IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-37408-w.html
   My bibliography  Save this article

A-MYB and BRDT-dependent RNA Polymerase II pause release orchestrates transcriptional regulation in mammalian meiosis

Author

Listed:
  • Adriana K. Alexander

    (Cornell University
    Cornell University)

  • Edward J. Rice

    (Cornell University)

  • Jelena Lujic

    (Cornell University)

  • Leah E. Simon

    (Cornell University)

  • Stephanie Tanis

    (Cornell University)

  • Gilad Barshad

    (Cornell University)

  • Lina Zhu

    (Cornell University)

  • Jyoti Lama

    (Cornell University)

  • Paula E. Cohen

    (Cornell University
    Cornell University)

  • Charles G. Danko

    (Cornell University
    Cornell University
    Cornell University)

Abstract

During meiotic prophase I, spermatocytes must balance transcriptional activation with homologous recombination and chromosome synapsis, biological processes requiring extensive changes to chromatin state. We explored the interplay between chromatin accessibility and transcription through prophase I of mammalian meiosis by measuring genome-wide patterns of chromatin accessibility, nascent transcription, and processed mRNA. We find that Pol II is loaded on chromatin and maintained in a paused state early during prophase I. In later stages, paused Pol II is released in a coordinated transcriptional burst mediated by the transcription factors A-MYB and BRDT, resulting in ~3-fold increase in transcription. Transcriptional activity is temporally and spatially segregated from key steps of meiotic recombination: double strand breaks show evidence of chromatin accessibility earlier during prophase I and at distinct loci from those undergoing transcriptional activation, despite shared chromatin marks. Our findings reveal mechanisms underlying chromatin specialization in either transcription or recombination in meiotic cells.

Suggested Citation

  • Adriana K. Alexander & Edward J. Rice & Jelena Lujic & Leah E. Simon & Stephanie Tanis & Gilad Barshad & Lina Zhu & Jyoti Lama & Paula E. Cohen & Charles G. Danko, 2023. "A-MYB and BRDT-dependent RNA Polymerase II pause release orchestrates transcriptional regulation in mammalian meiosis," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-37408-w
    DOI: 10.1038/s41467-023-37408-w
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-37408-w
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-37408-w?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. Alexander Widger & Shantha K. Mahadevaiah & Julian Lange & Elias ElInati & Jasmin Zohren & Takayuki Hirota & Sarai Pacheco & Andros Maldonado-Linares & Marcello Stanzione & Obah Ojarikre & Valdone Mac, 2018. "ATR is a multifunctional regulator of male mouse meiosis," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    2. Kevin Brick & Fatima Smagulova & Pavel Khil & R. Daniel Camerini-Otero & Galina V. Petukhova, 2012. "Genetic recombination is directed away from functional genomic elements in mice," Nature, Nature, vol. 485(7400), pages 642-645, May.
    3. Wu Zuo & Guangming Chen & Zhimei Gao & Shuai Li & Yanyan Chen & Chenhui Huang & Juan Chen & Zhengjun Chen & Ming Lei & Qian Bian, 2021. "Stage-resolved Hi-C analyses reveal meiotic chromosome organizational features influencing homolog alignment," Nature Communications, Nature, vol. 12(1), pages 1-20, 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. Emily G. Kaye & Kavyashree Basavaraju & Geoffrey M. Nelson & Helena D. Zomer & Debarun Roy & Irene Infancy Joseph & Reza Rajabi-Toustani & Huanyu Qiao & Karen Adelman & Prabhakara P. Reddi, 2024. "RNA polymerase II pausing is essential during spermatogenesis for appropriate gene expression and completion of meiosis," 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. Akbar Zainu & Pauline Dupaigne & Soumya Bouchouika & Julien Cau & Julie A. J. Clément & Pauline Auffret & Virginie Ropars & Jean-Baptiste Charbonnier & Bernard Massy & Raphael Mercier & Rajeev Kumar &, 2024. "FIGNL1-FIRRM is essential for meiotic recombination and prevents DNA damage-independent RAD51 and DMC1 loading," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    2. Hironori Abe & Yu-Han Yeh & Yasuhisa Munakata & Kei-Ichiro Ishiguro & Paul R. Andreassen & Satoshi H. Namekawa, 2022. "Active DNA damage response signaling initiates and maintains meiotic sex chromosome inactivation," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    3. Alexandre Nore & Ariadna B. Juarez-Martinez & Julie Clément & Christine Brun & Boubou Diagouraga & Hamida Laroussi & Corinne Grey & Henri Marc Bourbon & Jan Kadlec & Thomas Robert & Bernard Massy, 2022. "TOPOVIBL-REC114 interaction regulates meiotic DNA double-strand breaks," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    4. Úbeda, Francisco & Russell, Timothy W. & Jansen, Vincent A.A., 2019. "PRDM9 and the evolution of recombination hotspots," Theoretical Population Biology, Elsevier, vol. 126(C), pages 19-32.

    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_s41467-023-37408-w. 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.