IL-33 induces Th17-mediated airway inflammation via mast cells in ovalbumin-challenged mice

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 302, Issue 4, 2012, Pages

  Cho, Kyung Ah ^a   Suh, Jee Won ^a   Sohn, Jung Ho ^b,c   Park, Jung Won ^b   Lee, Hyejin ^a   Kang, JiHee Lee ^a   Woo, So Youn ^a   Cho, Young Joo ^d  

^a Ewha Womans University School of Medicine   (South Korea)

^b Yonsei University College of Medicine   (South Korea)

^c Hanyang University   (South Korea)

^d Mokdong Hospital   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 33; OVALBUMIN;

ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BAGG ALBINO MOUSE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RESPONSE; EOSINOPHIL COUNT; IMMUNOSTIMULATION; IN VITRO STUDY; MALE; MAST CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; RESPIRATORY TRACT INFLAMMATION; TH17 CELL; WILD TYPE;

ANIMALS; ASTHMA; BRONCHOALVEOLAR LAVAGE FLUID; BRONCHOCONSTRICTOR AGENTS; CELL COUNT; CELL DIFFERENTIATION; CYTOKINES; EOSINOPHILS; FEMALE; GENE EXPRESSION; INFLAMMATION; INTERLEUKINS; LUNG; MAST CELLS; METHACHOLINE CHLORIDE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; OVALBUMIN; RECEPTORS, INTERLEUKIN; TH17 CELLS; TH2 CELLS;

EID: 84863022201     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00252.2011     Document Type: Article

References (49)

1. Alcorn JF, Crowe CR, Kolls JK. TH17 cells in asthma and COPD. Annu Rev Physiol 72: 495-516, 2010.
2. Allakhverdi Z, Smith DE, Comeau MR, Delespesse G. Cutting edge: the ST2 ligand IL-33 potently activates and drives maturation of human mast cells. J Immunol 179: 2051-2054, 2007.
3. Boniface K, Diveu C, Morel F, Pedretti N, Froger J, Ravon E, Garcia M, Venereau E, Preisser L, Guignouard E, Guillet G, Dagregorio G, Pene J, Moles JP, Yssel H, Chevalier S, Bernard FX, Gascan H, Lecron JC. Oncostatin M secreted by skin infiltrating T lymphocytes is a potent keratinocyte activator involved in skin inflammation. J Immunol 178: 4615-4622, 2007.
4. Brattig NW, Medina-De la Garza CE, Tischendorf FW. Improved Randolph stain for direct leukocyte differentiation and determination of total eosinophil count in a hemocytometer. Biotech Histochem 68: 255-259, 1993.
5. Cayrol C, Girard JP. The IL-1-like cytokine IL-33 is inactivated after maturation by caspase-1. Proc Natl Acad Sci USA 106: 9021-9026, 2009.
6. Chackerian AA, Oldham ER, Murphy EE, Schmitz J, Pflanz S, Kastelein RA. IL-1 receptor accessory protein and ST2 comprise the IL-33 receptor complex. J Immunol 179: 2551-2555, 2007.
7. Douwes J, Gibson P, Pekkanen J, Pearce N. Non-eosinophilic asthma: importance and possible mechanisms. Thorax 57: 643-648, 2002.
8. Duncan JA, Gao X, Huang MT, O'Connor BP, Thomas CE, Willingham SB, Bergstralh DT, Jarvis GA, Sparling PF, Ting JP. Neisseria gonorrhoeae activates the proteinase cathepsin B to mediate the signaling activities of the NLRP3 and ASC-containing inflammasome. J Immunol 182: 6460-6469, 2009.
9. Fang C, Siew LQ, Corrigan CJ, Ying S. The role of thymic stromal lymphopoietin in allergic inflammation and chronic obstructive pulmonary disease. Arch Immunol Ther Exp (Warsz) 58: 81-90, 2010.
10. Fujiwara M, Hirose K, Kagami S, Takatori H, Wakashin H, Tamachi T, Watanabe N, Saito Y, Iwamoto I, Nakajima H. T-bet inhibits both TH2 cell-mediated eosinophil recruitment and TH17 cell-mediated neutrophil recruitment into the airways. J Allergy Clin Immunol 119: 662-670, 2007.
11. Gombart AF, Kwok SH, Anderson KL, Yamaguchi Y, Torbett BE, Koeffler HP. Regulation of neutrophil and eosinophil secondary granule gene expression by transcription factors C/EBP epsilon and PU.1. Blood 101: 3265-3273, 2003.
12. Hashizume M, Hayakawa N, Mihara M. IL-6 trans-signalling directly induces RANKL on fibroblast-like synovial cells and is involved in RANKL induction by TNF-alpha and IL-17. Rheumatology (Oxford) 47: 1635-1640, 2008.
13. Ho LH, Ohno T, Oboki K, Kajiwara N, Suto H, Iikura M, Okayama Y, Akira S, Saito H, Galli SJ, Nakae S. IL-33 induces IL-13 production by mouse mast cells independently of IgE-FcepsilonRI signals. J Leukoc Biol 82: 1481-1490, 2007.
14. Holgate ST. Pathogenesis of asthma. Clin Exp Allergy 38: 872-897, 2008.
15. Iikura M, Suto H, Kajiwara N, Oboki K, Ohno T, Okayama Y, Saito H, Galli SJ, Nakae S. IL-33 can promote survival, adhesion and cytokin production in human mast cells. Lab Invest 87: 971-978, 2007.
16. Kearley J, Buckland KF, Mathie SA, Lloyd CM. Resolution of allergic inflammation and airway hyperreactivity is dependent upon disruption ofthe T1/ST2-IL-33 pathway. Am J Respir Crit Care Med 179: 772-781, 2009.
17. Kim JE, Kim BJ, Jeong MS, Seo SJ, Kim MN, Hong CK, Ro BI. Expression and modulation of LL-37 in normal human keratinocytes, HaCaT cells, and inflammatory skin diseases. J Korean Med Sci 20: 649-654, 2005.
18. Koh Y, Hybertson BM, Jepson EK, Cho OJ, Repine JE. Cytokineinduced neutrophil chemoattractant is necessary for interleukin-1-induced lung leak in rats. J Appl Physiol 79: 472-478, 1995.
19. Kondo Y, Yoshimoto T, Yasuda K, Futatsugi-Yumikura S, Morimoto M, Hayashi N, Hoshino T, Fujimoto J, Nakanishi K. Administration of IL-33 induces airway hyperresponsiveness and goblet cell hyperplasia in the lungs in the absence of adaptive immune system. Int Immunol 20: 791-800, 2008.
20. Laan M, Cui ZH, Hoshino H, Lotvall J, Sjostrand M, Gruenert DC, Skoogh BE, Linden A. Neutrophil recruitment by human IL-17 via C-X-C chemokine release in the airways. J Immunol 162: 2347-2352, 1999.
21. Liu X, Li M, Wu Y, Zhou Y, Zeng L, Huang T. Anti-IL-33 antibody treatment inhibits airway inflammation in a murine model of allergic asthma. Biochem Biophys Res Commun 386: 181-185, 2009.
22. Lochner M, Peduto L, Cherrier M, Sawa S, Langa F, Varona R, Riethmacher D, Si-Tahar M, Di Santo JP, Eberl G. In vivo equilibrium of proinflammatory IL-17 and regulatory IL-10 Foxp3 RORgamma t T cells. J Exp Med 205: 1381-1393, 2008.
23. Mattes J, Yang M, Mahalingam S, Kuehr J, Webb DC, Simson L, Hogan SP, Koskinen A, McKenzie AN, Dent LA, Rothenberg ME, Matthaei KI, Young IG, Foster PS. Intrinsic defect in T cell production of interleukin (IL)-13 in the absence of both IL-5 and eotaxin precludes the development of eosinophilia and airways hyperreactivity in experimental asthma. J Exp Med 195: 1433-1444, 2002.
24. McKinley L, Alcorn JF, Peterson A, Dupont RB, Kapadia S, Logar A, Henry A, Irvin CG, Piganelli JD, Ray A, Kolls JK. TH17 cells mediate steroid-resistant airway inflammation and airway hyperresponsiveness in mice. J Immunol 181: 4089-4097, 2008.
25. Meng G, Zhang F, Fuss I, Kitani A, Strober W. A mutation in the Nlrp3 gene causing inflammasome hyperactivation potentiates Th17 cell-dominant immune responses. Immunity 30: 860-874, 2009.
26. Moulin D, Donze O, Talabot-Ayer D, Mezin F, Palmer G, Gabay C. Interleukin (IL)-33 induces the release of pro-inflammatory mediators by mast cells. Cytokine 40: 216-225, 2007.
27. Nakae S, Suto H, Berry GJ, Galli SJ. Mast cell-derived TNF can promote Th17 cell-dependent neutrophil recruitment in ovalbumin-challenged OTII mice. Blood 109: 3640-3648, 2007.
28. Nakajima H, Takatsu K. Role of cytokines in allergic airway inflammation. Int Arch Allergy Immunol 142: 265-273, 2007.
29. Nigrovic PA, Binstadt BA, Monach PA, Johnsen A, Gurish M, Iwakura Y, Benoist C, Mathis D, Lee DM. Mast cells contribute to initiation of autoantibody-mediated arthritis via IL-1. Proc Natl Acad Sci USA 104: 2325-2330, 2007.
30. 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 113: 1526-1534, 2009.
31. Prefontaine D, Lajoie-Kadoch S, Foley S, Audusseau S, Olivenstein R, Halayko AJ, Lemiere C, Martin JG, Hamid Q. Increased expression of IL-33 in severe asthma: evidence of expression by airway smooth muscle cells. J Immunol 183: 5094-5103, 2009.
32. Rank MA, Kobayashi T, Kozaki H, Bartemes KR, Squillace DL, Kita H. IL-33-activated dendritic cells induce an atypical TH2-type response. J Allergy Clin Immunol 123: 1047-1054, 2009.
33. Roussel L, Houle F, Chan C, Yao Y, Berube J, Olivenstein R, Martin JG, Huot J, Hamid Q, Ferri L, Rousseau S. IL-17 promotes p38 MAPK-dependent endothelial activation enhancing neutrophil recruitment to sites of inflammation. J Immunol 184: 4531-4537, 2010.
34. Schnyder B, Schnyder-Candrian S, Pansky A, Schmitz ML, Heim M, Ryffel B, Moser R. IL-17 reduces TNF-induced Rantes and VCAM-1 expression. Cytokine 31: 191-202, 2005.
35. Seki T, Kumagai T, Kwansa-Bentum B, Furushima-Shimogawara R, Anyan WK, Miyazawa Y, Iwakura Y, Ohta N. IL-4/IL-13 suppress excessive neutrophil infiltration and hepatocyte damage during acute murine schistosomiasis japonica. Infect Immun 80: 159-168, 2012.
36. Simpson JL, Grissell TV, Douwes J, Scott RJ, Boyle MJ, Gibson PG. Innate immune activation in neutrophilic asthma and bronchiectasis. Thorax 62: 211-218, 2007.
37. Smith DE. IL-33: a tissue derived cytokine pathway involved in allergic inflammation and asthma. Clin Exp Allergy 40: 200-208, 2010.
38. Sutton CE, Lalor SJ, Sweeney CM, Brereton CF, Lavelle EC, Mills KH. Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity 31: 331-341, 2009.
39. Turnquist HR, Sumpter TL, Tsung A, Zahorchak AF, Nakao A, Nau GJ, Liew FY, Geller DA, Thomson AW. IL-1beta-driven ST2L expression promotes maturation resistance in rapamycin-conditioned dendritic cells. J Immunol 181: 62-72, 2008.
40. Verri WA Jr, Guerrero AT, Fukada SY, Valerio DA, Cunha TM, Xu D, Ferreira SH, Liew FY, Cunha FQ. IL-33 mediates antigen-induced cutaneous and articular hypernociception in mice. Proc Natl Acad Sci USA 105: 2723-2728, 2008.
41. Walsh ER, Sahu N, Kearley J, Benjamin E, Kang BH, Humbles A, August A. Strain-specific requirement for eosinophils in the recruitment of T cells to the lung during the development of allergic asthma. J Exp Med 205: 1285-1292, 2008.
42. Walter DM, McIntire JJ, Berry G, McKenzie AN, Donaldson DD, DeKruyff RH, Umetsu DT. Critical role for IL-13 in the development of allergen-induced airway hyperreactivity. J Immunol 167: 4668-4675, 2001.
43. Wang YH, Angkasekwinai P, Lu N, Voo KS, Arima K, Hanabuchi S, Hippe A, Corrigan CJ, Dong C, Homey B, Yao Z, Ying S, Huston DP, Liu YJ. IL-25 augments type 2 immune responses by enhancing the expansion and functions of TSLP-DC-activated Th2 memory cells. J Exp Med 204: 1837-1847, 2007.
44. Wenzel SE, Schwartz LB, Langmack EL, Halliday JL, Trudeau JB, Gibbs RL, Chu HW. Evidence that severe asthma can be divided pathologically into two inflammatory subtypes with distinct physiologic and clinical characteristics. Am J Respir Crit Care Med 160: 1001-1008, 1999.
45. Wilson NJ, Boniface K, Chan JR, McKenzie BS, Blumenschein WM, Mattson JD, Basham B, Smith K, Chen T, Morel F, Lecron JC, Kastelein RA, Cua DJ, McClanahan TK, Bowman EP, de Waal Malefyt R. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat Immunol 8: 950-957, 2007.
46. Xu D, Jiang HR, Kewin P, Li Y, Mu R, Fraser AR, Pitman N, Kurowska-Stolarska M, McKenzie AN, McInnes IB, Liew FY. IL-33 exacerbates antigen-induced arthritis by activating mast cells. Proc Natl Acad Sci USA 105: 10913-10918, 2008.
47. Yang M, Kumar RK, Foster PS. Interferon-gamma and pulmonary macrophages contribute to the mechanisms underlying prolonged airway hyperresponsiveness. Clin Exp Allergy 40: 163-173, 2010.
48. Yu C, Cantor AB, Yang H, Browne C, Wells RA, Fujiwara Y, Orkin SH. Targeted deletion of a high-affinity GATA-binding site in the GATA-1 promoter leads to selective loss of the eosinophil lineage in vivo. J Exp Med 195: 1387-1395, 2002.
49. Zhou Q, Mrowietz U, Rostami-Yazdi M. Oxidative stress in the pathogenesis of psoriasis. Free Radic Biol Med 47: 891-905, 2009.