The IL-33/ST2 axis is crucial in type 2 airway responses induced by Staphylococcus aureus–derived serine protease–like protein D

Journal of Allergy and Clinical Immunology

Volumn 141, Issue 2, 2018, Pages 549-559.e7

  Teufelberger, Andrea R ^a,b   Nordengrün, Maria ^c   Braun, Harald ^a,b   Maes, Tania ^a   De Grove, Katrien ^a   Holtappels, Gabriele ^a   O'Brien, Clara ^a   Provoost, Sharen ^a   Hammad, Hamida ^a,b   Gonçalves, Amanda ^a,b   Beyaert, Rudi ^a,b   Declercq, Wim ^a,b   Vandenabeele, Peter ^a,b   Krysko, Dmitri V ^a   Bröker, Barbara M ^c   Bachert, Claus ^a   Krysko, Olga ^a  

^a GHENT UNIVERSITY   (Belgium)

^b DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^c UNIVERSITY MEDICINE GREIFSWALD   (Germany)

Author keywords

Allergy; asthma; sensitization; serine protease; Staphylococcus aureus

Indexed keywords

ANTIASTHMATIC AGENT; BACTERIAL PROTEIN; EOTAXIN; IMMUNOGLOBULIN E; INTERLEUKIN 13; INTERLEUKIN 33; INTERLEUKIN 5; RAG2 PROTEIN; RECOMBINANT PROTEIN; RECOMBINANT STAPHYLOCOCCUS AUREUS DERIVED SERINE PROTEASE LIKE PROTEIN; SOMATOSTATIN RECEPTOR 2; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; IL1RL1 PROTEIN, MOUSE; IL33 PROTEIN, MOUSE; INTERLEUKIN 1 RECEPTOR LIKE 1 PROTEIN; SERINE PROTEINASE;

ADAPTIVE IMMUNITY; ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRONCHUS HYPERREACTIVITY; CD4+ T LYMPHOCYTE; CELL HYPERPLASIA; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG MECHANISM; ENZYME LINKED IMMUNOSORBENT ASSAY; EOSINOPHILIA; FEMALE; FLOW CYTOMETRY; GOBLET CELL; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; LYMPHOID CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; TH2 CELL; WILD TYPE MOUSE; ANIMAL; ASTHMA; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECT; GENETICS; IMMUNOLOGY; PATHOGENICITY; PATHOLOGY; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS;

ANIMALS; ASTHMA; BACTERIAL PROTEINS; CD4-POSITIVE T-LYMPHOCYTES; DISEASE MODELS, ANIMAL; INTERLEUKIN-1 RECEPTOR-LIKE 1 PROTEIN; INTERLEUKIN-33; MICE; MICE, KNOCKOUT; SERINE PROTEASES; SIGNAL TRANSDUCTION; STAPHYLOCOCCUS AUREUS; TH2 CELLS;

EID: 85020927932     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2017.05.004     Document Type: Article

References (63)

1. Reginald, K., Westritschnig, K., Werfel, T., Heratizadeh, A., Novak, N., Focke-Tejkl, M., et al. Immunoglobulin E antibody reactivity to bacterial antigens in atopic dermatitis patients. Clin Exp Allergy 41 (2011), 357–369.
2. Bachert, C., Zhang, N., Holtappels, G., De Lobel, L., van Cauwenberge, P., Liu, S., et al. Presence of IL-5 protein and IgE antibodies to staphylococcal enterotoxins in nasal polyps is associated with comorbid asthma. J Allergy Clin Immunol 126 (2010), 962–968 e1-6.
3. Kobayashi, T., Glatz, M., Horiuchi, K., Kawasaki, H., Akiyama, H., Kaplan, D.H., et al. Dysbiosis and Staphylococcus aureus colonization drives inflammation in atopic dermatitis. Immunity 42 (2015), 756–766.
4. Sachse, F., Becker, K., von Eiff, C., Metze, D., Rudack, C., Staphylococcus aureus invades the epithelium in nasal polyposis and induces IL-6 in nasal epithelial cells in vitro. Allergy 65 (2010), 1430–1437.
5. Tomassen, P., Vandeplas, G., Van Zele, T., Cardell, L.-O., Arebro, J., Olze, H., et al. Inflammatory endotypes of chronic rhinosinusitis based on cluster analysis of biomarkers. J Allergy Clin Immunol 137 (2016), 1449–1456.e4.
6. Thammavongsa, V., Kim, H.K., Missiakas, D., Schneewind, O., Staphylococcal manipulation of host immune responses. Nat Rev Microbiol 13 (2015), 529–543.
7. Cho, S.H., Strickland, I., Tomkinson, A., Fehringer, A.P., Gelfand, E.W., Leung, D.Y., Preferential binding of Staphylococcus aureus to skin sites of Th2-mediated inflammation in a murine model. J Invest Dermatol 116 (2001), 658–663.
8. Nakamura, Y., Oscherwitz, J., Cease, K.B., Chan, S.M., Muñoz-Planillo, R., Hasegawa, M., et al. Staphylococcus δ-toxin induces allergic skin disease by activating mast cells. Nature 503 (2013), 397–401.
9. Bröker, B., Mrochen, D., Péton, V., The T cell response to Staphylococcus aureus. Pathogens, 5, 2016, 31.
10. Kusch, H., Engelmann, S., Secrets of the secretome in Staphylococcus aureus. Int J Med Microbiol 304 (2014), 133–141.
11. Schlievert, P.M., Strandberg, K.L., Lin, Y.-C., Peterson, M.L., Leung, D.Y.M., Secreted virulence factor comparison between methicillin-resistant and methicillin-sensitive Staphylococcus aureus, and its relevance to atopic dermatitis. J Allergy Clin Immunol 125 (2010), 39–49.
12. Bachert, C., Van Steen, K., Zhang, N., Holtappels, G., Cattaert, T., Maus, B., et al. Specific IgE against Staphylococcus aureus enterotoxins: an independent risk factor for asthma. J Allergy Clin Immunol 130 (2012), 376–381.e8.
13. Bachert, C., Akdis, C.A., Phenotypes and emerging endotypes of chronic rhinosinusitis. J allergy Clin Immunol Pract 4 (2016), 621–628.
14. Stentzel, S., Teufelberger, A., Nordengrün, M., Kolata, J., Schmidt, F., van Crombruggen, K., et al. Staphylococcal serine protease-like proteins are pacemakers of allergic airway reactions to Staphylococcus aureus. J Allergy Clin Immunol 139 (2017), 492–500.e8.
15. Zdzalik, M., Karim, A.Y., Wolski, K., Buda, P., Wojcik, K., Brueggemann, S., et al. Prevalence of genes encoding extracellular proteases in Staphylococcus aureus—important targets triggering immune response in vivo. FEMS Immunol Med Microbiol 66 (2012), 220–229.
16. de Boer, J.D., Van't Veer, C., Stroo, I., van der Meer, A.J., de Vos, A.F., van der Zee, J.S., et al. Protease-activated receptor-2 deficient mice have reduced house dust mite-evoked allergic lung inflammation. Innate Immun 20 (2014), 618–625.
17. Steelant, B., Farré R., Wawrzyniak, P., Belmans, J., Dekimpe, E., Vanheel, H., et al. Impaired barrier function in patients with house dust mite–induced allergic rhinitis is accompanied by decreased occludin and zonula occludens-1 expression. J Allergy Clin Immunol 137 (2016), 1043–1053.e5.
18. Hartl, D., Latzin, P., Hordijk, P., Marcos, V., Rudolph, C., Woischnik, M., et al. Cleavage of CXCR1 on neutrophils disables bacterial killing in cystic fibrosis lung disease. Nat Med 13 (2007), 1423–1430.
19. Takai, T., Kato, T., Ota, M., Yasueda, H., Kuhara, T., Okumura, K., et al. Recombinant Der p 1 and Der f 1 with in vitro enzymatic activity to cleave human CD23, CD25 and alpha1-antitrypsin, and in vivo IgE-eliciting activity in mice. Int Arch Allergy Immunol 137 (2005), 194–200.
20. Schmitz, J., Owyang, A., Oldham, E., Song, Y., Murphy, E., McClanahan, T.K., 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 23 (2005), 479–490.
21. Kouzaki, H., Iijima, K., Kobayashi, T., O'Grady, S.M., 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 186 (2011), 4375–4387.
22. Oboki, K., Nakae, S., Matsumoto, K., Saito, H., IL-33 and airway inflammation. Allergy Asthma Immunol Res 3 (2011), 81–88.
23. Lloyd, C.M., IL-33 family members and asthma—bridging innate and adaptive immune responses. Curr Opin Immunol 22 (2010), 800–806.
24. Hayakawa, H., Hayakawa, M., Kume, A., Tominaga, S., Soluble ST2 blocks interleukin-33 signaling in allergic airway inflammation. J Biol Chem 282 (2007), 26369–26380.
25. Willart, M.A.M., Deswarte, K., Pouliot, P., Braun, H., Beyaert, R., Lambrecht, B.N., et al. Interleukin-1 controls allergic sensitization to inhaled house dust mite via the epithelial release of GM-CSF and IL-33. J Exp Med 209 (2012), 1505–1517.
26. Fahy, J.V., Type 2 inflammation in asthma—present in most, absent in many. Nat Rev Immunol 15 (2015), 57–65.
27. Miller, A.M., Role of IL-33 in inflammation and disease. J Inflamm (Lond), 8, 2011, 22.
28. Murphy, J.M., Czabotar, P.E., Hildebrand, J.M., Lucet, I.S., Zhang, J.-G., Alvarez-Diaz, S., et al. The pseudokinase MLKL mediates necroptosis via a molecular switch mechanism. Immunity 39 (2013), 443–453.
29. Boitano, S., Flynn, A.N., Sherwood, C.L., Schulz, S.M., Hoffman, J., Gruzinova, I., et al. Alternaria alternata serine proteases induce lung inflammation and airway epithelial cell activation via PAR2. Am J Physiol Lung Cell Mol Physiol 300 (2011), L605–L614.
30. Jacquet, A., Innate immune responses in house dust mite allergy. ISRN Allergy 2013 (2013), 1–18.
31. Matsui, K., Nishikawa, A., Peptidoglycan from Staphylococcus aureus induces T(H)2 immune response in mice. J Investig Allergol Clin Immunol 22 (2012), 80–86.
32. Hammad, H., Chieppa, M., Perros, F., Willart, M.A., Germain, R.N., Lambrecht, B.N., House dust mite allergen induces asthma via TLR4 triggering of airway structural cells. Nat Med 15 (2009), 410–416.
33. De Grove, K.C., Provoost, S., Hendriks, R.W., McKenzie, A.N.J., Seys, L.J.M., Kumar, S., et al. Dysregulation of type 2 innate lymphoid cells and Th2 cells impairs pollutant-induced allergic airway responses. J Allergy Clin Immunol 139 (2016), 246–257.e4.
34. Lambrecht, B.N., Hammad, H., Allergens and the airway epithelium response: gateway to allergic sensitization. J Allergy Clin Immunol 134 (2015), 499–507.
35. Bartemes, K.R., Iijima, K., Kobayashi, T., Kephart, G.M., McKenzie, A.N., Kita, H., IL-33-responsive lineage- CD25+ CD44(hi) lymphoid cells mediate innate type 2 immunity and allergic inflammation in the lungs. J Immunol 188 (2012), 1503–1513.
36. Liew, F.Y., Pitman, N.I., McInnes, I.B., Disease-associated functions of IL-33: the new kid in the IL-1 family. Nat Rev Immunol 10 (2010), 103–110.
37. Mohapatra, A., Van Dyken, S.J., Schneider, C., Nussbaum, J.C., Liang, H.-E., Locksley, R.M., Group 2 innate lymphoid cells utilize the IRF4-IL-9 module to coordinate epithelial cell maintenance of lung homeostasis. Mucosal Immunol 9 (2016), 275–286.
38. Haenuki, Y., Matsushita, K., Futatsugi-Yumikura, S., Ishii, K.J., Kawagoe, T., Imoto, Y., et al. A critical role of IL-33 in experimental allergic rhinitis. J Allergy Clin Immunol 130 (2012), 184–194.e11.
39. Morita, H., Arae, K., Unno, H., Miyauchi, K., Toyama, S., Nambu, A., et al. An interleukin-33-mast cell-interleukin-2 axis suppresses papain-induced allergic inflammation by promoting regulatory T cell numbers. Immunity 43 (2015), 175–186.
40. Chu, D.K., Llop-Guevara, A., Walker, T.D., Flader, K., Goncharova, S., Boudreau, J.E., et al. IL-33, but not thymic stromal lymphopoietin or IL-25, is central to mite and peanut allergic sensitization. J Allergy Clin Immunol 131 (2013), 187–200 e1-8.
41. Li, C., Li, H., Jiang, Z., Zhang, T., Wang, Y., Li, Z., et al. Interleukin-33 increases antibacterial defense by activation of inducible nitric oxide synthase in skin. PLoS Pathog, 10, 2014, e1003918.
42. Matsuwaki, Y., Wada, K., White, T.A., Benson, L.M., Charlesworth, M.C., Checkel, J.L., et al. Recognition of fungal protease activities induces cellular activation and eosinophil-derived neurotoxin release in human eosinophils. J Immunol 183 (2009), 6708–6716.
43. Ebeling, C., Lam, T., Gordon, J.R., Hollenberg, M.D., Vliagoftis, H., Proteinase-activated receptor-2 promotes allergic sensitization to an inhaled antigen through a TNF-mediated pathway. J Immunol 179 (2007), 2910–2917.
44. López, M.L., Soriano-Sarabia, N., Bruges, G., Marquez, M.E., Preissner, K.T., Schmitz, M.L., et al. Expression pattern of protease activated receptors in lymphoid cells. Cell Immunol 288 (2014), 47–52.
45. Rothmeier, A.S., Ruf, W., Protease-activated receptor 2 signaling in inflammation. Semin Immunopathol 34 (2012), 133–149.
46. Christianson, C.A., Goplen, N.P., Zafar, I., Irvin, C., Good, J.T., Rollins, D.R., et al. Persistence of asthma requires multiple feedback circuits involving type 2 innate lymphoid cells and IL-33. J Allergy Clin Immunol 136 (2015), 59–68.e14.
47. Lefrançais, E., Duval, A., Mirey, E., Roga, S., Espinosa, E., Cayrol, C., et al. Central domain of IL-33 is cleaved by mast cell proteases for potent activation of group-2 innate lymphoid cells. Proc Natl Acad Sci U S A 111 (2014), 15502–15507.
48. Lefrancais, E., Roga, S., Gautier, V., Gonzalez-de-Peredo, A., Monsarrat, B., Girard, J.-P., et al. IL-33 is processed into mature bioactive forms by neutrophil elastase and cathepsin G. Proc Natl Acad Sci U S A 109 (2012), 1673–1678.
49. Zoltowska, A.M., Lei, Y., Fuchs, B., Rask, C., Adner, M., Nilsson, G.P., The interleukin-33 receptor ST2 is important for the development of peripheral airway hyperresponsiveness and inflammation in a house dust mite mouse model of asthma. Clin Exp Allergy 46 (2016), 479–490.
50. Iijima, K., Kobayashi, T., Hara, K., Kephart, G.M., Ziegler, S.F., McKenzie, A.N., et al. IL-33 and thymic stromal lymphopoietin mediate immune pathology in response to chronic airborne allergen exposure. J Immunol 193 (2014), 1549–1559.
51. Castanhinha, S., Sherburn, R., Walker, S., Gupta, A., Bossley, C.J., Buckley, J., et al. Pediatric severe asthma with fungal sensitization is mediated by steroid-resistant IL-33. J Allergy Clin Immunol 136 (2015), 312–322.e7.
52. van Helden, M.J., Lambrecht, B.N., Dendritic cells in asthma. Curr Opin Immunol 25 (2013), 745–754.
53. Rank, M.A., Kobayashi, T., Kozaki, H., Bartemes, K.R., Squillace, D.L., Kita, H., IL-33-activated dendritic cells induce an atypical TH2-type response. J Allergy Clin Immunol 123 (2009), 1047–1054.
54. Besnard, A.-G., Togbe, D., Guillou, N., Erard, F., Quesniaux, V., Ryffel, B., IL-33-activated dendritic cells are critical for allergic airway inflammation. Eur J Immunol 41 (2011), 1675–1686.
55. Halim, T.Y.F., Krauss, R.H., Sun, A.C., Takei, F., Lung natural helper cells are a critical source of Th2 cell-type cytokines in protease allergen-induced airway inflammation. Immunity 36 (2012), 451–463.
56. Halim, T.Y.F., MacLaren, A., Romanish, M.T., Gold, M.J., McNagny, K.M., Takei, F., Retinoic-acid-receptor-related orphan nuclear receptor alpha is required for natural helper cell development and allergic inflammation. Immunity 37 (2012), 463–474.
57. Halim, T.Y.F., Steer, C.A., Math, L., Gold, M.J., Martinez-Gonzalez, I., McNagny, K.M., et al. Group 2 innate lymphoid cells are critical for the initiation of adaptive T helper 2 cell-mediated allergic lung inflammation. Immunity 40 (2014), 425–435.
58. Huvenne, W., Callebaut, I., Plantinga, M., Vanoirbeek, J.A.J., Krysko, O., Bullens, D.M.A., et al. Staphylococcus aureus enterotoxin B facilitates allergic sensitization in experimental asthma. Clin Exp Allergy 40 (2010), 1079–1090.
59. Krysko, O., Maes, T., Plantinga, M., Holtappels, G., Imiru, R., Vandenabeele, P., et al. The adjuvant-like activity of staphylococcal enterotoxin B in a murine asthma model is independent of IL-1R signaling. Allergy 68 (2013), 446–453.
60. Maes, T., Provoost, S., Lanckacker, E., Cataldo, D.D., Vanoirbeek, J.J., Nemery, B., et al. Mouse models to unravel the role of inhaled pollutants on allergic sensitization and airway inflammation. Respir Res, 11, 2010, 7.
61. Reed, S.B., Wesson, C.A., Liou, L.E., Trumble, W.R., Schlievert, P.M., Bohach, G.A., et al. Molecular characterization of a novel Staphylococcus aureus serine protease operon. Infect Immun 69 (2001), 1521–1527.
62. Zdzalik, M., Kalinska, M., Wysocka, M., Stec-Niemczyk, J., Cichon, P., Stach, N., et al. Biochemical and structural characterization of SplD protease from Staphylococcus aureus. PLoS One, 8, 2013, e76812.
63. Stentzel, S., Teufelberger, A., Nordengrün, M., Kolata, J., Schmidt, F., van Crombruggen, K., et al. Staphylococcal serine protease-like proteins are pacemakers of allergic airway reactions to Staphylococcus aureus. J Allergy Clin Immunol 139 (2017), 492–500.e8.