Table of Contents Author Guidelines Submit a Manuscript
Journal of Biomedicine and Biotechnology
Volume 2007, Article ID 79401, 7 pages
http://dx.doi.org/10.1155/2007/79401
Review Article

Regulation of Defense Responses against Protozoan Infection by Interleukin-27 and Related Cytokines

1Department of Biomolecular Sciences, Faculty of Medicine, Saga University, Saga 849-8501, Japan
2Department of Parasitology, Graduate School of Medical Sciences, Kyushu University, Fukuoka 812-8582, Japan

Received 26 November 2006; Revised 2 February 2007; Accepted 26 February 2007

Academic Editor: Ali Ouaissi

Copyright © 2007 Hiroki Yoshida et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. Sacks and N. Noben-Trauth, “The immunology of susceptibility and resistance to Leishmania major in mice,” Nature Reviews Immunology, vol. 2, no. 11, pp. 845–858, 2002. View at Publisher · View at Google Scholar
  2. E. van de Vosse, M. A. Hoeve, and T. H. M. Ottenhoff, “Human genetics of intracellular infectious diseases: molecular and cellular immunity against mycobacteria and salmonellae,” Lancet Infectious Diseases, vol. 4, no. 12, pp. 739–749, 2004. View at Publisher · View at Google Scholar
  3. T. R. Mosmann and S. Sad, “The expanding universe of T-cell subsets: Th1, Th2 and more,” Immunology Today, vol. 17, no. 3, pp. 138–146, 1996. View at Publisher · View at Google Scholar
  4. S. L. Reiner and R. M. Locksley, “The regulation of immunity to Leishmania major,” Annual Review of Immunology, vol. 13, pp. 151–177, 1995. View at Publisher · View at Google Scholar
  5. F. D. Finkelman, T. Shea-Donohue, J. Goldhill et al., “Cytokine regulation of host defense against parasitic gastrointestinal nematodes: lessons from studies with rodent models,” Annual Review of Immunology, vol. 15, pp. 505–533, 1997. View at Publisher · View at Google Scholar
  6. K. M. Murphy, W. Ouyang, J. D. Farrar et al., “Signaling and transcription in T helper development,” Annual Review of Immunology, vol. 18, pp. 451–494, 2000. View at Publisher · View at Google Scholar
  7. C. L. Langrish, Y. Chen, W. M. Blumenschein et al., “IL-23 drives a pathogenic T cell population that induces autoimmune inflammation,” Journal of Experimental Medicine, vol. 201, no. 2, pp. 233–240, 2005. View at Publisher · View at Google Scholar
  8. H. Park, Z. Li, X. O. Yang et al., “A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17,” Nature Immunology, vol. 6, no. 11, pp. 1133–1141, 2005. View at Publisher · View at Google Scholar
  9. L. E. Harrington, R. D. Hatton, P. R. Mangan et al., “Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages,” Nature Immunology, vol. 6, no. 11, pp. 1123–1132, 2005. View at Publisher · View at Google Scholar
  10. A. C. Patera, L. Pesnicak, J. Bertin, and J. I. Cohen, “Interleukin 17 modulates the immune response to vaccinia virus infection,” Virology, vol. 299, no. 1, pp. 56–63, 2002. View at Publisher · View at Google Scholar
  11. P. Ye, P. B. Garvey, P. Zhang et al., “Interleukin-17 and lung host defense against Klebsiella pneumoniae infection,” American Journal of Respiratory Cell and Molecular Biology, vol. 25, no. 3, pp. 335–340, 2001. View at Google Scholar
  12. E. Bettelli, Y. Carrier, W. Gao et al., “Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells,” Nature, vol. 441, no. 7090, pp. 235–238, 2006. View at Publisher · View at Google Scholar
  13. M. Veldhoen, R. J. Hocking, C. J. Atkins, R. M. Locksley, and B. Stockinger, “TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells,” Immunity, vol. 24, no. 2, pp. 179–189, 2006. View at Publisher · View at Google Scholar
  14. C. Sutton, C. Brereton, B. Keogh, K. H. G. Mills, and E. C. Lavelle, “A crucial role for interleukin (IL)-1 in the induction of IL-17-producing T cells that mediate autoimmune encephalomyelitis,” Journal of Experimental Medicine, vol. 203, no. 7, pp. 1685–1691, 2006. View at Publisher · View at Google Scholar
  15. G. Trinchieri, “Interleukin-12 and the regulation of innate resistance and adaptive immunity,” Nature Reviews Immunology, vol. 3, no. 2, pp. 133–146, 2003. View at Publisher · View at Google Scholar
  16. S. Pflanz, J. C. Timans, J. Cheung et al., “IL-27, a heterodimeric cytokine composed of EBI3 and p28 protein, induces proliferation of naïve CD4+ T cells,” Immunity, vol. 16, no. 6, pp. 779–790, 2002. View at Publisher · View at Google Scholar
  17. B. Oppmann, R. Lesley, B. Blom 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, vol. 13, no. 5, pp. 715–725, 2000. View at Publisher · View at Google Scholar
  18. A. V. Villarino, E. Huang, and C. A. Hunter, “Understanding the pro- and anti-inflammatory properties of IL-27,” Journal of Immunology, vol. 173, no. 2, pp. 715–720, 2004. View at Google Scholar
  19. C. A. Hunter, “New IL-12-family members: IL-23 and IL-27, cytokines with divergent functions,” Nature Reviews Immunology, vol. 5, no. 7, pp. 521–531, 2005. View at Publisher · View at Google Scholar
  20. G. Trinchieri, S. Pflanz, and R. A. Kastelein, “The IL-12 family of heterodimeric cytokines: new players in the regulation of T cell responses,” Immunity, vol. 19, no. 5, pp. 641–644, 2003. View at Publisher · View at Google Scholar
  21. O. Devergne, M. Hummel, H. Koeppen et al., “A novel interleukin-12 p40-related protein induced by latent Epstein-Barr virus infection in B lymphocytes,” Journal of Virology, vol. 70, no. 2, pp. 1143–1153, 1996. View at Google Scholar
  22. L. Romani, P. Puccetti, and F. Bistoni, “Interleukin-12 in infectious diseases,” Clinical Microbiology Reviews, vol. 10, no. 4, pp. 611–636, 1997. View at Google Scholar
  23. M. P. Colombo and G. Trinchieri, “Interleukin-12 in anti-tumor immunity and immunotherapy,” Cytokine and Growth Factor Reviews, vol. 13, no. 2, pp. 155–168, 2002. View at Publisher · View at Google Scholar
  24. B. Y. Kang and T. S. Kim, “Targeting cytokines of the interleukin-12 family in autoimmunity,” Current Medicinal Chemistry, vol. 13, no. 10, pp. 1149–1156, 2006. View at Publisher · View at Google Scholar
  25. B. Skurkovich and S. Skurkovich, “Inhibition of IFN-γ as a method of treatment of various autoimmune diseases, including skin diseases,” Ernst Schering Research Foundation Workshop, no. 56, pp. 1–27, 2006. View at Google Scholar
  26. Y. Iwakura and H. Ishigame, “The IL-23/IL-17 axis in inflammation,” Journal of Clinical Investigation, vol. 116, no. 5, pp. 1218–1222, 2006. View at Publisher · View at Google Scholar
  27. B. S. McKenzie, R. A. Kastelein, and D. J. Cua, “Understanding the IL-23-IL-17 immune pathway,” Trends in Immunology, vol. 27, no. 1, pp. 17–23, 2006. View at Publisher · View at Google Scholar
  28. D. S. Robinson and A. O'Garra, “Further checkpoints in Th1 development,” Immunity, vol. 16, no. 6, pp. 755–758, 2002. View at Publisher · View at Google Scholar
  29. H. Yoshida, S. Hamano, G. Senaldi et al., “WSX-1 is required for the initiation of Th1 responses and resistance to L. major infection,” Immunity, vol. 15, no. 4, pp. 569–578, 2001. View at Publisher · View at Google Scholar
  30. S. Hamano, K. Himeno, Y. Miyazaki et al., “WSX-1 is required for resistance to Trypanosoma cruzi infection by regulation of proinflammatory cytokine production,” Immunity, vol. 19, no. 5, pp. 657–667, 2003. View at Publisher · View at Google Scholar
  31. A. Villarino, L. Hibbert, L. Lieberman et al., “The IL-27R (WSX-1) is required to suppress T cell hyperactivity during infection,” Immunity, vol. 19, no. 5, pp. 645–655, 2003. View at Publisher · View at Google Scholar
  32. L. E. Rosas, A. A. Satoskar, K. M. Roth et al., “Interleukin-27R (WSX-1/T-cell cytokine receptor) gene-deficient mice display enhanced resistance to Leishmania donovani infection but develop severe liver immunopathology,” American Journal of Pathology, vol. 168, no. 1, pp. 158–169, 2006. View at Publisher · View at Google Scholar
  33. J. S. Stumhofer, A. Laurence, E. H. Wilson et al., “Interleukin 27 negatively regulates the development of interleukin 17-producing T helper cells during chronic inflammation of the central nervous system,” Nature Immunology, vol. 7, no. 9, pp. 937–945, 2006. View at Publisher · View at Google Scholar
  34. S. Zahn, S. Wirtz, M. Birkenbach, R. S. Blumberg, M. F. Neurath, and E. von Stebut, “Impaired Th1 responses in mice deficient in Epstein-Barr virus-induced gene 3 and challenged with physiological doses of Leishmania major,” European Journal of Immunology, vol. 35, no. 4, pp. 1106–1112, 2005. View at Publisher · View at Google Scholar
  35. A. J. Bancroft, N. E. Humphreys, J. J. Worthington, H. Yoshida, and R. K. Grencis, “WSX-1: a key role in induction of chronic intestinal nematode infection,” Journal of Immunology, vol. 172, no. 12, pp. 7635–7641, 2004. View at Google Scholar
  36. D. Artis, A. Villarino, M. Silverman et al., “The IL-27 receptor (WSX-1) is an inhibitor of innate and adaptive elements of type 2 immunity,” Journal of Immunology, vol. 173, no. 9, pp. 5626–5634, 2004. View at Google Scholar
  37. Q. Chen, N. Ghilardi, H. Wang et al., “Development of Th1-type immune responses requires the type I cytokine receptor TCCR,” Nature, vol. 407, no. 6806, pp. 916–920, 2000. View at Publisher · View at Google Scholar
  38. C. A. Sprecher, F. J. Grant, J. W. Baumgartner et al., “Cloning and characterization of a novel class I cytokine receptor,” Biochemical and Biophysical Research Communications, vol. 246, no. 1, pp. 82–90, 1998. View at Publisher · View at Google Scholar
  39. S. Pflanz, L. Hibbert, J. Mattson et al., “WSX-1 and glycoprotein 130 constitute a signal-transducing receptor for IL-27,” Journal of Immunology, vol. 172, no. 4, pp. 2225–2231, 2004. View at Google Scholar
  40. T. Yoshimura, A. Takeda, S. Hamano et al., “Two-sided roles of IL-27: induction of Th1 differentiation on naïve CD4+ T cells versus suppression of proinflammatory cytokine production including IL-23-induced IL-17 on activated CD4+ T cells partially through STAT3-dependent mechanism,” Journal of Immunology, vol. 177, no. 8, pp. 5377–5385, 2006. View at Google Scholar
  41. A. Takeda, S. Hamano, A. Yamanaka et al., “Cutting edge: role of IL-27/WSX-1 signaling for induction of T-bet through activation of STAT1 during initial Th1 commitment,” Journal of Immunology, vol. 170, no. 10, pp. 4886–4890, 2003. View at Google Scholar
  42. M. A. Farrar, J. D. Campbell, and R. D. Schreiber, “Identification of a functionally important sequence in the C terminus of the interferon-γ receptor,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 24, pp. 11706–11710, 1992. View at Publisher · View at Google Scholar
  43. A. C. Greenlund, M. A. Farrar, B. L. Viviano, and R. D. Schreiber, “Ligand-induced IFN(γ) receptor tyrosine phosphorylation couples the receptor to its signal transduction system (p91),” EMBO Journal, vol. 13, no. 7, pp. 1591–1600, 1994. View at Google Scholar
  44. S. Lucas, N. Ghilardi, J. Li, and F. J. de Sauvage, “IL-27 regulates IL-12 responsiveness of naïve CD4+ T cells through STAT1-dependent and -independent mechanisms,” Proceedings of the National Academy of Sciences of the United States of America, vol. 100, no. 25, pp. 15047–15052, 2003. View at Publisher · View at Google Scholar
  45. S. Kamiya, T. Owaki, N. Morishima, F. Fukai, J. Mizuguchi, and T. Yoshimoto, “An indispensable role for STAT1 in IL-27-induced T-bet expression but not proliferation of naïve CD4+ T cells,” Journal of Immunology, vol. 173, no. 6, pp. 3871–3877, 2004. View at Google Scholar
  46. T. Owaki, M. Asakawa, N. Morishima et al., “A role for IL-27 in early regulation of Th1 differentiation,” Journal of Immunology, vol. 175, no. 4, pp. 2191–2200, 2005. View at Google Scholar
  47. M. Afkarian, J. R. Sedy, J. Yang et al., “T-bet is a STAT1-induced regulator for IL-12R expression in naïve CD4+ T cells,” Nature Immunology, vol. 3, no. 6, pp. 549–557, 2002. View at Publisher · View at Google Scholar
  48. A. A. Lighvani, D. M. Frucht, D. Jankovic et al., “T-bet is rapidly induced by interferon-? in lymphoid and myeloid cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 26, pp. 15137–15142, 2001. View at Publisher · View at Google Scholar
  49. A. Yamanaka, S. Hamano, Y. Miyazaki et al., “Hyperproduction of proinflammatory cytokines by WSX-1-deficient NKT cells in concanavalin a-induced hepatitis,” Journal of Immunology, vol. 172, no. 6, pp. 3590–3596, 2004. View at Google Scholar
  50. C. Hölscher, A. Hölscher, D. Rückerl et al., “The IL-27 receptor chain WSX-1 differentially regulates antibacterial immunity and survival during experimental tuberculosis,” Journal of Immunology, vol. 174, no. 6, pp. 3534–3544, 2005. View at Google Scholar
  51. D. Rückerl, M. Heßmann, T. Yoshimoto, S. Ehlers, and C. Hölscher, “Alternatively activated macrophages express the IL-27 receptor alpha chain WSX-1,” Immunobiology, vol. 211, no. 6–8, pp. 427–436, 2006. View at Publisher · View at Google Scholar
  52. S. Wirtz, I. Tubbe, P. R. Galle et al., “Protection from lethal septic peritonitis by neutralizing the biological function of interleukin 27,” Journal of Experimental Medicine, vol. 203, no. 8, pp. 1875–1881, 2006. View at Publisher · View at Google Scholar
  53. D. Artis, L. M. Johnson, K. Joyce et al., “Cutting edge: early IL-4 production governs the requirement for IL-27-WSX-1 signaling in the development of protective Th1 cytokine responses following Leishmania major Infection,” Journal of Immunology, vol. 172, no. 8, pp. 4672–4675, 2004. View at Google Scholar
  54. C. A. Hunter, A. Villarino, D. Artis, and P. Scott, “The role of IL-27 in the development of T-cell responses during parasitic infections,” Immunological Reviews, vol. 202, no. 1, pp. 106–114, 2004. View at Publisher · View at Google Scholar
  55. T. Owaki, M. Asakawa, S. Kamiya et al., “IL-27 suppresses CD28-medicated IL-2 production through suppressor of cytokine signaling 3,” Journal of Immunology, vol. 176, no. 5, pp. 2773–2780, 2006. View at Google Scholar
  56. A. V. Villarino, J. S. Stumhofer, C. J. M. Saris, R. A. Kastelein, F. J. de Sauvage, and C. A. Hunter, “IL-27 limits IL-2 production during Th1 differentiation,” Journal of Immunology, vol. 176, no. 1, pp. 237–247, 2006. View at Google Scholar
  57. M. Batten, J. Li, S. Yi et al., “Interleukin 27 limits autoimmune encephalomyelitis by suppressing the development of interleukin 17-producing T cells,” Nature Immunology, vol. 7, no. 9, pp. 929–936, 2006. View at Publisher · View at Google Scholar
  58. S. Aggarwal, N. Ghilardi, M.-H. Xie, F. J. de Sauvage, and A. L. Gurney, “Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17,” Journal of Biological Chemistry, vol. 278, no. 3, pp. 1910–1914, 2003. View at Publisher · View at Google Scholar
  59. J. K. Kolls and A. Lindén, “Interleukin-17 family members and inflammation,” Immunity, vol. 21, no. 4, pp. 467–476, 2004. View at Publisher · View at Google Scholar
  60. Y. Komiyama, S. Nakae, T. Matsuki et al., “IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis,” Journal of Immunology, vol. 177, no. 1, pp. 566–573, 2006. View at Google Scholar
  61. D. Yen, J. Cheung, H. Scheerens et al., “IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6,” Journal of Clinical Investigation, vol. 116, no. 5, pp. 1310–1316, 2006. View at Publisher · View at Google Scholar
  62. K. Sato, A. Suematsu, K. Okamoto et al., “Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction,” Journal of Experimental Medicine, vol. 203, no. 12, pp. 2673–2682, 2006. View at Publisher · View at Google Scholar
  63. M. N. Kelly, J. K. Kolls, K. Happel et al., “Interteukin-17/interleukin-17 receptor-mediated signaling is important for generation of an optimal polymorphonuclear response against Toxoplasma gondii infection,” Infection and Immunity, vol. 73, no. 1, pp. 617–621, 2005. View at Publisher · View at Google Scholar
  64. A. Takeda, S. Hamano, H. Shiraishi et al., “WSX-1 over-expression in CD4+ T cells leads to hyperproliferation and cytokine hyperproduction in response to TCR stimulation,” International Immunology, vol. 17, no. 7, pp. 889–897, 2005. View at Publisher · View at Google Scholar
  65. A. V. Villarino, J. Larkin III, C. J. M. Saris et al., “Positive and negative regulation of the IL-27 receptor during lymphoid cell activation,” Journal of Immunology, vol. 174, no. 12, pp. 7684–7691, 2005. View at Google Scholar