Cytokine & Growth Factor Reviews
Volume 21, Issue 6 , Pages 471-475 , December 2010

Interleukin-25: A two-edged sword in the control of immune-inflammatory responses

  • Giovanni Monteleone

      Affiliations

    • Dipartimento di Medicina Interna, Università Tor Vergata, Via Montpellier, 1, 00133 Rome, Italy
    • Corresponding Author InformationCorresponding author. Tel.: +39 06 72596150; fax: +39 06 72596391.
  • ,
  • Francesco Pallone

      Affiliations

    • Dipartimento di Medicina Interna, Università Tor Vergata, Via Montpellier, 1, 00133 Rome, Italy
  • ,
  • Thomas T. MacDonald

      Affiliations

    • Institute of Cell and Molecular Science, Bart's and the London School of Medicine and Dentistry, London, UK

References 

  1. Joffre O, Nolte MA, Spörri R, Reis e Sousa C. Inflammatory signals in dendritic cell activation and the induction of adaptive immunity. Immunol Rev. 2009;227:234–247
  2. Damsker JM, Hansen AM, Caspi RR. Th1 and Th17 cells: adversaries and collaborators. Ann N Y Acad Sci. 2010;1183:211–221
  3. Zhu J, Paul WE. Heterogeneity and plasticity of T helper cells. Cell Res. 2010;20:4–12
  4. de Jong E, Suddason T, Lord GM. Translational mini-review series on Th17 cells: development of mouse and human T helper 17 cells. Clin Exp Immunol. 2010;159:148–158
  5. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science. 2003;299:1057–1061
  6. Eyerich S, Eyerich K, Pennino D, Carbone T, Nasorri F, Pallotta S, et al. Th22 cells represent a distinct human T cell subset involved in epidermal immunity and remodeling. J Clin Invest. 2009;119:3573–3585
  7. Fort MM, Cheung J, Yen D, Li J, Zurawski SM, Lo S, et al. IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies in vivo. Immunity. 2001;15:985–995
  8. Angkasekwinai P, Park H, Wang YH, Wang YH, Chang SH, Corry DB, et al. Interleukin 25 promotes the initiation of proallergic type 2 responses. J Exp Med. 2007;204:1509–1517
  9. Zaph C, Du Y, Saenz SA, Nair MG, Perrigoue JG, Taylor BC, et al. Commensal-dependent expression of IL-25 regulates the IL-23-IL-17 axis in the intestine. J Exp Med. 2008;205:2191–2198
  10. Caruso R, Sarra M, Stolfi C, Rizzo A, Fina D, Fantini MC, et al. Interleukin-25 inhibits interleukin-12 production and Th1 cell-driven inflammation in the gut. Gastroenterology. 2009;136:2270–2279
  11. Ikeda K, Nakajima H, Suzuki K, Kagami S, Hirose K, Suto A, et al. Mast cells produce interleukin-25 upon Fc epsilon RI-mediated activation. Blood. 2003;101:3594–3596
  12. Kang CM, Jang AS, Ahn MH, Shin JA, Kim JH, Choi YS, et al. Interleukin-25 and interleukin-13 production by alveolar macrophages in response to particles. Am J Respir Cell Mol Biol. 2005;33:290–296
  13. Dolgachev V, Petersen BC, Budelsky AL, Berlin AA, Lukacs NW. Pulmonary IL-17E (IL-25) production and IL-17RB+ myeloid cell-derived Th2 cytokine production are dependent upon stem cell factor-induced responses during chronic allergic pulmonary disease. J Immunol. 2009;183:5705–5715
  14. Wang YH, Angkasekwinai P, Lu N, Voo KS, Arima K, Hanabuchi S, et al. IL-25 augments type 2 immune responses by enhancing the expansion and functions of TSLP-DC-activated Th2 memory cells. J Exp Med. 2007;204:1837–1847
  15. Sonobe Y, Takeuchi H, Kataoka K, Li H, Jin S, Mimuro M, et al. Interleukin-25 expressed by brain capillary endothelial cells maintains blood–brain barrier function in a protein kinase Cepsilon-dependent manner. J Biol Chem. 2009;284:31834–31842
  16. Rickel EA, Siegel LA, Yoon BR, Rottman JB, Kugler DG, Swart DA, et al. Identification of functional roles for both IL-17RB and IL-17RA in mediating IL-25-induced activities. J Immunol. 2008;181:4299–4310
  17. Lee J, Ho WH, Maruoka M, Corpuz RT, Baldwin DT, Foster JS, et al. IL-17E, a novel proinflammatory ligand for the IL-17 receptor homolog IL-17Rh1. J Biol Chem. 2001;276:1660–1664
  18. Caruso R, Stolfi C, Sarra M, Rizzo A, Fantini MC, Pallone F, et al. Inhibition of monocyte-derived inflammatory cytokines by IL-25 occurs via p38 Map kinase-dependent induction of Socs-3. Blood. 2009;113:3512–3519
  19. Terashima A, Watarai H, Inoue S, Sekine E, Nakagawa R, Hase K, et al. A novel subset of mouse NKT cells bearing the IL-17 receptor B responds to IL-25 and contributes to airway hyperreactivity. J Exp Med. 2008;205:2727–2733
  20. Stock P, Lombardi V, Kohlrautz V, Akbari O. Induction of airway hyperreactivity by IL-25 is dependent on a subset of invariant NKT cells expressing IL-17RB. J Immunol. 2009;182:5116–5122
  21. Wong CK, Cheung PF, Ip WK, Lam CW. Interleukin-25-induced chemokines and interleukin-6 release from eosinophils is mediated by p38 mitogen-activated protein kinase, c-Jun N-terminal kinase, and nuclear factor-kappaB. Am J Respir Cell Mol Biol. 2005;33:186–194
  22. Maezawa Y, Nakajima H, Suzuki K, Tamachi T, Ikeda K, Inoue J, et al. Involvement of TNF receptor-associated factor 6 in IL-25 receptor signaling. J Immunol. 2006;176:1013–1018
  23. Chang SH, Park H, Dong C. Act1 adaptor protein is an immediate and essential signaling component of interleukin-17 receptor. J Biol Chem. 2006;281:35603–35607
  24. Novatchkova M, Leibbrandt A, Werzowa J, Neubüser A, Eisenhaber F. The STIR-domain superfamily in signal transduction, development and immunity. Trends Biochem Sci. 2003;28:226–229
  25. Swaidani S, Bulek K, Kang Z, Liu C, Lu Y, Yin W, et al. The critical role of epithelial-derived Act1 in IL-17- and IL-25-mediated pulmonary inflammation. J Immunol. 2009;182:1631–1640
  26. Louten J, Boniface K, de Waal Malefyt R. Development and function of TH17 cells in health and disease. J Allergy Clin Immunol. 2009;123:1004–1011
  27. Fallon PG, Ballantyne SJ, Mangan NE, Barlow JL, Dasvarma A, Hewett DR, et al. 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. 2006;203:1105–1116
  28. Hurst SD, Muchamuel T, Gorman DM, Gilbert JM, Clifford T, Kwan S, et al. New IL-17 family members promote Th1 or Th2 responses in the lung: in vivo function of the novel cytokine IL-25. J Immunol. 2002;169:443–453
  29. Kim MR, Manoukian R, Yeh R, Silbiger SM, Danilenko DM, Scully S, et al. Transgenic overexpression of human IL-17E results in eosinophilia, B-lymphocyte hyperplasia, and altered antibody production. Blood. 2002;100:2330–2340
  30. Pan G, French D, Mao W, Maruoka M, Risser P, Lee J, et al. Forced expression of murine IL-17E induces growth retardation, jaundice, a Th2-biased response, and multiorgan inflammation in mice. J Immunol. 2001;167:6559–6567
  31. Sharkhuu T, Matthaei KI, Forbes E, Mahalingam S, Hogan SP, Hansbro PM, et al. Mechanism of interleukin-25 (IL-17E)-induced pulmonary inflammation and airways hyper-reactivity. Clin Exp Allergy. 2006;36:1575–1583
  32. Shinkai K, Mohrs M, Locksley RM. Helper T cells regulate type-2 innate immunity in vivo. Nature. 2002;420:825–829
  33. Voehringer D, Shinkai K. Locksley RM. Type 2 immunity reflects orchestrated recruitment of cells committed to IL-4 production. Immunity. 2004;20:267–277
  34. Claudio E, Sønder SU, Saret S, Carvalho G, Ramalingam TR, Wynn TA, et al. The adaptor protein CIKS/Act1 is essential for IL-25-mediated allergic airway inflammation. J Immunol. 2009;182:1617–1630
  35. Saenz SA, Siracusa MC, Perrigoue JG, Spencer SP, Urban JF, Tocker JE, et al. IL25 elicits a multipotent progenitor cell population that promotes T(H)2 cytokine responses. Nature. 2010;March 3 [Epub ahead of print]
  36. Tamachi T, Maezawa Y, Ikeda K, Kagami S, Hatano M, Seto Y, et al. IL-25 enhances allergic airway inflammation by amplifying a TH2 cell-dependent pathway in mice. J Allergy Clin Immunol. 2006;118:606–614
  37. Jarnicki AG, Fallon PG. T helper type-2 cytokine responses: potential therapeutic targets. Curr Opin Pharmacol. 2003;3:449–455
  38. Veldhoen M, Uyttenhove C, van Snick J, Helmby H, Westendorf A, Buer J, et al. Transforming growth factor-beta ‘reprograms’ the differentiation of T helper 2 cells and promotes an interleukin 9-producing subset. Nat Immunol. 2008;9:1341–1346
  39. Angkasekwinai P, Chang SH, Thapa M, Watarai H, Dong C. Regulation of IL-9 expression by IL-25 signaling. Nat Immunol. 2010;11:250–256
  40. Owyang AM, Zaph C, Wilson EH, Guild KJ, McClanahan T, Miller HR, et al. Interleukin 25 regulates type 2 cytokine-dependent immunity and limits chronic inflammation in the gastrointestinal tract. J Exp Med. 2006;203:843–849
  41. Kleinschek MA, Owyang AM, Joyce-Shaikh B, Langrish CL, Chen Y, Gorman DM, et al. IL-25 regulates Th17 function in autoimmune inflammation. J Exp Med. 2007;204:161–170
  42. Mchenga SS, Wang D, Li C, Shan F, Lu C. Inhibitory effect of recombinant IL-25 on the development of dextran sulfate sodium-induced experimental colitis in mice. Cell Mol Immunol. 2008;5:425–431
  43. Emamaullee JA, Davis J, Merani S, Toso C, Elliott JF, Thiesen A, et al. Inhibition of Th17 cells regulates autoimmune diabetes in NOD mice. Diabetes. 2009;58:1302–1311
  44. Létuvé S, Lajoie-Kadoch S, Audusseau S, Rothenberg ME, Fiset PO, Ludwig MS, et al. IL-17E upregulates the expression of proinflammatory cytokines in lung fibroblasts. J Allergy Clin Immunol. 2006;117:590–596
  45. Breese EJ, Michie CA, Nicholls SW, Murch SH, Williams CB, Domizio P, et al. Tumor necrosis factor alpha-producing cells in the intestinal mucosa of children with inflammatory bowel disease. Gastroenterology. 1994;106:1455–1466
  46. Forsberg G, Hernell O, Melgar S, Israelsson A, Hammarström S, Hammarström ML. Paradoxical coexpression of proinflammatory and down-regulatory cytokines in intestinal T cells in childhood celiac disease. Gastroenterology. 2002;123:667–678

PII: S1359-6101(10)00035-3

doi: 10.1016/j.cytogfr.2010.05.001

Cytokine & Growth Factor Reviews
Volume 21, Issue 6 , Pages 471-475 , December 2010