Phosphorylation of FOXN3 by NEK6 promotes pulmonary fibrosis through Smad signaling

Abstract The transcriptional repressor FOXN3 plays a key role in regulating pulmonary inflammatory responses, which are crucial in the development of pulmonary fibrosis. However, its specific regulatory function in lung fibrosis remains unclear. Here, we show that FOXN3 suppresses pulmonary fibrosis...

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Main Authors: Jinjin Yu, Yingke Li, Yiming Li, Xiaotian Liu, Qingyang Huo, Nan Wu, Yangxia Zhang, Taoling Zeng, Yong Zhang, Henry You Li, Jie Lian, Jihong Zhou, Emmanuel Jairaj Moses, Jian Geng, Juntang Lin, Wei Li, Xinxing Zhu
Format: Article
Language:English
Published: Nature Portfolio 2025-02-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-56922-7
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author Jinjin Yu
Yingke Li
Yiming Li
Xiaotian Liu
Qingyang Huo
Nan Wu
Yangxia Zhang
Taoling Zeng
Yong Zhang
Henry You Li
Jie Lian
Jihong Zhou
Emmanuel Jairaj Moses
Jian Geng
Juntang Lin
Wei Li
Xinxing Zhu
author_facet Jinjin Yu
Yingke Li
Yiming Li
Xiaotian Liu
Qingyang Huo
Nan Wu
Yangxia Zhang
Taoling Zeng
Yong Zhang
Henry You Li
Jie Lian
Jihong Zhou
Emmanuel Jairaj Moses
Jian Geng
Juntang Lin
Wei Li
Xinxing Zhu
author_sort Jinjin Yu
collection DOAJ
description Abstract The transcriptional repressor FOXN3 plays a key role in regulating pulmonary inflammatory responses, which are crucial in the development of pulmonary fibrosis. However, its specific regulatory function in lung fibrosis remains unclear. Here, we show that FOXN3 suppresses pulmonary fibrosis by inhibiting Smad transcriptional activity. FOXN3 targets a substantial number of Smad response gene promoters, facilitating Smad4 ubiquitination, which disrupts the association of the Smad2/3/4 complex with chromatin and abolishes its transcriptional response. In response to pro-fibrotic stimuli, NEK6 phosphorylates FOXN3 at S412 and S416, leading to its degradation. The loss of FOXN3 inhibits β-TrCP-mediated ubiquitination of Smad4, stabilizing the Smad complex’s association with its responsive elements and promoting transcriptional activation, thus contributing to the development of pulmonary fibrosis. Notably, we found a significant inverse expression pattern between FOXN3 and Smad4 in clinical pulmonary fibrosis cases, underscoring the importance of the NEK6-FOXN3-Smad axis in the pathological process of pulmonary fibrosis.
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spelling doaj-art-c79fa6fcbd4542f78c38d40e98d4fb412025-08-20T03:10:52ZengNature PortfolioNature Communications2041-17232025-02-0116111910.1038/s41467-025-56922-7Phosphorylation of FOXN3 by NEK6 promotes pulmonary fibrosis through Smad signalingJinjin Yu0Yingke Li1Yiming Li2Xiaotian Liu3Qingyang Huo4Nan Wu5Yangxia Zhang6Taoling Zeng7Yong Zhang8Henry You Li9Jie Lian10Jihong Zhou11Emmanuel Jairaj Moses12Jian Geng13Juntang Lin14Wei Li15Xinxing Zhu16Anhui Province Key Laboratory of Respiratory Tumor and Infectious Disease, Department of Respiratory and Critical Care Medicine, First Affiliated Hospital, Bengbu Medical UniversityHenan Joint International Research Laboratory of Stem Cell Medicine, School of Medical Engineering, Xinxiang Medical UniversityResearch Center of Clinical Laboratory Science, School of Laboratory Medicine, Bengbu Medical UniversityResearch Center of Clinical Laboratory Science, School of Laboratory Medicine, Bengbu Medical UniversityHenan Joint International Research Laboratory of Stem Cell Medicine, School of Medical Engineering, Xinxiang Medical UniversityMolecular Diagnosis Center, First Affiliated Hospital, Bengbu Medical UniversityHenan Joint International Research Laboratory of Stem Cell Medicine, School of Medical Engineering, Xinxiang Medical UniversityState Key Laboratory of Cellular Stress Biology, Innovation Center for Cell Biology, School of Life Sciences, Xiamen UniversityAnhui Province Key Laboratory of Respiratory Tumor and Infectious Disease, Department of Respiratory and Critical Care Medicine, First Affiliated Hospital, Bengbu Medical UniversityBiomolecular Interaction Centre, University of CanterburyHenan Joint International Research Laboratory of Stem Cell Medicine, School of Medical Engineering, Xinxiang Medical UniversityResearch Center of Clinical Laboratory Science, School of Laboratory Medicine, Bengbu Medical UniversityRegenerative Medicine Sciences Cluster, Advanced Medical and Dental Institute, Universiti Sains MalaysiaResearch Center of Clinical Laboratory Science, School of Laboratory Medicine, Bengbu Medical UniversityHenan Joint International Research Laboratory of Stem Cell Medicine, School of Medical Engineering, Xinxiang Medical UniversityAnhui Province Key Laboratory of Respiratory Tumor and Infectious Disease, Department of Respiratory and Critical Care Medicine, First Affiliated Hospital, Bengbu Medical UniversityAnhui Province Key Laboratory of Respiratory Tumor and Infectious Disease, Department of Respiratory and Critical Care Medicine, First Affiliated Hospital, Bengbu Medical UniversityAbstract The transcriptional repressor FOXN3 plays a key role in regulating pulmonary inflammatory responses, which are crucial in the development of pulmonary fibrosis. However, its specific regulatory function in lung fibrosis remains unclear. Here, we show that FOXN3 suppresses pulmonary fibrosis by inhibiting Smad transcriptional activity. FOXN3 targets a substantial number of Smad response gene promoters, facilitating Smad4 ubiquitination, which disrupts the association of the Smad2/3/4 complex with chromatin and abolishes its transcriptional response. In response to pro-fibrotic stimuli, NEK6 phosphorylates FOXN3 at S412 and S416, leading to its degradation. The loss of FOXN3 inhibits β-TrCP-mediated ubiquitination of Smad4, stabilizing the Smad complex’s association with its responsive elements and promoting transcriptional activation, thus contributing to the development of pulmonary fibrosis. Notably, we found a significant inverse expression pattern between FOXN3 and Smad4 in clinical pulmonary fibrosis cases, underscoring the importance of the NEK6-FOXN3-Smad axis in the pathological process of pulmonary fibrosis.https://doi.org/10.1038/s41467-025-56922-7
spellingShingle Jinjin Yu
Yingke Li
Yiming Li
Xiaotian Liu
Qingyang Huo
Nan Wu
Yangxia Zhang
Taoling Zeng
Yong Zhang
Henry You Li
Jie Lian
Jihong Zhou
Emmanuel Jairaj Moses
Jian Geng
Juntang Lin
Wei Li
Xinxing Zhu
Phosphorylation of FOXN3 by NEK6 promotes pulmonary fibrosis through Smad signaling
Nature Communications
title Phosphorylation of FOXN3 by NEK6 promotes pulmonary fibrosis through Smad signaling
title_full Phosphorylation of FOXN3 by NEK6 promotes pulmonary fibrosis through Smad signaling
title_fullStr Phosphorylation of FOXN3 by NEK6 promotes pulmonary fibrosis through Smad signaling
title_full_unstemmed Phosphorylation of FOXN3 by NEK6 promotes pulmonary fibrosis through Smad signaling
title_short Phosphorylation of FOXN3 by NEK6 promotes pulmonary fibrosis through Smad signaling
title_sort phosphorylation of foxn3 by nek6 promotes pulmonary fibrosis through smad signaling
url https://doi.org/10.1038/s41467-025-56922-7
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