Histone methyltransferase KMT2A promotes pulmonary fibrogenesis via targeting pro‐fibrotic factor PU.1 in fibroblasts

Abstract Background Idiopathic pulmonary fibrosis (IPF) is a fibrotic disease driven by both environmental and genetic factors. Epigenetics refers to changes in gene expression or cellular phenotype that do not involve alterations to DNA sequence. KMT2A is a member of the SET family which catalyses...

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Main Authors: Wenting Lyu, Hui Wang, Tong Ji, Ling Liu, Haoran Chen, Li Fan, Guanning Zhong, Naihui Wan, Suwan Chen, Jingyu Chen, Hourong Cai, Hongyang Xu, Dongjin Wang, Jinghong Dai
Format: Article
Language:English
Published: Wiley 2025-02-01
Series:Clinical and Translational Medicine
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Online Access:https://doi.org/10.1002/ctm2.70217
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author Wenting Lyu
Hui Wang
Tong Ji
Ling Liu
Haoran Chen
Li Fan
Guanning Zhong
Naihui Wan
Suwan Chen
Jingyu Chen
Hourong Cai
Hongyang Xu
Dongjin Wang
Jinghong Dai
author_facet Wenting Lyu
Hui Wang
Tong Ji
Ling Liu
Haoran Chen
Li Fan
Guanning Zhong
Naihui Wan
Suwan Chen
Jingyu Chen
Hourong Cai
Hongyang Xu
Dongjin Wang
Jinghong Dai
author_sort Wenting Lyu
collection DOAJ
description Abstract Background Idiopathic pulmonary fibrosis (IPF) is a fibrotic disease driven by both environmental and genetic factors. Epigenetics refers to changes in gene expression or cellular phenotype that do not involve alterations to DNA sequence. KMT2A is a member of the SET family which catalyses H3K4 methylation. Results Through microarray and single‐cell sequencing data, we discovered KMT2A‐positive fibroblasts were increased in IPF lung tissues. KMT2A level was increased in IPF and bleomycin‐induced pulmonary fibrosis mice lung tissues collected in our centre. Mice with AAV6‐induced KMT2A knockdown in fibroblast showed attenuated pulmonary fibrosis after bleomycin treatment. Bioinformation also revealed that transcription factor PU.1 was a target of KMT2A. We demonstrated that PU.1 levels were increased in IPF tissues, bleomycin‐induced mice lung tissues and primary fibrotic fibroblasts. KMT2A knockdown decreases PU.1 expression in vitro while KMT2A overexpression induces PU.1 activation. PU.1 fibroblast‐specific knockout mice showed attenuated lung fibrosis induced by bleomycin. Furthermore, we demonstrated KMT2A up‐regulated PU.1 in fibroblasts by catalysing H3K4me3 at the promoter of the PU.1 gene. The KMT2A transcription complex inhibitor mm102 treatment attenuated bleomycin‐induced pulmonary fibrosis. Conclusion The current study indicated that histone modification participates in the pathogenesis of IPF and KMT2A may have the potential to be a therapeutic target of IPF treatment. Key points KMT2A plays a role in pulmonary fibrogenesis. KMT2A regulates PU.1 transcription in fibroblasts through H3K4me3 at promoter. KMT2A inhibitor attenuates pulmonary fibrosis in mice.
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spelling doaj-art-e678422d31c044b09bb45b04599b72812025-08-20T02:09:37ZengWileyClinical and Translational Medicine2001-13262025-02-01152n/an/a10.1002/ctm2.70217Histone methyltransferase KMT2A promotes pulmonary fibrogenesis via targeting pro‐fibrotic factor PU.1 in fibroblastsWenting Lyu0Hui Wang1Tong Ji2Ling Liu3Haoran Chen4Li Fan5Guanning Zhong6Naihui Wan7Suwan Chen8Jingyu Chen9Hourong Cai10Hongyang Xu11Dongjin Wang12Jinghong Dai13Department of Pulmonary and Critical Care Medicine The Affiliated Drum Tower Hospital of Nanjing University Medical School Nanjing Jiangsu ChinaDepartment of Respiratory and Critical Care Medicine Shanghai Pulmonary Hospital School of Medicine Tongji University Shanghai ChinaDepartment of Pulmonary and Critical Care Medicine The Affiliated Drum Tower Hospital of Nanjing University Medical School Nanjing Jiangsu ChinaDepartment of Pulmonary and Critical Care Medicine The Affiliated Drum Tower Hospital of Nanjing University Medical School Nanjing Jiangsu ChinaDepartment of Pulmonary and Critical Care Medicine The Second Affiliated Hospital of Soochow University Suzhou ChinaDepartment of Respiratory and Critical Care Medicine The Second People's Hospital of Yibin Yibin Sichuan ChinaDepartment of Pulmonary and Critical Care Medicine The Affiliated Drum Tower Hospital of Nanjing University Medical School Nanjing Jiangsu ChinaDepartment of Pulmonary and Critical Care Medicine The Affiliated Drum Tower Hospital of Nanjing University Medical School Nanjing Jiangsu ChinaDepartment of Pulmonary and Critical Care Medicine The Affiliated Drum Tower Hospital of Nanjing University Medical School Nanjing Jiangsu ChinaDepartment of Critical Care Medicine The Affiliated Wuxi People's Hospital of Nanjing Medical University Wuxi People's Hospital Wuxi Medical Center Nanjing Medical University Nanjing ChinaDepartment of Pulmonary and Critical Care Medicine The Affiliated Drum Tower Hospital of Nanjing University Medical School Nanjing Jiangsu ChinaDepartment of Critical Care Medicine The Affiliated Wuxi People's Hospital of Nanjing Medical University Wuxi People's Hospital Wuxi Medical Center Nanjing Medical University Nanjing ChinaDepartment of Cardiothoracic Surgery The Affiliated Drum Tower Hospital of Nanjing University Medical School Nanjing Jiangsu ChinaDepartment of Pulmonary and Critical Care Medicine The Affiliated Drum Tower Hospital of Nanjing University Medical School Nanjing Jiangsu ChinaAbstract Background Idiopathic pulmonary fibrosis (IPF) is a fibrotic disease driven by both environmental and genetic factors. Epigenetics refers to changes in gene expression or cellular phenotype that do not involve alterations to DNA sequence. KMT2A is a member of the SET family which catalyses H3K4 methylation. Results Through microarray and single‐cell sequencing data, we discovered KMT2A‐positive fibroblasts were increased in IPF lung tissues. KMT2A level was increased in IPF and bleomycin‐induced pulmonary fibrosis mice lung tissues collected in our centre. Mice with AAV6‐induced KMT2A knockdown in fibroblast showed attenuated pulmonary fibrosis after bleomycin treatment. Bioinformation also revealed that transcription factor PU.1 was a target of KMT2A. We demonstrated that PU.1 levels were increased in IPF tissues, bleomycin‐induced mice lung tissues and primary fibrotic fibroblasts. KMT2A knockdown decreases PU.1 expression in vitro while KMT2A overexpression induces PU.1 activation. PU.1 fibroblast‐specific knockout mice showed attenuated lung fibrosis induced by bleomycin. Furthermore, we demonstrated KMT2A up‐regulated PU.1 in fibroblasts by catalysing H3K4me3 at the promoter of the PU.1 gene. The KMT2A transcription complex inhibitor mm102 treatment attenuated bleomycin‐induced pulmonary fibrosis. Conclusion The current study indicated that histone modification participates in the pathogenesis of IPF and KMT2A may have the potential to be a therapeutic target of IPF treatment. Key points KMT2A plays a role in pulmonary fibrogenesis. KMT2A regulates PU.1 transcription in fibroblasts through H3K4me3 at promoter. KMT2A inhibitor attenuates pulmonary fibrosis in mice.https://doi.org/10.1002/ctm2.70217epigeneticsfibroblasthistone methylationidiopathic pulmonary fibrosis
spellingShingle Wenting Lyu
Hui Wang
Tong Ji
Ling Liu
Haoran Chen
Li Fan
Guanning Zhong
Naihui Wan
Suwan Chen
Jingyu Chen
Hourong Cai
Hongyang Xu
Dongjin Wang
Jinghong Dai
Histone methyltransferase KMT2A promotes pulmonary fibrogenesis via targeting pro‐fibrotic factor PU.1 in fibroblasts
Clinical and Translational Medicine
epigenetics
fibroblast
histone methylation
idiopathic pulmonary fibrosis
title Histone methyltransferase KMT2A promotes pulmonary fibrogenesis via targeting pro‐fibrotic factor PU.1 in fibroblasts
title_full Histone methyltransferase KMT2A promotes pulmonary fibrogenesis via targeting pro‐fibrotic factor PU.1 in fibroblasts
title_fullStr Histone methyltransferase KMT2A promotes pulmonary fibrogenesis via targeting pro‐fibrotic factor PU.1 in fibroblasts
title_full_unstemmed Histone methyltransferase KMT2A promotes pulmonary fibrogenesis via targeting pro‐fibrotic factor PU.1 in fibroblasts
title_short Histone methyltransferase KMT2A promotes pulmonary fibrogenesis via targeting pro‐fibrotic factor PU.1 in fibroblasts
title_sort histone methyltransferase kmt2a promotes pulmonary fibrogenesis via targeting pro fibrotic factor pu 1 in fibroblasts
topic epigenetics
fibroblast
histone methylation
idiopathic pulmonary fibrosis
url https://doi.org/10.1002/ctm2.70217
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