Advertisement

IL-25, another promoter of allergy

  • Pornpimon Angkasekwinai
  • Chen Dong
Part of the Progress in Inflammation Research book series (PIR)

Abstract

Although there have been significant insights into the mechanism underlying the initiation of type 1 immune response, how type 2-mediated pathology especially allergic diseases is developed remains unclear. Cytokine environment is important in shaping and initiating Th2 responses. IL-25, also called IL-17E, belongs to the IL-17 family but, unlike other IL-17 cytokine members, possesses a unique function in regulating type 2 immune responses. Here we summarize recent work demonstrating the role of this cytokine in promoting allergy, and discuss its potential producer and responder cells during allergic inflammation. IL-25 thus serves as a novel target for pharmaceutical intervention of allergic asthma disease.

Keywords

Allergic Disease Allergy Clin Immunol Lung Epithelial Cell Allergic Inflammation Allergic Airway Disease 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Umetsu DT, McIntire JJ, Akbari O, Macaubas C, DeKruyff RH (2002) Asthma: An epidemic of dysregulated immunity. Nat Immunol 3: 715–720PubMedCrossRefGoogle Scholar
  2. 2.
    Renauld JC (2001) New insights into the role of cytokines in asthma. J Clin Pathol 54: 577–589PubMedCrossRefGoogle Scholar
  3. 3.
    Yao Z, Fanslow WC, Seldin MF, Rousseau AM, Painter SL, Comeau MR, Cohen JI, Spriggs MK (1995) Herpesvirus Saimiri encodes a new cytokine, IL-17, which binds to a novel cytokine receptor. Immunity 3: 811–821PubMedCrossRefGoogle Scholar
  4. 4.
    Li H, Chen J, Huang A, Stinson J, Heldens S, Foster J, Dowd P, Gurney AL, Wood WI (2000) Cloning and characterization of IL-17B and IL-17C, two new members of the IL-17 cytokine family. Proc Natl Acad Sci USA 97: 773–778PubMedCrossRefGoogle Scholar
  5. 5.
    Starnes T, Robertson MJ, Sledge G, Kelich S, Nakshatri H, Broxmeyer HE, Hromas R (2001) Cutting edge: IL-17F, a novel cytokine selectively expressed in activated T cells and monocytes, regulates angiogenesis and endothelial cell cytokine production. J Immunol 167: 4137–4140PubMedGoogle Scholar
  6. 6.
    Starnes T, Broxmeyer HE, Robertson MJ, Hromas R (2002) Cutting edge: IL-17D, a novel member of the IL-17 family, stimulates cytokine production and inhibits hemopoiesis. J Immunol 169: 642–646PubMedGoogle Scholar
  7. 7.
    Fort MM, Cheung J, Yen D, Li J, Zurawski SM, Lo S, Menon S, Clifford T, Hunte B, Lesley R et al (2001) IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies in vivo. Immunity 15: 985–995PubMedCrossRefGoogle Scholar
  8. 8.
    Hurst SD, Muchamuel T, Gorman DM, Gilbert JM, Clifford T, Kwan S, Menon S, Seymour B, Jackson C, Kung TT et al (2002) New IL-17 family members promote Th1 or Th2 responses in the lung: In vivo function of the novel cytokine IL-25. J Immunol 169: 443–453PubMedGoogle Scholar
  9. 9.
    Kang CM, Jang AS, Ahn MH, Shin JA, Kim JH, Choi YS, Rhim TY, Park CS (2005) Interleukin-25 and interleukin-13 production by alveolar macrophages in response to particles. Am J Respir Cell Mol Biol 33: 290–296PubMedCrossRefGoogle Scholar
  10. 10.
    Sharkhuu T, Matthaei KI, Forbes E, Mahalingam S, Hogan SP, Hansbro PM, Foster PS (2006) Mechanism of interleukin-25 (IL-17E)-induced pulmonary inflammation and airways hyper-reactivity. Clin Exp Allergy 36: 1575–1583PubMedCrossRefGoogle Scholar
  11. 11.
    Tamachi T, Maezawa Y, Ikeda K, Kagami S, Hatano M, Seto Y, Suto A, Suzuki K, Watanabe N, Saito Y et al (2006) IL-25 enhances allergic airway inflammation by amplifying a TH2 cell-dependent pathway in mice. J Allergy Clin Immunol 118: 606–614PubMedCrossRefGoogle Scholar
  12. 12.
    Angkasekwinai P, Park H, Wang YH, Chang SH, Corry DB, Liu YJ, Zhu Z, Dong C (2007) Interleukin 25 promotes the initiation of proallergic type 2 responses. J Exp Med 204: 1509–1517PubMedCrossRefGoogle Scholar
  13. 13.
    Wang YH, Angkasekwinai P, Lu N, Voo KS, Arima K, Hanabuchi S, Hippe A, Corrigan CJ, Dong C, Homey B et al (2007) IL-25 augments type 2 immune responses by enhancing the expansion and functions of TSLP-DC activated Th2 memory cells. J Exp Med 204: 1837–1847PubMedCrossRefGoogle Scholar
  14. 14.
    Ballantyne SJ, Barlow JL, Jolin HE, Nath P, Williams AS, Chung KF, Sturton G, Wong SH, McKenzie AN (2007) Blocking IL-25 prevents airway hyperresponsiveness in allergic asthma. J Allergy Clin Immunol 120: 1324–1331PubMedCrossRefGoogle Scholar
  15. 15.
    Lee J, Ho WH, Maruoka M, Corpuz RT, Baldwin DT, Foster JS, Goddard AD, Yansura DG, Vandlen RL, Wood WI et al (2001) IL-17E, a novel proinflammatory ligand for the IL-17 receptor homolog IL-17Rh1. J Biol Chem 276: 1660–1664PubMedCrossRefGoogle Scholar
  16. 16.
    Ikeda K, Nakajima H, Suzuki K, Kagami S, Hirose K, Suto A, Saito Y, Iwamoto I (2003) Mast cells produce interleukin-25 upon Fc epsilon RI-mediated activation. Blood 101: 3594–3596PubMedCrossRefGoogle Scholar
  17. 17.
    Shi Y, Ullrich SJ, Zhang J, Connolly K, Grzegorzewski KJ, Barber MC, Wang W, Wathen K, Hodge V, Fisher CL et al (2000) A novel cytokine receptor-ligand pair. Identification, molecular characterization, and in vivo immunomodulatory activity. J Biol Chem 275: 19167–19176PubMedCrossRefGoogle Scholar
  18. 18.
    Tian E, Sawyer JR, Largaespada DA, Jenkins NA, Copeland NG, Shaughnessy JD Jr (2000) Evi27 encodes a novel membrane protein with homology to the IL17 receptor. Oncogene 19: 2098–2109PubMedCrossRefGoogle Scholar
  19. 19.
    Maezawa Y, Nakajima H, Suzuki K, Tamachi T, Ikeda K, Inoue J, Saito Y, Iwamoto I (2006) Involvement of TNF receptor-associated factor 6 in IL-25 receptor signaling. J Immunol 176: 1013–1018PubMedGoogle Scholar
  20. 20.
    Fallon PG, Ballantyne SJ, Mangan NE, Barlow JL, Dasvarma A, Hewett DR, McIlgorm A, Jolin HE, McKenzie AN (2006) Identification of an interleukin (IL)-25-dependent cell population that provides IL-4, IL-5, and IL-13 at the onset of helminth expulsion. J Exp Med 203: 1105–1116PubMedCrossRefGoogle Scholar
  21. 21.
    Pan G, French D, Mao W, Maruoka M, Risser P, Lee J, Foster J, Aggarwal S, Nicholes K, Guillet S et al (2001) Forced expression of murine IL-17E induces growth retardation, jaundice, a Th2-biased response, and multiorgan inflammation in mice. J Immunol 167: 6559–6567PubMedGoogle Scholar
  22. 22.
    Kim MR, Manoukian R, Yeh R, Silbiger SM, Danilenko DM, Scully S, Sun J, DeRose ML, Stolina M, Chang D et al (2002) Transgenic overexpression of human IL-17E results in eosinophilia, B-lymphocyte hyperplasia, and altered antibody production. Blood 100: 2330–2340PubMedCrossRefGoogle Scholar
  23. 23.
    Schleimer RP, Kato A, Kern R, Kuperman D, Avila PC (2007) Epithelium: At the interface of innate and adaptive immune responses. J Allergy Clin Immunol 120: 1279–1284PubMedCrossRefGoogle Scholar
  24. 24.
    Letuve S, Lajoie-Kadoch S, Audusseau S, Rothenberg ME, Fiset PO, Ludwig MS, Hamid Q (2006) IL-17E upregulates the expression of proinflammatory cytokines in lung fibroblasts. J Allergy Clin Immunol 117: 590–596PubMedCrossRefGoogle Scholar
  25. 25.
    Chtanova T, Tangye SG, Newton R, Frank N, Hodge MR, Rolph MS, Mackay CR (2004) T follicular helper cells express a distinctive transcriptional profile, reflecting their role as non-Th1/Th2 effector cells that provide help for B cells. J Immunol 173: 68–78PubMedGoogle Scholar
  26. 26.
    Wang YH, Ito T, Homey B, Watanabe N, Martin R, Barnes CJ, McIntyre BW, Gilliet M, Kumar R, Yao Z et al (2006) Maintenance and polarization of human TH2 central memory T cells by thymic stromal lymphopoietin-activated dendritic cells. Immunity 24: 827–838PubMedCrossRefGoogle Scholar
  27. 27.
    Szabo SJ, Kim ST, Costa GL, Zhang X, Fathman CG, Glimcher LH (2000) A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100: 655–669PubMedCrossRefGoogle Scholar
  28. 28.
    Zheng W, Flavell RA (1997) The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell 89: 587–596PubMedCrossRefGoogle Scholar
  29. 29.
    Takeda K, Tanaka T, Shi W, Matsumoto M, Minami M, Kashiwamura S, Nakanishi K, Yoshida N, Kishimoto T, Akira S (1996) Essential role of Stat6 in IL-4 signalling. Nature 380: 627–630PubMedCrossRefGoogle Scholar
  30. 30.
    Kaplan MH, Schindler U, Smiley ST, Grusby MJ (1996) Stat6 is required for mediating responses to IL-4 and for development of Th2 cells. Immunity 4: 313–319PubMedCrossRefGoogle Scholar
  31. 31.
    Ranger AM, Hodge MR, Gravallese EM, Oukka M, Davidson L, Alt FW, de la Brousse FC, Hoey T, Grusby M, Glimcher LH (1998) Delayed lymphoid repopulation with defects in IL-4-driven responses produced by inactivation of NF-ATc. Immunity 8: 125–134PubMedCrossRefGoogle Scholar
  32. 32.
    Flavell RA, Li B, Dong C, Lu HT, Yang DD, Enslen H, Tournier C, Whitmarsh A, Wysk M, Conze D et al (1999) Molecular basis of T-cell differentiation. Cold Spring Harb Symp Quant Biol 64: 563–571PubMedCrossRefGoogle Scholar

Copyright information

© Birkhäuser Verlag Basel/Switzerland 2009

Authors and Affiliations

  • Pornpimon Angkasekwinai
    • 1
    • 2
  • Chen Dong
    • 1
  1. 1.Department of Immunology, MD Anderson Cancer Center and Graduate School of Biomedical ScienceUniversity of TexasHoustonUSA
  2. 2.Faculty of Allied Health SciencesThammasat UniversityPathum-thaniThailand

Personalised recommendations