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Epigenetic homogeneity in histone methylation underlies sperm programming for embryonic transcription

Author

Listed:
  • Mami Oikawa

    (Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge
    University of Cambridge)

  • Angela Simeone

    (Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge
    University of Cambridge)

  • Eva Hormanseder

    (Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge
    University of Cambridge)

  • Marta Teperek

    (Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge
    University of Cambridge)

  • Vincent Gaggioli

    (Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge
    University of Cambridge)

  • Alan O’Doherty

    (University College Dublin)

  • Emma Falk

    (CRTI, INSERM, UNIV Nantes)

  • Matthieu Sporniak

    (CRTI, INSERM, UNIV Nantes)

  • Clive D’Santos

    (Cancer Research UK Cambridge Institute, University of Cambridge)

  • Valar Nila Roamio Franklin

    (Cancer Research UK Cambridge Institute, University of Cambridge)

  • Kamal Kishore

    (Cancer Research UK Cambridge Institute, University of Cambridge)

  • Charles R. Bradshaw

    (Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge
    University of Cambridge)

  • Declan Keane

    (ReproMed Ireland)

  • Thomas Freour

    (Service de Biologie de la Reproduction, CHU Nantes)

  • Laurent David

    (CRTI, INSERM, UNIV Nantes)

  • Adrian T. Grzybowski

    (The University of Chicago)

  • Alexander J. Ruthenburg

    (The University of Chicago)

  • John Gurdon

    (Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge
    University of Cambridge)

  • Jerome Jullien

    (Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge
    University of Cambridge
    CRTI, INSERM, UNIV Nantes)

Abstract

Sperm contributes genetic and epigenetic information to the embryo to efficiently support development. However, the mechanism underlying such developmental competence remains elusive. Here, we investigated whether all sperm cells have a common epigenetic configuration that primes transcriptional program for embryonic development. Using calibrated ChIP-seq, we show that remodelling of histones during spermiogenesis results in the retention of methylated histone H3 at the same genomic location in most sperm cell. This homogeneously methylated fraction of histone H3 in the sperm genome is maintained during early embryonic replication. Such methylated histone fraction resisting post-fertilisation reprogramming marks developmental genes whose expression is perturbed upon experimental reduction of histone methylation. A similar homogeneously methylated histone H3 fraction is detected in human sperm. Altogether, we uncover a conserved mechanism of paternal epigenetic information transmission to the embryo through the homogeneous retention of methylated histone in a sperm cells population.

Suggested Citation

  • Mami Oikawa & Angela Simeone & Eva Hormanseder & Marta Teperek & Vincent Gaggioli & Alan O’Doherty & Emma Falk & Matthieu Sporniak & Clive D’Santos & Valar Nila Roamio Franklin & Kamal Kishore & Charl, 2020. "Epigenetic homogeneity in histone methylation underlies sperm programming for embryonic transcription," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-17238-w
    DOI: 10.1038/s41467-020-17238-w
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    Cited by:

    1. Xinyun Jing & Niubing Zhang & Xiaojuan Zhou & Ping Chen & Jie Gong & Kaixiang Zhang & Xueting Wu & Wenjuan Cai & Bang-Ce Ye & Pei Hao & Guo-ping Zhao & Sheng Yang & Xuan Li, 2024. "Creating a bacterium that forms eukaryotic nucleosome core particles," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

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