The microbiota protects against respiratory infection via GM-CSF signaling

Brown, Rebecca L.; Sequeira, Richard P.; Clarke, Thomas B.

doi:10.1038/s41467-017-01803-x

Cited by 380Gut microbiota and healthImmune Response and InflammationPlant-Microbe Interactions and Immunity

The microbiota protects against respiratory infection via GM-CSF signaling

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Brown, Rebecca L., Sequeira, Richard P., Clarke, Thomas B.·2017·Nature Communications

DOI 10.1038/s41467-017-01803-xPMC PMC5688119

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Abstract

The microbiota promotes resistance to respiratory infection, but the mechanistic basis for this is poorly defined. Here, we identify members of the microbiota that protect against respiratory infection by the major human pathogens Streptococcus pneumoniae and Klebsiella pneumoniae. We show that the microbiota enhances respiratory defenses via granulocyte-macrophage colony-stimulating factor (GM-CSF) signaling, which stimulates pathogen killing and clearance by alveolar macrophages through extracellular signal-regulated kinase signaling. Increased pulmonary GM-CSF production in response to infection is primed by the microbiota through interleukin-17A. By combining models of commensal colonization in antibiotic-treated and germ-free mice, using cultured commensals from the Actinobacteria, Bacteroidetes, Firmicutes, and Proteobacteria phyla, we found that potent Nod-like receptor-stimulating bacteria in the upper airway (Staphylococcus aureus and Staphylococcus epidermidis) and intestinal microbiota (Lactobacillus reuteri, Enterococcus faecalis, Lactobacillus crispatus and Clostridium orbiscindens) promote resistance to lung infection through Nod2 and GM-CSF. Our data reveal the identity, location, and properties of bacteria within the microbiota that regulate lung immunity, and delineate the host signaling axis they activate to protect against respiratory infection.

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Administration of Lactobacillus reuteri, Enterococcus faecalis, Lactobacillus crispatus, and Clostridium orbiscindens, which are strong stimulators of NOD2, are able to protect against bacterial pneumonia by enhancing GM-CSF production.
“administration of Lactobacillus reuteri, Enterococcus faecalis, Lactobacillus crispatus, and Clostridium orbiscindens, which are strong stimulators of NOD2 (i.e., cytosolic receptor for muramyl dipeptide, which is found in cell walls of certain bacteria), are able to protect against bacterial pneumonia by enhancing GM-CSF production”
From Respiratory viral infection-induced microbiome alterations and secondary bacterial pneumonia. (2018) · cites this paper as [66]

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Authors: Brown, R. L., Sequeira, R. P., & Clarke, T. B.
Affiliations: Imperial College London (GB)
Corresponding author: Clarke, Thomas B.
ORCID: Sequeira, Richard P.
Clarke, Thomas B.
Venue: Nature Communications
Publisher: Springer Science and Business Media LLC
Published: 2017-11-15
Volume: 8
Issue: 1
Pages: 1512-1512
ISSN: 2041-1723 (ISSN-L)
DOI: 10.1038/s41467-017-01803-x
PMC: PMC5688119
OpenAlex: W2768027710
Cited by: 378
References: 50
Citations by year: 2026: 30 · 2025: 39 · 2024: 53 · 2023: 36 · 2022: 56 · 2021: 52 · 2020: 68 · 2019: 27 · 2018: 17
FWCI: 12.74
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0 (tdm)
creativecommons.org/licenses/by/4.0 (vor)
Locations: Nature Communications (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Spiral (Imperial College London) (submittedVersion, cc-by)
Funders: Wellcome Trust (107660/Z/15/Z, 107660)
Medical Research Council (MR/J006874/1)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant-Microbe Interactions and Immunity
Keywords: gut microbiota, respiratory infections, GM-CSF signaling, Streptococcus pneumoniae, Klebsiella pneumoniae, alveolar macrophages, ERK signaling, IL-17A, NOD2, NOD-like receptors, Staphylococcus aureus, Staphylococcus epidermidis, Lactobacillus reuteri, Enterococcus faecalis, lung immunity, commensal bacteria, germ-free mice, antibiotic-treated mice
MeSH terms: Animals, Humans, Klebsiella pneumoniae, Lung, Mice, Inbred C57BL, Respiratory Tract Infections, Streptococcus pneumoniae, Signal Transduction, Granulocyte-Macrophage Colony-Stimulating Factor, Macrophages, Alveolar, Mice, Knockout, Interleukin-17, Microbial Interactions, HEK293 Cells, Microbiota

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