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Research Article

Lambda Interferon Restructures the Nasal Microbiome and Increases Susceptibility to Staphylococcus aureus Superinfection

Paul J. Planet, Dane Parker, Taylor S. Cohen, Hannah Smith, Justinne D. Leon, Chanelle Ryan, Tobin J. Hammer, Noah Fierer, Emily I. Chen, Alice S. Prince
Olaf Schneewind, Editor
Paul J. Planet
aDepartment of Pediatrics, Division of Pediatric Infectious Diseases, Columbia University, College of Physicians and Surgeons, New York, New York, USA
bSackler Institute for Comparative Genomics, American Museum of Natural History, New York, New York, USA
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Dane Parker
aDepartment of Pediatrics, Division of Pediatric Infectious Diseases, Columbia University, College of Physicians and Surgeons, New York, New York, USA
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Taylor S. Cohen
aDepartment of Pediatrics, Division of Pediatric Infectious Diseases, Columbia University, College of Physicians and Surgeons, New York, New York, USA
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Hannah Smith
aDepartment of Pediatrics, Division of Pediatric Infectious Diseases, Columbia University, College of Physicians and Surgeons, New York, New York, USA
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Justinne D. Leon
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Chanelle Ryan
aDepartment of Pediatrics, Division of Pediatric Infectious Diseases, Columbia University, College of Physicians and Surgeons, New York, New York, USA
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Tobin J. Hammer
cDepartment of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado, USA
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Noah Fierer
cDepartment of Ecology and Evolutionary Biology, University of Colorado, Boulder, Colorado, USA
dCooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, Colorado, USA
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Emily I. Chen
eProteomics Shared Resource at the Herbert Irving Comprehensive Cancer Center & Department of Pharmacology, Columbia University Medical Center, New York, New York, USA
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Alice S. Prince
aDepartment of Pediatrics, Division of Pediatric Infectious Diseases, Columbia University, College of Physicians and Surgeons, New York, New York, USA
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Olaf Schneewind
University of Chicago
Roles: Editor
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DOI: 10.1128/mBio.01939-15
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ABSTRACT

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.

  • Copyright © 2016 Planet et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-ShareAlike 3.0 Unported license, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Lambda Interferon Restructures the Nasal Microbiome and Increases Susceptibility to Staphylococcus aureus Superinfection
Paul J. Planet, Dane Parker, Taylor S. Cohen, Hannah Smith, Justinne D. Leon, Chanelle Ryan, Tobin J. Hammer, Noah Fierer, Emily I. Chen, Alice S. Prince
mBio Feb 2016, 7 (1) e01939-15; DOI: 10.1128/mBio.01939-15

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Lambda Interferon Restructures the Nasal Microbiome and Increases Susceptibility to Staphylococcus aureus Superinfection
Paul J. Planet, Dane Parker, Taylor S. Cohen, Hannah Smith, Justinne D. Leon, Chanelle Ryan, Tobin J. Hammer, Noah Fierer, Emily I. Chen, Alice S. Prince
mBio Feb 2016, 7 (1) e01939-15; DOI: 10.1128/mBio.01939-15
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