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Allergic inflammation is initiated by IL-33–dependent crosstalk between mast cells and basophils


Autoři: Chia-Lin Hsu aff001;  Krishan D. Chhiba aff001;  Rebecca Krier-Burris aff001;  Shweta Hosakoppal aff001;  Sergejs Berdnikovs aff001;  Mendy L. Miller aff001;  Paul J. Bryce aff001
Působiště autorů: Division of Allergy-Immunology, Department of Medicine, Feinberg School of Medicine, Northwestern University, Chicago, IL, United States of America aff001
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0226701

Souhrn

IgE-primed mast cells in peripheral tissues, including the skin, lung, and intestine, are key initiators of allergen-triggered edema and inflammation. Particularly in severe forms of allergy, this inflammation becomes strongly neutrophil dominated, and yet how mast cells coordinate this type of response is unknown. We and others have reported that activated mast cells––a hematopoietic cell type––can produce IL-33, a cytokine known to participate in allergic responses but generally considered as being of epithelial origin and driving Type 2 immune responses (e.g., ILC2 and eosinophil activation). Using models of skin anaphylaxis, our data reveal that mast cell-derived IL-33 also initiates neutrophilic inflammation. We demonstrate a cellular crosstalk mechanism whereby activated mast cells crosstalk to IL-33 receptor–bearing basophils, driving these basophils to adopt a unique response signature rich in neutrophil-associated molecules. We further establish that basophil expression of CXCL1 is necessary for IgE-driven neutrophilic inflammation. Our findings thus unearth a new mechanism by which mast cells initiate local inflammation after antigen triggering and might explain the complex inflammatory phenotypes observed in severe allergic diseases. Moreover, our findings (i) establish a functional link from IL-33 to neutrophilic inflammation that extends IL-33–mediated biology well beyond that of Type 2 immunity, and (ii) demonstrate the functional importance of hematopoietic cell–derived IL-33 in allergic pathogenesis.

Klíčová slova:

Basophils – Cytokines – Ears – Flow cytometry – Inflammation – Inflammatory diseases – Mast cells – Neutrophils


Zdroje

1. Johnston LK, Chien KB, Bryce PJ. The immunology of food allergy. J Immunol. 2014;192(6):2529–34. Epub 2014/03/13. doi: 10.4049/jimmunol.1303026 24610821; PubMed Central PMCID: PMC3988470.

2. Wershil BK, Wang ZS, Gordon JR, Galli SJ. Recruitment of neutrophils during IgE-dependent cutaneous late phase reactions in the mouse is mast cell-dependent. Partial inhibition of the reaction with antiserum against tumor necrosis factor-alpha. The Journal of clinical investigation. 1991;87(2):446–53. Epub 1991/02/01. doi: 10.1172/JCI115016 1991831; PubMed Central PMCID: PMC295096.

3. Kalesnikoff J, Galli SJ. New developments in mast cell biology. Nature immunology. 2008;9(11):1215–23. Epub 2008/10/22. doi: 10.1038/ni.f.216 18936782; PubMed Central PMCID: PMC2856637.

4. Galli SJ, Grimbaldeston M, Tsai M. Immunomodulatory mast cells: negative, as well as positive, regulators of immunity. Nature reviews. 2008;8(6):478–86. doi: 10.1038/nri2327 18483499.

5. Grimbaldeston MA, Nakae S, Kalesnikoff J, Tsai M, Galli SJ. Mast cell-derived interleukin 10 limits skin pathology in contact dermatitis and chronic irradiation with ultraviolet B. Nature immunology. 2007;8(10):1095–104. Epub 2007/09/04. doi: 10.1038/ni1503 17767162.

6. Hsu CL, Neilsen CV, Bryce PJ. IL-33 is produced by mast cells and regulates IgE-dependent inflammation. PloS one. 2010;5(8):e11944. Epub 2010/08/07. doi: 10.1371/journal.pone.0011944 20689814; PubMed Central PMCID: PMC2914748.

7. 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(5):479–90. Epub 2005/11/16. doi: 10.1016/j.immuni.2005.09.015 16286016.

8. Grotenboer NS, Ketelaar ME, Koppelman GH, Nawijn MC. Decoding asthma: translating genetic variation in IL33 and IL1RL1 into disease pathophysiology. The Journal of allergy and clinical immunology. 2013;131(3):856–65. Epub 2013/02/06. doi: 10.1016/j.jaci.2012.11.028 23380221.

9. 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(7):4780–90. Epub 2008/09/20. doi: 10.4049/jimmunol.181.7.4780 18802081.

10. Rank MA, Kobayashi T, Kozaki H, Bartemes KR, Squillace DL, Kita H. IL-33-activated dendritic cells induce an atypical TH2-type response. The Journal of allergy and clinical immunology. 2009;123(5):1047–54. Epub 2009/04/14. doi: 10.1016/j.jaci.2009.02.026 19361843; PubMed Central PMCID: PMC2711963.

11. Saglani S, Lui S, Ullmann N, Campbell GA, Sherburn RT, Mathie SA, et al. IL-33 promotes airway remodeling in pediatric patients with severe steroid-resistant asthma. The Journal of allergy and clinical immunology. 2013;132(3):676–85 e13. Epub 2013/06/14. doi: 10.1016/j.jaci.2013.04.012 23759184.

12. Hsu CL, Bryce PJ. Inducible IL-33 expression by mast cells is regulated by a calcium-dependent pathway. J Immunol. 2012;189(7):3421–9. Epub 2012/08/28. doi: 10.4049/jimmunol.1201224 22922818; PubMed Central PMCID: PMC3541686.

13. Zhao WH, Hu ZQ. Up-regulation of IL-33 expression in various types of murine cells by IL-3 and IL-4. Cytokine. 2012;58(2):267–73. Epub 2012/03/01. doi: 10.1016/j.cyto.2012.01.019 22370606.

14. Tjota MY, Williams JW, Lu T, Clay BS, Byrd T, Hrusch CL, et al. IL-33-dependent induction of allergic lung inflammation by FcgammaRIII signaling. The Journal of clinical investigation. 2013;123(5):2287–97. doi: 10.1172/JCI63802 23585480; PubMed Central PMCID: PMC3635716.

15. Tjota MY, Hrusch CL, Blaine KM, Williams JW, Barrett NA, Sperling AI. Signaling through FcRgamma-associated receptors on dendritic cells drives IL-33-dependent TH2-type responses. The Journal of allergy and clinical immunology. 2014;134(3):706–13 e8. Epub 2014/08/05. doi: 10.1016/j.jaci.2014.06.013 25088053; PubMed Central PMCID: PMC4149927.

16. Wills-Karp M, Rani R, Dienger K, Lewkowich I, Fox JG, Perkins C, et al. Trefoil factor 2 rapidly induces interleukin 33 to promote type 2 immunity during allergic asthma and hookworm infection. The Journal of experimental medicine. 2012;209(3):607–22. Epub 2012/02/15. doi: 10.1084/jem.20110079 22329990; PubMed Central PMCID: PMC3302229.

17. Anthony RM, Kobayashi T, Wermeling F, Ravetch JV. Intravenous gammaglobulin suppresses inflammation through a novel T(H)2 pathway. Nature. 2011;475(7354):110–3. Epub 2011/06/21. doi: 10.1038/nature10134 21685887; PubMed Central PMCID: PMC3694429.

18. Haraldsen G, Balogh J, Pollheimer J, Sponheim J, Kuchler AM. Interleukin-33—cytokine of dual function or novel alarmin? Trends in immunology. 2009;30(5):227–33. doi: 10.1016/j.it.2009.03.003 19359217.

19. Verri WA Jr., Souto FO, Vieira SM, Almeida SC, Fukada SY, Xu D, et al. IL-33 induces neutrophil migration in rheumatoid arthritis and is a target of anti-TNF therapy. Annals of the rheumatic diseases. 2010;69(9):1697–703. Epub 2010/05/18. doi: 10.1136/ard.2009.122655 20472598.

20. Han GW, Zeng LW, Liang CX, Cheng BL, Yu BS, Li HM, et al. Serum levels of IL-33 is increased in patients with ankylosing spondylitis. Clin Rheumatol. 2011;30(12):1583–8. Epub 2011/10/05. doi: 10.1007/s10067-011-1843-x 21968692.

21. Chhiba KD, Hsu CL, Berdnikovs S, Bryce PJ. Transcriptional Heterogeneity of Mast Cells and Basophils upon Activation. Journal of immunology. 2017;198(12):4868–78. doi: 10.4049/jimmunol.1601825 28476932.

22. Brint EK, Xu D, Liu H, Dunne A, McKenzie AN, O'Neill LA, et al. ST2 is an inhibitor of interleukin 1 receptor and Toll-like receptor 4 signaling and maintains endotoxin tolerance. Nature immunology. 2004;5(4):373–9. doi: 10.1038/ni1050 15004556.

23. Hueber AJ, Alves-Filho JC, Asquith DL, Michels C, Millar NL, Reilly JH, et al. IL-33 induces skin inflammation with mast cell and neutrophil activation. European journal of immunology. 2011;41(8):2229–37. Epub 2011/06/16. doi: 10.1002/eji.201041360 21674479.

24. Han H, Roan F, Johnston LK, Smith DE, Bryce PJ, Ziegler SF. IL-33 promotes gastrointestinal allergy in a TSLP-independent manner. Mucosal Immunol. 2018;11(2):394–403. doi: 10.1038/mi.2017.61 28656964; PubMed Central PMCID: PMC5745299.

25. Kondo Y, Yoshimoto T, Yasuda K, Futatsugi-Yumikura S, Morimoto M, Hayashi N, et al. Administration of IL-33 induces airway hyperresponsiveness and goblet cell hyperplasia in the lungs in the absence of adaptive immune system. International immunology. 2008;20(6):791–800. Epub 2008/05/02. doi: 10.1093/intimm/dxn037 18448455.

26. Obata K, Mukai K, Tsujimura Y, Ishiwata K, Kawano Y, Minegishi Y, et al. Basophils are essential initiators of a novel type of chronic allergic inflammation. Blood. 2007;110(3):913–20. doi: 10.1182/blood-2007-01-068718 17409268.

27. Sullivan BM, Liang HE, Bando JK, Wu D, Cheng LE, McKerrow JK, et al. Genetic analysis of basophil function in vivo. Nature immunology. 2011;12(6):527–35. Epub 2011/05/10. doi: 10.1038/ni.2036 21552267; PubMed Central PMCID: PMC3271435.

28. Perrigoue JG, Saenz SA, Siracusa MC, Allenspach EJ, Taylor BC, Giacomin PR, et al. MHC class II-dependent basophil-CD4+ T cell interactions promote T(H)2 cytokine-dependent immunity. Nature immunology. 2009;10(7):697–705. Epub 2009/05/26. doi: 10.1038/ni.1740 19465906; PubMed Central PMCID: PMC2711559.

29. Siracusa MC, Saenz SA, Hill DA, Kim BS, Headley MB, Doering TA, et al. TSLP promotes interleukin-3-independent basophil haematopoiesis and type 2 inflammation. Nature. 2011;477(7363):229–33. Epub 2011/08/16. doi: 10.1038/nature10329 21841801; PubMed Central PMCID: PMC3263308.

30. Schneider E, Petit-Bertron AF, Bricard R, Levasseur M, Ramadan A, Girard JP, et al. IL-33 activates unprimed murine basophils directly in vitro and induces their in vivo expansion indirectly by promoting hematopoietic growth factor production. Journal of immunology. 2009;183(6):3591–7. doi: 10.4049/jimmunol.0900328 19684081.

31. 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. International immunology. 2008;20(8):1019–30. Epub 2008/06/14. doi: 10.1093/intimm/dxn060 18550585.

32. Suzukawa M, Iikura M, Koketsu R, Nagase H, Tamura C, Komiya A, et al. An IL-1 cytokine member, IL-33, induces human basophil activation via its ST2 receptor. Journal of immunology. 2008;181(9):5981–9. doi: 10.4049/jimmunol.181.9.5981 18941187.

33. Kroeger KM, Sullivan BM, Locksley RM. IL-18 and IL-33 elicit Th2 cytokines from basophils via a MyD88- and p38alpha-dependent pathway. J Leukoc Biol. 2009;86(4):769–78. doi: 10.1189/jlb.0708452 19451398; PubMed Central PMCID: PMC2752018.

34. Motomura Y, Morita H, Moro K, Nakae S, Artis D, Endo TA, et al. Basophil-derived interleukin-4 controls the function of natural helper cells, a member of ILC2s, in lung inflammation. Immunity. 2014;40(5):758–71. doi: 10.1016/j.immuni.2014.04.013 24837103.

35. Silver MR, Margulis A, Wood N, Goldman SJ, Kasaian M, Chaudhary D. IL-33 synergizes with IgE-dependent and IgE-independent agents to promote mast cell and basophil activation. Inflamm Res. 2010;59(3):207–18. doi: 10.1007/s00011-009-0088-5 19763788.

36. Cayrol C, Girard JP. IL-33: an alarmin cytokine with crucial roles in innate immunity, inflammation and allergy. Current opinion in immunology. 2014;31:31–7. Epub 2014/10/04. doi: 10.1016/j.coi.2014.09.004 25278425.

37. Moffatt MF, Gut IG, Demenais F, Strachan DP, Bouzigon E, Heath S, et al. A large-scale, consortium-based genomewide association study of asthma. The New England journal of medicine. 2010;363(13):1211–21. doi: 10.1056/NEJMoa0906312 20860503; PubMed Central PMCID: PMC4260321.

38. Jackson DJ, Makrinioti H, Rana BM, Shamji BW, Trujillo-Torralbo MB, Footitt J, et al. IL-33-dependent type 2 inflammation during rhinovirus-induced asthma exacerbations in vivo. American journal of respiratory and critical care medicine. 2014;190(12):1373–82. Epub 2014/10/29. doi: 10.1164/rccm.201406-1039OC 25350863; PubMed Central PMCID: PMC4299647.

39. Pichery M, Mirey E, Mercier P, Lefrancais E, Dujardin A, Ortega N, et al. Endogenous IL-33 Is Highly Expressed in Mouse Epithelial Barrier Tissues, Lymphoid Organs, Brain, Embryos, and Inflamed Tissues: In Situ Analysis Using a Novel Il-33-LacZ Gene Trap Reporter Strain. J Immunol. 2012;188(7):3488–95. Epub 2012/03/01. doi: 10.4049/jimmunol.1101977 22371395.

40. Hardman CS, Panova V, McKenzie AN. IL-33 citrine reporter mice reveal the temporal and spatial expression of IL-33 during allergic lung inflammation. European journal of immunology. 2013;43(2):488–98. doi: 10.1002/eji.201242863 23169007; PubMed Central PMCID: PMC3734634.

41. Tashiro H, Takahashi K, Hayashi S, Kato G, Kurata K, Kimura S, et al. Interleukin-33 from Monocytes Recruited to the Lung Contributes to House Dust Mite-Induced Airway Inflammation in a Mouse Model. PloS one. 2016;11(6):e0157571. Epub 2016/06/17. doi: 10.1371/journal.pone.0157571 27310495; PubMed Central PMCID: PMC4910993.

42. Enoksson M, Moller-Westerberg C, Wicher G, Fallon PG, Forsberg-Nilsson K, Lunderius-Andersson C, et al. Intraperitoneal influx of neutrophils in response to IL-33 is mast cell-dependent. Blood. 2013;121(3):530–6. Epub 2012/10/25. doi: 10.1182/blood-2012-05-434209 23093619.

43. Meephansan J, Tsuda H, Komine M, Tominaga S, Ohtsuki M. Regulation of IL-33 expression by IFN-gamma and tumor necrosis factor-alpha in normal human epidermal keratinocytes. The Journal of investigative dermatology. 2012;132(11):2593–600. Epub 2012/06/08. doi: 10.1038/jid.2012.185 22673732.

44. Allakhverdi Z, Smith DE, Comeau MR, Delespesse G. Cutting edge: The ST2 ligand IL-33 potently activates and drives maturation of human mast cells. Journal of immunology. 2007;179(4):2051–4. Epub 2007/08/07. doi: 10.4049/jimmunol.179.4.2051 17675461.

45. Cho KA, Suh JW, Sohn JH, Park JW, Lee H, Kang JL, et al. IL-33 induces Th17-mediated airway inflammation via mast cells in ovalbumin-challenged mice. Am J Physiol Lung Cell Mol Physiol. 2012;302(4):L429–40. Epub 2011/12/20. doi: 10.1152/ajplung.00252.2011 22180658.

46. 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(7):1526–34. Epub 2008/10/29. doi: 10.1182/blood-2008-05-157818 18955562; PubMed Central PMCID: PMC2644080.

47. Caproni M, Giomi B, Volpi W, Melani L, Schincaglia E, Macchia D, et al. Chronic idiopathic urticaria: infiltrating cells and related cytokines in autologous serum-induced wheals. Clin Immunol. 2005;114(3):284–92. doi: 10.1016/j.clim.2004.10.007 15721839.

48. Ito Y, Satoh T, Takayama K, Miyagishi C, Walls AF, Yokozeki H. Basophil recruitment and activation in inflammatory skin diseases. Allergy. 2011;66(8):1107–13. doi: 10.1111/j.1398-9995.2011.02570.x 21371044.

49. Jin G, Matsushita T, Hamaguchi Y, Le Huu D, Ishii T, Hasegawa M, et al. Basophils and mast cells play critical roles for leukocyte recruitment in IgE-mediated cutaneous reverse passive Arthus reaction. J Dermatol Sci. 2012;67(3):181–9. Epub 2012/07/13. doi: 10.1016/j.jdermsci.2012.06.005 22784785.

50. Venturelli N, Lexmond WS, Ohsaki A, Nurko S, Karasuyama H, Fiebiger E, et al. Allergic skin sensitization promotes eosinophilic esophagitis through the IL-33-basophil axis in mice. The Journal of allergy and clinical immunology. 2016;138(5):1367–80 e5. doi: 10.1016/j.jaci.2016.02.034 27233150.

51. Imai Y, Yasuda K, Sakaguchi Y, Haneda T, Mizutani H, Yoshimoto T, et al. Skin-specific expression of IL-33 activates group 2 innate lymphoid cells and elicits atopic dermatitis-like inflammation in mice. Proceedings of the National Academy of Sciences of the United States of America. 2013;110(34):13921–6. Epub 2013/08/07. doi: 10.1073/pnas.1307321110 23918359; PubMed Central PMCID: PMC3752227.

52. Roediger B, Kyle R, Yip KH, Sumaria N, Guy TV, Kim BS, et al. Cutaneous immunosurveillance and regulation of inflammation by group 2 innate lymphoid cells. Nature immunology. 2013;14(6):564–73. Epub 2013/04/23. doi: 10.1038/ni.2584 23603794; PubMed Central PMCID: PMC4282745.

53. Xue L, Salimi M, Panse I, Mjosberg JM, McKenzie AN, Spits H, et al. Prostaglandin D2 activates group 2 innate lymphoid cells through chemoattractant receptor-homologous molecule expressed on TH2 cells. The Journal of allergy and clinical immunology. 2014;133(4):1184–94. Epub 2014/01/07. doi: 10.1016/j.jaci.2013.10.056 24388011; PubMed Central PMCID: PMC3979107.

54. Marichal T, Tsai M, Galli SJ. Mast cells: potential positive and negative roles in tumor biology. Cancer immunology research. 2013;1(5):269–79. Epub 2014/04/30. doi: 10.1158/2326-6066.CIR-13-0119 24777963.

55. Christy AL, Walker ME, Hessner MJ, Brown MA. Mast cell activation and neutrophil recruitment promotes early and robust inflammation in the meninges in EAE. Journal of autoimmunity. 2013;42:50–61. Epub 2012/12/27. doi: 10.1016/j.jaut.2012.11.003 23267561.

56. Chiba N, Shimada K, Chen S, Jones HD, Alsabeh R, Slepenkin AV, et al. Mast cells play an important role in chlamydia pneumoniae lung infection by facilitating immune cell recruitment into the airway. J Immunol. 2015;194(8):3840–51. Epub 2015/03/11. doi: 10.4049/jimmunol.1402685 25754739; PubMed Central PMCID: PMC4390505.

57. Ganeshan K, Johnston LK, Bryce PJ. TGF-beta1 Limits the Onset of Innate Lung Inflammation by Promoting Mast Cell-Derived IL-6. J Immunol. 2013;190(11):5731–8. Epub 2013/05/01. doi: 10.4049/jimmunol.1203362 23630359.

58. Roussel L, Farias R, Rousseau S. IL-33 is expressed in epithelia from patients with cystic fibrosis and potentiates neutrophil recruitment. The Journal of allergy and clinical immunology. 2013;131(3):913–6. Epub 2012/12/12. doi: 10.1016/j.jaci.2012.10.019 23219168.

59. Baumann C, Bonilla WV, Frohlich A, Helmstetter C, Peine M, Hegazy AN, et al. T-bet- and STAT4-dependent IL-33 receptor expression directly promotes antiviral Th1 cell responses. Proceedings of the National Academy of Sciences of the United States of America. 2015;112(13):4056–61. Epub 2015/04/02. doi: 10.1073/pnas.1418549112 25829541.

60. Townsend MJ, Fallon PG, Matthews DJ, Jolin HE, McKenzie AN. T1/ST2-deficient mice demonstrate the importance of T1/ST2 in developing primary T helper cell type 2 responses. J Exp Med. 2000;191(6):1069–76. Epub 2000/03/23. doi: 10.1084/jem.191.6.1069 10727469; PubMed Central PMCID: PMC2193113.

61. Jin L, Batra S, Douda DN, Palaniyar N, Jeyaseelan S. CXCL1 contributes to host defense in polymicrobial sepsis via modulating T cell and neutrophil functions. Journal of immunology. 2014;193(7):3549–58. Epub 2014/08/31. doi: 10.4049/jimmunol.1401138 25172493; PubMed Central PMCID: PMC4170008.

62. Vukman KV, Metz M, Maurer M, O'Neill SM. Isolation and culture of bone marrow-derived mast cells. Bio-protocol; 2014.


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