IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v12y2021i1d10.1038_s41467-021-26413-6.html
   My bibliography  Save this article

Arginine methylation and ubiquitylation crosstalk controls DNA end-resection and homologous recombination repair

Author

Listed:
  • Maria Pilar Sanchez-Bailon

    (University of Birmingham
    Max Delbrück Center for Molecular Medicine)

  • Soo-Youn Choi

    (University of Birmingham)

  • Elizabeth R. Dufficy

    (University of Birmingham)

  • Karan Sharma

    (University of Birmingham)

  • Gavin S. McNee

    (University of Birmingham)

  • Emma Gunnell

    (University of Nottingham)

  • Kelly Chiang

    (University of Birmingham)

  • Debashish Sahay

    (University of Birmingham)

  • Sarah Maslen

    (MRC Laboratory of Molecular Biology)

  • Grant S. Stewart

    (University of Birmingham)

  • J. Mark Skehel

    (MRC Laboratory of Molecular Biology
    The Francis Crick Institute)

  • Ingrid Dreveny

    (University of Nottingham)

  • Clare C. Davies

    (University of Birmingham)

Abstract

Cross-talk between distinct protein post-translational modifications is critical for an effective DNA damage response. Arginine methylation plays an important role in maintaining genome stability, but how this modification integrates with other enzymatic activities is largely unknown. Here, we identify the deubiquitylating enzyme USP11 as a previously uncharacterised PRMT1 substrate, and demonstrate that the methylation of USP11 promotes DNA end-resection and the repair of DNA double strand breaks (DSB) by homologous recombination (HR), an event that is independent from another USP11-HR activity, the deubiquitylation of PALB2. We also show that PRMT1 is a ubiquitylated protein that it is targeted for deubiquitylation by USP11, which regulates the ability of PRMT1 to bind to and methylate MRE11. Taken together, our findings reveal a specific role for USP11 during the early stages of DSB repair, which is mediated through its ability to regulate the activity of the PRMT1-MRE11 pathway.

Suggested Citation

  • Maria Pilar Sanchez-Bailon & Soo-Youn Choi & Elizabeth R. Dufficy & Karan Sharma & Gavin S. McNee & Emma Gunnell & Kelly Chiang & Debashish Sahay & Sarah Maslen & Grant S. Stewart & J. Mark Skehel & I, 2021. "Arginine methylation and ubiquitylation crosstalk controls DNA end-resection and homologous recombination repair," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26413-6
    DOI: 10.1038/s41467-021-26413-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-021-26413-6
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-021-26413-6?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. Valerie Garcia & Sarah E. L. Phelps & Stephen Gray & Matthew J. Neale, 2011. "Bidirectional resection of DNA double-strand breaks by Mre11 and Exo1," Nature, Nature, vol. 479(7372), pages 241-244, November.
    2. Bandish Kapadia & Nahid M. Nanaji & Kavita Bhalla & Binny Bhandary & Rena Lapidus & Afshin Beheshti & Andrew M. Evens & Ronald B. Gartenhaus, 2018. "Fatty Acid Synthase induced S6Kinase facilitates USP11-eIF4B complex formation for sustained oncogenic translation in DLBCL," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    3. Alexandre Orthwein & Sylvie M. Noordermeer & Marcus D. Wilson & Sébastien Landry & Radoslav I. Enchev & Alana Sherker & Meagan Munro & Jordan Pinder & Jayme Salsman & Graham Dellaire & Bing Xia & Matt, 2015. "A mechanism for the suppression of homologous recombination in G1 cells," Nature, Nature, vol. 528(7582), pages 422-426, December.
    4. Elda Cannavo & Petr Cejka, 2014. "Sae2 promotes dsDNA endonuclease activity within Mre11–Rad50–Xrs2 to resect DNA breaks," Nature, Nature, vol. 514(7520), pages 122-125, October.
    5. Grant S. Stewart & Bin Wang & Colin R. Bignell & A. Malcolm R. Taylor & Stephen J. Elledge, 2003. "MDC1 is a mediator of the mammalian DNA damage checkpoint," Nature, Nature, vol. 421(6926), pages 961-966, February.
    6. Charles Vadnais & Riyan Chen & Jennifer Fraszczak & Zhenbao Yu & Jonathan Boulais & Jordan Pinder & Daria Frank & Cyrus Khandanpour & Josée Hébert & Graham Dellaire & Jean-François Côté & Stéphane Ric, 2018. "GFI1 facilitates efficient DNA repair by regulating PRMT1 dependent methylation of MRE11 and 53BP1," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    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. Lorenzo Galanti & Martina Peritore & Robert Gnügge & Elda Cannavo & Johannes Heipke & Maria Dilia Palumbieri & Barbara Steigenberger & Lorraine S. Symington & Petr Cejka & Boris Pfander, 2024. "Dbf4-dependent kinase promotes cell cycle controlled resection of DNA double-strand breaks and repair by homologous recombination," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    2. Daipayan Banerjee & Kurt Langberg & Salar Abbas & Eric Odermatt & Praveen Yerramothu & Martin Volaric & Matthew A. Reidenbach & Kathy J. Krentz & C. Dustin Rubinstein & David L. Brautigan & Tarek Abba, 2021. "A non-canonical, interferon-independent signaling activity of cGAMP triggers DNA damage response signaling," Nature Communications, Nature, vol. 12(1), pages 1-24, December.
    3. Jun Dai & Shuyu Zheng & Matías M. Falco & Jie Bao & Johanna Eriksson & Sanna Pikkusaari & Sofia Forstén & Jing Jiang & Wenyu Wang & Luping Gao & Fernando Perez-Villatoro & Olli Dufva & Khalid Saeed & , 2024. "Tracing back primed resistance in cancer via sister cells," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    4. Tianyi Fan & Huijia Kang & Di Wu & Xinyu Zhu & Lin Huang & Jiabing Wu & Yan Zhu, 2022. "Arabidopsis γ-H2A.X-INTERACTING PROTEIN participates in DNA damage response and safeguards chromatin stability," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    5. Rajashree A. Deshpande & Alberto Marin-Gonzalez & Hannah K. Barnes & Phillip R. Woolley & Taekjip Ha & Tanya T. Paull, 2023. "Genome-wide analysis of DNA-PK-bound MRN cleavage products supports a sequential model of DSB repair pathway choice," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    6. Emilie Renaud & Filippo Rosselli, 2013. "FANC Pathway Promotes UV-Induced Stalled Replication Forks Recovery by Acting Both Upstream and Downstream Polη and Rev1," PLOS ONE, Public Library of Science, vol. 8(1), pages 1-13, January.
    7. Amr M. Al-Zain & Mattie R. Nester & Iffat Ahmed & Lorraine S. Symington, 2023. "Double-strand breaks induce inverted duplication chromosome rearrangements by a DNA polymerase δ-dependent mechanism," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    8. Vera M. Kissling & Giordano Reginato & Eliana Bianco & Kristina Kasaciunaite & Janny Tilma & Gea Cereghetti & Natalie Schindler & Sung Sik Lee & Raphaël Guérois & Brian Luke & Ralf Seidel & Petr Cejka, 2022. "Mre11-Rad50 oligomerization promotes DNA double-strand break repair," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    9. Priya Kapoor-Vazirani & Sandip K. Rath & Xu Liu & Zhen Shu & Nicole E. Bowen & Yitong Chen & Ramona Haji-Seyed-Javadi & Waaqo Daddacha & Elizabeth V. Minten & Diana Danelia & Daniela Farchi & Duc M. D, 2022. "SAMHD1 deacetylation by SIRT1 promotes DNA end resection by facilitating DNA binding at double-strand breaks," Nature Communications, Nature, vol. 13(1), pages 1-18, 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:12:y:2021:i:1:d:10.1038_s41467-021-26413-6. 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.