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Single-nucleosome imaging unveils that condensins and nucleosome–nucleosome interactions differentially constrain chromatin to organize mitotic chromosomes

Author

Listed:
  • Kayo Hibino

    (National Institute of Genetics
    SOKENDAI)

  • Yuji Sakai

    (Yokohama City University
    Kyoto University)

  • Sachiko Tamura

    (National Institute of Genetics)

  • Masatoshi Takagi

    (RIKEN Cluster for Pioneering Research
    RIKEN Center for Brain Science)

  • Katsuhiko Minami

    (National Institute of Genetics
    SOKENDAI)

  • Toyoaki Natsume

    (SOKENDAI
    National Institute of Genetics
    Tokyo Metropolitan Institute of Medical Science)

  • Masa A. Shimazoe

    (National Institute of Genetics
    SOKENDAI)

  • Masato T. Kanemaki

    (SOKENDAI
    National Institute of Genetics
    The University of Tokyo)

  • Naoko Imamoto

    (RIKEN Cluster for Pioneering Research
    Jikei University of Health Care Sciences)

  • Kazuhiro Maeshima

    (National Institute of Genetics
    SOKENDAI)

Abstract

For accurate mitotic cell division, replicated chromatin must be assembled into chromosomes and faithfully segregated into daughter cells. While protein factors like condensin play key roles in this process, it is unclear how chromosome assembly proceeds as molecular events of nucleosomes in living cells and how condensins act on nucleosomes to organize chromosomes. To approach these questions, we investigate nucleosome behavior during mitosis of living human cells using single-nucleosome tracking, combined with rapid-protein depletion technology and computational modeling. Our results show that local nucleosome motion becomes increasingly constrained during mitotic chromosome assembly, which is functionally distinct from condensed apoptotic chromatin. Condensins act as molecular crosslinkers, locally constraining nucleosomes to organize chromosomes. Additionally, nucleosome-nucleosome interactions via histone tails constrain and compact whole chromosomes. Our findings elucidate the physical nature of the chromosome assembly process during mitosis.

Suggested Citation

  • Kayo Hibino & Yuji Sakai & Sachiko Tamura & Masatoshi Takagi & Katsuhiko Minami & Toyoaki Natsume & Masa A. Shimazoe & Masato T. Kanemaki & Naoko Imamoto & Kazuhiro Maeshima, 2024. "Single-nucleosome imaging unveils that condensins and nucleosome–nucleosome interactions differentially constrain chromatin to organize mitotic chromosomes," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-51454-y
    DOI: 10.1038/s41467-024-51454-y
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    References listed on IDEAS

    as
    1. Stephen E. Farr & Esmae J. Woods & Jerelle A. Joseph & Adiran Garaizar & Rosana Collepardo-Guevara, 2021. "Nucleosome plasticity is a critical element of chromatin liquid–liquid phase separation and multivalent nucleosome interactions," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    2. Kazuhiro Maeshima, 2022. "A phase transition for chromosome transmission when cells divide," Nature, Nature, vol. 609(7925), pages 35-36, September.
    3. Sara Cuylen & Claudia Blaukopf & Antonio Z. Politi & Thomas Müller-Reichert & Beate Neumann & Ina Poser & Jan Ellenberg & Anthony A. Hyman & Daniel W. Gerlich, 2016. "Ki-67 acts as a biological surfactant to disperse mitotic chromosomes," Nature, Nature, vol. 535(7611), pages 308-312, July.
    4. Aisha Yesbolatova & Yuichiro Saito & Naomi Kitamoto & Hatsune Makino-Itou & Rieko Ajima & Risako Nakano & Hirofumi Nakaoka & Kosuke Fukui & Kanae Gamo & Yusuke Tominari & Haruki Takeuchi & Yumiko Saga, 2020. "The auxin-inducible degron 2 technology provides sharp degradation control in yeast, mammalian cells, and mice," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
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