Selective oxidative protection leads to tissue topological changes orchestrated by macrophage during ulcerative colitis

Juan Du (), Junlei Zhang, Lin Wang, Xun Wang, Yaxing Zhao, Jiaoying Lu, Tingmin Fan, Meng Niu, Jie Zhang, Fei Cheng, Jun Li, Qi Zhu, Daoqiang Zhang, Hao Pei, Guang Li, Xingguang Liang, He Huang, Xiaocang Cao (), Xinjuan Liu (), Wei Shao () and Jianpeng Sheng ()
Additional contact information
Juan Du: Zhejiang University School of Medicine
Junlei Zhang: Zhejiang University School of Medicine
Lin Wang: Zhejiang University School of Medicine
Xun Wang: Zhejiang University School of Medicine
Yaxing Zhao: Zhejiang University School of Medicine
Jiaoying Lu: Zhejiang University School of Medicine
Tingmin Fan: the First Affiliated Hospital, Zhejiang University School of Medicine
Meng Niu: Zhejiang University School of Medicine
Jie Zhang: Zhejiang University School of Medicine
Fei Cheng: Zhejiang University School of Medicine
Jun Li: Zhejiang University School of Medicine
Qi Zhu: Nanjing University of Aeronautics and Astronautics
Daoqiang Zhang: Nanjing University of Aeronautics and Astronautics
Hao Pei: MobiDrop (Zhejiang)
Guang Li: Capital Medical University, Chaoyang District
Xingguang Liang: the First Affiliated Hospital, Zhejiang University School of Medicine
He Huang: Tianjin University
Xiaocang Cao: National Clinical Research Center for Blood Diseases, Haihe Laboratory of Cell Ecosystem, Institute of Hematology & Blood Diseases Hospital, Chinese Academy of Medical Sciences & Peking Union Medical College
Xinjuan Liu: Capital Medical University, Chaoyang District
Wei Shao: Nanjing University of Aeronautics and Astronautics
Jianpeng Sheng: Zhejiang University School of Medicine

Nature Communications, 2023, vol. 14, issue 1, 1-17

Abstract: Abstract Ulcerative colitis is a chronic inflammatory bowel disorder with cellular heterogeneity. To understand the composition and spatial changes of the ulcerative colitis ecosystem, here we use imaging mass cytometry and single-cell RNA sequencing to depict the single-cell landscape of the human colon ecosystem. We find tissue topological changes featured with macrophage disappearance reaction in the ulcerative colitis region, occurring only for tissue-resident macrophages. Reactive oxygen species levels are higher in the ulcerative colitis region, but reactive oxygen species scavenging enzyme SOD2 is barely detected in resident macrophages, resulting in distinct reactive oxygen species vulnerability for inflammatory macrophages and resident macrophages. Inflammatory macrophages replace resident macrophages and cause a spatial shift of TNF production during ulcerative colitis via a cytokine production network formed with T and B cells. Our study suggests components of a mechanism for the observed macrophage disappearance reaction of resident macrophages, providing mechanistic hints for macrophage disappearance reaction in other inflammation or infection situations.

Date: 2023
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DOI: 10.1038/s41467-023-39173-2

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