Investigation of inflammatory and allergic responses to common mold species: Results from in vitro experiments, from a mouse model of asthma, and from a group of asthmatic patients.
Vincent, Murielle; Percier, Pauline; De Prins, Sophieet al.
Air Microbiology; Air Pollution, Indoor; Alternaria/isolation & purification; Animals; Aspergillus/isolation & purification; Asthma/immunology; Bronchoalveolar Lavage Fluid; Cladosporium/isolation & purification; Cytokines/immunology; Female; Humans; Hypersensitivity/immunology; Immunoglobulin E/blood; Inflammation/immunology; Lung/pathology; Mice; Mice, Inbred C57BL; Penicillium/isolation & purification; asthma; dot-blot assay; indoor molds; inflammatory properties of molds; mold sensitization; mouse model of asthma
Abstract :
[en] Most studies on molds focus on Alternaria alternata and Aspergillus fumigatus. Here, we report on inflammatory and allergenic properties of more typical indoor species Aspergillus versicolor, P. chrysogenum, C. cladosporioïdes, and C. sphaerospermum that were compared to A. alternata and A. fumigatus. In a mouse model, after intranasal instillation, A. alternaria, A. versicolor, and C. sphaerospermum induced the early recruitment of neutrophils and the strong expression of inflammatory markers in the bronchoalveolar lavages fluids. A. fumigatus also induced the early accumulation of neutrophils but with lower levels of inflammatory markers. Chronic treatment induced variable response according to species: P. chrysogenum and A. fumigatus appeared strong pro-allergenic inducers compared to A. alternata and C. sphaerospermum while A. versicolor and C. cladosporioides induced a mixed pro-allergenic/pro-inflammatory response. In mold-sensitized asthmatics, mold-specific Immunoglobulin E (IgE) were detected with an in-house dot-blot assay. A. fumigatus and A. alternata were the most frequent sensitizers. Altogether, P. chrysogenum, P. brevicompactum, C. sphaerospermum, and C. cladosporïoides were the "major sensitizer" (defined as the strongest response against a single mold species) for almost 30% of the asthmatics. These results show that, not only A. alternata and A. fumigatus, but also indoor species have strong inflammatory and allergic properties and a harmful potency.
Disciplines :
Immunology & infectious disease
Author, co-author :
Vincent, Murielle
Percier, Pauline
De Prins, Sophie
Huygen, Kris
Potemberg, Georges ; Centre Hospitalier Universitaire de Liège - CHU > Département de Physique Médicale > STA Assurance qualité
Romano, Marta
Michel, Olivier
Muraille, Eric
Denis, Olivier
Language :
English
Title :
Investigation of inflammatory and allergic responses to common mold species: Results from in vitro experiments, from a mouse model of asthma, and from a group of asthmatic patients.
Twaroch TE, Curin M, Valenta R, Swoboda I. Mold allergens in respiratory allergy: from structure to therapy. Allergy Asthma Immunol Res. 2015;7:205-220.
Drummond RA, Saijo S, Iwakura Y, Brown GD. The role of Syk/CARD9 coupled C-type lectins in antifungal immunity. Eur J Immunol. 2011;41:276-281.
Werner JL, Metz AE, Horn D, et al. Requisite role for the dectin-1 beta-glucan receptor in pulmonary defense against Aspergillus fumigatus. J Immunol. 2009;182:4938-4946.
Rivera A. Protective immune responses to fungal infections. Parasite Immunol. 2014;36:453-462.
Rivera A, Hohl TM, Collins N, et al. Dectin-1 diversifies Aspergillus fumigatus-specific T cell responses by inhibiting T helper type 1 CD4 T cell differentiation. J Exp Med. 2011;208:369-381.
Romani L. Immunity to fungal infections. Nat Rev Immunol. 2011;11:275-288.
Scheurer S, Toda M, Vieths S. What makes an allergen? Clin Exp Allergy. 2015;45:1150-1161.
Shakib F, Ghaemmaghami AM, Sewell HF. The molecular basis of allergenicity. Trends Immunol. 2008;29:633-642.
Umetsu DT, McIntire JJ, Akbari O, Macaubas C, DeKruyff RH. Asthma: an epidemic of dysregulated immunity. Nat Immunol. 2002;3:715-720.
Barnes PJ. Pathophysiology of allergic inflammation. Immunol Rev. 2011;242:31-50.
Lambrecht BN, Hammad H. The immunology of asthma. Nat Immunol. 2015;16:45-56.
Al-Ramli W, Prefontaine D, Chouiali F, et al. T(H)17-associated cytokines (IL-17A and IL-17F) in severe asthma. J Allergy Clin Immunol. 2009;123:1185-1187.
Zureik M, Neukirch C, Leynaert B, Liard R, Bousquet J, Neukirch F. Sensitisation to airborne moulds and severity of asthma: cross sectional study from European Community respiratory health survey. BMJ. 2002;325:411-414.
Black PN, Udy AA, Brodie SM. Sensitivity to fungal allergens is a risk factor for life-threatening asthma. Allergy. 2000;55:501-504.
Nevalainen A, Taubel M, Hyvarinen A. Indoor fungi: companions and contaminants. Indoor Air. 2015;25:125-156.
Portnoy JM, Barnes CS, Kennedy K. Importance of mold allergy in asthma. Curr Allergy Asthma Rep. 2008;8:71-78.
Choi H, Byrne S, Larsen LS, et al. Residential culturable fungi, (1-3, 1-6)-beta-d-glucan, and ergosterol concentrations in dust are not associated with asthma, rhinitis, or eczema diagnoses in children. Indoor Air. 2014;24:158-170.
Fisk WJ, Eliseeva EA, Mendell MJ. Association of residential dampness and mold with respiratory tract infections and bronchitis: a meta-analysis. Environ Health. 2010;9:72.
Mendell MJ, Mirer AG, Cheung K, Tong M, Douwes J. Respiratory and allergic health effects of dampness, mold, and dampness-related agents: a review of the epidemiologic evidence. Environ Health Perspect. 2011;119:748-756.
Behbod B, Sordillo JE, Hoffman EB, et al. Asthma and allergy development: contrasting influences of yeasts and other fungal exposures. Clin Exp Allergy. 2015;45:154-163.
Sharpe RA, Bearman N, Thornton CR, Husk K, Osborne NJ. Indoor fungal diversity and asthma: a meta-analysis and systematic review of risk factors. J Allergy Clin Immunol. 2015;135:110-122.
Beguin H. Mould biodiversity in homes. I. Air and surfaces analysis of 130 dwellings. Aerobiologia. 1994;10:157-166.
Bellanger AP, Reboux G, Roussel S, et al. Indoor fungal contamination of moisture-damaged and allergic patient housing analysed using real-time PCR. Lett Appl Microbiol. 2009;49:260-266.
Horner WE, Worthan AG, Morey PR. Air- and dustborne mycoflora in houses free of water damage and fungal growth. Appl Environ Microbiol. 2004;70:6394-6400.
Reboux G, Bellanger AP, Roussel S, et al. Indoor mold concentration in Eastern France. Indoor Air. 2009;19:446-453.
Achatz G, Oberkofler H, Lechenauer E, et al. Molecular cloning of major and minor allergens of Alternaria alternata and Cladosporium herbarum. Mol Immunol. 1995;32:213-227.
Inaba K, Inaba M, Romani N, et al. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med. 1992;176:1693-1702.
Denis O, van den Brule S, Heymans J, et al. Chronic intranasal administration of mould spores or extracts to unsensitized mice leads to lung allergic inflammation, hyper-reactivity and remodelling. Immunology. 2007;122:268-278.
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. Clin Exp Immunol. 2005;139:179-188.
Korf JE, Pynaert G, Tournoy K, et al. Macrophage reprogramming by mycolic acid promotes a tolerogenic response in experimental asthma. Am J Respir Crit Care Med. 2006;174:152-160.
GINA: Global Initiative for Asthma: Global Strategy for Asthma Management and Prevention. In 2014. 2014.
Vincent M, Romano M, Corazza F, Huygen K, Michel O, Denis O. Development of a dot-blot assay for the detection of mould-specific IgE in the Belgian population. Mycopathologia. 2016;182:319-329.
Crameri R, Garbani M, Rhyner C, Huitema C. Fungi: the neglected allergenic sources. Allergy. 2014;69:176-185.
Soeria-Atmadja D, Onell A, Borga A. IgE sensitization to fungi mirrors fungal phylogenetic systematics. J Allergy Clin Immunol. 2010;125:1379-1386.
Jaakkola MS, Quansah R, Hugg TT, Heikkinen SA, Jaakkola JJ. Association of indoor dampness and molds with rhinitis risk: a systematic review and meta-analysis. J Allergy Clin Immunol. 2013;132:1099-1110.
Quansah R, Jaakkola MS, Hugg TT, Heikkinen SA, Jaakkola JJ. Residential dampness and molds and the risk of developing asthma: a systematic review and meta-analysis. PLoS One. 2012;7:e47526.
Karvonen AM, Hyvarinen A, Korppi M, et al. Moisture damage and asthma: a birth cohort study. Pediatrics. 2015;135:e598-e606.
Rocchi S, Reboux G, Frossard V, et al. Microbiological characterization of 3193 French dwellings of Elfe cohort children. Sci Total Environ. 2015;505:1026-1035.
Hardison SE, Brown GD. C-type lectin receptors orchestrate antifungal immunity. Nat Immunol. 2012;13:817-822.
Fei M, Bhatia S, Oriss TB, et al. TNF-alpha from inflammatory dendritic cells (DCs) regulates lung IL-17A/IL-5 levels and neutrophilia versus eosinophilia during persistent fungal infection. Proc Natl Acad Sci USA. 2011;108:5360-5365.
Lee YS, Yang H, Yang JY, et al. Interleukin-1 (IL-1) signaling in intestinal stromal cells controls KC/CXCL1 secretion, which correlates with recruitment of IL-22- secreting neutrophils at early stages of Citrobacter rodentium infection. Infect Immun. 2015;83:3257-3267.
van de Veerdonk FL, Joosten LA, Netea MG. The interplay between inflammasome activation and antifungal host defense. Immunol Rev. 2015;265:172-180.
Mintz-Cole RA, Gibson AM, Bass SA, Budelsky AL, Reponen T, Hershey GK. Dectin-1 and IL-17A suppress murine asthma induced by Aspergillus versicolor but not Cladosporium cladosporioides due to differences in beta-glucan surface exposure. J Immunol. 2012;189:3609-3617.
Shimoda K, van Deursen J, Sangster MY, et al. Lack of IL-4-induced Th2 response and IgE class switching in mice with disrupted Stat6 gene. Nature. 1996;380:630-633.
Bartemes KR, Iijima K, Kobayashi T, Kephart GM, McKenzie AN, Kita H. IL-33-responsive lineage- CD25+ CD44(hi) lymphoid cells mediate innate type 2 immunity and allergic inflammation in the lungs. J Immunol. 2012;188:1503-1513.
Denis O, Vincent M, Havaux X, De PS, Treutens G, Huygen K. Induction of the specific allergic immune response is independent of proteases from the fungus Alternaria alternata. Eur J Immunol. 2013;43:907-917.
Lefrancais E, Roga S, Gautier V, et al. IL-33 is processed into mature bioactive forms by neutrophil elastase and cathepsin G. Proc Natl Acad Sci USA. 2012;109:1673-1678.
Mintz-Cole RA, Brandt EB, Bass SA, Gibson AM, Reponen T, Khurana Hershey GK. Surface availability of beta-glucans is critical determinant of host immune response to Cladosporium cladosporioides. J Allergy Clin Immunol. 2013;132:159-169.
Chamilos G, Ganguly D, Lande R, et al. Generation of IL-23 producing dendritic cells (DCs) by airborne fungi regulates fungal pathogenicity via the induction of T(H)-17 responses. PLoS One. 2010;5:e12955.
McKinley L, Alcorn JF, Peterson A, et al. TH17 cells mediate steroid-resistant airway inflammation and airway hyperresponsiveness in mice. J Immunol. 2008;181:4089-4097.
Newcomb DC, Peebles RS Jr. Th17-mediated inflammation in asthma. Curr Opin Immunol. 2013;25:755-760.
Zijlstra GJ, Ten Hacken NH, Hoffmann RF, van Oosterhout AJ, Heijink IH. Interleukin-17A induces glucocorticoid insensitivity in human bronchial epithelial cells. Eur Respir J. 2012;39:439-445.
Crameri R, Zeller S, Glaser AG, Vilhelmsson M, Rhyner C. Cross-reactivity among fungal allergens: a clinically relevant phenomenon? Mycoses. 2009;52:99-106.
Simon-Nobbe B, Denk U, Poll V, Rid R, Breitenbach M. The spectrum of fungal allergy. Int Arch Allergy Immunol. 2008;145:58-86.
Platts-Mills TA, Schuyler AJ, Erwin EA, Commins SP, Woodfolk JA. IgE in the diagnosis and treatment of allergic disease. J Allergy Clin Immunol. 2016;137:1662-1670.