Interleukin-33: A mediator of inflammation targeting hematopoietic stem and progenitor cells and their progenies

Frontiers in Immunology

Volumn 4, Issue MAY, 2013, Pages

  Le, Hongnga ^a   Kim, Wonyoung ^b   Kim, Juyang ^b   Cho, Hong R ^b   Kwon, Byungsuk ^a,b  

^a University of Ulsan   (South Korea)

^b Ulsan University College of Medicine   (South Korea)

Author keywords

Alarmin; Hematopoietic stem and progenitor cell; IL 33; Inflammation; Inflammatory cytokine; Innate lymphoid cell

Indexed keywords

CHEMOKINE RECEPTOR CXCR2; CXCL1 CHEMOKINE; CXCL3 CHEMOKINE; GAMMA INTERFERON; GLYCOPROTEIN P 15095; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HIGH MOBILITY GROUP B1 PROTEIN; INTERLEUKIN 13; INTERLEUKIN 18; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 3; INTERLEUKIN 33; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 5 RECEPTOR ALPHA; INTERLEUKIN 6; INTERLEUKIN 7; INTERLEUKIN 8; INTERLEUKIN 9; RHODOPSIN KINASE; STAT5 PROTEIN; SUBSTANCE P RECEPTOR; THYMIC STROMAL LYMPHOPOIETIN; TOLL LIKE RECEPTOR 7; TRANSCRIPTION FACTOR NFAT; UNINDEXED DRUG;

ALLERGIC AIRWAY INFLAMMATION; BONE MARROW CELL; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; EOSINOPHIL; FUNGICIDAL ACTIVITY; HEMATOPOIETIC STEM CELL; HUMAN; IMMUNOSURVEILLANCE; INFLAMMATION; INNATE IMMUNITY; LYMPHOCYTE; LYMPHOID CELL; MAST CELL; NECROSIS; NONHUMAN; PHAGOCYTOSIS; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROTEIN SYNTHESIS REGULATION; REVIEW; SIGNAL TRANSDUCTION; TISSUE INJURY;

EID: 84883804540     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00104     Document Type: Review

References (99)

1. Akcay, A., Nguyen, Q., He, Z., Turkmen, K., Won Lee, D., Hernando, A. A., et al. (2011). IL-33 exacerbates acute kidney injury. J. Am. Soc. Nephrol. 22, 2057-2067.
2. Ali, S., Mohs, A., Thomas, M., Klare, J., Ross, R., Schmitz, M. L., et al. (2011). The dual function cytokine IL-33 interacts with the transcription factor NF-κB to dampen NF-κB-stimulated gene transcription. J. Immunol. 187, 1609-1616.
3. Ali, S., Nguyen, D. Q., Falk, W., and Martin, M. U. (2010). Caspase 3 inactivates biologically active full length interleukin-33 as a classical cytokine but does not prohibit nuclear translocation. Biochem. Biophys. Res. Commun. 391, 1512-1526.
4. Allakhverdi, Z., Comeau, M. R., Smith, D. E., Toy, D., Endam, L. M., Desrosiers, M., et al. (2009). CD34+ hematopoietic progenitor cells are potent effectors of allergic inflammation. J. Allergy Clin. Immunol. 123, 472-478.
5. Allakhverdi, Z., Smith, D. E., Comeau, M. R., and Delespesse, G. (2007). Cutting edge: the ST2 ligand IL-33 potently activates and drives maturation of human mast cells. J. Immunol. 179, 2051-2054.
6. Alves-Filho, J. C., Freitas, A., Souto, F. O., Spiller, F., Paula-Neto, H., Silva, J. S., et al. (2009). Regulation of chemokine receptor by Toll-like receptor 2 is critical to neutrophil migration and resistance to polymicrobial sepsis. Proc. Natl. Acad. Sci. U.S.A. 106, 4018-4023.
7. Alves-Filho, J. C., Sônego, F., Souto, F. O., Freitas, A., Verri, W. A. Jr., Auxiliadora-Martins, M., et al. (2010). Interleukin-33 attenuates sepsis by enhancing neutrophil influx to the site of infection. Nat. Med. 16, 708-712.
8. Anthony, R. M., Kobayashi, T., Wermeling, F., and Ravetch, J. V. (2011). Intravenous gammaglobulin suppresses inflammation through a novel TH2 pathway. Nature 475, 110-113.
9. Arshad, M. I., Piquet-Pellorce, C., L'Helgoualc'h, A., Rauch, M., Patrat-Delon, S., Ezan, F., et al. (2012). TRAIL but not FasL and TNFα, regulates IL-33 expression in murine hepatocytes during acute hepatitis. Hepatology 56, 2353-2362.
10. Arshad, M. I., Rauch, M., L'Helgoualc'h, A., Julia, V., Leite-de-Moraes, M. C., Lucas-Clerc, C., et al. (2011). NKT cells are required to induce high IL-33 expression in hepatocytes during ConA-induced acute hepatitis. Eur. J. Immunol. 41, 2341-2348.
11. Baekkevold, E. S., Roussigné, M., Yamanaka, T., Johansen, F. E., Jahnsen, F. L., Amalric, F., et al. (2003). Molecular characterization of NF-HEV, a nuclear factor preferentially expressed in human high endothelial venules. Am. J. Pathol. 163, 69-79.
12. Bartemes, K. R., Iijima, K., Kobayashi, T., Kephart, G. M., McKenzie, A. N., and Kita, H. (2012). IL-33-responsive lineage- CD25+ CD44hi lymphoid cells mediate innate type 2 immunity and allergic inflammation in the lungs. J. Immunol. 188, 1503-1513.
13. Bartemes, K. R., and Kita, H. (2012). Dynamic role of epithelium-derived cytokines in asthma. Clin. Immunol. 143, 222-235.
14. Besnard, A. G., Togbe, D., Guillou, N., Erard, F., Quesniaux, V., and Ryffel, B. (2011). IL-33-activated dendritic cells are critical for allergic airway inflammation. Eur. J. Immunol. 41, 1675-1686.
15. Blom, L., Poulsen, B. C., Jensen, B. M., Hansen, A., and Poulsen, L. K. (2011). IL-33 induces IL-9 production in human CD4+ T cells and basophils. PLoS ONE 6:e21695. doi:10.1371/journal.pone.0021695
16. Bonilla, W. V., Fröhlich, A., Senn, K., Kallert, S., Fernandez, M., Johnson, S., et al. (2012). The alarmin interleukin-33 drives protective antiviral CD8+ T cell responses. Science 335, 984-989.
17. Bourgeois, E., Van, L. P., Samson, M., Diem, S., Barra, A., Roga, S., et al. (2009). The pro-Th2 cytokine IL-33 directly interacts with invariant NKT and NK cells to induce IFN-gamma production. Eur. J. Immunol. 39, 1046-1055.
18. Carriere, V., Roussel, L., Ortega, N., Lacorre, D. A., Americh, L., Aguilar, L., et al. (2007). 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, 282-287.
19. Cayrol, C., and Girard, J. P. (2009). The IL-1-like cytokine IL-33 is inactivated after maturation by caspase-1. Proc. Natl. Acad. Sci. U.S.A. 106, 9021-9026.
20. Chang, Y. J., Kim, H. Y., Albacker, L. A., Baumgarth, N., McKenzie, A. N., Smith, D. E., et al. (2011). Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity. Nat. Immunol. 12, 631-638.
21. Chen, J., Duan, L., Xiong, A., Zhang, H., Zheng, F., Tan, Z., et al. (2012). Blockade of IL-33 ameliorates Con A-induced hepatic injury by reducing NKT cell activation and IFN-γ production in mice. J. Mol. Med. 90, 1505-1515.
22. Cherry, W. B., Yoon, J., Bartemes, K. R., Iijima, K., and Kita, H. (2008). A novel IL-1 family cytokine, IL-33, potently activates human eosinophils. J. Allergy Clin. Immunol. 121, 1484-1490.
23. Choi, Y. S., Choi, H. J., Min, J. K., Pyun, B. J., Maeng, Y. S., Park, H., et al. (2009). Interleukin-33 induces angiogenesis and vascular permeability through ST2/TRAF6-mediated endothelial nitric oxide production. Blood 114, 3117-3126.
24. Chow, J. Y., Wong, C. K., Cheung, P. F., and Lam, C. W. (2010). Intracellular signaling mechanisms regulating the activation of human eosinophils by the novel Th2 cytokine IL-33: implications for allergic inflammation. Cell. Mol. Immunol. 7, 26-34.
25. Enoksson, M., Lyberg, K., Möller-Westerberg, C., Fallon, P. G., Nilsson, G., and Lunderius-Andersson, C. (2011). Mast cells as sensors of cell injury through IL-33 recognition. J. Immunol. 186, 2523-2528.
26. Enoksson, M., Möller-Westerberg, C., Wicher, G., Fallon, P. G., Forsberg-Nilsson, K., Lunderius-Andersson, C., et al. (2012). Intraperitoneal influx of neutrophils in response to IL-33 is mast cell dependent. Blood 121, 530-536.
27. Espinassous, Q., Garcia-de-Paco, E., Garcia-Verdugo, I., Synguelakis, M., von Aulock, S., Sallenave, J. M., et al. (2009). IL-33 enhances lipopolysaccharide-induced inflammatory cytokine production from mouse macrophages by regulating lipopolysaccharide receptor complex. J. Immunol. 183, 1446-1455.
28. Fujita, J., Kawaguchi, M., Kokubu, F., Ohara, G., Ota, K., Huang, S. K., et al. (2012). Interleukin-33 induces interleukin-17F in bronchial epithelial cells. Allergy 67, 744-750.
29. Griseri, T., McKenzie, B. S., Schiering, C., and Powrie, F. (2012). Dysregulated hematopoietic stem and progenitor cell activity promotes interleukin-23-driven chronic intestinal inflammation. Immunity 37, 1116-1129.
30. Groβ, P., Doser, K., Falk, W., Obermeier, F., and Hofmann, C. (2012). IL-33 attenuates development and perpetuation of chronic intestinal inflammation. Inflamm. Bowel Dis. 18, 1900-1909.
31. Guo, L., Junttila, I. S., and Paul, W. E. (2012). Cytokine-induced cytokine production by conventional and innate lymphoid cells. Trends Immunol. 33, 598-606.
32. Guo, L., Wei, G., Zhu, J., Liao, W., Leonard, W. J., Zhao, K., et al. (2009). IL-1 family members and STAT activators induce cytokine production by Th2, Th17, and Th1 cells. Proc. Natl. Acad. Sci. U.S.A. 106, 13463-13468.
33. Halim, T. Y., MacLaren, A., Romanish, M. T., Gold, M. J., McNagny, K. M., and Takei, F. (2012). Retinoic-acid-receptor-related orphan nuclear receptor alpha is required for natural helper cell development and allergic inflammation. Immunity 37, 463-474.
34. Haraldsen, G., Balogh, J., Pollheimer, J., Sponheim, J., and Küchler, A. M. (2009). Interleukin-33-cytokine of dual function or novel alarmin? Trends Immunol. 30, 227-233.
35. Hazlett, L. D., McClellan, S. A., Barrett, R. P., Huang, X., Zhang, Y., Wu, M., et al. (2010). IL-33 shifts macrophage polarization, promoting resistance against Pseudomonas aeruginosa keratitis. Invest. Ophthalmol. Vis. Sci. 51, 1524-1532.
36. Hepworth, M. R., Danilowicz-Luebert, E., Rausch, S., Metz, M., Klotz, C., Maurer, M., et al. (2012). Mast cells orchestrate type 2 immunity to helminths through regulation of tissue-derived cytokines. Proc. Natl. Acad. Sci. U.S.A. 109, 6644-6649.
37. Ho, L. H., Ohno, T., Oboki, K., Kajiwara, N., Suto, H., Iikura, M., et al. (2007). IL-33 induces IL-13 production by mouse mast cells independently of IgE-FcepsilonRI signals. J. Leukoc. Biol. 82, 1481-1490.
38. Hoyler, T., Klose, C. S., Souabni, A., Turqueti-Neves, A., Pfeifer, D., Rawlins, E. L., et al. (2012). The transcription factor GATA-3 controls cell fate and maintenance of type 2 innate lymphoid cells. Immunity 37, 634-648.
39. Hsu, C. L., and Bryce, P. J. (2012). Inducible IL-33 expression by mast cells is regulated by a calcium-dependent pathway. J. Immunol. 189, 3421-3429.
40. Iikura, M., Suto, H., Kajiwara, N., Oboki, K., Ohno, T., Okayama, Y., et al. (2007). IL-33 can promote survival, adhesion and cytokine production in human mast cells. Lab. Invest. 87, 971-978.
41. Ikutani, M., Yanagibashi, T., Ogasawara, M., Tsuneyama, K., Yamamoto, S., Hattori, Y., et al. (2012). Identification of innate IL-5-producing cells and their role in lung eosinophil regulation and antitumor immunity. J. Immunol. 188, 703-713.
42. Kaieda, S., Shin, K., Nigrovic, P. A., Seki, K., Lee, R. T., Stevens, R. L., et al. (2010). Synovial fibroblasts promote the expression and granule accumulation of tryptase via interleukin-33 and its receptor ST-2 (IL1RL1). J. Biol. Chem. 285, 21478-21486.
43. Kakkar, R., Hei, H., Dobner, S., and Lee, R. T. (2012). Interleukin 33 as a mechanically responsive cytokine secreted by living cells. J. Biol. Chem. 287, 6941-6948.
44. Kang, Z., Swaidani, S., Yin, W., Wang, C., Barlow, J. L., Gulen, M. F., et al. (2012). Epithelial cell-specific Act1 adaptor mediates interleukin-25-dependent helminth expulsion through expansion of Lin(-)c-Kit(+) innate cell population. Immunity 36, 821-833.
45. Kim, H. Y., Chang, Y. J., Subramanian, S., Lee, H. H., Albacker, L. A., Matangkasombut, P., et al. (2012a). Innate lymphoid cells responding to IL-33 mediate airway hyperreactivity independently of adaptive immunity. J. Allergy Clin. Immunol. 129, 216-227.
46. Kim, H. J., Lee, J. S., Kim, J. D., Cha, H. J., Kim, A., Lee, S. K., et al. (2012b). Reverse signaling through the costimulatory ligand CD137L in epithelial cells is essential for natural killer cell-mediated acute tissue inflammation. Proc. Natl. Acad. Sci. U.S.A. 109, E13-E22.
47. Kim, W., Kim, J., Shin, C., Kim, H., Doh, Y., Cho, H. R., et al. (2010). A novel method for procuring a large quantity of mature murine eosinophils in vivo. J. Immunol. Methods 363, 90-94.
48. Komai-Koma, M., Gilchrist, D. S., McKenzie, A. N., Goodyear, C. S., Xu, D., and Liew, F. Y. (2011). IL-33 activates B1 cells and exacerbates contact sensitivity. J. Immunol. 186, 2584-2591.
49. Kouzaki, H., Iijima, K., Kobayashi, T., O'Grady, S. M., and Kita, H. (2012). The danger signal, extracellular ATP, is a sensor for an airborne allergen and triggers IL-33 release and innate Th2-type responses. J. Immunol. 186, 4375-4387.
50. Kurowska-Stolarska, M., Kewin, P., Murphy, G., Russo, R. C., Stolarski, B., Garcia, C. C., et al. (2008). IL-33 induces antigen-specific IL-5+ T cells and promotes allergic-induced airway inflammation independent of IL-4. J. Immunol. 181, 4170-4790.
51. Kurowska-Stolarska, M., Stolarski, B., Kewin, P., Murphy, G., Corrigan, C. J., Ying, S., et al. (2009). IL-33 amplifies the polarization of alternatively activated macrophages that contribute to airway inflammation. J. Immunol. 183, 6469-6477.
52. Lamkanifi, M., and Dixit, V. M. (2009). IL-33 raises alarm. Immunity 31, 5-7.
53. Le, H. T., Tran, V. G., Kim, W., Kim, J., Cho, H. R., and Kwon, B. (2012). IL-33 priming regulates multiple steps of the neutrophil-mediated anti-Candida albicans response by modulating TLR and dectin-1 signals. J. Immunol. 189, 287-295.
54. Lefrançais, E., Roga, S., Gautier, V., Gonzalez-de-Peredo, A., Monsarrat, B., Girard, J. P., et al. (2012). IL-33 is processed into mature bioactive forms by neutrophil elastase and cathepsin G. Proc. Natl. Acad. Sci. U.S.A. 109, 1673-1678.
55. Lunderius-Andersson, C., Enoksson, M., and Nilsson, G. (2012). Mast cells respond to cell injury through the recognition of IL-33. Front. Immunol. 3:82. doi:10.3389/fimmu.2012.00082
56. Lüthi, A. U., Cullen, S. P., McNeela, E. A., Duriez, P. J., Afonina, I. S., Sheridan, C., et al. (2009). Suppression of interleukin-33 bioactivity through proteolysis by apoptotic caspases. Immunity 31, 84-98.
57. Luzina, I. G., Pickering, E. M., Kopach, P., Kang, P. H., Lockatell, V., Todd, N. W., et al. (2012). Full-length IL-33 promotes inflammation but not Th2 response in vivo in an ST2-independent fashion. J. Immunol. 189, 403-410.
58. Massberg, S., Schaerli, P., Knezevic-Maramica, I., Köllnberger, M., Tubo, N., Moseman, E. A., et al. (2007). Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell 131, 994-1008.
59. Medzhitov, R. (2008). Original and physiological roles of inflammation. Nature 454, 428-435.
60. Miller, A. M., Xu, D., Asquith, D. L., Denby, L., Li, Y., Sattar, N., et al. (2008). IL-33 reduces the development of atherosclerosis. J. Exp. Med. 205, 339-346.
61. Milovanovic, M., Volarevic, V., Ljujic, B., Radosavljevic, G., Jovanovic, I., Arsenijevic, N., et al. (2012). Deletion of IL-33R (ST2) abrogates resistance to EAE in BALB/C mice by enhancing polarization of APC to inflammatory phenotype. PLoS ONE 7:e45225. doi:10.1371/journal.pone.0045225
62. Mirchandani, A. S., Salmond, R. J., and Liew, F. Y. (2012). Interleukin-33 and the function of innate lymphoid cells. Trends Immunol. 33, 389-396.
63. Monticelli, L. A., Sonnenberg, G. F., Abt, M. C., Alenghat, T., Ziegler, C. G., Doering, T. A., et al. (2011). D. Innate lymphoid cells promote lung-tissue homeostasis after infection with influenza virus. Nat. Immunol. 12, 1045-1054.
64. Moro, K., Yamada, T., Tanabe, M., Takeuchi, T., Ikawa, T., Kawamoto, H., et al. (2010). Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature 463, 540-544.
65. Moulin, D., Donzé, O., Talabot-Ayer, D., Mézin, F., Palmer, G., and Gabay, C. (2007). Interleukin (IL)-33 induces the release of pro-inflammatory mediators by mast cells. Cytokine 40, 216-225.
66. Moussion, C., and Girard, J. P. (2008). The IL-1-like cytokine IL-33 is constitutively expressed in the nucleus of endothelial cells and epithelial cells in vivo: a novel "alarmin"? PLoS ONE 3:e3331. doi:10.1371/journal.pone.0003331
67. Nagai, Y., Garrett, K. P., Ohta, S., Bahrun, U., Kouro, T., Akira, S., et al. (2006). Toll-like receptors on hematopoietic progenitor cells stimulate innate immune system replenishment. Immunity 24, 801-812.
68. Neill, D. R., Wong, S. H., Bellosi, A., Flynn, R. J., Daly, M., Langford, T. K., et al. (2010). Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464, 1367-1370.
69. Nelson, M. P., Christmann, B. S., Werner, J. L., Metz, A. E., Trevor, J. L., Lowell, C. A., et al. (2011). IL-33 and M2a alveolar macrophages promote lung defense against the atypical fungal pathogen Pneumocystis murina. J. Immunol. 186, 2372-2381.
70. Pastorelli, L., Garg, R. R., Hoang, S. B., Spina, L., Mattioli, B., Scarpa, M., et al. (2010). 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, 8017-8022.
71. Pecaric-Petkovic, T., Didichenko, S. A., Kaempfer, S., Spiegl, N., and Dahinden, C. A. (2009). Human basophils and eosinophils are the direct target leukocytes of the novel IL-1 family member IL-33. Blood 113, 1526-1534.
72. Price, A. E., Liang, H. E., Sullivan, B. M., Reinhardt, R. L., Eisley, C. J., Erle, D. J., et al. (2010). Systemically dispersed innate IL-13-expressing cells in type 2 immunity. Proc. Natl. Acad. Sci. U.S.A. 107, 11489-11494.
73. Rank, M. A., Kobayashi, T., Kozaki, H., Bartemes, K. R., Squillace, D. L., and Kita, H. (2009). IL-33-activated dendritic cells induce an atypical TH2-type response. J. Allergy Clin. Immunol. 123, 1047-1054.
74. Rankin, A. L., Mumm, J. B., Murphy, E., Turner, S., Yu, N., McClanahan, T. K., et al. (2010). IL-33 induces IL-13-dependent cutaneous fibrosis. J. Immunol. 184, 1526-1535.
75. Roussel, L., Erard, M., Cayrol, C., and Girard, J. P. (2008). Molecular mimicry between IL-33 and KSHV for attachment to chromatin through the H2A-H2B acidic pocket. EMBO Rep. 9, 1006-1012.
76. Saenz, S. A., Siracusa, M. C., Perrigoue, J. G., Spencer, S. P., Urban, J. F. Jr., Tocker, J. E., et al. (2011). IL25 elicits a multipotent progenitor cell population that promotes T(H)2 cytokine responses. Nature 464, 1362-1366.
77. Sakai, N., Van Sweringenb, H. L., Quillin, R. C., Schuster, R., Blanchard, J., Burns, J. M., et al. (2012). Interleukin-33 is hepatoprotective during liver ischemia/reperfusion in mice. Hepatology 56, 1468-1478.
78. Schmitz, J., Owyang, A., Oldham, E., Song, Y., Murphy, E., McClanahan, T. K., et al. (2005). 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, 479-490.
79. Schneider, E., Petit-Bertron, A. F., Bricard, R., Levasseur, M., Ramadan, A., Girard, J. P., et al. (2009). IL-33 activates unprimed murine basophils directly in vitro and induces their in vivo expansion indirectly by promoting hematopoietic growth factor production. J. Immunol. 183, 3591-3597.
80. Silver, M. R., Margulis, A., Wood, N., Goldman, S. J., Kasaian, M., and Chaudhary, D. (2010). IL-33 synergizes with IgE-dependent and IgE-independent agents to promote mast cell and basophil activation. Inflamm. Res. 59, 207-218.
81. Smithgall, M. D., Comeau, M. R., Yoon, B. R., Kaufman, D., Armitage, R., and Smith, D. E. (2008). 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. 20, 1019-1030.
82. Stolarski, B., Kurowska-Stolarska, M., Kewin, P., Xu, D., and Liew, F. Y. (2010). IL-33 exacerbates eosinophil-mediated airway inflammation. J. Immunol. 185, 3472-3480.
83. Suzukawa, M., Koketsu, R., Iikura, M., Nakae, S., Matsumoto, K., Nagase, H., et al. (2008a). Interleukin-33 enhances adhesion, CD11b expression and survival in human eosinophils. Lab. Invest. 88, 1245-1253.
84. Suzukawa, M., Iikura, M., Koketsu, R., Nagase, H., Tamura, C., Komiya, A., et al. (2008b). An IL-1 cytokine member, IL-33, induces human basophil activation via its ST2 receptor. J. Immunol. 181, 5981-5989.
85. Swamy, M., Jamora, C., Havran, W., and Hayday, A. (2010). Epithelial decision makers: in search of the "epimmunome." Nat. Immunol. 11, 656-665.
86. Takizawa, H., Boettcher, S., and Manz, M. G. (2012). Demand-adapted regulation of early hematopoiesis in infection and inflammation. Blood 119, 29913002.
87. Talabot-Ayer, D., Calo, N., Vigne, S., Lamacchia, C., Gabay, C., and Palmer, G. (2012). The mouse interleukin (Il)33 gene is expressed in a cell type- and stimulus-dependent manner from two alternative promoters. J. Leukoc. Biol. 91, 119-125.
88. Talabot-Ayer, D., Lamacchia, C., Gabay, C., and Palmer, G. (2009). Interleukin-33 is biologically active independently of caspase-1 cleavage. J. Biol. Chem. 284, 19420-19426.
89. Theoharides, T. C., Zhang, B., Kempuraj, D., Tagen, M., Vasiadi, M., Angelidou, A., et al. (2010). IL-33 augments substance P-induced VEGF secretion from human mast cells and is increased in psoriatic skin. Proc. Natl. Acad. Sci. U. S.A. 2010, 4448-4453.
90. Turnquist, H. R., Sumpter, T. L., Tsung, A., Zahorchak, A. F., Nakao, A., Nau, G. J., et al. (2008). IL-1beta-driven ST2L expression promotes maturation resistance in rapamycin-conditioned dendritic cells. J. Immunol. 181, 62-72.
91. Verri, W. A. Jr., Souto, F. O., Vieira, S. M., Almeida, S. C., Fukada, S. Y., Xu, D., et al. (2010). IL-33 induces neutrophil migration in rheumatoid arthritis and is a target of anti-TNF therapy. Ann. Rheum. Dis. 69, 1697-1703.
92. Waern, I., Lundequist, A., Pejler, G., and Wernersson, S. (2012). Mast cell chymase modulates IL-33 levels and controls allergic sensitization in dust-mite induced airway inflammation. Mucosal Immunol. doi:10.1038/mi.2012.129. [Epub ahead of print].
93. Willart, M. A., Deswarte, K., Pouliot, P., Braun, H., Beyaert, R., Lambrecht, B. N., et al. (2012). Interleukin-1α controls allergic sensitization to inhaled house dust mite via the epithelial release of GM-CSF and IL-33. J. Exp. Med. 209, 1505-1517.
94. Wills-Karp, M., Rani, R., Dienger, K., Lewkowich, I., Fox, J. G., Perkins, C., et al. (2012). Trefoil factor 2 rapidly induces interleukin 33 to promote type 2 immunity during allergic asthma and hookworm infection. J. Exp. Med. 209, 607-622.
95. Wong, S. H., Walker, J. A., Jolin, H. E., Drynan, L. F., Hams, E., Camelo, A., et al. (2012). Transcription factor RORα is critical for nuocyte development. Nat. Immunol. 13, 229-236.
96. Xu, D., Chan, W. L., Leung, B. P., Huang, F. P., Wheeler, R., Piedrafita, D., et al. (1998). Selective expression of a stable cell surface molecule on type 2 but not type 1 helper T cells. J. Exp. Med. 187, 787-794.
97. Yagami, A., Orihara, K., Morita, H., Futamura, K., Hashimoto, N., Matsumoto, K., et al. (2010). IL-33 mediates inflammatory responses in human lung tissue cells. J. Immunol. 185, 5743-5750.
98. Yang, Q., Li, G., Zhu, Y., Liu, L., Chen, E., Turnquist, H., et al. (2011). IL-33 synergizes with TCR and IL-12 signaling to promote the effector function of CD8+ T cells. Eur. J. Immunol. 41, 3351-3360.
99. Yokota, Y., Mansouri, A., Mori, S., Sugawara, S., Adachi, S., Nishikawa, S., et al. (1999). Development of peripheral lymphoid organs and natural killer cells depends on the helix-loop-helix inhibitor Id2. Nature 397, 702-706.