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Structural basis of nucleosome assembly by the Abo1 AAA+ ATPase histone chaperone

Author

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  • Carol Cho

    (Korea Advanced Institute of Science and Technology (KAIST))

  • Juwon Jang

    (Korea Advanced Institute of Science and Technology (KAIST))

  • Yujin Kang

    (Ulsan National Institute of Science and Technology)

  • Hiroki Watanabe

    (National Institutes of Natural Sciences
    National Institutes of Natural Sciences)

  • Takayuki Uchihashi

    (National Institutes of Natural Sciences
    Nagoya University)

  • Seung Joong Kim

    (Korea Advanced Institute of Science and Technology (KAIST))

  • Koichi Kato

    (National Institutes of Natural Sciences
    National Institutes of Natural Sciences
    Nagoya City University)

  • Ja Yil Lee

    (Ulsan National Institute of Science and Technology)

  • Ji-Joon Song

    (Korea Advanced Institute of Science and Technology (KAIST))

Abstract

The fundamental unit of chromatin, the nucleosome, is an intricate structure that requires histone chaperones for assembly. ATAD2 AAA+ ATPases are a family of histone chaperones that regulate nucleosome density and chromatin dynamics. Here, we demonstrate that the fission yeast ATAD2 homolog, Abo1, deposits histone H3–H4 onto DNA in an ATP-hydrolysis-dependent manner by in vitro reconstitution and single-tethered DNA curtain assays. We present cryo-EM structures of an ATAD2 family ATPase to atomic resolution in three different nucleotide states, revealing unique structural features required for histone loading on DNA, and directly visualize the transitions of Abo1 from an asymmetric spiral (ATP-state) to a symmetric ring (ADP- and apo-states) using high-speed atomic force microscopy (HS-AFM). Furthermore, we find that the acidic pore of ATP-Abo1 binds a peptide substrate which is suggestive of a histone tail. Based on these results, we propose a model whereby Abo1 facilitates H3–H4 loading by utilizing ATP.

Suggested Citation

  • Carol Cho & Juwon Jang & Yujin Kang & Hiroki Watanabe & Takayuki Uchihashi & Seung Joong Kim & Koichi Kato & Ja Yil Lee & Ji-Joon Song, 2019. "Structural basis of nucleosome assembly by the Abo1 AAA+ ATPase histone chaperone," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-13743-9
    DOI: 10.1038/s41467-019-13743-9
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    Cited by:

    1. Ian Cooney & Heidi L. Schubert & Karina Cedeno & Olivia N. Fisher & Richard Carson & John C. Price & Christopher P. Hill & Peter S. Shen, 2024. "Visualization of the Cdc48 AAA+ ATPase protein unfolding pathway," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    2. Nathaniel G. Jones & Vincent Geoghegan & Gareth Moore & Juliana B. T. Carnielli & Katherine Newling & Félix Calderón & Raquel Gabarró & Julio Martín & Rab K. Prinjha & Inmaculada Rioja & Anthony J. Wi, 2022. "Bromodomain factor 5 is an essential regulator of transcription in Leishmania," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    3. Yang Xu & Han Han & Ian Cooney & Yuxuan Guo & Noah G. Moran & Nathan R. Zuniga & John C. Price & Christopher P. Hill & Peter S. Shen, 2022. "Active conformation of the p97-p47 unfoldase complex," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    4. Yangang Pan & Jingyu Zhan & Yining Jiang & Di Xia & Simon Scheuring, 2023. "A concerted ATPase cycle of the protein transporter AAA-ATPase Bcs1," Nature Communications, Nature, vol. 14(1), pages 1-13, December.

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