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ZNF143 mediates CTCF-bound promoter–enhancer loops required for murine hematopoietic stem and progenitor cell function

Author

Listed:
  • Qiling Zhou

    (Cancer Science Institute of Singapore, National University of Singapore
    YLL School of Medicine, National University of Singapore)

  • Miao Yu

    (School of Life Sciences, Fudan University)

  • Roberto Tirado-Magallanes

    (Cancer Science Institute of Singapore, National University of Singapore)

  • Bin Li

    (Ludwig Institute for Cancer Research)

  • Lingshi Kong

    (Cancer Science Institute of Singapore, National University of Singapore)

  • Mingrui Guo

    (Cancer Science Institute of Singapore, National University of Singapore
    YLL School of Medicine, National University of Singapore)

  • Zi Hui Tan

    (Cancer Science Institute of Singapore, National University of Singapore)

  • Sanghoon Lee

    (Cancer Science Institute of Singapore, National University of Singapore
    The University of Texas MD Anderson Cancer Center)

  • Li Chai

    (Brigham and Women’s Hospital)

  • Akihiko Numata

    (Cancer Science Institute of Singapore, National University of Singapore
    Medicine and Biosystemic Science, Kyushu University Graduate School of Medical Science)

  • Touati Benoukraf

    (Cancer Science Institute of Singapore, National University of Singapore
    Division of BioMedical Sciences, Faculty of Medicine, Memorial University of Newfoundland)

  • Melissa Jane Fullwood

    (Cancer Science Institute of Singapore, National University of Singapore
    School of Biological Sciences, Nanyang Technological University
    Institute of Molecular and Cell Biology, Agency for Science, Technology and Research (A*STAR))

  • Motomi Osato

    (Cancer Science Institute of Singapore, National University of Singapore)

  • Bing Ren

    (Ludwig Institute for Cancer Research
    Moores Cancer Center and Institute of Genome Medicine, UCSD School of Medicine)

  • Daniel G. Tenen

    (Cancer Science Institute of Singapore, National University of Singapore
    Harvard Stem Cell Institute, Harvard Medical School)

Abstract

CCCTC binding factor (CTCF) is an important factor in the maintenance of chromatin–chromatin interactions, yet the mechanism regulating its binding to chromatin is unknown. We demonstrate that zinc finger protein 143 (ZNF143) is a key regulator for CTCF-bound promoter–enhancer loops. In the murine genome, a large percentage of CTCF and ZNF143 DNA binding motifs are distributed 37 bp apart in the convergent orientation. Furthermore, deletion of ZNF143 leads to loss of CTCF binding on promoter and enhancer regions associated with gene expression changes. CTCF-bound promoter–enhancer loops are also disrupted after excision of ZNF143. ZNF143-CTCF-bound promoter–enhancer loops regulate gene expression patterns essential for maintenance of murine hematopoietic stem and progenitor cell integrity. Our data suggest a common feature of gene regulation is that ZNF143 is a critical factor for CTCF-bound promoter–enhancer loops.

Suggested Citation

  • Qiling Zhou & Miao Yu & Roberto Tirado-Magallanes & Bin Li & Lingshi Kong & Mingrui Guo & Zi Hui Tan & Sanghoon Lee & Li Chai & Akihiko Numata & Touati Benoukraf & Melissa Jane Fullwood & Motomi Osato, 2021. "ZNF143 mediates CTCF-bound promoter–enhancer loops required for murine hematopoietic stem and progenitor cell function," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-020-20282-1
    DOI: 10.1038/s41467-020-20282-1
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    Cited by:

    1. 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.
    2. Yanli Liu & Zhong Wu & Jin Zhou & Dinesh K. A. Ramadurai & Katelyn L. Mortenson & Estrella Aguilera-Jimenez & Yifei Yan & Xiaojun Yang & Alison M. Taylor & Katherine E. Varley & Jason Gertz & Peter S., 2021. "A predominant enhancer co-amplified with the SOX2 oncogene is necessary and sufficient for its expression in squamous cancer," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    3. Muran Xiao & Shinji Kondo & Masaki Nomura & Shinichiro Kato & Koutarou Nishimura & Weijia Zang & Yifan Zhang & Tomohiro Akashi & Aaron Viny & Tsukasa Shigehiro & Tomokatsu Ikawa & Hiromi Yamazaki & Mi, 2023. "BRD9 determines the cell fate of hematopoietic stem cells by regulating chromatin state," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    4. Shuai Liu & Yaqiang Cao & Kairong Cui & Qingsong Tang & Keji Zhao, 2022. "Hi-TrAC reveals division of labor of transcription factors in organizing chromatin loops," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    5. Zhao Wang & Qian Liang & Xinyi Qian & Bolang Hu & Zhanye Zheng & Jianhua Wang & Yuelin Hu & Zhengkai Bao & Ke Zhao & Yao Zhou & Xiangling Feng & Xianfu Yi & Jin Li & Jiandang Shi & Zhe Liu & Jihui Hao, 2023. "An autoimmune pleiotropic SNP modulates IRF5 alternative promoter usage through ZBTB3-mediated chromatin looping," Nature Communications, Nature, vol. 14(1), pages 1-23, December.

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