IL-10 released by concomitant TLR2 stimulation blocks the induction of a subset of Th1 cytokines that are specifically induced by TLR4 or TLR3 in human dendritic cells

Journal of Immunology

Volumn 173, Issue 12, 2004, Pages 7548-7555

  Re, Fabio ^a,b   Strominger, Jack L ^a  

^a DANA FARBER CANCER INSTITUTE   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 15; MYELOID DIFFERENTIATION FACTOR 88; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 7;

ANTIGEN RECOGNITION; ARTICLE; AUTOCRINE EFFECT; CONTROLLED STUDY; CYTOKINE RELEASE; DENDRITIC CELL; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE INDUCTION; HUMAN; HUMAN CELL; MYCOBACTERIUM TUBERCULOSIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; RIBONUCLEASE PROTECTION ASSAY; TH1 CELL;

EID: 10344243503     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.173.12.7548     Document Type: Article

References (43)

1. + T cells. Annu. Rev. Immunol. 12:635.
2. Moser, M., and K. M. Murphy. 2000. Dendritic cell regulation of TH1-TH2 development. Nat. Immunol. 1:199.
3. Re, F., and J. L. Strominger. 2004. Heterogeneity of TLR induced responses in dendritic cells: from innate to adaptive immunity. Immunobiology 209:191.
4. Akira, S., and S. Sato. 2003. Toll-like receptors and their signaling mechanisms. Scand. J. Infect. Dis. 35:555.
5. Beutler, B., K. Hoebe, X. Du, and R. J. Ulevitch. 2003. How we detect microbes and respond to them: the Toll-like receptors and their transducers. J. Leukocyte Biol. 74:479.
6. Ozinsky, A., D. M. Underhill, J. D. Fontenot, A. M. Hajjar, K. D. Smith, C. B. Wilson, L. Schroeder, and A. Aderem. 2000. The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between Toll-like receptors. Proc. Natl. Acad. Sci. USA 97:13766.
7. Kawai, T., O. Adachi, T. Ogawa, K. Takeda, and S. Akira. 1999. Unresponsiveness of MyD88-deficient mice to endotoxin. Immunity 11:115.
8. Yamamoto, M., S. Sato, H. Hemmi, K. Hoshino, T. Kaisho, H. Sanjo, O. Takeuchi, M. Sugiyama, M. Okabe, K. Takeda, and S, Akira. 2003. Role of adaptor TRIF in the MyD88-independent Toll-like receptor signaling pathway. Science 301:640.
9. Oshiumi, H., M. Sasai, K. Shida, T. Fujita, M. Matsumoto, and T. Seya. 2003. TIR-containing adapter molecule (TICAM)-2, a bridging adapter recruiting to Toll-like receptor 4 TICAM-1 that induces interferon-β. J. Biol. Chem. 278:49751.
10. Fitzgerald, K. A., S. M. McWhirter, K. L. Faia, D. C. Rowe, E. Latz, D. T. Golenbock, A. J. Coyle, S. M. Liao, and T. Maniatis. 2003. IKKε and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 4:491.
11. Doyle, S., S. Vaidya, R. O'Connell, H. Dadgostar, P. Dempsey, T. Wu, G. Rao, R. Sun, M. Haberland, R. Modlin, and G. Cheng. 2002. IRF3 mediates a TLR3/ TLR4-specific antiviral gene program. Immunity 17:251.
12. Kawai, T., O. Takeuchi, T. Fujita, J. Inoue, P. F. Muhlradt, S. Sato, K. Hoshino, and S. Akira. 2001. Lipopolysaccharide stimulates the MyD88-independent pathway and results in activation of IFN-regulatory factor 3 and the expression of a subset of lipopolysaccharide-inducible genes. J. Immunol. 167:5887.
13. Hirschfeld, M., J. J. Weis, V. Toshchakov, C. A. Salkowski, M. J. Cody, D. C. Ward, N. Qureshi, S. M. Michalek, and S. N. Vogel. 2001. Signaling by Toll-like receptor 2 and 4 agonists results in differential gene expression in murine macrophages. Infect. Immun. 69:1477.
14. Re, F., and J. L. Strominger. 2001. Toll-like receptor 2 (TLR2) and TLR4 differentially activate human dendritic cells. J. Biol. Chem. 276:37692.
15. 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.
16. Redecke, V., H. Hacker, S. K. Datta, A. Fermin, P. M. Pitha, D. H. Broide, and E. Raz. 2004. Cutting edge: Activation of Toll-like receptor 2 induces a Th2 immune response and promotes experimental asthma. J. Immunol. 172:2739.
17. Agrawal, S., A. Agrawal, B. Doughty, A. Gerwitz, J. Blenis, T. Van Dyke, and B. Pulendran. 2003. Cutting edge: Different Toll-like receptor agonists instruct dendritic cells to induce distinct Th responses via differential modulation of extracellular signal-regulated kinase-mitogen-activated protein kinase and c-Fos. J. Immunol. 171:4984.
18. Jotwani, R., B. Pulendran, S. Agrawal, and C. W. Cutler. 2003. Human dendritic cells respond to Porphyromonas gingivalis LPS by promoting a Th2 effector response in vitro. Eur. J. Immunol. 33:2980.
19. Qi, H., T. L. Denning, and L. Soong. 2003. Differential induction of interleukin-10 and interleukin-12 in dendritic cells by microbial Toll-like receptor activators and skewing of T-cell cytokine profiles. Infect. Immun. 71:3337.
20. Hirschfeld, M., Y. Ma, J. H. Weis, S. N. Vogel, and J. J. Weis. 2000. Cutting edge: Repurification of lipopolysaccharide eliminates signaling through both human and murine Toll-like receptor 2. J. Immunol. 165:618.
21. Cognet, I., A. B. de Coignac, G. Magistrelli, P. Jeannin, J. P. Aubry, K. Maisnier-Patin, G. Caron, S. Chevalier, F. Humbert, T. Nguyen, et al. 2003. Expression of recombinant proteins in a lipid A mutant of Escherichia coli BL21 with a strongly reduced capacity to induce dendritic cell activation and maturation. J. Immunol. Methods 272:199.
22. Komai-Koma, M., L. Jones, G. S. Ogg, D. Xu, and F. Y. Liew. 2004. TLR2 is expressed on activated T cells as a costimulatory receptor. Proc. Natl. Acad. Sci. USA 101:3029.
23. Becker, I., N. Salaiza, M. Aguirre, J. Delgado, N. Carrillo-Carrasco, L. G. Kobeh, A. Ruiz, R. Cervantes, A. P. Torres, N. Cabrera, et al. 2003. Leishmania lipophosphoglycan (LPG) activates NK cells through Toll-like receptor-2. Mol. Biochem. Parasitol. 130:65.
24. Fiorentino, D. F., A. Zlotnik, T. R. Mosmann, M. Howard, and A. O'Garra. 1991. IL-10 inhibits cytokine production by activated macrophages. J. Immunol. 147:3815.
25. Kopydlowski, K. M., C. A. Salkowski, M. J. Cody, N. van Rooijen, J. Major, T. A. Hamilton, and S. N. Vogel. 1999. Regulation of macrophage chemokine expression by lipopolysaccharide in vitro and in vivo. J. Immunol. 163:1537.
26. D'Andrea, A., M. Aste-Amezaga, N. M. Valiante, X. Ma, M. Kubin, and G. Trinchieri. 1993. Interleukin 10 (IL-10) inhibits human lymphocyte interferon γ-production by suppressing natural killer cell stimulatory factor/TL-12 synthesis in accessory cells. J. Exp. Med. 178:1041.
27. Carson, W. E., M. E. Ross, R. A. Baiocchi, M. J. Marien, N. Boiani, K. Grabstein, and M. A. Caligiuri. 1995. Endogenous production of interleukin 15 by activated human monocytes is critical for optimal production of interferon-γ by natural killer cells in vitro. J. Clin. Invest. 96:2578.
28. Toshchakov, V., B. W. Jones, P. Y. Perera, K. Thomas, M. J. Cody, S. Zhang, B. R. Williams, J. Major, T. A. Hamilton, M. J. Fenton, and S. N. Vogel. 2002. TLR4, but not TLR2, mediates TFN-β-induced STAT1α/β- dependent gene expression in macrophages. Nat. Immunol. 3:392.
29. Ito, T., R. Amakawa, T. Kaisho, H. Hemmi, K. Tajima, K. Uehira, Y. Ozaki, H. Tomizawa, S. Akira, and S. Fukuhara. 2002. Interferon-α and interleukin-12 are induced differentially by Toll-like receptor 7 ligands in human blood dendritic cell subsets. J. Exp. Med. 193:1507.
30. O'Neill, L. A., K. A. Fitzgerald, and A. G. Bowie. 2003. The Toll-IL-1 receptor adaptor family grows to five members. Trends Immunol. 24:286.
31. Yamamoto, M., K. Takeda, and S. Akira. 2004. TIR domain-containing adaptors define the specificity of TLR signaling. Mol. Immunol. 40:861.
32. Fitzgerald, K. A., E. M. Palsson-McDermott, A. G. Bowie, C. A. Jefferies, A. S. Mansell, G. Brady, E. Brint, A. Dunne, P. Gray, M. T. Harte, et al. 2001. Mal (MyD88-adapter-like) is required for Toll-like receptor-4 signal transduction. Nature 413:78.
33. Horng, T., G. M. Barton, R. A. Flavell, and R. Medzhitov. 2002. The adaptor molecule TIRAP provides signalling specificity for Toll-like receptors. Nature 420:329.
34. Hoebe, K., X. Du, P. Georgel, E. Janssen, K. Tabeta, S. O. Kim, J. Goode, P. Lin, N. Mann, S. Mudd, et al. 2003. Identification of Lps2 as a key transducer of MyD88-independent TIR signalling. Nature 424:743.
35. Yamamoto, M., S. Sato, H. Hemmi, S. Uematsu, K. Hoshino, T. Kaisho, O. Takeuchi, K. Takeda, and S. Akira. 2003. TRAM is specifically involved in the Toll-like receptor 4-mediated MyD88-independent signaling pathway. Nat. Immunol. 4:1144.
36. Persing, D. H., R. N. Coler, M. J. Lacy, D. A. Johnson, J. R. Baldridge, R. M. Hershberg, and S. G. Reed. 2002. Taking toll: lipid A mimetics as adjuvants and immunomodulators. Trends Microbiol. 10:S32.
37. Fulton, S. A., S. M. Reba, R. K. Pai, M. Pennini, M. Torres, C. V. Harding, and W. H. Boom. 2004. Inhibition of major histocompatibility complex II expression and antigen processing in murine alveolar macrophages by Mycobacterium bovis BCG and the 19-kilodalton mycobacterial lipoprotein. Infect. Immun. 72:2101.
38. Fortune, S. M., A. Solache, A. Jaeger, P. J. Hill, J. T. Belisle, B. R. Bloom, E. J. Rubin, and J. D. Ernst. 2004. Mycobacterium tuberculosis inhibits macrophage responses to IFN-γ through myeloid differentiation factor 88-dependent and -independent mechanisms. J. Immunol. 172:6272.
39. Netea, M. G., R. Sutmuller, C. Hermann, C. A. Van der Graaf, J. W. Van der Meer, J. H. van Krieken, T. Hartung, G. Adema, and B. J. Kullberg. 2004. Toll-like receptor 2 suppresses immunity against Candida albicans through induction of IL-10 and regulatory T cells. J. Immunol. 172:3712.
40. Feng, C. G., M. C. Kullberg, D. Jankovic, A. W. Cheever, P. Caspar, R. L. Coffman, and A. Sher. 2002. Transgenic mice expressing human interleukin-10 in the antigen-presenting cell compartment show increased susceptibility to infection with Mycobacterium avium associated with decreased macrophage effector function and apoptosis. Infect. Immun. 70:6672.
41. Lang, R., R. L. Rutschman, D. R. Greaves, and P. J. Murray. 2002. Autocrine deactivation of macrophages in transgenic mice constitutively overexpressing IL-10 under control of the human CD68 promoter. J. Immunol. 168:3402.
42. Murray, P. J., and R. A. Young. 1999. Increased antimycobacterial immunity in interleukin-10-deficient mice. Infect. Immun. 67:3087.
43. McCullers, J. A., and J. E. Rehg. 2002. Lethal synergism between influenza virus and Streptococcus pneumoniae: characterization of a mouse model and the role of platelet-activating factor receptor. J. Infect. Dis. 186:341.