CD103+ T Cells Eliminate Damaged Alveolar Epithelial Type II Cells Under Oxidative Stress to Prevent Lung Tumorigenesis

Abstract The nexus between aging‐associated immune deteriorations and tumorigenesis of lung cancers remains elusive. In a mouse model with Med23 depletion in T cells (Med23 −/−), it is found a strong association between the decline of CD103+ T cells and spontaneous alveolar epithelial type II cell (...

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Main Authors: Yu Xu, Haorui Luo, Jiahao Wang, Haifeng Liu, Luonan Chen, Hongbin Ji, Zimu Deng, Xiaolong Liu
Format: Article
Language:English
Published: Wiley 2025-07-01
Series:Advanced Science
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Online Access:https://doi.org/10.1002/advs.202503557
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author Yu Xu
Haorui Luo
Jiahao Wang
Haifeng Liu
Luonan Chen
Hongbin Ji
Zimu Deng
Xiaolong Liu
author_facet Yu Xu
Haorui Luo
Jiahao Wang
Haifeng Liu
Luonan Chen
Hongbin Ji
Zimu Deng
Xiaolong Liu
author_sort Yu Xu
collection DOAJ
description Abstract The nexus between aging‐associated immune deteriorations and tumorigenesis of lung cancers remains elusive. In a mouse model with Med23 depletion in T cells (Med23 −/−), it is found a strong association between the decline of CD103+ T cells and spontaneous alveolar epithelial type II cell (AT2 cell)‐originated lung adenocarcinomas. The reduction of CD103+ T cells in the lung results in an accumulation of AT2 cells bearing oxidative damages, which appears to be the major origin of the lung adenocarcinoma. Functional experiments reveal CD103+ T cells can eradicate oxidative‐damage‐bearing AT2 cells as well as ROS‐dependent, KRAS (G12D)‐driven tumorigenesis. In vitro co‐cultures prove CD103+ T cells, especially CD103+ CD8+ T cells, exhibit a killing capacity that matches the oxidative stress level in the target cells. In aged animals, it is found the abundance of CD103+ CD8+ T cells in the lung declines with age, accompanied by an accumulation of oxidative‐damage‐bearing AT2 cells. Collectively, the study establishes the vital function of CD103+ T cells in surveilling epithelial cells under oxidative stress to prevent malignancies, and unravels a potential immuno‐dysregulation in the aged lung which contributes to tumorigenesis.
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publishDate 2025-07-01
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spelling doaj-art-96a7fafd6f44487a8ce8f1b39940d54f2025-08-20T03:15:29ZengWileyAdvanced Science2198-38442025-07-011228n/an/a10.1002/advs.202503557CD103+ T Cells Eliminate Damaged Alveolar Epithelial Type II Cells Under Oxidative Stress to Prevent Lung TumorigenesisYu Xu0Haorui Luo1Jiahao Wang2Haifeng Liu3Luonan Chen4Hongbin Ji5Zimu Deng6Xiaolong Liu7Key Laboratory of Multicellular Systems CAS Center for Excellence in Molecular Cell Science Shanghai Institute of Biochemistry and Cell Biology University of Chinese Academy of Sciences Chinese Academy of Sciences 320 Yueyang Road Shanghai 200031 ChinaKey Laboratory of Multicellular Systems CAS Center for Excellence in Molecular Cell Science Shanghai Institute of Biochemistry and Cell Biology University of Chinese Academy of Sciences Chinese Academy of Sciences 320 Yueyang Road Shanghai 200031 ChinaKey Laboratory of Multicellular Systems CAS Center for Excellence in Molecular Cell Science Shanghai Institute of Biochemistry and Cell Biology University of Chinese Academy of Sciences Chinese Academy of Sciences 320 Yueyang Road Shanghai 200031 ChinaKey Laboratory of Multicellular Systems CAS Center for Excellence in Molecular Cell Science Shanghai Institute of Biochemistry and Cell Biology University of Chinese Academy of Sciences Chinese Academy of Sciences 320 Yueyang Road Shanghai 200031 ChinaKey Laboratory of Multicellular Systems CAS Center for Excellence in Molecular Cell Science Shanghai Institute of Biochemistry and Cell Biology University of Chinese Academy of Sciences Chinese Academy of Sciences 320 Yueyang Road Shanghai 200031 ChinaKey Laboratory of Multicellular Systems CAS Center for Excellence in Molecular Cell Science Shanghai Institute of Biochemistry and Cell Biology University of Chinese Academy of Sciences Chinese Academy of Sciences 320 Yueyang Road Shanghai 200031 ChinaKey Laboratory of Multicellular Systems CAS Center for Excellence in Molecular Cell Science Shanghai Institute of Biochemistry and Cell Biology University of Chinese Academy of Sciences Chinese Academy of Sciences 320 Yueyang Road Shanghai 200031 ChinaKey Laboratory of Multicellular Systems CAS Center for Excellence in Molecular Cell Science Shanghai Institute of Biochemistry and Cell Biology University of Chinese Academy of Sciences Chinese Academy of Sciences 320 Yueyang Road Shanghai 200031 ChinaAbstract The nexus between aging‐associated immune deteriorations and tumorigenesis of lung cancers remains elusive. In a mouse model with Med23 depletion in T cells (Med23 −/−), it is found a strong association between the decline of CD103+ T cells and spontaneous alveolar epithelial type II cell (AT2 cell)‐originated lung adenocarcinomas. The reduction of CD103+ T cells in the lung results in an accumulation of AT2 cells bearing oxidative damages, which appears to be the major origin of the lung adenocarcinoma. Functional experiments reveal CD103+ T cells can eradicate oxidative‐damage‐bearing AT2 cells as well as ROS‐dependent, KRAS (G12D)‐driven tumorigenesis. In vitro co‐cultures prove CD103+ T cells, especially CD103+ CD8+ T cells, exhibit a killing capacity that matches the oxidative stress level in the target cells. In aged animals, it is found the abundance of CD103+ CD8+ T cells in the lung declines with age, accompanied by an accumulation of oxidative‐damage‐bearing AT2 cells. Collectively, the study establishes the vital function of CD103+ T cells in surveilling epithelial cells under oxidative stress to prevent malignancies, and unravels a potential immuno‐dysregulation in the aged lung which contributes to tumorigenesis.https://doi.org/10.1002/advs.202503557AT2 cellCD103+ T celllung adenocarcinomaMED23oxidative stresstumorigenesis
spellingShingle Yu Xu
Haorui Luo
Jiahao Wang
Haifeng Liu
Luonan Chen
Hongbin Ji
Zimu Deng
Xiaolong Liu
CD103+ T Cells Eliminate Damaged Alveolar Epithelial Type II Cells Under Oxidative Stress to Prevent Lung Tumorigenesis
Advanced Science
AT2 cell
CD103+ T cell
lung adenocarcinoma
MED23
oxidative stress
tumorigenesis
title CD103+ T Cells Eliminate Damaged Alveolar Epithelial Type II Cells Under Oxidative Stress to Prevent Lung Tumorigenesis
title_full CD103+ T Cells Eliminate Damaged Alveolar Epithelial Type II Cells Under Oxidative Stress to Prevent Lung Tumorigenesis
title_fullStr CD103+ T Cells Eliminate Damaged Alveolar Epithelial Type II Cells Under Oxidative Stress to Prevent Lung Tumorigenesis
title_full_unstemmed CD103+ T Cells Eliminate Damaged Alveolar Epithelial Type II Cells Under Oxidative Stress to Prevent Lung Tumorigenesis
title_short CD103+ T Cells Eliminate Damaged Alveolar Epithelial Type II Cells Under Oxidative Stress to Prevent Lung Tumorigenesis
title_sort cd103 t cells eliminate damaged alveolar epithelial type ii cells under oxidative stress to prevent lung tumorigenesis
topic AT2 cell
CD103+ T cell
lung adenocarcinoma
MED23
oxidative stress
tumorigenesis
url https://doi.org/10.1002/advs.202503557
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