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Topoisomerase I is an evolutionarily conserved key regulator for satellite DNA transcription

Author

Listed:
  • Zhen Teng

    (Tulane University School of Medicine)

  • Lu Yang

    (Tulane University School of Medicine)

  • Qian Zhang

    (Tulane University School of Medicine)

  • Yujue Chen

    (Tulane University School of Medicine)

  • Xianfeng Wang

    (Tulane University School of Medicine)

  • Yiran Zheng

    (Tulane University School of Medicine)

  • Aiguo Tian

    (Tulane University School of Medicine
    Tulane University School of Medicine
    Tulane University School of Medicine)

  • Di Tian

    (Tulane University School of Medicine)

  • Zhen Lin

    (Tulane University School of Medicine
    Tulane University School of Medicine)

  • Wu-Min Deng

    (Tulane University School of Medicine
    Tulane University School of Medicine)

  • Hong Liu

    (Tulane University School of Medicine
    Tulane University School of Medicine
    Tulane University School of Medicine)

Abstract

RNA Polymerase (RNAP) II transcription on non-coding repetitive satellite DNAs plays an important role in chromosome segregation, but a little is known about the regulation of satellite transcription. We here show that Topoisomerase I (TopI), not TopII, promotes the transcription of α-satellite DNAs, the main type of satellite DNAs on human centromeres. Mechanistically, TopI localizes to centromeres, binds RNAP II and facilitates RNAP II elongation. Interestingly, in response to DNA double-stranded breaks (DSBs), α-satellite transcription is dramatically stimulated in a DNA damage checkpoint-independent but TopI-dependent manner, and these DSB-induced α-satellite RNAs form into strong speckles in the nucleus. Remarkably, TopI-dependent satellite transcription also exists in mouse 3T3 and Drosophila S2 cells and in Drosophila larval imaginal wing discs and tumor tissues. Altogether, our findings herein reveal an evolutionally conserved mechanism with TopI as a key player for the regulation of satellite transcription at both cellular and animal levels.

Suggested Citation

  • Zhen Teng & Lu Yang & Qian Zhang & Yujue Chen & Xianfeng Wang & Yiran Zheng & Aiguo Tian & Di Tian & Zhen Lin & Wu-Min Deng & Hong Liu, 2024. "Topoisomerase I is an evolutionarily conserved key regulator for satellite DNA transcription," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49567-5
    DOI: 10.1038/s41467-024-49567-5
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    References listed on IDEAS

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    1. Duygu Yilmaz & Audrey Furst & Karen Meaburn & Aleksandra Lezaja & Yanlin Wen & Matthias Altmeyer & Bernardo Reina-San-Martin & Evi Soutoglou, 2021. "Activation of homologous recombination in G1 preserves centromeric integrity," Nature, Nature, vol. 600(7890), pages 748-753, December.
    2. Glennis A. Logsdon & Mitchell R. Vollger & PingHsun Hsieh & Yafei Mao & Mikhail A. Liskovykh & Sergey Koren & Sergey Nurk & Ludovica Mercuri & Philip C. Dishuck & Arang Rhie & Leonardo G. Lima & Tatia, 2021. "The structure, function and evolution of a complete human chromosome 8," Nature, Nature, vol. 593(7857), pages 101-107, May.
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