Lambda interferon restructures the nasal microbiome and increases susceptibility to staphylococcus aureus superinfection
Open accessAbstract
UNLABELLED: Much of the morbidity and mortality associated with influenza virus respiratory infection is due to bacterial coinfection with pathogens that colonize the upper respiratory tract such as methicillin-resistant Staphylococcus aureus (MRSA) and Streptococcus pneumoniae. A major component of the immune response to influenza virus is the production of type I and III interferons. Here we show that the immune response to infection with influenza virus causes an increase and restructuring of the upper respiratory microbiota in wild-type (WT) mice but not in Il28r(-/-) mutant mice lacking the receptor for type III interferon. Mice lacking the IL-28 receptor fail to induce STAT1 phosphorylation and expression of its regulator, SOCS1. Il28r(-/-) mutant mice have increased expression of interleukin-22 (IL-22), as well as Ngal and RegIIIγ, in the nasal cavity, the source of organisms that would be aspirated to cause pneumonia. Proteomic analysis reveals changes in several cytoskeletal proteins that contribute to barrier function in the nasal epithelium that may contribute to the effects of IL-28 signaling on the microbiota. The importance of the effects of IL-28 signaling in the pathogenesis of MRSA pneumonia after influenza virus infection was confirmed by showing that WT mice nasally colonized before or after influenza virus infection had significantly higher levels of infection in the upper airways, as well as significantly greater susceptibility to MRSA pneumonia than Il28r(-/-) mutant mice did. Our results suggest that activation of the type III interferon in response to influenza virus infection has a major effect in expanding the upper airway microbiome and increasing susceptibility to lower respiratory tract infection. IMPORTANCE: S. aureus and influenza virus are important respiratory pathogens, and coinfection with these organisms is associated with significant morbidity and mortality. The ability of influenza virus to increase susceptibility to S. aureus infection is less well understood. We show here that influenza virus leads to a change in the upper airway microbiome in a type III interferon-dependent manner. Mice lacking the type III interferon receptor have altered STAT1 and IL-22 signaling. In coinfection studies, mice without the type III interferon receptor had significantly less nasal S. aureus colonization and subsequent pneumonia than infected WT mice did. This work demonstrates that type III interferons induced by influenza virus contribute to nasal colonization and pneumonia due to S. aureus superinfection.
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Animal studies have suggested that antiviral immune activation contributes to changes in the URT microbiome and facilitate colonization by potential pathogens, such as S. aureus.
“Although the data are still preliminary, animal studies have suggested that antiviral immune activation contributes to changes in the URT microbiome and facilitate colonization by potential pathogens, such as S. aureus.”
From Respiratory viral infection-induced microbiome alterations and secondary bacterial pneumonia. (2018) · cites this paper as [123]
Increased upper respiratory tract persistence of S. aureus as well as increased risk of S. aureus pneumonia was observed in flu-infected wildtype mice compared to mice lacking the type III IFN receptor.
“Increased upper respiratory tract persistence of S. aureus as well as increased risk of S. aureus pneumonia was observed in flu-infected wildtype mice compared to mice lacking the type III IFN receptor (123).”
From Respiratory viral infection-induced microbiome alterations and secondary bacterial pneumonia. (2018) · cites this paper as [123]
Type III IFN, which is also induced during influenza infections, led to changes in the nasal microbiome, including increased numbers of culturable bacteria.
“Type III IFN, which is also induced during influenza infections, led to changes in the nasal microbiome, including increased numbers of culturable bacteria.”
From Respiratory viral infection-induced microbiome alterations and secondary bacterial pneumonia. (2018) · cites this paper as [123]
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- Authors
- Planet, P. J., Parker, D., Cohen, T. S., Smith, H., Leon, J. D., Ryan, C., Hammer, T. J., Fierer, N., Chen, E. I., & Prince, A. S.
- Affiliations
- American Museum of Natural History (US)
- Columbia University (US)
- Herbert Irving Comprehensive Cancer Center (US)
- University of Colorado Boulder (US)
- Cooperative Institute for Research in Environmental Sciences (US)
- Columbia University Irving Medical Center (US)
- Corresponding author
- Prince, Alice S.
- ORCID
- Venue
- mBio
- Publisher
- American Society for Microbiology
- Published
- 2016-03-02
- Volume
- 7
- Issue
- 1
- Pages
- e01939-15
- ISSN
- 2150-7511 (ISSN-L)
- 2161-2129
- PMC
- PMC4752601
- OpenAlex
- W2261043905
- Cited by
- 113
- References
- 62
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 7 · 2023: 10 · 2022: 9 · 2021: 16 · 2020: 27 · 2019: 13 · 2018: 13 · 2017: 6 · 2016: 7
- FWCI
- 7.87
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- mBio (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- CU Scholar (University of Colorado Boulder) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- HHS | National Institutes of Health (K08AI101005, HL079395, P30CA013696, R56HL125653)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
- Health Sciences › Medicine › Epidemiology › Influenza Virus Research Studies
- Health Sciences › Medicine › Epidemiology › Respiratory viral infections research
- Keywords
- interferon lambda, influenza virus, Staphylococcus aureus, MRSA pneumonia, upper respiratory tract microbiome, nasal microbiota, secondary bacterial infection, IL-22, STAT1 signaling, SOCS1, nasal epithelial barrier, cytoskeletal proteins, bacterial co-infection
- MeSH terms
- Interferon Lambda, Animals, Interleukins, Nasal Cavity, Orthomyxoviridae Infections, Pneumonia, Staphylococcal, Staphylococcus aureus, Superinfection, Cytokines, Mice, Knockout, Mice, Microbiota
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