IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-35060-4.html
   My bibliography  Save this article

Rad52’s DNA annealing activity drives template switching associated with restarted DNA replication

Author

Listed:
  • Anastasiya Kishkevich

    (University of Oxford)

  • Sanjeeta Tamang

    (University of Oxford)

  • Michael O. Nguyen

    (University of Oxford)

  • Judith Oehler

    (University of Oxford)

  • Elena Bulmaga

    (University of Oxford)

  • Christos Andreadis

    (University of Oxford)

  • Carl A. Morrow

    (University of Oxford)

  • Manisha Jalan

    (University of Oxford)

  • Fekret Osman

    (University of Oxford)

  • Matthew C. Whitby

    (University of Oxford)

Abstract

It is thought that many of the simple and complex genomic rearrangements associated with congenital diseases and cancers stem from mistakes made during the restart of collapsed replication forks by recombination enzymes. It is hypothesised that this recombination-mediated restart process transitions from a relatively accurate initiation phase to a less accurate elongation phase characterised by extensive template switching between homologous, homeologous and microhomologous DNA sequences. Using an experimental system in fission yeast, where fork collapse is triggered by a site-specific replication barrier, we show that ectopic recombination, associated with the initiation of recombination-dependent replication (RDR), is driven mainly by the Rad51 recombinase, whereas template switching, during the elongation phase of RDR, relies more on DNA annealing by Rad52. This finding provides both evidence and a mechanistic basis for the transition hypothesis.

Suggested Citation

  • Anastasiya Kishkevich & Sanjeeta Tamang & Michael O. Nguyen & Judith Oehler & Elena Bulmaga & Christos Andreadis & Carl A. Morrow & Manisha Jalan & Fekret Osman & Matthew C. Whitby, 2022. "Rad52’s DNA annealing activity drives template switching associated with restarted DNA replication," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35060-4
    DOI: 10.1038/s41467-022-35060-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-35060-4
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-35060-4?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. Karel Naiman & Eduard Campillo-Funollet & Adam T. Watson & Alice Budden & Izumi Miyabe & Antony M. Carr, 2021. "Replication dynamics of recombination-dependent replication forks," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    2. Yilong Li & Nicola D. Roberts & Jeremiah A. Wala & Ofer Shapira & Steven E. Schumacher & Kiran Kumar & Ekta Khurana & Sebastian Waszak & Jan O. Korbel & James E. Haber & Marcin Imielinski & Joachim We, 2020. "Patterns of somatic structural variation in human cancer genomes," Nature, Nature, vol. 578(7793), pages 112-121, February.
    3. Hong Zan & Connie Tat & Zhifang Qiu & Julia R. Taylor & Justin A. Guerrero & Tian Shen & Paolo Casali, 2017. "Rad52 competes with Ku70/Ku86 for binding to S-region DSB ends to modulate antibody class-switch DNA recombination," Nature Communications, Nature, vol. 8(1), pages 1-16, April.
    4. Catherine E. Smith & Bertrand Llorente & Lorraine S. Symington, 2007. "Template switching during break-induced replication," Nature, Nature, vol. 447(7140), pages 102-105, May.
    5. Saed Mohebi & Ken’Ichi Mizuno & Adam Watson & Antony M. Carr & Johanne M. Murray, 2015. "Checkpoints are blind to replication restart and recombination intermediates that result in gross chromosomal rearrangements," Nature Communications, Nature, vol. 6(1), pages 1-9, May.
    6. Sheroy Minocherhomji & Songmin Ying & Victoria A. Bjerregaard & Sara Bursomanno & Aiste Aleliunaite & Wei Wu & Hocine W. Mankouri & Huahao Shen & Ying Liu & Ian D. Hickson, 2015. "Replication stress activates DNA repair synthesis in mitosis," Nature, Nature, vol. 528(7581), pages 286-290, December.
    7. Natalie Saini & Sreejith Ramakrishnan & Rajula Elango & Sandeep Ayyar & Yu Zhang & Angela Deem & Grzegorz Ira & James E. Haber & Kirill S. Lobachev & Anna Malkova, 2013. "Migrating bubble during break-induced replication drives conservative DNA synthesis," Nature, Nature, vol. 502(7471), pages 389-392, October.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. 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.

    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. Sameer Bikram Shah & Youhang Li & Shibo Li & Qing Hu & Tong Wu & Yanmeng Shi & Tran Nguyen & Isaac Ive & Linda Shi & Hailong Wang & Xiaohua Wu, 2024. "53BP1 deficiency leads to hyperrecombination using break-induced replication (BIR)," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    2. Yi-Li Feng & Qian Liu & Ruo-Dan Chen & Si-Cheng Liu & Zhi-Cheng Huang & Kun-Ming Liu & Xiao-Ying Yang & An-Yong Xie, 2022. "DNA nicks induce mutational signatures associated with BRCA1 deficiency," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    3. 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.
    4. Ronan Broderick & Veronica Cherdyntseva & Jadwiga Nieminuszczy & Eleni Dragona & Maria Kyriakaki & Theodora Evmorfopoulou & Sarantis Gagos & Wojciech Niedzwiedz, 2023. "Pathway choice in the alternative telomere lengthening in neoplasia is dictated by replication fork processing mediated by EXD2’s nuclease activity," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Michelle Dietzen & Haoran Zhai & Olivia Lucas & Oriol Pich & Christopher Barrington & Wei-Ting Lu & Sophia Ward & Yanping Guo & Robert E. Hynds & Simone Zaccaria & Charles Swanton & Nicholas McGranaha, 2024. "Replication timing alterations are associated with mutation acquisition during breast and lung cancer evolution," Nature Communications, Nature, vol. 15(1), pages 1-23, December.
    6. Yasuhiko Haga & Yoshitaka Sakamoto & Keiko Kajiya & Hitomi Kawai & Miho Oka & Noriko Motoi & Masayuki Shirasawa & Masaya Yotsukura & Shun-Ichi Watanabe & Miyuki Arai & Junko Zenkoh & Kouya Shiraishi &, 2023. "Whole-genome sequencing reveals the molecular implications of the stepwise progression of lung adenocarcinoma," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    7. Liyuan Zhou & Qiongzi Qiu & Qing Zhou & Jianwei Li & Mengqian Yu & Kezhen Li & Lingling Xu & Xiaohui Ke & Haiming Xu & Bingjian Lu & Hui Wang & Weiguo Lu & Pengyuan Liu & Yan Lu, 2022. "Long-read sequencing unveils high-resolution HPV integration and its oncogenic progression in cervical cancer," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    8. Adam C. Weiner & Marc J. Williams & Hongyu Shi & Ignacio Vázquez-García & Sohrab Salehi & Nicole Rusk & Samuel Aparicio & Sohrab P. Shah & Andrew McPherson, 2024. "Inferring replication timing and proliferation dynamics from single-cell DNA sequencing data," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    9. Yu Chen & Amy Y. Wang & Courtney A. Barkley & Yixin Zhang & Xinyang Zhao & Min Gao & Mick D. Edmonds & Zechen Chong, 2023. "Deciphering the exact breakpoints of structural variations using long sequencing reads with DeBreak," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    10. Jinhyun Kim & Sungsik Kim & Huiran Yeom & Seo Woo Song & Kyoungseob Shin & Sangwook Bae & Han Suk Ryu & Ji Young Kim & Ahyoun Choi & Sumin Lee & Taehoon Ryu & Yeongjae Choi & Hamin Kim & Okju Kim & Yu, 2023. "Barcoded multiple displacement amplification for high coverage sequencing in spatial genomics," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    11. Frederick Richards & Marta J. Llorca-Cardenosa & Jamie Langton & Sara C. Buch-Larsen & Noor F. Shamkhi & Abhishek Bharadwaj Sharma & Michael L. Nielsen & Nicholas D. Lakin, 2023. "Regulation of Rad52-dependent replication fork recovery through serine ADP-ribosylation of PolD3," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    12. Alexander Martinez-Fundichely & Austin Dixon & Ekta Khurana, 2022. "Modeling tissue-specific breakpoint proximity of structural variations from whole-genomes to identify cancer drivers," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    13. Wei Wu & Szymon A. Barwacz & Rahul Bhowmick & Katrine Lundgaard & Marisa M. Gonçalves Dinis & Malgorzata Clausen & Masato T. Kanemaki & Ying Liu, 2023. "Mitotic DNA synthesis in response to replication stress requires the sequential action of DNA polymerases zeta and delta in human cells," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    14. Daniela Muoio & Natalie Laspata & Rachel L. Dannenberg & Caroline Curry & Simone Darkoa-Larbi & Mark Hedglin & Shikhar Uttam & Elise Fouquerel, 2024. "PARP2 promotes Break Induced Replication-mediated telomere fragility in response to replication stress," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    15. Yijiang Xu & Hang Zhou & Ginell Post & Hong Zan & Paolo Casali, 2022. "Rad52 mediates class-switch DNA recombination to IgD," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    16. Chunyang Bao & Richard W. Tourdot & Gregory J. Brunette & Chip Stewart & Lili Sun & Hideo Baba & Masayuki Watanabe & Agoston T. Agoston & Kunal Jajoo & Jon M. Davison & Katie S. Nason & Gad Getz & Ken, 2023. "Genomic signatures of past and present chromosomal instability in Barrett’s esophagus and early esophageal adenocarcinoma," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    17. Luan Nguyen & Arne Hoeck & Edwin Cuppen, 2022. "Machine learning-based tissue of origin classification for cancer of unknown primary diagnostics using genome-wide mutation features," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    18. Eva G. Álvarez & Jonas Demeulemeester & Paula Otero & Clemency Jolly & Daniel García-Souto & Ana Pequeño-Valtierra & Jorge Zamora & Marta Tojo & Javier Temes & Adrian Baez-Ortega & Bernardo Rodriguez-, 2021. "Aberrant integration of Hepatitis B virus DNA promotes major restructuring of human hepatocellular carcinoma genome architecture," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    19. Stefano Gnan & Joseph M. Josephides & Xia Wu & Manuela Spagnuolo & Dalila Saulebekova & Mylène Bohec & Marie Dumont & Laura G. Baudrin & Daniele Fachinetti & Sylvain Baulande & Chun-Long Chen, 2022. "Kronos scRT: a uniform framework for single-cell replication timing analysis," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    20. Yoshitaka Sakamoto & Shuhei Miyake & Miho Oka & Akinori Kanai & Yosuke Kawai & Satoi Nagasawa & Yuichi Shiraishi & Katsushi Tokunaga & Takashi Kohno & Masahide Seki & Yutaka Suzuki & Ayako Suzuki, 2022. "Phasing analysis of lung cancer genomes using a long read sequencer," Nature Communications, Nature, vol. 13(1), pages 1-17, 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:13:y:2022:i:1:d:10.1038_s41467-022-35060-4. 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.