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Human centromere repositioning activates transcription and opens chromatin fibre structure

Author

Listed:
  • Catherine Naughton

    (The University of Edinburgh)

  • Covadonga Huidobro

    (The University of Edinburgh)

  • Claudia R. Catacchio

    (The University of Edinburgh
    University of Bari)

  • Adam Buckle

    (The University of Edinburgh)

  • Graeme R. Grimes

    (The University of Edinburgh)

  • Ryu-Suke Nozawa

    (The University of Edinburgh)

  • Stefania Purgato

    (The University of Edinburgh
    University of Bologna)

  • Mariano Rocchi

    (University of Bari)

  • Nick Gilbert

    (The University of Edinburgh)

Abstract

Human centromeres appear as constrictions on mitotic chromosomes and form a platform for kinetochore assembly in mitosis. Biophysical experiments led to a suggestion that repetitive DNA at centromeric regions form a compact scaffold necessary for function, but this was revised when neocentromeres were discovered on non-repetitive DNA. To test whether centromeres have a special chromatin structure we have analysed the architecture of a neocentromere. Centromere repositioning is accompanied by RNA polymerase II recruitment and active transcription to form a decompacted, negatively supercoiled domain enriched in ‘open’ chromatin fibres. In contrast, centromerisation causes a spreading of repressive epigenetic marks to surrounding regions, delimited by H3K27me3 polycomb boundaries and divergent genes. This flanking domain is transcriptionally silent and partially remodelled to form ‘compact’ chromatin, similar to satellite-containing DNA sequences, and exhibits genomic instability. We suggest transcription disrupts chromatin to provide a foundation for kinetochore formation whilst compact pericentromeric heterochromatin generates mechanical rigidity.

Suggested Citation

  • Catherine Naughton & Covadonga Huidobro & Claudia R. Catacchio & Adam Buckle & Graeme R. Grimes & Ryu-Suke Nozawa & Stefania Purgato & Mariano Rocchi & Nick Gilbert, 2022. "Human centromere repositioning activates transcription and opens chromatin fibre structure," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33426-2
    DOI: 10.1038/s41467-022-33426-2
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    References listed on IDEAS

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    1. Adam G. Larson & Daniel Elnatan & Madeline M. Keenen & Michael J. Trnka & Jonathan B. Johnston & Alma L. Burlingame & David A. Agard & Sy Redding & Geeta J. Narlikar, 2017. "Liquid droplet formation by HP1α suggests a role for phase separation in heterochromatin," Nature, Nature, vol. 547(7662), pages 236-240, July.
    2. Flora Paldi & Bonnie Alver & Daniel Robertson & Stephanie A. Schalbetter & Alastair Kerr & David A. Kelly & Jonathan Baxter & Matthew J. Neale & Adele L. Marston, 2020. "Convergent genes shape budding yeast pericentromeres," Nature, Nature, vol. 582(7810), pages 119-123, June.
    3. Oscar Molina & Giulia Vargiu & Maria Alba Abad & Alisa Zhiteneva & A. Arockia Jeyaprakash & Hiroshi Masumoto & Natalay Kouprina & Vladimir Larionov & William C. Earnshaw, 2016. "Epigenetic engineering reveals a balance between histone modifications and transcription in kinetochore maintenance," Nature Communications, Nature, vol. 7(1), pages 1-16, December.
    4. Amy R. Strom & Alexander V. Emelyanov & Mustafa Mir & Dmitry V. Fyodorov & Xavier Darzacq & Gary H. Karpen, 2017. "Phase separation drives heterochromatin domain formation," Nature, Nature, vol. 547(7662), pages 241-245, July.
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