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Cell-cycle dynamics of chromosomal organization at single-cell resolution

Author

Listed:
  • Takashi Nagano

    (Nuclear Dynamics Programme, The Babraham Insitute)

  • Yaniv Lubling

    (Weizmann Institute of Science)

  • Csilla Várnai

    (Nuclear Dynamics Programme, The Babraham Insitute)

  • Carmel Dudley

    (Weizmann Institute of Science)

  • Wing Leung

    (Nuclear Dynamics Programme, The Babraham Insitute)

  • Yael Baran

    (Weizmann Institute of Science)

  • Netta Mendelson Cohen

    (Weizmann Institute of Science)

  • Steven Wingett

    (Nuclear Dynamics Programme, The Babraham Insitute)

  • Peter Fraser

    (Nuclear Dynamics Programme, The Babraham Insitute
    Florida State University)

  • Amos Tanay

    (Weizmann Institute of Science)

Abstract

Chromosomes in proliferating metazoan cells undergo marked structural metamorphoses every cell cycle, alternating between highly condensed mitotic structures that facilitate chromosome segregation, and decondensed interphase structures that accommodate transcription, gene silencing and DNA replication. Here we use single-cell Hi-C (high-resolution chromosome conformation capture) analysis to study chromosome conformations in thousands of individual cells, and discover a continuum of cis-interaction profiles that finely position individual cells along the cell cycle. We show that chromosomal compartments, topological-associated domains (TADs), contact insulation and long-range loops, all defined by bulk Hi-C maps, are governed by distinct cell-cycle dynamics. In particular, DNA replication correlates with a build-up of compartments and a reduction in TAD insulation, while loops are generally stable from G1 to S and G2 phase. Whole-genome three-dimensional structural models reveal a radial architecture of chromosomal compartments with distinct epigenomic signatures. Our single-cell data therefore allow re-interpretation of chromosome conformation maps through the prism of the cell cycle.

Suggested Citation

  • Takashi Nagano & Yaniv Lubling & Csilla Várnai & Carmel Dudley & Wing Leung & Yael Baran & Netta Mendelson Cohen & Steven Wingett & Peter Fraser & Amos Tanay, 2017. "Cell-cycle dynamics of chromosomal organization at single-cell resolution," Nature, Nature, vol. 547(7661), pages 61-67, July.
  • Handle: RePEc:nat:nature:v:547:y:2017:i:7661:d:10.1038_nature23001
    DOI: 10.1038/nature23001
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    Citations

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    Cited by:

    1. Jingxuan Xu & Xiang Xu & Dandan Huang & Yawen Luo & Lin Lin & Xuemei Bai & Yang Zheng & Qian Yang & Yu Cheng & An Huang & Jingyi Shi & Xiaochen Bo & Jin Gu & Hebing Chen, 2024. "A comprehensive benchmarking with interpretation and operational guidance for the hierarchy of topologically associating domains," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    2. Rebecca J. Harris & Maninder Heer & Mark D. Levasseur & Tyrell N. Cartwright & Bethany Weston & Jennifer L. Mitchell & Jonathan M. Coxhead & Luke Gaughan & Lisa Prendergast & Daniel Rico & Jonathan M., 2023. "Release of Histone H3K4-reading transcription factors from chromosomes in mitosis is independent of adjacent H3 phosphorylation," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    3. Stefano Gnan & Joseph M. Josephides & Xia Wu & Manuela Spagnuolo & Dalila Saulebekova & Mylène Bohec & Marie Dumont & Laura G. Baudrin & Daniele Fachinetti & Sylvain Baulande & Chun-Long Chen, 2022. "Kronos scRT: a uniform framework for single-cell replication timing analysis," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    4. Markus Götz & Olivier Messina & Sergio Espinola & Jean-Bernard Fiche & Marcelo Nollmann, 2022. "Multiple parameters shape the 3D chromatin structure of single nuclei at the doc locus in Drosophila," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    5. Aayush Kant & Zixian Guo & Vinayak Vinayak & Maria Victoria Neguembor & Wing Shun Li & Vasundhara Agrawal & Emily Pujadas & Luay Almassalha & Vadim Backman & Melike Lakadamyali & Maria Pia Cosma & Viv, 2024. "Active transcription and epigenetic reactions synergistically regulate meso-scale genomic organization," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    6. Nimrod Rappoport & Elad Chomsky & Takashi Nagano & Charlie Seibert & Yaniv Lubling & Yael Baran & Aviezer Lifshitz & Wing Leung & Zohar Mukamel & Ron Shamir & Peter Fraser & Amos Tanay, 2023. "Single cell Hi-C identifies plastic chromosome conformations underlying the gastrulation enhancer landscape," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    7. Claire Marchal & Nivedita Singh & Zachary Batz & Jayshree Advani & Catherine Jaeger & Ximena Corso-Díaz & Anand Swaroop, 2022. "High-resolution genome topology of human retina uncovers super enhancer-promoter interactions at tissue-specific and multifactorial disease loci," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    8. Yufan Zhou & Tian Li & Lavanya Choppavarapu & Kun Fang & Shili Lin & Victor X. Jin, 2024. "Integration of scHi-C and scRNA-seq data defines distinct 3D-regulated and biological-context dependent cell subpopulations," Nature Communications, Nature, vol. 15(1), pages 1-11, December.

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