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Th17 responses and host defense against microorganisms: an overview

  • Van De Veerdonk, Frank L. (Department of Medicine, Radboud University Nijmegen Medical Centre) ;
  • Gresnigt, Mark S. (Nijmegen Institute for Infection, Inflammation and Immunity (N4i)) ;
  • Kullberg, Bart Jan (Department of Medicine, Radboud University Nijmegen Medical Centre) ;
  • Van Der Meer, Jos W.M. (Department of Medicine, Radboud University Nijmegen Medical Centre) ;
  • Joosten, Leo A.B. (Department of Medicine, Radboud University Nijmegen Medical Centre) ;
  • Netea, Mihai G. (Department of Medicine, Radboud University Nijmegen Medical Centre)
  • Published : 2009.12.31
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Abstract

T helper (Th) 17 cells have recently been described as a third subset of T helper cells, and have provided new insights into the mechanisms that are important in the development of autoimmune diseases and the immune responses that are essential for effective antimicrobial host defense. Both protective and harmful effects of Th17 responses during infection have been described. In general, Th17 responses are critical for mucosal and epithelial host defense against extracellular bacteria and fungi. However, recent studies have reported that Th17 responses can also contribute to viral persistence and chronic inflammation associated with parasitic infection. It has become evident that the type of microorganisms and the setting in which they trigger the Th17 response determines the outcome of the delicate balancethat exists between Th17 induced protection and immunopathogenesis.

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References

  1. Mosmann, T. R. and Coffman, R. L. (1989) TH1 and TH2 cells: different patterns of lymphokine secretion lead to different functional properties. Annu. Rev. Immunol. 7, 145-173 https://doi.org/10.1146/annurev.iy.07.040189.001045
  2. Park, H., Li, Z., Yang, X. O., Chang, S. H., Nurieva, R., Wang, Y. H., Wang, Y., Hood, L., Zhu, Z., Tian, Q. and Dong, C. (2005) A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6, 1133-1141 https://doi.org/10.1038/ni1261
  3. Locksley, R. M. (2009) Nine lives: plasticity among T helper cell subsets. J. Exp. Med. 206, 1643-1646 https://doi.org/10.1084/jem.20091442
  4. Ouyang, W., Kolls, J. K. and Zheng, Y. (2008) The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 28, 454-467 https://doi.org/10.1016/j.immuni.2008.03.004
  5. Grimbacher, B., Holland, S. M., Gallin, J. I., Greenberg, F., Hill, S. C., Malech, H. L., Miller, J. A., O'Connell, A. C. and Puck, J. M. (1999) Hyper-IgE syndrome with recurrent infections--an autosomal dominant multisystem disorder. N. Engl. J. Med. 340, 692-702 https://doi.org/10.1056/NEJM199903043400904
  6. Milner, J. D., Brenchley, J. M., Laurence, A., Freeman, A. F., Hill, B. J., Elias, K. M., Kanno, Y., Spalding, C., Elloumi, H. Z., Paulson, M. L., Davis, J., Hsu, A., Asher, A. I., O'Shea, J., Holland, S. M., Paul, W. E. and Douek, D. C. (2008) Impaired T(H)17 cell differentiation in subjects with autosomal dominant hyper-IgE syndrome. Nature 452, 773-776 https://doi.org/10.1038/nature06764
  7. Huang, W., Na, L., Fidel, P. L. and Schwarzenberger, P. (2004) Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice. J. Infect. Dis. 190, 624-631 https://doi.org/10.1086/422329
  8. Conti, H. R., Shen, F., Nayyar, N., Stocum, E., Sun, J. N., Lindemann, M. J., Ho, A. W., Hai, J. H., Yu, J. J., Jung, J. W., Filler, S. G., Masso-Welch, P., Edgerton, M. and Gaffen, S. L. (2009) Th17 cells and IL-17 receptor signalingare essential for mucosal host defense against oral candidiasis. J. Exp. Med. 206, 299-311 https://doi.org/10.1084/jem.20081463
  9. Zelante, T., De Luca, A., Bonifazi, P., Montagnoli, C., Bozza, S., Moretti,S., Belladonna, M. L., Vacca, C., Conte, C., Mosci, P., Bistoni, F., Puccetti,P., Kastelein, R. A., Kopf, M. and Romani, L. (2007) IL-23 and the Th17 pathway promote inflammation and impair antifungal immune resistance. Eur. J. Immunol. 37, 2695-2706 https://doi.org/10.1002/eji.200737409
  10. Bozza, S., Zelante, T., Moretti, S., Bonifazi, P., DeLuca, A., D'Angelo, C., Giovannini, G., Garlanda, C., Boon, L., Bistoni, F., Puccetti, P., Mantovani, A. and Romani, L. (2008) Lack of Toll IL-1R8 exacerbates Th17 cell responses in fungal infection. J. Immunol. 180, 4022-4031 https://doi.org/10.4049/jimmunol.180.6.4022
  11. Eyerich, K., Foerster, S., Rombold, S., Seidl, H. P., Behrendt H., Hofmann, H., Ring, J. and Traidl-Hoffmann, C. (2008) Patients with chronic mucocutaneous candidiasis exhibit reduced production of Th17-associated cytokines IL-17 and IL-22. J. Invest. Dermatol. 128, 2640-2645 https://doi.org/10.1038/jid.2008.139
  12. van de Veerdonk, F. L., Marijnissen, R. J., Kullberg, B. J., Koenen, H. J., Cheng, S. C., Joosten, I., van den Berg, W. B., Williams, D. L., van der Meer, J. W., Joosten, L. A. and Netea, M. G. (2009) The macrophage mannose receptorinduces IL-17 in response to Candida albicans. Cell Host Microbe 5, 329-340 https://doi.org/10.1016/j.chom.2009.02.006
  13. LeibundGut-Landmann, S., Gross, O., Robinson, M. J., Osorio, F., Slack, E. C., Tsoni, S. V., Schweighoffer, E., Tybulewicz, V., Brown, G. D., Ruland, J. and Reis e Sousa, C. (2007) Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat. Immunol. 8, 630-638 https://doi.org/10.1038/ni1460
  14. Robinson, M. J., Osorio, F., Rosas, M., Freitas, R. P., Schweighoffer, E., Gross, O., Verbeek, J. S., Ruland, J., Tybulewicz, V., Brown, G. D., Moita, L. F., Taylor, P. R. and Reis e Sousa, C. (2009) Dectin-2 is a Syk-coupled pattern ecognition receptor crucial for Th17 responses to fungal infection. J. Exp. Med. 206, 2037-2051 https://doi.org/10.1084/jem.20082818
  15. Glocker, E. O., Hennigs, A., Nabavi, M., Schaffer, A. A., Woellner, C., Salzer, U., Pfeifer, D., Veelken, H., Warnatz, K., Tahami, F., Jamal, S., Manguiat, A., Rezaei, N., Amirzargar, A. A., Plebani, A., Hannesschlager, N., Gross, O., Ruland, J. and Grimbacher, B. (2009) A homozygous CARD9 mutation in a family with susceptibility to fungal infections. N. Engl. J. Med. 361, 1727-1735 https://doi.org/10.1056/NEJMoa0810719
  16. Ferwerda, B., Ferwerda, G., Plantinga, T. S., Willment, J. A., van Spriel, A. B., Venselaar, H., Elbers, C. C., Johnson, M. D., Cambi, A., Huysamen, C., Jacobs, L., Jansen, T., Verheijen, K., Masthoff, L., Morre, S. A., Vriend, G., Williams, D. L., Perfect, J. R., Joosten, L. A., Wijmenga, C., van der Meer, J. W., Adema, G. J., Kullberg, B. J., Brown, G. D. and Netea, M. G. (2009) Human dectin-1 deficiency and mucocutaneous fungal infections. N. Engl. J. Med. 361, 1760-1767 https://doi.org/10.1056/NEJMoa0901053
  17. Romani, L., Fallarino, F., De Luca, A., Montagnoli, C., D'Angelo, C., Zelante, T., Vacca, C., Bistoni, F., Fioretti, M. C., Grohmann, U., Segal, B. H. and Puccetti, P. (2008) Defective tryptophan catabolism underlies inflammation in mouse chronic granulomatous disease. Nature 451, 211-215 https://doi.org/10.1038/nature06471
  18. Rudner, X. L., Happel, K. I., Young, E. A. and Shellito, J. E. (2007) Interleukin-23 (IL-23)-IL-17 cytokine axis in murine Pneumocystis carinii infection. Infect. Immun. 75, 3055-3061 https://doi.org/10.1128/IAI.01329-06
  19. Kleinschek, M. A., Muller, U., Brodie, S. J., Stenzel, W., Kohler, G., Blumenschein, W. M., Straubinger, R. K., McClanahan, T., Kastelein, R. A. and Alber, G. (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 https://doi.org/10.4049/jimmunol.176.2.1098
  20. Loures, F. V., Pina, A., Felonato, M. and Calich, V. L. (2009) TLR2 is a negative regulator of Th17 cells and tissue pathology in a pulmonary model of fungal infection. J. Immunol. 183, 1279-1290 https://doi.org/10.4049/jimmunol.0801599
  21. Infante-Duarte, C., Horton, H. F., Byrne, M. C. and Kamradt, T. (2000) Microbial lipopeptides induce the production of IL-17 in Th cells. J. Immunol. 165, 6107-6115 https://doi.org/10.4049/jimmunol.165.11.6107
  22. Knauer, J., Siegemund, S., Muller, U., Al-Robaiy, S., Kastelein, R. A., Alber, G. and Straubinger, R. K. (2007) Borrelia burgdorferi potently activates bone marrow-derived conventional dendritic cells for production of IL-23 required for IL-17 release by T cells. FEMS Immunol. Med. Microbiol. 49, 353-363 https://doi.org/10.1111/j.1574-695X.2006.00210.x
  23. Codolo, G., Amedei, A., Steere, A. C., Papinutto, E., Cappon, A., Polenghi, A., Benagiano, M., Paccani, S. R., Sambri, V., Del Prete, G., Baldari, C. T., Zanotti, G., Montecucco, C., D'Elios, M. M. and de Bernard, M. (2008) Borrelia burgdorferi NapA-driven Th17 cell inflammation in lyme arthritis. Arthritis. Rheum. 58, 3609-3617 https://doi.org/10.1002/art.23972
  24. Burchill, M. A., Nardelli, D. T., England, D. M., DeCoster, D. J., Christopherson, J. A., Callister, S. M. and Schell, R. F. (2003) Inhibition of interleukin-17 prevents the development of arthritis in vaccinated mice challenged with Borrelia burgdorferi. Infect. Immun. 71, 3437-3442 https://doi.org/10.1128/IAI.71.6.3437-3442.2003
  25. Kotloski, N. J., Nardelli, D. T., Peterson, S. H., Torrealba, J. R., Warner, T. F., Callister, S. M. and Schell, R. F. (2008) Interleukin-23 is required for development of arthritis in mice vaccinated and challenged with Borrelia Species. Clin. Vaccine Immunol. 15, 1199-1207 https://doi.org/10.1128/CVI.00129-08
  26. Luzza, F., Parrello, T., Monteleone, G., Sebkova, L., Romano, M., Zarrilli, R., Imeneo, M. and Pallone, F. (2000) Up-regulation of IL-17 is associated with bioactive IL-8 expression in Helicobacter pylori-infected human gastric mucosa. J. Immunol. 165, 5332-5337 https://doi.org/10.4049/jimmunol.165.9.5332
  27. Caruso, R., Fina, D., Paoluzi, O. A., Del Vecchio Blanco, G., Stolfi, C., Rizzo, A., Caprioli, F., Sarra, M., Andrei, F., Fantini, M. C., MacDonald, T. T., Pallone, F. and Monteleone, G. (2008) IL-23-mediated regulation of IL-17 production in Helicobacter pylori-infected gastric mucosa. Eur. J. Immunol. 38, 470-478 https://doi.org/10.1002/eji.200737635
  28. Otani, K., Watanabe, T., Tanigawa, T., Okazaki, H., Yamagami, H., Watanabe, K., Tominaga, K., Fujiwara, Y., Oshitani, N. and Arakawa, T. (2009) Anti-inflammatory effects of IL-17A on Helicobacter pylori-induced gastritis. Biochem. Biophys. Res. Commun. 382, 252-258 https://doi.org/10.1016/j.bbrc.2009.02.107
  29. Algood, H. M., Allen, S. S., Washington, M. K., Peek, R. M., Jr., Miller, G. G. and Cover, T. L. (2009) Regulation of gastric b cell recruitment is dependent on IL-17 receptor a signaling in a model of chronic bacterial infection. J. Immunol. 183, 5837-5846 https://doi.org/10.4049/jimmunol.0901206
  30. Ye, P., Garvey, P. B., Zhang, P., Nelson, S., Bagby, G., Summer, W. R., Schwarzenberger, P., Shellito, J. E. and Kolls, J. K. (2001) Interleukin-17 and lung host defense against Klebsiella pneumoniae infection. Am. J. Respir. Cell. Mol. Biol. 25, 335-340 https://doi.org/10.1165/ajrcmb.25.3.4424
  31. Happel, K. I., Zheng, M., Young, E., Quinton, L. J., Lockhart, E., Ramsay, A. J., Shellito, J. E., Schurr, J. R., Bagby, G. J., Nelson, S. and Kolls, J. K. (2003) Cutting edge: roles of Toll-like receptor 4 and IL-23 in IL-17 xpression in response to Klebsiella pneumoniae infection. J. Immunol. 170, 4432-4436 https://doi.org/10.4049/jimmunol.170.9.4432
  32. Happel, K. I., Dubin, P. J., Zheng, M., Ghilardi, N., Lockhart, C., Quinton, L. J., Odden, A. R., Shellito, J. E., Bagby, G. J., Nelson, S. and Kolls, J. K. (2005) Divergent roles of IL-23 and IL-12 in host defense against Klebsiella pneumoniae. J. Exp. Med. 202, 761-769 https://doi.org/10.1084/jem.20050193
  33. Aujla, S. J., Chan, Y. R., Zheng, M., Fei, M., Askew, D. J., Pociask, D. A., Reinhart, T. A., McAllister, F., Edeal, J., Gaus, K., Husain, S., Kreindler, J. L., Dubin, P. J., Pilewski, J. M., Myerburg, M. M., Mason, C. A., Iwakura, Y. and Kolls, J. K. (2008) IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia. Nat. Med. 14, 275-281 https://doi.org/10.1038/nm1710
  34. Chan, Y. R., Liu, J. S., Pociask, D. A., Zheng, M., Mietzner, T. A., Berger, T., Mak, T. W., Clifton, M. C., Strong, R. K., Ray, P. and Kolls, J. K. (2009) Lipocalin 2 is required for pulmonary host defense against Klebsiella infection. J. Immunol. 182, 4947-4956 https://doi.org/10.4049/jimmunol.0803282
  35. Mangan, P. R., Harrington, L. E., O'Quinn, D. B., Helms, W. S., Bullard, D. C., Elson, C. O., Hatton, R. D., Wahl, S. M., Schoeb, T. R. and Weaver, C. T. (2006) Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 441, 231-234 https://doi.org/10.1038/nature04754
  36. Ishigame, H., Kakuta, S., Nagai, T., Kadoki, M., Nambu, A., Komiyama, Y., Fujikado, N., Tanahashi, Y., Akitsu, A., Kotaki, H., Sudo, K., Nakae, S., Sasakawa, C. and Iwakura, Y. (2009) Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 30, 108-119 https://doi.org/10.1016/j.immuni.2008.11.009
  37. Zheng, Y., Valdez, P. A., Danilenko, D. M., Hu, Y., Sa, S. M., Gong, Q., Abbas, A. R., Modrusan, Z., Ghilardi, N., de Sauvage, F. J. and Ouyang, W. (2008) Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 14, 282-289 https://doi.org/10.1038/nm1720
  38. Ivanov, II, Frutos Rde, L., Manel, N., Yoshinaga, K., Rifkin, D. B., Sartor, R. B., Finlay, B. B. and Littman, D. R. (2008) Specific microbiota direct the differentiation of IL-17-producing Thelper cells in the mucosa of the small intestine. Cell Host Microbe. 4, 337-349 https://doi.org/10.1016/j.chom.2008.09.009
  39. Ivanov, II, Atarashi, K., Manel, N., Brodie, E. L., Shima, T., Karaoz, U., Wei, D., Goldfarb, K. C., Santee, C. A., Lynch, S. V., Tanoue, T., Imaoka, A., Itoh, K., Takeda, K., Umesaki, Y., Honda, K. and Littman, D. R. (2009) Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell. 139, 485-498 https://doi.org/10.1016/j.cell.2009.09.033
  40. Raffatellu, M., Santos, R. L., Chessa, D., Wilson, R. P., Winter, S. E., Rossetti, C. A., Lawhon, S. D., Chu, H., Lau, T., Bevins, C. L., Adams, L. G. and Baumler, A. J. (2007) The capsule encoding the viaB locus reduces interleukin-17 expression and mucosal innate responses in the bovine intestinal mucosa during infection with Salmonella enterica serotype Typhi. Infect. Immun. 75, 4342-4350 https://doi.org/10.1128/IAI.01571-06
  41. Godinez, I., Raffatellu, M., Chu, H., Paixao, T. A., Haneda, T., Santos, R. L., Bevins, C. L., Tsolis, R. M. and Baumler, A. J. (2009) Interleukin-23 orchestrates mucosal responses to Salmonella enterica serotype Typhimurium in the intestine. Infect. Immun. 77, 387-398 https://doi.org/10.1128/IAI.00933-08
  42. Schulz, S. M., Kohler, G., Schutze, N., Knauer, J., Straubinger, R. K., Chackerian, A. A., Witte, E., Wolk, K., Sabat, R., Iwakura, Y., Holscher, C., Muller, U., Kastelein, R. A. and Alber, G. (2008) Protective immunity to systemic infection with attenuated Salmonella enterica serovar enteritidis in the absence of IL-12 is associated with IL-23-dependent IL-22, but not IL-17. J. Immunol. 181, 7891-7901 https://doi.org/10.4049/jimmunol.181.11.7891
  43. Raffatellu, M., Santos, R. L., Verhoeven, D. E., George, M D., Wilson, R. P., Winter, S. E., Godinez, I., Sankaran, S., Paixao, T. A., Gordon, M. A., Kolls, J. K., Dandekar, S. and Baumler, A. J. (2008) Simian immunodeficiency virus-induced mucosal interleukin-17 deficiency promotes Salmonella dissemination from the gut. Nat. Med. 14, 421-428 https://doi.org/10.1038/nm1743
  44. Glaser, J. B., Morton-Kute, L., Berger, S. R., Weber, J., Siegal, F. P., Lopez, C., Robbins, W. and Landesman, S. H. (1985) Recurrent Salmonella typhimurium bacteremia associated with the acquired immunodeficiency syndrome. Ann. Intern. Med. 102, 189-193 https://doi.org/10.7326/0003-4819-102-2-189
  45. Khader, S. A., Pearl, J. E., Sakamoto, K., Gilmartin, L., Bell, G. K., Jelley-Gibbs, D. M., Ghilardi, N., deSauvage, F. and Cooper, A. M. (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 https://doi.org/10.4049/jimmunol.175.2.788
  46. Cruz, A., Khader, S. A., Torrado, E., Fraga, A., Pearl, J. E., Pedrosa, J., Cooper, A. M. and Castro, A. G. (2006) Cutting edge: IFN-gamma regulates the induction and expansion of IL-17-producing CD4 T cells during mycobacterial infection. J. Immunol. 177, 1416-1420 https://doi.org/10.4049/jimmunol.177.3.1416
  47. Aujla, S. J., Dubin, P. J. and Kolls, J. K. (2007) Th17 cells and mucosal host defense. Semin. Immunol. 19, 377-382 https://doi.org/10.1016/j.smim.2007.10.009
  48. Khader, S. A. and Cooper, A. M. (2008) IL-23 and IL-17 in tuberculosis. Cytokine. 41, 79-83 https://doi.org/10.1016/j.cyto.2007.11.022
  49. Umemura, M., Yahagi, A., Hamada, S., Begum, M. D., Watanabe, H., Kawakami, K., Suda, T., Sudo, K., Nakae, S., Iwakura, Y. and Matsuzaki, G. (2007) IL-17-mediated regulation of innate and acquired immune response against pulmonary Mycobacterium bovis bacille Calmette-Guerin infection. J. Immunol. 178, 3786-3796 https://doi.org/10.4049/jimmunol.178.6.3786
  50. Mills, K. H. (2001) Immunity to Bordetella pertussis. Microbes. Infect. 3, 655-677 https://doi.org/10.1016/S1286-4579(01)01421-6
  51. Higgins, S. C., Jarnicki, A. G., Lavelle, E. C. and Mills, K. H. (2006) TLR4 mediates vaccine-induced protective cellular immunity to Bordetella pertussis: role of IL-17-producing T cells. J. Immunol. 177, 7980-7989 https://doi.org/10.4049/jimmunol.177.11.7980
  52. Andreasen, C., Powell, D. A. and Carbonetti, N. H. (2009) Pertussis toxin stimulates IL-17 production in response to Bordetella pertussis infection in mice. PLoS One 4, e7079 https://doi.org/10.1371/journal.pone.0007079
  53. Siciliano, N. A., Skinner, J. A. and Yuk, M. H. (2006) Bordetella bronchiseptica modulates macrophage phenotype leading to the inhibition of CD4+ T cell proliferation and the initiation of a Th17 immune response. J. Immunol. 177, 7131-7138 https://doi.org/10.4049/jimmunol.177.10.7131
  54. Oda, T., Yoshie, H. and Yamazaki, K. (2003) Porphyromonas gingivalis antigen preferentially stimulates T cells to express IL-17 but not receptor activator of NF-kappaB ligand in vitro. Oral Microbiol. Immunol. 18, 30-36 https://doi.org/10.1034/j.1399-302X.2003.180105.x
  55. Yu, J. J., Ruddy, M. J., Wong, G. C., Sfintescu, C., Baker, P. J., Smith, J. B., Evans, R. T. and Gaffen, S. L. (2007) An essential role for IL-17 in preventing pathogen-initiated bone destruction: recruitment of neutrophils to inflamedbone requires IL-17 receptor-dependent signals. Blood 109, 3794-3802 https://doi.org/10.1182/blood-2005-09-010116
  56. Wu, Q., Martin, R. J., Rino, J. G., Breed, R., Torres, R. M. and Chu, H. W. (2007) IL-23-dependent IL-17 production is essential in neutrophil recruitment and activity in mouse lung defense against respiratory Mycoplasma pneumoniae infection. Microbes. Infect. 9, 78-86 https://doi.org/10.1016/j.micinf.2006.10.012
  57. Stern, R. C. (1997) The diagnosis of cystic fibrosis. N. Engl. J. Med. 336, 487-491 https://doi.org/10.1056/NEJM199702133360707
  58. McAllister, F., Henry, A., Kreindler, J. L., Dubin, P. J., Ulrich, L., Steele, C., Finder, J. D., Pilewski, J. M., Carreno, B. M., Goldman, S. J., Pirhonen, J. and Kolls, J. K. (2005) Role of IL-17A, IL-17F, and the IL-17 receptor in regulating growth-related oncogene-alpha and granulocyte colony-stimulating factor in bronchial epithelium: implications for airway inflammation in cystic fibrosis. J. Immunol. 175, 404-412 https://doi.org/10.4049/jimmunol.175.1.404
  59. Dubin, P. J. and Kolls, J. K. (2007) IL-23 mediates inflammatory responses to mucoid Pseudomonas aeruginosa lung infection in mice. Am. J. Physiol. Lung. Cell. Mol. Physiol. 292, L519-528 https://doi.org/10.1152/ajplung.00312.2006
  60. Priebe, G. P., Walsh, R. L., Cederroth, T. A., Kamei, A., Coutinho-Sledge, Y. S., Goldberg, J. B. and Pier, G. B. (2008) IL-17 is a critical component of vaccine-induced protection against lung infection by lipopolysaccharideheterologous strains of Pseudomonas aeruginosa. J. Immunol. 181, 4965-4975 https://doi.org/10.4049/jimmunol.181.7.4965
  61. Chung, D. R., Kasper, D. L., Panzo, R. J., Chitnis, T., Grusby, M. J., Sayegh, M. H. and Tzianabos, A. O. (2003) CD4+ T cells mediate abscess formation in intra-abdominal sepsis by an IL-17-dependent mechanism. J. Immunol. 170, 1958-1963 https://doi.org/10.4049/jimmunol.170.4.1958
  62. Holland, S. M., DeLeo, F. R., Elloumi, H. Z., Hsu, A. P., Uzel, G., Brodsky, N., Freeman, A. F., Demidowich, A., Davis, J., Turner, M. L., Anderson, V. L., Darnell, D. N., Welch, P. A., Kuhns, D. B., Frucht, D. M., Malech, H. L., Gallin, J. I., Kobayashi, S. D., Whitney, A. R., Voyich, J. M., Musser, J. M., Woellner, C., Schaffer, A. A., Puck, J. M. and Grimbacher, B. (2007) STAT3 mutations in the hyper-IgE syndrome. N. Engl. J. Med. 357, 1608-1619 https://doi.org/10.1056/NEJMoa073687
  63. Ma, C. S., Chew, G. Y., Simpson, N., Priyadarshi, A., Wong, M., Grimbacher, B., Fulcher, D. A., Tangye, S. G. and Cook, M. C. (2008) Deficiency of Th17 cells in hyper IgE syndrome due to mutations in STAT3. J. Exp. Med. 205, 1551-1557 https://doi.org/10.1084/jem.20080218
  64. Minegishi, Y., Saito, M., Nagasawa, M., Takada, H., Hara, T., Tsuchiya, S., Agematsu, K., Yamada, M., Kawamura, N., Ariga, T., Tsuge, I. and Karasuyama, H. (2009) Molecular explanation for the contradiction between systemic Th17 defect and localized bacterial infection in hyper-IgE syndrome. J. Exp. Med. 206, 1291-1301 https://doi.org/10.1084/jem.20082767
  65. Lockhart, E., Green, A. M. and Flynn, J. L. (2006) IL-17 production is dominated by gammadelta T cells rather than CD4 T cells during Mycobacterium tuberculosis infection. J. Immunol. 177, 4662-4669 https://doi.org/10.4049/jimmunol.177.7.4662
  66. Peng, M. Y., Wang, Z. H., Yao, C. Y., Jiang, L. N., Jin, Q. L., Wang, J. and Li, B. Q. (2008) Interleukin 17-producing gamma delta T cells increased in patients with active pulmonary tuberculosis. Cell Mol. Immunol. 5, 203-208 https://doi.org/10.1038/cmi.2008.25
  67. Hamada, S., Umemura, M., Shiono, T., Hara, H., Kishihara, K., Tanaka, K., Mayuzumi, H., Ohta, T. and Matsuzaki, G. (2008) Importance of murine Vdelta1gammadelta T cells expressing interferon-gamma and interleukin-17A in innate protection against Listeria monocytogenes infection. Immunology 125, 170-177 https://doi.org/10.1111/j.1365-2567.2008.02841.x
  68. Hamada, S., Umemura, M., Shiono, T., Tanaka, K., Yahagi, A., Begum, M. D., Oshiro, K., Okamoto, Y., Watanabe, H., Kawakami, K., Roark, C., Born, W. K., O'Brien, R., Ikuta, K., Ishikawa, H., Nakae, S., Iwakura, Y., Ohta, T. and Matsuzaki, G. (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 https://doi.org/10.4049/jimmunol.181.5.3456
  69. Shibata, K., Yamada, H., Hara, H., Kishihara, K. and Yoshikai, Y. (2007) Resident Vdelta1+ gammadelta T cells control early infiltration of neutrophils after Escherichia coli infection via IL-17 production. J. Immunol. 178, 4466-4472 https://doi.org/10.4049/jimmunol.178.7.4466
  70. Martin, B., Hirota, K., Cua, D. J., Stockinger, B. and Veldhoen, M. (2009) Interleukin-17-producing gammadelta T cells selectively expand in response to pathogen products and environmental signals. Immunity 31, 321-330 https://doi.org/10.1016/j.immuni.2009.06.020
  71. Patera, A. C., Pesnicak, L., Bertin, J. and Cohen, J. I. (2002) Interleukin 17 modulates the immune response to vaccinia virus infection. Virology 299, 56-63 https://doi.org/10.1006/viro.2002.1400
  72. Kohyama, S., Ohno, S., Isoda, A., Moriya, O., Belladonna, M. L., Hayashi, H., Iwakura, Y., Yoshimoto, T., Akatsuka, T. and Matsui, M. (2007) IL-23 enhances host defense against vaccinia virus infection via a mechanism partly involving IL-17. J. Immunol. 179, 3917-3925 https://doi.org/10.4049/jimmunol.179.6.3917
  73. Kawakami, Y., Tomimori, Y., Yumoto, K., Hasegawa, S., Ando, T., Tagaya, Y., Crotty, S. and Kawakami, T. (2009) Inhibition of NK cell activity by IL-17 allows vaccinia virus to induce severe skin lesions in a mouse model of eczema vaccinatum. J. Exp. Med. 206, 1219-1225 https://doi.org/10.1084/jem.20082835
  74. Oyoshi, M. K., Elkhal, A., Kumar, L., Scott, J. E., Koduru, S., He, R., Leung, D. Y., Howell, M. D., Oettgen, H. C., Murphy, G. F. and Geha, R. S. (2009) Vaccinia virus inoculation in sites of allergic skin inflammation elicits avigorous cutaneous IL-17 response. Proc. Natl. Acad. Sci. U.S.A. 106, 14954-14959 https://doi.org/10.1073/pnas.0904021106
  75. Petro, T. M. (2005) ERK-MAP-kinases differentially regulate expression of IL-23 p19 compared with p40 and IFN-beta in Theiler's virus-infected RAW264.7 cells.Immunol. Lett. 97, 47-53 https://doi.org/10.1016/j.imlet.2004.09.013
  76. Hou, W., Kang, H. S. and Kim, B. S. (2009) Th17 cells enhance viral persistence and inhibit T cell cytotoxicity in a model of chronic virus infection. J. Exp. Med. 206, 313-328 https://doi.org/10.1084/jem.20082030
  77. Maertzdorf, J., Osterhaus, A. D. and Verjans, G. M. (2002) IL-17 expression in human herpetic stromal keratitis: modulatory effects on chemokine production by corneal fibroblasts. J. Immunol. 169, 5897-5903 https://doi.org/10.4049/jimmunol.169.10.5897
  78. Molesworth-Kenyon, S. J., Yin, R., Oakes, J. E. and Lausch, R. N. (2008) IL-17 receptor signaling influences virus-induced corneal inflammation. J. Leukoc. Biol. 83, 401-408 https://doi.org/10.1189/jlb.0807571
  79. Kim, B., Sarangi, P. P., Azkur, A. K., Kaistha, S. D. and Rouse, B. T. (2008) Enhanced viral immunoinflammatory lesions in mice lacking IL-23 responses. Microbes. Infect. 10, 302-312 https://doi.org/10.1016/j.micinf.2007.12.007
  80. Maek, A. N. W., Buranapraditkun, S., Klaewsongkram, J. and Ruxrungtham, K. (2007) Increased interleukin-17 production both in helper T cell subset Th17 and CD4-negative T cells in human immunodeficiency virus infection. Viral. Immunol. 20, 66-75 https://doi.org/10.1089/vim.2006.0063
  81. Misse, D., Yssel, H., Trabattoni, D., Oblet, C., Lo Caputo, S., Mazzotta, F., Pene, J., Gonzalez, J. P., Clerici, M. and Veas, F. (2007) IL-22 participates in an innate anti-HIV-1 host-resistance network through acute-phase protein induction. J. Immunol. 178, 407-415 https://doi.org/10.4049/jimmunol.178.1.407
  82. Rowan, A. G., Fletcher, J. M., Ryan, E. J., Moran, B., Hegarty, J. E., O'Farrelly, C. and Mills, K. H. (2008) Hepatitis C virus-specific Th17 cells are suppressed by virus-induced TGF-beta. J. Immunol. 181, 4485-4494 https://doi.org/10.4049/jimmunol.181.7.4485
  83. Ge, J., Wang, K., Meng, Q. H., Qi, Z. X., Meng, F. L. and Fan, Y. C. (2009) Implication of Th17 and Th1 Cells in Patients with Chronic Active Hepatitis B. J. Clin. Immunol
  84. Zenewicz, L. A., Yancopoulos, G. D., Valenzuela, D. M., Murphy, A. J., Karow, M. and Flavell, R. A. (2007) Interleukin-22 but not interleukin-17 provides protection to hepatocytes during acute liver inflammation. Immunity 27, 647-659 https://doi.org/10.1016/j.immuni.2007.07.023
  85. Intlekofer, A. M., Banerjee, A., Takemoto, N., Gordon, S. M., Dejong, C. S., Shin, H., Hunter, C. A., Wherry, E. J., Lindsten, T. and Reiner, S. L. (2008) Anomalous type 17 response to viral infection by CD8+ T cells lacking T-bet and eomesodermin. Science 321, 408-411 https://doi.org/10.1126/science.1159806
  86. Dodon, M. D., Li, Z., Hamaia, S. and Gazzolo, L. (2004) Tax protein of human T-cell leukaemia virus type 1 induces interleukin 17 gene expression in T cells. J. Gen. Virol. 85, 1921-1932 https://doi.org/10.1099/vir.0.79921-0
  87. Wiehler, S. and Proud, D. (2007) Interleukin-17A modulates human airway epithelial responses to human rhinovirus infection. Am. J. Physiol. Lung. Cell. Mol. Physiol. 293, L505-515 https://doi.org/10.1152/ajplung.00066.2007
  88. McKinstry, K. K., Strutt, T. M., Buck, A., Curtis, J. D., Dibble, J. P., Huston, G., Tighe, M., Hamada, H., Sell, S., Dutton, R. W. and Swain, S. L. (2009) IL-10 deficiency unleashes an influenza-specific Th17 response and enhances survival against high-dose challenge. J. Immunol. 182, 7353-7363 https://doi.org/10.4049/jimmunol.0900657
  89. Kelly, M. N., Kolls, J. K., Happel, K., Schwartzman, J. D., Schwarzenberger, P., Combe, C., Moretto, M. and Khan, I. A. (2005) Interleukin-17/interleukin-17 receptor-mediated signaling is important for generation of an optimal polymorphonuclear response against Toxoplasma gondii infection. Infect. Immun. 73, 617-621 https://doi.org/10.1128/IAI.73.1.617-621.2005
  90. Stumhofer, J. S., Laurence, A., Wilson, E. H., Huang, E., Tato, C. M., Johnson, L. M., Villarino, A. V., Huang, Q., Yoshimura, A., Sehy, D., Saris, C. J., O'Shea, J. J., Hennighausen, L., Ernst, M. and Hunter, C. A. (2006) Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic inflammation of the central nervous system. Nat. Immunol. 7, 937-945 https://doi.org/10.1038/ni1376
  91. Yoshida, H. and Miyazaki, Y. (2008) Regulation of immune responses by interleukin-27. Immunol. Rev. 226, 234-247 https://doi.org/10.1111/j.1600-065X.2008.00710.x
  92. Pitta, M. G., Romano, A., Cabantous, S., Henri, S., Hammad, A., Kouriba, B., Argiro, L., el Kheir, M., Bucheton, B., Mary, C., El-Safi, S. H. and Dessein, A. (2009) IL-17 and IL-22 are associated with protection against human kala azar caused by Leishmania donovani. J. Clin. Invest. 119, 2379-2387
  93. Anderson, C. F., Stumhofer, J. S., Hunter, C. A. and Sacks, D. (2009) IL-27 regulates IL-10 and IL-17 from CD4+ cells in nonhealing Leishmania major infection. J. Immunol. 183, 4619-4627 https://doi.org/10.4049/jimmunol.0804024
  94. Monteiro, A. C., Schmitz, V., Morrot, A., de Arruda, L. B., Nagajyothi, F., Granato, A., Pesquero, J. B., Muller-Esterl, W., Tanowitz, H. B. and Scharfstein, J. (2007) Bradykinin B2 Receptors of dendritic cells, acting as sensors of kinins proteolytically released by Trypanosoma cruzi, are critical for the development of protective type-1 responses. PLoS Pathog. 3, e185 https://doi.org/10.1371/journal.ppat.0030185
  95. Vargas-Inchaustegui, D. A., Xin, L. and Soong, L. (2008) Leishmania braziliensis infection induces dendritic cell activation, ISG15 transcription, and the generation of protective immune responses. J. Immunol. 180, 7537-7545 https://doi.org/10.4049/jimmunol.180.11.7537
  96. Rutitzky, L. I., Lopes da Rosa, J. R. and Stadecker, M. J. (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- 3926 https://doi.org/10.4049/jimmunol.175.6.3920
  97. Rutitzky, L. I. and Stadecker, M. J. (2006) CD4 T cells producing pro-inflammatory interleukin-17 mediate high pathology in schistosomiasis. Mem. Inst. Oswaldo. Cruz. 101(Suppl 1), 327-330
  98. Tallima, H., Salah, M., Guirguis, F. R. and El Ridi, R. (2009) Transforming growth factor-beta and Th17 responses in resistance to primary murine schistosomiasis mansoni. Cytokine. 48, 239-245 https://doi.org/10.1016/j.cyto.2009.07.581
  99. Owyang, A. M., Zaph, C., Wilson, E. H., Guild, K. J., McClanahan, T., Miller, H. R., Cua, D. J., Goldschmidt, M., Hunter, C. A., Kastelein, R. A. and Artis, D. (2006) Interleukin 25 regulates type 2 cytokine-dependent immunity and limits chronic inflammation in the gastrointestinal tract. J. Exp. Med. 203, 843-849 https://doi.org/10.1084/jem.20051496
  100. Ehigiator, H. N., McNair, N. and Mead, J. R. (2007) Cryptosporidium parvum: the contribution of Th1-inducing pathways to the resolution of infection in mice. Exp. Parasitol. 115, 107-113 https://doi.org/10.1016/j.exppara.2006.07.001

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