Interleukin‐33 amplifies I g E synthesis and triggers mast cell degranulation via interleukin‐4 in naïve mice

Abstract

Background The regulation and function of I g E in healthy individuals and in antigen‐naïve animals is not well understood. IL ‐33 administration increases serum I g E in mice with unknown mechanism. We tested the hypothesis that IL ‐33 provides an antigen‐independent stimulus for I g E production and mast cell degranulation. Methods IL ‐33 was administered to naïve wild‐type ( WT ), nude and ST 2 −/− , IL ‐4 −/− , IL 4Rα −/− and T ‐or B ‐cell‐specific IL ‐4 R α −/− mice. I g E and cytokines were quantified by ELISA . T ‐ and B ‐lymphocyte numbers and CD 40L expression were determined by flow cytometry. Anaphylaxis was measured by temperature, mast cell degranulation and histamine release. Results IL ‐33 enhanced I g E production in naïve WT , T‐ IL ‐4 R α −/− but not in ST 2 −/− , IL ‐4 −/− , IL ‐4 R α −/− or B ‐cell‐specific IL ‐4 R α −/− mice, demonstrating IL ‐33 specificity and IL ‐4 dependency. Moreover, IL ‐4 was required for IL ‐33‐induced B ‐cell proliferation and T ‐cell CD 40 L expression, which promotes I g E production. IL ‐33‐induced IL ‐4 production was mainly from innate cells including mast cells and eosinophils. IL ‐33 increased mast cell surface I g E and triggered degranulation and systemic anaphylaxis in allergen‐naïve WT but not in IL ‐4 R α −/− mice. Conclusion IL ‐33 amplifies I g E synthesis and triggers anaphylaxis in naïve mice via IL ‐4, independent of allergen. IL ‐33 may play an important role in nonatopic allergy and idiopathic anaphylaxis.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 35

1. 1.

   Gould HJ, Sutton BJ. IgE in allergy and asthma today. Nat Rev Immunol. 2008;67:205-217.

   Not in our library10.1038/nri2273

2. 2.

   Vercelli D, Jabara HH, Arai K, Geha RS. Induction of human IgE synthesis requires interleukin 4 and T/B cell interactions involving the T cell receptor/CD3 complex and MHC class II antigens. J Exp Med. 1989;169:1295-1307.

   Not in our library10.1084/jem.169.4.1295

3. 3.

   McCoy KD, Harris NL, Diener P, Hatak S, Odermatt B, Hangartner L, et al. Natural IgE production in the absence of MHC Class II cognate help. Immunity. 2006;24:329-339.

   Not in our library10.1016/j.immuni.2006.01.013

4. 4.

   Finkelman FD, Holmes J, Katona IM, Urban JF, Beckmann MP, Park LS, et al. Lymphokine control of in vivo immunoglobulin isotype selection. Annu Rev Immunol. 1990;8:303-333.

   Not in our library10.1146/annurev.iy.08.040190.001511

5. 5.

   Asai K, Kitaura J, Kawakami Y, Yamagata N, Tsai M, Carbone DP, et al. Regulation of mast cell survival by IgE. Immunity. 2001;14:791-800.

   Not in our library10.1016/s1074-7613(01)00157-1

6. 6.

   Kalesnikoff J, Huber M, Lam V, Damen JE, Zhang J, Siraganian RP, et al. Monomeric IgE stimulates signaling pathways in mast cells that lead to cytokine production and cell survival. Immunity. 2001;14:801-811.

   Not in our library10.1016/s1074-7613(01)00159-5

7. 7.

   Bryce PJ, Miller ML, Miyajima I, Tsai M, Galli SJ, Oettgen HC. Immune sensitization in the skin is enhanced by antigen-independent effects of IgE. Immunity. 2004;20:381-392.

   Not in our library10.1016/s1074-7613(04)00080-9

8. 8.

   Galli SJ, Kalesnikoff J, Grimbaldeston MA, Piliponsky AM, Williams CM, Tsai M. Mast cells as “tunable” effector and immunoregulatory cells: recent advances. Annu Rev Immunol. 2005;23:749-786.

   Not in our library10.1146/annurev.immunol.21.120601.141025

9. 9.

   Schmitz J, Owyang A, Oldham E, Song Y, Murphy E, McClanahan TK, et al. IL-33, an interleukin-1-like cytokine that signals via the IL-1 receptor-related protein ST2 and induces T helper type 2-associated cytokines. Immunity. 2005;23:479-490.

   Not in our library10.1016/j.immuni.2005.09.015

10. 10.

    Ali S, Huber M, Kollewe C, Bischoff SC, Falk W, Martin MU. IL-1 receptor accessory protein is essential for IL-33-induced activation of T lymphocytes and mast cells. Proc Natl Acad Sci U S A. 2007;104:18660-18665.

    Not in our library10.1073/pnas.0705939104

11. 11.

    Luthi AU, Cullen SP, McNeela EA, Duriez PJ, Afonina IS, Sheridan C, et al. Suppression of interleukin-33 bioactivity through proteolysis by apoptotic caspases. Immunity. 2009;31:84-98.

    Not in our library10.1016/j.immuni.2009.05.007

12. 12.

    Trajkovic V, Sweet MJ, Xu D. T1/ST2–an IL-1 receptor-like modulator of immune responses. Cytokine Growth Factor Rev. 2004;15:87-95.

    Not in our library10.1016/j.cytogfr.2004.02.004

13. 13.

    Oboki K, Ohno T, Kajiwara N, Arae K, Morita H, Ishii A, et al. IL-33 is a crucial amplifier of innate rather than acquired immunity. Proc Natl Acad Sci U S A. 2010;107:18581-18586.

    Not in our library10.1073/pnas.1003059107

14. 14.

    Pecaric-Petkovic T, Didichenko SA, Kaempfer S, Spiegl N, Dahinden CA. Human basophils and eosinophils are the direct target leukocytes of the novel IL-1 family member IL-33. Blood. 2009;113:1526-1534.

    Not in our library10.1182/blood-2008-05-157818

15. 15.

    Kurowska-Stolarska M, Stolarski B, Kewin P, Murphy G, Corrigan CJ, Ying S, et al. IL-33 amplifies the polarization of alternatively activated macrophages that contribute to airway inflammation. J Immunol. 2009;183:6469-6477.

    Not in our library10.4049/jimmunol.0901575

16. 16.

    Smithgall MD, Comeau MR, Yoon BR, Kaufman D, Armitage R, Smith DE. IL-33 amplifies both Th1- and Th2-type responses through its activity on human basophils, allergen-reactive Th2 cells, iNKT and NK cells. Int Immunol. 2008;20:1019-1030.

    Not in our library10.1093/intimm/dxn060

17. 17.

    Kurowska-Stolarska M, Kewin P, Murphy G, Russo RC, Stolarski B, Garcia CC, et al. IL-33 induces antigen-specific IL-5 + T cells and promotes allergic-induced airway inflammation independent of IL-4. J Immunol. 2008;181:4780-4790.

    Not in our library10.4049/jimmunol.181.7.4780

18. 18.

    Xu D, Chan WL, Leung BP, Huang F, Wheeler R, Piedrafita D, et al. Selective expression of a stable cell surface molecule on type 2 but not type 1 helper T cells. J Exp Med. 1998;187:787-794.

    Not in our library10.1084/jem.187.5.787

19. 19.

    Xu D, Jiang HR, Kewin P, Li Y, Mu R, Fraser AR, et al. IL-33 exacerbates antigen-induced arthritis by activating mast cells. Proc Natl Acad Sci U S A. 2008;105:10913-10918.

    Not in our library10.1073/pnas.0801898105

20. 20.

    Xu D, Jiang HR, Li Y, Pushparaj PN, Kurowska-Stolarska M, Leung BP, et al. IL-33 exacerbates autoantibody-induced arthritis. J Immunol. 2010;184:2620-2626.

    Not in our library10.4049/jimmunol.0902685

21. 21.

    Mohrs M, Ledermann B, Kohler G, Dorfmuller A, Gessner A, Brombacher F. Differences between IL-4- and IL-4 receptor alpha-deficient mice in chronic leishmaniasis reveal a protective role for IL-13 receptor signaling. J Immunol. 1999;162:7302-7308.

    Not in our library

22. 22.

    Radwanska M, Cutler AJ, Hoving JC, Magez S, Holscher C, Bohms A, et al. Deletion of IL-4Ralpha on CD4 T cells renders BALB/c mice resistant to Leishmania major infection. PLoS Pathog. 2007;3:e68.

    Not in our library10.1371/journal.ppat.0030068

23. 23.

    Miller AM, Xu D, Asquith DL, Denby L, Li Y, Sattar N, et al. IL-33 reduces the development of atherosclerosis. J Exp Med. 2008;205:339-346.

    Not in our library10.1084/jem.20071868

24. 24.

    Zurawski G, de VriesJE. Interleukin 13, an interleukin 4-like cytokine that acts on monocytes and B cells, but not on T cells. Immunol Today. 1994;15:19-26.

    Not in our library10.1016/0167-5699(94)90021-3

25. 25.

    Brewer JM, Conacher M, Hunter CA, Mohrs M, Brombacher F, Alexander J. Aluminium hydroxide adjuvant initiates strong antigen-specific Th2 responses in the absence of IL-4- or IL-13-mediated signaling. J Immunol. 1999;163:6448-6454.

    Not in our library

26. 26.

    Komai-Koma M, Gilchrist DS, McKenzie AN, Goodyear CS, Xu D, Liew FY. IL-33 activates B1 cells and exacerbates contact sensitivity. J Immunol. 2011;186:2584-2591.

    Not in our library10.4049/jimmunol.1002103

27. 27.

    Yoshimoto T, Min B, Sugimoto T, Hayashi N, Ishikawa Y, Sasaki Y, et al. Nonredundant roles for CD1d-restricted natural killer T cells and conventional CD4 + T cells in the induction of immunoglobulin E antibodies in response to interleukin 18 treatment of mice. J Exp Med. 2003;197:997-1005.

    Not in our library10.1084/jem.20021701

28. 28.

    Golden DB. What is anaphylaxis? Curr Opin Allergy Clin Immunol. 2007;7:331-336.

    Not in our library10.1097/aci.0b013e3281f8290c

29. 29.

    Metcalfe DD, Peavy RD, Gilfillan AM. Mechanisms of mast cell signaling in anaphylaxis. J Allergy Clin Immunol. 2009;124.

    Not in our library10.1016/j.jaci.2009.08.035

30. 30.

    Lenchner K, Grammer LC. A current review of idiopathic anaphylaxis. Curr Opin Allergy Clin Immunol. 2003;3:305-311.

    Not in our library10.1097/00130832-200308000-00012

31. 31.

    Strait RT, Morris SC, Smiley K, Urban JF, Finkelman FD. IL-4 exacerbates anaphylaxis. J Immunol. 2003;170:3835-3842.

    Not in our library10.4049/jimmunol.170.7.3835

32. 32.

    Sakashita M, Yoshimoto T, Hirota T, Harada M, Okubo K, Osawa Y, et al. Association of serum interleukin-33 level and the interleukin-33 genetic variant with Japanese cedar pollinosis. Clin Exp Allergy. 2008;38:1875-1881.

    Not in our library10.1111/j.1365-2222.2008.03114.x

33. 33.

    Shimizu M, Matsuda A, Yanagisawa K, Hirota T, Akahoshi M, Inomata N, et al. Functional SNPs in the distal promoter of the ST2 gene are associated with atopic dermatitis. Hum Mol Genet. 2005;14:2919-2927.

    Not in our library10.1093/hmg/ddi323

34. 34.

    Pearce N, Pekkanen J, Beasley R. How much asthma is really attributable to atopy? Thorax. 1999;54:268-272.

    Not in our library10.1136/thx.54.3.268

35. 35.

    Moffatt MF, Gut IG, Demenais F, Strachan DP, Bouzigon E, Heath S, et al. A large-scale, consortium-based genomewide association study of asthma. N Engl J Med. 2010;363:1211-1221.

    Not in our library10.1056/nejmoa0906312

Cited by papers we hold 4

• IL-33-mediated mast cell activation promotes gastric cancer through macrophage mobilization · 2019
  No notice
• The ST2/IL-33 Axis in Immune Cells during Inflammatory Diseases · 2017
  No notice
• The role of IL‐33 and mast cells in allergy and inflammation · 2015
  No notice
• IL ‐33 drives airway hyper‐responsiveness through IL ‐13‐mediated mast cell: airway smooth muscle crosstalk · 2015
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.