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Communication between DNA polymerases and Replication Protein A within the archaeal replisome

Author

Listed:
  • Markel Martínez-Carranza

    (Université Paris Cité, CNRS UMR 3528)

  • Léa Vialle

    (Univ Brest, Ifremer, CNRS, Biologie et Ecologie des Ecoystèmes marins profonds (BEEP))

  • Clément Madru

    (Université Paris Cité, CNRS UMR 3528)

  • Florence Cordier

    (Université Paris Cité, CNRS UMR 3528
    Université Paris Cité, CNRS UMR 3528)

  • Ayten Dizkirici Tekpinar

    (Université Paris Cité, CNRS UMR 3528
    Van Yüzüncü Yil University)

  • Ahmed Haouz

    (Université Paris Cité, CNRS UMR 3528)

  • Pierre Legrand

    (L’Orme des Merisiers)

  • Rémy A. Meur

    (Université Paris Cité, CNRS UMR 3528)

  • Patrick England

    (Université Paris Cité, CNRS UMR 3528)

  • Rémi Dulermo

    (Univ Brest, Ifremer, CNRS, Biologie et Ecologie des Ecoystèmes marins profonds (BEEP))

  • J. Iñaki Guijarro

    (Université Paris Cité, CNRS UMR 3528)

  • Ghislaine Henneke

    (Univ Brest, Ifremer, CNRS, Biologie et Ecologie des Ecoystèmes marins profonds (BEEP))

  • Ludovic Sauguet

    (Université Paris Cité, CNRS UMR 3528)

Abstract

Replication Protein A (RPA) plays a pivotal role in DNA replication by coating and protecting exposed single-stranded DNA, and acting as a molecular hub that recruits additional replication factors. We demonstrate that archaeal RPA hosts a winged-helix domain (WH) that interacts with two key actors of the replisome: the DNA primase (PriSL) and the replicative DNA polymerase (PolD). Using an integrative structural biology approach, combining nuclear magnetic resonance, X-ray crystallography and cryo-electron microscopy, we unveil how RPA interacts with PriSL and PolD through two distinct surfaces of the WH domain: an evolutionarily conserved interface and a novel binding site. Finally, RPA is shown to stimulate the activity of PriSL in a WH-dependent manner. This study provides a molecular understanding of the WH-mediated regulatory activity in central replication factors such as RPA, which regulate genome maintenance in Archaea and Eukaryotes.

Suggested Citation

  • Markel Martínez-Carranza & Léa Vialle & Clément Madru & Florence Cordier & Ayten Dizkirici Tekpinar & Ahmed Haouz & Pierre Legrand & Rémy A. Meur & Patrick England & Rémi Dulermo & J. Iñaki Guijarro &, 2024. "Communication between DNA polymerases and Replication Protein A within the archaeal replisome," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-55365-w
    DOI: 10.1038/s41467-024-55365-w
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    References listed on IDEAS

    as
    1. Clément Madru & Ghislaine Henneke & Pierre Raia & Inès Hugonneau-Beaufet & Gérard Pehau-Arnaudet & Patrick England & Erik Lindahl & Marc Delarue & Marta Carroni & Ludovic Sauguet, 2020. "Structural basis for the increased processivity of D-family DNA polymerases in complex with PCNA," Nature Communications, Nature, vol. 11(1), pages 1-12, December.
    2. Qixiang He & Xiuhua Lin & Bianca L. Chavez & Sourav Agrawal & Benjamin L. Lusk & Ci Ji Lim, 2022. "Structures of the human CST-Polα–primase complex bound to telomere templates," Nature, Nature, vol. 608(7924), pages 826-832, August.
    3. Mark D. Greci & Joseph D. Dooher & Stephen D. Bell, 2022. "The combined DNA and RNA synthetic capabilities of archaeal DNA primase facilitate primer hand-off to the replicative DNA polymerase," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    4. Sung-Ho Bae & Kwang-Hee Bae & Jung-Ae Kim & Yeon-Soo Seo, 2001. "RPA governs endonuclease switching during processing of Okazaki fragments in eukaryotes," Nature, Nature, vol. 412(6845), pages 456-461, July.
    5. Leonardo Betancurt-Anzola & Markel Martínez-Carranza & Marc Delarue & Kelly M. Zatopek & Andrew F. Gardner & Ludovic Sauguet, 2023. "Molecular basis for proofreading by the unique exonuclease domain of Family-D DNA polymerases," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    6. Clément Madru & Markel Martínez-Carranza & Sébastien Laurent & Alessandra C. Alberti & Maelenn Chevreuil & Bertrand Raynal & Ahmed Haouz & Rémy A. Meur & Marc Delarue & Ghislaine Henneke & Didier Flam, 2023. "DNA-binding mechanism and evolution of replication protein A," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    7. Jiawei Ding & Xiangting Li & Jiangchuan Shen & Yiling Zhao & Shuchen Zhong & Luhua Lai & Hengyao Niu & Zhi Qi, 2023. "ssDNA accessibility of Rad51 is regulated by orchestrating multiple RPA dynamics," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    8. Ludovic Sauguet & Pierre Raia & Ghislaine Henneke & Marc Delarue, 2016. "Shared active site architecture between archaeal PolD and multi-subunit RNA polymerases revealed by X-ray crystallography," Nature Communications, Nature, vol. 7(1), pages 1-12, November.
    9. Chih-Chao Liang & Luke A. Greenhough & Laura Masino & Sarah Maslen & Ilirjana Bajrami & Marcel Tuppi & Mark Skehel & Ian A. Taylor & Stephen C. West, 2024. "Mechanism of single-stranded DNA annealing by RAD52–RPA complex," Nature, Nature, vol. 629(8012), pages 697-703, May.
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