Virulent Salmonella enterica infections can be exacerbated by concomitant infection of the host with a live attenuated S. enterica vaccine via Toll-like receptor 4-dependent interleukin-10 production with the involvement of both TRIF and MyD88

Immunology

Volumn 124, Issue 4, 2008, Pages 469-479

  Foster, Gemma L ^a   Barr, Tom A ^b   Grant, Andrew J ^a   McKinley, Trevelyan J ^a   Bryant, Clare E ^a   MacDonald, Andrew ^b   Gray, David ^b   Yamamoto, Masahiro ^c   Akira, Shizuo ^c   Maskell, Duncan J ^a   Mastroeni, Pietro ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c OSAKA UNIVERSITY   (Japan)

Author keywords

Exacerbation; Immunity; Infection; Interleukin 10; Myeloid differentiation factor 88; Salmonella; Toll like receptor 4; Toll interleukin 1 receptor domain containing adaptor inducing interferon

Indexed keywords

BETA INTERFERON; INTERLEUKIN 10; LIVE VACCINE; MYELOID DIFFERENTIATION FACTOR 88; SALMONELLOSIS VACCINE; TOLL INTERLEUKIN 1 RECEPTOR DOMAIN CONTAINING ADAPTOR INDUCING INTERFERON BETA; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL COUNT; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE EXACERBATION; DISEASE SEVERITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; SEROTYPE; WILD TYPE;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; INTERLEUKIN-10; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MYELOID DIFFERENTIATION FACTOR 88; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; SALMONELLA VACCINES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4; VACCINES, ATTENUATED; VIRULENCE;

EID: 46949100416     PISSN: 00192805     EISSN: 13652567     Source Type: Journal    
DOI: 10.1111/j.1365-2567.2007.02798.x     Document Type: Article

References (62)

1. Crump JA, Luby SP, Mintz ED. The global burden of typhoid fever. Bull World Health Organ 2004 82 : 346 53.
2. Bachou H, Tylleskar T, Kaddu-Mulindwa DH, Tumwine JK. Bacteraemia among severely malnourished children infected and uninfected with the human immunodeficiency virus-1 in Kampala, Uganda. BMC Infect Dis 2006 6 : 160.
3. Enwere G, Biney E, Cheung YB et al. Epidemiologic and clinical characteristics of community-acquired invasive bacterial infections in children aged 2-29 months in The Gambia. Pediatr Infect Dis J 2006 25 : 700 5.
4. Gilks CF, Brindle RJ, Otieno LS et al. Life-threatening bacteraemia in HIV-1 seropositive adults admitted to hospital in Nairobi, Kenya. Lancet 1990 336 : 545 9.
5. Gordon MA, Banda HT, Gondwe M et al. Non-typhoidal Salmonella bacteraemia among HIV-infected Malawian adults: high mortality and frequent recrudescence. Aids 2002 16 : 1633 41.
6. Graham SM, Hart CA, Molyneux EM, Walsh AL, Molyneux ME. Malaria and Salmonella infections: cause or coincidence? Trans R Soc Trop Med Hyg 2000 94 : 227.
7. Graham SM, Molyneux EM, Walsh AL, Cheesbrough JS, Molyneux ME, Hart CA. Nontyphoidal Salmonella infections of children in tropical Africa. Pediatr Infect Dis J 2000 19 : 1189 96.
8. Graham SM, Walsh AL, Molyneux EM, Phiri AJ, Molyneux ME. Clinical presentation of non-typhoidal Salmonella bacteraemia in Malawian children. Trans R Soc Trop Med Hyg 2000 94 : 310 4.
9. Hohmann EL. Nontyphoidal salmonellosis. Clin Infect Dis 2001 32 : 263 9.
10. Kankwatira AM, Mwafulirwa GA, Gordon MA. Non-typhoidal Salmonella bacteraemia - an under-recognized feature of AIDS in African adults. Trop Doct 2004 34 : 198 200.
11. Mastroeni P, Ugrinovic S, Chandra A, MacLennan C, Doffinger R, Kumararatne D. Resistance and susceptibility to Salmonella infections: lessons from mice and patients with immunodeficiencies. Rev Med Microbiol 2003 14 : 53 62.
12. Mulholland EK, Adegbola RA. Bacterial infections - a major cause of death among children in Africa. N Engl J Med 2005 352 : 75 7.
13. Walsh AL, Phiri AJ, Graham SM, Molyneux EM, Molyneux ME. Bacteremia in febrile Malawian children: clinical and microbiologic features. Pediatr Infect Dis J 2000 19 : 312 8.
14. Levine MM, Ferreccio C, Black RE, Tacket CO, Germanier R. Progress in vaccines against typhoid fever. Rev Infect Dis 1989 11 (Suppl 3 S552 67.
15. Kirkpatrick BD, McKenzie R, O'Neill JP et al. Evaluation of Salmonella enterica serovar Typhi (Ty2 aroC-ssaV-) M01ZH09, with a defined mutation in the Salmonella pathogenicity island 2, as a live, oral typhoid vaccine in human volunteers. Vaccine 2006 24 : 116 23.
16. Biozzi G, Howard JG, Halpern BN, Stiffel C, Mouton D. The kinetics of blood clearance of isotopically labelled Salmonella enteritidis by the reticulo-endothelial system in mice. Immunology 1960 3 : 74 89.
17. Dunlap NE, Benjamin WH, McCall RD, Tilden AB, Briles DE. A 'safe-site' for Salmonella typhimurium is within splenic cells during the early phase of infection in mice. Microb Pathog 1991 10 : 297 310.
18. Salcedo SP, Noursadeghi M, Cohen J, Holden DW. Intracellular replication of Salmonella typhimurium strains in specific subsets of splenic macrophages in vivo. Cell Microbiol 2001 3 : 587 97.
19. 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 80.
20. 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.
21. 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 64.
22. Hess J, Ladel C, Miko D, Kaufmann SH. 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 6.
23. Hirose K, Nishimura H, Matsuguchi T, Yoshikai Y. Endogenous IL-15 might be responsible for early protection by natural killer cells against infection with an avirulent strain of Salmonella choleraesuis in mice. J Leukoc Biol 1999 66 : 382 90.
24. Kincy-Cain T, Clements JD, Bost KL. Endogenous and exogenous interleukin-12 augment the protective immune response in mice orally challenged with Salmonella dublin. Infect Immun 1996 64 : 1437 40.
25. Mastroeni P, Clare S, Khan S, Harrison JA, Hormaeche CE, Okamura H, Kurimoto M, Dougan G. Interleukin 18 contributes to host resistance and gamma interferon production in mice infected with virulent Salmonella typhimurium. Infect Immun 1999 67 : 478 83.
26. 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 96.
27. Mastroeni P, Harrison JA, Robinson JH, Clare S, Khan S, Maskell DJ, Dougan G, Hormaeche CE. 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 76.
28. Mastroeni P, Skepper JN, Hormaeche CE. Effect of anti-tumor necrosis factor alpha antibodies on histopathology of primary Salmonella infections. Infect Immun 1995 63 : 3674 82.
29. Mastroeni P, Villarreal B, Demarco de Hormaeche R, Hormaeche CE. Serum TNF alpha inhibitor in mouse typhoid. Microb Pathog 1992 12 : 343 9.
30. 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 80.
31. Muotiala A, Makela PH. Role of gamma interferon in late stages of murine salmonellosis. Infect Immun 1993 61 : 4248 53.
32. 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 4.
33. Tite JP, Dougan G, Chatfield SN. The involvement of tumor necrosis factor in immunity to Salmonella infection. J Immunol 1991 147 : 3161 4.
34. Sheppard M, Webb C, Heath F, Mallows V, Emilianus R, Maskell D, Mastroeni P. Dynamics of bacterial growth and distribution within the liver during Salmonella infection. Cell Microbiol 2003 5 : 593 600.
35. Brown SP, Cornell SJ, Sheppard M, Grant AJ, Maskell DJ, Grenfell BT, Mastroeni P. Intracellular demography and the dynamics of Salmonella enterica infections. PLoS Biol 2006 4 : e349.
36. Maskell DJ, Hormaeche CE, Harrington KA, Joysey HS, Liew FY. The initial suppression of bacterial growth in a Salmonella infection is mediated by a localized rather than a systemic response. Microb Pathog 1987 2 : 295 305.
37. Mastroeni P, Arena A, Costa GB, Liberto MC, Bonina L, Hormaeche CE. Serum TNF alpha in mouse typhoid and enhancement of a Salmonella infection by anti-TNF alpha antibodies. Microb Pathog 1991 11 : 33 8.
38. Muotiala A, Makela PH. The role of IFN-gamma in murine Salmonella typhimurium infection. Microb Pathog 1990 8 : 135 41.
39. Hormaeche CE. Dead salmonellae or their endotoxin accelerate the early course of a Salmonella infection in mice. Microb Pathog 1990 9 : 213 8.
40. Wilson GS. The Hazards of Immunization. London : Athlone press, 1967 : 265 80.
41. Hoshino K, Takeuchi O, Kawai T, Sanjo H, Ogawa T, Takeda Y, Takeda K, Akira S. Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the lps gene product. J Immunol 1999 162 : 3749 52.
42. Yamamoto M, Sato S, Hemmi H et al. Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 2003 301 : 640 3.
43. Adachi O, Kawai T, Takeda K, Matsumoto M, Tsutsui H, Sakagami M, Nakanishi K, Akira S. Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 1998 9 : 143 50.
44. Kuhn R, Lohler J, Rennick D, Rajewsky K, Muller W. Interleukin-10- deficient mice develop chronic enterocolitis. Cell 1993 75 : 263 74.
45. Hormaeche CE. Natural resistance to Salmonella typhimurium in different inbred mouse strains. Immunology 1979 37 : 311 8.
46. Hoiseth SK, Stocker BA. Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 1981 291 : 238 9.
47. Canty A. Bootstrap R (S- Plus) Functions. R package version 2007 1.2-28. (R port, Ripley B). Vienna : R Development core team. http://www.R-project.org (accessed 22 January 2008).
48. Boonstra A, Rajsbaum R, Holman M et al. Macrophages and myeloid dendritic cells, but not plasmacytoid dendritic cells, produce IL-10 in response to MyD88- and TRIF-dependent TLR signals, and TLR-independent signals. J Immunol 2006 177 : 7551 8.
49. Dunne A, O'Neill LA. Adaptor usage and Toll-like receptor signaling specificity. FEBS Lett 2005 579 : 3330 5.
50. Anthony Jones E, Summerfield JA. The Liver: Pathobiology, 2nd edn. New York : Raven Press, 1988 : 683 704.
51. van Furth R, Diesselhoff-den Dulk MM. Dual origin of mouse spleen macrophages. J Exp Med 1984 160 : 1273 83.
52. Gonnella PA, Starr S, Rodrick ML, Wilmore DW. Induced hyporesponsiveness in rat Kupffer cells is not specific for lipopolysaccharide. Immunology 1994 81 : 402 6.
53. Fiorentino DF, Zlotnik A, Mosmann TR, Howard M, O'Garra A. IL-10 inhibits cytokine production by activated macrophages. J Immunol 1991 147 : 3815 22.
54. Gazzinelli RT, Oswald IP, James SL, Sher A. IL-10 inhibits parasite killing and nitrogen oxide production by IFN-gamma-activated macrophages. J Immunol 1992 148 : 1792 6.
55. Laichalk LL, Danforth JM, Standiford TJ. Interleukin-10 inhibits neutrophil phagocytic and bactericidal activity. FEMS Immunol Med Microbiol 1996 15 : 181 7.
56. Bogdan C, Vodovotz Y, Nathan C. Macrophage deactivation by interleukin 10. J Exp Med 1991 174 : 1549 55.
57. Arai T, Hiromatsu K, Nishimura H, Kimura Y, Kobayashi N, Ishida H, Nimura Y, Yoshikai Y. Effects of in vivo administration of anti-IL-10 monoclonal antibody on the host defence mechanism against murine Salmonella infection. Immunology 1995 85 : 381 8.
58. Benjamin WH, Hall P Jr., Roberts SJ, Briles DE. The primary effect of the Ity locus is on the rate of growth of Salmonella typhimurium that are relatively protected from killing. J Immunol 1990 144 : 3143 51.
59. 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 9.
60. Lembo A, Kalis C, Kirschning CJ, Mitolo V, Jirillo E, Wagner H, Galanos C, Freudenberg MA. Differential contribution of Toll-like receptors 4 and 2 to the cytokine response to Salmonella enterica serovar Typhimurium and Staphylococcus aureus in mice. Infect Immun 2003 71 : 6058 62.
61. Takeuchi O, Hoshino K, Kawai T, Sanjo H, Takada H, Ogawa T, Takeda K, Akira S. Differential roles of TLR2 and TLR4 in recognition of Gram-negative and Gram-positive bacterial cell wall components. Immunity 1999 11 : 443 51.
62. Chang EY, Guo B, Doyle SE, Cheng G. Cutting edge: involvement of the type I IFN production and signaling pathway in lipopolysaccharide-induced IL-10 production. J Immunol 2007 178 : 6705 9.