Toll-like receptor 4-mediated innate IL-10 activates antigen-specific regulatory T cells and confers resistance to Bordetella pertussis by inhibiting inflammatory pathology

Journal of Immunology

Volumn 171, Issue 6, 2003, Pages 3119-3127

  Higgins, Sarah C ^a   Lavelle, Ed C ^a   McCann, Chantelle ^a   Keogh, Brian ^a   McNeela, Edel ^a   Byrne, Patricia ^a   O'Gorman, Brian ^a   Jarnicki, Andrew ^a   McGuirk, Peter ^a   Mills, Kingston H G ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CHEMOKINE; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; TOLL LIKE RECEPTOR 4;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ANTIGEN SPECIFICITY; ARTICLE; BORDETELLA PERTUSSIS; CELL INFILTRATION; CELL MATURATION; CONTROLLED STUDY; DENDRITIC CELL; INFECTION RESISTANCE; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TH1 CELL;

EID: 0042333419     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.171.6.3119     Document Type: Article

References (37)

1. Underhill, D. M., and A. Ozinsky. 2002. Toll-like receptors: key mediators of microbe detection. Curr. Opin. Immunol. 14:103.
2. Poltorak, A., X. He, I. Smirnova, M. Y. Liu, C. V. Huffel, X. Du, D. Birdwell, E. Alejos, M. Silva, C. Galanos, et al. 1998. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282:2085.
3. Pulendran, B., P. Kumar, C. W. Cutler, M. Mohamadzadeh, T. Van Dyke, and J. Banchereau. 2001. Lipopolysaccharides from distinct pathogens induce different classes of immune responses in vivo. J. Immunol. 167:5067.
4. Werts, C., R. I. Tapping, J. C. Mathison, T. H. Chuang, V. Kravchenko, I. Saint Girons, D. A. Haake, P. J. Godowski, F. Hayashi, A. Ozinsky, et al. 2001. Leptospiral lipopolysaccharide activates cells through a TLR2-dependent mechanism. Nat. Immun. 2:346.
5. Akashi, S., R. Shimazu, H. Ogata, Y. Nagai, K. Takeda, M. Kimoto, and K. Miyake. 2000. Cutting edge: cell surface expression and lipopolysaccharide signaling via the Toll-like receptor 4-MD-2 complex on mouse peritoneal macrophages. J. Immunol. 164:3471.
6. Zhang, F. X., C. J. Kirschning, R. Mancinelli, X. P. Xu, Y. Jin, E. Faure, A. Mantovani, M. Rothe, M. Muzio, and M. Arditi. 1999. Bacterial lipopolysaccharide activates nuclear factor-κB through interleukin-1 signaling mediators in cultured human dermal endothelial cells and mononuclear phagocytes. J. Biol. Chem. 274:7611.
7. Hemmi, H., O. Takeuchi, T. Kawai, T. Kaisho, S. Sato, H. Sanjo, M. Matsumoto, K. Hoshino, H. Wagner, K. Takeda, and S. Akira. 2000. A Toll-like receptor recognizes bacterial DNA. Nature 408:740.
8. Hayashi, F., K. D. Smith, A. Ozinsky, T. R. Hawn, E. C. Yi, D. R. Goodlett, J. K. Eng, S. Akira, D. M. Underhill, and A. Aderem. 2001. The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410:1099.
9. Alexopoulou, L., A. C. Holt, R. Medzhitov, and R. A. Flavell. 2001. Recognition of double-stranded RNA and activation of NF-κB by Toll-like receptor 3. Nature 413:732.
10. d'Ostiani, C. F., G. Del Sero, A. Bacci, C. Montagnoli, A. Spreca, A. Mencacci, P. Ricciardi-Castagnoli, and L. Romani. 2000. Dendritic cells discriminate between yeasts and hyphae of the fungus Candida albicans: implications for initiation of T helper cell immunity in vitro and in vivo. J. Exp. Med. 191:1661.
11. Whelan, M., M. M. Harnett, K. M. Houston, V. Patel, W. Harnett, and K. P. Rigley. 2000. A filarial nematode-secreted product signals dendritic cells to acquire a phenotype that drives development of Th2 cells. J. Immunol. 164:6453.
12. Gagliardi, M. C., F. Sallusto, M. Marinaro, A. Langenkamp, A. Lanzavecchia, and M. T. De Magistris. 2000. Cholera toxin induces maturation of human dendritic cells and licenses them for Th2 priming. Eur. J. Immunol. 30:2394.
13. McGuirk, P., and K. H. G. Mills. 2000. Direct anti-inflammatory effect of a bacterial virulence factor: IL-10-dependent suppression of IL-12 production by filamentous hemagglutinin from Bordetella pertussis. Eur. J. Immunol. 30:415.
14. McGuirk, P., C. McCann, and K. H. G. Mills. 2002. Pathogen-specific T regulatory 1 cells induced in the respiratory tract by a bacterial molecule that stimulates interleukin 10 production by dendritic cells: a novel strategy for evasion of protective T helper type 1 responses by Bordetella pertussis. J. Exp. Med. 195:221.
15. Mills, K. H. G., A. Barnard, J. Watkins, and K. Redhead. 1993. Cell-mediated immunity to Bordetella pertussis: role of Th1 cells in bacterial clearance in a murine respiratory infection model. Infect. Immun. 61:399.
16. Ryan, M., G. Murphy, L. Gothefors, L. Nilsson, J. Storsaeter, and K. H. G. Mills. 1997. Bordetella pertussis respiratory infection in children is associated with preferential activation of type 1 T helper cells. J. Infect. Dis. 175:1246.
17. Mahon, B. P., B. J. Sheahan, F. Griffin, G. Murphy, and K. H. G. Mills. 1997. Atypical disease after Bordetella pertussis respiratory infection of mice with targeted disruptions of interferon-γ receptor or immunoglobulin μ chain genes. J. Exp. Med. 186:1843.
18. Harvill, E. T., P. A. Cotter, and J. F. Miller. 1999. Pregenomic comparative analysis between Bordetella bronchiseptica RB50 and Bordetella pertussis tohama I in murine models of respiratory tract infection. Infect. Immun. 67:6109.
19. McGuirk, P., B. P. Mahon, F. Griffin, and K. H. G. Mills. 1998. Compartmentalization of T cell responses following respiratory infection with Bordetella pertussis: hyporesponsiveness of lung T cells is associated with modulated expression of the co-stimulatory molecule CD28. Eur. J. Immunol. 28:153.
20. Mills, K. H. G. 1999. Murine T cell culture. In Lymphocytes: A Practical Approach. S. Rowland Jones and A. McMichael, eds. IRL Press, Oxford, p. 95.
21. Kurt-Jones, E. A., L. Popova, L. Kwinn, L. M. Haynes, L. P. Jones, R. A. Tripp, E. E. Walsh, M. W. Freeman, D. T. Golenbock, L. I. Anderson, and R. W. Finberg. 2000. Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat. Immun. 1:398.
22. Wang, X., C. Moser, J. P. Louboutin, E. S. Lysenko, D. J. Weiner, J. N. Weiser, and J. M. Wilson. 2002. Toll-like receptor 4 mediates innate immune responses to Haemophilus influenzae infection in mouse lung. J. Immunol. 168:810.
23. Abel, B., N. Thieblemont, V. J. Quesniaux, N. Brown, J. Mpagi, K. Miyake, F. Bihl, and B. Ryffel. 2002. Toll-like receptor 4 expression is required to control chronic Mycobacterium tuberculosis infection in mice. J. Immunol. 169:3155.
24. Rescigno, M., M. Urbano, M. Rimoldi, B. Valzasina, G. Rotta, F. Granucci, and P. Ricciardi-Castagnoli. 2002. Toll-like receptor 4 is not required for the full maturation of dendritic cells or for the degradation of Gram-negative bacteria. Eur. J. Immunol. 32:2800.
25. Standiford, T. J., S. L. Kunkel, M. J. Greenberger, L. L. Laichalk, and R. M. Strieter. 1996. Expression and regulation of chemokines in bacterial pneumonia. J. Leukocyte Biol. 59:24.
26. Mizgerd, J. P., M. R. Spieker, and C. M. Doerschuk. 2001. Early response cytokines and innate immunity: essential roles for TNF receptor 1 and type I IL-1 receptor during Escherichia coli pneumonia in mice. J. Immunol. 166:4042.
27. McGuirk, P., and K. H. G Mills. 2000. A regulatory role for interleukin 4 in differential inflammatory responses in the lung following infection of mice primed with Th1- or Th2-inducing pertussis vaccines. Infect. Immun. 68:1383.
28. Dabbagh, K., M. E. Dahl, P. Stepick-Biek, and D. B. Lewis. 2002. Toll-like receptor 4 is required for optimal development of Th2 immune responses: role of dendritic cells. J. Immunol. 168:4524.
29. Sing, A., D. Rost, N. Tvardovskaia, A. Roggenkamp, A. Wiedemann, C. J. Kirschning, M. Aepfelbacher, and J. Heesemann. 2002. Yersinia V-antigen exploits Toll-like receptor 2 and CD14 for interleukin 10-mediated immunosuppression. J. Exp. Med. 196:1017.
30. Kopp, E., and R. Medzhitov. 2002. A plague on host defense. J. Exp. Med. 196:1009.
31. + T regulatory cells suppress Helicobacter hepaticus-induced colitis. J. Exp. Med. 196:505.
32. + T cell-mediated pulmonary hyperinflammation driven by Pneumocystis carinii in immunodeficient mice. Eur. J. Immunol. 32:1282.
33. Sing, A., A. Roggenkamp, A. M. Geiger, and J. Heesemann. 2002. Yersinia enterocolitica evasion of the host innate immune response by V antigen-induced IL-10 production of macrophages is abrogated in IL-10-deficient mice. J. Immunol. 68:1315.
34. Jacobs, M., N. Brown, N. Allie, R. Gulert, and B. Ryffel. 2000. Increased resistance to mycobacterial infection in the absence of interleukin-10. Immunology 100:494.
35. Deckert, M., S. Soltek, G. Geginat, S. Lutjen, M. Montesinos-Rongen, H. Hof, and D. Schluter. 2001. Endogenous interleukin-10 is required for prevention of a hyperinflammatory intracerebral immune response in Listeria monocytogenes meningoencephalitis. Infect. Immun. 69:4561.
36. Sewnath, M. E., D. P. Olszyna, R. Birjmohun, F. J. ten Kate, D. J. Gouma, and T. van Der Poll. 2001. IL-10-deficient mice demonstrate multiple organ failure and increased mortality during Escherichia coli peritonitis despite an accelerated bacterial clearance. J. Immunol. 166:6323.
37. Kullberg, M. C., A. G. Rothfuchs, D. Iankovic, P. Caspar, T. A. Wynn, P. L. Gorelick, A. W. Cheever, and A. Sher. 2001. Helicobacter hepaticus-induced colitis in interleukin-10-deficient mice: cytokine requirements for the induction and maintenance of intestinal inflammation. Infect. Immun. 69:4232.