Respiratory influenza virus infection induces intestinal immune injury via microbiota-mediated Th17 cell-dependent inflammation
Open accessAbstract
Influenza in humans is often accompanied by gastroenteritis-like symptoms such as diarrhea, but the underlying mechanism is not yet understood. We explored the occurrence of gastroenteritis-like symptoms using a mouse model of respiratory influenza infection. We found that respiratory influenza infection caused intestinal injury when lung injury occurred, which was not due to direct intestinal viral infection. Influenza infection altered the intestinal microbiota composition, which was mediated by IFN-γ produced by lung-derived CCR9(+)CD4(+) T cells recruited into the small intestine. Th17 cells markedly increased in the small intestine after PR8 infection, and neutralizing IL-17A reduced intestinal injury. Moreover, antibiotic depletion of intestinal microbiota reduced IL-17A production and attenuated influenza-caused intestinal injury. Further study showed that the alteration of intestinal microbiota significantly stimulated IL-15 production from intestinal epithelial cells, which subsequently promoted Th17 cell polarization in the small intestine in situ. Thus, our findings provide new insights into an undescribed mechanism by which respiratory influenza infection causes intestinal disease.
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In a murine model of influenza infection, although total numbers of bacteria in the gut did not decrease, there was a reduction in quantities of segmented filamentous bacteria (SFB) and Lactobacillus/Lactococcus, accompanied by increases in Enterobacteriaceae.
“In a murine model of influenza infection, the investigators found that although the total numbers of bacteria in the gut did not decrease, there was a reduction in the quantities of segmented filamentous bacteria (SFB) and Lactobacillus/Lactococcus, accompanied by increases in Enterobacteriaceae.”
From Respiratory viral infection-induced microbiome alterations and secondary bacterial pneumonia. (2018) · cites this paper as [43]
In flu-infected mice, increased IL-17A levels and numbers of Th17 cells in the small intestine and colon appeared to contribute to intestinal injury.
“flu-infected mice had increased IL-17A levels and numbers of Th17 cells in the small intestine and colon, which appeared to contribute to intestinal injury”
From Respiratory viral infection-induced microbiome alterations and secondary bacterial pneumonia. (2018) · cites this paper as [43]
Antibiotic treatment prior to influenza infection ameliorated the degree of intestinal injury, but not lung injury, suggesting that gut dysbiosis contributed to local but not systemic inflammation.
“antibiotic treatment prior to influenza infection ameliorated the degree of intestinal injury, but not lung injury, suggesting that gut dysbiosis contributed to local but not systemic inflammation”
From Respiratory viral infection-induced microbiome alterations and secondary bacterial pneumonia. (2018) · cites this paper as [43]
Influenza infection alters intestinal microbiota composition through type II IFN produced by lung-derived T cells recruited to the intestine.
“influenza infection alters intestinal microbiota composition through type II IFN produced by lung-derived T cells recruited to the intestine”
From Respiratory viral infection-induced microbiome alterations and secondary bacterial pneumonia. (2018) · cites this paper as [43]
Using animal models of pulmonary infections by influenza and RSV, multiple groups have shown that the gut microbiome is clearly impacted by respiratory viral infections, despite the lack of detectable respiratory virus in the gut.
“Using animal models of pulmonary infections by influenza and respiratory syncytial virus (RSV), multiple groups have shown that the gut microbiome is clearly impacted by respiratory viral infections, despite the lack of detectable respiratory virus in the gut”
From Respiratory viral infection-induced microbiome alterations and secondary bacterial pneumonia. (2018) · cites this paper as [43]
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- Authors
- Wang, J., Li, F., Wei, H., Lian, Z.-X., Sun, R., & Tian, Z.
- Affiliations
- University of Science and Technology of China (CN)
- Corresponding author
- Tian, Zhigang
- Venue
- Journal of Experimental Medicine
- Publisher
- Rockefeller University Press
- Published
- 2014-11-03
- Volume
- 211
- Issue
- 12
- Pages
- 2397-2410
- ISSN
- 0022-1007 (ISSN-L)
- 1540-9538
- PMC
- PMC4235643
- OpenAlex
- W2145520421
- Cited by
- 490
- References
- 56
- Citations by year
- 2026: 32 · 2025: 46 · 2024: 56 · 2023: 41 · 2022: 69 · 2021: 90 · 2020: 50 · 2019: 27 · 2018: 17 · 2017: 22 · 2016: 21 · 2015: 14 · 2014: 3 · 2013: 1
- FWCI
- 15.11
- Type
- journal article
- Language
- en
- Update notices
- correction (2014-12-08)
- Open access
- bronze
- doi.org
- Locations
- The Journal of Experimental Medicine (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Funders
- National Natural Science Foundation of China
- China Postdoctoral Science Foundation
- Shandong Academy of Medical Sciences
- Fundamental Research Funds for the Central Universities
- Topics
- Health Sciences › Medicine › Epidemiology › Influenza Virus Research Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
- Keywords
- influenza, intestinal injury, gut microbiota, Th17 cells, IL-17A, IL-15, interferon-gamma, small bowel inflammation, intestinal epithelial cells, antibiotic depletion
- MeSH terms
- Animals, Epithelial Cells, Flow Cytometry, Humans, Inflammation, Intestines, Lung, Male, Mice, Inbred C57BL, Orthomyxoviridae Infections, CD4-Positive T-Lymphocytes, Mice, Knockout, Interleukin-15, Chemokines, CC, Reverse Transcriptase Polymerase Chain Reaction, Interleukin-17, Influenza A Virus, H1N1 Subtype, Receptors, CCR, Host-Pathogen Interactions, Antibodies, Neutralizing, Th17 Cells, Microbiota
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Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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