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Parental genomes segregate into distinct blastomeres during multipolar zygotic divisions leading to mixoploid and chimeric blastocysts

Tine De Coster (UGent) , Heleen Masset, Olga Tsuiko, Maaike Catteeuw (UGent) , Yan Zhao, Nicolas Dierckxsens, Ainhoa Larreategui Aparicio, Eftychia Dimitriadou, Sophie Debrock, Karen Peeraer, et al.
(2022) GENOME BIOLOGY. 23(1).
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Abstract
Background During normal zygotic division, two haploid parental genomes replicate, unite and segregate into two biparental diploid blastomeres. Results Contrary to this fundamental biological tenet, we demonstrate here that parental genomes can segregate to distinct blastomeres during the zygotic division resulting in haploid or uniparental diploid and polyploid cells, a phenomenon coined heterogoneic division. By mapping the genomic landscape of 82 blastomeres from 25 bovine zygotes, we show that multipolar zygotic division is a tell-tale of whole-genome segregation errors. Based on the haplotypes and live-imaging of zygotic divisions, we demonstrate that various combinations of androgenetic, gynogenetic, diploid, and polyploid blastomeres arise via distinct parental genome segregation errors including the formation of additional paternal, private parental, or tripolar spindles, or by extrusion of paternal genomes. Hence, we provide evidence that private parental spindles, if failing to congress before anaphase, can lead to whole-genome segregation errors. In addition, anuclear blastomeres are common, indicating that cytokinesis can be uncoupled from karyokinesis. Dissociation of blastocyst-stage embryos further demonstrates that whole-genome segregation errors might lead to mixoploid or chimeric development in both human and cow. Yet, following multipolar zygotic division, fewer embryos reach the blastocyst stage and diploidization occurs frequently indicating that alternatively, blastomeres with genome-wide errors resulting from whole-genome segregation errors can be selected against or contribute to embryonic arrest. Conclusions Heterogoneic zygotic division provides an overarching paradigm for the development of mixoploid and chimeric individuals and moles and can be an important cause of embryonic and fetal arrest following natural conception or IVF.
Keywords
PATERNAL UNIPARENTAL DISOMY, IN-VITRO FERTILIZATION, CHROMOSOMAL, MOSAICISM, HUMAN OOCYTES, DIPLOID/TRIPLOID MOSAICISM, CYTOGENETIC, ANALYSIS, BOVINE EMBRYOS, INVITRO FERTILIZATION, ERROR-PRONE, FOLLOW-UP, Zygote, Mitosis, Whole-genome segregation errors, Chromosomal, instability, Triploidy, Chimerism, Mixoploidy, Mola, Multipolar, division, Heterogoneic division

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MLA
De Coster, Tine, et al. “Parental Genomes Segregate into Distinct Blastomeres during Multipolar Zygotic Divisions Leading to Mixoploid and Chimeric Blastocysts.” GENOME BIOLOGY, vol. 23, no. 1, 2022, doi:10.1186/s13059-022-02763-2.
APA
De Coster, T., Masset, H., Tsuiko, O., Catteeuw, M., Zhao, Y., Dierckxsens, N., … Vermeesch, J. R. (2022). Parental genomes segregate into distinct blastomeres during multipolar zygotic divisions leading to mixoploid and chimeric blastocysts. GENOME BIOLOGY, 23(1). https://doi.org/10.1186/s13059-022-02763-2
Chicago author-date
De Coster, Tine, Heleen Masset, Olga Tsuiko, Maaike Catteeuw, Yan Zhao, Nicolas Dierckxsens, Ainhoa Larreategui Aparicio, et al. 2022. “Parental Genomes Segregate into Distinct Blastomeres during Multipolar Zygotic Divisions Leading to Mixoploid and Chimeric Blastocysts.” GENOME BIOLOGY 23 (1). https://doi.org/10.1186/s13059-022-02763-2.
Chicago author-date (all authors)
De Coster, Tine, Heleen Masset, Olga Tsuiko, Maaike Catteeuw, Yan Zhao, Nicolas Dierckxsens, Ainhoa Larreategui Aparicio, Eftychia Dimitriadou, Sophie Debrock, Karen Peeraer, Marta de Ruijter-Villani, Katrien Smits, Ann Van Soom, and Joris Robert Vermeesch. 2022. “Parental Genomes Segregate into Distinct Blastomeres during Multipolar Zygotic Divisions Leading to Mixoploid and Chimeric Blastocysts.” GENOME BIOLOGY 23 (1). doi:10.1186/s13059-022-02763-2.
Vancouver
1.
De Coster T, Masset H, Tsuiko O, Catteeuw M, Zhao Y, Dierckxsens N, et al. Parental genomes segregate into distinct blastomeres during multipolar zygotic divisions leading to mixoploid and chimeric blastocysts. GENOME BIOLOGY. 2022;23(1).
IEEE
[1]
T. De Coster et al., “Parental genomes segregate into distinct blastomeres during multipolar zygotic divisions leading to mixoploid and chimeric blastocysts,” GENOME BIOLOGY, vol. 23, no. 1, 2022.
@article{8771375,
  abstract     = {{Background During normal zygotic division, two haploid parental genomes replicate, unite and segregate into two biparental diploid blastomeres. Results Contrary to this fundamental biological tenet, we demonstrate here that parental genomes can segregate to distinct blastomeres during the zygotic division resulting in haploid or uniparental diploid and polyploid cells, a phenomenon coined heterogoneic division. By mapping the genomic landscape of 82 blastomeres from 25 bovine zygotes, we show that multipolar zygotic division is a tell-tale of whole-genome segregation errors. Based on the haplotypes and live-imaging of zygotic divisions, we demonstrate that various combinations of androgenetic, gynogenetic, diploid, and polyploid blastomeres arise via distinct parental genome segregation errors including the formation of additional paternal, private parental, or tripolar spindles, or by extrusion of paternal genomes. Hence, we provide evidence that private parental spindles, if failing to congress before anaphase, can lead to whole-genome segregation errors. In addition, anuclear blastomeres are common, indicating that cytokinesis can be uncoupled from karyokinesis. Dissociation of blastocyst-stage embryos further demonstrates that whole-genome segregation errors might lead to mixoploid or chimeric development in both human and cow. Yet, following multipolar zygotic division, fewer embryos reach the blastocyst stage and diploidization occurs frequently indicating that alternatively, blastomeres with genome-wide errors resulting from whole-genome segregation errors can be selected against or contribute to embryonic arrest. Conclusions Heterogoneic zygotic division provides an overarching paradigm for the development of mixoploid and chimeric individuals and moles and can be an important cause of embryonic and fetal arrest following natural conception or IVF.}},
  articleno    = {{201}},
  author       = {{De Coster, Tine and Masset, Heleen and Tsuiko, Olga and Catteeuw, Maaike and Zhao, Yan and Dierckxsens, Nicolas and Aparicio, Ainhoa Larreategui and Dimitriadou, Eftychia and Debrock, Sophie and Peeraer, Karen and de Ruijter-Villani, Marta and Smits, Katrien and Van Soom, Ann and Vermeesch, Joris Robert}},
  issn         = {{1474-760X}},
  journal      = {{GENOME BIOLOGY}},
  keywords     = {{PATERNAL UNIPARENTAL DISOMY,IN-VITRO FERTILIZATION,CHROMOSOMAL,MOSAICISM,HUMAN OOCYTES,DIPLOID/TRIPLOID MOSAICISM,CYTOGENETIC,ANALYSIS,BOVINE EMBRYOS,INVITRO FERTILIZATION,ERROR-PRONE,FOLLOW-UP,Zygote,Mitosis,Whole-genome segregation errors,Chromosomal,instability,Triploidy,Chimerism,Mixoploidy,Mola,Multipolar,division,Heterogoneic division}},
  language     = {{eng}},
  number       = {{1}},
  pages        = {{29}},
  title        = {{Parental genomes segregate into distinct blastomeres during multipolar zygotic divisions leading to mixoploid and chimeric blastocysts}},
  url          = {{http://doi.org/10.1186/s13059-022-02763-2}},
  volume       = {{23}},
  year         = {{2022}},
}
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