IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43778-y.html
   My bibliography  Save this article

RIF1 regulates early replication timing in murine B cells

Author

Listed:
  • Daniel Malzl

    (Research Institute of Molecular Pathology (IMP), Vienna Biocenter
    CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences)

  • Mihaela Peycheva

    (Research Institute of Molecular Pathology (IMP), Vienna Biocenter
    CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences)

  • Ali Rahjouei

    (Max-Delbruck Center for Molecular Medicine in the Helmholtz Association (MDC))

  • Stefano Gnan

    (University of Edinburgh)

  • Kyle N. Klein

    (San Diego Biomedical Research Institute)

  • Mariia Nazarova

    (Research Institute of Molecular Pathology (IMP), Vienna Biocenter)

  • Ursula E. Schoeberl

    (Research Institute of Molecular Pathology (IMP), Vienna Biocenter)

  • David M. Gilbert

    (San Diego Biomedical Research Institute)

  • Sara C. B. Buonomo

    (University of Edinburgh)

  • Michela Virgilio

    (Max-Delbruck Center for Molecular Medicine in the Helmholtz Association (MDC))

  • Tobias Neumann

    (Research Institute of Molecular Pathology (IMP), Vienna Biocenter
    Quantro Therapeutics, Vienna Biocenter)

  • Rushad Pavri

    (Research Institute of Molecular Pathology (IMP), Vienna Biocenter)

Abstract

The mammalian DNA replication timing (RT) program is crucial for the proper functioning and integrity of the genome. The best-known mechanism for controlling RT is the suppression of late origins of replication in heterochromatin by RIF1. Here, we report that in antigen-activated, hypermutating murine B lymphocytes, RIF1 binds predominantly to early-replicating active chromatin and promotes early replication, but plays a minor role in regulating replication origin activity, gene expression and genome organization in B cells. Furthermore, we find that RIF1 functions in a complementary and non-epistatic manner with minichromosome maintenance (MCM) proteins to establish early RT signatures genome-wide and, specifically, to ensure the early replication of highly transcribed genes. These findings reveal additional layers of regulation within the B cell RT program, driven by the coordinated activity of RIF1 and MCM proteins.

Suggested Citation

  • Daniel Malzl & Mihaela Peycheva & Ali Rahjouei & Stefano Gnan & Kyle N. Klein & Mariia Nazarova & Ursula E. Schoeberl & David M. Gilbert & Sara C. B. Buonomo & Michela Virgilio & Tobias Neumann & Rush, 2023. "RIF1 regulates early replication timing in murine B cells," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43778-y
    DOI: 10.1038/s41467-023-43778-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43778-y
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-43778-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. Stefano Gnan & Ilya M. Flyamer & Kyle N. Klein & Eleonora Castelli & Alexander Rapp & Andreas Maiser & Naiming Chen & Patrick Weber & Elin Enervald & M. Cristina Cardoso & Wendy A. Bickmore & David M., 2021. "Nuclear organisation and replication timing are coupled through RIF1–PP1 interaction," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    2. Benjamin D. Pope & Tyrone Ryba & Vishnu Dileep & Feng Yue & Weisheng Wu & Olgert Denas & Daniel L. Vera & Yanli Wang & R. Scott Hansen & Theresa K. Canfield & Robert E. Thurman & Yong Cheng & Günhan G, 2014. "Topologically associating domains are stable units of replication-timing regulation," Nature, Nature, vol. 515(7527), pages 402-405, November.
    3. Olivier Brison & Sami El-Hilali & Dana Azar & Stéphane Koundrioukoff & Mélanie Schmidt & Viola Nähse & Yan Jaszczyszyn & Anne-Marie Lachages & Bernard Dutrillaux & Claude Thermes & Michelle Debatisse , 2019. "Transcription-mediated organization of the replication initiation program across large genes sets common fragile sites genome-wide," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    4. Qian Du & Saul A. Bert & Nicola J. Armstrong & C. Elizabeth Caldon & Jenny Z. Song & Shalima S. Nair & Cathryn M. Gould & Phuc-Loi Luu & Timothy Peters & Amanda Khoury & Wenjia Qu & Elena Zotenko & Cl, 2019. "Replication timing and epigenome remodelling are associated with the nature of chromosomal rearrangements in cancer," Nature Communications, Nature, vol. 10(1), pages 1-15, December.
    5. Nataliya Petryk & Malik Kahli & Yves d'Aubenton-Carafa & Yan Jaszczyszyn & Yimin Shen & Maud Silvain & Claude Thermes & Chun-Long Chen & Olivier Hyrien, 2016. "Replication landscape of the human genome," Nature Communications, Nature, vol. 7(1), pages 1-13, April.
    6. Man Liu & Jamie L. Duke & Daniel J. Richter & Carola G. Vinuesa & Christopher C. Goodnow & Steven H. Kleinstein & David G. Schatz, 2008. "Two levels of protection for the B cell genome during somatic hypermutation," Nature, Nature, vol. 451(7180), pages 841-845, February.
    7. Laura Pasqualucci & Peter Neumeister & Tina Goossens & Gouri Nanjangud & R. S. K. Chaganti & Ralf Küppers & Riccardo Dalla-Favera, 2001. "Hypermutation of multiple proto-oncogenes in B-cell diffuse large-cell lymphomas," Nature, Nature, vol. 412(6844), pages 341-346, July.
    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 Corazzi & Vivien S. Ionasz & Sergej Andrejev & Li-Chin Wang & Athanasios Vouzas & Marco Giaisi & Giulia Di Muzio & Boyu Ding & Anna J. M. Marx & Jonas Henkenjohann & Michael M. Allers & David , 2024. "Linear interaction between replication and transcription shapes DNA break dynamics at recurrent DNA break Clusters," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    2. 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.
    3. 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.
    4. Cristiana Bersaglieri & Jelena Kresoja-Rakic & Shivani Gupta & Dominik Bär & Rostyslav Kuzyakiv & Martina Panatta & Raffaella Santoro, 2022. "Genome-wide maps of nucleolus interactions reveal distinct layers of repressive chromatin domains," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    5. Alon Diament & Tamir Tuller, 2015. "Improving 3D Genome Reconstructions Using Orthologous and Functional Constraints," PLOS Computational Biology, Public Library of Science, vol. 11(5), pages 1-22, May.
    6. 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.
    7. Khalid H. Bhat & Saurabh Priyadarshi & Sarah Naiyer & Xinyan Qu & Hammad Farooq & Eden Kleiman & Jeffery Xu & Xue Lei & Jose F. Cantillo & Robert Wuerffel & Nicole Baumgarth & Jie Liang & Ann J. Feene, 2023. "An Igh distal enhancer modulates antigen receptor diversity by determining locus conformation," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    8. Koon-Kiu Yan & Shaoke Lou & Mark Gerstein, 2017. "MrTADFinder: A network modularity based approach to identify topologically associating domains in multiple resolutions," PLOS Computational Biology, Public Library of Science, vol. 13(7), pages 1-22, July.
    9. Congcong Tian & Jiaqi Zhou & Xinran Li & Yuan Gao & Qing Wen & Xing Kang & Nan Wang & Yuan Yao & Jiuhang Jiang & Guibing Song & Tianjun Zhang & Suili Hu & JingYi Liao & Chuanhe Yu & Zhiquan Wang & Xia, 2023. "Impaired histone inheritance promotes tumor progression," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    10. Martin Boström & Erik Larsson, 2022. "Somatic mutation distribution across tumour cohorts provides a signal for positive selection in cancer," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    11. Li-Hsin Chang & Sourav Ghosh & Andrea Papale & Jennifer M. Luppino & Mélanie Miranda & Vincent Piras & Jéril Degrouard & Joanne Edouard & Mallory Poncelet & Nathan Lecouvreur & Sébastien Bloyer & Amél, 2023. "Multi-feature clustering of CTCF binding creates robustness for loop extrusion blocking and Topologically Associating Domain boundaries," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    12. Paola Cornejo-Páramo & Veronika Petrova & Xuan Zhang & Robert S. Young & Emily S. Wong, 2024. "Emergence of enhancers at late DNA replicating regions," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    13. Cuifang Liu & Juan Yu & Aoqun Song & Min Wang & Jiansen Hu & Ping Chen & Jicheng Zhao & Guohong Li, 2023. "Histone H1 facilitates restoration of H3K27me3 during DNA replication by chromatin compaction," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    14. Manisha Jalan & Aman Sharma & Xin Pei & Nils Weinhold & Erika S. Buechelmaier & Yingjie Zhu & Sana Ahmed-Seghir & Abhirami Ratnakumar & Melody Bona & Niamh McDermott & Joan Gomez-Aguilar & Kyrie S. An, 2024. "RAD52 resolves transcription-replication conflicts to mitigate R-loop induced genome instability," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    15. Jianli Tao & Qi Wang & Carlos Mendez-Dorantes & Kathleen H. Burns & Roberto Chiarle, 2022. "Frequency and mechanisms of LINE-1 retrotransposon insertions at CRISPR/Cas9 sites," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    16. Jamie L. Endicott & Paula A. Nolte & Hui Shen & Peter W. Laird, 2022. "Cell division drives DNA methylation loss in late-replicating domains in primary human cells," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    17. Wenting Zhang & Yue Wang & Yongjie Liu & Cuifang Liu & Yizhou Wang & Lin He & Xiao Cheng & Yani Peng & Lu Xia & Xiaodi Wu & Jiajing Wu & Yu Zhang & Luyang Sun & Ping Chen & Guohong Li & Qiang Tu & Jin, 2023. "NFIB facilitates replication licensing by acting as a genome organizer," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    18. Dashiell J. Massey & Amnon Koren, 2022. "High-throughput analysis of single human cells reveals the complex nature of DNA replication timing control," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    19. Nikolai Schleussner & Pierre Cauchy & Vedran Franke & Maciej Giefing & Oriol Fornes & Naveen Vankadari & Salam A. Assi & Mariantonia Costanza & Marc A. Weniger & Altuna Akalin & Ioannis Anagnostopoulo, 2023. "Transcriptional reprogramming by mutated IRF4 in lymphoma," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    20. Silvia Peripolli & Leticia Meneguello & Chiara Perrod & Tanya Singh & Harshil Patel & Sazia T. Rahman & Koshiro Kiso & Peter Thorpe & Vincenzo Calvanese & Cosetta Bertoli & Robertus A. M. de Bruin, 2024. "Oncogenic c-Myc induces replication stress by increasing cohesins chromatin occupancy in a CTCF-dependent manner," Nature Communications, Nature, vol. 15(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_s41467-023-43778-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.