IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-28642-9.html
   My bibliography  Save this article

Global and transcription-coupled repair of 8-oxoG is initiated by nucleotide excision repair proteins

Author

Listed:
  • Namrata Kumar

    (University of Pittsburgh School of Medicine
    UPMC Hillman Cancer Center)

  • Arjan F. Theil

    (University Medical Center Rotterdam, Dr. Molewaterplein 40)

  • Vera Roginskaya

    (UPMC Hillman Cancer Center
    University of Pittsburgh School of Medicine)

  • Yasmin Ali

    (University of Pittsburgh School of Medicine)

  • Michael Calderon

    (University of Pittsburgh)

  • Simon C. Watkins

    (University of Pittsburgh)

  • Ryan P. Barnes

    (UPMC Hillman Cancer Center
    University of Pittsburgh Graduate School of Public Health)

  • Patricia L. Opresko

    (UPMC Hillman Cancer Center
    University of Pittsburgh Graduate School of Public Health)

  • Alex Pines

    (University Medical Center Rotterdam, Dr. Molewaterplein 40)

  • Hannes Lans

    (University Medical Center Rotterdam, Dr. Molewaterplein 40)

  • Wim Vermeulen

    (University Medical Center Rotterdam, Dr. Molewaterplein 40)

  • Bennett Houten

    (University of Pittsburgh School of Medicine
    UPMC Hillman Cancer Center
    University of Pittsburgh School of Medicine)

Abstract

UV-DDB, consisting of subunits DDB1 and DDB2, recognizes UV-induced photoproducts during global genome nucleotide excision repair (GG-NER). We recently demonstrated a noncanonical role of UV-DDB in stimulating base excision repair (BER) which raised several questions about the timing of UV-DDB arrival at 8-oxoguanine (8-oxoG), and the dependency of UV-DDB on the recruitment of downstream BER and NER proteins. Using two different approaches to introduce 8-oxoG in cells, we show that DDB2 is recruited to 8-oxoG immediately after damage and colocalizes with 8-oxoG glycosylase (OGG1) at sites of repair. 8-oxoG removal and OGG1 recruitment is significantly reduced in the absence of DDB2. NER proteins, XPA and XPC, also accumulate at 8-oxoG. While XPC recruitment is dependent on DDB2, XPA recruitment is DDB2-independent and transcription-coupled. Finally, DDB2 accumulation at 8-oxoG induces local chromatin unfolding. We propose that DDB2-mediated chromatin decompaction facilitates the recruitment of downstream BER proteins to 8-oxoG lesions.

Suggested Citation

  • Namrata Kumar & Arjan F. Theil & Vera Roginskaya & Yasmin Ali & Michael Calderon & Simon C. Watkins & Ryan P. Barnes & Patricia L. Opresko & Alex Pines & Hannes Lans & Wim Vermeulen & Bennett Houten, 2022. "Global and transcription-coupled repair of 8-oxoG is initiated by nucleotide excision repair proteins," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28642-9
    DOI: 10.1038/s41467-022-28642-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-28642-9
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-28642-9?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. Karolin Luger & Armin W. Mäder & Robin K. Richmond & David F. Sargent & Timothy J. Richmond, 1997. "Crystal structure of the nucleosome core particle at 2.8 Å resolution," Nature, Nature, vol. 389(6648), pages 251-260, September.
    2. Syota Matsumoto & Simone Cavadini & Richard D. Bunker & Ralph S. Grand & Alessandro Potenza & Julius Rabl & Junpei Yamamoto & Andreas D. Schenk & Dirk Schübeler & Shigenori Iwai & Kaoru Sugasawa & Hit, 2019. "DNA damage detection in nucleosomes involves DNA register shifting," Nature, Nature, vol. 571(7763), pages 79-84, July.
    3. Syota Matsumoto & Simone Cavadini & Richard D. Bunker & Ralph S. Grand & Alessandro Potenza & Julius Rabl & Junpei Yamamoto & Andreas D. Schenk & Dirk Schübeler & Shigenori Iwai & Kaoru Sugasawa & Hit, 2019. "Publisher Correction: DNA damage detection in nucleosomes involves DNA register shifting," Nature, Nature, vol. 571(7764), pages 6-6, July.
    4. Cristina Ribeiro-Silva & Mariangela Sabatella & Angela Helfricht & Jurgen A. Marteijn & Arjan F. Theil & Wim Vermeulen & Hannes Lans, 2020. "Ubiquitin and TFIIH-stimulated DDB2 dissociation drives DNA damage handover in nucleotide excision repair," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    5. Anita Schlierf & Eva Altmann & Jean Quancard & Anne B. Jefferson & René Assenberg & Martin Renatus & Matthew Jones & Ulrich Hassiepen & Michael Schaefer & Michael Kiffe & Andreas Weiss & Christian Wie, 2016. "Targeted inhibition of the COP9 signalosome for treatment of cancer," Nature Communications, Nature, vol. 7(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. Shaqraa Musawi & Lise-Marie Donnio & Zehui Zhao & Charlène Magnani & Phoebe Rassinoux & Olivier Binda & Jianbo Huang & Arnaud Jacquier & Laurent Coudert & Patrick Lomonte & Cécile Martinat & Laurent S, 2023. "Nucleolar reorganization after cellular stress is orchestrated by SMN shuttling between nuclear compartments," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    2. Brittany N. Vandenberg & Marian F. Laughery & Cameron Cordero & Dalton Plummer & Debra Mitchell & Jordan Kreyenhagen & Fatimah Albaqshi & Alexander J. Brown & Piotr A. Mieczkowski & John J. Wyrick & S, 2023. "Contributions of replicative and translesion DNA polymerases to mutagenic bypass of canonical and atypical UV photoproducts," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    3. Athanasios Siametis & Kalliopi Stratigi & Despoina Giamaki & Georgia Chatzinikolaou & Alexia Akalestou-Clocher & Evi Goulielmaki & Brian Luke & Björn Schumacher & George A. Garinis, 2024. "Transcription stress at telomeres leads to cytosolic DNA release and paracrine senescence," Nature Communications, Nature, vol. 15(1), pages 1-20, 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. Charlotte Blessing & Katja Apelt & Diana Heuvel & Claudia Gonzalez-Leal & Magdalena B. Rother & Melanie Woude & Román González-Prieto & Adi Yifrach & Avital Parnas & Rashmi G. Shah & Tia Tyrsett Kuo &, 2022. "XPC–PARP complexes engage the chromatin remodeler ALC1 to catalyze global genome DNA damage repair," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    2. Tyler M. Weaver & Nicole M. Hoitsma & Jonah J. Spencer & Lokesh Gakhar & Nicholas J. Schnicker & Bret D. Freudenthal, 2022. "Structural basis for APE1 processing DNA damage in the nucleosome," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    3. Anna Sefer & Eleni Kallis & Tobias Eilert & Carlheinz Röcker & Olga Kolesnikova & David Neuhaus & Sebastian Eustermann & Jens Michaelis, 2022. "Structural dynamics of DNA strand break sensing by PARP-1 at a single-molecule level," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    4. Corina Maritz & Reihaneh Khaleghi & Michelle N. Yancoskie & Sarah Diethelm & Sonja Brülisauer & Natalia Santos Ferreira & Yang Jiang & Shana J. Sturla & Hanspeter Naegeli, 2023. "ASH1L-MRG15 methyltransferase deposits H3K4me3 and FACT for damage verification in nucleotide excision repair," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    5. Alba Muniesa-Vargas & Carlota Davó-Martínez & Cristina Ribeiro-Silva & Melanie van der Woude & Karen L. Thijssen & Ben Haspels & David Häckes & Ülkem U. Kaynak & Roland Kanaar & Jurgen A. Marteijn & A, 2024. "Persistent TFIIH binding to non-excised DNA damage causes cell and developmental failure," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    6. Masaki Kikuchi & Satoshi Morita & Masatoshi Wakamori & Shin Sato & Tomomi Uchikubo-Kamo & Takehiro Suzuki & Naoshi Dohmae & Mikako Shirouzu & Takashi Umehara, 2023. "Epigenetic mechanisms to propagate histone acetylation by p300/CBP," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    7. Zhen Hou & Frank Nightingale & Yanan Zhu & Craig MacGregor-Chatwin & Peijun Zhang, 2023. "Structure of native chromatin fibres revealed by Cryo-ET in situ," Nature Communications, Nature, vol. 14(1), pages 1-7, December.
    8. Marko Dunjić & Felix Jonas & Gilad Yaakov & Roye More & Yoav Mayshar & Yoach Rais & Ayelet-Hashahar Orenbuch & Saifeng Cheng & Naama Barkai & Yonatan Stelzer, 2023. "Histone exchange sensors reveal variant specific dynamics in mouse embryonic stem cells," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    9. Rina Hirano & Haruhiko Ehara & Tomoya Kujirai & Tamami Uejima & Yoshimasa Takizawa & Shun-ichi Sekine & Hitoshi Kurumizaka, 2022. "Structural basis of RNA polymerase II transcription on the chromatosome containing linker histone H1," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    10. Timothy A. Daugird & Yu Shi & Katie L. Holland & Hosein Rostamian & Zhe Liu & Luke D. Lavis & Joseph Rodriguez & Brian D. Strahl & Wesley R. Legant, 2024. "Correlative single molecule lattice light sheet imaging reveals the dynamic relationship between nucleosomes and the local chromatin environment," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    11. Jaeyoon Lee & Meiling Wu & James T. Inman & Gundeep Singh & Seong ha Park & Joyce H. Lee & Robert M. Fulbright & Yifeng Hong & Joshua Jeong & James M. Berger & Michelle D. Wang, 2023. "Chromatinization modulates topoisomerase II processivity," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    12. Nithya Ramakrishnan & Sibi Raj B Pillai & Ranjith Padinhateeri, 2022. "High fidelity epigenetic inheritance: Information theoretic model predicts threshold filling of histone modifications post replication," PLOS Computational Biology, Public Library of Science, vol. 18(2), pages 1-22, February.
    13. Jiayi Fan & Andrew T. Moreno & Alexander S. Baier & Joseph J. Loparo & Craig L. Peterson, 2022. "H2A.Z deposition by SWR1C involves multiple ATP-dependent steps," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    14. Dian Spakman & Tinka V. M. Clement & Andreas S. Biebricher & Graeme A. King & Manika I. Singh & Ian D. Hickson & Erwin J. G. Peterman & Gijs J. L. Wuite, 2022. "PICH acts as a force-dependent nucleosome remodeler," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    15. Xiaowei Xu & Shoufu Duan & Xu Hua & Zhiming Li & Richard He & Zhiguo Zhang, 2022. "Stable inheritance of H3.3-containing nucleosomes during mitotic cell divisions," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    16. Victoria S. Frisbie & Hideharu Hashimoto & Yixuan Xie & Francisca N. De Luna Vitorino & Josue Baeza & Tam Nguyen & Zhangerjiao Yuan & Janna Kiselar & Benjamin A. Garcia & Erik W. Debler, 2024. "Two DOT1 enzymes cooperatively mediate efficient ubiquitin-independent histone H3 lysine 76 tri-methylation in kinetoplastids," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    17. Shuxiang Li & Tiejun Wei & Anna R. Panchenko, 2023. "Histone variant H2A.Z modulates nucleosome dynamics to promote DNA accessibility," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    18. Un Seng Chio & Eugene Palovcak & Anton A. A. Smith & Henriette Autzen & Elise N. Muñoz & Zanlin Yu & Feng Wang & David A. Agard & Jean-Paul Armache & Geeta J. Narlikar & Yifan Cheng, 2024. "Functionalized graphene-oxide grids enable high-resolution cryo-EM structures of the SNF2h-nucleosome complex without crosslinking," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    19. Kook Son & Vakil Takhaveev & Visesato Mor & Hobin Yu & Emma Dillier & Nicola Zilio & Nikolai J. L. Püllen & Dmitri Ivanov & Helle D. Ulrich & Shana J. Sturla & Orlando D. Schärer, 2024. "Trabectedin derails transcription-coupled nucleotide excision repair to induce DNA breaks in highly transcribed genes," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    20. Yu Zhang & Min Ma & Meng Liu & Aiqing Sun & Xiaoyun Zheng & Kunpeng Liu & Chunmei Yin & Chuanshun Li & Cizhong Jiang & Xiaoyu Tu & Yuda Fang, 2023. "Histone H2A monoubiquitination marks are targeted to specific sites by cohesin subunits in Arabidopsis," Nature Communications, Nature, vol. 14(1), pages 1-12, 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_s41467-022-28642-9. 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.