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Zygotic spindle orientation defines cleavage pattern and nuclear status of human embryos

Author

Listed:
  • Volodymyr Porokh

    (Masaryk University)

  • Drahomíra Kyjovská

    (Clinic of Reproductive Medicine)

  • Martina Martonová

    (Clinic of Reproductive Medicine)

  • Tereza Klenková

    (Clinic of Reproductive Medicine)

  • Pavel Otevřel

    (Clinic of Reproductive Medicine)

  • Soňa Kloudová

    (Masaryk University
    Clinic of Reproductive Medicine)

  • Zuzana Holubcová

    (Masaryk University
    Clinic of Reproductive Medicine)

Abstract

The first embryonic division represents a starting point for the development of a new individual. In many species, tight control over the first embryonic division ensures its accuracy. However, the first division in humans is often erroneous and can impair embryo development. To delineate the spatiotemporal organization of the first mitotic division typical for normal human embryo development, we systematically analyzed a unique timelapse dataset of 300 IVF embryos that developed into healthy newborns. The zygotic division pattern of these best-quality embryos was compared to their siblings that failed to implant or arrested during cleavage stage. We show that division at the right angle to the juxtaposed pronuclei is preferential and supports faithful zygotic division. Alternative configurations of the first mitosis are associated with reduced clustering of nucleoli and multinucleation at the 2-cell stage, which are more common in women of advanced age. Collectively, these data imply that orientation of the first division predisposes human embryos to genetic (in)stability and may contribute to aneuploidy and age-related infertility.

Suggested Citation

  • Volodymyr Porokh & Drahomíra Kyjovská & Martina Martonová & Tereza Klenková & Pavel Otevřel & Soňa Kloudová & Zuzana Holubcová, 2024. "Zygotic spindle orientation defines cleavage pattern and nuclear status of human embryos," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-50732-z
    DOI: 10.1038/s41467-024-50732-z
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    References listed on IDEAS

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    1. Emily L. Fishman & Kyoung Jo & Quynh P. H. Nguyen & Dong Kong & Rachel Royfman & Anthony R. Cekic & Sushil Khanal & Ann L. Miller & Calvin Simerly & Gerald Schatten & Jadranka Loncarek & Vito Mennella, 2018. "Author Correction: A novel atypical sperm centriole is functional during human fertilization," Nature Communications, Nature, vol. 9(1), pages 1-1, December.
    2. Lia Mara Gomes Paim & Greg FitzHarris, 2019. "Tetraploidy causes chromosomal instability in acentriolar mouse embryos," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    3. Takashi Hiiragi & Davor Solter, 2004. "First cleavage plane of the mouse egg is not predetermined but defined by the topology of the two apposing pronuclei," Nature, Nature, vol. 430(6997), pages 360-364, July.
    4. Emily L. Fishman & Kyoung Jo & Quynh P. H. Nguyen & Dong Kong & Rachel Royfman & Anthony R. Cekic & Sushil Khanal & Ann L. Miller & Calvin Simerly & Gerald Schatten & Jadranka Loncarek & Vito Mennella, 2018. "A novel atypical sperm centriole is functional during human fertilization," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
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