Differential IL-10 production by DCs determines the distinct adjuvant effects of LPS and PTX in EAE induction

European Journal of Immunology

Volumn 44, Issue 5, 2014, Pages 1352-1362

  Zhou, Haiyan ^a   Wang, Yanming ^b   Lian, Qiaoshi ^a   Yang, Bo ^b   Ma, Yonglei ^a   Wu, Xiaodong ^a   Sun, Shuhui ^c   Liu, Yongjun ^d,e   Sun, Bing ^a,d  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b UNIVERSITY OF SCIENCE AND TECHNOLOGY OF CHINA   (China)

^c FUDAN UNIVERSITY   (China)

^d INSTITUTE PASTEUR OF SHANGHAI   (China)

^e BAYLOR INSTITUTE FOR IMMUNOLOGY RESEARCH   (United States)

Author keywords

Dendritic cells; EAE; IL 10; LPS; Pertussis toxin (PTX)

Indexed keywords

ADJUVANT; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; LIPOPOLYSACCHARIDE; PERTUSSIS TOXIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CELL CULTURE; CELLULAR IMMUNITY; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; GENE OVEREXPRESSION; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; TH1 CELL; TH17 CELL; WILD TYPE;

DENDRITIC CELLS; EAE; IL-10; LPS; PERTUSSIS TOXIN (PTX);

ADJUVANTS, IMMUNOLOGIC; ANIMALS; DENDRITIC CELLS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-17; LIPOPOLYSACCHARIDES; MICE; MICE, KNOCKOUT; PERTUSSIS TOXIN;

EID: 84899539204     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201343744     Document Type: Article

References (44)

1. + effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 2005. 6: 1123-1132.
2. + T helper cells. Cell 2006. 126: 1121-1133.
3. Park, H., Li, Z., Yang, X. O., Chang, S. H., Nurieva, R., Wang, Y. H., Wang, Y. et al., A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 2005. 6: 1133-1141.
4. Schneider, O. D., Weiss, A. A. and Miller, W. E., Pertussis toxin signals through the TCR to initiate cross-desensitization of the chemokine receptor CXCR4. J. Immunol. 2009. 182: 5730-5739.
5. Brabb, T., Goldrath, A. W., von Dassow, P., Paez, A., Liggitt, H. D. and Goverman, J., Triggers of autoimmune disease in a murine TCR-transgenic model for multiple sclerosis. J. Immunol. 1997. 159: 497-507.
6. Kerfoot, S. M., Long, E. M., Hickey, M. J., Andonegui, G., Lapointe, B. M., Zanardo, R. C., Bonder, C. et al., TLR4 contributes to disease-inducing mechanisms resulting in central nervous system autoimmune disease. J. Immunol. 2004. 173: 7070-7077.
7. Witvliet, M. H., Vogel, M. L., Wiertz, E. J. and Poolman, J. T., Interaction of pertussis toxin with human T lymphocytes. Infect. Immun. 1992. 60: 5085-5090.
8. He, J., Gurunathan, S., Iwasaki, A., Ash-Shaheed, B. and Kelsall, B. L., Primary role for Gi protein signaling in the regulation of interleukin 12 production and the induction of T helper cell type 1 responses. J. Exp. Med. 2000. 191: 1605-1610.
9. Ryan, M., McCarthy, L., Rappuoli, R., Mahon, B. P. and Mills, K. H., Pertussis toxin potentiates Th1 and Th2 responses to co-injected antigen: adjuvant action is associated with enhanced regulatory cytokine production and expression of the co-stimulatory molecules B7-1, B7-2 and CD28. Int. Immunol. 1998. 10: 651-662.
10. Shive, C. L., Hofstetter, H., Arredondo, L., Shaw, C. and Forsthuber, T. G., The enhanced antigen-specific production of cytokines induced by pertussis toxin is due to clonal expansion of T cells and not to altered effector functions of long-term memory cells. Eur. J. Immunol. 2000. 30: 2422-2431.
11. Hou, W., Wu, Y., Sun, S., Shi, M., Sun, Y., Yang, C., Pei, G. et al., Pertussis toxin enhances Th1 responses by stimulation of dendritic cells. J. Immunol. 2003. 170: 1728-1736.
12. Fedele, G., Spensieri, F., Palazzo, R., Nasso, M., Cheung, G. Y., Coote, J. G. and Ausiello, C. M., Bordetella pertussis commits human dendritic cells to promote a Th1/Th17 response through the activity of adenylate cyclase toxin and MAPK-pathways. PLoS One 2010. 5: e8734.
13. Locht, C., Coutte, L. and Mielcarek, N., The ins and outs of pertussis toxin. FEBS J. 2011. 278: 4668-4682.
14. Nasso, M., Fedele, G., Spensieri, F., Palazzo, R., Costantino, P., Rappuoli, R. and Ausiello, C. M., Genetically detoxified pertussis toxin induces Th1/Th17 immune response through MAPKs and IL-10-dependent mechanisms. J. Immunol. 2009. 183: 1892-1899.
15. Barton, G. M. and Medzhitov, R., Toll-like receptor signaling pathways. Science 2003. 300: 1524-1525.
16. Stetson, D. B. and Medzhitov, R., Type I interferons in host defense. Immunity 2006. 25: 373-381.
17. McAleer, J. P., Rossi, R. J. and Vella, A. T., Lipopolysaccharide potentiates effector T cell accumulation into nonlymphoid tissues through TRIF. J. Immunol. 2009. 182: 5322-5330.
18. + cells. J. Immunol. 2007. 179: 6524-6535.
19. + T cells. J. Immunol. 1997. 159: 591-598.
20. Assoian, R. K., Fleurdelys, B. E., Stevenson, H. C., Miller, P. J., Madtes, D. K., Raines, E. W., Ross, R. et al., Expression and secretion of type beta transforming growth factor by activated human macrophages. Proc. Natl. Acad. Sci. USA 1987. 84: 6020-6024.
21. Re, F. and Strominger, J. L., Toll-like receptor 2 (TLR2) and TLR4 differentially activate human dendritic cells. J. Biol. Chem. 2001. 276: 37692-37699.
22. Veldhoen, M., Hocking, R. J., Atkins, C. J., Locksley, R. M. and Stockinger, B., TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 2006. 24: 179-189.
23. Iyer, S. S., Ghaffari, A. A. and Cheng, G., Lipopolysaccharide-mediated IL-10 transcriptional regulation requires sequential induction of type I IFNs and IL-27 in macrophages. J. Immunol. 2010. 185: 6599-6607.
24. Samoilova, E. B., Horton, J. L. and Chen, Y., Acceleration of experimental autoimmune encephalomyelitis in interleukin-10-deficient mice: roles of interleukin-10 in disease progression and recovery. Cell Immunol. 1998. 188: 118-124.
25. Cua, D. J., Groux, H., Hinton, D. R., Stohlman, S. A. and Coffman, R. L., Transgenic interleukin 10 prevents induction of experimental autoimmune encephalomyelitis. J. Exp. Med. 1999. 189: 1005-1010.
26. Yu, P., Gregg, R. K., Bell, J. J., Ellis, J. S., Divekar, R., Lee, H. H., Jain, R. et al., Specific T regulatory cells display broad suppressive functions against experimental allergic encephalomyelitis upon activation with cognate antigen. J. Immunol. 2005. 174: 6772-6780.
27. Kroenke, M. A., Carlson, T. J., Andjelkovic, A. V. and Segal, B. M., IL-12- and IL-23-modulated T cells induce distinct types of EAE based on histology, CNS chemokine profile, and response to cytokine inhibition. J. Exp. Med. 2008. 205: 1535-1541.
28. Stromnes, I. M., Cerretti, L. M., Liggitt, D., Harris, R. A. and Goverman, J. M., Differential regulation of central nervous system autoimmunity by T(H)1 and T(H)17 cells. Nat. Med. 2008. 14: 337-342.
29. Codarri, L., Gyulveszi, G., Tosevski, V., Hesske, L., Fontana, A., Magnenat, L., Suter, T. et al., RORgammat drives production of the cytokine GM-CSF in helper T cells, which is essential for the effector phase of autoimmune neuroinflammation. Nat. Immunol. 2011. 12: 560-567.
30. El-Behi, M., Ciric, B., Dai, H., Yan, Y., Cullimore, M., Safavi, F., Zhang, G. X. et al., The encephalitogenicity of T(H)17 cells is dependent on IL-1- and IL-23-induced production of the cytokine GM-CSF. Nat. Immunol. 2011. 12: 568-575.
31. Odobasic, D., Leech, M. T., Xue, J. R. and Holdsworth, S. R., Distinct in vivo roles of CD80 and CD86 in the effector T-cell responses inducing antigen-induced arthritis. Immunology 2008. 124: 503-513.
32. Murphy, K. M. and Reiner, S. L., The lineage decisions of helper T cells. Nat. Rev. Immunol. 2002. 2: 933-944.
33. Dong, C., TH17 cells in development: an updated view of their molecular identity and genetic programming. Nat. Rev. Immunol. 2008. 8: 337-348.
34. Chaudhry, A., Samstein, R. M., Treuting, P., Liang, Y., Pils, M. C., Heinrich, J. M., Jack, R. S. et al., Interleukin-10 signaling in regulatory T cells is required for suppression of Th17 cell-mediated inflammation. Immunity 2011. 34: 566-578.
35. +) regulatory T cells. Immunity 2012. 37: 264-275.
36. Eggert, A. A., Schreurs, M. W., Boerman, O. C., Oyen, W. J., de Boer, A. J., Punt, C. J., Figdor, C. G. et al., Biodistribution and vaccine efficiency of murine dendritic cells are dependent on the route of administration. Cancer Res. 1999. 59: 3340-3345.
37. Buttmann, M. and Rieckmann, P., Interferon-beta1b in multiple sclerosis. Expert. Rev. Neurother. 2007. 7: 227-239.
38. Guo, B., Chang, E. Y. and Cheng, G., The type I IFN induction pathway constrains Th17-mediated autoimmune inflammation in mice. J. Clin. Invest. 2008. 118: 1680-1690.
39. Arnason, B. G., Immunologic therapy of multiple sclerosis. Annu. Rev. Med. 1999. 50: 291-302.
40. Inoue, M., Williams, K. L., Oliver, T., Vandenabeele, P., Rajan, J. V., Miao, E. A. and Shinohara, M. L., Interferon-therapy against EAE is effective only when development of the disease depends on the NLRP3 inflammasome. Sci. Signal. 2012. 5: ra38.
41. Saraiva, M. and O'Garra, A., The regulation of IL-10 production by immune cells. Nat. Rev. Immunol. 2010. 10: 170-181.
42. Adib-Conquy, M., Moine, P., Asehnoune, K., Edouard, A., Espevik, T., Miyake, K., Werts, C. et al., Toll-like receptor-mediated tumor necrosis factor and interleukin-10 production differ during systemic inflammation. Am. J. Respir. Crit. Care. Med. 2003. 168: 158-164.
43. Ausiello, C. M., Fedele, G., Urbani, F., Lande, R., Di Carlo, B. and Cassone, A., Native and genetically inactivated pertussis toxins induce human dendritic cell maturation and synergize with lipopolysaccharide in promoting T helper type 1 responses. J. Infect. Dis. 2002. 186: 351-360.
44. Mata-Haro, V., Cekic, C., Martin, M., Chilton, P. M., Casella, C. R. and Mitchell, T. C., The vaccine adjuvant monophosphoryl lipid A as a TRIF-biased agonist of TLR4. Science 2007. 316: 1628-1632.