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Phase separation of BuGZ regulates gut regeneration and aging through interaction with m6A regulators

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  • Qiaoqiao Zhang

    (Sichuan University
    Sichuan University
    Sun Yat-sen University)

  • Kai Deng

    (Sichuan University
    Sichuan University)

  • Mengyou Liu

    (Sichuan University)

  • Shengye Yang

    (Sichuan University)

  • Wei Xu

    (Sichuan University)

  • Tong Feng

    (Sun Yat-sen University)

  • Minwen Jie

    (Sichuan University)

  • Zhiming Liu

    (Sichuan University)

  • Xiao Sheng

    (Sichuan University)

  • Haiyang Chen

    (Sichuan University)

  • Hao Jiang

    (Sichuan University)

Abstract

Exploring the role of phase separation in intracellular compartment formation is an active area of research. However, the associations of phase separation with intestinal stem cell (ISC)-dependent regeneration and aging remain unclear. Here, we demonstrate that BuGZ, a coacervating mitotic effector, shows age- and injury-associated condensation in Drosophila ISC nuclei during interphase. BuGZ condensation promotes ISC proliferation, affecting Drosophila gut repair and longevity. Moreover, m6A reader YT521-B acts as the transcriptional and functional downstream of BuGZ. The binding of YT521-B promotor or m6A writer Ime4/ Mettl14 to BuGZ controls its coacervation, indicating that the promotor may accelerate the phase transition of its binding transcription factor. Hence, we propose that phase separation and m6A regulators may be critical for ameliorating ISC-dependent gut regeneration and aging and requires further study.

Suggested Citation

  • Qiaoqiao Zhang & Kai Deng & Mengyou Liu & Shengye Yang & Wei Xu & Tong Feng & Minwen Jie & Zhiming Liu & Xiao Sheng & Haiyang Chen & Hao Jiang, 2023. "Phase separation of BuGZ regulates gut regeneration and aging through interaction with m6A regulators," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42474-1
    DOI: 10.1038/s41467-023-42474-1
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    References listed on IDEAS

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    1. Patrick Cramer, 2019. "Organization and regulation of gene transcription," Nature, Nature, vol. 573(7772), pages 45-54, September.
    2. Junho Choe & Shuibin Lin & Wencai Zhang & Qi Liu & Longfei Wang & Julia Ramirez-Moya & Peng Du & Wantae Kim & Shaojun Tang & Piotr Sliz & Pilar Santisteban & Rani E. George & William G. Richards & Kwo, 2018. "mRNA circularization by METTL3–eIF3h enhances translation and promotes oncogenesis," Nature, Nature, vol. 561(7724), pages 556-560, September.
    3. Fang Fang & Ninuo Xia & Benjamin Angulo & Joseph Carey & Zackery Cady & Jens Durruthy-Durruthy & Theo Bennett & Vittorio Sebastiano & Renee A. Reijo Pera, 2018. "A distinct isoform of ZNF207 controls self-renewal and pluripotency of human embryonic stem cells," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    4. Joshua A. Riback & Lian Zhu & Mylene C. Ferrolino & Michele Tolbert & Diana M. Mitrea & David W. Sanders & Ming-Tzo Wei & Richard W. Kriwacki & Clifford P. Brangwynne, 2020. "Composition-dependent thermodynamics of intracellular phase separation," Nature, Nature, vol. 581(7807), pages 209-214, May.
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