IL-33 signaling regulates innate and adaptive immunity to Cryptococcus neoformans

Journal of Immunology

Volumn 191, Issue 5, 2013, Pages 2503-2513

  Flaczyk, Adam ^a   Duerr, Claudia U ^a   Shourian, Mitra ^a   Lafferty, Erin I ^a   Fritz, Jörg H ^a   Qureshi, Salman T ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN E; INTERLEUKIN 13; INTERLEUKIN 33; INTERLEUKIN 5;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN; CONTROLLED STUDY; CRYPTOCOCCUS NEOFORMANS; EOSINOPHILIA; FUNGAL VIRULENCE; GOBLET CELL; HOST RESISTANCE; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOPATHOGENESIS; INNATE IMMUNITY; LUNG; LUNG ALVEOLUS CELL TYPE 2; LUNG EXTRAVASCULAR FLUID; LYMPHOID CELL; MACROPHAGE ACTIVATION; MOUSE; MUCUS SECRETION; NONHUMAN; PRIORITY JOURNAL; PULMONARY CRYPTOCOCCOSIS; SIGNAL TRANSDUCTION; SPLEEN; SURVIVAL RATE;

ADAPTIVE IMMUNITY; ANIMALS; CELL SEPARATION; CRYPTOCOCCOSIS; CRYPTOCOCCUS NEOFORMANS; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; IMMUNITY, INNATE; INTERLEUKINS; LUNG DISEASES, FUNGAL; MICE; MICE, INBRED BALB C; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 84883396780     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300426     Document Type: Article

References (53)

1. Mitchell, T. G., and J. R. Perfect. 1995. Cryptococcosis in the era of AIDS - 100 years after the discovery of Cryptococcus neoformans. Clin. Microbiol. Rev. 8: 515-548.
2. Cohen, M. L. 2000. Changing patterns of infectious disease. Nature 406: 762-767.
3. Pappas, P. G. 2010. Opportunistic fungi: a view to the future. Am. J. Med. Sci. 340: 253-257.
4. Park, B. J., K. A. Wannemuehler, B. J. Marston, N. Govender, P. G. Pappas, and T. M. Chiller. 2009. Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. AIDS 23: 525-530.
5. Voelz, K., and R. C. May. 2010. Cryptococcal interactions with the host immune system. Eukaryot. Cell 9: 835-846.
6. Arora, S., and G. B. Huffnagle. 2005. Immune regulation during allergic bronchopulmonary mycosis: lessons taught by two fungi. Immunol. Res. 33: 53-68.
7. Romani, L. 2011. Immunity to fungal infections. Nat. Rev. Immunol. 11: 275-288.
8. Chen, G.-H., D. A. McNamara, Y. Hernandez, G. B. Huffnagle, G. B. Toews, and M. A. Olszewski. 2008. Inheritance of immune polarization patterns is linked to resistance versus susceptibility to Cryptococcus neoformans in a mouse model. Infect. Immun. 76: 2379-2391.
9. Jain, A. V., Y. Zhang, W. B. Fields, D. A. McNamara, M. Y. Choe, G.-H. Chen, J. Erb-Downward, J. J. Osterholzer, G. B. Toews, G. B. Huffnagle, and M. A. Olszewski. 2009. Th2 but not Th1 immune bias results in altered lung functions in a murine model of pulmonary Cryptococcus neoformans infection. Infect. Immun. 77: 5389-5399.
10. Guillot, L., S. F. Carroll, M. Badawy, and S. T. Qureshi. 2008. Cryptococcus neoformans induces IL-8 secretion and CXCL1 expression by human bronchial epithelial cells. Respir. Res. 9: 9.
11. Swamy, M., C. Jamora, W. Havran, and A. Hayday. 2010. Epithelial decision makers: in search of the 'epimmunome.' Nat. Immunol. 11: 656-665.
12. Saenz, S. A., B. C. Taylor, and D. Artis. 2008. Welcome to the neighborhood: epithelial cell-derived cytokines license innate and adaptive immune responses at mucosal sites. Immunol. Rev. 226: 172-190.
13. Liew, F. Y., N. I. Pitman, and I. B. McInnes. 2010. Disease-associated functions of IL-33: the new kid in the IL-1 family. Nat. Rev. Immunol. 10: 103-110.
14. Xu, D., W. L. Chan, B. P. Leung, Fp. Huang, R. Wheeler, D. Piedrafita, J. H. Robinson, and F. Y. Liew. 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.
15. Komai-Koma, M., D. S. Gilchrist, A. N. J. McKenzie, C. S. Goodyear, D. Xu, and F. Y. Liew. 2011. IL-33 activates B1 cells and exacerbates contact sensitivity. J. Immunol. 186: 2584-2591.
16. Kurowska-Stolarska, M., P. Kewin, G. Murphy, R. C. Russo, B. Stolarski, C. C. Garcia, M. Komai-Koma, N. Pitman, Y. Li, W. Niedbala, 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: 4780-4790.
17. Moulin, D., O. Donzé, D. Talabot-Ayer, F. Mézin, G. Palmer, and C. Gabay. 2007. Interleukin (IL)-33 induces the release of pro-inflammatory mediators by mast cells. Cytokine 40: 216-225.
18. Smithgall, M. D., M. R. Comeau, B.-R. P. Yoon, D. Kaufman, R. Armitage, and D. E. Smith. 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.
19. Rank, M. A., T. Kobayashi, H. Kozaki, K. R. Bartemes, D. L. Squillace, and H. Kita. 2009. IL-33-activated dendritic cells induce an atypical TH2-type response. J. Allergy Clin. Immunol. 123: 1047-1054.
20. Neill, D. R., S. H. Wong, A. Bellosi, R. J. Flynn, M. Daly, T. K. A. Langford, C. Bucks, C. M. Kane, P. G. Fallon, R. Pannell, et al. 2010. Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464: 1367-1370.
21. Price, A. E., H.-E. Liang, B. M. Sullivan, R. L. Reinhardt, C. J. Eisley, D. J. Erle, and R. M. Locksley. 2010. Systemically dispersed innate IL-13-expressing cells in type 2 immunity. Proc. Natl. Acad. Sci. USA 107: 11489-11494.
22. Moro, K., T. Yamada, M. Tanabe, T. Takeuchi, T. Ikawa, H. Kawamoto, J.-I. Furusawa, M. Ohtani, H. Fujii, and S. Koyasu. 2010. Innate production of T(H)2 cytokines by adipose tissue-associated c-Kit(+)Sca-1(+) lymphoid cells. Nature 463: 540-544.
23. Mjösberg, J., J. Bernink, K. Golebski, J. J. Karrich, C. P. Peters, B. Blom, A. A. te Velde, W. J. Fokkens, C. M. van Drunen, and H. Spits. 2012. The transcription factor GATA3 is essential for the function of human type 2 innate lymphoid cells. Immunity 37: 649-659.
24. Bartemes, K. R., K. Iijima, T. Kobayashi, G. M. Kephart, A. N. McKenzie, and H. Kita. 2012. IL-33-responsive lineage- CD25+ CD44(hi) lymphoid cells mediate innate type 2 immunity and allergic inflammation in the lungs. J. Immunol. 188: 1503-1513.
25. Klein Wolterink, R. G., A. Kleinjan, M. van Nimwegen, I. Bergen, M. de Bruijn, Y. Levani, and R. W. Hendriks. 2012. Pulmonary innate lymphoid cells are major producers of IL-5 and IL-13 in murine models of allergic asthma. Eur. J. Immunol. 42: 1106-1116.
26. Townsend, M. J., P. G. Fallon, D. J. Matthews, H. E. Jolin, and A. N. McKenzie. 2000. T1/ST2-deficient mice demonstrate the importance of T1/ST2 in developing primary T helper cell type 2 responses. J. Exp. Med. 191: 1069-1076.
27. Huffnagle, G. B., M. B. Boyd, N. E. Street, and M. F. Lipscomb. 1998. IL-5 is required for eosinophil recruitment, crystal deposition, and mononuclear cell recruitment during a pulmonary Cryptococcus neoformans infection in genetically susceptible mice (C57BL/6). J. Immunol. 160: 2393-2400.
28. Hernandez, Y., S. Arora, J. R. Erb-Downward, R. A. McDonald, G. B. Toews, and G. B. Huffnagle. 2005. Distinct roles for IL-4 and IL-10 in regulating T2 immunity during allergic bronchopulmonary mycosis. J. Immunol. 174: 1027-1036.
29. Müller, U., W. Stenzel, G. Köhler, C. Werner, T. Polte, G. Hansen, N. Schütze, R. K. Straubinger, M. Blessing, A. N. J. McKenzie, et al. 2007. IL-13 induces disease-promoting type 2 cytokines, alternatively activated macrophages and allergic inflammation during pulmonary infection of mice with Cryptococcus neoformans. J. Immunol. 179: 5367-5377.
30. Zhang, Y., F. Wang, K. C. Tompkins, A. McNamara, A. V. Jain, B. B. Moore, G. B. Toews, G. B. Huffnagle, and M. A. Olszewski. 2009. Robust Th1 and Th17 immunity supports pulmonary clearance but cannot prevent systemic dissemination of highly virulent Cryptococcus neoformans H99. Am. J. Pathol. 175: 2489-2500.
31. Schmitz, J., A. Owyang, E. Oldham, Y. Song, E. Murphy, T. K. McClanahan, G. Zurawski, M. Moshrefi, J. Qin, X. Li, 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.
32. Osterholzer, J. J., J. E. Milam, G.-H. Chen, G. B. Toews, G. B. Huffnagle, and M. A. Olszewski. 2009. Role of dendritic cells and alveolar macrophages in regulating early host defense against pulmonary infection with Cryptococcus neoformans. Infect. Immun. 77: 3749-3758.
33. Osterholzer, J. J., G.-H. Chen, M. A. Olszewski, Y.-M. Zhang, J. L. Curtis, G. B. Huffnagle, and G. B. Toews. 2011. Chemokine receptor 2-mediated accumulation of fungicidal exudate macrophages in mice that clear cryptococcal lung infection. Am. J. Pathol. 178: 198-211.
34. Hardison, S. E., S. Ravi, K. L. Wozniak, M. L. Young, M. A. Olszewski, and F. L. Wormley, Jr. 2010. Pulmonary infection with an interferon- gammaproducing Cryptococcus neoformans strain results in classical macrophage activation and protection. Am. J. Pathol. 176: 774-785.
35. Huffnagle, G. B., J. L. Yates, and M. F. Lipscomb. 1991. T cell-mediated immunity in the lung: a Cryptococcus neoformans pulmonary infection model using SCID and athymic nude mice. Infect. Immun. 59: 1423-1433.
36. Zheng, C. F., L. L. Ma, G. J. Jones, M. J. Gill, A. M. Krensky, P. Kubes, and C. H. Mody. 2007. Cytotoxic CD4+ T cells use granulysin to kill Cryptococcus neoformans, and activation of this pathway is defective in HIV patients. Blood 109: 2049-2057.
37. Palmer, G., and C. Gabay. 2011. Interleukin-33 biology with potential insights into human diseases. Nat. Rev. Rheumatol. 7: 321-329.
38. Moussion, C., N. Ortega, and J.-P. Girard. 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.
39. Humphreys, N. E., D. Xu, M. R. Hepworth, F. Y. Liew, and R. K. Grencis. 2008. IL-33, a potent inducer of adaptive immunity to intestinal nematodes. J. Immunol. 180: 2443-2449.
40. Nelson, M. P., B. S. Christmann, J. L. Werner, A. E. Metz, J. L. Trevor, C. A. Lowell, and C. Steele. 2011. IL-33 and M2a alveolar macrophages promote lung defense against the atypical fungal pathogen Pneumocystis murina. J. Immunol. 186: 2372-2381.
41. Ramaprakash, H., T. Shibata, K. E. Duffy, U. B. Ismailoglu, R. M. Bredernitz, A. P. Moreira, A. L. Coelho, A. M. Das, N. Fursov, G. L. Chupp, and C. M. Hogaboam. 2011. Targeting ST2L potentiates CpG-mediated therapeutic effects in a chronic fungal asthma model. Am. J. Pathol. 179: 104-115.
42. Scanlon, S. T., and A. N. McKenzie. 2012. Type 2 innate lymphoid cells: new players in asthma and allergy. Curr. Opin. Immunol. 24: 707-712.
43. Chang, Y.-J., H. Y. Kim, L. A. Albacker, N. Baumgarth, A. N. J. McKenzie, D. E. Smith, R. H. Dekruyff, and D. T. Umetsu. 2011. Innate lymphoid cells mediate influenza-induced airway hyper-reactivity independently of adaptive immunity. Nat. Immunol. 12: 631-638.
44. Halim, T. Y. F., R. H. Krauss, A. C. Sun, and F. Takei. 2012. Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergen-induced airway inflammation. Immunity 36: 451-463.
45. Kurowska-Stolarska, M., B. Stolarski, P. Kewin, G. Murphy, C. J. Corrigan, S. Ying, N. Pitman, A. Mirchandani, B. Rana, N. van Rooijen, et al. 2009. IL-33 amplifies the polarization of alternatively activated macrophages that contribute to airway inflammation. J. Immunol. 183: 6469-6477.
46. Guillot, L., S. F. Carroll, R. Homer, and S. T. Qureshi. 2008. Enhanced innate immune responsiveness to pulmonary Cryptococcus neoformans infection is associated with resistance to progressive infection. Infect. Immun. 76: 4745-4756.
47. Pecaric-Petkovic, T., S. A. Didichenko, S. Kaempfer, N. Spiegl, and C. A. Dahinden. 2009. Human basophils and eosinophils are the direct target leukocytes of the novel IL-1 family member IL-33. Blood 113: 1526-1534.
48. Zhou, B., M. R. Comeau, T. De Smedt, H. D. Liggitt, M. E. Dahl, D. B. Lewis, D. Gyarmati, T. Aye, D. J. Campbell, and S. F. Ziegler. 2005. Thymic stromal lymphopoietin as a key initiator of allergic airway inflammation in mice. Nat. Immunol. 6: 1047-1053.
49. Angkasekwinai, P., H. Park, Y. H. Wang, Y. H. Wang, S. H. Chang, D. B. Corry, Y. J. Liu, Z. Zhu, and C. Dong. 2007. Interleukin 25 promotes the initiation of proallergic type 2 responses. J. Exp. Med. 204: 1509-1517.
50. Mirchandani, A. S., R. J. Salmond, and F. Y. Liew. 2012. Interleukin-33 and the function of innate lymphoid cells. Trends Immunol. 33: 389-396.
51. Paul, W. E., and J. Zhu. 2010. How are T(H)2-type immune responses initiated and amplified? Nat. Rev. Immunol. 10: 225-235.
52. Piehler, D., A. Grahnert, M. Eschke, T. Richter, G. Köhler, W. Stenzel, and G. Alber. 2013. T1/ST2 promotes T helper 2 cell activation and polyfunctionality in bronchopulmonary mycosis. Mucosal Immunol. 6: 405-414.
53. Pulendran, B., and D. Artis. 2012. New paradigms in type 2 immunity. Science 337: 431-435.