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Immunity, Apr 24 2025, S1074-7613(25)00167-0 | https://doi.org/10.1016/j.immuni.2025.04.004
IL-10 sensing by lung interstitial macrophages prevents bacterial dysbiosis-driven pulmonary inflammation and maintains immune homeostasis
Seung Hyeon Kim,1,14 Zachary White,2,14 Anastasiia Gainullina,3 Soeun Kang,4 Jiseon Kim,1 Joseph R. Dominguez,1 Yeonwoo Choi,1 Ivan Cabrera,2 Madison Plaster,5 Michihiro Takahama,5 Rafael S. Czepielewski,6,7 Jinki Yeom,8,9 Matthias Gunzer,10,11 Nissim Hay,4,12 Odile David,12,13 Nicolas Chevrier,5 Teruyuki Sano,2,12,* and Ki-Wook Kim 1,12,15,*
1Department of Pharmacology and Regenerative Medicine, University of Illinois College of Medicine, Chicago, IL, USA
2Department of Microbiology and Immunology, University of Illinois College of Medicine, Chicago, IL, USA
3Life Improvement by Future Technologies (LIFT) Center, Skolkovo, Moscow, Russia
4Department of Biochemistry and Genetics, University of Illinois College of Medicine, Chicago, IL, USA
5Pritzker School of Molecular Engineering, University of Chicago, Chicago, IL, USA
6Immunology Center of Georgia, Department of Physiology, Medical College of Georgia, Augusta University, Augusta, GA, USA
7Georgia Cancer Center, Augusta University, Augusta, GA, USA
8Department of Microbiology and Immunology, College of Medicine, Seoul National University, Seoul, Republic of Korea
9Cancer Research Institute, Seoul National University, Seoul, Republic of Korea
10Institute for Experimental Immunology and Imaging, University Hospital Essen, University of Duisburg-Essen, Essen, Germany
11Leibniz-Institut fu¨r Analytische Wissenschaften - ISAS - e.V., Dortmund, Germany
12University of Illinois Cancer Center, University of Illinois at Chicago, Chicago, IL, USA
13Department of Pathology, University of Illinois College of Medicine, Chicago, IL, USA
14These authors contributed equally
15Lead contact
2Department of Microbiology and Immunology, University of Illinois College of Medicine, Chicago, IL, USA
3Life Improvement by Future Technologies (LIFT) Center, Skolkovo, Moscow, Russia
4Department of Biochemistry and Genetics, University of Illinois College of Medicine, Chicago, IL, USA
5Pritzker School of Molecular Engineering, University of Chicago, Chicago, IL, USA
6Immunology Center of Georgia, Department of Physiology, Medical College of Georgia, Augusta University, Augusta, GA, USA
7Georgia Cancer Center, Augusta University, Augusta, GA, USA
8Department of Microbiology and Immunology, College of Medicine, Seoul National University, Seoul, Republic of Korea
9Cancer Research Institute, Seoul National University, Seoul, Republic of Korea
10Institute for Experimental Immunology and Imaging, University Hospital Essen, University of Duisburg-Essen, Essen, Germany
11Leibniz-Institut fu¨r Analytische Wissenschaften - ISAS - e.V., Dortmund, Germany
12University of Illinois Cancer Center, University of Illinois at Chicago, Chicago, IL, USA
13Department of Pathology, University of Illinois College of Medicine, Chicago, IL, USA
14These authors contributed equally
15Lead contact
*Corresponding authors: correspondence to Teruyuki Sano or Ki-Wook Kim
Abstract
Crosstalk between the immune system and the microbiome is critical for maintaining immune homeostasis. Here, we examined this communication and the impact of immune-suppressive IL-10 signaling on pulmonary homeostasis. We found that IL-10 sensing by interstitial macrophages (IMs) is required to prevent spontaneous lung inflammation. Loss of IL-10 signaling in IMs initiated an inflammatory cascade through the activation of classical monocytes and CD4+ T cell subsets, leading to chronic lung inflammation with age. Analyses of antibiotic-treated and germ-free mice established that lung inflammation in the animals lacking IL-10 signaling was triggered by commensal bacteria. 16S rRNA sequencing revealed Delftia acidovorans and Rhodococcus erythropolis as potential drivers of lung inflammation. Intranasal administration of these bacteria or transplantation of human fecal microbiota elicited lung inflammation in gnotobiotic Il10-deficient mice. These findings highlight that IL-10 sensing by IMs contributes to pulmonary homeostasis by preventing lung inflammation caused by commensal dysbiosis.
논문정보
- Research article
- 2025년 04월 (BRIC 등록일 2025-05-07)
- 국내+국외 연구진
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