The Beta-Glucan Receptor Dectin-1 Recognizes Specific Morphologies of Aspergillus fumigatus

Steele, Chad; Rapaka, Rekha R; Metz, Allison; Pop, Shannon M; Williams, David L; Gordon, Siamon; Kolls, Jay K; Brown, Gordon D

doi:10.1371/journal.ppat.0010042

Cited by 509Antifungal resistance and susceptibilityImmune Response and InflammationFungal and yeast genetics research

The Beta-Glucan Receptor Dectin-1 Recognizes Specific Morphologies of Aspergillus fumigatus

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Steele, Chad, Rapaka, Rekha R, Metz, Allison, Pop, Shannon M, Williams, David L, Gordon, Siamon, Kolls, Jay K, Brown, Gordon D·2005·PLoS Pathogens

DOI 10.1371/journal.ppat.0010042PMC PMC1311140

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Abstract

Alveolar macrophages represent a first-line innate host defense mechanism for clearing inhaled Aspergillus fumigatus from the lungs, yet contradictory data exist as to which alveolar macrophage recognition receptor is critical for innate immunity to A. fumigatus. Acknowledging that the A. fumigatus cell wall contains a high beta-1,3-glucan content, we questioned whether the beta-glucan receptor dectin-1 played a role in this recognition process. Monoclonal antibody, soluble receptor, and competitive carbohydrate blockage indicated that the alveolar macrophage inflammatory response, specifically the production of tumor necrosis factor-alpha (TNF-alpha), interleukin-1alpha (IL-1alpha), IL-1beta, IL-6, CXCL2/macrophage inflammatory protein-2 (MIP-2), CCL3/macrophage inflammatory protein-1alpha (MIP-1alpha), granulocyte-colony stimulating factor (G-CSF), and granulocyte monocyte-CSF (GM-CSF), to live A. fumigatus was dependent on recognition via the beta-glucan receptor dectin-1. The inflammatory response was triggered at the highest level by A. fumigatus swollen conidia and early germlings and correlated to the levels of surface-exposed beta glucans, indicating that dectin-1 preferentially recognizes specific morphological forms of A. fumigatus. Intratracheal administration of A. fumigatus conidia to mice in the presence of a soluble dectin-Fc fusion protein reduced both lung proinflammatory cytokine/chemokine levels and cellular recruitment while modestly increasing the A. fumigatus fungal burden, illustrating the importance of beta-glucan-initiated dectin-1 signaling in defense against this pathogen. Collectively, these data show that dectin-1 is centrally required for the generation of alveolar macrophage proinflammatory responses to A. fumigatus and to our knowledge provides the first in vivo evidence for the role of dectin-1 in fungal innate defense.

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The discovery of selective activation of Dectin-1/Syk signaling during germination of Aspergillus conidia due to stage-specific surface exposure of β-glucan and the ability of PRR to regulate phagosome maturation provided the conceptual framework of PAMPs masking as a mechanism employed by fungi to escape macrophage killing.
“The discovery of selective activation of Dectin-1/Syk signaling during germination of Aspergillus conidia due to stage-specific surface exposure of β-glucan (194, 246, 247) and the ability of PRR to regulate phagosome maturation (248) provided the conceptual framework of pathogen-associated molecular patterns (PAMPs) masking as a mechanism employed by fungi to escape macrophage killing.”
From Aspergillus fumigatus and Aspergillosis in 2019 (2019) · cites this paper as [246]

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Authors: Steele, C., Rapaka, R. R., Metz, A., Pop, S. M., Williams, D. L., Gordon, S., Kolls, J. K., & Brown, G. D.
Affiliations: University of Pittsburgh (US)
East Tennessee State University (US)
University of Oxford (GB)
University of Cape Town (ZA)
Corresponding author: Steele, Chad
ORCID: Steele, Chad
Rapaka, Rekha R
Williams, David L
Gordon, Siamon
Kolls, Jay K
Brown, Gordon D
Venue: PLoS Pathogens
Publisher: Public Library of Science (PLoS)
Published: 2005-12-09
Volume: 1
Issue: 4
Pages: e42
ISSN: 1553-7366 (ISSN-L)
1553-7374
DOI: 10.1371/journal.ppat.0010042
PMC: PMC1311140
OpenAlex: W1985371834
Cited by: 509
References: 46
Citations by year: 2026: 11 · 2025: 12 · 2024: 12 · 2023: 14 · 2022: 17 · 2021: 23 · 2020: 27 · 2019: 15 · 2018: 22 · 2017: 28 · 2016: 25 · 2015: 32 · 2014: 27 · 2013: 31 · 2012: 32
FWCI: 17.34
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS Pathogens (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
D-Scholarship@Pitt (University of Pittsburgh) (acceptedVersion)
Digital Commons - East Tennessee State University (East Tennessee State University) (submittedVersion, cc-by)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Open University of Cape Town (University of Cape Town) (submittedVersion, cc-by)
Funders: American Lung Association
Wellcome Trust (055109, 070018)
National Heart, Lung, and Blood Institute (HL 61721, R01HL080317, HL080317, R01HL062052, HL62052)
Topics: Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Keywords: Dectin-1, beta-glucan receptor, Aspergillus fumigatus, alveolar macrophages, conidial morphology, germlings, inflammatory cytokines, chemokines, fungal clearance
MeSH terms: Dectin-1, Aspergillosis, Aspergillus fumigatus, Fungal Proteins, Humans, Inflammation, Membrane Proteins, Nerve Tissue Proteins, Cytokines, Macrophages, Alveolar, Chemokines, Lectins, C-Type

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The Beta-Glucan Receptor Dectin-1 Recognizes Specific Morphologies of Aspergillus fumigatus

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