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PCGF1-PRC1 links chromatin repression with DNA replication during hematopoietic cell lineage commitment

Author

Listed:
  • Junichiro Takano

    (RIKEN Center for Integrative Medical Sciences (RIKEN-IMS)
    RIKEN Center for Integrative Medical Sciences
    Graduate School of Medical and Pharmaceutical Sciences, Chiba University)

  • Shinsuke Ito

    (RIKEN Center for Integrative Medical Sciences)

  • Yixing Dong

    (RIKEN Center for Integrative Medical Sciences)

  • Jafar Sharif

    (RIKEN Center for Integrative Medical Sciences)

  • Yaeko Nakajima-Takagi

    (The Institute of Medical Science, University of Tokyo)

  • Taichi Umeyama

    (Laboratory for Microbiome Sciences, RIKEN-IMS)

  • Yong-Woon Han

    (Laboratory for Integrative Genomics, RIKEN-IMS)

  • Kyoichi Isono

    (RIKEN Center for Integrative Medical Sciences
    Wakayama Medical University)

  • Takashi Kondo

    (RIKEN Center for Integrative Medical Sciences)

  • Yusuke Iizuka

    (RIKEN Center for Integrative Medical Sciences)

  • Tomohiro Miyai

    (RIKEN Center for Integrative Medical Sciences)

  • Yoko Koseki

    (RIKEN Center for Integrative Medical Sciences)

  • Mika Ikegaya

    (RIKEN Center for Integrative Medical Sciences (RIKEN-IMS)
    RIKEN Center for Integrative Medical Sciences)

  • Mizuki Sakihara

    (Tokyo University of Science, Noda)

  • Manabu Nakayama

    (Kazusa DNA Research Institute)

  • Osamu Ohara

    (Kazusa DNA Research Institute)

  • Yoshinori Hasegawa

    (Kazusa DNA Research Institute)

  • Kosuke Hashimoto

    (Institute for Protein Research
    Laboratory for Transcriptome Technology, RIKEN-IMS)

  • Erik Arner

    (Laboratory for Applied Regulatory Genomics Network Analysis, RIKEN-IMS)

  • Robert J. Klose

    (University of Oxford)

  • Atsushi Iwama

    (The Institute of Medical Science, University of Tokyo)

  • Haruhiko Koseki

    (RIKEN Center for Integrative Medical Sciences
    Graduate School of Medical and Pharmaceutical Sciences, Chiba University)

  • Tomokatsu Ikawa

    (RIKEN Center for Integrative Medical Sciences (RIKEN-IMS)
    Tokyo University of Science, Noda)

Abstract

Polycomb group proteins (PcG), polycomb repressive complexes 1 and 2 (PRC1 and 2), repress lineage inappropriate genes during development to maintain proper cellular identities. It has been recognized that PRC1 localizes at the replication fork, however, the precise functions of PRC1 during DNA replication are elusive. Here, we reveal that a variant PRC1 containing PCGF1 (PCGF1-PRC1) prevents overloading of activators and chromatin remodeling factors on nascent DNA and thereby mediates proper deposition of nucleosomes and correct downstream chromatin configurations in hematopoietic stem and progenitor cells (HSPCs). This function of PCGF1-PRC1 in turn facilitates PRC2-mediated repression of target genes such as Hmga2 and restricts premature myeloid differentiation. PCGF1-PRC1, therefore, maintains the differentiation potential of HSPCs by linking proper nucleosome configuration at the replication fork with PcG-mediated gene silencing to ensure life-long hematopoiesis.

Suggested Citation

  • Junichiro Takano & Shinsuke Ito & Yixing Dong & Jafar Sharif & Yaeko Nakajima-Takagi & Taichi Umeyama & Yong-Woon Han & Kyoichi Isono & Takashi Kondo & Yusuke Iizuka & Tomohiro Miyai & Yoko Koseki & M, 2022. "PCGF1-PRC1 links chromatin repression with DNA replication during hematopoietic cell lineage commitment," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34856-8
    DOI: 10.1038/s41467-022-34856-8
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    References listed on IDEAS

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    1. Andrea Piunti & Alessandra Rossi & Aurora Cerutti & Mareike Albert & Sriganesh Jammula & Andrea Scelfo & Laura Cedrone & Giulia Fragola & Linda Olsson & Haruhiko Koseki & Giuseppe Testa & Stefano Caso, 2014. "Polycomb proteins control proliferation and transformation independently of cell cycle checkpoints by regulating DNA replication," Nature Communications, Nature, vol. 5(1), pages 1-14, May.
    2. Hiroki Sugishita & Takashi Kondo & Shinsuke Ito & Manabu Nakayama & Nayuta Yakushiji-Kaminatsui & Eiryo Kawakami & Yoko Koseki & Yasuhide Ohinata & Jafar Sharif & Mio Harachi & Neil P. Blackledge & Ro, 2021. "Variant PCGF1-PRC1 links PRC2 recruitment with differentiation-associated transcriptional inactivation at target genes," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    3. Madison J. Kelly & Joan So & Amy J. Rogers & Gareth Gregory & Jason Li & Magnus Zethoven & Micah D. Gearhart & Vivian J. Bardwell & Ricky W. Johnstone & Stephin J. Vervoort & Lev M. Kats, 2019. "Bcor loss perturbs myeloid differentiation and promotes leukaemogenesis," Nature Communications, Nature, vol. 10(1), pages 1-14, December.
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