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Regulated interaction of ID2 with the anaphase-promoting complex links progression through mitosis with reactivation of cell-type-specific transcription

Author

Listed:
  • Sang Bae Lee

    (Columbia University Medical Center
    Jeonbuk National University)

  • Luciano Garofano

    (Columbia University Medical Center)

  • Aram Ko

    (Columbia University Medical Center)

  • Fulvio D’Angelo

    (Columbia University Medical Center)

  • Brulinda Frangaj

    (Columbia University Medical Center)

  • Danika Sommer

    (Columbia University Medical Center)

  • Qiwen Gan

    (Columbia University Medical Center)

  • KyeongJin Kim

    (Inha University)

  • Timothy Cardozo

    (NYU Langone Health)

  • Antonio Iavarone

    (Columbia University Medical Center
    Columbia University Medical Center
    Columbia University Medical Center
    Columbia University Medical Center)

  • Anna Lasorella

    (Columbia University Medical Center
    Columbia University Medical Center
    Columbia University Medical Center
    Columbia University Medical Center)

Abstract

Tissue-specific transcriptional activity is silenced in mitotic cells but it remains unclear whether the mitotic regulatory machinery interacts with tissue-specific transcriptional programs. We show that such cross-talk involves the controlled interaction between core subunits of the anaphase-promoting complex (APC) and the ID2 substrate. The N-terminus of ID2 is independently and structurally compatible with a pocket composed of core APC/C subunits that may optimally orient ID2 onto the APCCDH1 complex. Phosphorylation of serine-5 by CDK1 prevented the association of ID2 with core APC, impaired ubiquitylation and stabilized ID2 protein at the mitosis-G1 transition leading to inhibition of basic Helix-Loop-Helix (bHLH)-mediated transcription. The serine-5 phospho-mimetic mutant of ID2 that inefficiently bound core APC remained stable during mitosis, delayed exit from mitosis and reloading of bHLH transcription factors on chromatin. It also locked cells into a “mitotic stem cell” transcriptional state resembling the pluripotent program of embryonic stem cells. The substrates of APCCDH1 SKP2 and Cyclin B1 share with ID2 the phosphorylation-dependent, D-box-independent interaction with core APC. These results reveal a new layer of control of the mechanism by which substrates are recognized by APC.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29502-2
    DOI: 10.1038/s41467-022-29502-2
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    References listed on IDEAS

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