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The first mitotic division of human embryos is highly error prone

Author

Listed:
  • Cerys E. Currie

    (University of Warwick
    University of Warwick)

  • Emma Ford

    (University of Warwick
    University of Warwick)

  • Lucy Benham Whyte

    (University Hospitals Coventry and Warwickshire NHS Trust
    Fetal Medicine Research Institute)

  • Deborah M. Taylor

    (University Hospitals Coventry and Warwickshire NHS Trust)

  • Bettina P. Mihalas

    (University of Edinburgh)

  • Muriel Erent

    (University of Warwick
    University of Warwick)

  • Adele L. Marston

    (University of Edinburgh)

  • Geraldine M. Hartshorne

    (University of Warwick
    University Hospitals Coventry and Warwickshire NHS Trust
    University of Warwick)

  • Andrew D. McAinsh

    (University of Warwick
    University of Warwick
    University of Warwick)

Abstract

Human beings are made of ~50 trillion cells which arise from serial mitotic divisions of a single cell - the fertilised egg. Remarkably, the early human embryo is often chromosomally abnormal, and many are mosaic, with the karyotype differing from one cell to another. Mosaicism presumably arises from chromosome segregation errors during the early mitotic divisions, although these events have never been visualised in living human embryos. Here, we establish live cell imaging of chromosome segregation using normally fertilised embryos from an egg-share-to-research programme, as well as embryos deselected during fertility treatment. We reveal that the first mitotic division has an extended prometaphase/metaphase and exhibits phenotypes that can cause nondisjunction. These included multipolar chromosome segregations and lagging chromosomes that lead to formation of micronuclei. Analysis of nuclear number and size provides evidence of equivalent phenotypes in 2-cell human embryos that gave rise to live births. Together this shows that errors in the first mitotic division can be tolerated in human embryos and uncovers cell biological events that contribute to preimplantation mosaicism.

Suggested Citation

  • Cerys E. Currie & Emma Ford & Lucy Benham Whyte & Deborah M. Taylor & Bettina P. Mihalas & Muriel Erent & Adele L. Marston & Geraldine M. Hartshorne & Andrew D. McAinsh, 2022. "The first mitotic division of human embryos is highly error prone," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-34294-6
    DOI: 10.1038/s41467-022-34294-6
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    References listed on IDEAS

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    1. Helen Bolton & Sarah J. L. Graham & Niels Van der Aa & Parveen Kumar & Koen Theunis & Elia Fernandez Gallardo & Thierry Voet & Magdalena Zernicka-Goetz, 2016. "Mouse model of chromosome mosaicism reveals lineage-specific depletion of aneuploid cells and normal developmental potential," Nature Communications, Nature, vol. 7(1), pages 1-12, September.
    2. Karen Crasta & Neil J. Ganem & Regina Dagher & Alexandra B. Lantermann & Elena V. Ivanova & Yunfeng Pan & Luigi Nezi & Alexei Protopopov & Dipanjan Chowdhury & David Pellman, 2012. "DNA breaks and chromosome pulverization from errors in mitosis," Nature, Nature, vol. 482(7383), pages 53-58, February.
    3. Avery Davis Bell & Curtis J. Mello & James Nemesh & Sara A. Brumbaugh & Alec Wysoker & Steven A. McCarroll, 2020. "Insights into variation in meiosis from 31,228 human sperm genomes," Nature, Nature, vol. 583(7815), pages 259-264, July.
    4. Yogo Sakakibara & Shu Hashimoto & Yoshiharu Nakaoka & Anna Kouznetsova & Christer Höög & Tomoya S. Kitajima, 2015. "Bivalent separation into univalents precedes age-related meiosis I errors in oocytes," Nature Communications, Nature, vol. 6(1), pages 1-8, November.
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