IL-17 promotes progression of cutaneous leishmaniasis in susceptible mice

Journal of Immunology

Volumn 182, Issue 5, 2009, Pages 3039-3046

  Kostka, Susanna Lopez ^a   Dinges, Stephanie ^a   Griewank, Klaus ^a   Iwakura, Yoichiro ^b   Udey, Mark C ^c   Von Stebut, Esther ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b UNIVERSITY OF TOKYO   (Japan)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL2 CHEMOKINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 23; INTERLEUKIN 4; INTERLEUKIN 6; TRANSFORMING GROWTH FACTOR BETA1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BAGG ALBINO MOUSE; C57BL 6 MOUSE; CD4+ T LYMPHOCYTE; CELL MIGRATION; CONTROLLED STUDY; DENDRITIC CELL; DISEASE COURSE; INFECTION SENSITIVITY; LEISHMANIA MAJOR; MOUSE; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; SKIN DEFECT; SKIN LEISHMANIASIS; TH1 CELL; TH2 CELL; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; CELLULAR IMMUNITY; COMPARATIVE STUDY; GENETIC PREDISPOSITION; GENETICS; IMMUNOLOGY; MOUSE MUTANT; PARASITOLOGY; PATHOLOGY; PHYSIOLOGY; SECRETION; SPECIES DIFFERENCE; UPREGULATION;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; DENDRITIC CELLS; DISEASE PROGRESSION; GENETIC PREDISPOSITION TO DISEASE; IMMUNITY, CELLULAR; INTERLEUKIN-17; INTERLEUKIN-23; LEISHMANIA MAJOR; LEISHMANIASIS, CUTANEOUS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHILS; SPECIES SPECIFICITY; TH2 CELLS; UP-REGULATION;

EID: 64849086164     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0713598     Document Type: Article

References (40)

1. Sacks, D., and C. Anderson. 2004. Re-examination of the immunosuppressive mechanisms mediating non-cure of Leishmania infection in mice. Immunol. Rev. 201: 225-238.
2. Woelbing, F., S. Lopez Kostka, K. Moelle, Y. Belkaid, C. Sunderkoetter, S. Verbeek, A. Waisman, A. P. Nigg, J. Knop, M. C. Udey, and E. von Stebut. 2006. Uptake of Leishmania major by dendritic cells is mediated by Fcγ receptors and facilitates acquisition of protective immunity. J. Exp. Med. 203: 177-188.
3. von Stebut, E., and M. C. Udey. 2004. Requirements for Th1-dependent immunity against infection with Leishmania major. Microbes Infect. 6: 1102-1109.
4. + T cell polarization in mice is modulated by strain-specific major histocompatibility complex-independent differences within dendritic cells. J. Exp. Med. 198: 201-209.
5. von Stebut, E., J. M. Ehrchen, Y. Belkaid, S. Lopez Kostka, K. Mölle, J. Knop, C. Sunderkötter, and M. C. Udey. 2003. IL-1α promotes Th1-differentiation and inhibits disease progression in Leishmania major-susceptible BALB/c mice. J. Exp. Med. 198: 191-199.
6. Nigg, A. P., S. Zahn, D. Ruckerl, C. Holscher, T. Yoshimoto, J. M. Ehrchen, F. Wolbing, M. C. Udey, and E. von Stebut. 2007. Dendritic cell-derived IL-12p40 homodimer contributes to susceptibility in cutaneous leishmaniasis in BALB/c mice. J. Immunol. 78: 7251-7258.
7. Iwakura, Y., and H. Ishigame. 2006. The IL-23/IL-17 axis in inflammation. J. Clin. Invest. 116: 1218-1222.
8. H2. Nat. Immunol. 6: 1069-1070.
9. Tato, C. M., and J. J. O'Shea. 2006. Immunology: what does it mean to be just 17? Nature 441: 166-168.
10. 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.
11. Miossec, P. 2003. Interleukin-17 in rheumatoid arthritis: if T cells were to contribute to inflammation and destruction through synergy. Arthritis Rheum. 48: 594-601.
12. Nakae, S., S. Saijo, R. Horai, K. Sudo, S. Mori, and Y. Iwakura. 2003. IL-17 production from activated T cells is required for the spontaneous development of destructive arthritis in mice deficient in IL-1 receptor antagonist. Proc. Natl. Acad. Sci. USA 100: 5986-5590.
13. Matsuki, T., S. Nakae, K. Sudo, R. Horai, and Y. Iwakura. 2006. Abnormal T cell activation caused by the imbalance of the IL-1/IL-1R antagonist system is responsible for the development of experimental autoimmune encephalomyelitis. Int. Immunol. 18: 399-407.
14. Cho, M. L., J. W. Kang, Y. M. Moon, H. J. Nam, J. Y. Jhun, S. B. Heo, H. T. Jin, S. Y. Min, J. H. Ju, K. S. Park, et al. 2006. STAT3 and NF-κB signal pathway is required for IL-23-mediated IL-17 production in spontaneous arthritis animal model IL-1 receptor antagonist-deficient mice. J. Immunol. 176: 5652-5661.
15. Sutton, C., C. Brereton, B. Keogh, K. H. Mills, and E. C. Lavelle. 2006. A crucial role for interleukin (IL)-1 in the induction of IL-17-producing T cells that mediate autoimmune encephalomyelitis. J. Exp. Med. 203: 1685-1691.
16. + Th2 response in BALB/c mice infected with Leishmania major. J. Immunol. 165: 2628-2636.
17. Ribeiro-Gomes, F. L., A. C. Otero, N. A. Gomes, M. C. Moniz-De-Souza, L. Cysne-Finkelstein, A. C. Arnholdt, V. L. Calich, S. G. Coutinho, M. F. Lopes, and G. A. DosReis. 2004. Macrophage interactions with neutrophils regulate Leishmania major infection. J. Immunol. 172: 4454-4462.
18. Inaba, K., M. Inaba, N. Romani, H. Aya, M. Deguchi, S. Ikehara, S. Muramatsu, and R. M. Steinman. 1992. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 176: 1693-1702.
19. Flohe, S. B., C. Bauer, S. Flohe, and H. Moll. 1998. Antigen-pulsed epidermal Langerhans cells protect susceptible mice from infection with the intracellular parasite Leishmania major. Eur. J. Immunol. 28: 3800-3811.
20. von Stebut, E., Y. Belkaid, T. Jakob, D. L. Sacks, and M. C. Udey. 1998. Uptake of Leishmania major amastigotes results in activation and interleukin 12 release from murine skin-derived dendritic cells: implications for the initiation of anti-Leishmania immunity. J. Exp. Med. 188: 1547-1552.
21. von Stebut, E., Y. Belkaid, B. V. Nguyen, M. Cushing, D. L. Sacks, and M. C. Udey. 2000. Leishmania major-infected murine Langerhans cell-like dendritic cells from susceptible mice release IL-12 after infection and vaccinate against experimental cutaneous leishmaniasis. Eur. J. Immunol. 30: 3498-3506.
22. Shibuya, K., D. Robinson, F. Zonin, S. B. Hartley, S. E. Macatonia, C. Somoza, C. A. Hunter, K. M. Murphy, and A. O'Garra. 1998. IL-1α and TNF-α are required for IL-12-induced development of Th1 cells producing high levels of IFN-γ in BALB/c but not C57BL/6 mice. J. Immunol. 160: 1708-1716.
23. Ji, J., J. Sun, and L. Soong. 2003. Impaired expression of inflammatory cytokines and chemokines at early stages of infection with Leishmania amazonensis. Infect. Immun. 71: 4278-4288.
24. H-17 cell-mediated pathology. Nat. Immunol. 8: 1390-1397.
25. Veldhoen, M., R. J. Hocking, C. J. Atkins, R. M. Locksley, and B. Stockinger. 2006. TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24: 179-189.
26. 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.
27. H17 lineage. Nature 441: 231-234.
28. 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.
29. Yu, J. J., M. J. Ruddy, G. C. Wong, C. Sfintescu, P. J. Baker, J. B. Smith, R. T. Evans, and S. L. Gaffen. 2007. An essential role for IL-17 in preventing pathogen-initiated bone destruction: recruitment of neutrophils to inflamed bone requires IL-17 receptor-dependent signals. Blood 109: 3794-3802.
30. Liang, S. C., A. J. Long, F. Bennett, M. J. Whitters, R. Karim, M. Collins, S. J. Goldman, K. Dunussi-Joannopoulos, C. M. Williams, J. F. Wright, and L. A. Fouser. 2007. An IL-17F/A heterodimer protein is produced by mouse Th17 cells and induces airway neutrophil recruitment. J. Immunol. 179: 7791-7799.
31. Aggarwal, S., N. Ghilardi, M. H. Xie, F. J. de Sauvage, and A. L. Gurney. 2003. Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J. Biol. Chem. 278: 1910-1914.
32. Parham, C., M. Chirica, J. Timans, E. Vaisberg, M. Travis, J. Cheung, S. Pflanz, R. Zhang, K. P. Singh, F. Vega, et al. 2002. A receptor for the heterodimeric cytokine IL-23 is composed of IL-12Rβ1 and a novel cytokine receptor subunit, IL-23R. J. Immunol. 168: 5699-5708.
33. Lima, G. M., A. L. Vallochi, U. R. Silva, E. M. Bevilacqua, M. M. Kiffer, and I. A. Abrahamsohn. 1998. The role of polymorphonuclear leukocytes in the resistance to cutaneous leishmaniasis. Immunol. Lett. 64: 145-151.
34. Chen, L., Z. H. Zhang, T. Watanabe, T. Yamashita, T. Kobayakawa, A. Kaneko, H. Fujiwara, and F. Sendo. 2005. The involvement of neutrophils in the resistance to Leishmania major infection in susceptible but not in resistant mice. Parasitol. Int. 54: 109-118.
35. Jacobs, T., J. Andra, I. Gaworski, S. Graefe, K. Mellenthin, M. Kromer, R. Halter, J. Borlak, and J. Clos. 2005. Complement C3 is required for the progression of cutaneous lesions and neutrophil attraction in Leishmania major infection. Med. Microbiol. Immunol. 194: 143-149.
36. Beil, W. J., G. Meinardus-Hager, D. C. Neugebauer, and C. Sorg. 1992. Differences in the onset of the inflammatory response to cutaneous leishmaniasis in resistant and susceptible mice. J. Leukocyte Biol. 52: 135-142.
37. Muller, K., G. van Zandbergen, B. Hansen, H. Laufs, N. Jahnke, W. Solbach, and T. Laskay. 2001. Chemokines, natural killer cells and granulocytes in the early course of Leishmania major infection in mice. Med. Microbiol. Immunol. 190: 73-76.
38. Hunter, C. A. 2005. New IL-12-family members: IL-23 and IL-27, cytokines with divergent functions. Nat. Rev. Immunol. 5: 521-531.
39. Kleinschek, M. A., U. Muller, S. J. Brodie, W. Stenzel, G. Kohler, W. M. Blumenschein, R. K. Straubinger, T. McClanahan, R. A. Kastelein, and G. Alber. 2006. IL-23 enhances the inflammatory cell response in Cryptococcus neoformans infection and induces a cytokine pattern distinct from IL-12. J. Immunol. 176: 1098-1106.
40. Rutitzky, L. I., J. R. Lopes da Rosa, and M. J. Stadecker. 2005. Severe CD4 T cell-mediated immunopathology in murine schistosomiasis is dependent on IL-12p40 and correlates with high levels of IL-17. J. Immunol. 175: 3920-3906.