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Coordinated action of multiple active histone modifications shapes the zygotic genome activation in teleost embryos

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  • Hiroto S. Fukushima

    (The University of Tokyo
    RIKEN)

  • Hiroyuki Takeda

    (The University of Tokyo
    Kyoto Sangyo University)

Abstract

Zygotic genome activation (ZGA) is a critical developmental milestone characterized by the rapid and simultaneous activation of genome-widely silenced chromatin. Various active histone modifications accumulate upon ZGA and have long been implicated in ZGA. However, their biological relevance still remains unclear. Here, we comprehensively examined the functional significance of active histone modifications and their writers during ZGA in teleost embryos. Our data propose that developmental genes and housekeeping genes are distinctively regulated during ZGA; CBP/P300 activity is required for developmental gene activation, whereas housekeeping genes depend on non-CBP/P300 histone acetylations H3K9ac/H4K16ac/H3K14ac. Moreover, accumulation of H3K4me2/3 is not prerequisite for activation of all types of genes during ZGA, in contrast to previous reports with cell lines. Finally, temporal accumulation of H3.3S31ph greatly enhances CBP/P300 activity specifically at ZGA, ensuring the activation of developmental genes. Our data demonstrate that multiple histone modifications cooperatively shape ZGA-specific gene activation programs in non-mammalian vertebrates.

Suggested Citation

  • Hiroto S. Fukushima & Hiroyuki Takeda, 2025. "Coordinated action of multiple active histone modifications shapes the zygotic genome activation in teleost embryos," Nature Communications, Nature, vol. 16(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:16:y:2025:i:1:d:10.1038_s41467-025-60246-x
    DOI: 10.1038/s41467-025-60246-x
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    1. Hua Wang & Zheng Fan & Pavel V. Shliaha & Matthew Miele & Ronald C. Hendrickson & Xuejun Jiang & Kristian Helin, 2023. "Publisher Correction: H3K4me3 regulates RNA polymerase II promoter-proximal pause-release," Nature, Nature, vol. 616(7956), pages 7-7, April.
    2. David Sitbon & Ekaterina Boyarchuk & Florent Dingli & Damarys Loew & Geneviève Almouzni, 2020. "Histone variant H3.3 residue S31 is essential for Xenopus gastrulation regardless of the deposition pathway," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    3. Panagis Filippakopoulos & Jun Qi & Sarah Picaud & Yao Shen & William B. Smith & Oleg Fedorov & Elizabeth M. Morse & Tracey Keates & Tyler T. Hickman & Ildiko Felletar & Martin Philpott & Shonagh Munro, 2010. "Selective inhibition of BET bromodomains," Nature, Nature, vol. 468(7327), pages 1067-1073, December.
    4. Hua Wang & Zheng Fan & Pavel V. Shliaha & Matthew Miele & Ronald C. Hendrickson & Xuejun Jiang & Kristian Helin, 2023. "Author Correction: H3K4me3 regulates RNA polymerase II promoter-proximal pause-release," Nature, Nature, vol. 623(7987), pages 8-8, November.
    5. Caryn S. Ross-Innes & Rory Stark & Andrew E. Teschendorff & Kelly A. Holmes & H. Raza Ali & Mark J. Dunning & Gordon D. Brown & Ondrej Gojis & Ian O. Ellis & Andrew R. Green & Simak Ali & Suet-Feung C, 2012. "Differential oestrogen receptor binding is associated with clinical outcome in breast cancer," Nature, Nature, vol. 481(7381), pages 389-393, January.
    6. John Arne Dahl & Inkyung Jung & Håvard Aanes & Gareth D. Greggains & Adeel Manaf & Mads Lerdrup & Guoqiang Li & Samantha Kuan & Bin Li & Ah Young Lee & Sebastian Preissl & Ingunn Jermstad & Mads Haugl, 2016. "Broad histone H3K4me3 domains in mouse oocytes modulate maternal-to-zygotic transition," Nature, Nature, vol. 537(7621), pages 548-552, September.
    7. Hua Wang & Zheng Fan & Pavel V. Shliaha & Matthew Miele & Ronald C. Hendrickson & Xuejun Jiang & Kristian Helin, 2023. "H3K4me3 regulates RNA polymerase II promoter-proximal pause-release," Nature, Nature, vol. 615(7951), pages 339-348, March.
    8. Nadine L. Vastenhouw & Yong Zhang & Ian G. Woods & Farhad Imam & Aviv Regev & X. Shirley Liu & John Rinn & Alexander F. Schier, 2010. "Chromatin signature of embryonic pluripotency is established during genome activation," Nature, Nature, vol. 464(7290), pages 922-926, April.
    9. Francesco Cardamone & Annamaria Piva & Eva Löser & Bastian Eichenberger & Mari Carmen Romero-Mulero & Fides Zenk & Emily J. Shields & Nina Cabezas-Wallscheid & Roberto Bonasio & Guido Tiana & Yinxiu Z, 2025. "Chromatin landscape at cis-regulatory elements orchestrates cell fate decisions in early embryogenesis," Nature Communications, Nature, vol. 16(1), pages 1-22, December.
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