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A DNA tumor virus globally reprograms host 3D genome architecture to achieve immortal growth

Author

Listed:
  • Chong Wang

    (Brigham and Women’s Hospital and Harvard Medical School
    University of Minnesota)

  • Xiang Liu

    (H. Lee Moffitt Cancer Center and Research Institute)

  • Jun Liang

    (Brigham and Women’s Hospital and Harvard Medical School)

  • Yohei Narita

    (Brigham and Women’s Hospital and Harvard Medical School)

  • Weiyue Ding

    (Brigham and Women’s Hospital and Harvard Medical School)

  • Difei Li

    (Brigham and Women’s Hospital and Harvard Medical School)

  • Luyao Zhang

    (Brigham and Women’s Hospital and Harvard Medical School)

  • Hongbo Wang

    (Brigham and Women’s Hospital and Harvard Medical School)

  • Merrin Man Long Leong

    (Brigham and Women’s Hospital and Harvard Medical School)

  • Isabella Hou

    (Brigham and Women’s Hospital and Harvard Medical School)

  • Catherine Gerdt

    (Brigham and Women’s Hospital and Harvard Medical School)

  • Chang Jiang

    (Brigham and Women’s Hospital and Harvard Medical School
    H. Lee Moffitt Cancer Center and Research Institute)

  • Qian Zhong

    (Sun Yat-sen University Cancer Center)

  • Zhonghui Tang

    (Sun Yat-sen University)

  • Carmy Forney

    (Cincinnati Children’s Hospital Medical Center)

  • Leah Kottyan

    (Cincinnati Children’s Hospital Medical Center)

  • Matthew T. Weirauch

    (Cincinnati Children’s Hospital Medical Center)

  • Benjamin E. Gewurz

    (Brigham and Women’s Hospital and Harvard Medical School)

  • Mu-sheng Zeng

    (Sun Yat-sen University Cancer Center)

  • Sizun Jiang

    (Beth Israel Deaconess Medical Center and Harvard Medical School)

  • Mingxiang Teng

    (H. Lee Moffitt Cancer Center and Research Institute)

  • Bo Zhao

    (Brigham and Women’s Hospital and Harvard Medical School)

Abstract

Epstein-Barr virus (EBV) immortalization of resting B lymphocytes (RBLs) to lymphoblastoid cell lines (LCLs) models human DNA tumor virus oncogenesis. RBL and LCL chromatin interaction maps are compared to identify the spatial and temporal genome architectural changes during EBV B cell transformation. EBV induces global genome reorganization where contact domains frequently merge or subdivide during transformation. Repressed B compartments in RBLs frequently switch to active A compartments in LCLs. LCLs gain 40% new contact domain boundaries. Newly gained LCL boundaries have strong CTCF binding at their borders while in RBLs, the same sites have much less CTCF binding. Some LCL CTCF sites also have EBV nuclear antigen (EBNA) leader protein EBNALP binding. LCLs have more local interactions than RBLs at LCL dependency factors and super-enhancer targets. RNA Pol II HiChIP and FISH of RBL and LCL further validate the Hi-C results. EBNA3A inactivation globally alters LCL genome interactions. EBNA3A inactivation reduces CTCF and RAD21 DNA binding. EBNA3C inactivation rewires the looping at the CDKN2A/B and AICDA loci. Disruption of a CTCF site at AICDA locus increases AICDA expression. These data suggest that EBV controls lymphocyte growth by globally reorganizing host genome architecture to facilitate the expression of key oncogenes.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37347-6
    DOI: 10.1038/s41467-023-37347-6
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    References listed on IDEAS

    as
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