IL-33 drives eosinophil infiltration and pathogenic type 2 helper T-cell immune responses leading to chronic experimental ileitis

American Journal of Pathology

Volumn 186, Issue 4, 2016, Pages 885-898

  De Salvo, Carlo ^a,b   Wang, Xiao Ming ^a   Pastorelli, Luca ^a,b   Mattioli, Benedetta ^a   Omenetti, Sara ^a   Buela, Kristine A ^a   Chowdhry, Saleem ^a   Garg, Rekha R ^a   Goodman, Wendy A ^a   Rodriguez Palacios, Alex ^a   Smith, Dirk E ^c   Abbott, Derek W ^a   Cominelli, Fabio ^a   Bamias, Giorgos ^d   Xin, Wei ^a   Lee, James J ^e   Vecchi, Maurizio ^b   Pizarro, Theresa T ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MILAN   (Italy)

^c AMGEN INC   (United States)

^d UNIVERSITY OF ATHENS   (Greece)

^e MAYO GRADUATE SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EOTAXIN; INTERLEUKIN 33; CYTOKINE; IL33 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CELLULAR IMMUNITY; CHRONIC DISEASE; COLON MUCOSA; CONTROLLED STUDY; DISEASE COURSE; EOSINOPHIL INFILTRATION; EOSINOPHILIA; EXPERIMENTAL DISEASE; HUMAN; HUMAN TISSUE; ILEITIS; IN VIVO STUDY; INTESTINE MUCOSA; MICROBIOME; MOUSE; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TH2 CELL; UPREGULATION; ANIMAL; CYTOLOGY; DISEASE MODEL; EOSINOPHIL; IMMUNOLOGY; INFLAMMATION; METABOLISM; PATHOLOGY;

ANIMALS; CYTOKINES; DISEASE MODELS, ANIMAL; EOSINOPHILS; ILEITIS; INFLAMMATION; INTERLEUKIN-33; INTESTINAL MUCOSA; MICE; TH2 CELLS; UP-REGULATION;

EID: 84962508048     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2015.11.028     Document Type: Article

References (50)

1. J. Schmitz, A. Owyang, E. Oldham, Y. Song, E. Murphy, T.K. McClanahan, G. Zurawski, M. Moshrefi, J. Qin, X. Li, D.M. Gorman, J.F. Bazan, and R.A. Kastelein 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 23 2005 479 490
2. V. Carriere, L. Roussel, N. Ortega, D.A. Lacorre, L. Americh, L. Aguilar, G. Bouche, and J.P. Girard IL-33, the IL-1-like cytokine ligand for ST2 receptor, is a chromatin-associated nuclear factor in vivo Proc Natl Acad Sci U S A 104 2007 282 287
3. L. Pastorelli, R.R. Garg, S.B. Hoang, L. Spina, B. Mattioli, M. Scarpa, C. Fiocchi, M. Vecchi, and T.T. Pizarro Epithelial-derived IL-33 and its receptor ST2 are dysregulated in ulcerative colitis and in experimental Th1/Th2 driven enteritis Proc Natl Acad Sci U S A 107 2010 8017 8022
4. D.R. Neill, S.H. Wong, A. Bellosi, R.J. Flynn, M. Daly, T.K. Langford, C. Bucks, C.M. Kane, P.G. Fallon, R. Pannell, H.E. Jolin, and A.N. McKenzie Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity Nature 464 2010 1367 1370
5. M. Kurowska-Stolarska, P. Kewin, G. Murphy, R.C. Russo, B. Stolarski, C.C. Garcia, M. Komai-Koma, N. Pitman, Y. Li, W. Niedbala, A.N. McKenzie, M.M. Teixeira, F.Y. Liew, and D. Xu IL-33 induces antigen-specific IL-5+ T cells and promotes allergic-induced airway inflammation independent of IL-4 J Immunol 181 2008 4780 4790
6. D. Xu, H.R. Jiang, P. Kewin, Y. Li, R. Mu, A.R. Fraser, N. Pitman, M. Kurowska-Stolarska, A.N. McKenzie, I.B. McInnes, and F.Y. Liew IL-33 exacerbates antigen-induced arthritis by activating mast cells Proc Natl Acad Sci U S A 105 2008 10913 10918
7. G. Palmer, D. Talabot-Ayer, C. Lamacchia, D. Toy, C.A. Seemayer, S. Viatte, A. Finckh, D.E. Smith, and C. Gabay Inhibition of interleukin-33 signaling attenuates the severity of experimental arthritis Arthritis Rheum 60 2009 738 749
8. B. Stolarski, M. Kurowska-Stolarska, P. Kewin, D. Xu, and F.Y. Liew IL-33 exacerbates eosinophil-mediated airway inflammation J Immunol 185 2010 3472 3480
9. L.Y. Hung, I.P. Lewkowich, L.A. Dawson, J. Downey, Y. Yang, D.E. Smith, and D.R. Herbert IL-33 drives biphasic IL-13 production for noncanonical Type 2 immunity against hookworms Proc Natl Acad Sci U S A 110 2013 282 287
10. A. Mishra, S.P. Hogan, J.J. Lee, P.S. Foster, and M.E. Rothenberg Fundamental signals that regulate eosinophil homing to the gastrointestinal tract J Clin Invest 103 1999 1719 1727
11. S.P. Hogan, H.F. Rosenberg, R. Moqbel, S. Phipps, P.S. Foster, P. Lacy, A.B. Kay, and M.E. Rothenberg Eosinophils: biological properties and role in health and disease Clin Exp Allergy 38 2008 709 750
12. M. Lampinen, A. Ronnblom, K. Amin, G. Kristjansson, F. Rorsman, P. Sangfelt, B. Safsten, M. Wagner, A. Wanders, O. Winqvist, and M. Carlson Eosinophil granulocytes are activated during the remission phase of ulcerative colitis Gut 54 2005 1714 1720
13. M. Lampinen, M. Backman, O. Winqvist, F. Rorsman, A. Ronnblom, P. Sangfelt, and M. Carlson Different regulation of eosinophil activity in Crohn's disease compared with ulcerative colitis J Leukoc Biol 84 2008 1392 1399
14. R. Ahrens, A. Waddell, L. Seidu, C. Blanchard, R. Carey, E. Forbes, M. Lampinen, T. Wilson, E. Cohen, K. Stringer, E. Ballard, A. Munitz, H. Xu, N. Lee, J.J. Lee, M.E. Rothenberg, L. Denson, and S.P. Hogan Intestinal macrophage/epithelial cell-derived CCL11/eotaxin-1 mediates eosinophil recruitment and function in pediatric ulcerative colitis J Immunol 181 2008 7390 7399
15. M. Lampinen, A. Waddell, R. Ahrens, M. Carlson, and S.P. Hogan CD14+CD33+ myeloid cell-CCL11-eosinophil signature in ulcerative colitis J Leukoc Biol 94 2013 1061 1070
16. J.B. Seidelin, J.T. Bjerrum, M. Coskun, B. Widjaya, B. Vainer, and O.H. Nielsen IL-33 is upregulated in colonocytes of ulcerative colitis Immunol Lett 128 2010 80 85
17. C.J. Beltran, L.E. Nunez, D. Diaz-Jimenez, N. Farfan, E. Candia, C. Heine, F. Lopez, M.J. Gonzalez, R. Quera, and M.A. Hermoso Characterization of the novel ST2/IL-33 system in patients with inflammatory bowel disease Inflamm Bowel Dis 16 2010 1097 1107
18. A. Kobori, Y. Yagi, H. Imaeda, H. Ban, S. Bamba, T. Tsujikawa, Y. Saito, Y. Fujiyama, and A. Andoh Interleukin-33 expression is specifically enhanced in inflamed mucosa of ulcerative colitis J Gastroenterol 45 2010 999 1007
19. J. Sponheim, J. Pollheimer, T. Olsen, J. Balogh, C. Hammarstrom, T. Loos, M. Kasprzycka, D.R. Sorensen, H.R. Nilsen, A.M. Kuchler, M.H. Vatn, and G. Haraldsen Inflammatory bowel disease-associated interleukin-33 is preferentially expressed in ulceration-associated myofibroblasts Am J Pathol 177 2010 2804 2815
20. K. Oboki, T. Ohno, N. Kajiwara, K. Arae, H. Morita, A. Ishii, A. Nambu, T. Abe, H. Kiyonari, K. Matsumoto, K. Sudo, K. Okumura, H. Saito, and S. Nakae IL-33 is a crucial amplifier of innate rather than acquired immunity Proc Natl Acad Sci U S A 107 2010 18581 18586
21. H. Imaeda, A. Andoh, T. Aomatsu, K. Uchiyama, S. Bamba, T. Tsujikawa, Y. Naito, and Y. Fujiyama Interleukin-33 suppresses Notch ligand expression and prevents goblet cell depletion in dextran sulfate sodium-induced colitis Int J Mol Med 28 2011 573 578
22. R. Rani, A.G. Smulian, D.R. Greaves, S.P. Hogan, and D.R. Herbert TGF-beta limits IL-33 production and promotes the resolution of colitis through regulation of macrophage function Eur J Immunol 41 2011 2000 2009
23. M.A. Sedhom, M. Pichery, J.R. Murdoch, B. Foligne, N. Ortega, S. Normand, K. Mertz, D. Sanmugalingam, L. Brault, T. Grandjean, E. Lefrancais, P.G. Fallon, V. Quesniaux, L. Peyrin-Biroulet, G. Cathomas, T. Junt, M. Chamaillard, J.P. Girard, and B. Ryffel Neutralisation of the interleukin-33/ST2 pathway ameliorates experimental colitis through enhancement of mucosal healing in mice Gut 62 2013 1714 1723
24. L. Duan, J. Chen, H. Zhang, H. Yang, P. Zhu, A. Xiong, Q. Xia, F. Zheng, Z. Tan, F. Gong, and M. Fang Interleukin-33 ameliorates experimental colitis through promoting Th2/Foxp3(+) regulatory T-cell responses in mice Mol Med 18 2012 753 761
25. P. Groß, K. Doser, W. Falk, F. Obermeier, and C. Hofmann IL-33 attenuates development and perpetuation of chronic intestinal inflammation Inflamm Bowel Dis 18 2012 1900 1909
26. T.T. Pizarro, L. Pastorelli, G. Bamias, R.R. Garg, B.K. Reuter, J.R. Mercado, M. Chieppa, K.O. Arseneau, K. Ley, and F. Cominelli SAMP1/YitFc mouse strain: a spontaneous model of Crohn's disease-like ileitis Inflamm Bowel Dis 17 2011 2566 2584
27. S. Matsumoto, Y. Okabe, H. Setoyama, K. Takayama, J. Ohtsuka, H. Funahashi, A. Imaoka, Y. Okada, and Y. Umesaki Inflammatory bowel disease-like enteritis and caecitis in a senescence accelerated mouse P1/Yit strain Gut 43 1998 71 78
28. M.M. Kosiewicz, C.C. Nast, A. Krishnan, J. Rivera-Nieves, C.A. Moskaluk, S. Matsumoto, K. Kozaiwa, and F. Cominelli Th1-type responses mediate spontaneous ileitis in a novel murine model of Crohn's disease J Clin Invest 107 2001 695 702
29. G. Bamias, C. Martin, M. Mishina, W.G. Ross, J. Rivera-Nieves, M. Marini, and F. Cominelli Proinflammatory effects of TH2 cytokines in a murine model of chronic small intestinal inflammation Gastroenterology 128 2005 654 666
30. C. Protheroe, S.A. Woodruff, G. de Petris, V. Mukkada, S.I. Ochkur, S. Janarthanan, J.C. Lewis, S. Pasha, T. Lunsford, L. Harris, V.K. Sharma, M.P. McGarry, N.A. Lee, G.T. Furuta, and J.J. Lee A novel histologic scoring system to evaluate mucosal biopsies from patients with eosinophilic esophagitis Clin Gastroenterol Hepatol 7 2009 749 755.e11
31. G. Bamias, A. Okazawa, J. Rivera-Nieves, K.O. Arseneau, S.A. De La Rue, T.T. Pizarro, and F. Cominelli Commensal bacteria exacerbate intestinal inflammation but are not essential for the development of murine ileitis J Immunol 178 2007 1809 1818
32. G. Woerly, N. Roger, S. Loiseau, D. Dombrowicz, A. Capron, and M. Capron Expression of CD28 and CD86 by human eosinophils and role in the secretion of type 1 cytokines (interleukin 2 and interferon gamma): inhibition by immunoglobulin a complexes J Exp Med 190 1999 487 495
33. J.C. Masterson, E.N. McNamee, P. Jedlicka, S. Fillon, J. Ruybal, L. Hosford, J. Rivera-Nieves, J.J. Lee, and G.T. Furuta CCR3 blockade attenuates eosinophilic ileitis and associated remodeling Am J Pathol 179 2011 2302 2314
34. J.C. Masterson, K.E. Capocelli, L. Hosford, K. Biette, E.N. McNamee, E.F. de Zoeten, R. Harris, S.D. Fernando, P. Jedlicka, C. Protheroe, J.J. Lee, and G.T. Furuta Eosinophils and IL-33 perpetuate chronic inflammation and fibrosis in a pediatric population with stricturing Crohn's ileitis Inflamm Bowel Dis 21 2015 2429 2440
35. H. Takedatsu, K. Mitsuyama, S. Matsumoto, K. Handa, A. Suzuki, H. Takedatsu, H. Funabashi, Y. Okabe, T. Hara, A. Toyonaga, and M. Sata Interleukin-5 participates in the pathogenesis of ileitis in SAMP1/Yit mice Eur J Immunol 34 2004 1561 1569
36. N. Zimmermann, G.K. Hershey, P.S. Foster, and M.E. Rothenberg Chemokines in asthma: cooperative interaction between chemokines and IL-13 J Allergy Clin Immunol 111 2003 227 242 quiz 43
37. T.S. Olson, B.K. Reuter, K.G. Scott, M.A. Morris, X.M. Wang, L.N. Hancock, T.L. Burcin, S.M. Cohn, P.B. Ernst, F. Cominelli, J.B. Meddings, K. Ley, and T.T. Pizarro The primary defect in experimental ileitis originates from a nonhematopoietic source J Exp Med 203 2006 541 552
38. J. Rivera-Nieves, G. Bamias, A. Vidrich, M. Marini, T.T. Pizarro, M.J. McDuffie, C.A. Moskaluk, S.M. Cohn, and F. Cominelli Emergence of perianal fistulizing disease in the SAMP1/YitFc mouse, a spontaneous model of chronic ileitis Gastroenterology 124 2003 972 982
39. J.C. Nussbaum, S.J. Van Dyken, J. von Moltke, L.E. Cheng, A. Mohapatra, A.B. Molofsky, E.E. Thornton, M.F. Krummel, A. Chawla, H.E. Liang, and R.M. Locksley Type 2 innate lymphoid cells control eosinophil homeostasis Nature 502 2013 245 248
40. L.A. Monticelli, L.C. Osborne, M. Noti, S.V. Tran, D.M. Zaiss, and D. Artis IL-33 promotes an innate immune pathway of intestinal tissue protection dependent on amphiregulin-EGFR interactions Proc Natl Acad Sci U S A 112 2015 10762 10767
41. S.G. Smith, R. Chen, M. Kjarsgaard, C. Huang, J.P. Oliveria, P.M. O'Byrne, G.M. Gauvreau, L.P. Boulet, C. Lemiere, J. Martin, P. Nair, and R. Sehmi Increased numbers of activated group 2 innate lymphoid cells in the airways of patients with severe asthma and persistent airway eosinophilia J Allergy Clin Immunol 137 2016 75 86.e8
42. M. Hashiguchi, Y. Kashiwakura, H. Kojima, A. Kobayashi, Y. Kanno, and T. Kobata IL-33 activates eosinophils of visceral adipose tissue both directly and via innate lymphoid cells Eur J Immunol 45 2015 876 885
43. R. Goldberg, N. Prescott, G.M. Lord, T.T. MacDonald, and N. Powell The unusual suspects: innate lymphoid cells as novel therapeutic targets in IBD Nat Rev Gastroenterol Hepatol 12 2015 271 283
44. J.R. Bailey, P.W. Bland, J.F. Tarlton, I. Peters, M. Moorghen, P.A. Sylvester, C.S. Probert, and C.V. Whiting IL-13 promotes collagen accumulation in Crohn's disease fibrosis by down-regulation of fibroblast MMP synthesis: a role for innate lymphoid cells? PLoS One 7 2012 e52332
45. T. McHedlidze, M. Waldner, S. Zopf, J. Walker, A.L. Rankin, M. Schuchmann, D. Voehringer, A.N. McKenzie, M.F. Neurath, S. Pflanz, and S. Wirtz Interleukin-33-dependent innate lymphoid cells mediate hepatic fibrosis Immunity 39 2013 357 371
46. D. Li, R. Guabiraba, A.G. Besnard, M. Komai-Koma, M.S. Jabir, L. Zhang, G.J. Graham, M. Kurowska-Stolarska, F.Y. Liew, C. McSharry, and D. Xu IL-33 promotes ST2-dependent lung fibrosis by the induction of alternatively activated macrophages and innate lymphoid cells in mice J Allergy Clin Immunol 134 2014 1422 1432.e11
47. P.N. Pushparaj, D. Li, M. Komai-Koma, R. Guabiraba, J. Alexander, C. McSharry, and D. Xu Interleukin-33 exacerbates acute colitis via interleukin-4 in mice Immunology 140 2013 70 77
48. P. Biancheri, A. Di Sabatino, F. Ammoscato, F. Facciotti, F. Caprioli, R. Curciarello, S.S. Hoque, A. Ghanbari, I. Joe-Njoku, P. Giuffrida, L. Rovedatti, J. Geginat, G.R. Corazza, and T.T. MacDonald Absence of a role for interleukin-13 in inflammatory bowel disease Eur J Immunol 44 2014 370 385
49. W. Reinisch, J. Panes, S. Khurana, G. Toth, F. Hua, G.M. Comer, M. Hinz, K. Page, M. O'Toole, T.M. Moorehead, H. Zhu, Y. Sun, and F. Cataldi Anrukinzumab, an anti-interleukin 13 monoclonal antibody, in active UC: efficacy and safety from a phase IIa randomised multicentre study Gut 64 2015 894 900
50. C. Schiering, T. Krausgruber, A. Chomka, A. Frohlich, K. Adelmann, E.A. Wohlfert, J. Pott, T. Griseri, J. Bollrath, A.N. Hegazy, O.J. Harrison, B.M. Owens, M. Lohning, Y. Belkaid, P.G. Fallon, and F. Powrie The alarmin IL-33 promotes regulatory T-cell function in the intestine Nature 513 2014 564 568