IL-17A-producing γδT cells promote CTL responses against Listeria monocytogenes infection by enhancing dendritic cell cross-presentation

Journal of Immunology

Volumn 185, Issue 10, 2010, Pages 5879-5887

  Xu, Sheng ^a   Han, Yanmei ^a   Xu, Xiongfei ^a   Bao, Yan ^a   Zhang, Minggang ^a   Cao, Xuetao ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 12P70; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 6;

ADAPTIVE IMMUNITY; ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; CONTROLLED STUDY; CROSS PRESENTATION; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; DENDRITIC CELL; GAMMADELTA T LYMPHOCYTE; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; LISTERIOSIS; LIVER; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPLEEN; T LYMPHOCYTE SUBPOPULATION; TH17 CELL;

ADOPTIVE TRANSFER; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL SEPARATION; CROSS-PRIMING; CYTOTOXICITY, IMMUNOLOGIC; DENDRITIC CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; INTERLEUKIN-17; LISTERIA MONOCYTOGENES; LISTERIOSIS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTE SUBSETS; TH17 CELLS;

EID: 78650703319     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1001763     Document Type: Article

References (56)

1. Park, H., Z. Li, X. O. Yang, S. H. Chang, R. Nurieva, Y. H. Wang, Y. Wang, L. Hood, Z. Zhu, Q. Tian, and C. Dong. 2005. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6:1133-1141.
2. + effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 6:1123-1132.
3. Kolls, J. K., and A. Lindén. 2004. Interleukin-17 family members and inflammation. Immunity 21:467-476.
4. Weaver, C. T., R. D. Hatton, P. R. Mangan, and L. E. Harrington. 2007. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu. Rev. Immunol. 25:821-852.
5. Korn, T., E. Bettelli, M. Oukka, and V. K. Kuchroo. 2009. IL-17 and Th17 Cells. Annu. Rev. Immunol. 27:485-517.
6. Doreau, A., A. Belot, J. Bastid, B. Riche, M. C. Trescol-Biemont, B. Ranchin, N. Fabien, P. Cochat, C. Pouteil-Noble, P. Trolliet, et al. 2009. Interleukin 17 acts in synergy with B cell-activating factor to influence B cell biology and the pathophysiology of systemic lupus erythematosus. Nat. Immunol. 10:778-785.
7. Khader, S. A., S. L. Gaffen, and J. K. Kolls. 2009. Th17 cells at the crossroads of innate and adaptive immunity against infectious diseases at the mucosa. Mucosal Immunol. 2:403-411.
8. Xu, S., and X. Cao. 2010. Interleukin-17 and its expanding biological functions. Cell. Mol. Immunol. 7:164-174.
9. Happel, K. I., P. J. Dubin, M. Zheng, N. Ghilardi, C. Lockhart, L. J. Quinton, A. R. Odden, J. E. Shellito, G. J. Bagby, S. Nelson, and J. K. Kolls. 2005. Divergent roles of IL-23 and IL-12 in host defense against Klebsiella pneumoniae. J. Exp. Med. 202:761-769.
10. Ishigame, H., S. Kakuta, T. Nagai, M. Kadoki, A. Nambu, Y. Komiyama, N. Fujikado, Y. Tanahashi, A. Akitsu, H. Kotaki, et al. 2009. Differential roles of interleukin-17A and-17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 30:108-119.
11. Dubin, P. J., and J. K. Kolls. 2007. IL-23 mediates inflammatory responses to mucoid Pseudomonas aeruginosa lung infection in mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 292: L519-L528.
12. Khader, S. A., J. E. Pearl, K. Sakamoto, L. Gilmartin, G. K. Bell, D. M. Jelley-Gibbs, N. Ghilardi, F. deSauvage, and A. M. Cooper. 2005. IL-23 compensates for the absence of IL-12p70 and is essential for the IL-17 response during tuberculosis but is dispensable for protection and antigen-specific IFN-gamma responses if IL-12p70 is available. J. Immunol. 175:788-795.
13. Raffatellu, M., R. L. Santos, D. E. Verhoeven, M. D. George, R. P. Wilson, S. E. Winter, I. Godinez, S. Sankaran, T. A. Paixao, M. A. Gordon, et al. 2008. Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nat. Med. 14:421-428.
14. Lin, Y., S. Ritchea, A. Logar, S. Slight, M. Messmer, J. Rangel-Moreno, L. Guglani, J. F. Alcorn, H. Strawbridge, S. M. Park, et al. 2009. Interleukin-17 is required for T helper 1 cell immunity and host resistance tothe intracellular pathogen Francisella tularensis. Immunity 31:799-810.
15. Khader, S. A., G. K. Bell, J. E. Pearl, J. J. Fountain, J. Rangel-Moreno, G. E. Cilley, F. Shen, S. M. Eaton, S. L. Gaffen, S. L. Swain, et al. 2007. IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat. Immunol. 8:369-377.
16. Hamada, S., M. Umemura, T. Shiono, K. Tanaka, A. Yahagi, M. D. Begum, K. Oshiro, Y. Okamoto, H. Watanabe, K. Kawakami, et al. 2008. IL-17A produced by gammadelta T cells plays a critical role in innate immunity against listeria monocytogenes infection in the liver. J. Immunol. 181:3456-3463.
17. Nakae, S., Y. Komiyama, A. Nambu, K. Sudo, M. Iwase, I. Homma, K. Sekikawa, M. Asano, and Y. Iwakura. 2002. Antigen-specific T cell sensitization is impaired in IL-17-deficient mice, causing suppression of allergic cellular and humoral responses. Immunity 17:375-387.
18. O'Connor, W., Jr., M. Kamanaka, C. J. Booth, T. Town, S. Nakae, Y. Iwakura, J. K. Kolls, and R. A. Flavell. 2009. A protective function for interleukin 17A in T cell-mediated intestinal inflammation. Nat. Immunol. 10:603-609.
19. Beetz, S., D. Wesch, L. Marischen, S. Welte, H. H. Oberg, and D. Kabelitz. 2008. Innate immune functions of human gammadelta T cells. Immunobiology 213:173-182.
20. Girardi, M. 2006. Immunosurveillance and immunoregulation by gammadelta T cells. J. Invest. Dermatol. 126:25-31.
21. Shen, Y., D. Zhou, L. Qiu, X. Lai, M. Simon, L. Shen, Z. Kou, Q. Wang, L. Jiang, J. Estep, et al. 2002. Adaptive immune response of Vgamma2Vdelta2+ T cells during mycobacterial infections. Science 295:2255-2258.
22. Hayday, A., and R. Tigelaar. 2003. Immunoregulation in the tissues by gammadelta T cells. Nat. Rev. Immunol. 3:233-242.
23. Lockhart, E., A. M. Green, and J. L. Flynn. 2006. IL-17 production is dominated by gammadelta T cells rather than CD4 T cells during Mycobacterium tuberculosis infection. J. Immunol. 177:4662-4669.
24. Shibata, K., H. Yamada, H. Hara, K. Kishihara, and Y. Yoshikai. 2007. Resident Vdelta1+ gammadelta T cells control early infiltration of neutrophils after Escherichia coli infection via IL-17 production. J. Immunol. 178:4466-4472.
25. Han, C., J. Jin, S. Xu, H. Liu, N. Li, and X. Cao. 2010. Integrin CD11b negatively regulates TLR-triggered inflammatory responses by activating Syk and promoting degradation of MyD88 and TRIF via Cbl-b. Nat. Immunol. 11:734-742.
26. Zhang, M., H. Tang, Z. Guo, H. An, X. Zhu, W. Song, J. Guo, X. Huang, T. Chen, J. Wang, and X. Cao. 2004. Splenic stroma drives mature dendritic cells to differentiate into regulatory dendritic cells. Nat. Immunol. 5:1124-1133.
27. Qian, C., H. An, Y. Yu, S. Liu, and X. Cao. 2007. TLR agonists induce regulatory dendritic cells to recruit Th1 cells via preferential IP-10 secretion and inhibit Th1 proliferation. Blood 109:3308-3315.
28. Vremec, D., J. Pooley, H. Hochrein, L. Wu, and K. Shortman. 2000. CD4 and CD8 expression by dendritic cell subtypes in mouse thymus and spleen. J. Immunol. 164:2978-2986.
29. Wherry, E. J., V. Teichgráber, T. C. Becker, D. Masopust, S. M. Kaech, R. Antia, U. H. von Andrian, and R. Ahmed. 2003. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat. Immunol. 4:225-234.
30. Wu, Y., T. Wan, X. Zhou, B. Wang, F. Yang, N. Li, G. Chen, S. Dai, S. Liu, M. Zhang, and X. Cao. 2005. Hsp70-like protein 1 fusion protein enhances induction of carcinoembryonic antigen-specific CD8+ CTL response by dendritic cell vaccine. Cancer Res. 65:4947-4954.
31. Williams, M. A., and M. J. Bevan. 2007. Effector and memory CTL differentiation. Annu. Rev. Immunol. 25:171-192.
32. Prlic, M., G. Hernandez-Hoyos, and M. J. Bevan. 2006. Duration of the initial TCR stimulus controls the magnitude but not functionality of the CD8+ T cell response. J. Exp. Med. 203:2135-2143.
33. Pearce, E. L., and H. Shen. 2007. Generation of CD8 T cell memory is regulated by IL-12. J. Immunol. 179:2074-2081.
34. Pooley, J. L., W. R. Heath, and K. Shortman. 2001. Cutting edge: intravenous soluble antigen is presented to CD4 T cells by CD8-dendritic cells, but crosspresented to CD8 T cells by CD8+ dendritic cells. J. Immunol. 166:5327-5330.
35. den Haan, J. M., S. M. Lehar, and M. J. Bevan. 2000. CD8 (+) but not CD8 (-) dendritic cells cross-prime cytotoxic T cells in vivo. J. Exp. Med. 192:1685-1696.
36. Belz, G. T., K. Shortman, M. J. Bevan, and W. R. Heath. 2005. CD8alpha+ dendritic cells selectively present MHC class I-restricted noncytolytic viral and intracellular bacterial antigens in vivo. J. Immunol. 175:196-200.
37. Veldhoen, M., R. J. Hocking, C. J. Atkins, R. M. Locksley, and B. Stockinger. 2006. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24:179-189.
38. Mangan, P. R., L. E. Harrington, D. B. O'Quinn, W. S. Helms, D. C. Bullard, C. O. Elson, R. D. Hatton, S. M. Wahl, T. R. Schoeb, and C. T. Weaver. 2006. Transforming growth factor-beta induces development of the T (H) 17 lineage. Nature 441:231-234.
39. Bettelli, E., Y. Carrier, W. Gao, T. Korn, T. B. Strom, M. Oukka, H. L. Weiner, and V. K. Kuchroo. 2006. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441:235-238.
40. Martin-Orozco, N., P. Muranski, Y. Chung, X. O. Yang, T. Yamazaki, S. Lu, P. Hwu, N. P. Restifo, W. W. Overwijk, and C. Dong. 2009. T helper 17 cells promote cytotoxic T cell activation in tumor immunity. Immunity 31:787-798.
41. Ye, P., F. H. Rodriguez, S. Kanaly, K. L. Stocking, J. Schurr, P. Schwarzenberger, P. Oliver, W. Huang, P. Zhang, J. Zhang, et al. 2001. Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colonystimulating factor expression, neutrophil recruitment, and host defense. J. Exp. Med. 194:519-527.
42. + T cell responses to bacterial antigens. J. Immunol. 173:1994-2002.
43. von Vietinghoff, S., K. Ley; von. 2009. IL-17A controls IL-17F production and maintains blood neutrophil counts in mice. J. Immunol. 183:865-873.
44. Wick, M. J., and H. G. Ljunggren. 1999. Processing of bacterial antigens for peptide presentation on MHC class I molecules. Immunol. Rev. 172:153-162.
45. Steinman, R. M., and J. Banchereau. 2007. Taking dendritic cells into medicine. Nature 449:419-426.
46. Sutton, C. E., S. J. Lalor, C. M. Sweeney, C. F. Brereton, E. C. Lavelle, and K. H. Mills. 2009. Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity 31:331-341.
47. den Haan, J. M., and M. J. Bevan. 2001. Antigen presentation to CD8+ T cells: cross-priming in infectious diseases. Curr. Opin. Immunol. 13:437-441.
48. + dendritic cells are required for efficient entry of Listeria monocytogenes into the spleen. Immunity 25:619-630.
49. Martin, B., K. Hirota, D. J. Cua, B. Stockinger, and M. Veldhoen. 2009. Interleukin-17-producing gammadelta T cells selectively expand in response to pathogen products and environmental signals. Immunity 31:321-330.
50. + T helper cells. Cell 126:1121-1133.
51. Jensen, K. D., X. Su, S. Shin, L. Li, S. Youssef, S. Yamasaki, L. Steinman, T. Saito, R. M. Locksley, M. M. Davis, et al. 2008. Thymic selection determines gammadelta T cell effector fate: antigen-naive cells make interleukin-17 and antigen-experienced cells make interferon gamma. Immunity 29:90-100.
52. Shedlock, D. J., and H. Shen. 2003. Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science 300:337-339.
53. Sun, J. C., and M. J. Bevan. 2003. Defective CD8 T cell memory following acute infection without CD4 T cell help. Science 300:339-342.
54. + cytotoxic T cells in immune response against the intracellular bacteria Listeria monocytogenes. Immunology 95:226-233.
55. Fedele, G., M. Nasso, F. Spensieri, R. Palazzo, L. Frasca, M. Watanabe, and C. M. Ausiello. 2008. Lipopolysaccharides from Bordetella pertussis and Bordetella parapertussis differently modulate human dendritic cell functions resulting in divergent prevalence of Th17-polarized responses. J. Immunol. 181:208-216.
56. Cua, D. J., J. Sherlock, Y. Chen, C. A. Murphy, B. Joyce, B. Seymour, L. Lucian, W. To, S. Kwan, T. Churakova, et al. 2003. Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421:744-748.