IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38048-w.html
   My bibliography  Save this article

DNA-binding mechanism and evolution of replication protein A

Author

Listed:
  • Clément Madru

    (Institut Pasteur, Université Paris Cité, CNRS)

  • Markel Martínez-Carranza

    (Institut Pasteur, Université Paris Cité, CNRS)

  • Sébastien Laurent

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

  • Alessandra C. Alberti

    (Institut Pasteur, Université Paris Cité, CNRS)

  • Maelenn Chevreuil

    (C2RT, Institut Pasteur, Université Paris Cité, CNRS)

  • Bertrand Raynal

    (C2RT, Institut Pasteur, Université Paris Cité, CNRS)

  • Ahmed Haouz

    (C2RT, Institut Pasteur, Université Paris Cité, CNRS)

  • Rémy A. Meur

    (C2RT, Institut Pasteur, Université Paris Cité, CNRS)

  • Marc Delarue

    (Institut Pasteur, Université Paris Cité, CNRS)

  • Ghislaine Henneke

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

  • Didier Flament

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

  • Mart Krupovic

    (Institut Pasteur, Université Paris Cité, CNRS)

  • Pierre Legrand

    (Institut Pasteur, Université Paris Cité, CNRS
    Synchrotron SOLEIL, HelioBio group, L’Orme des Merisiers)

  • Ludovic Sauguet

    (Institut Pasteur, Université Paris Cité, CNRS)

Abstract

Replication Protein A (RPA) is a heterotrimeric single stranded DNA-binding protein with essential roles in DNA replication, recombination and repair. Little is known about the structure of RPA in Archaea, the third domain of life. By using an integrative structural, biochemical and biophysical approach, we extensively characterize RPA from Pyrococcus abyssi in the presence and absence of DNA. The obtained X-ray and cryo-EM structures reveal that the trimerization core and interactions promoting RPA clustering on ssDNA are shared between archaea and eukaryotes. However, we also identified a helical domain named AROD (Acidic Rpa1 OB-binding Domain), and showed that, in Archaea, RPA forms an unanticipated tetrameric supercomplex in the absence of DNA. The four RPA molecules clustered within the tetramer could efficiently coat and protect stretches of ssDNA created by the advancing replisome. Finally, our results provide insights into the evolution of this primordial replication factor in eukaryotes.

Suggested Citation

  • 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.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38048-w
    DOI: 10.1038/s41467-023-38048-w
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38048-w
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-38048-w?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Kathryn Tunyasuvunakool & Jonas Adler & Zachary Wu & Tim Green & Michal Zielinski & Augustin Žídek & Alex Bridgland & Andrew Cowie & Clemens Meyer & Agata Laydon & Sameer Velankar & Gerard J. Kleywegt, 2021. "Highly accurate protein structure prediction for the human proteome," Nature, Nature, vol. 596(7873), pages 590-596, August.
    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. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
    4. Luke A. Yates & Ricardo J. Aramayo & Nilisha Pokhrel & Colleen C. Caldwell & Joshua A. Kaplan & Rajika L. Perera & Maria Spies & Edwin Antony & Xiaodong Zhang, 2018. "A structural and dynamic model for the assembly of Replication Protein A on single-stranded DNA," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    5. Anja Spang & Jimmy H. Saw & Steffen L. Jørgensen & Katarzyna Zaremba-Niedzwiedzka & Joran Martijn & Anders E. Lind & Roel van Eijk & Christa Schleper & Lionel Guy & Thijs J. G. Ettema, 2015. "Complex archaea that bridge the gap between prokaryotes and eukaryotes," Nature, Nature, vol. 521(7551), pages 173-179, May.
    6. Yang Liu & Kira S. Makarova & Wen-Cong Huang & Yuri I. Wolf & Anastasia N. Nikolskaya & Xinxu Zhang & Mingwei Cai & Cui-Jing Zhang & Wei Xu & Zhuhua Luo & Lei Cheng & Eugene V. Koonin & Meng Li, 2021. "Expanded diversity of Asgard archaea and their relationships with eukaryotes," Nature, Nature, vol. 593(7860), pages 553-557, May.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. 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.
    2. David Moi & Shunsuke Nishio & Xiaohui Li & Clari Valansi & Mauricio Langleib & Nicolas G. Brukman & Kateryna Flyak & Christophe Dessimoz & Daniele de Sanctis & Kathryn Tunyasuvunakool & John Jumper & , 2022. "Discovery of archaeal fusexins homologous to eukaryotic HAP2/GCS1 gamete fusion proteins," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    3. Tomoyuki Hatano & Saravanan Palani & Dimitra Papatziamou & Ralf Salzer & Diorge P. Souza & Daniel Tamarit & Mehul Makwana & Antonia Potter & Alexandra Haig & Wenjue Xu & David Townsend & David Rochest, 2022. "Asgard archaea shed light on the evolutionary origins of the eukaryotic ubiquitin-ESCRT machinery," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    4. Pierre Azoulay & Joshua Krieger & Abhishek Nagaraj, 2024. "Old Moats for New Models: Openness, Control, and Competition in Generative AI," NBER Chapters, in: Entrepreneurship and Innovation Policy and the Economy, volume 4, National Bureau of Economic Research, Inc.
    5. Deyun Qiu & Jinxin V. Pei & James E. O. Rosling & Vandana Thathy & Dongdi Li & Yi Xue & John D. Tanner & Jocelyn Sietsma Penington & Yi Tong Vincent Aw & Jessica Yi Han Aw & Guoyue Xu & Abhai K. Tripa, 2022. "A G358S mutation in the Plasmodium falciparum Na+ pump PfATP4 confers clinically-relevant resistance to cipargamin," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    6. Shuo-Shuo Liu & Tian-Xia Jiang & Fan Bu & Ji-Lan Zhao & Guang-Fei Wang & Guo-Heng Yang & Jie-Yan Kong & Yun-Fan Qie & Pei Wen & Li-Bin Fan & Ning-Ning Li & Ning Gao & Xiao-Bo Qiu, 2024. "Molecular mechanisms underlying the BIRC6-mediated regulation of apoptosis and autophagy," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    7. Xiaoke Yang & Mingqi Zhu & Xue Lu & Yuxin Wang & Junyu Xiao, 2024. "Architecture and activation of human muscle phosphorylase kinase," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    8. Efren Garcia-Maldonado & Andrew D. Huber & Sergio C. Chai & Stanley Nithianantham & Yongtao Li & Jing Wu & Shyaron Poudel & Darcie J. Miller & Jayaraman Seetharaman & Taosheng Chen, 2024. "Chemical manipulation of an activation/inhibition switch in the nuclear receptor PXR," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    9. Kristy Rochon & Brianna L. Bauer & Nathaniel A. Roethler & Yuli Buckley & Chih-Chia Su & Wei Huang & Rajesh Ramachandran & Maria S. K. Stoll & Edward W. Yu & Derek J. Taylor & Jason A. Mears, 2024. "Structural basis for regulated assembly of the mitochondrial fission GTPase Drp1," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    10. Fan Lu & Liang Zhu & Thomas Bromberger & Jun Yang & Qiannan Yang & Jianmin Liu & Edward F. Plow & Markus Moser & Jun Qin, 2022. "Mechanism of integrin activation by talin and its cooperation with kindlin," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    11. Martin F. Peter & Christian Gebhardt & Rebecca Mächtel & Gabriel G. Moya Muñoz & Janin Glaenzer & Alessandra Narducci & Gavin H. Thomas & Thorben Cordes & Gregor Hagelueken, 2022. "Cross-validation of distance measurements in proteins by PELDOR/DEER and single-molecule FRET," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    12. Jutta Diessl & Jens Berndtsson & Filomena Broeskamp & Lukas Habernig & Verena Kohler & Carmela Vazquez-Calvo & Arpita Nandy & Carlotta Peselj & Sofia Drobysheva & Ludovic Pelosi & F.-Nora Vögtle & Fab, 2022. "Manganese-driven CoQ deficiency," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    13. Alexander Kroll & Sahasra Ranjan & Martin K. M. Engqvist & Martin J. Lercher, 2023. "A general model to predict small molecule substrates of enzymes based on machine and deep learning," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    14. Lisa-Marie Appel & Vedran Franke & Johannes Benedum & Irina Grishkovskaya & Xué Strobl & Anton Polyansky & Gregor Ammann & Sebastian Platzer & Andrea Neudolt & Anna Wunder & Lena Walch & Stefanie Kais, 2023. "The SPOC domain is a phosphoserine binding module that bridges transcription machinery with co- and post-transcriptional regulators," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    15. Maciej K. Kocylowski & Hande Aypek & Wolfgang Bildl & Martin Helmstädter & Philipp Trachte & Bernhard Dumoulin & Sina Wittösch & Lukas Kühne & Ute Aukschun & Carolin Teetzen & Oliver Kretz & Botond Ga, 2022. "A slit-diaphragm-associated protein network for dynamic control of renal filtration," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    16. Jonathan Filée & Hubert F. Becker & Lucille Mellottee & Rima Zein Eddine & Zhihui Li & Wenlu Yin & Jean-Christophe Lambry & Ursula Liebl & Hannu Myllykallio, 2023. "Bacterial origins of thymidylate metabolism in Asgard archaea and Eukarya," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    17. Michael A. Longo & Sunetra Roy & Yue Chen & Karl-Heinz Tomaszowski & Andrew S. Arvai & Jordan T. Pepper & Rebecca A. Boisvert & Selvi Kunnimalaiyaan & Caezanne Keshvani & David Schild & Albino Bacolla, 2023. "RAD51C-XRCC3 structure and cancer patient mutations define DNA replication roles," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    18. Zachary C. Drake & Justin T. Seffernick & Steffen Lindert, 2022. "Protein complex prediction using Rosetta, AlphaFold, and mass spectrometry covalent labeling," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    19. Karin Vogel & Tobias Bläske & Marie-Kristin Nagel & Christoph Globisch & Shane Maguire & Lorenz Mattes & Christian Gude & Michael Kovermann & Karin Hauser & Christine Peter & Erika Isono, 2022. "Lipid-mediated activation of plasma membrane-localized deubiquitylating enzymes modulate endosomal trafficking," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    20. Robin Anger & Laetitia Pieulle & Meriam Shahin & Odile Valette & Hugo Guenno & Artemis Kosta & Vladimir Pelicic & Rémi Fronzes, 2023. "Structure of a heteropolymeric type 4 pilus from a monoderm bacterium," Nature Communications, Nature, vol. 14(1), pages 1-11, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38048-w. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.