IL-23-dependent IL-17 drives Th1-cell responses following Mycobacterium bovis BCG vaccination

European Journal of Immunology

Volumn 42, Issue 2, 2012, Pages 364-373

  Gopal, Radha ^a   Lin, Yinyao ^a   Obermajer, Nataša ^a   Slight, Samantha ^a   Nuthalapati, Nikhil ^a   Ahmed, Mushtaq ^a   Kalinski, Pawel ^a   Khader, Shabaana A ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Immune regulation; Immune responses; Intracellular bacteria; T helper cells

Indexed keywords

BCG VACCINE; CELECOXIB; CYCLOOXYGENASE 2; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 23; PROSTAGLANDIN E2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL POLARITY; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; DRUG EXPOSURE; ENZYME INHIBITION; IN VIVO STUDY; MOUSE; MYCOBACTERIUM BOVIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TH1 CELL; TH17 CELL; TREATMENT RESPONSE; TUBERCULOSIS; VACCINATION;

ANIMALS; BACTERIAL LOAD; DINOPROSTONE; DISEASE MODELS, ANIMAL; HUMANS; IMMUNOMODULATION; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-17; INTERLEUKIN-23; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MYCOBACTERIUM BOVIS; PARACRINE COMMUNICATION; TH1 CELLS; TUBERCULOSIS; VACCINATION;

EID: 84862923858     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201141569     Document Type: Article

References (38)

1. Dye, C., Williams, B., Espinal, M. and Raviglione, M., Erasing the world's slow stain: strategies to beat multidrug-resistant tuberculosis. Science 2002. 295: 2042-2046.
2. Akahoshi, M., Nakashima, H., Miyake, K., Inoue, Y., Shimizu, S., Tanaka, Y., Okada, K. et al., Influence of interleukin-12 receptor beta1 polymorphisms on tuberculosis. Hum. Genet. 2003. 112: 237-243.
3. Cooper, A. M., Roberts, A. D., Rhoades, E. R., Callahan, J. E., Getzy, D. M. and Orme, I. M., The role of interleukin-12 in acquired immunity to Mycobacterium tuberculosis infection. Immunology 1995. 84: 423-432.
4. Goter-Robinson, C., Derrick, S. C., Yang, A. L., Jeon, B. Y. and Morris, S. L., Protection against an aerogenic Mycobacterium tuberculosis infection in BCG-immunized and DNA-vaccinated mice is associated with early type I cytokine responses. Vaccine 2006. 24: 3522-3529.
5. Trinchieri, G., Pflanz, S. and Kastelein, R., The IL-12 family of heterodimeric cytokines: new players in the regulation of T cell responses. Immunity 2003. 19: 641-644.
6. Oppmann, B., Lesley, R., Blom, B., Timans, J., Xu, Y., Hunte, B., Vega, F. et al., Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity 2000. 13: 715-725.
7. 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.
8. Harrington, L. E., Hatton, R. D., Mangan, P. R., Turner, H., Murphy, T. L., Murphy, K. M. and Weaver, C. T., Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat. Immunol. 2005. 6: 1123-1132.
9. Ouyang, W., Kolls, J. K. and Zheng, Y., The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 2008. 28: 454-467.
10. Langrish, C. L., Chen, Y., Blumenschein, W. M., Mattson, J., Basham, B., Sedgwick, J. D., McClanahan et al., IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 2005. 201: 233-240.
11. Ye, P., Rodriguez, F. H., Kanaly, S., Stocking, K. L., Schurr, J., Schwarzenberger, P., Oliver, P. et al., Requirement of interleukin 17 receptor signaling for lung CXC chemokine and granulocyte colony-stimulating factor expression, neutrophil recruitment, and host defense. J. Exp. Med. 2001. 194: 519-527.
12. Lin, Y., Ritchea, S., Logar, A., Slight, S., Messmer, M., Rangel-Moreno, J., Guglani, L. et al., Interleukin-17 is required for T helper 1 cell immunity and host resistance to the intracellular pathogen Francisella tularensis. Immunity 2009. 31: 799-810.
13. Bai, H., Cheng, J., Gao, X., Joyee, A. G., Fan, Y., Wang, S., Jiao, L. et al., IL-17/Th17 promotes type 1 T cell immunity against pulmonary intracellular bacterial infection through modulating dendritic cell function. J. Immunol. 2009. 183: 5886-5895.
14. Umemura, M., Yahagi, A., Hamada, S., Begum, M. D., Watanabe, H., Kawakami, K., Suda, T. et al., IL-17-mediated regulation of innate and acquired immune response against pulmonary Mycobacterium bovis bacille Calmette-Guerin infection. J. Immunol. 2007. 178: 3786-3796.
15. van der Pouw Kraan, T. C., Boeije, L. C., Smeenk, R. J., Wijdenes, J. and Aarden, L. A., Prostaglandin-E2 is a potent inhibitor of human interleukin 12 production. J. Exp. Med. 1995. 181: 775-779.
16. Kalinski, P., Hilkens, C. M., Snijders, A., Snijdewint, F. G. and Kapsenberg, M. L., IL-12-deficient dendritic cells, generated in the presence of prostaglandin E2, promote type 2 cytokine production in maturing human naive T helper cells. J. Immunol. 1997. 159: 28-35.
17. Kalinski, P., Vieira, P. L., Schuitemaker, J. H. N., de Jong, E. C. and Kapsenberg, M. L., Prostaglandin E2 is a selective inducer of interleukin-12 p40 (IL-12p40) production and an inhibitor of bioactive IL-12p70 heterodimer. Blood 2001. 97: 3466-3469.
18. Boniface, K., Bak-Jensen, K. S., Li, Y., Blumenschein, W. M., McGeachy, M. J., McClanahan, T. K., McKenzie et al., Prostaglandin E2 regulates Th17 cell differentiation and function through cyclic AMP and EP2/EP4 receptor signaling. J. Exp. Med. 2009. 206: 535-548.
19. Khayrullina, T., Yen, J. H., Jing, H. and Ganea, D., In vitro differentiation of dendritic cells in the presence of prostaglandin E2 alters the IL-12/IL-23 balance and promotes differentiation of Th17 cells. J. Immunol. 2008. 181: 721-735.
20. Yanagisawa, S., Koike, M., Kariyone, A., Nagai, S. and Takatsu, K., Mapping of V beta 11+ helper T cell epitopes on mycobacterial antigen in mouse primed with Mycobacterium tuberculosis. Int. Immunol. 1997. 9: 227-237.
21. Szabo, S. J., Kim, S. T., Coosta, G. L., Zhang, X., Fathman, C. G. and Glimcher, L., A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 2000. 100: 655-659.
22. Ivanov, II, McKenzie, B. S., Zhou, L., Tadokoro, C. E., Lepelley, A., Lafaille, J. J., Cua, D. J. and Littman, D. R., The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 2006. 126: 1121-1133.
23. Khader, S. A., Pearl, J. E., Sakamoto, K., Gilmartin, L., Bell, G. K., Jelley-Gibbs, D. M., Ghilardi, N. et al., 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. 2005. 175: 788-795.
24. Cruz, A., Khader, S., Torrado, E., Fraga, A., Pearl, J., Pedrosa, J., Cooper, A. and Castro, A., CE:IFN-g regulates the induction and expansion of IL-17-producing CD4 T cells during mycobacterial infection1. J. Immunol. 2006. 177: 1416-1420.
25. Khader, S. A., Bell, G. K., Pearl, J. E., Fountain, J. J., Rangel-Moreno, J., Cilley, G. E., Shen, F. et al., IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat. Immunol. 2007. 8: 369-377.
26. D'Andrea, A., Aste-Amezaga, M., Valiante, N. m., Ma, X., Kubin, M. and Trinchieri, G., Interleukin 10 (IL-10) inhibits human lymphocyte interferon gamma-production by suppressing natural killer cell stimulatory factor/IL-12 synthesis in accessory cells. J. Exp. Med. 1993. 178: 1041-1048.
27. Demangel, C., Bertolino, P. and Britton, W. J., Autocrine IL-10 impairs dendritic cell (DC)-derived immune responses to mycobacterial infection by suppressing DC trafficking to draining lymph nodes and local IL-12 production. Eur. J. Immunol. 2002. 32: 994-1002.
28. Redford, P. S., Boonstra, A., Read, S., Pitt, J., Graham, C., Stavropoulos, E., Bancroft, G. J. and O'Garra, A., Enhanced protection to Mycobacterium tuberculosis infection in IL-10-deficient mice is accompanied by early and enhanced Th1 responses in the lung. Eur. J. Immunol. 2010. 40: 2200-2210.
29. Schuler-Thurner, B., Schultz, E. S., Berger, T. G., Weinlich, G., Ebner, S., Woerl, P., Bender, A. et al., Rapid induction of tumor-specific type 1 T helper cells in metastatic melanoma patients by vaccination with mature, cryopreserved, peptide-loaded monocyte-derived dendritic cells. J. Exp. Med. 2002. 195: 1279-1288.
30. Thurner, B., Haendle, I., Roder, C., Dieckmann, D., Keikavoussi, P., Jonuleit, H., Bender, A. et al., Vaccination with mage-3A1 peptide-pulsed mature, monocyte-derived dendritic cells expands specific cytotoxic T cells and induces regression of some metastases in advanced stage IV melanoma. J. Exp. Med. 1999. 190: 1669-1678.
31. Shen, F. and Gaffen, S. L., Structure-function relationships in the IL-17 receptor: implications for signal transduction and therapy. Cytokine 2008. 41: 92-104.
32. Ishigame, H., Kakuta, S., Nagai, T., Kadoki, M., Nambu, A., Komiyama, Y., Fujikado, N. et al., Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 2009. 30: 108-119.
33. Da Silva, C. A., Hartl, D., Liu, W., Lee, C. G. and Elias, J. A., TLR-2 and IL-17A in chitin-induced macrophage activation and acute inflammation. J. Immunol. 2008. 181: 4279-4286.
34. Higgins, S. C., Jarnicki, A. G., Lavelle, E. C. and Mills, K. H., TLR4 mediates vaccine-induced protective cellular immunity to Bordetella pertussis: role of IL-17-producing T cells. J. Immunol. 2006. 177: 7980-7989.
35. Duerr, R., Taylor, K., Brant, S., Rioux, J., Silverberg, M., Daly, M., Steinhart, A. et al., A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science 2006. 314: 1461-1463.
36. Kaufmann, S. H., Hussey, G. and Lambert, P. H., New vaccines for tuberculosis. Lancet 2010. 375: 2110-2119.
37. Ghilardi, N., Kljavin, N., Chen, Q., Lucas, S., Gurney, A. L. and De Sauvage, F. J., Compromised humoral and delayed-type hypersensitivity responses in IL-23-deficient mice. J. Immunol. 2004. 172: 2827-2833.
38. Corinti, S., Albanesi, C., la Sala, A., Pastore, S. and Girolomoni, G., Regulatory activity of autocrine IL-10 on dendritic cell functions. J. Immunol. 2001. 166: 4312-4318.