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Epigenetic modulation via the C-terminal tail of H2A.Z

Author

Listed:
  • László Imre

    (Faculty of Medicine, University of Debrecen)

  • Péter Nánási

    (Faculty of Medicine, University of Debrecen)

  • Ibtissem Benhamza

    (Faculty of Medicine, University of Debrecen)

  • Kata Nóra Enyedi

    (Institute of Chemistry, Eötvös Loránd University
    Supported Research Groups, Research Group of Peptide Chemistry)

  • Gábor Mocsár

    (Department of Biophysics and Cell Biology, University of Debrecen, Faculty of Medicine)

  • Rosevalentine Bosire

    (Faculty of Medicine, University of Debrecen)

  • Éva Hegedüs

    (Faculty of Medicine, University of Debrecen)

  • Erfaneh Firouzi Niaki

    (Faculty of Medicine, University of Debrecen)

  • Ágota Csóti

    (Faculty of Medicine, University of Debrecen)

  • Zsuzsanna Darula

    (Hungarian Centre of Excellence for Molecular Medicine
    HUN-REN Biological Research Centre)

  • Éva Csősz

    (Faculty of Medicine, University of Debrecen)

  • Szilárd Póliska

    (Faculty of Medicine, University of Debrecen)

  • Beáta Scholtz

    (Faculty of Medicine, University of Debrecen)

  • Gábor Mező

    (Institute of Chemistry, Eötvös Loránd University
    Supported Research Groups, Research Group of Peptide Chemistry)

  • Zsolt Bacsó

    (Faculty of Medicine, University of Debrecen)

  • H. T. Marc Timmers

    (Medical Center-University of Freiburg)

  • Masayuki Kusakabe

    (Kobe University)

  • Margit Balázs

    (Faculty of Medicine, University of Debrecen)

  • György Vámosi

    (Faculty of Medicine, University of Debrecen)

  • Juan Ausio

    (University of Victoria)

  • Peter Cheung

    (York University)

  • Katalin Tóth

    (Faculty of Medicine, University of Debrecen)

  • David Tremethick

    (The Australian National University)

  • Masahiko Harata

    (Graduate School of Agricultural Science, Tohoku University)

  • Gábor Szabó

    (Faculty of Medicine, University of Debrecen)

Abstract

H2A.Z-nucleosomes are present in both euchromatin and heterochromatin and it has proven difficult to interpret their disparate roles in the context of their stability features. Using an in situ assay of nucleosome stability and DT40 cells expressing engineered forms of the histone variant we show that native H2A.Z, but not C-terminally truncated H2A.Z (H2A.Z∆C), is released from nucleosomes of peripheral heterochromatin at unusually high salt concentrations. H2A.Z and H3K9me3 landscapes are reorganized in H2A.Z∆C-nuclei and overall sensitivity of chromatin to nucleases is increased. These tail-dependent differences are recapitulated upon treatment of HeLa nuclei with the H2A.Z-tail-peptide (C9), with MNase sensitivity being increased genome-wide. Fluorescence correlation spectroscopy revealed C9 binding to reconstituted nucleosomes. When introduced into live cells, C9 elicited chromatin reorganization, overall nucleosome destabilization and changes in gene expression. Thus, H2A.Z-nucleosomes influence global chromatin architecture in a tail-dependent manner, what can be modulated by introducing the tail-peptide into live cells.

Suggested Citation

  • László Imre & Péter Nánási & Ibtissem Benhamza & Kata Nóra Enyedi & Gábor Mocsár & Rosevalentine Bosire & Éva Hegedüs & Erfaneh Firouzi Niaki & Ágota Csóti & Zsuzsanna Darula & Éva Csősz & Szilárd Pól, 2024. "Epigenetic modulation via the C-terminal tail of H2A.Z," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53514-9
    DOI: 10.1038/s41467-024-53514-9
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    References listed on IDEAS

    as
    1. Lauren Cole & Sebastian Kurscheid & Maxim Nekrasov & Renae Domaschenz & Daniel L. Vera & Jonathan H. Dennis & David J. Tremethick, 2021. "Multiple roles of H2A.Z in regulating promoter chromatin architecture in human cells," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    2. Sergei Rudnizky & Adaiah Bavly & Omri Malik & Lilach Pnueli & Philippa Melamed & Ariel Kaplan, 2016. "H2A.Z controls the stability and mobility of nucleosomes to regulate expression of the LH genes," Nature Communications, Nature, vol. 7(1), pages 1-12, December.
    3. Jakub Mieczkowski & April Cook & Sarah K. Bowman & Britta Mueller & Burak H. Alver & Sharmistha Kundu & Aimee M. Deaton & Jennifer A. Urban & Erica Larschan & Peter J. Park & Robert E. Kingston & Mich, 2016. "MNase titration reveals differences between nucleosome occupancy and chromatin accessibility," Nature Communications, Nature, vol. 7(1), pages 1-11, September.
    4. Shuxiang Li & Tiejun Wei & Anna R. Panchenko, 2023. "Histone variant H2A.Z modulates nucleosome dynamics to promote DNA accessibility," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    5. Kristin E. Murphy & Fanju W. Meng & Claire E. Makowski & Patrick J. Murphy, 2020. "Genome-wide chromatin accessibility is restricted by ANP32E," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    6. Haizhen Long & Liwei Zhang & Mengjie Lv & Zengqi Wen & Wenhao Zhang & Xiulan Chen & Peitao Zhang & Tongqing Li & Luyuan Chang & Caiwei Jin & Guozhao Wu & Xi Wang & Fuquan Yang & Jianfeng Pei & Ping Ch, 2020. "H2A.Z facilitates licensing and activation of early replication origins," Nature, Nature, vol. 577(7791), pages 576-581, January.
    7. Alexander Gansen & Suren Felekyan & Ralf Kühnemuth & Kathrin Lehmann & Katalin Tóth & Claus A. M. Seidel & Jörg Langowski, 2018. "High precision FRET studies reveal reversible transitions in nucleosomes between microseconds and minutes," Nature Communications, Nature, vol. 9(1), pages 1-13, December.
    8. Joanna Achinger-Kawecka & Fatima Valdes-Mora & Phuc-Loi Luu & Katherine A. Giles & C. Elizabeth Caldon & Wenjia Qu & Shalima Nair & Sebastian Soto & Warwick J. Locke & Nicole S. Yeo-Teh & Cathryn M. G, 2020. "Epigenetic reprogramming at estrogen-receptor binding sites alters 3D chromatin landscape in endocrine-resistant breast cancer," Nature Communications, Nature, vol. 11(1), pages 1-17, December.
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