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Surface hydrophobin prevents immune recognition of airborne fungal spores

A Corrigendum to this article was published on 17 June 2010


The air we breathe is filled with thousands of fungal spores (conidia) per cubic metre, which in certain composting environments can easily exceed 109 per cubic metre. They originate from more than a hundred fungal species belonging mainly to the genera Cladosporium, Penicillium, Alternaria and Aspergillus1,2,3,4. Although these conidia contain many antigens and allergens5,6,7, it is not known why airborne fungal microflora do not activate the host innate immune cells continuously and do not induce detrimental inflammatory responses following their inhalation. Here we show that the surface layer on the dormant conidia masks their recognition by the immune system and hence prevents immune response. To explore this, we used several fungal members of the airborne microflora, including the human opportunistic fungal pathogen Aspergillus fumigatus, in in vitro assays with dendritic cells and alveolar macrophages and in in vivo murine experiments. In A. fumigatus, this surface ‘rodlet layer’ is composed of hydrophobic RodA protein covalently bound to the conidial cell wall through glycosylphosphatidylinositol-remnants. RodA extracted from conidia of A. fumigatus was immunologically inert and did not induce dendritic cell or alveolar macrophage maturation and activation, and failed to activate helper T-cell immune responses in vivo. The removal of this surface ‘rodlet/hydrophobin layer’ either chemically (using hydrofluoric acid), genetically (ΔrodA mutant) or biologically (germination) resulted in conidial morphotypes inducing immune activation. All these observations show that the hydrophobic rodlet layer on the conidial cell surface immunologically silences airborne moulds.

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Figure 1: Aspergillus fumigatus conidial surface-hydrophobin, RodA, fails to activate human dendritic cells and CD4+ T lymphocytes.
Figure 2: Dormant conidia of Δ rodA mutant in contrast to wild-type conidia induce maturation and activation of human dendritic cells.
Figure 3: Biological (conidial germination), chemical (hydrofluoric acid-treatment) or genetic (Δ rodA mutant) removal of RodA from dormant conidia induces activation of human dendritic cells and murine alveolar macrophages in vitro.
Figure 4: RodA and wild-type dormant A. fumigatus conidia do not activate murine immune system in vivo , contrary to Δ rodA -dormant or wild-type-germinated conidia.

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We thank J. Vani, Y. Repesse and C. Galeotti for help with dendritic cell experiments; and R. Winkler, S. Behnken and M. Pötsch for help with the MALDI-TOF/TOF analysis. The research of O.K. and A.A.B. was supported by the Deutsche Forschungsgemeinschaft (DFG) Priority Programme 1160, and the EU-STREP Fungwall LSHB-CT-2004-511952 and MANASP LSGBH37899 were also awarded to J.-P.L., A.A.B. and L.R. J.B and S.V.K are supported by INSERM, CNRS and Universities Paris 5 and 6.

Author Contributions J.-P.L. initiated the study; V.A., J.B., L.R. and J.-P.L. designed the research; V.A., C.C., S.P. and J.-P.L. prepared and characterized conidia and fungal materials; J.B., S.R.E. and S.V.K. performed experiments with human dendritic cells; S.B., K.P. and L.R. performed experiments with T-cell clones, murine dendritic cells and macrophages; O.K. and A.A.B. performed protein sequence analysis; V.A., J.B., S.B., O.K., K.P., L.R. and J.-P.L. analysed the results; and V.A., J.B., O.K., L.R. and J.-P.L. wrote the paper.

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Correspondence to Jean-Paul Latgé.

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Aimanianda, V., Bayry, J., Bozza, S. et al. Surface hydrophobin prevents immune recognition of airborne fungal spores. Nature 460, 1117–1121 (2009).

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