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Gene expression and cell identity controlled by anaphase-promoting complex

Author

Listed:
  • Eugene Oh

    (University of California at Berkeley
    University of California at Berkeley)

  • Kevin G. Mark

    (University of California at Berkeley
    University of California at Berkeley)

  • Annamaria Mocciaro

    (University of California at Berkeley
    University of California at Berkeley
    Berkeley Lights)

  • Edmond R. Watson

    (Max Planck Institute of Biochemistry)

  • J. Rajan Prabu

    (Max Planck Institute of Biochemistry)

  • Denny D. Cha

    (University of California at Berkeley
    University of California at Berkeley)

  • Martin Kampmann

    (University of California at San Francisco
    University of California at San Francisco
    Chan Zuckerberg Biohub)

  • Nathan Gamarra

    (University of California at San Francisco)

  • Coral Y. Zhou

    (University of California at San Francisco)

  • Michael Rape

    (University of California at Berkeley
    University of California at Berkeley)

Abstract

Metazoan development requires the robust proliferation of progenitor cells, the identities of which are established by tightly controlled transcriptional networks1. As gene expression is globally inhibited during mitosis, the transcriptional programs that define cell identity must be restarted in each cell cycle2–5 but how this is accomplished is poorly understood. Here we identify a ubiquitin-dependent mechanism that integrates gene expression with cell division to preserve cell identity. We found that WDR5 and TBP, which bind active interphase promoters6,7, recruit the anaphase-promoting complex (APC/C) to specific transcription start sites during mitosis. This allows APC/C to decorate histones with ubiquitin chains branched at Lys11 and Lys48 (K11/K48-branched ubiquitin chains) that recruit p97 (also known as VCP) and the proteasome, which ensures the rapid expression of pluripotency genes in the next cell cycle. Mitotic exit and the re-initiation of transcription are thus controlled by a single regulator (APC/C), which provides a robust mechanism for maintaining cell identity throughout cell division.

Suggested Citation

  • Eugene Oh & Kevin G. Mark & Annamaria Mocciaro & Edmond R. Watson & J. Rajan Prabu & Denny D. Cha & Martin Kampmann & Nathan Gamarra & Coral Y. Zhou & Michael Rape, 2020. "Gene expression and cell identity controlled by anaphase-promoting complex," Nature, Nature, vol. 579(7797), pages 136-140, March.
    • Handle: RePEc:nat:nature:v:579:y:2020:i:7797:d:10.1038_s41586-020-2034-1
    DOI: 10.1038/s41586-020-2034-1
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    Cited by:

    1. Amir Pozner & Li Li & Shiv Prakash Verma & Shuxin Wang & Jared J. Barrott & Mary L. Nelson & Jamie S. E. Yu & Gian Luca Negri & Shane Colborne & Christopher S. Hughes & Ju-Fen Zhu & Sydney L. Lambert , 2024. "ASPSCR1-TFE3 reprograms transcription by organizing enhancer loops around hexameric VCP/p97," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    2. Sang Bae Lee & Luciano Garofano & Aram Ko & Fulvio D’Angelo & Brulinda Frangaj & Danika Sommer & Qiwen Gan & KyeongJin Kim & Timothy Cardozo & Antonio Iavarone & Anna Lasorella, 2022. "Regulated interaction of ID2 with the anaphase-promoting complex links progression through mitosis with reactivation of cell-type-specific transcription," Nature Communications, Nature, vol. 13(1), pages 1-14, December.

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