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Regulation of chromatin accessibility by the histone chaperone CAF-1 sustains lineage fidelity

Author

Listed:
  • Reuben Franklin

    (University of California, Riverside
    University of California, Riverside)

  • Yiming Guo

    (University of California, Riverside
    University of California, Riverside)

  • Shiyang He

    (University of California, Riverside)

  • Meijuan Chen

    (University of California, Riverside
    University of California, Riverside)

  • Fei Ji

    (Massachusetts General Hospital)

  • Xinyue Zhou

    (O’Neal Comprehensive Cancer Center, University of Alabama at Birmingham)

  • David Frankhouser

    (Department of Population Sciences City of Hope National Medical Center)

  • Brian T. Do

    (Massachusetts Institute of Technology
    Massachusetts Institute of Technology
    Harvard Medical School)

  • Carmen Chiem

    (University of California, Riverside
    University of California, Riverside)

  • Mihyun Jang

    (Division of Mathematical Oncology, City of Hope National Medical Center)

  • M. Andres Blanco

    (University of Pennsylvania)

  • Matthew G. Vander Heiden

    (Massachusetts Institute of Technology
    Massachusetts Institute of Technology
    Harvard Medical School)

  • Russell C. Rockne

    (Division of Mathematical Oncology, City of Hope National Medical Center)

  • Maria Ninova

    (University of California, Riverside)

  • David B. Sykes

    (Massachusetts General Hospital)

  • Konrad Hochedlinger

    (Massachusetts General Hospital
    Harvard Medical School
    Harvard Stem Cell Institute
    Cancer Center, Massachusetts General Hospital)

  • Rui Lu

    (O’Neal Comprehensive Cancer Center, University of Alabama at Birmingham)

  • Ruslan I. Sadreyev

    (Massachusetts General Hospital
    Massachusetts General Hospital and Harvard Medical School)

  • Jernej Murn

    (University of California, Riverside)

  • Andrew Volk

    (Cincinnati Children’s Hospital Medical Center)

  • Sihem Cheloufi

    (University of California, Riverside
    University of California, Riverside)

Abstract

Cell fate commitment is driven by dynamic changes in chromatin architecture and activity of lineage-specific transcription factors (TFs). The chromatin assembly factor-1 (CAF-1) is a histone chaperone that regulates chromatin architecture by facilitating nucleosome assembly during DNA replication. Accumulating evidence supports a substantial role of CAF-1 in cell fate maintenance, but the mechanisms by which CAF-1 restricts lineage choice remain poorly understood. Here, we investigate how CAF-1 influences chromatin dynamics and TF activity during lineage differentiation. We show that CAF-1 suppression triggers rapid differentiation of myeloid stem and progenitor cells into a mixed lineage state. We find that CAF-1 sustains lineage fidelity by controlling chromatin accessibility at specific loci, and limiting the binding of ELF1 TF at newly-accessible diverging regulatory elements. Together, our findings decipher key traits of chromatin accessibility that sustain lineage integrity and point to a powerful strategy for dissecting transcriptional circuits central to cell fate commitment.

Suggested Citation

  • Reuben Franklin & Yiming Guo & Shiyang He & Meijuan Chen & Fei Ji & Xinyue Zhou & David Frankhouser & Brian T. Do & Carmen Chiem & Mihyun Jang & M. Andres Blanco & Matthew G. Vander Heiden & Russell C, 2022. "Regulation of chromatin accessibility by the histone chaperone CAF-1 sustains lineage fidelity," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29730-6
    DOI: 10.1038/s41467-022-29730-6
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    References listed on IDEAS

    as
    1. Joana Carrelha & Yiran Meng & Laura M. Kettyle & Tiago C. Luis & Ruggiero Norfo & Verónica Alcolea & Hanane Boukarabila & Francesca Grasso & Adriana Gambardella & Amit Grover & Kari Högstrand & Allegr, 2018. "Hierarchically related lineage-restricted fates of multipotent haematopoietic stem cells," Nature, Nature, vol. 554(7690), pages 106-111, February.
    2. Elisa Laurenti & Berthold Göttgens, 2018. "From haematopoietic stem cells to complex differentiation landscapes," Nature, Nature, vol. 553(7689), pages 418-426, January.
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