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DNA sequence-dependent formation of heterochromatin nanodomains

Author

Listed:
  • Graeme J. Thorn

    (University of Essex
    Queen Mary University of London)

  • Christopher T. Clarkson

    (University of Essex
    University College London)

  • Anne Rademacher

    (German Cancer Research Center (DKFZ) & Bioquant)

  • Hulkar Mamayusupova

    (University of Essex)

  • Gunnar Schotta

    (Ludwig-Maximilians-University (LMU) Munich)

  • Karsten Rippe

    (German Cancer Research Center (DKFZ) & Bioquant)

  • Vladimir B. Teif

    (University of Essex)

Abstract

The mammalian epigenome contains thousands of heterochromatin nanodomains (HNDs) marked by di- and trimethylation of histone H3 at lysine 9 (H3K9me2/3), which have a typical size of 3–10 nucleosomes. However, what governs HND location and extension is only partly understood. Here, we address this issue by introducing the chromatin hierarchical lattice framework (ChromHL) that predicts chromatin state patterns with single-nucleotide resolution. ChromHL is applied to analyse four HND types in mouse embryonic stem cells that are defined by histone methylases SUV39H1/2 or GLP, transcription factor ADNP or chromatin remodeller ATRX. We find that HND patterns can be computed from PAX3/9, ADNP and LINE1 sequence motifs as nucleation sites and boundaries that are determined by DNA sequence (e.g. CTCF binding sites), cooperative interactions between nucleosomes as well as nucleosome-HP1 interactions. Thus, ChromHL rationalizes how patterns of H3K9me2/3 are established and changed via the activity of protein factors in processes like cell differentiation.

Suggested Citation

  • Graeme J. Thorn & Christopher T. Clarkson & Anne Rademacher & Hulkar Mamayusupova & Gunnar Schotta & Karsten Rippe & Vladimir B. Teif, 2022. "DNA sequence-dependent formation of heterochromatin nanodomains," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-29360-y
    DOI: 10.1038/s41467-022-29360-y
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    References listed on IDEAS

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    1. Andrew Angel & Jie Song & Caroline Dean & Martin Howard, 2011. "A Polycomb-based switch underlying quantitative epigenetic memory," Nature, Nature, vol. 476(7358), pages 105-108, August.
    2. Yin Shen & Feng Yue & David F. McCleary & Zhen Ye & Lee Edsall & Samantha Kuan & Ulrich Wagner & Jesse Dixon & Leonard Lee & Victor V. Lobanenkov & Bing Ren, 2012. "A map of the cis-regulatory sequences in the mouse genome," Nature, Nature, vol. 488(7409), pages 116-120, August.
    3. Yu-Ching Teng & Aishwarya Sundaresan & Ryan O’Hara & Vincent U. Gant & Minhua Li & Sara Martire & Jane N. Warshaw & Amrita Basu & Laura A. Banaszynski, 2021. "ATRX promotes heterochromatin formation to protect cells from G-quadruplex DNA-mediated stress," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    4. Michaela J. Obersriebnig & Emil M. H. Pallesen & Kim Sneppen & Ala Trusina & Geneviève Thon, 2016. "Nucleation and spreading of a heterochromatic domain in fission yeast," Nature Communications, Nature, vol. 7(1), pages 1-11, September.
    5. Michael B. Stadler & Rabih Murr & Lukas Burger & Robert Ivanek & Florian Lienert & Anne Schöler & Erik van Nimwegen & Christiane Wirbelauer & Edward J. Oakeley & Dimos Gaidatzis & Vijay K. Tiwari & Di, 2011. "DNA-binding factors shape the mouse methylome at distal regulatory regions," Nature, Nature, vol. 480(7378), pages 490-495, December.
    6. Veronika Ostapcuk & Fabio Mohn & Sarah H. Carl & Anja Basters & Daniel Hess & Vytautas Iesmantavicius & Lisa Lampersberger & Matyas Flemr & Aparna Pandey & Nicolas H. Thomä & Joerg Betschinger & Marc , 2018. "Activity-dependent neuroprotective protein recruits HP1 and CHD4 to control lineage-specifying genes," Nature, Nature, vol. 557(7707), pages 739-743, May.
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