Denis, Olivier
[Program Allergology, WIV-ISP (site Ukkel), Brussels, Belgium]
Vincent, Muriel
[Program Allergology, WIV-ISP (site Ukkel), Brussels, Belgium]
Havaux, Xavier
[UCL]
De Prins, Sofie
[Program Allergology, WIV-ISP (site Ukkel), Brussels, Belgium]
Treutens, Greta
[Program Allergology, WIV-ISP (site Ukkel), Brussels, Belgium]
Huygen, Kris
[Scientific Service Immunology, WIV-ISP (site Ukkel), Brussels, Belgium]
We have analyzed the importance of proteases for the induction of allergic responses against the mold Alternaria alternata. Responses induced in vivo with untreated or heat treated (protease inactivated) extracts were compared in BALB/c, C57BL/6, TLR4 KO, and MyD88 KO mice. In BALB/c mice, both extracts induced similar lung inflammation, upregulation of inflammatory mediators, Th2 cytokines, and Alternaria-specific antibodies. However heat inactivation abrogated polyclonal IgE production. Similar results were obtained in C57BL/6 albeit lung expression of some Th2 mediators was decreased in mice stimulated with the heat-treated extract. Treatment of the extract with protease inhibitors did not affect the induction of the allergic response either, except again for the polyclonal IgE response. Th2 responses and lung inflammation were readily induced in TLR4 knockout mice. In contrast, lung inflammation, Th2 responses, cytokine productions, and antibody synthesis were strongly suppressed in MyD88-deficient mice. Early lung IL-33 and IL-1-α expression were also suppressed. In conclusion, albeit some heat labile proteases are required for the stimulation of the polyclonal IgE secretion, fungal proteases, and TLR4 signaling are not required while MyD88 is essential for triggering the systemic immune response and for the development of lung allergic inflammation in response to Alternaria extracts. © 2013 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim.
- Umetsu Dale T., McIntire Jennifer J., Akbari Omid, Macaubas Claudia, DeKruyff Rosemarie H., Asthma: an epidemic of dysregulated immunity, 10.1038/ni0802-715
- Romagnani Sergio, The increased prevalence of allergy and the hygiene hypothesis: missing immune deviation, reduced immune suppression, or both?, 10.1111/j.1365-2567.2004.01925.x
- Akbari Omid, DeKruyff Rosemarie H., Umetsu Dale T., 10.1038/90667
- Shakib Farouk, Ghaemmaghami Amir M., Sewell Herb F., The molecular basis of allergenicity, 10.1016/j.it.2008.08.007
- RUNSWICK Sarah, MITCHELL Thomas, DAVIES Paul, ROBINSON Clive, GARROD David R., Pollen proteolytic enzymes degrade tight junctions, 10.1111/j.1440-1843.2007.01175.x
- Kauffman Henk F., van der Heide Sicco, Exposure, sensitization, and mechanisms of fungus-induced asthma, 10.1007/s11882-003-0080-z
- Wan H., Winton H. L., Soeller C., Taylor G. W., Gruenert D. C., Thompson P. J., Cannell M. B., Stewart G. A., Garrod D. R., Robinson C., The transmembrane protein occludin of epithelial tight junctions is a functional target for serine peptidases from faecal pellets of Dermatophagoides pteronyssinus, 10.1046/j.1365-2222.2001.00970.x
- Bhat R. K., Page K., Tan A., Hershenson M. B., German cockroach extract increases bronchial epithelial cell interleukin-8 expression, 10.1046/j.1365-2222.2002.01481.x
- Borger P., Koëter G. H., Timmerman J. A. B., Vellenga E., Tomee J. F. C., Kauffman H. F., Proteases fromAspergillus fumigatusInduce Interleukin (IL)–6 and IL‐8 Production in Airway Epithelial Cell Lines by Transcriptional Mechanisms, 10.1086/315027
- Chiu L.-L., Perng D.-W., Yu C.-H., Su S.-N., Chow L.-P., Mold Allergen, Pen c 13, Induces IL-8 Expression in Human Airway Epithelial Cells by Activating Protease-Activated Receptor 1 and 2, 10.4049/jimmunol.178.8.5237
- Wills-Karp M, Nathan A, Page K, Karp C L, New insights into innate immune mechanisms underlying allergenicity, 10.1038/mi.2009.138
- Kheradmand F., Kiss A., Xu J., Lee S.-H., Kolattukudy P. E., Corry D. B., A Protease-Activated Pathway Underlying Th Cell Type 2 Activation and Allergic Lung Disease, 10.4049/jimmunol.169.10.5904
- McKerrow James H., Caffrey Conor, Kelly Ben, Loke P'ng, Sajid Mohammed, PROTEASES IN PARASITIC DISEASES, 10.1146/annurev.pathol.1.110304.100151
- Sokol Caroline L, Barton Gregory M, Farr Andrew G, Medzhitov Ruslan, A mechanism for the initiation of allergen-induced T helper type 2 responses, 10.1038/ni1558
- Bush Robert K., Prochnau Jay J., Alternaria-induced asthma☆, 10.1016/j.jaci.2003.11.023
- Havaux X., Zeine A., Dits A., Denis O., A new mouse model of lung allergy induced by the spores of Alternaria alternata and Cladosporium herbarum molds, 10.1111/j.1365-2249.2004.02679.x
- Denis Olivier, van den Brûle Sybille, Heymans Julie, Havaux Xavier, Rochard Christelle, Huaux François, Huygen Kris, Chronic intranasal administration of mould spores or extracts to unsensitized mice leads to lung allergic inflammation, hyper-reactivity and remodelling, 10.1111/j.1365-2567.2007.02636.x
- Gueders Maud M., Paulissen Genevieve, Crahay Celine, Quesada-Calvo Florence, Hacha Jonathan, Van Hove Chris, Tournoy Kurt, Louis Renaud, Foidart Jean-Michel, Noël Agnes, Cataldo Didier D., Mouse models of asthma: a comparison between C57BL/6 and BALB/c strains regarding bronchial responsiveness, inflammation, and cytokine production, 10.1007/s00011-009-0054-2
- Hollingsworth J. W., Whitehead G. S., Lin K. L., Nakano H., Gunn M. D., Schwartz D. A., Cook D. N., TLR4 Signaling Attenuates Ongoing Allergic Inflammation, 10.4049/jimmunol.176.10.5856
- Eisenbarth Stephanie C., Piggott Damani A., Huleatt James W., Visintin Irene, Herrick Christina A., Bottomly Kim, Lipopolysaccharide-enhanced, Toll-like Receptor 4–dependent T Helper Cell Type 2 Responses to Inhaled Antigen, 10.1084/jem.20021340
- Tan A. M., Chen H.-C., Pochard P., Eisenbarth S. C., Herrick C. A., Bottomly H. K., TLR4 Signaling in Stromal Cells Is Critical for the Initiation of Allergic Th2 Responses to Inhaled Antigen, 10.4049/jimmunol.0900340
- Hammad Hamida, Chieppa Marcello, Perros Frederic, Willart Monique A, Germain Ronald N, Lambrecht Bart N, House dust mite allergen induces asthma via Toll-like receptor 4 triggering of airway structural cells, 10.1038/nm.1946
- Kouzaki H., O'Grady S. M., Lawrence C. B., Kita H., Proteases Induce Production of Thymic Stromal Lymphopoietin by Airway Epithelial Cells through Protease-Activated Receptor-2, 10.4049/jimmunol.0900904
- Matsuwaki Y., Wada K., White T. A., Benson L. M., Charlesworth M. C., Checkel J. L., Inoue Y., Hotta K., Ponikau J. U., Lawrence C. B., Kita H., Recognition of Fungal Protease Activities Induces Cellular Activation and Eosinophil-Derived Neurotoxin Release in Human Eosinophils, 10.4049/jimmunol.0901220
- Kobayashi T., Iijima K., Radhakrishnan S., Mehta V., Vassallo R., Lawrence C. B., Cyong J.-C., Pease L. R., Oguchi K., Kita H., Asthma-Related Environmental Fungus, Alternaria, Activates Dendritic Cells and Produces Potent Th2 Adjuvant Activity, 10.4049/jimmunol.0802773
- Gough Lucy, Schulz Oliver, Sewell Herb F., Shakib Farouk, The Cysteine Protease Activity of the Major Dust Mite Allergen Der P 1 Selectively Enhances the Immunoglobulin E Antibody Response, 10.1084/jem.190.12.1897
- Boitano S., Flynn A. N., Sherwood C. L., Schulz S. M., Hoffman J., Gruzinova I., Daines M. O., Alternaria alternata serine proteases induce lung inflammation and airway epithelial cell activation via PAR2, 10.1152/ajplung.00359.2010
- Doherty T. A., Khorram N., Sugimoto K., Sheppard D., Rosenthal P., Cho J. Y., Pham A., Miller M., Croft M., Broide D. H., Alternaria Induces STAT6-Dependent Acute Airway Eosinophilia and Epithelial FIZZ1 Expression That Promotes Airway Fibrosis and Epithelial Thickness, 10.4049/jimmunol.1101632
- Porter P, Susarla S C, Polikepahad S, Qian Y, Hampton J, Kiss A, Vaidya S, Sur S, Ongeri V, Yang T, Delclos G L, Abramson S, Kheradmand F, Corry D B, Link between allergic asthma and airway mucosal infection suggested by proteinase-secreting household fungi, 10.1038/mi.2009.102
- Pastor F.J., Guarro J., Alternaria infections: laboratory diagnosis and relevant clinical features, 10.1111/j.1469-0691.2008.02024.x
- Willart Monique A.M., Deswarte Kim, Pouliot Philippe, Braun Harald, Beyaert Rudi, Lambrecht Bart N., Hammad Hamida, Interleukin-1α controls allergic sensitization to inhaled house dust mite via the epithelial release of GM-CSF and IL-33, 10.1084/jem.20112691
- Mjösberg Jenny, Bernink Jochem, Peters Charlotte, Spits Hergen, Transcriptional control of innate lymphoid cells : HIGHLIGHTS, 10.1002/eji.201242639
- Scanlon Seth T, McKenzie Andrew NJ, Type 2 innate lymphoid cells: new players in asthma and allergy, 10.1016/j.coi.2012.08.009
- Doherty T. A., Khorram N., Chang J. E., Kim H.-K., Rosenthal P., Croft M., Broide D. H., STAT6 regulates natural helper cell proliferation during lung inflammation initiated by Alternaria, 10.1152/ajplung.00174.2012
- Zhang Lili, Lu Rong, Zhao Guiqiu, Pflugfelder Stephen C., Li De-Quan, TLR-mediated induction of pro-allergic cytokine IL-33 in ocular mucosal epithelium, 10.1016/j.biocel.2011.06.003
- Kouzaki Hideaki, Iijima Koji, Kobayashi Takao, O’Grady Scott M., Kita Hirohito, The Danger Signal, Extracellular ATP, Is a Sensor for an Airborne Allergen and Triggers IL-33 Release and Innate Th2-Type Responses, 10.4049/jimmunol.1003020
- Kroeger K. M., Sullivan B. M., Locksley R. M., IL-18 and IL-33 elicit Th2 cytokines from basophils via a MyD88- and p38 -dependent pathway, 10.1189/jlb.0708452
- Lee Chun Geun, Da Silva Carla A., Dela Cruz Charles S., Ahangari Farida, Ma Bing, Kang Min-Jong, He Chuan-Hua, Takyar Seyedtaghi, Elias Jack A., Role of Chitin and Chitinase/Chitinase-Like Proteins in Inflammation, Tissue Remodeling, and Injury, 10.1146/annurev-physiol-012110-142250
- Da Silva Carla A., Pochard Pierre, Lee Chun Geun, Elias Jack A., Chitin Particles Are Multifaceted Immune Adjuvants, 10.1164/rccm.200912-1877oc
- Reese Tiffany A., Liang Hong-Erh, Tager Andrew M., Luster Andrew D., Van Rooijen Nico, Voehringer David, Locksley Richard M., Chitin induces accumulation in tissue of innate immune cells associated with allergy, 10.1038/nature05746
- Nathan Amy T., Peterson Elizabeth A., Chakir Jamila, Wills-Karp Marsha, Innate immune responses of airway epithelium to house dust mite are mediated through β-glucan–dependent pathways, 10.1016/j.jaci.2008.12.006
- Huang H-J, Lin Y-L, Liu C-F, Kao H-F, Wang J-Y, Mite allergen decreases DC-SIGN expression and modulates human dendritic cell differentiation and function in allergic asthma, 10.1038/mi.2011.17
- Shreffler W. G., Castro R. R., Kucuk Z. Y., Charlop-Powers Z., Grishina G., Yoo S., Burks A. W., Sampson H. A., The Major Glycoprotein Allergen from Arachis hypogaea, Ara h 1, Is a Ligand of Dendritic Cell-Specific ICAM-Grabbing Nonintegrin and Acts as a Th2 Adjuvant In Vitro, 10.4049/jimmunol.177.6.3677
- Thomas P. G., Carter M. R., Da'dara A. A., DeSimone T. M., Harn D. A., A Helminth Glycan Induces APC Maturation via Alternative NF- B Activation Independent of I B Degradation, 10.4049/jimmunol.175.4.2082
- Harn Donald A., McDonald Jasmine, Atochina Olga, Da’dara Akram A., Modulation of host immune responses by helminth glycans, 10.1111/j.1600-065x.2009.00799.x
- Paris S., Fitting C., Latgé J.P., Herman D., Guinnepain M.T., David B., Comparison of Conidial and Mycelial Allergens of Alternaria alternata, 10.1159/000235216
- Korf Johanna E., Pynaert Gwenda, Tournoy Kurt, Boonefaes Tom, Van Oosterhout Antoon, Ginneberge Daisy, Haegeman Anuschka, Verschoor Jan A., De Baetselier Patrick, Grooten Johan, Macrophage Reprogramming by Mycolic Acid Promotes a Tolerogenic Response in Experimental Asthma, 10.1164/rccm.200507-1175oc
Bibliographic reference |
Denis, Olivier ; Vincent, Muriel ; Havaux, Xavier ; De Prins, Sofie ; Treutens, Greta ; et. al. Induction of the specific allergic immune response is independent of proteases from the fungus Alternaria alternata. In: European Journal of Immunology, Vol. 43, no. 4, p. 907-917 (2013) |
Permanent URL |
http://hdl.handle.net/2078.1/160671 |