The imbalance of pulmonary Th17/Treg cells in BALB/c suckling mice infected with respiratory syncytial virus-mediated intestinal immune damage and gut microbiota changes

Jiling Liu; Yixuan Huang; Nian Liu; Huan Qiu; Xiaoyan Zhang; Xiaojie Liu; Maozhang He; Mingwei Chen; Shenghai Huang

doi:10.1128/spectrum.03283-23

Microbiology Spectrum (Jun 2024)

The imbalance of pulmonary Th17/Treg cells in BALB/c suckling mice infected with respiratory syncytial virus-mediated intestinal immune damage and gut microbiota changes

Jiling Liu,
Yixuan Huang,
Nian Liu,
Huan Qiu,
Xiaoyan Zhang,
Xiaojie Liu,
Maozhang He,
Mingwei Chen,
Shenghai Huang

Affiliations

Jiling Liu: Department of Microbiology, The Key Laboratory of Microbiology and Parasitology of Anhui Province, The Key Laboratory of Zoonoses of High Institutions in Anhui, School of Basic Medical Sciences, Anhui Medical University, Hefei, Anhui, China
Yixuan Huang: Department of Endocrinology, The First Affiliated Hospital of Anhui Medical University, Hefei, Anhui, China
Nian Liu: Department of Critical Care Medicine, The First Affiliated Hospital of Anhui Medical University, Hefei, Anhui, China
Huan Qiu: School of Nursing, Anhui Medical University, Hefei, Anhui, China
Xiaoyan Zhang: Department of Microbiology, The Key Laboratory of Microbiology and Parasitology of Anhui Province, The Key Laboratory of Zoonoses of High Institutions in Anhui, School of Basic Medical Sciences, Anhui Medical University, Hefei, Anhui, China
Xiaojie Liu: Department of Microbiology, The Key Laboratory of Microbiology and Parasitology of Anhui Province, The Key Laboratory of Zoonoses of High Institutions in Anhui, School of Basic Medical Sciences, Anhui Medical University, Hefei, Anhui, China
Maozhang He: Department of Microbiology, The Key Laboratory of Microbiology and Parasitology of Anhui Province, The Key Laboratory of Zoonoses of High Institutions in Anhui, School of Basic Medical Sciences, Anhui Medical University, Hefei, Anhui, China
Mingwei Chen: Department of Endocrinology, The First Affiliated Hospital of Anhui Medical University, Hefei, Anhui, China
Shenghai Huang: Department of Microbiology, The Key Laboratory of Microbiology and Parasitology of Anhui Province, The Key Laboratory of Zoonoses of High Institutions in Anhui, School of Basic Medical Sciences, Anhui Medical University, Hefei, Anhui, China

DOI: https://doi.org/10.1128/spectrum.03283-23
Journal volume & issue: Vol. 12, no. 6

Abstract

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ABSTRACT The immune response induced by respiratory syncytial virus (RSV) infection is closely related to changes in the composition and function of gastrointestinal microorganisms. However, the specific mechanism remains unknown and the pulmonary-intestinal axis deserves further study. In this study, the mRNA levels of ROR-γt and Foxp3 in the lung and intestine increased first and then decreased. IL-17 and IL-22 reached the maximum on the third day after infection in the lung, and on the second day after infection in the small intestine and colon, respectively. RegⅢγ in intestinal tissue reached the maximum on the third day after RSV infection. Moreover, the genus enriched in the RSV group was Aggregatibacter, and Proteus was reduced. RSV infection not only causes Th17/Treg cell imbalance in the lungs of mice but also leads to the release of excessive IL-22 from the lungs through blood circulation which binds to IL-22 receptors on the intestinal surface, inducing RegⅢγ overexpression, impaired intestinal Th17/Treg development, and altered gut microbiota composition. Our research reveals a significant link between the pulmonary and intestinal axis after RSV infection.IMPORTANCERSV is the most common pathogen causing acute lower respiratory tract infections in infants and young children, but the complex interactions between the immune system and gut microbiota induced by RSV infection still requires further research. In this study, it was suggested that RSV infection in 7-day-old BALB/c suckling mice caused lung inflammation and disruption of Th17/Treg cells development, and altered the composition of gut microbiota through IL-22 induced overexpression of RegⅢγ, leading to intestinal immune injury and disruption of gut microbiota. This research reveals that IL-22 may be the link between the lung and gut. This study may provide a new insight into the intestinal symptoms caused by RSV and other respiratory viruses and the connection between the lung and gut axis, as well as new therapeutic ideas for the treatment of RSV-infected children.

Published in Microbiology Spectrum

ISSN: 2165-0497 (Online)
Publisher: American Society for Microbiology
Country of publisher: United States
LCC subjects: Science: Microbiology
Website: https://journals.asm.org/journal/spectrum

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