IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38793-y.html
   My bibliography  Save this article

Serine ADP-ribosylation in Drosophila provides insights into the evolution of reversible ADP-ribosylation signalling

Author

Listed:
  • Pietro Fontana

    (University of Oxford, South Parks Road
    Harvard Medical School
    Boston Children’s Hospital)

  • Sara C. Buch-Larsen

    (University of Copenhagen, Blegdamsvej 3B)

  • Osamu Suyari

    (University of Oxford, South Parks Road)

  • Rebecca Smith

    (University of Oxford, South Parks Road)

  • Marcin J. Suskiewicz

    (University of Oxford, South Parks Road
    Centre de Biophysique Moléculaire, UPR4301 CNRS, rue Charles Sadron, CEDEX 2)

  • Kira Schützenhofer

    (University of Oxford, South Parks Road)

  • Antonio Ariza

    (University of Oxford, South Parks Road
    School of Biosciences, University of Sheffield, Western Bank)

  • Johannes Gregor Matthias Rack

    (University of Oxford, South Parks Road
    MRC Centre for Medical Mycology, School of Biosciences, University of Exeter, Geoffrey Pope Building)

  • Michael L. Nielsen

    (University of Copenhagen, Blegdamsvej 3B)

  • Ivan Ahel

    (University of Oxford, South Parks Road)

Abstract

In the mammalian DNA damage response, ADP-ribosylation signalling is of crucial importance to mark sites of DNA damage as well as recruit and regulate repairs factors. Specifically, the PARP1:HPF1 complex recognises damaged DNA and catalyses the formation of serine-linked ADP-ribosylation marks (mono-Ser-ADPr), which are extended into ADP-ribose polymers (poly-Ser-ADPr) by PARP1 alone. Poly-Ser-ADPr is reversed by PARG, while the terminal mono-Ser-ADPr is removed by ARH3. Despite its significance and apparent evolutionary conservation, little is known about ADP-ribosylation signalling in non-mammalian Animalia. The presence of HPF1, but absence of ARH3, in some insect genomes, including Drosophila species, raises questions regarding the existence and reversal of serine-ADP-ribosylation in these species. Here we show by quantitative proteomics that Ser-ADPr is the major form of ADP-ribosylation in the DNA damage response of Drosophila melanogaster and is dependent on the dParp1:dHpf1 complex. Moreover, our structural and biochemical investigations uncover the mechanism of mono-Ser-ADPr removal by Drosophila Parg. Collectively, our data reveal PARP:HPF1-mediated Ser-ADPr as a defining feature of the DDR in Animalia. The striking conservation within this kingdom suggests that organisms that carry only a core set of ADP-ribosyl metabolising enzymes, such as Drosophila, are valuable model organisms to study the physiological role of Ser-ADPr signalling.

Suggested Citation

  • Pietro Fontana & Sara C. Buch-Larsen & Osamu Suyari & Rebecca Smith & Marcin J. Suskiewicz & Kira Schützenhofer & Antonio Ariza & Johannes Gregor Matthias Rack & Michael L. Nielsen & Ivan Ahel, 2023. "Serine ADP-ribosylation in Drosophila provides insights into the evolution of reversible ADP-ribosylation signalling," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38793-y
    DOI: 10.1038/s41467-023-38793-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38793-y
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-38793-y?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. Dea Slade & Mark S. Dunstan & Eva Barkauskaite & Ria Weston & Pierre Lafite & Neil Dixon & Marijan Ahel & David Leys & Ivan Ahel, 2011. "The structure and catalytic mechanism of a poly(ADP-ribose) glycohydrolase," Nature, Nature, vol. 477(7366), pages 616-620, September.
    2. Marcin J. Suskiewicz & Florian Zobel & Tom E. H. Ogden & Pietro Fontana & Antonio Ariza & Ji-Chun Yang & Kang Zhu & Lily Bracken & William J. Hawthorne & Dragana Ahel & David Neuhaus & Ivan Ahel, 2020. "HPF1 completes the PARP active site for DNA damage-induced ADP-ribosylation," Nature, Nature, vol. 579(7800), pages 598-602, March.
    3. Silvija Bilokapic & Marcin J. Suskiewicz & Ivan Ahel & Mario Halic, 2020. "Bridging of DNA breaks activates PARP2–HPF1 to modify chromatin," Nature, Nature, vol. 585(7826), pages 609-613, September.
    4. Sejal Vyas & Ivan Matic & Lilen Uchima & Jenny Rood & Roko Zaja & Ronald T. Hay & Ivan Ahel & Paul Chang, 2014. "Family-wide analysis of poly(ADP-ribose) polymerase activity," Nature Communications, Nature, vol. 5(1), pages 1-13, December.
    5. Hana Hanzlikova & Evgeniia Prokhorova & Katerina Krejcikova & Zuzana Cihlarova & Ilona Kalasova & Jan Kubovciak & Jana Sachova & Richard Hailstone & Jan Brazina & Shereen Ghosh & Sebahattin Cirak & Jo, 2020. "Pathogenic ARH3 mutations result in ADP-ribose chromatin scars during DNA strand break repair," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    6. Mark S. Dunstan & Eva Barkauskaite & Pierre Lafite & Claire E. Knezevic & Amy Brassington & Marijan Ahel & Paul J. Hergenrother & David Leys & Ivan Ahel, 2012. "Structure and mechanism of a canonical poly(ADP-ribose) glycohydrolase," Nature Communications, Nature, vol. 3(1), pages 1-6, January.
    7. Ivo A. Hendriks & Sara C. Buch-Larsen & Evgeniia Prokhorova & Jonas D. Elsborg & Alexandra K.L.F.S. Rebak & Kang Zhu & Dragana Ahel & Claudia Lukas & Ivan Ahel & Michael L. Nielsen, 2021. "The regulatory landscape of the human HPF1- and ARH3-dependent ADP-ribosylome," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    8. Fa-Hui Sun & Peng Zhao & Nan Zhang & Lu-Lu Kong & Catherine C. L. Wong & Cai-Hong Yun, 2021. "HPF1 remodels the active site of PARP1 to enable the serine ADP-ribosylation of histones," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    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. Edoardo José Longarini & Ivan Matić, 2024. "Preserving ester-linked modifications reveals glutamate and aspartate mono-ADP-ribosylation by PARP1 and its reversal by PARG," Nature Communications, Nature, vol. 15(1), pages 1-17, 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. Marie-France Langelier & Ramya Billur & Aleksandr Sverzhinsky & Ben E. Black & John M. Pascal, 2021. "HPF1 dynamically controls the PARP1/2 balance between initiating and elongating ADP-ribose modifications," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    2. Ivo A. Hendriks & Sara C. Buch-Larsen & Evgeniia Prokhorova & Jonas D. Elsborg & Alexandra K.L.F.S. Rebak & Kang Zhu & Dragana Ahel & Claudia Lukas & Ivan Ahel & Michael L. Nielsen, 2021. "The regulatory landscape of the human HPF1- and ARH3-dependent ADP-ribosylome," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    3. Edoardo José Longarini & Ivan Matić, 2024. "Preserving ester-linked modifications reveals glutamate and aspartate mono-ADP-ribosylation by PARP1 and its reversal by PARG," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    4. Zita Fábián & Ellen S. Kakulidis & Ivo A. Hendriks & Ulrike Kühbacher & Nicolai B. Larsen & Marta Oliva-Santiago & Junhui Wang & Xueyuan Leng & A. Barbara Dirac-Svejstrup & Jesper Q. Svejstrup & Micha, 2024. "PARP1-dependent DNA-protein crosslink repair," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    5. Luka Bacic & Guillaume Gaullier & Jugal Mohapatra & Guanzhong Mao & Klaus Brackmann & Mikhail Panfilov & Glen Liszczak & Anton Sabantsev & Sebastian Deindl, 2024. "Asymmetric nucleosome PARylation at DNA breaks mediates directional nucleosome sliding by ALC1," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    6. Simon D. Schwarz & Jianming Xu & Kapila Gunasekera & David Schürmann & Cathrine B. Vågbø & Elena Ferrari & Geir Slupphaug & Michael O. Hottiger & Primo Schär & Roland Steinacher, 2024. "Covalent PARylation of DNA base excision repair proteins regulates DNA demethylation," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    7. 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.
    8. 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.
    9. Tong Wang & Kush Coshic & Mohsen Badiee & Maranda R. McDonald & Aleksei Aksimentiev & Lois Pollack & Anthony K. L. Leung, 2024. "Cation-induced intramolecular coil-to-globule transition in poly(ADP-ribose)," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    10. Ozge Saatci & Metin Cetin & Meral Uner & Unal Metin Tokat & Ioulia Chatzistamou & Pelin Gulizar Ersan & Elodie Montaudon & Aytekin Akyol & Sercan Aksoy & Aysegul Uner & Elisabetta Marangoni & Mathew S, 2023. "Toxic PARP trapping upon cAMP-induced DNA damage reinstates the efficacy of endocrine therapy and CDK4/6 inhibitors in treatment-refractory ER+ breast cancer," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    11. Lingling Li & Dongxian Jiang & Hui Liu & Chunmei Guo & Rui Zhao & Qiao Zhang & Chen Xu & Zhaoyu Qin & Jinwen Feng & Yang Liu & Haixing Wang & Weijie Chen & Xue Zhang & Bin Li & Lin Bai & Sha Tian & Su, 2023. "Comprehensive proteogenomic characterization of early duodenal cancer reveals the carcinogenesis tracks of different subtypes," Nature Communications, Nature, vol. 14(1), pages 1-24, December.
    12. Zhengrui Zhang & Jiaqi Fu & Johannes Gregor Matthias Rack & Chuang Li & Jim Voorneveld & Dmitri V. Filippov & Ivan Ahel & Zhao-Qing Luo & Chittaranjan Das, 2024. "Legionella metaeffector MavL reverses ubiquitin ADP-ribosylation via a conserved arginine-specific macrodomain," Nature Communications, Nature, vol. 15(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:14:y:2023:i:1:d:10.1038_s41467-023-38793-y. 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.