Airway epithelial cells initiate the allergen response through transglutaminase 2 by inducing IL-33 expression and a subsequent Th2 response

Respiratory Research

Volumn 14, Issue 1, 2013, Pages

  Oh, Keunhee ^a,b,c   Seo, Myung Won ^a   Lee, Ga Young ^a   Byoun, Ok Jin ^a   Kang, Hye Ryun ^d   Cho, Sang Heon ^d   Lee, Dong Sup ^a,b,c,d  

^a Laboratory of Immunology and Cancer Biology   (South Korea)

^b Cancer Research Center   (South Korea)

^c Transplantation Research Institute   (South Korea)

^d Seoul National University College of Medicine   (South Korea)

Author keywords

Animal models; Asthma; Epithelium; IL 33; Transglutaminase 2

Indexed keywords

ALLERGEN; GAMMA INTERFERON; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 33; INTERLEUKIN 4; MERCAPTAMINE; OVALBUMIN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; GUANINE NUCLEOTIDE BINDING PROTEIN; INTERLEUKIN 33, MOUSE; INTERLEUKIN DERIVATIVE; INTERLEUKIN-33, MOUSE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE;

ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHEMOTAXIS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOKINE PRODUCTION; EOSINOPHIL; EPITHELIUM CELL; FEMALE; FLOW CYTOMETRY; LUNG LAVAGE; LYMPHOCYTE DIFFERENTIATION; MACROPHAGE; MOUSE; NONHUMAN; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RESPIRATORY EPITHELIUM; RESPIRATORY TRACT ALLERGY; SIGNAL TRANSDUCTION; TH17 CELL; TH2 CELL; WILD TYPE; ANIMAL; ASTHMA; BAGG ALBINO MOUSE; CYTOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; IMMUNOLOGY; INFLAMMATION; LUNG; METABOLISM; PATHOLOGY; RESPIRATORY TRACT MUCOSA;

ALLERGENS; ANIMALS; ASTHMA; BRONCHOALVEOLAR LAVAGE FLUID; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION; GTP-BINDING PROTEINS; INFLAMMATION; INTERLEUKINS; LUNG; MICE; MICE, INBRED BALB C; MICROSCOPY, CONFOCAL; RESPIRATORY MUCOSA; SIGNAL TRANSDUCTION; TH2 CELLS; TRANSGLUTAMINASES;

EID: 84874790984     PISSN: 14659921     EISSN: 1465993X     Source Type: Journal    
DOI: 10.1186/1465-9921-14-35     Document Type: Article

References (36)

1. Elias JA, Lee CG, Zheng T, Ma B, Homer RJ, Zhu Z. New insights into the pathogenesis of asthma. J Clin Invest 2003, 111:291-297. 151878, 12569150.
2. Araujo MI, Campos RA, Cardoso LS, Oliveira SC, Carvalho EM. Immunomodulation of the allergic inflammatory response: new developments. Inflamm Allergy Drug Targets 2010, 9:73-82. 10.2174/187152810791292836, 20402649.
3. Holgate ST. Innate and adaptive immune responses in asthma. Nat Med 2012, 18:673-683. 10.1038/nm.2731, 22561831.
4. Saenz SA, Taylor BC, Artis D. Welcome to the neighborhood: epithelial cell-derived cytokines license innate and adaptive immune responses at mucosal sites. Immunol Rev 2008, 226:172-190. 10.1111/j.1600-065X.2008.00713.x, 2683382, 19161424.
5. Tam A, Wadsworth S, Dorscheid D, Man SF, Sin DD. The airway epithelium: more than just a structural barrier. Ther Adv Respir Dis 2011, 5:255-273. 10.1177/1753465810396539, 21372121.
6. Vareille M, Kieninger E, Edwards MR, Regamey N. The airway epithelium: soldier in the fight against respiratory viruses. Clin Microbiol Rev 2011, 24:210-229. 10.1128/CMR.00014-10, 3021210, 21233513.
7. Evans SE, Xu Y, Tuvim MJ, Dickey BF. Inducible innate resistance of lung epithelium to infection. Annu Rev Physiol 2010, 72:413-435. 10.1146/annurev-physiol-021909-135909, 20148683.
8. Oh K, Park HB, Byoun OJ, Shin DM, Jeong EM, Kim YW, Kim YS, Melino G, Kim IG, Lee DS. Epithelial transglutaminase 2 is needed for T cell interleukin-17 production and subsequent pulmonary inflammation and fibrosis in bleomycin-treated mice. J Exp Med 2011, 208:1707-1719. 10.1084/jem.20101457, 3149214, 21746810.
9. Fesus L, Piacentini M. Transglutaminase 2: an enigmatic enzyme with diverse functions. Trends Biochem Sci 2002, 27:534-539. 10.1016/S0968-0004(02)02182-5, 12368090.
10. Lorand L, Graham RM. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat Rev Mol Cell Biol 2003, 4:140-156. 10.1038/nrm1014, 12563291.
11. Weinberg JB, Pippen AM, Greenberg CS. Extravascular fibrin formation and dissolution in synovial tissue of patients with osteoarthritis and rheumatoid arthritis. Arthritis Rheum 1991, 34:996-1005. 10.1002/art.1780340809, 1677574.
12. Rose DM, Sydlaske AD, Agha-Babakhani A, Johnson K, Terkeltaub R. Transglutaminase 2 limits murine peritoneal acute gout-like inflammation by regulating macrophage clearance of apoptotic neutrophils. Arthritis Rheum 2006, 54:3363-3371. 10.1002/art.22137, 17009310.
13. Shweke N, Boulos N, Jouanneau C, Vandermeersch S, Melino G, Dussaule JC, Chatziantoniou C, Ronco P, Boffa JJ. Tissue transglutaminase contributes to interstitial renal fibrosis by favoring accumulation of fibrillar collagen through TGF-beta activation and cell infiltration. Am J Pathol 2008, 173:631-642. 10.2353/ajpath.2008.080025, 2527082, 18688035.
14. Sollid LM, Jabri B. Celiac disease and transglutaminase 2: a model for posttranslational modification of antigens and HLA association in the pathogenesis of autoimmune disorders. Curr Opin Immunol 2011, 23:732-738. 10.1016/j.coi.2011.08.006, 3428143, 21917438.
15. Lee SM, Jeong EM, Jeong J, Shin DM, Lee HJ, Kim HJ, Lim J, Lee JH, Cho SY, Kim MK, Wee WR, Lee JH, Kim IG. Cysteamine prevents the development of lens opacity in a rat model of selenite-induced cataract. Invest Ophthalmol Vis Sci 2012, 53:1452-1459. 10.1167/iovs.11-8636, 22281827.
16. Karpuj MV, Becher MW, Springer JE, Chabas D, Youssef S, Pedotti R, Mitchell D, Steinman L. Prolonged survival and decreased abnormal movements in transgenic model of Huntington disease, with administration of the transglutaminase inhibitor cystamine. Nat Med 2002, 8:143-149. 10.1038/nm0202-143, 11821898.
17. Szondy Z, Sarang Z, Molnar P, Nemeth T, Piacentini M, Mastroberardino PG, Falasca L, Aeschlimann D, Kovacs J, Kiss I, Szegezdi E, Lakos G, Rajnavolgyi E, Birckbichler PJ, Melino G, Fesus L. Transglutaminase 2-/- mice reveal a phagocytosis-associated crosstalk between macrophages and apoptotic cells. Proc Natl Acad Sci USA 2003, 100:7812-7817. 10.1073/pnas.0832466100, 164670, 12810961.
18. Falasca L, Farrace MG, Rinaldi A, Tuosto L, Melino G, Piacentini M. Transglutaminase type II is involved in the pathogenesis of endotoxic shock. J Immunol 2008, 180:2616-2624.
19. Oh K, Park HB, Seo MW, Byoun OJ, Lee DS. Transglutaminase 2 exacerbates experimental autoimmune encephalomyelitis through positive regulation of encephalitogenic T cell differentiation and inflammation. Clin Immunol 2012, 145:122-132. 10.1016/j.clim.2012.08.009, 23001131.
20. Kim Y, Eom S, Kim K, Lee YS, Choe J, Hahn JH, Lee H, Kim YM, Ha KS, Ro JY, Jeoung D. Transglutaminase II interacts with rac1, regulates production of reactive oxygen species, expression of snail, secretion of Th2 cytokines and mediates in vitro and in vivo allergic inflammation. Mol Immunol 2010, 47:1010-1022. 10.1016/j.molimm.2009.11.017, 20004474.
21. Sohn J, Kim TI, Yoon YH, Kim JY, Kim SY. Novel transglutaminase inhibitors reverse the inflammation of allergic conjunctivitis. J Clin Invest 2003, 111:121-128. 151832, 12511595.
22. Kim DY, Park BS, Hong GU, Lee BJ, Park JW, Kim SY, Ro JY. Anti-inflammatory effects of the R2 peptide, an inhibitor of transglutaminase 2, in a mouse model of allergic asthma, induced by ovalbumin. Br J Pharmacol 2011, 162:210-225. 10.1111/j.1476-5381.2010.01033.x, 3012417, 20840469.
23. Hur GY, Kim SH, Park SM, Ye YM, Kim CW, Jang AS, Park CS, Hong CS, Park HS. Tissue transglutaminase can be involved in airway inflammation of toluene diisocyanate-induced occupational asthma. J Clin Immunol 2009, 29:786-794. 10.1007/s10875-009-9314-8, 19562471.
24. Hallstrand TS, Wurfel MM, Lai Y, Ni Z, Gelb MH, Altemeier WA, Beyer RP, Aitken ML, Henderson WR. Transglutaminase 2, a novel regulator of eicosanoid production in asthma revealed by genome-wide expression profiling of distinct asthma phenotypes. PLoS One 2010, 5:e8583. 10.1371/journal.pone.0008583, 2797392, 20052409.
25. Pre'fontaine D, Nadigel J, Chouiali F, Audusseau S, Semlali A, Chakir J, Martin JG, Hamid Q. Increased IL-33 expression by epithelial cells in bronchial asthma. J Allergy Clin Immunol 2010, 125:752-754. 10.1016/j.jaci.2009.12.935, 20153038.
26. Hayakawa H, Hayakawa M, Kume A, Tominaga S. Soluble ST2 blocks interleukin-33 signaling in allergic airway inflammation. J Biol Chem 2007, 282:26369-26380. 10.1074/jbc.M704916200, 17623648.
27. 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 2008, 20:791-800. 10.1093/intimm/dxn037, 18448455.
28. Zhiguang X, Wei C, Steven R, Wei D, Wei Z, Rong M, Zhanguo L, Lianfeng Z. Over-expression of IL-33 leads to spontaneous pulmonary inflammation in mIL-33 transgenic mice. Immunol Lett 2010, 131:159-165. 10.1016/j.imlet.2010.04.005, 20412815.
29. Oboki K, Ohno T, Kajiwara N, Arae K, Morita H, Ishii A, Nambu A, Abe T, Kiyonari H, Matsumoto K, Sudo K, Okumura K, Saito H, Nakae S. IL-33 is a crucial amplifier of innate rather than acquired immunity. Proc Natl Acad Sci USA 2010, 107:18581-18586. 10.1073/pnas.1003059107, 2972966, 20937871.
30. Coyle AJ, Lloyd C, Tian J, Nguyen T, Erikkson C, Wang L, Ottoson P, Persson P, Delaney T, Lehar S, Lin S, Poisson L, Meisel C, Kamradt T, Bjerke T, Levinson D, Gutierrez-Ramos JC. Crucial role of the interleukin 1 receptor family member T1/ST2 in T helper cell type 2-mediated lung mucosal immune responses. J Exp Med 1999, 190:895-902. 10.1084/jem.190.7.895, 2195643, 10510079.
31. Milovanovic M, Volarevic V, Radosavljevic G, Jovanovic I, Pejnovic N, Arsenijevic N, Lukic ML. IL-33/ST2 axis in inflammation and immunopathology. Immunol Res 2012, 52:89-99. 10.1007/s12026-012-8283-9, 22392053.
32. Humphreys NE, Xu D, Hepworth MR, Liew FY, Grencis RK. IL-33, a potent inducer of adaptive immunity to intestinal nematodes. J Immunol 2008, 180:2443-2449.
33. Kouzaki H, Iijima K, Kobayashi T, O'Grady SM, Kita H. The danger signal, extracellular ATP, is a sensor for an airborne allergen and triggers IL-33 release and innate Th2-type responses. J Immunol 2011, 186:4375-4387. 10.4049/jimmunol.1003020, 3062674, 21357533.
34. Swamy M, Jamora C, Havran W, Hayday A. Epithelial decision makers: in search of the 'epimmunome'. Nat Immunol 2010, 11:656-665. 10.1038/ni.1905, 2950874, 20644571.
35. Proud D, Leigh R. Epithelial cells and airway diseases. Immunol Rev 2011, 242:186-204. 10.1111/j.1600-065X.2011.01033.x, 21682746.
36. Bartemes KR, Kita H. Dynamic role of epithelium-derived cytokines in asthma. Clin Immunol 2012, 143:222-235. 10.1016/j.clim.2012.03.001, 22534317.