Shape of the first mitotic spindles impacts multinucleation in human embryos

Yuki Ono (), Hiromitsu Shirasawa, Kazumasa Takahashi, Mayumi Goto, Takahiro Ono, Taichi Sakaguchi, Motonari Okabe, Takeo Hirakawa, Takuya Iwasawa, Akiko Fujishima, Tae Sugawara, Kenichi Makino, Hiroshi Miura, Noritaka Fukunaga, Yoshimasa Asada, Yukiyo Kumazawa and Yukihiro Terada
Additional contact information
Yuki Ono: Akita University Graduate School of Medicine
Hiromitsu Shirasawa: Akita University Graduate School of Medicine
Kazumasa Takahashi: Akita University Graduate School of Medicine
Mayumi Goto: Akita University Graduate School of Medicine
Takahiro Ono: Akita University Graduate School of Medicine
Taichi Sakaguchi: Akita University Graduate School of Medicine
Motonari Okabe: Akita University Graduate School of Medicine
Takeo Hirakawa: Akita University Graduate School of Medicine
Takuya Iwasawa: Akita University Graduate School of Medicine
Akiko Fujishima: Akita University Graduate School of Medicine
Tae Sugawara: Akita University Graduate School of Medicine
Kenichi Makino: Akita University Graduate School of Medicine
Hiroshi Miura: Akita University Graduate School of Medicine
Noritaka Fukunaga: Asada Ladies Clinic
Yoshimasa Asada: Asada Ladies Clinic
Yukiyo Kumazawa: Akita University Graduate School of Medicine
Yukihiro Terada: Akita University Graduate School of Medicine

Nature Communications, 2024, vol. 15, issue 1, 1-13

Abstract: Abstract During human embryonic development, early cleavage-stage embryos are more susceptible to errors. Studies have shown that many problems occur during the first mitosis, such as direct cleavage, chromosome segregation errors, and multinucleation. However, the mechanisms whereby these errors occur during the first mitosis in human embryos remain unknown. To clarify this aspect, in the present study, we image discarded living human two-pronuclear stage zygotes using fluorescent labeling and confocal microscopy without microinjection of DNA or mRNA and investigate the association between spindle shape and nuclear abnormality during the first mitosis. We observe that the first mitotic spindles vary, and low-aspect-ratio-shaped spindles tend to lead to the formation of multiple nuclei at the 2-cell stage. Moreover, we observe defocusing poles in many of the first mitotic spindles, which are strongly associated with multinucleation. Additionally, we show that differences in the positions of the centrosomes cause spindle abnormality in the first mitosis. Furthermore, many multinuclei are modified to form mononuclei after the second mitosis because the occurrence of pole defocusing is firmly reduced. Our study will contribute markedly to research on the occurrence of mitotic errors during the early cleavage of human embryos.

Date: 2024
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DOI: 10.1038/s41467-024-49815-8

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