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PARP3 is a sensor of nicked nucleosomes and monoribosylates histone H2BGlu2

Author

Listed:
  • Gabrielle J. Grundy

    (Genome Damage and Stability Centre, School of Life Sciences, University of Sussex)

  • Luis M. Polo

    (Cancer Research UK DNA Repair Enzymes Group, Genome Damage and Stability Centre, School of Life Sciences, University of Sussex)

  • Zhihong Zeng

    (Genome Damage and Stability Centre, School of Life Sciences, University of Sussex)

  • Stuart L. Rulten

    (Genome Damage and Stability Centre, School of Life Sciences, University of Sussex)

  • Nicolas C. Hoch

    (Genome Damage and Stability Centre, School of Life Sciences, University of Sussex
    CAPES Foundation, Ministry of Education of Brazil)

  • Pathompong Paomephan

    (Genome Damage and Stability Centre, School of Life Sciences, University of Sussex)

  • Yingqi Xu

    (Cross-faculty NMR centre, Faculty of Natural Sciences, Imperial College London)

  • Steve M. Sweet

    (Genome Damage and Stability Centre, School of Life Sciences, University of Sussex)

  • Alan W. Thorne

    (Institute of Biomedical and Biomolecular Sciences, University of Portsmouth)

  • Antony W. Oliver

    (Cancer Research UK DNA Repair Enzymes Group, Genome Damage and Stability Centre, School of Life Sciences, University of Sussex)

  • Steve J. Matthews

    (Cross-faculty NMR centre, Faculty of Natural Sciences, Imperial College London)

  • Laurence H. Pearl

    (Cancer Research UK DNA Repair Enzymes Group, Genome Damage and Stability Centre, School of Life Sciences, University of Sussex)

  • Keith W. Caldecott

    (Genome Damage and Stability Centre, School of Life Sciences, University of Sussex)

Abstract

PARP3 is a member of the ADP-ribosyl transferase superfamily that we show accelerates the repair of chromosomal DNA single-strand breaks in avian DT40 cells. Two-dimensional nuclear magnetic resonance experiments reveal that PARP3 employs a conserved DNA-binding interface to detect and stably bind DNA breaks and to accumulate at sites of chromosome damage. PARP3 preferentially binds to and is activated by mononucleosomes containing nicked DNA and which target PARP3 trans-ribosylation activity to a single-histone substrate. Although nicks in naked DNA stimulate PARP3 autoribosylation, nicks in mononucleosomes promote the trans-ribosylation of histone H2B specifically at Glu2. These data identify PARP3 as a molecular sensor of nicked nucleosomes and demonstrate, for the first time, the ribosylation of chromatin at a site-specific DNA single-strand break.

Suggested Citation

  • Gabrielle J. Grundy & Luis M. Polo & Zhihong Zeng & Stuart L. Rulten & Nicolas C. Hoch & Pathompong Paomephan & Yingqi Xu & Steve M. Sweet & Alan W. Thorne & Antony W. Oliver & Steve J. Matthews & Lau, 2016. "PARP3 is a sensor of nicked nucleosomes and monoribosylates histone H2BGlu2," Nature Communications, Nature, vol. 7(1), pages 1-12, November.
    • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms12404
    DOI: 10.1038/ncomms12404
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    Cited by:

    1. Edoardo José Longarini & Ivan Matić, 2024. "Preserving ester-linked modifications reveals glutamate and aspartate mono-ADP-ribosylation by PARP1 and its reversal by PARG," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Zhen Huang & Ivanete De O. Furo & Jing Liu & Valentina Peona & Anderson J. B. Gomes & Wan Cen & Hao Huang & Yanding Zhang & Duo Chen & Ting Xue & Qiujin Zhang & Zhicao Yue & Quanxi Wang & Lingyu Yu & , 2022. "Recurrent chromosome reshuffling and the evolution of neo-sex chromosomes in parrots," Nature Communications, Nature, vol. 13(1), pages 1-11, December.

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