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Retroviral integration into nucleosomes through DNA looping and sliding along the histone octamer

Author

Listed:
  • Marcus D. Wilson

    (The Francis Crick Institute
    University of Edinburgh)

  • Ludovic Renault

    (The Francis Crick Institute
    University of Leiden)

  • Daniel P. Maskell

    (The Francis Crick Institute
    Faculty of Biological Sciences)

  • Mohamed Ghoneim

    (MRC London Institute for Medical Science
    Imperial College London)

  • Valerie E. Pye

    (The Francis Crick Institute)

  • Andrea Nans

    (The Francis Crick Institute)

  • David S. Rueda

    (MRC London Institute for Medical Science
    Imperial College London)

  • Peter Cherepanov

    (The Francis Crick Institute
    St-Maryʹs Campus, Norfolk Place)

  • Alessandro Costa

    (The Francis Crick Institute)

Abstract

Retroviral integrase can efficiently utilise nucleosomes for insertion of the reverse-transcribed viral DNA. In face of the structural constraints imposed by the nucleosomal structure, integrase gains access to the scissile phosphodiester bonds by lifting DNA off the histone octamer at the site of integration. To clarify the mechanism of DNA looping by integrase, we determined a 3.9 Å resolution structure of the prototype foamy virus intasome engaged with a nucleosome core particle. The structural data along with complementary single-molecule Förster resonance energy transfer measurements reveal twisting and sliding of the nucleosomal DNA arm proximal to the integration site. Sliding the nucleosomal DNA by approximately two base pairs along the histone octamer accommodates the necessary DNA lifting from the histone H2A-H2B subunits to allow engagement with the intasome. Thus, retroviral integration into nucleosomes involves the looping-and-sliding mechanism for nucleosomal DNA repositioning, bearing unexpected similarities to chromatin remodelers.

Suggested Citation

  • Marcus D. Wilson & Ludovic Renault & Daniel P. Maskell & Mohamed Ghoneim & Valerie E. Pye & Andrea Nans & David S. Rueda & Peter Cherepanov & Alessandro Costa, 2019. "Retroviral integration into nucleosomes through DNA looping and sliding along the histone octamer," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-12007-w
    DOI: 10.1038/s41467-019-12007-w
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    Cited by:

    1. Guillermo Abascal-Palacios & Laura Jochem & Carlos Pla-Prats & Fabienne Beuron & Alessandro Vannini, 2021. "Structural basis of Ty3 retrotransposon integration at RNA Polymerase III-transcribed genes," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    2. Gayan Senavirathne & James London & Anne Gardner & Richard Fishel & Kristine E. Yoder, 2023. "DNA strand breaks and gaps target retroviral intasome binding and integration," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Allison Ballandras-Colas & Vidya Chivukula & Dominika T. Gruszka & Zelin Shan & Parmit K. Singh & Valerie E. Pye & Rebecca K. McLean & Gregory J. Bedwell & Wen Li & Andrea Nans & Nicola J. Cook & Hind, 2022. "Multivalent interactions essential for lentiviral integrase function," Nature Communications, Nature, vol. 13(1), pages 1-16, December.

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