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An embryonic stem cell-specific heterochromatin state promotes core histone exchange in the absence of DNA accessibility

Author

Listed:
  • Carmen Navarro

    (Karolinska Institutet
    Stockholm node, Karolinska Institutet)

  • Jing Lyu

    (Karolinska Institutet
    Stockholm node, Karolinska Institutet)

  • Anna-Maria Katsori

    (Karolinska Institutet
    Stockholm node, Karolinska Institutet)

  • Rozina Caridha

    (Karolinska Institutet
    Stockholm node, Karolinska Institutet)

  • Simon J. Elsässer

    (Karolinska Institutet
    Stockholm node, Karolinska Institutet)

Abstract

Nucleosome turnover concomitant with incorporation of the replication-independent histone variant H3.3 is a hallmark of regulatory regions in the animal genome. Nucleosome turnover is known to be universally linked to DNA accessibility and histone acetylation. In mouse embryonic stem cells, H3.3 is also highly enriched at interstitial heterochromatin, most prominently at intracisternal A-particle endogenous retroviral elements. Interstitial heterochromatin is established over confined domains by the TRIM28-KAP1/SETDB1 corepressor complex and has stereotypical features of repressive chromatin, such as H3K9me3 and recruitment of all HP1 isoforms. Here, we demonstrate that fast histone turnover and H3.3 incorporation is compatible with these hallmarks of heterochromatin. Further, we find that Smarcad1 chromatin remodeler evicts nucleosomes generating accessible DNA. Free DNA is repackaged via DAXX-mediated nucleosome assembly with histone variant H3.3 in this dynamic heterochromatin state. Loss of H3.3 in mouse embryonic stem cells elicits a highly specific opening of interstitial heterochromatin with minimal effects on other silent or active regions of the genome.

Suggested Citation

  • Carmen Navarro & Jing Lyu & Anna-Maria Katsori & Rozina Caridha & Simon J. Elsässer, 2020. "An embryonic stem cell-specific heterochromatin state promotes core histone exchange in the absence of DNA accessibility," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-18863-1
    DOI: 10.1038/s41467-020-18863-1
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    Cited by:

    1. Yuichi Saito & Akihito Harada & Miho Ushijima & Kaori Tanaka & Ryota Higuchi & Akemi Baba & Daisuke Murakami & Stephen L. Nutt & Takashi Nakagawa & Yasuyuki Ohkawa & Yoshihiro Baba, 2024. "Plasma cell differentiation is regulated by the expression of histone variant H3.3," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    2. Sophia Groh & Anna Viktoria Milton & Lisa Katherina Marinelli & Cara V. Sickinger & Angela Russo & Heike Bollig & Gustavo Pereira de Almeida & Andreas Schmidt & Ignasi Forné & Axel Imhof & Gunnar Scho, 2021. "Morc3 silences endogenous retroviruses by enabling Daxx-mediated histone H3.3 incorporation," Nature Communications, Nature, vol. 12(1), pages 1-18, December.

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