IL-33 induces skin inflammation with mast cell and neutrophil activation

European Journal of Immunology

Volumn 41, Issue 8, 2011, Pages 2229-2237

  Hueber, Axel J ^a   Alves Filho, Jose C ^a   Asquith, Darren L ^a   Michels, Chesney ^a   Millar, Neal L ^a   Reilly, James H ^a   Graham, Gerry J ^a   Liew, Foo Y ^a   Miller, Ashley M ^a   McInnes, Iain B ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Cytokine; Inflammation; Interleukin; Psoriasis

Indexed keywords

CXCL1 CHEMOKINE; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 33; PHORBOL ESTER; RECOMBINANT CYTOKINE; RECOMBINANT INTERLEUKIN 33; ST2 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL ACTIVATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; EAR; EPIDERMIS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; INJECTION; MALE; MAST CELL; MEDIATOR; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PSORIASIS; RECEPTOR UPREGULATION; SKIN; SKIN DEFECT; SKIN INFLAMMATION; WILD TYPE;

ANIMALS; CHEMOKINE CXCL1; DERMATITIS; FLOW CYTOMETRY; HUMANS; INTERLEUKINS; MALE; MAST CELLS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHIL ACTIVATION; NEUTROPHIL INFILTRATION; NEUTROPHILS; PSORIASIS; RECEPTORS, INTERLEUKIN; SKIN; TETRADECANOYLPHORBOL ACETATE;

EID: 79960732317     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201041360     Document Type: Article

References (40)

1. Fitch, E., Harper, E., Skorcheva, I., Kurtz, S. E. and Blauvelt, A., Pathophysiology of psoriasis: recent advances on IL-23 and Th17 cytokines. Curr. Rheumatol. Rep. 2007. 9: 461-467.
2. Lowes, M. A., Bowcock, A. M. and Krueger, J. G., Pathogenesis and therapy of psoriasis. Nature 2007. 445: 866-873.
3. Schmitz, J., Owyang, A., Oldham, E., Song, Y., Murphy, E., McClanahan, T. K., Zurawski, G. 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: 479-490.
4. Chackerian, A. A., Oldham, E. R., Murphy, E. E., Schmitz, J., Pflanz, S. and Kastelein, R. A., IL-1 receptor accessory protein and ST2 comprise the IL-33 receptor complex. J. Immunol. 2007. 179: 2551-2555.
5. Kurowska-Stolarska, M., Kewin, P., Murphy, G., Russo, R. C., Stolarski, B., Garcia, C. C., Komai-Koma, M. 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: 4780-4790.
6. Smithgall, M. D., Comeau, M. R., Yoon, B. R., Kaufman, D., Armitage, R. and Smith, D. E., 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. 2008. 20: 1019-1030.
7. Allakhverdi, Z., Smith, D. E., Comeau, M. R. and Delespesse, G., Cutting edge: the ST2 ligand IL-33 potently activates and drives maturation of human mast cells. J. Immunol. 2007. 179: 2051-2054.
8. Alves-Filho, J. C., Sonego, F., Souto, F. O., Freitas, A., Verri, W. A., Jr., Auxiliadora-Martins, M., Basile-Filho, A. et al., Interleukin-33 attenuates sepsis by enhancing neutrophil influx to the site of infection. Nat. Med. 2010. 16: 708-712.
9. Verri, W. A., Jr., Souto, F. O., Vieira, S. M., Almeida, S. C., Fukada, S. Y., Xu, D., Alves-Filho, J. C. et al., IL-33 induces neutrophil migration in rheumatoid arthritis and is a target of anti-TNF therapy. Ann. Rheum. Dis. 2010. 69: 1697-1703.
10. Komai-Koma, M., Gilchrist, D. S., McKenzie, A. N., Goodyear, C. S., Xu, D. and Liew, F. Y., IL-33 activates B1 cells and exacerbates contact sensitivity. J. Immunol. 2011. 186: 2584-2591.
11. Moussion, C., Ortega, N. and Girard, J. P., 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 2008. 3: e3331.
12. Carriere, V., Roussel, L., Ortega, N., Lacorre, D. A., Americh, L., Aguilar, L., Bouche, G. et al., IL-33, the IL-1-like cytokine ligand for ST2 receptor, is a chromatin-associated nuclear factor in vivo. Proc. Natl. Acad. Sci. USA 2007. 104: 282-287.
13. Kuchler, A. M., Pollheimer, J., Balogh, J., Sponheim, J., Manley, L., Sorensen, D. R., De Angelis, P. M. et al., Nuclear interleukin-33 is generally expressed in resting endothelium but rapidly lost upon angiogenic or proinflammatory activation. Am. J. Pathol. 2008. 173: 1229-1242.
14. Luthi, A. U., Cullen, S. P., McNeela, E. A., Duriez, P. J., Afonina, I. S., Sheridan, C., Brumatti, G. et al., Suppression of interleukin-33 bioactivity through proteolysis by apoptotic caspases. Immunity 2009. 31: 84-98.
15. Cayrol, C. and Girard, J. P., The IL-1-like cytokine IL-33 is inactivated after maturation by caspase-1. Proc. Natl. Acad. Sci. USA 2009. 106: 9021-9026.
16. Talabot-Ayer, D., Lamacchia, C., Gabay, C. and Palmer, G., Interleukin-33 is biologically active independently of caspase-1 cleavage. J. Biol. Chem. 2009. 284: 19420-19426.
17. Pushparaj, P. N., Tay, H. K., H'Ng, S. C., Pitman, N., Xu, D., McKenzie, A., Liew, F. Y. et al., The cytokine interleukin-33 mediates anaphylactic shock. Proc. Natl. Acad. Sci. USA 2009. 106: 9773-9778.
18. Theoharides, T. C., Zhang, B., Kempuraj, D., Tagen, M., Vasiadi, M., Angelidou, A., Alysandratos, K. D. et al., IL-33 augments substance P-induced VEGF secretion from human mast cells and is increased in psoriatic skin. Proc. Natl. Acad. Sci. USA 2010. 107: 4448-4453.
19. Rankin, A. L., Mumm, J. B., Murphy, E., Turner, S., Yu, N., McClanahan, T. K., Bourne, P. A. et al., IL-33 induces IL-13-dependent cutaneous fibrosis. J. Immunol. 2010. 184: 1526-1535.
20. Jamieson, T., Cook, D. N., Nibbs, R. J., Rot, A., Nixon, C., McLean, P., Alcami, A. et al., The chemokine receptor D6 limits the inflammatory response in vivo. Nat. Immunol. 2005. 6: 403-411.
21. Zheng, Y., Danilenko, D. M., Valdez, P., Kasman, I., Eastham-Anderson, J., Wu, J. and Ouyang, W., Interleukin-22, a T(H)17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 2007. 445: 648-651.
22. De Filippo, K., Henderson, R. B., Laschinger, M. and Hogg, N., Neutrophil chemokines KC and macrophage-inflammatory protein-2 are newly synthesized by tissue macrophages using distinct TLR signaling pathways. J. Immunol. 2008. 180: 4308-4315.
23. Vieira, S. M., Lemos, H. P., Grespan, R., Napimoga, M. H., Dal-Secco, D., Freitas, A., Cunha, T. M. et al., A crucial role for TNF-alpha in mediating neutrophil influx induced by endogenously generated or exogenous chemokines, KC/CXCL1 and LIX/CXCL5. Br. J. Pharmacol. 2009. 158: 779-789.
24. Iikura, M., Suto, H., Kajiwara, N., Oboki, K., Ohno, T., Okayama, Y., Saito, H. et al., IL-33 can promote survival, adhesion and cytokine production in human mast cells. Lab. Invest. 2007. 87: 971-978.
25. Kojima, T., Cromie, M. A., Fisher, G. J., Voorhees, J. J. and Elder, J. T., GRO-alpha mRNA is selectively overexpressed in psoriatic epidermis and is reduced by cyclosporin A in vivo, but not in cultured keratinocytes. J. Invest. Dermatol. 1993. 101: 767-772.
26. Kulke, R., Todt-Pingel, I., Rademacher, D., Rowert, J., Schroder, J. M. and Christophers, E., Co-localized overexpression of GRO-alpha and IL-8 mRNA is restricted to the suprapapillary layers of psoriatic lesions. J. Invest. Dermatol. 1996. 106: 526-530.
27. Gillitzer, R., Ritter, U., Spandau, U., Goebeler, M. and Brocker, E. B., Differential expression of GRO-alpha and IL-8 mRNA in psoriasis: a model for neutrophil migration and accumulation in vivo. J. Invest. Dermatol. 1996. 107: 778-782.
28. Kristensen, M., Deleuran, B., Eedy, D. J., Feldmann, M., Breathnach, S. M. and Brennan, F. M., Distribution of interleukin 1 receptor antagonist protein (IRAP), interleukin 1 receptor, and interleukin 1 alpha in normal and psoriatic skin. Decreased expression of IRAP in psoriatic lesional epidermis. Br. J. Dermatol. 1992. 127: 305-311.
29. Lundqvist E. N. and Egelrud, T., Biologically active, alternatively processed interleukin-1 beta in psoriatic scales. Eur. J. Immunol. 1997. 27: 2165-2171.
30. Debets, R., Hegmans, J. P., Croughs, P., Troost, R. J., Prins, J. B., Benner, R. and Prens, E. P., The IL-1 system in psoriatic skin: IL-1 antagonist sphere of influence in lesional psoriatic epidermis. J. Immunol. 1997. 158: 2955-2963.
31. Dowd, P. M., Camp, R. D. and Greaves, M. W., Human recombinant interleukin-1 alpha is proinflammatory in normal human skin. Skin Pharmacol. 1988. 1: 30-37.
32. Camp, R., Fincham, N., Ross, J., Bird, C. and Gearing, A., Potent inflammatory properties in human skin of interleukin-1 alpha-like material isolated from normal skin. J. Invest. Dermatol. 1990. 94: 735-741.
33. Groves, R. W., Ross, E., Barker, J. N., Ross, J. S., Camp, R. D. and MacDonald, D. M., Effect of in vivo interleukin-1 on adhesion molecule expression in normal human skin. J. Invest. Dermatol. 1992. 98: 384-387.
34. Groves, R. W., Mizutani, H., Kieffer, J. D. and Kupper, T. S., Inflammatory skin disease in transgenic mice that express high levels of interleukin 1 alpha in basal epidermis. Proc. Natl. Acad. Sci. USA 1995. 92: 11874-11878.
35. Shepherd, J., Little, M. C. and Nicklin, M. J., Psoriasis-like cutaneous inflammation in mice lacking interleukin-1 receptor antagonist. J. Invest. Dermatol. 2004. 122: 665-669.
36. Ohta, Y., Hamada, Y. and Katsuoka, K., Expression of IL-18 in psoriasis. Arch. Dermatol. Res. 2001. 293: 334-342.
37. Arican, O., Aral, M., Sasmaz, S. and Ciragil, P., Serum levels of TNF-alpha, IFN-gamma, IL-6, IL-8, IL-12, IL-17, and IL-18 in patients with active psoriasis and correlation with disease severity. Mediators Inflamm. 2005. 2005: 273-279.
38. Blumberg, H., Dinh, H., Trueblood, E. S., Pretorius, J., Kugler, D., Weng, N., Kanaly, S. T. et al., Opposing activities of two novel members of the IL-1 ligand family regulate skin inflammation. J. Exp. Med. 2007. 204: 2603-2614.
39. Grimbaldeston, M. A., Chen, C. C., Piliponsky, A. M., Tsai, M., Tam, S. Y. and Galli, S. J., Mast cell-deficient W-sash c-kit mutant Kit W-sh/W-sh mice as a model for investigating mast cell biology in vivo. Am. J. Pathol. 2005. 167: 835-848.
40. Hedrick, M. N., Lonsdorf, A. S., Shirakawa, A. K., Richard Lee, C. C., Liao, F., Singh, S. P., Zhang, H. H. et al., CCR6 is required for IL-23-induced psoriasis-like inflammation in mice. J. Clin. Invest. 2009. 119: 2317-2329.