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H2A.Z deposition by SWR1C involves multiple ATP-dependent steps

Author

Listed:
  • Jiayi Fan

    (University of Massachusetts Chan Medical School
    University of Massachusetts Chan Medical School)

  • Andrew T. Moreno

    (Blavatnik Institute, Harvard Medical School)

  • Alexander S. Baier

    (University of Massachusetts Chan Medical School
    University of Massachusetts Chan Medical School)

  • Joseph J. Loparo

    (Blavatnik Institute, Harvard Medical School)

  • Craig L. Peterson

    (University of Massachusetts Chan Medical School)

Abstract

Histone variant H2A.Z is a conserved feature of nucleosomes flanking protein-coding genes. Deposition of H2A.Z requires ATP-dependent replacement of nucleosomal H2A by a chromatin remodeler related to the multi-subunit enzyme, yeast SWR1C. How these enzymes use ATP to promote this nucleosome editing reaction remains unclear. Here we use single-molecule and ensemble methodologies to identify three ATP-dependent phases in the H2A.Z deposition reaction. Real-time analysis of single nucleosome remodeling events reveals an initial priming step that occurs after ATP addition that involves a combination of both transient DNA unwrapping from the nucleosome and histone octamer deformations. Priming is followed by rapid loss of histone H2A, which is subsequently released from the H2A.Z nucleosomal product. Surprisingly, rates of both priming and the release of the H2A/H2B dimer are sensitive to ATP concentration. This complex reaction pathway provides multiple opportunities to regulate timely and accurate deposition of H2A.Z at key genomic locations.

Suggested Citation

  • Jiayi Fan & Andrew T. Moreno & Alexander S. Baier & Joseph J. Loparo & Craig L. Peterson, 2022. "H2A.Z deposition by SWR1C involves multiple ATP-dependent steps," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34861-x
    DOI: 10.1038/s41467-022-34861-x
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    References listed on IDEAS

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    1. Istvan Albert & Travis N. Mavrich & Lynn P. Tomsho & Ji Qi & Sara J. Zanton & Stephan C. Schuster & B. Franklin Pugh, 2007. "Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome," Nature, Nature, vol. 446(7135), pages 572-576, March.
    2. Meijing Li & Xian Xia & Yuanyuan Tian & Qi Jia & Xiaoyu Liu & Ying Lu & Ming Li & Xueming Li & Zhucheng Chen, 2019. "Mechanism of DNA translocation underlying chromatin remodelling by Snf2," Nature, Nature, vol. 567(7748), pages 409-413, March.
    3. Timothy R. Blosser & Janet G. Yang & Michael D. Stone & Geeta J. Narlikar & Xiaowei Zhuang, 2009. "Dynamics of nucleosome remodelling by individual ACF complexes," Nature, Nature, vol. 462(7276), pages 1022-1027, December.
    4. 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.
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