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Chromatin structure dynamics during the mitosis-to-G1 phase transition

Author

Listed:
  • Haoyue Zhang

    (The Children’s Hospital of Philadelphia)

  • Daniel J. Emerson

    (University of Pennsylvania)

  • Thomas G. Gilgenast

    (University of Pennsylvania)

  • Katelyn R. Titus

    (University of Pennsylvania)

  • Yemin Lan

    (University of Pennsylvania)

  • Peng Huang

    (The Children’s Hospital of Philadelphia)

  • Di Zhang

    (The Children’s Hospital of Philadelphia
    University of Pennsylvania)

  • Hongxin Wang

    (The Children’s Hospital of Philadelphia)

  • Cheryl A. Keller

    (Pennsylvania State University)

  • Belinda Giardine

    (Pennsylvania State University)

  • Ross C. Hardison

    (Pennsylvania State University)

  • Jennifer E. Phillips-Cremins

    (University of Pennsylvania)

  • Gerd A. Blobel

    (The Children’s Hospital of Philadelphia
    University of Pennsylvania)

Abstract

Features of higher-order chromatin organization—such as A/B compartments, topologically associating domains and chromatin loops—are temporarily disrupted during mitosis1,2. Because these structures are thought to influence gene regulation, it is important to understand how they are re-established after mitosis. Here we examine the dynamics of chromosome reorganization by Hi-C after mitosis in highly purified, synchronous mouse erythroid cell populations. We observed rapid establishment of A/B compartments, followed by their gradual intensification and expansion. Contact domains form from the ‘bottom up’—smaller subTADs are formed initially, followed by convergence into multi-domain TAD structures. CTCF is partially retained on mitotic chromosomes and immediately resumes full binding in ana/telophase. By contrast, cohesin is completely evicted from mitotic chromosomes and regains focal binding at a slower rate. The formation of CTCF/cohesin co-anchored structural loops follows the kinetics of cohesin positioning. Stripe-shaped contact patterns—anchored by CTCF—grow in length, which is consistent with a loop-extrusion process after mitosis. Interactions between cis-regulatory elements can form rapidly, with rates exceeding those of CTCF/cohesin-anchored contacts. Notably, we identified a group of rapidly emerging transient contacts between cis-regulatory elements in ana/telophase that are dissolved upon G1 entry, co-incident with the establishment of inner boundaries or nearby interfering chromatin loops. We also describe the relationship between transcription reactivation and architectural features. Our findings indicate that distinct but mutually influential forces drive post-mitotic chromatin reconfiguration.

Suggested Citation

  • Haoyue Zhang & Daniel J. Emerson & Thomas G. Gilgenast & Katelyn R. Titus & Yemin Lan & Peng Huang & Di Zhang & Hongxin Wang & Cheryl A. Keller & Belinda Giardine & Ross C. Hardison & Jennifer E. Phil, 2019. "Chromatin structure dynamics during the mitosis-to-G1 phase transition," Nature, Nature, vol. 576(7785), pages 158-162, December.
  • Handle: RePEc:nat:nature:v:576:y:2019:i:7785:d:10.1038_s41586-019-1778-y
    DOI: 10.1038/s41586-019-1778-y
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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. Botong Zhou & Ping Hu & Guichun Liu & Zhou Chang & Zhiwei Dong & Zihe Li & Yuan Yin & Zunzhe Tian & Ge Han & Wen Wang & Xueyan Li, 2024. "Evolutionary patterns and functional effects of 3D chromatin structures in butterflies with extensive genome rearrangements," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    4. Maëlle Bellec & Jérémy Dufourt & George Hunt & Hélène Lenden-Hasse & Antonio Trullo & Amal Zine El Aabidine & Marie Lamarque & Marissa M. Gaskill & Heloïse Faure-Gautron & Mattias Mannervik & Melissa , 2022. "The control of transcriptional memory by stable mitotic bookmarking," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    5. 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.
    6. Jia-Yong Zhong & Longjian Niu & Zhuo-Bin Lin & Xin Bai & Ying Chen & Feng Luo & Chunhui Hou & Chuan-Le Xiao, 2023. "High-throughput Pore-C reveals the single-allele topology and cell type-specificity of 3D genome folding," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    7. Shuai Liu & Yaqiang Cao & Kairong Cui & Qingsong Tang & Keji Zhao, 2022. "Hi-TrAC reveals division of labor of transcription factors in organizing chromatin loops," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    8. Guilherme M. Oliveira & Attila Oravecz & Dominique Kobi & Manon Maroquenne & Kerstin Bystricky & Tom Sexton & Nacho Molina, 2021. "Precise measurements of chromatin diffusion dynamics by modeling using Gaussian processes," Nature Communications, Nature, vol. 12(1), pages 1-11, December.

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