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Histone exchange sensors reveal variant specific dynamics in mouse embryonic stem cells

Author

Listed:
  • Marko Dunjić

    (Weizmann Institute of Science)

  • Felix Jonas

    (Weizmann Institute of Science)

  • Gilad Yaakov

    (Weizmann Institute of Science)

  • Roye More

    (Weizmann Institute of Science)

  • Yoav Mayshar

    (Weizmann Institute of Science)

  • Yoach Rais

    (Weizmann Institute of Science)

  • Ayelet-Hashahar Orenbuch

    (Weizmann Institute of Science)

  • Saifeng Cheng

    (Weizmann Institute of Science)

  • Naama Barkai

    (Weizmann Institute of Science)

  • Yonatan Stelzer

    (Weizmann Institute of Science)

Abstract

Eviction of histones from nucleosomes and their exchange with newly synthesized or alternative variants is a central epigenetic determinant. Here, we define the genome-wide occupancy and exchange pattern of canonical and non-canonical histone variants in mouse embryonic stem cells by genetically encoded exchange sensors. While exchange of all measured variants scales with transcription, we describe variant-specific associations with transcription elongation and Polycomb binding. We found considerable exchange of H3.1 and H2B variants in heterochromatin and repeat elements, contrasting the occupancy and little exchange of H3.3 in these regions. This unexpected association between H3.3 occupancy and exchange of canonical variants is also evident in active promoters and enhancers, and further validated by reduced H3.1 dynamics following depletion of H3.3-specific chaperone, HIRA. Finally, analyzing transgenic mice harboring H3.1 or H3.3 sensors demonstrates the vast potential of this system for studying histone exchange and its impact on gene expression regulation in vivo.

Suggested Citation

  • Marko Dunjić & Felix Jonas & Gilad Yaakov & Roye More & Yoav Mayshar & Yoach Rais & Ayelet-Hashahar Orenbuch & Saifeng Cheng & Naama Barkai & Yonatan Stelzer, 2023. "Histone exchange sensors reveal variant specific dynamics in mouse embryonic stem cells," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39477-3
    DOI: 10.1038/s41467-023-39477-3
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    References listed on IDEAS

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    1. Simon J. Elsässer & Kyung-Min Noh & Nichole Diaz & C. David Allis & Laura A. Banaszynski, 2015. "Histone H3.3 is required for endogenous retroviral element silencing in embryonic stem cells," Nature, Nature, vol. 522(7555), pages 240-244, June.
    2. Tim J. Stevens & David Lando & Srinjan Basu & Liam P. Atkinson & Yang Cao & Steven F. Lee & Martin Leeb & Kai J. Wohlfahrt & Wayne Boucher & Aoife O’Shaughnessy-Kirwan & Julie Cramard & Andre J. Faure, 2017. "3D structures of individual mammalian genomes studied by single-cell Hi-C," Nature, Nature, vol. 544(7648), pages 59-64, April.
    3. M. L. Richter & I. K. Deligiannis & K. Yin & A. Danese & E. Lleshi & P. Coupland & C. A. Vallejos & K. P. Matchett & N. C. Henderson & M. Colome-Tatche & C. P. Martinez-Jimenez, 2021. "Single-nucleus RNA-seq2 reveals functional crosstalk between liver zonation and ploidy," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    4. Jesse R. Dixon & Siddarth Selvaraj & Feng Yue & Audrey Kim & Yan Li & Yin Shen & Ming Hu & Jun S. Liu & Bing Ren, 2012. "Topological domains in mammalian genomes identified by analysis of chromatin interactions," Nature, Nature, vol. 485(7398), pages 376-380, May.
    5. Michael Lawrence & Wolfgang Huber & Hervé Pagès & Patrick Aboyoun & Marc Carlson & Robert Gentleman & Martin T Morgan & Vincent J Carey, 2013. "Software for Computing and Annotating Genomic Ranges," PLOS Computational Biology, Public Library of Science, vol. 9(8), pages 1-10, August.
    6. Karolin Luger & Armin W. Mäder & Robin K. Richmond & David F. Sargent & Timothy J. Richmond, 1997. "Crystal structure of the nucleosome core particle at 2.8 Å resolution," Nature, Nature, vol. 389(6648), pages 251-260, September.
    7. Michael B. Stadler & Rabih Murr & Lukas Burger & Robert Ivanek & Florian Lienert & Anne Schöler & Erik van Nimwegen & Christiane Wirbelauer & Edward J. Oakeley & Dimos Gaidatzis & Vijay K. Tiwari & Di, 2011. "DNA-binding factors shape the mouse methylome at distal regulatory regions," Nature, Nature, vol. 480(7378), pages 490-495, December.
    8. Alvaro Rada-Iglesias & Ruchi Bajpai & Tomek Swigut & Samantha A. Brugmann & Ryan A. Flynn & Joanna Wysocka, 2011. "A unique chromatin signature uncovers early developmental enhancers in humans," Nature, Nature, vol. 470(7333), pages 279-283, February.
    9. Parysatis Sachs & Dong Ding & Philipp Bergmaier & Boris Lamp & Christina Schlagheck & Florian Finkernagel & Andrea Nist & Thorsten Stiewe & Jacqueline E. Mermoud, 2019. "SMARCAD1 ATPase activity is required to silence endogenous retroviruses in embryonic stem cells," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
    10. Elphège P. Nora & Laura Caccianini & Geoffrey Fudenberg & Kevin So & Vasumathi Kameswaran & Abigail Nagle & Alec Uebersohn & Bassam Hajj & Agnès Le Saux & Antoine Coulon & Leonid A. Mirny & Katherine , 2020. "Molecular basis of CTCF binding polarity in genome folding," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    11. Darko Barisic & Michael B. Stadler & Mario Iurlaro & Dirk Schübeler, 2019. "Mammalian ISWI and SWI/SNF selectively mediate binding of distinct transcription factors," Nature, Nature, vol. 569(7754), pages 136-140, May.
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