DNA probe pulldown screening uncovers O-GlcNAcylation modulation of transcription factor DNA interactions

Abstract O-linked β-N-acetylglucosamine (O-GlcNAc), a critical post-translational modification predominantly found in the nucleus, plays a substantial role in regulating gene expression by modulating transcription factors (TFs) activity. However, quantitative analysis investigating the influence of...

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Main Authors: Guofang Li, Fanxu Meng, Xiaomin Zhong, Kairan Yu, Nana Zhang, Keren Zhang, Huang Huang, Wenli Li, Jianing Zhang, Wei Wang, Yan Ren, Yubo Liu
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-025-07074-7
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author Guofang Li
Fanxu Meng
Xiaomin Zhong
Kairan Yu
Nana Zhang
Keren Zhang
Huang Huang
Wenli Li
Jianing Zhang
Wei Wang
Yan Ren
Yubo Liu
author_facet Guofang Li
Fanxu Meng
Xiaomin Zhong
Kairan Yu
Nana Zhang
Keren Zhang
Huang Huang
Wenli Li
Jianing Zhang
Wei Wang
Yan Ren
Yubo Liu
author_sort Guofang Li
collection DOAJ
description Abstract O-linked β-N-acetylglucosamine (O-GlcNAc), a critical post-translational modification predominantly found in the nucleus, plays a substantial role in regulating gene expression by modulating transcription factors (TFs) activity. However, quantitative analysis investigating the influence of O-GlcNAcylation on protein-DNA interactions at a proteome scale remains undone. Herein, a pulldown screening approach using a consensus TF response element (catTFRE) was employed to unravel the impact of fluctuating levels of O-GlcNAcylation on the DNA binding efficiency of endogenous TFs/co-factors. Utilizing quantitative proteomics, we identified a substantial enhancement in the binding capacity of 241 nuclear proteins (NPs) to DNA sequences due to elevated levels of O-GlcNAcylation, whereas a decrease in DNA binding was observed for 2 NPs concurrently. Intriguingly, the O-GlcNAcylation elevation significantly enhanced the binding of 146 TFs/co-factors to specific DNA sequences. We further established that the O-GlcNAcylation of several Forkhead family TFs, including FOXA1 and FOXC1, notably enhances their binding to specific DNA sequences in living cells. Our research presents an efficacious approach to assessing the impact of O-GlcNAcylation on the interactions between proteins and DNA. This significantly enhances our understanding of the role O-GlcNAcylation plays in the regulation of transcription.
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spelling doaj-art-344d5e074e84486f85034a77b8650bb62025-08-20T03:37:20ZengNature PortfolioScientific Reports2045-23222025-07-0115111510.1038/s41598-025-07074-7DNA probe pulldown screening uncovers O-GlcNAcylation modulation of transcription factor DNA interactionsGuofang Li0Fanxu Meng1Xiaomin Zhong2Kairan Yu3Nana Zhang4Keren Zhang5Huang Huang6Wenli Li7Jianing Zhang8Wei Wang9Yan Ren10Yubo Liu11Cancer Hospital of Dalian University of Technology, Liaoning Cancer Hospital & InstituteCancer Hospital of Dalian University of Technology, Liaoning Cancer Hospital & InstituteDepartment of Oncology, The Affiliated Huaian No.1 People’s Hospital of Nanjing Medical UniversityCancer Hospital of Dalian University of Technology, Liaoning Cancer Hospital & InstituteDepartment of Life and Pharmaceutical Sciences, Dalian University of TechnologyDepartment of Chemistry, College of Science, Southern University of Science and TechnologyDepartment of Life and Pharmaceutical Sciences, Dalian University of TechnologyDepartment of Life and Pharmaceutical Sciences, Dalian University of TechnologyDepartment of Life and Pharmaceutical Sciences, Dalian University of TechnologyDepartment of Thoracic Surgery, Liaoning Cancer Hospital & Institute, Cancer Hospital of Dalian University of TechnologyExperiment Center for Science and Technology, Shanghai University of Traditional Chinese MedicineCancer Hospital of Dalian University of Technology, Liaoning Cancer Hospital & InstituteAbstract O-linked β-N-acetylglucosamine (O-GlcNAc), a critical post-translational modification predominantly found in the nucleus, plays a substantial role in regulating gene expression by modulating transcription factors (TFs) activity. However, quantitative analysis investigating the influence of O-GlcNAcylation on protein-DNA interactions at a proteome scale remains undone. Herein, a pulldown screening approach using a consensus TF response element (catTFRE) was employed to unravel the impact of fluctuating levels of O-GlcNAcylation on the DNA binding efficiency of endogenous TFs/co-factors. Utilizing quantitative proteomics, we identified a substantial enhancement in the binding capacity of 241 nuclear proteins (NPs) to DNA sequences due to elevated levels of O-GlcNAcylation, whereas a decrease in DNA binding was observed for 2 NPs concurrently. Intriguingly, the O-GlcNAcylation elevation significantly enhanced the binding of 146 TFs/co-factors to specific DNA sequences. We further established that the O-GlcNAcylation of several Forkhead family TFs, including FOXA1 and FOXC1, notably enhances their binding to specific DNA sequences in living cells. Our research presents an efficacious approach to assessing the impact of O-GlcNAcylation on the interactions between proteins and DNA. This significantly enhances our understanding of the role O-GlcNAcylation plays in the regulation of transcription.https://doi.org/10.1038/s41598-025-07074-7
spellingShingle Guofang Li
Fanxu Meng
Xiaomin Zhong
Kairan Yu
Nana Zhang
Keren Zhang
Huang Huang
Wenli Li
Jianing Zhang
Wei Wang
Yan Ren
Yubo Liu
DNA probe pulldown screening uncovers O-GlcNAcylation modulation of transcription factor DNA interactions
Scientific Reports
title DNA probe pulldown screening uncovers O-GlcNAcylation modulation of transcription factor DNA interactions
title_full DNA probe pulldown screening uncovers O-GlcNAcylation modulation of transcription factor DNA interactions
title_fullStr DNA probe pulldown screening uncovers O-GlcNAcylation modulation of transcription factor DNA interactions
title_full_unstemmed DNA probe pulldown screening uncovers O-GlcNAcylation modulation of transcription factor DNA interactions
title_short DNA probe pulldown screening uncovers O-GlcNAcylation modulation of transcription factor DNA interactions
title_sort dna probe pulldown screening uncovers o glcnacylation modulation of transcription factor dna interactions
url https://doi.org/10.1038/s41598-025-07074-7
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