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ANP32E is a histone chaperone that removes H2A.Z from chromatin

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  • Arnaud Obri

    (Institut de Génétique et Biologie Moléculaire et Cellulaire (IGBMC), Université de Strasbourg, CNRS, INSERM, 1 rue Laurent Fries, B.P. 10142, 67404 Illkirch Cedex, France)

  • Khalid Ouararhni

    (Institut de Génétique et Biologie Moléculaire et Cellulaire (IGBMC), Université de Strasbourg, CNRS, INSERM, 1 rue Laurent Fries, B.P. 10142, 67404 Illkirch Cedex, France)

  • Christophe Papin

    (Institut de Génétique et Biologie Moléculaire et Cellulaire (IGBMC), Université de Strasbourg, CNRS, INSERM, 1 rue Laurent Fries, B.P. 10142, 67404 Illkirch Cedex, France)

  • Marie-Laure Diebold

    (Institut de Génétique et Biologie Moléculaire et Cellulaire (IGBMC), Université de Strasbourg, CNRS, INSERM, 1 rue Laurent Fries, B.P. 10142, 67404 Illkirch Cedex, France)

  • Kiran Padmanabhan

    (Equipe labélisée Ligue contre le Cancer, INSERM/Université Joseph Fourier , Institut Albert Bonniot, U823, Site Santé-BP 170, 38042 Grenoble Cedex 9, France)

  • Martin Marek

    (Institut de Génétique et Biologie Moléculaire et Cellulaire (IGBMC), Université de Strasbourg, CNRS, INSERM, 1 rue Laurent Fries, B.P. 10142, 67404 Illkirch Cedex, France)

  • Isabelle Stoll

    (Institut de Génétique et Biologie Moléculaire et Cellulaire (IGBMC), Université de Strasbourg, CNRS, INSERM, 1 rue Laurent Fries, B.P. 10142, 67404 Illkirch Cedex, France)

  • Ludovic Roy

    (Institut de Génétique et Biologie Moléculaire et Cellulaire (IGBMC), Université de Strasbourg, CNRS, INSERM, 1 rue Laurent Fries, B.P. 10142, 67404 Illkirch Cedex, France)

  • Patrick T. Reilly

    (Laboratory of Inflammation Biology, National Cancer Centre)

  • Tak W. Mak

    (Laboratory of Inflammation Biology, National Cancer Centre
    The Campbell Family Institute for Breast Cancer Research, University Health Network, Toronto, Ontario, Canada)

  • Stefan Dimitrov

    (Equipe labélisée Ligue contre le Cancer, INSERM/Université Joseph Fourier , Institut Albert Bonniot, U823, Site Santé-BP 170, 38042 Grenoble Cedex 9, France)

  • Christophe Romier

    (Institut de Génétique et Biologie Moléculaire et Cellulaire (IGBMC), Université de Strasbourg, CNRS, INSERM, 1 rue Laurent Fries, B.P. 10142, 67404 Illkirch Cedex, France)

  • Ali Hamiche

    (Institut de Génétique et Biologie Moléculaire et Cellulaire (IGBMC), Université de Strasbourg, CNRS, INSERM, 1 rue Laurent Fries, B.P. 10142, 67404 Illkirch Cedex, France)

Abstract

H2A.Z is an essential histone variant implicated in the regulation of key nuclear events. However, the metazoan chaperones responsible for H2A.Z deposition and its removal from chromatin remain unknown. Here we report the identification and characterization of the human protein ANP32E as a specific H2A.Z chaperone. We show that ANP32E is a member of the presumed H2A.Z histone-exchange complex p400/TIP60. ANP32E interacts with a short region of the docking domain of H2A.Z through a new motif termed H2A.Z interacting domain (ZID). The 1.48 Å resolution crystal structure of the complex formed between the ANP32E-ZID and the H2A.Z/H2B dimer and biochemical data support an underlying molecular mechanism for H2A.Z/H2B eviction from the nucleosome and its stabilization by ANP32E through a specific extension of the H2A.Z carboxy-terminal α-helix. Finally, analysis of H2A.Z localization in ANP32E−/− cells by chromatin immunoprecipitation followed by sequencing shows genome-wide enrichment, redistribution and accumulation of H2A.Z at specific chromatin control regions, in particular at enhancers and insulators.

Suggested Citation

  • Arnaud Obri & Khalid Ouararhni & Christophe Papin & Marie-Laure Diebold & Kiran Padmanabhan & Martin Marek & Isabelle Stoll & Ludovic Roy & Patrick T. Reilly & Tak W. Mak & Stefan Dimitrov & Christoph, 2014. "ANP32E is a histone chaperone that removes H2A.Z from chromatin," Nature, Nature, vol. 505(7485), pages 648-653, January.
  • Handle: RePEc:nat:nature:v:505:y:2014:i:7485:d:10.1038_nature12922
    DOI: 10.1038/nature12922
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    Cited by:

    1. Christopher J. Gilbert & Charles P. Rabolli & Volha A. Golubeva & Kristina M. Sattler & Meifang Wang & Arsh Ketabforoush & W. David Arnold & Christoph Lepper & Federica Accornero, 2024. "YTHDF2 governs muscle size through a targeted modulation of proteostasis," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    2. Wenqi Sun & Qianhua Dong & Xueqing Li & Jinxin Gao & Xianwen Ye & Chunyi Hu & Fei Li & Yong Chen, 2024. "The SUN-family protein Sad1 mediates heterochromatin spatial organization through interaction with histone H2A-H2B," Nature Communications, Nature, vol. 15(1), pages 1-13, December.

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