An IL-9 fate reporter demonstrates the induction of an innate IL-9 response in lung inflammation

Christoph Wilhelm; Keiji Hirota; Benjamin Stieglitz; Jacques Van Snick; Mauro Tolaini; Katharina Lahl; Tim Sparwasser; Helena Helmby; Brigitta Stockinger

doi:10.1038/ni.2133

journal article Open Access Oct 09, 2011

An IL-9 fate reporter demonstrates the induction of an innate IL-9 response in lung inflammation

Christoph Wilhelm

Keiji Hirota Benjamin Stieglitz

Jacques Van Snick Mauro Tolaini Katharina Lahl

Tim Sparwasser Helena Helmby Brigitta Stockinger

Nature Immunology Vol. 12 No. 11 pp. 1071-1077 · Springer Science and Business Media LLC

View at Publisher Save 10.1038/ni.2133

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References

41

[1]

Erpenbeck, V.J. et al. Segmental allergen challenge in patients with atopic asthma leads to increased IL-9 expression in bronchoalveolar lavage fluid lymphocytes. J. Allergy Clin. Immunol. 111, 1319–1327 (2003). 10.1067/mai.2003.1485

[2]

Shimbara, A. et al. IL-9 and its receptor in allergic and nonallergic lung disease: increased expression in asthma. J. Allergy Clin. Immunol. 105, 108–115 (2000). 10.1016/s0091-6749(00)90185-4

[3]

White, B., Leon, F., White, W. & Robbie, G. Two first-in-human, open-label, phase I dose-escalation safety trials of MEDI-528, a monoclonal antibody against interleukin-9, in healthy adult volunteers. Clin. Ther. 31, 728–740 (2009). 10.1016/j.clinthera.2009.04.019

[4]

Temann, U.A., Laouar, Y., Eynon, E.E., Homer, R. & Flavell, R.A. IL9 leads to airway inflammation by inducing IL13 expression in airway epithelial cells. Int. Immunol. 19, 1–10 (2007). 10.1093/intimm/dxl117

[5]

Temann, U.A., Geba, G.P., Rankin, J.A. & Flavell, R.A. Expression of interleukin 9 in the lungs of transgenic mice causes airway inflammation, mast cell hyperplasia, and bronchial hyperresponsiveness. J. Exp. Med. 188, 1307–1320 (1998). 10.1084/jem.188.7.1307

[6]

Temann, U.A., Ray, P. & Flavell, R.A. Pulmonary overexpression of IL-9 induces Th2 cytokine expression, leading to immune pathology. J. Clin. Invest. 109, 29–39 (2002). 10.1172/jci0213696

[7]

Cheng, G. et al. Anti-interleukin-9 antibody treatment inhibits airway inflammation and hyperreactivity in mouse asthma model. Am. J. Respir. Crit. Care Med. 166, 409–416 (2002). 10.1164/rccm.2105079

[8]

Kung, T.T. et al. Effect of anti-mIL-9 antibody on the development of pulmonary inflammation and airway hyperresponsiveness in allergic mice. Am. J. Respir. Cell Mol. Biol. 25, 600–605 (2001). 10.1165/ajrcmb.25.5.4533

[9]

Townsend, J.M. et al. IL-9-deficient mice establish fundamental roles for IL-9 in pulmonary mastocytosis and goblet cell hyperplasia but not T cell development. Immunity 13, 573–583 (2000). 10.1016/s1074-7613(00)00056-x

[10]

Kearley, J. et al. IL-9 governs allergen-induced mast cell numbers in the lung and chronic remodeling of the airways. Am. J. Respir. Crit. Care Med. 183, 865–875 (2010). 10.1164/rccm.200909-1462oc

[11]

Wynn, T.A. IL-13 effector functions. Annu. Rev. Immunol. 21, 425–456 (2003). 10.1146/annurev.immunol.21.120601.141142

[12]

Cho, J.Y. et al. Inhibition of airway remodeling in IL-5-deficient mice. J. Clin. Invest. 113, 551–560 (2004). 10.1172/jci19133

[13]

Faulkner, H., Renauld, J.C., Van Snick, J. & Grencis, R.K. Interleukin-9 enhances resistance to the intestinal nematode Trichuris muris. Infect. Immun. 66, 3832–3840 (1998). 10.1128/iai.66.8.3832-3840.1998

[14]

Faulkner, H., Humphreys, N., Renauld, J.C., Van Snick, J. & Grencis, R. Interleukin-9 is involved in host protective immunity to intestinal nematode infection. Eur. J. Immunol. 27, 2536–2540 (1997). 10.1002/eji.1830271011

[15]

Richard, M., Grencis, R.K., Humphreys, N.E., Renauld, J.C. & Van Snick, J. Anti-IL-9 vaccination prevents worm expulsion and blood eosinophilia in Trichuris muris-infected mice. Proc. Natl. Acad. Sci. USA 97, 767–772 (2000). 10.1073/pnas.97.2.767

[16]

Angkasekwinai, P., Chang, S.H., Thapa, M., Watarai, H. & Dong, C. Regulation of IL-9 expression by IL-25 signaling. Nat. Immunol. 11, 250–256 (2010). 10.1038/ni.1846

[17]

Chang, H.C. et al. The transcription factor PU.1 is required for the development of IL-9-producing T cells and allergic inflammation. Nat. Immunol. 11, 527–534 (2010). 10.1038/ni.1867

[18]

Staudt, V. et al. Interferon-regulatory factor 4 is essential for the developmental program of T helper 9 cells. Immunity 33, 192–202 (2010). 10.1016/j.immuni.2010.07.014

[19]

Veldhoen, M. et al. Transforming growth factor-beta 'reprograms' the differentiation of T helper 2 cells and promotes an interleukin 9-producing subset. Nat. Immunol. 9, 1341–1346 (2008). 10.1038/ni.1659

[20]

Gounni, A.S. et al. IL-9 expression by human eosinophils: regulation by IL-1beta and TNF-alpha. J. Allergy Clin. Immunol. 106, 460–466 (2000). 10.1067/mai.2000.109172

[21]

Hültner, L. et al. In activated mast cells, IL-1 up-regulates the production of several Th2-related cytokines including IL-9. J. Immunol. 164, 5556–5563 (2000). 10.4049/jimmunol.164.11.5556

[22]

Stassen, M. et al. Murine bone marrow-derived mast cells as potent producers of IL-9: costimulatory function of IL-10 and kit ligand in the presence of IL-1. J. Immunol. 164, 5549–5555 (2000). 10.4049/jimmunol.164.11.5549

[23]

Fallon, P.G. 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. 203, 1105–1116 (2006). 10.1084/jem.20051615

[24]

Hurst, S.D. 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. 169, 443–453 (2002). 10.4049/jimmunol.169.1.443

[25]

Fort, M.M. et al. IL-25 induces IL-4, IL-5, and IL-13 and Th2-associated pathologies in vivo. Immunity 15, 985–995 (2001). 10.1016/s1074-7613(01)00243-6

[26]

Saenz, S.A. et al. IL25 elicits a multipotent progenitor cell population that promotes T(H)2 cytokine responses. Nature 464, 1362–1366 (2010). 10.1038/nature08901

[27]

Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity

Daniel R. Neill, See Heng Wong, Agustin Bellosi et al.

Nature 2010 10.1038/nature08900

[28]

Moro, K. et al. Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit+Sca-1+ lymphoid cells. Nature 463, 540–544 (2010). 10.1038/nature08636

[29]

Systemically dispersed innate IL-13–expressing cells in type 2 immunity

April E. Price, Hong-Erh Liang, Brandon M. Sullivan et al.

Proceedings of the National Academy of Sciences 2010 10.1073/pnas.1003988107

[30]

Spits, H. & Di Santo, J.P. The expanding family of innate lymphoid cells: regulators and effectors of immunity and tissue remodeling. Nat. Immunol. 12, 21–27 (2011). 10.1038/ni.1962

[31]

Tan, C. et al. Antigen-specific Th9 cells exhibit uniqueness in their kinetics of cytokine production and short retention at the inflammatory site. J. Immunol. 185, 6795–6801 (2010). 10.4049/jimmunol.1001676

[32]

Novey, H.S., Marchioli, L.E., Sokol, W.N. & Wells, I.D. Papain-induced asthma–physiological and immunological features. J. Allergy Clin. Immunol. 63, 98–103 (1979). 10.1016/0091-6749(79)90198-2

[33]

Sokol, C.L., Barton, G.M., Farr, A.G. & Medzhitov, R. A mechanism for the initiation of allergen-induced T helper type 2 responses. Nat. Immunol. 9, 310–318 (2008). 10.1038/ni1558

[34]

Oboki, K. et al. IL-33 is a crucial amplifier of innate rather than acquired immunity. Proc. Natl. Acad. Sci. USA 107, 18581–18586 (2010). 10.1073/pnas.1003059107

[35]

Wang, Y.H. et al. A novel subset of CD4+ T(H)2 memory/effector cells that produce inflammatory IL-17 cytokine and promote the exacerbation of chronic allergic asthma. J. Exp. Med. 207, 2479–2491 (2010). 10.1084/jem.20101376

[36]

Hirota, K. et al. Fate mapping of IL-17-producing T cells in inflammatory responses. Nat. Immunol. 12, 255–263 (2011). 10.1038/ni.1993

[37]

Houssiau, F.A. et al. A cascade of cytokines is responsible for IL-9 expression in human T cells. Involvement of IL-2, IL-4, and IL-10. J. Immunol. 154, 2624–2630 (1995). 10.4049/jimmunol.154.6.2624

[38]

Houssiau, F.A., Renauld, J.C., Fibbe, W.E. & Van Snick, J. IL-2 dependence of IL-9 expression in human T lymphocytes. J. Immunol. 148, 3147–3151 (1992). 10.4049/jimmunol.148.10.3147

[39]

Belyaev, N.N. et al. Induction of an IL7-R+c-Kit(hi) myelolymphoid progenitor critically dependent on IFN-γ signaling during acute malaria. Nat. Immunol. 11, 477–485 (2010). 10.1038/ni.1869

[40]

Chang, Y.J. et al. Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity. Nat. Immunol. 12, 631–638 (2011). 10.1038/ni.2045

[41]

Steenwinckel, V. et al. IL-9 promotes IL-13-dependent paneth cell hyperplasia and up-regulation of innate immunity mediators in intestinal mucosa. J. Immunol. 182, 4737–4743 (2009). 10.4049/jimmunol.0801941

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Published: Oct 09, 2011
Vol/Issue: 12(11)
Pages: 1071-1077
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Cite This Article

Christoph Wilhelm, Keiji Hirota, Benjamin Stieglitz, et al. (2011). An IL-9 fate reporter demonstrates the induction of an innate IL-9 response in lung inflammation. Nature Immunology, 12(11), 1071-1077. https://doi.org/10.1038/ni.2133

An IL-9 fate reporter demonstrates the induction of an innate IL-9 response in lung inflammation

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