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The nuclear pore primes recombination-dependent DNA synthesis at arrested forks by promoting SUMO removal

Author

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  • Karol Kramarz

    (PSL Research University, UMR3348
    CNRS UMR3348 “Genome integrity, RNA and Cancer”, “Equipe labellisée LIGUE 2020”
    Paris-Saclay University, UMR3348)

  • Kamila Schirmeisen

    (PSL Research University, UMR3348
    CNRS UMR3348 “Genome integrity, RNA and Cancer”, “Equipe labellisée LIGUE 2020”
    Paris-Saclay University, UMR3348)

  • Virginie Boucherit

    (PSL Research University, UMR3348
    CNRS UMR3348 “Genome integrity, RNA and Cancer”, “Equipe labellisée LIGUE 2020”
    Paris-Saclay University, UMR3348)

  • Anissia Ait Saada

    (PSL Research University, UMR3348
    CNRS UMR3348 “Genome integrity, RNA and Cancer”, “Equipe labellisée LIGUE 2020”
    Paris-Saclay University, UMR3348)

  • Claire Lovo

    (PSL Research University, UMR3348
    CNRS UMR3348 “Genome integrity, RNA and Cancer”, “Equipe labellisée LIGUE 2020”)

  • Benoit Palancade

    (CNRS, Institut Jacques Monod)

  • Catherine Freudenreich

    (Tufts University)

  • Sarah A. E. Lambert

    (PSL Research University, UMR3348
    CNRS UMR3348 “Genome integrity, RNA and Cancer”, “Equipe labellisée LIGUE 2020”
    Paris-Saclay University, UMR3348)

Abstract

Nuclear Pore complexes (NPCs) act as docking sites to anchor particular DNA lesions facilitating DNA repair by elusive mechanisms. Using replication fork barriers in fission yeast, we report that relocation of arrested forks to NPCs occurred after Rad51 loading and its enzymatic activity. The E3 SUMO ligase Pli1 acts at arrested forks to safeguard integrity of nascent strands and generates poly-SUMOylation which promote relocation to NPCs but impede the resumption of DNA synthesis by homologous recombination (HR). Anchorage to NPCs allows SUMO removal by the SENP SUMO protease Ulp1 and the proteasome, promoting timely resumption of DNA synthesis. Preventing Pli1-mediated SUMO chains was sufficient to bypass the need for anchorage to NPCs and the inhibitory effect of poly-SUMOylation on HR-mediated DNA synthesis. Our work establishes a novel spatial control of Recombination-Dependent Replication (RDR) at a unique sequence that is distinct from mechanisms engaged at collapsed-forks and breaks within repeated sequences.

Suggested Citation

  • Karol Kramarz & Kamila Schirmeisen & Virginie Boucherit & Anissia Ait Saada & Claire Lovo & Benoit Palancade & Catherine Freudenreich & Sarah A. E. Lambert, 2020. "The nuclear pore primes recombination-dependent DNA synthesis at arrested forks by promoting SUMO removal," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-19516-z
    DOI: 10.1038/s41467-020-19516-z
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    Cited by:

    1. Rishi Kumar Nageshan & Raquel Ortega & Nevan Krogan & Julia Promisel Cooper, 2024. "Fate of telomere entanglements is dictated by the timing of anaphase midregion nuclear envelope breakdown," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. Judith Oehler & Carl A. Morrow & Matthew C. Whitby, 2023. "Gene duplication and deletion caused by over-replication at a fork barrier," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Arianna Penzo & Marion Dubarry & Clémentine Brocas & Myriam Zheng & Raphaël M. Mangione & Mathieu Rougemaille & Coralie Goncalves & Ophélie Lautier & Domenico Libri & Marie-Noëlle Simon & Vincent Géli, 2023. "A R-loop sensing pathway mediates the relocation of transcribed genes to nuclear pore complexes," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

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