The Vi-capsule prevents Toll-like receptor 4 recognition of Salmonella

Cellular Microbiology

Volumn 10, Issue 4, 2008, Pages 876-890

  Wilson, R Paul ^a   Raffatellu, Manuela ^a   Chessa, Daniela ^a   Winter, Sebastian E ^a   Tükel, Çagla ^a   Bäumler, Andreas J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; BACTERIAL DNA; BACTERIUM LIPOPOLYSACCHARIDE; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 6; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VI CAPSULAR ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL PERITONITIS; BIOSYNTHESIS; BONE MARROW CELL; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME INHIBITION; FEMALE; GENE LOCUS; HOST PATHOGEN INTERACTION; IN VITRO STUDY; IN VIVO STUDY; LIVER; MACROPHAGE; MOLECULAR CLONING; MOLECULAR RECOGNITION; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; SALMONELLA ENTERICA; SALMONELLOSIS; SEPSIS; WILD TYPE;

ANIMALS; BACTERIAL CAPSULES; CELL LINE; FEMALE; INTERLEUKIN-6; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MICROSCOPY, IMMUNOELECTRON; NITRIC OXIDE SYNTHASE; SALMONELLA TYPHI; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA;

MURINAE; MUS; SALMONELLA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHI; SALMONELLA TYPHIMURIUM;

EID: 40749136669     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2007.01090.x     Document Type: Article

References (72)

1. Agace, W., Hedges, S., and Svanborg, C. (1992) Lps genotype in the C57 black mouse background and its influence on the interleukin-6 response to E. coli urinary tract infection. Scand J Immunol 35: 531-538.
2. Alvarado, T. (1983) Faecal leucocytes in patients with infectious diarrhoea. Trans R Soc Trop Med Hyg 77: 316-320.
3. Beutler, B., and Kruys, V. (1995) Lipopolysaccharide signal transduction, regulation of tumor necrosis factor biosynthesis, and signaling by tumor necrosis factor itself. J Cardiovasc Pharmacol 25 (Suppl. 2): S1-S8.
4. Beutler, B., Milsark, I.W., and Cerami, A.C. (1985) Passive immunization against cachectin/tumor necrosis factor protects mice from lethal effect of endotoxin. Science 229: 869-871.
5. Bueno, S.M., Santiviago, C.A., Murillo, A.A., Fuentes, J.A., Trombert, A.N., Rodas, P.I., et al. (2004) Precise excision of the large pathogenicity island, SPI7, in Salmonella enterica serovar Typhi. J Bacteriol 186: 3202-3213.
6. Butler, T., Bell, W.R., Levin, J., Linh, N.N., and Arnold, K. (1978) Typhoid fever. Studies of blood coagulation, bacteremia, and endotoxemia. Arch Intern Med 138: 407-410.
7. Butler, T., Ho, M., Acharya, G., Tiwari, M., and Gallati, H. (1993) Interleukin-6, gamma interferon, and tumor necrosis factor receptors in typhoid fever related to outcome of antimicrobial therapy. Antimicrob Agents Chemother 37: 2418-2421.
8. Cao, Y., Wen, Z., and Lu, D. (1992) Construction of a recombinant oral vaccine against Salmonella typhi and Salmonella typhimurium. Infect Immun 60: 2823-2827.
9. Chen, L.M., Kaniga, K., and Galan, J.E. (1996) Salmonella spp are cytotoxic for cultured macrophages. Mol Microbiol 21: 1101-1115.
10. Collins, F.M., and Carter, P.B. (1978) Growth of salmonellae in orally infected germfree mice. Infect Immun 21: 41-47.
11. Cookson, B.T., and Brennan, M.A. (2001) Pro-inflammatory programmed cell death. Trends Microbiol 9: 113-114.
12. Cummings, L.A., Wilkerson, W.D., Bergsbaken, T., and Cookson, B.T. (2006) In vivo, fliC expression by Salmonella enterica serovar Typhimurium is heterogeneous, regulated by ClpX, and anatomically restricted. Mol Microbiol 61: 795-809.
13. Cunha, F.Q., Assreuy, J., Moss, D.W., Rees, D., Leal, L.M., Moncada, S., et al. (1994) Differential induction of nitric oxide synthase in various organs of the mouse during endotoxaemia: Role of TNF-alpha and IL-1-beta. Immunology 81: 211-215.
14. Daniels, E.M., Schneerson, R., Egan, W.M., Szu, S.C., and Robbins, J.B. (1989) Characterization of the Salmonella paratyphi C Vi polysaccharide. Infect Immun 57: 3159-3164.
15. Day, D.W., Mandal, B.K., and Morson, B.C. (1978) The rectal biopsy appearances in Salmonella colitis. Histopathology 2: 117-131.
16. Dharmana, E., Keuter, M., Netea, M.G., Verschueren, I.C., and Kullberg, B.J. (2002) Divergent effects of tumor necrosis factor-alpha and lymphotoxin-alpha on lethal endotoxemia and infection with live Salmonella typhimurium in mice. Eur Cytokine Netw 13: 104-109.
17. Dziarski, R., and Gupta, D. (2000) Role of MD-2 in TLR2- and TLR4-mediated recognition of Gram-negative and Gram-positive bacteria and activation of chemokine genes. J Endotoxin Res 6: 401-405.
18. Engelberts, I., von Asmuth, E.J., van der Linden, C.J., and Buurman, W.A. (1991) The interrelation between TNF, IL-6, and PAF secretion induced by LPS in an in vivo and in vitro murine model. Lymphokine Cytokine Res 10: 127-131.
19. Felix, A., Bhatnagar, S.S., and Pitt, R.M. (1934) Observations on the properties of the Vi antigen of B.typhosus. Br J Exp Pathol 15: 346-354.
20. Felix, A., and Pitt, R.M. (1934) A new antigen of B.typhosus. Lancet 227: 186-191.
21. Gewirtz, A.T., Navas, T.A., Lyons, S., Godowski, P.J., and Madara, J.L. (2001) Cutting edge: Bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol 167: 1882-1885.
22. Girardin, E., Grau, G.E., Dayer, J.M., Roux-Lombard, P., and Lambert, P.H. (1988) Tumor necrosis factor and interleukin-1 in the serum of children with severe infectious purpura. N Engl J Med 319: 397-400.
23. Gordon, M.A., Walsh, A.L., Chaponda, M., Soko, D., Mbvwinji, M., Molyneux, M.E., and Gordon, S.B. (2001) Bacteraemia and mortality among adult medical admissions in Malawi -predominance of non-typhi salmonellae and Streptococcus pneumoniae. J Infect 42: 44-49.
24. Gordon, M.A., Banda, H.T., Gondwe, M., Gordon, S.B., Boeree, M.J., Walsh, A.L., et al. (2002) Non-typhoidal Salmonella bacteraemia among HIV-infected Malawian adults: High mortality and frequent recrudescence. Aids 16: 1633-1641.
25. Guilloteau, L.A., Wallis, T.S., Gautier, A.V., Macintyre, S., Platt, D.J., and Lax, A.J. (1996) The Salmonella virulence plasmid enhances Salmonella -induced lysis of macrophages and influences inflammatory responses. Infect Immun 64: 3385-3393.
26. Guyot, J., Gonvers, J.J., Pyndiah, N., and Heitz, M. (1984) [Value of fecal leukocyte studies in cases of acute diarrhea]. Schweiz Med Wochenschr 114: 634-636.
27. Harris, J.C., Dupont, H.L., and Hornick, R.B. (1972) Fecal leukocytes in diarrheal illness. Ann Intern Med 76: 697-703.
28. Hayashi, F., Smith, K.D., Ozinsky, A., Hawn, T.R., Yi, E.C., Goodlett, D.R., et al. (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410: 1099-1103.
29. Heyns, K., and Kiessling, G. (1967) Strukturaufklarung des Vi-antigens aus Citrobacter freundii (E. coli) 5396/38. Carbohydr Res 3: 340-353.
30. Hirose, K., Ezaki, T., Miyake, M., Li, T., Khan, A.Q., Kawamura, Y., et al. (1997) Survival of Vi-capsulated and Vi-deleted Salmonella typhi strains in cultured macrophage expressing different levels of CD14 antigen. FEMS Microbiol Lett 147: 259-265.
31. Humphries, A.D., Raffatellu, M., Winter, S., Weening, E.H., Kingsley, R.A., Droleskey, R., et al. (2003) The use of flow cytometry to detect expression of subunits encoded by 11 Salmonella enterica serotype Typhimurium fimbrial operons. Mol Microbiol 48: 1357-1376.
32. Jiang, Q., Akashi, S., Miyake, K., and Petty, H.R. (2000) Lipopolysaccharide induces physical proximity between CD14 and toll-like receptor 4 (TLR4) prior to nuclear translocation of NF-kappa B. J Immunol 165: 3541-3544.
33. Jones, B.D., Nichols, W.A., Gibson, B.W., Sunshine, M.G., and Apicella, M.A. (1997) Study of the role of the htrB gene in Salmonella typhimurium virulence. Infect Immun 65: 4778-4783.
34. Kankwatira, A.M., Mwafulirwa, G.A., and Gordon, M.A. (2004) Non-typhoidal Salmonella bacteraemia -an under-recognized feature of AIDS in African adults. Trop Doct 34: 198-200.
35. Keuter, M., Dharmana, E., Gasem, M.H., van der Ven-Jongekrijg, J., Djokomoeljanto, R., Dolmans, W.M., et al. (1994) Patterns of proinflammatory cytokines and inhibitors during typhoid fever. J Infect Dis 169: 1306-1311.
36. Khan, S.A., Everest, P., Servos, S., Foxwell, N., Zahringer, U., Brade, H., et al. (1998) A lethal role for lipid A in Salmonella infections. Mol Microbiol 29: 571-579.
37. Kocabas, C., Katsenelson, N., Kanswal, S., Kennedy, M.N., Cui, X., Blake, M.S., et al. (2007) Neisseria meningitidis type C capsular polysaccharide inhibits lipooligosaccharide-induced cell activation by binding to CD14. Cell Microbiol 9: 1297-1310.
38. Kraus, M.D., Amatya, B., and Kimula, Y. (1999) Histopathology of typhoid enteritis: Morphologic and immunophenotypic findings. Mod Pathol 12: 949-955.
39. Lindgren, S.W., Stojiljkovic, I., and Heffron, F. (1996) Macrophage killing is an essential virulence mechanism of Salmonella typhimurium. Proc Natl Acad Sci USA 93: 4197-4201.
40. McClelland, M., Sanderson, K.E., Spieth, J., Clifton, S.W., Latreille, P., Courtney, L., et al. (2001) Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413: 852-856.
41. McGovern, V.J., and Slavutin, L.J. (1979) Pathology of Salmonella colitis. Am J Surg Pathol 3: 483-490.
42. Means, T.K., Hayashi, F., Smith, K.D., Aderem, A., and Luster, A.D. (2003) The Toll-like receptor 5 stimulus bacterial flagellin induces maturation and chemokine production in human dendritic cells. J Immunol 170: 5165-5175.
43. Medzhitov, R., Preston-Hurlburt, P., and Janeway, C.A. Jr (1997) A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 388: 394-397.
44. Monack, D.M., Raupach, B., Hromockyj, A.E., and Falkow, S. (1996) Salmonella typhimurium invasion induces apoptosis in infected macrophages. Proc Natl Acad Sci USA 93: 9833-9838.
45. Mukawi, T.J. (1978) Histopathological study of typhoid perforation of the small intestines. Southeast Asian J Trop Med Public Health 9: 252-255.
46. Murray, S.R., Bermudes, D., de Felipe, K.S., and Low, K.B. (2001) Extragenic suppressors of growth defects in msbB Salmonella. J Bacteriol 183: 5554-5561.
47. Nair, S., Alokam, S., Kothapalli, S., Porwollik, S., Proctor, E., Choy, C., et al. (2004) Salmonella enterica serovar Typhi strains from which SPI7, a 134-kilobase island with genes for Vi exopolysaccharide and other functions, has been deleted. J Bacteriol 186: 3214-3223.
48. Nguyen, Q.C., Everest, P., Tran, T.K., House, D., Murch, S., Parry, C., et al. (2004) A clinical, microbiological, and pathological study of intestinal perforation associated with typhoid fever. Clin Infect Dis 39: 61-67.
49. Parkhill, J., Dougan, G., James, K.D., Thomson, N.R., Pickard, D., Wain, J., et al. (2001) Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 413: 848-852.
50. Raffatellu, M., Chessa, D., Wilson, R.P., Dusold, R., Rubino, S., and Bäumler, A.J. (2005a) The Vi capsular antigen of Salmonella enterica serotype Typhi reduces Toll-like receptor-dependent interleukin-8 expression in the intestinal mucosa. Infect Immun 73: 3367-3374.
51. Raffatellu, M., Wilson, R.P., Chessa, D., Andrews-Polymenis, H., Tran, Q.T., Lawhon, S., et al. (2005b) SipA, SopA, SopB, SopD and SopE2 contribute to Salmonella enterica serotype Typhimurium invasion of epithelial cells. Infect Immun 73: 146-154.
52. Raffatellu, M., Sun, Y.H., Wilson, R.P., Tran, Q.T., Chessa, D., Andrews-Polymenis, H.L., et al. (2005c) Host restriction of Salmonella enterica serotype Typhi is not caused by functional alteration of SipA, SopB, or SopD. Infect Immun 73: 7817-7826.
53. Raffatellu, M., Chessa, D., Wilson, R.P., Tukel, C., Akcelik, M., and Bäumler, A.J. (2006) Capsule-mediated immune evasion: A new hypothesis explaining aspects of typhoid fever pathogenesis. Infect Immun 74: 19-27.
54. Raffatellu, M., Santos, R.L., Chessa, D., Wilson, R.P., Winter, S., Rossetti, C.A., et al. (2007) The Capsule encoding viaB locus reduces IL-17 expression and mucosal innate responses in the bovine intestinal mucosa during infection with Salmonella enterica serotype Typhi. Infect Immun 75: 4342-4350.
55. Robbins, J.D., and Robbins, J.B. (1984) Reexamination of the protective role of the capsular polysaccharide (Vi antigen) of Salmonella typhi. J Infect Dis 150: 436-449.
56. Rolan, H.G., and Tsolis, R.M. (2007) Mice lacking components of adaptive immunity show increased Brucella abortus virB mutant colonization. Infect Immun 75: 2965-2973.
57. Roux, C.M., Rolan, H.G., Santos, R.L., Beremand, P.D., Thomas, T.L., Adams, L.G., and Tsolis, R.M. (2007) Brucella requires a functional Type IV secretion system to elicit innate immune responses in mice. Cell Microbiol 9: 1851-1869.
58. Santos, R.L., Zhang, S., Tsolis, R.M., Kingsley, R.A., Adams, L.G., and Bäumler, A.J. (2001) Animal Models of Salmonella Infections: Enteritis vs. Typhoid Fever. Mircrob Infect 3: 1335-1344.
59. Schmitt, C.K., Ikeda, J.S., Darnell, S.C., Watson, P.R., Bispham, J., Wallis, T.S., et al. (2001) Absence of all components of the flagellar export and synthesis machinery differentially alters virulence of Salmonella enterica serovar Typhimurium in models of typhoid fever, survival in macrophages, tissue culture invasiveness, and calf enterocolitis. Infect Immun 69: 5619-5625.
60. Sharma, A., and Qadri, A. (2004) 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 101: 17492-17497.
61. Somerville, J.E. Jr, Cassiano, L., Bainbridge, B., Cunningham, M.D., and Darveau, R.P. (1996) A novel Escherichia coli lipid A mutant that produces an antiinflammatory lipopolysaccharide. J Clin Invest 97: 359-365.
62. Sprinz, H., Gangarosa, E.J., Williams, M., Hornick, R.B., and Woodward, T.E. (1966) Histopathology of the upper small intestines in typhoid fever. Biopsy study of experimental disease in man. Am J Dig Dis 11: 615-624.
63. Stojiljkovic, I., Bäumler, A.J., and Heffron, F. (1995) Ethanolamine utilization in Salmonella typhimurium: Nucleotide sequence, protein expression and mutational analysis of the cchA cchB eutE eutJ eutG eutH gene cluster. J Bacteriol 177: 1357-1366.
64. Tsolis, R.M., Adams, L.G., Ficht, T.A., and Bäumler, A.J. (1999) Contribution of Salmonella typhimurium virulence factors to diarrheal disease in calves. Infect Immun 67: 4879-4885.
65. Virlogeux, I., Waxin, H., Ecobichon, C., and Popoff, M.Y. (1995) Role of the viaB locus in synthesis, transport and expression of Salmonella typhi Vi antigen. Microbiology 141: 3039-3047.
66. Waage, A., Brandtzaeg, P., Halstensen, A., Kierulf, P., and Espevik, T. (1989) The complex pattern of cytokines in serum from patients with meningococcal septic shock. Association between interleukin 6, interleukin 1, and fatal outcome. J Exp Med 169: 333-338.
67. Wang, R.F., and Kushner, S.R. (1991) Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100: 195-199.
68. Winter, S.E., Raffatellu, M., Wilson, R.P., Rüssmann, H., and Bäumler, A.J. (2007) The Salmonella enterica serotype Typhi regulator TviA reduces IL-8 production in intestinal epithelial cells by repressing flagellin secretion. Cellular Microbiology 10: 247-261.
69. Wortel, C.H., von der Mohlen, M.A., van Deventer, S.J., Sprung, C.L., Jastremski, M., Lubbers, M.J., et al. (1992) Effectiveness of a human monoclonal anti-endotoxin antibody (HA-1A) in Gram-negative sepsis: relationship to endotoxin and cytokine levels. J Infect Dis 166: 1367-1374.
70. Zhang, S., Adams, L.G., Nunes, J., Khare, S., Tsolis, R.M., and Bäumler, A.J. (2003) Secreted effector proteins of Salmonella enterica serotype typhimurium elicit host-specific chemokine profiles in animal models of typhoid fever and enterocolitis. Infect Immun 71: 4795-4803.
71. Zhang, S., Santos, R.L., Tsolis, R.M., Mirold, S., Hardt, W.-D., Adams, L.G., and Bäumler, A.J. (2002b) Phage mediated horizontal transfer of the sopE1 gene increases enteropathogenicity of Salmonella enterica serotype Typhimurium for calves. FEMS Microbiol Lett 217: 243-247.
72. Zhang, S., Santos, R.L., Tsolis, R.M., Stender, S., Hardt, W.-D., Bäumler, A.J., and Adams, L.G. (2002a) SipA, SopA, SopB, SopD and SopE2 act in concert to induce diarrhea in calves infected with Salmonella enterica serotype Typhimurium. Infect Immun 70: 3843-3855.