Elevated nitric oxide during colitis restrains GM-CSF production in ILC3 cells via suppressing an AhR-Cyp4f13-NF-κB axis

Abstract Inflammatory bowel disease (IBD) presents a significant clinical challenge, yet the way bioactive gases are implicated remains elusive. We detect elevated colonic Nos2 levels in both IBD patients and mice undergoing diverse colitis. Additionally, Nos2 deficiency significantly aggravates ant...

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Main Authors: Xingyu Zhao, Jun Li, Yime Zhang, Luni Hu, Di Wu, Jiayu Wu, Ruiqing Lyu, Peng Li, Gao An, Rongli Cui, Tao Sun, Pingping Zhu, Lin Bai, Changtao Jiang, Chao Zhong
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-60969-x
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author Xingyu Zhao
Jun Li
Yime Zhang
Luni Hu
Di Wu
Jiayu Wu
Ruiqing Lyu
Peng Li
Gao An
Rongli Cui
Tao Sun
Pingping Zhu
Lin Bai
Changtao Jiang
Chao Zhong
author_facet Xingyu Zhao
Jun Li
Yime Zhang
Luni Hu
Di Wu
Jiayu Wu
Ruiqing Lyu
Peng Li
Gao An
Rongli Cui
Tao Sun
Pingping Zhu
Lin Bai
Changtao Jiang
Chao Zhong
author_sort Xingyu Zhao
collection DOAJ
description Abstract Inflammatory bowel disease (IBD) presents a significant clinical challenge, yet the way bioactive gases are implicated remains elusive. We detect elevated colonic Nos2 levels in both IBD patients and mice undergoing diverse colitis. Additionally, Nos2 deficiency significantly aggravates anti-CD40-induced colitis, along with an increase in GM-CSF production by ILC3s. We identified a previously unappreciated role of the crucial ILC3 regulator, AhR, in promoting Cyp4f13 expression to allow ILC3s to bind with externally derived nitric oxide (NO). This further restrains Cyp4f13-catalyzed ROS generation and thereby diminishes NF-κB activation strictly necessary for GM-CSF production. Accordingly, the exacerbated anti-CD40-induced colitis due to defective NO generation in Nos2 deficient mice is efficiently recovered by a Cyp4f13 inhibitor, HET0016. Importantly, IBD patients with elevated NO binding to colonic ILC3s show decreased disease activity. Thus, our findings uncover a crucial regulatory mechanism for restraining colitogenic GM-CSF production in ILC3s and underscores its implication in IBD therapy.
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spelling doaj-art-9b66d387f3584dda8d12dbca03110d362025-08-20T03:37:37ZengNature PortfolioNature Communications2041-17232025-07-0116111810.1038/s41467-025-60969-xElevated nitric oxide during colitis restrains GM-CSF production in ILC3 cells via suppressing an AhR-Cyp4f13-NF-κB axisXingyu Zhao0Jun Li1Yime Zhang2Luni Hu3Di Wu4Jiayu Wu5Ruiqing Lyu6Peng Li7Gao An8Rongli Cui9Tao Sun10Pingping Zhu11Lin Bai12Changtao Jiang13Chao Zhong14Department of Immunology, School of Basic Medical Sciences, NHC Key Laboratory of Medical Immunology, Medicine Innovation Center for Fundamental Researches on Major Immunology-Related Diseases, Peking UniversityDepartment of Gastroenterology, Peking University Third HospitalDepartment of Immunology, School of Basic Medical Sciences, NHC Key Laboratory of Medical Immunology, Medicine Innovation Center for Fundamental Researches on Major Immunology-Related Diseases, Peking UniversityInstitute of Systems Biomedicine, Beijing Key Laboratory of Tumor Systems Biology, Peking University Health Science CenterInstitute of Systems Biomedicine, Beijing Key Laboratory of Tumor Systems Biology, Peking University Health Science CenterDepartment of Immunology, School of Basic Medical Sciences, NHC Key Laboratory of Medical Immunology, Medicine Innovation Center for Fundamental Researches on Major Immunology-Related Diseases, Peking UniversityDepartment of Biophysics, School of Basic Medical Sciences, Peking UniversityDepartment of Immunology, School of Basic Medical Sciences, NHC Key Laboratory of Medical Immunology, Medicine Innovation Center for Fundamental Researches on Major Immunology-Related Diseases, Peking UniversityInstitute of Systems Biomedicine, Beijing Key Laboratory of Tumor Systems Biology, Peking University Health Science CenterDepartment of Gastroenterology, Peking University Third HospitalGeneral Surgery Department, Peking University Third HospitalSchool of Life Sciences, Zhengzhou UniversityDepartment of Biophysics, School of Basic Medical Sciences, Peking UniversityDepartment of Immunology, School of Basic Medical Sciences, NHC Key Laboratory of Medical Immunology, Medicine Innovation Center for Fundamental Researches on Major Immunology-Related Diseases, Peking UniversityDepartment of Immunology, School of Basic Medical Sciences, NHC Key Laboratory of Medical Immunology, Medicine Innovation Center for Fundamental Researches on Major Immunology-Related Diseases, Peking UniversityAbstract Inflammatory bowel disease (IBD) presents a significant clinical challenge, yet the way bioactive gases are implicated remains elusive. We detect elevated colonic Nos2 levels in both IBD patients and mice undergoing diverse colitis. Additionally, Nos2 deficiency significantly aggravates anti-CD40-induced colitis, along with an increase in GM-CSF production by ILC3s. We identified a previously unappreciated role of the crucial ILC3 regulator, AhR, in promoting Cyp4f13 expression to allow ILC3s to bind with externally derived nitric oxide (NO). This further restrains Cyp4f13-catalyzed ROS generation and thereby diminishes NF-κB activation strictly necessary for GM-CSF production. Accordingly, the exacerbated anti-CD40-induced colitis due to defective NO generation in Nos2 deficient mice is efficiently recovered by a Cyp4f13 inhibitor, HET0016. Importantly, IBD patients with elevated NO binding to colonic ILC3s show decreased disease activity. Thus, our findings uncover a crucial regulatory mechanism for restraining colitogenic GM-CSF production in ILC3s and underscores its implication in IBD therapy.https://doi.org/10.1038/s41467-025-60969-x
spellingShingle Xingyu Zhao
Jun Li
Yime Zhang
Luni Hu
Di Wu
Jiayu Wu
Ruiqing Lyu
Peng Li
Gao An
Rongli Cui
Tao Sun
Pingping Zhu
Lin Bai
Changtao Jiang
Chao Zhong
Elevated nitric oxide during colitis restrains GM-CSF production in ILC3 cells via suppressing an AhR-Cyp4f13-NF-κB axis
Nature Communications
title Elevated nitric oxide during colitis restrains GM-CSF production in ILC3 cells via suppressing an AhR-Cyp4f13-NF-κB axis
title_full Elevated nitric oxide during colitis restrains GM-CSF production in ILC3 cells via suppressing an AhR-Cyp4f13-NF-κB axis
title_fullStr Elevated nitric oxide during colitis restrains GM-CSF production in ILC3 cells via suppressing an AhR-Cyp4f13-NF-κB axis
title_full_unstemmed Elevated nitric oxide during colitis restrains GM-CSF production in ILC3 cells via suppressing an AhR-Cyp4f13-NF-κB axis
title_short Elevated nitric oxide during colitis restrains GM-CSF production in ILC3 cells via suppressing an AhR-Cyp4f13-NF-κB axis
title_sort elevated nitric oxide during colitis restrains gm csf production in ilc3 cells via suppressing an ahr cyp4f13 nf κb axis
url https://doi.org/10.1038/s41467-025-60969-x
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