cell activation during microbial infection. Nat Immunol 2003; 4: 1230-1237.
110. 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.
111. Rhee SJ, Walker WA, Cherayil BJ. Developmentally regulated intestinal expression of IFN-gamma and its target genes and the age-specific response to enteric Salmonella infection. J Immunol 2005; 175: 1127-1136.
112. Mastroeni P, Harrison JA, Chabalgoity JA, Hormaeche CE. Effect of interleukin 12 neutralization on host resistance and gamma interferon production in mouse typhoid. Infect Immun 1996; 64: 189-196.
113. Lehmann J, Bellmann S, Werner C, Schroder R, Schutze N, Alber G. IL-12p40-dependent agonistic effects on the development of protective innate and adaptive immunity against Salmonella enteritidis. J Immunol 2001; 167: 5304-5315.
114. Dybing JK, Walters N, Pascual DW. Role of endogenous interleukin-18 in resolving wild-type and attenuated Salmonella typhimurium infections. Infect Immun 1999; 67: 6242-6248.
115. Mastroeni P, Clare S, Khan S, Harrison JA, Hormaeche CE, Okamura H 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.