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Sperm derived H2AK119ub1 is required for embryonic development in Xenopus laevis

Author

Listed:
  • Valentin Francois--Campion

    (UMR 1064)

  • Florian Berger

    (UMR 1064)

  • Mami Oikawa

    (Hachioji)

  • Maissa Goumeidane

    (UMR 1064)

  • Nolwenn Mouniée

    (UMR 1064)

  • Vanessa Chenouard

    (UMR 1064)

  • Kseniya Petrova

    (Harvard Medical School)

  • Jose G. Abreu

    (Harvard Medical School
    Universidade Federal do Rio de Janeiro)

  • Cynthia Fourgeux

    (UMR 1064)

  • Jeremie Poschmann

    (UMR 1064)

  • Leonid Peshkin

    (Harvard Medical School)

  • Romain Gibeaux

    (IGDR (Institut de Génétique et Développement de Rennes) - UMR 6290)

  • Jérôme Jullien

    (UMR 1064)

Abstract

Ubiquitylation of H2A (H2AK119ub1) by the polycomb repressive complexe-1 plays a key role in the initiation of facultative heterochromatin formation in somatic cells. Here we evaluate the contribution of sperm derived H2AK119ub1 to embryo development. In Xenopus laevis we found that H2AK119ub1 is present during spermiogenesis and into early embryonic development, highlighting its credential for a role in the transmission of epigenetic information from the sperm to the embryo. In vitro treatment of sperm with USP21, a H2AK119ub1 deubiquitylase, just prior to injection to egg, results in developmental defects associated with gene upregulation. Sperm H2AK119ub1 editing disrupts egg factor mediated paternal chromatin remodelling processes. It leads to post-replication accumulation of H2AK119ub1 on repeat element of the genome instead of CpG islands. This shift in post-replication H2AK119ub1 distribution triggered by sperm epigenome editing entails a loss of H2AK119ub1 from genes misregulated in embryos derived from USP21 treated sperm. We conclude that sperm derived H2AK119ub1 instructs egg factor mediated epigenetic remodelling of paternal chromatin and is required for embryonic development.

Suggested Citation

  • Valentin Francois--Campion & Florian Berger & Mami Oikawa & Maissa Goumeidane & Nolwenn Mouniée & Vanessa Chenouard & Kseniya Petrova & Jose G. Abreu & Cynthia Fourgeux & Jeremie Poschmann & Leonid Pe, 2025. "Sperm derived H2AK119ub1 is required for embryonic development in Xenopus laevis," Nature Communications, Nature, vol. 16(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-58615-7
    DOI: 10.1038/s41467-025-58615-7
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    References listed on IDEAS

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    1. Jiali Jin & Jian Liu & Cong Chen & Zhenping Liu & Cong Jiang & Hongshang Chu & Weijuan Pan & Xinbo Wang & Lingqiang Zhang & Bin Li & Cizhong Jiang & Xin Ge & Xin Xie & Ping Wang, 2016. "The deubiquitinase USP21 maintains the stemness of mouse embryonic stem cells via stabilization of Nanog," Nature Communications, Nature, vol. 7(1), pages 1-15, December.
    2. 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.
    3. Heui-Yun Joo & Ling Zhai & Chunying Yang & Shuyi Nie & Hediye Erdjument-Bromage & Paul Tempst & Chenbei Chang & Hengbin Wang, 2007. "Regulation of cell cycle progression and gene expression by H2A deubiquitination," Nature, Nature, vol. 449(7165), pages 1068-1072, October.
    4. Adam M. Session & Yoshinobu Uno & Taejoon Kwon & Jarrod A. Chapman & Atsushi Toyoda & Shuji Takahashi & Akimasa Fukui & Akira Hikosaka & Atsushi Suzuki & Mariko Kondo & Simon J. van Heeringen & Ian Qu, 2016. "Genome evolution in the allotetraploid frog Xenopus laevis," Nature, Nature, vol. 538(7625), pages 336-343, October.
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