IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-29730-6.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-29730-6
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-29730-6?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Mina N. F. Morcos & Congxin Li & Clara M. Munz & Alessandro Greco & Nicole Dressel & Susanne Reinhardt & Katrin Sameith & Andreas Dahl & Nils B. Becker & Axel Roers & Thomas Höfer & Alexander Gerbaule, 2022. "Fate mapping of hematopoietic stem cells reveals two pathways of native thrombopoiesis," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    2. Qiang Shan & Xiang Li & Xia Chen & Zhouhao Zeng & Shaoqi Zhu & Kexin Gai & Weiqun Peng & Hai-Hui Xue, 2021. "Tcf1 and Lef1 provide constant supervision to mature CD8+ T cell identity and function by organizing genomic architecture," Nature Communications, Nature, vol. 12(1), pages 1-20, December.
    3. Kensuke Miyake & Junya Ito & Jun Nakabayashi & Shigeyuki Shichino & Kenji Ishiwata & Hajime Karasuyama, 2023. "Single cell transcriptomics clarifies the basophil differentiation trajectory and identifies pre-basophils upstream of mature basophils," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    4. Tiago C. Luis & Nikolaos Barkas & Joana Carrelha & Alice Giustacchini & Stefania Mazzi & Ruggiero Norfo & Bishan Wu & Affaf Aliouat & Jose A. Guerrero & Alba Rodriguez-Meira & Tiphaine Bouriez-Jones &, 2023. "Perivascular niche cells sense thrombocytopenia and activate hematopoietic stem cells in an IL-1 dependent manner," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    5. Taichi Nakatani & Tatsuki Sugiyama & Yoshiki Omatsu & Hitomi Watanabe & Gen Kondoh & Takashi Nagasawa, 2023. "Ebf3+ niche-derived CXCL12 is required for the localization and maintenance of hematopoietic stem cells," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    6. Tianyu Zhu & Huige Tong & Zhaozhen Du & Stephan Beck & Andrew E. Teschendorff, 2024. "An improved epigenetic counter to track mitotic age in normal and precancerous tissues," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    7. Brandon Hadland & Barbara Varnum-Finney & Stacey Dozono & Tessa Dignum & Cynthia Nourigat-McKay & Adam M. Heck & Takashi Ishida & Dana L. Jackson & Tomer Itkin & Jason M. Butler & Shahin Rafii & Cole , 2022. "Engineering a niche supporting hematopoietic stem cell development using integrated single-cell transcriptomics," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    8. Yinghui Li & Mei He & Wenshan Zhang & Wei Liu & Hui Xu & Ming Yang & Hexiao Zhang & Haiwei Liang & Wenjing Li & Zhaozhao Wu & Weichao Fu & Shiqi Xu & Xiaolei Liu & Sibin Fan & Liwei Zhou & Chaoqun Wan, 2023. "Expansion of human megakaryocyte-biased hematopoietic stem cells by biomimetic Microniche," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    9. Yuxuan Liu & Zhimin Gu & Hui Cao & Pranita Kaphle & Junhua Lyu & Yuannyu Zhang & Wenhuo Hu & Stephen S. Chung & Kathryn E. Dickerson & Jian Xu, 2021. "Convergence of oncogenic cooperation at single-cell and single-gene levels drives leukemic transformation," Nature Communications, Nature, vol. 12(1), pages 1-17, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29730-6. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.