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Genome-wide analysis in the mouse embryo reveals the importance of DNA methylation for transcription integrity

Author

Listed:
  • Thomas Dahlet

    (University of Strasbourg
    CNRS UMR7242)

  • Andrea Argüeso Lleida

    (University of Strasbourg
    CNRS UMR7242)

  • Hala Al Adhami

    (University of Strasbourg
    CNRS UMR7242)

  • Michael Dumas

    (University of Strasbourg
    CNRS UMR7242)

  • Ambre Bender

    (University of Strasbourg
    CNRS UMR7242)

  • Richard P. Ngondo

    (University of Strasbourg
    CNRS UMR7242
    IBMP, CNRS UPR2357)

  • Manon Tanguy

    (University of Strasbourg
    CNRS UMR7242)

  • Judith Vallet

    (University of Strasbourg
    CNRS UMR7242)

  • Ghislain Auclair

    (University of Strasbourg
    CNRS UMR7242)

  • Anaïs F. Bardet

    (University of Strasbourg
    CNRS UMR7242)

  • Michael Weber

    (University of Strasbourg
    CNRS UMR7242)

Abstract

Mouse embryos acquire global DNA methylation of their genome during implantation. However the exact roles of DNA methyltransferases (DNMTs) in embryos have not been studied comprehensively. Here we systematically analyze the consequences of genetic inactivation of Dnmt1, Dnmt3a and Dnmt3b on the methylome and transcriptome of mouse embryos. We find a strict division of function between DNMT1, responsible for maintenance methylation, and DNMT3A/B, solely responsible for methylation acquisition in development. By analyzing severely hypomethylated embryos, we uncover multiple functions of DNA methylation that is used as a mechanism of repression for a panel of genes including not only imprinted and germline genes, but also lineage-committed genes and 2-cell genes. DNA methylation also suppresses multiple retrotransposons and illegitimate transcripts from cryptic promoters in transposons and gene bodies. Our work provides a thorough analysis of the roles of DNA methyltransferases and the importance of DNA methylation for transcriptome integrity in mammalian embryos.

Suggested Citation

  • Thomas Dahlet & Andrea Argüeso Lleida & Hala Al Adhami & Michael Dumas & Ambre Bender & Richard P. Ngondo & Manon Tanguy & Judith Vallet & Ghislain Auclair & Anaïs F. Bardet & Michael Weber, 2020. "Genome-wide analysis in the mouse embryo reveals the importance of DNA methylation for transcription integrity," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-16919-w
    DOI: 10.1038/s41467-020-16919-w
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    Cited by:

    1. Simon Andrews & Christel Krueger & Maravillas Mellado-Lopez & Myriam Hemberger & Wendy Dean & Vicente Perez-Garcia & Courtney W. Hanna, 2023. "Mechanisms and function of de novo DNA methylation in placental development reveals an essential role for DNMT3B," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    2. Ariane Lismer & Sarah Kimmins, 2023. "Emerging evidence that the mammalian sperm epigenome serves as a template for embryo development," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    3. Qing Li & Jiansen Lu & Xidi Yin & Yunjian Chang & Chao Wang & Meng Yan & Li Feng & Yanbo Cheng & Yun Gao & Beiying Xu & Yao Zhang & Yingyi Wang & Guizhong Cui & Luang Xu & Yidi Sun & Rong Zeng & Yixue, 2023. "Base editing-mediated one-step inactivation of the Dnmt gene family reveals critical roles of DNA methylation during mouse gastrulation," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    4. Andrea Lauria & Guohua Meng & Valentina Proserpio & Stefania Rapelli & Mara Maldotti & Isabelle Laurence Polignano & Francesca Anselmi & Danny Incarnato & Anna Krepelova & Daniela Donna & Chiara Levra, 2023. "DNMT3B supports meso-endoderm differentiation from mouse embryonic stem cells," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    5. Kentaro Mochizuki & Jafar Sharif & Kenjiro Shirane & Kousuke Uranishi & Aaron B. Bogutz & Sanne M. Janssen & Ayumu Suzuki & Akihiko Okuda & Haruhiko Koseki & Matthew C. Lorincz, 2021. "Repression of germline genes by PRC1.6 and SETDB1 in the early embryo precedes DNA methylation-mediated silencing," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    6. Amir D. Hay & Noah J. Kessler & Daniel Gebert & Nozomi Takahashi & Hugo Tavares & Felipe K. Teixeira & Anne C. Ferguson-Smith, 2023. "Epigenetic inheritance is unfaithful at intermediately methylated CpG sites," Nature Communications, Nature, vol. 14(1), pages 1-11, December.

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