IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-47048-3.html
   My bibliography  Save this article

The PTM profiling of CTCF reveals the regulation of 3D chromatin structure by O-GlcNAcylation

Author

Listed:
  • Xiuxiao Tang

    (Sun Yat-Sen University
    Sun Yat-Sen University
    Sun Yat-Sen University
    Sun Yat-Sen University)

  • Pengguihang Zeng

    (Sun Yat-Sen University
    Sun Yat-Sen University
    Sun Yat-Sen University
    Sun Yat-Sen University)

  • Kezhi Liu

    (Sun Yat-Sen University
    Sun Yat-Sen University
    Sun Yat-Sen University
    Sun Yat-Sen University)

  • Li Qing

    (Sun Yat-Sen University
    Sun Yat-Sen University
    Sun Yat-Sen University
    Sun Yat-Sen University)

  • Yifei Sun

    (Sun Yat-Sen University
    Sun Yat-Sen University
    Sun Yat-Sen University
    Sun Yat-Sen University)

  • Xinyi Liu

    (Sun Yat-Sen University
    Sun Yat-Sen University
    Sun Yat-Sen University
    Sun Yat-Sen University)

  • Lizi Lu

    (Sun Yat-Sen University
    Sun Yat-Sen University
    Sun Yat-Sen University
    Sun Yat-Sen University)

  • Chao Wei

    (Sun Yat-Sen University
    Sun Yat-Sen University
    Sun Yat-Sen University
    Sun Yat-Sen University)

  • Jia Wang

    (Guangzhou Medical University)

  • Shaoshuai Jiang

    (Sun Yat-Sen University
    Sun Yat-Sen University
    Sun Yat-Sen University
    Sun Yat-Sen University)

  • Jun Sun

    (Sichuan University
    Sichuan University)

  • Wakam Chang

    (University of Macau)

  • Haopeng Yu

    (Sichuan University
    Sichuan University)

  • Hebing Chen

    (Institute of Health Service and Transfusion Medicine)

  • Jiaguo Zhou

    (Sun Yat-Sen University)

  • Chengfang Xu

    (The obstetric and gynecology Department of The third affiliated hospital of Sun Yat-Sen University)

  • Lili Fan

    (Jinan University)

  • Yi-Liang Miao

    (Huazhong Agricultural University)

  • Junjun Ding

    (Sun Yat-Sen University
    Sun Yat-Sen University
    Sun Yat-Sen University
    Sun Yat-Sen University)

Abstract

CCCTC-binding factor (CTCF), a ubiquitously expressed and highly conserved protein, is known to play a critical role in chromatin structure. Post-translational modifications (PTMs) diversify the functions of protein to regulate numerous cellular processes. However, the effects of PTMs on the genome-wide binding of CTCF and the organization of three-dimensional (3D) chromatin structure have not been fully understood. In this study, we uncovered the PTM profiling of CTCF and demonstrated that CTCF can be O-GlcNAcylated and arginine methylated. Functionally, we demonstrated that O-GlcNAcylation inhibits CTCF binding to chromatin. Meanwhile, deficiency of CTCF O-GlcNAcylation results in the disruption of loop domains and the alteration of chromatin loops associated with cellular development. Furthermore, the deficiency of CTCF O-GlcNAcylation increases the expression of developmental genes and negatively regulates maintenance and establishment of stem cell pluripotency. In conclusion, these results provide key insights into the role of PTMs for the 3D chromatin structure.

Suggested Citation

  • Xiuxiao Tang & Pengguihang Zeng & Kezhi Liu & Li Qing & Yifei Sun & Xinyi Liu & Lizi Lu & Chao Wei & Jia Wang & Shaoshuai Jiang & Jun Sun & Wakam Chang & Haopeng Yu & Hebing Chen & Jiaguo Zhou & Cheng, 2024. "The PTM profiling of CTCF reveals the regulation of 3D chromatin structure by O-GlcNAcylation," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47048-3
    DOI: 10.1038/s41467-024-47048-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-47048-3
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-47048-3?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Jesse R. Dixon & Siddarth Selvaraj & Feng Yue & Audrey Kim & Yan Li & Yin Shen & Ming Hu & Jun S. Liu & Bing Ren, 2012. "Topological domains in mammalian genomes identified by analysis of chromatin interactions," Nature, Nature, vol. 485(7398), pages 376-380, May.
    2. Hao Nie & Haixing Ju & Jiayi Fan & Xiaoliu Shi & Yaxian Cheng & Xiaohui Cang & Zhiguo Zheng & Xiaotao Duan & Wen Yi, 2020. "O-GlcNAcylation of PGK1 coordinates glycolysis and TCA cycle to promote tumor growth," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    3. Adam C. Bell & Gary Felsenfeld, 2000. "Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene," Nature, Nature, vol. 405(6785), pages 482-485, May.
    4. Shengli Li & Li Yuan & Zhi-Yuan Xu & Jing-Li Xu & Gui-Ping Chen & Xiaoqing Guan & Guang-Zhao Pan & Can Hu & Jinyun Dong & Yi-An Du & Li-Tao Yang & Mao-Wei Ni & Rui-Bin Jiang & Xiu Zhu & Hang Lv & Han-, 2023. "Integrative proteomic characterization of adenocarcinoma of esophagogastric junction," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    5. Teresa Olbrich & Maria Vega-Sendino & Desiree Tillo & Wei Wu & Nicholas Zolnerowich & Raphael Pavani & Andy D. Tran & Catherine N. Domingo & Mariajose Franco & Marta Markiewicz-Potoczny & Gianluca Peg, 2021. "CTCF is a barrier for 2C-like reprogramming," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    6. Jeong Hyun Ahn & Eric S. Davis & Timothy A. Daugird & Shuai Zhao & Ivana Yoseli Quiroga & Hidetaka Uryu & Jie Li & Aaron J. Storey & Yi-Hsuan Tsai & Daniel P. Keeley & Samuel G. Mackintosh & Ricky D. , 2021. "Phase separation drives aberrant chromatin looping and cancer development," Nature, Nature, vol. 595(7868), pages 591-595, July.
    7. Yi Hao & Xinqi Fan & Yujie Shi & Che Zhang & De-en Sun & Ke Qin & Wei Qin & Wen Zhou & Xing Chen, 2019. "Next-generation unnatural monosaccharides reveal that ESRRB O-GlcNAcylation regulates pluripotency of mouse embryonic stem cells," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Julia Minderjahn & Alexander Fischer & Konstantin Maier & Karina Mendes & Margit Nuetzel & Johanna Raithel & Hanna Stanewsky & Ute Ackermann & Robert Månsson & Claudia Gebhard & Michael Rehli, 2022. "Postmitotic differentiation of human monocytes requires cohesin-structured chromatin," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    2. Zhaowei Yu & Qi Wang & Qichen Zhang & Yawen Tian & Guo Yan & Jidong Zhu & Guangya Zhu & Yong Zhang, 2024. "Decoding the genomic landscape of chromatin-associated biomolecular condensates," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    3. Dominic D. G. Owens & Giorgio Anselmi & A. Marieke Oudelaar & Damien J. Downes & Alessandro Cavallo & Joe R. Harman & Ron Schwessinger & Akin Bucakci & Lucas Greder & Sara Ornellas & Danuta Jeziorska , 2022. "Dynamic Runx1 chromatin boundaries affect gene expression in hematopoietic development," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    4. Zhen-Hui Wang & Xin-Feng Wang & Tianyuan Lu & Ming-Rui Li & Peng Jiang & Jing Zhao & Si-Tong Liu & Xue-Qi Fu & Jonathan F. Wendel & Yves Peer & Bao Liu & Lin-Feng Li, 2022. "Reshuffling of the ancestral core-eudicot genome shaped chromatin topology and epigenetic modification in Panax," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    5. Matthias Wielscher & Pooja R. Mandaviya & Brigitte Kuehnel & Roby Joehanes & Rima Mustafa & Oliver Robinson & Yan Zhang & Barbara Bodinier & Esther Walton & Pashupati P. Mishra & Pascal Schlosser & Ro, 2022. "DNA methylation signature of chronic low-grade inflammation and its role in cardio-respiratory diseases," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    6. Halima H. Schede & Pradeep Natarajan & Arup K. Chakraborty & Krishna Shrinivas, 2023. "A model for organization and regulation of nuclear condensates by gene activity," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    7. Zihao Guo & Yang Zhang & Haoyue Wang & Liming Liao & Lingdi Ma & Yiliang Zhao & Ronghui Yang & Xuexue Li & Jing Niu & Qiaoyun Chu & Yanxia Fu & Binghui Li & Chuanzhen Yang, 2024. "Hypoxia-induced downregulation of PGK1 crotonylation promotes tumorigenesis by coordinating glycolysis and the TCA cycle," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    8. Bhuwan Khatri & Kandice L. Tessneer & Astrid Rasmussen & Farhang Aghakhanian & Tove Ragna Reksten & Adam Adler & Ilias Alevizos & Juan-Manuel Anaya & Lara A. Aqrawi & Eva Baecklund & Johan G. Brun & S, 2022. "Genome-wide association study identifies Sjögren’s risk loci with functional implications in immune and glandular cells," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    9. Chong Wang & Xiang Liu & Jun Liang & Yohei Narita & Weiyue Ding & Difei Li & Luyao Zhang & Hongbo Wang & Merrin Man Long Leong & Isabella Hou & Catherine Gerdt & Chang Jiang & Qian Zhong & Zhonghui Ta, 2023. "A DNA tumor virus globally reprograms host 3D genome architecture to achieve immortal growth," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    10. Liyuan Zhou & Qiongzi Qiu & Qing Zhou & Jianwei Li & Mengqian Yu & Kezhen Li & Lingling Xu & Xiaohui Ke & Haiming Xu & Bingjian Lu & Hui Wang & Weiguo Lu & Pengyuan Liu & Yan Lu, 2022. "Long-read sequencing unveils high-resolution HPV integration and its oncogenic progression in cervical cancer," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    11. Vinícius G. Contessoto & Olga Dudchenko & Erez Lieberman Aiden & Peter G. Wolynes & José N. Onuchic & Michele Pierro, 2023. "Interphase chromosomes of the Aedes aegypti mosquito are liquid crystalline and can sense mechanical cues," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    12. Yi Li & James Lee & Lu Bai, 2024. "DNA methylation-based high-resolution mapping of long-distance chromosomal interactions in nucleosome-depleted regions," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    13. Hossein Salari & Geneviève Fourel & Daniel Jost, 2024. "Transcription regulates the spatio-temporal dynamics of genes through micro-compartmentalization," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    14. Alon Diament & Tamir Tuller, 2015. "Improving 3D Genome Reconstructions Using Orthologous and Functional Constraints," PLOS Computational Biology, Public Library of Science, vol. 11(5), pages 1-22, May.
    15. Andrea Wilderman & Eva D’haene & Machteld Baetens & Tara N. Yankee & Emma Wentworth Winchester & Nicole Glidden & Ellen Roets & Jo Dorpe & Sandra Janssens & Danny E. Miller & Miranda Galey & Kari M. B, 2024. "A distant global control region is essential for normal expression of anterior HOXA genes during mouse and human craniofacial development," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    16. Lindsay Lee & Hongyu Yu & Bojing Blair Jia & Adam Jussila & Chenxu Zhu & Jiawen Chen & Liangqi Xie & Antonina Hafner & Shreya Mishra & Duan Dennis Wang & Caterina Strambio-De-Castillia & Alistair Boet, 2023. "SnapFISH: a computational pipeline to identify chromatin loops from multiplexed DNA FISH data," Nature Communications, Nature, vol. 14(1), pages 1-7, December.
    17. Sonali Narang & Yohana Ghebrechristos & Nikki A. Evensen & Nina Murrell & Sylwia Jasinski & Talia H. Ostrow & David T. Teachey & Elizabeth A. Raetz & Timothee Lionnet & Matthew Witkowski & Iannis Aifa, 2024. "Clonal evolution of the 3D chromatin landscape in patients with relapsed pediatric B-cell acute lymphoblastic leukemia," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    18. Jin Woo Oh & Michael A. Beer, 2024. "Gapped-kmer sequence modeling robustly identifies regulatory vocabularies and distal enhancers conserved between evolutionarily distant mammals," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    19. Da Lin & Weize Xu & Ping Hong & Chengchao Wu & Zhihui Zhang & Siheng Zhang & Lingyu Xing & Bing Yang & Wei Zhou & Qin Xiao & Jinyue Wang & Cong Wang & Yu He & Xi Chen & Xiaojian Cao & Jiangwei Man & A, 2022. "Decoding the spatial chromatin organization and dynamic epigenetic landscapes of macrophage cells during differentiation and immune activation," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    20. Brent S. Perlman & Noah Burget & Yeqiao Zhou & Gregory W. Schwartz & Jelena Petrovic & Zora Modrusan & Robert B. Faryabi, 2024. "Enhancer-promoter hubs organize transcriptional networks promoting oncogenesis and drug resistance," Nature Communications, Nature, vol. 15(1), pages 1-21, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47048-3. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.