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Revisiting the mystery of centrioles at the beginning of mammalian embryogenesis

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Abstract

The prevailing assumption has been that the human spermatozoon provides only one centriole to the zygote: the proximal centriole, with a canonical, cylinder-like shape. This overly simplistic view has come under challenge since discovering that the human spermatozoon provides a second, atypical centriole to the zygote. The study of human zygotes is challenging for ethical reasons, and bovine zygotes provide an important model due to a similarity in centrosome embryonic inherence and function. Detailed ultrastructural analyses by Uzbekov and colleagues identify the persistence of atypical centrioles in bovine early embryos, raising questions about the original single-centriole model. Whether the parental origin of nascent atypical centrioles or their wide structural diversity and deviation from the canonical centriolar form in blastomeres constitutes sufficient evidence to warrant a reconsideration of the single-centriole model is discussed herein. Because previous human studies identified only one canonical centriole in the zygote, atypical centrioles are likely present in the early human embryo; therefore, it is time to rethink the role of paternal centrioles in human development.

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References

  1. Manandhar G, Simerly C, Schatten G. Highly degenerated distal centrioles in rhesus and human spermatozoa. Hum Reprod. 2000;15(2):256–63.

    Article  CAS  PubMed  Google Scholar 

  2. Crozet N. Behavior of the sperm centriole during sheep oocyte fertilization. Eur J Cell Biol. 1990;53(2):326–32.

    CAS  PubMed  Google Scholar 

  3. Avidor-Reiss T. Rapid evolution of sperm produces diverse centriole structures that reveal the most rudimentary structure needed for function. Cells. 2018;7(7):67.

    Article  PubMed  PubMed Central  Google Scholar 

  4. Fishman EL, et al. A novel atypical sperm centriole is functional during human fertilization. Nat Commun. 2018;9(1):2210.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Uzbekov R, et al. Centrosome formation in the bovine early embryo. Cells. 2023;12(9):1335.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Schatten H, et al. Behavior of centrosomes during fertilization and cell division in mouse oocytes and in sea urchin eggs. Proc Natl Acad Sci U S A. 1986;83(1):105–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Leung MR, et al. The multi-scale architecture of mammalian sperm flagella and implications for ciliary motility. EMBO J. 2021;40(7):e107410.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Khanal S, et al. A dynamic basal complex modulates mammalian sperm movement. Nat Commun. 2021;12(1):3808.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Amargant F, et al. The human sperm basal body is a complex centrosome important for embryo preimplantation development. Mol Hum Reprod. 2021;27(11);gaab062.

  10. Nakamura S, et al. Human sperm aster formation and pronuclear decondensation in bovine eggs following intracytoplasmic sperm injection using a Piezo-driven pipette: a novel assay for human sperm centrosomal function. Biol Reprod. 2001;65(5):1359–63.

    Article  CAS  PubMed  Google Scholar 

  11. Simerly C, et al. The paternal inheritance of the centrosome, the cell's microtubule-organizing center, in humans, and the implications for infertility. Nat Med. 1995;1(1):47–52.

    Article  PubMed  Google Scholar 

  12. Cavazza T, et al. Parental genome unification is highly error-prone in mammalian embryos. Cell. 2021;184(11):2860–2877 e22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Schneider I, et al. Dual spindles assemble in bovine zygotes despite the presence of paternal centrosomes. J Cell Biol. 2021;220(11):e202010106.

  14. Loppin B, Dubruille R, Horard B. The intimate genetics of Drosophila fertilization. Open Biol. 2015;5(8):150076.

  15. Kawamura N. Fertilization and the first cleavage mitosis in insects. Dev Growth Differ. 2001;43(4):343–9.

    Article  CAS  PubMed  Google Scholar 

  16. Sathananthan AH, et al. The sperm centriole: its inheritance, replication and perpetuation in early human embryos. Hum Reprod. 1996;11(2):345–56.

    Article  CAS  PubMed  Google Scholar 

  17. Sathananthan AH, et al. Centrioles in the beginning of human development. Proc Natl Acad Sci U S A. 1991;88(11):4806–10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Reese ST, et al. Pregnancy loss in beef cattle: a meta-analysis. Anim Reprod Sci. 2020;212:106251.

    Article  CAS  PubMed  Google Scholar 

  19. Quenby S, et al. Miscarriage matters: the epidemiological, physical, psychological, and economic costs of early pregnancy loss. Lancet. 2021;397(10285):1658–67.

    Article  CAS  PubMed  Google Scholar 

  20. Macklon NS, Geraedts JP, Fauser BC. Conception to ongoing pregnancy: the 'black box' of early pregnancy loss. Hum Reprod Update. 2002;8(4):333–43.

    Article  CAS  PubMed  Google Scholar 

  21. ACOG. ACOG Practice bulletin No. 200: Early pregnancy loss. Obstet Gynecol. 2018;132(5):e197–e207.

  22. Koyama H, et al. Analysis of polarity of bovine and rabbit embryos by scanning electron microscopy. Biol Reprod. 1994;50(1):163–70.

    Article  CAS  PubMed  Google Scholar 

  23. Bangs FK, et al. Lineage specificity of primary cilia in the mouse embryo. Nat Cell Biol. 2015;17(2):113–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank Derek Kluczynski, Katerina Turner, Luke A. Achinger, Nahshon Puente, and David Albertini for editing and commenting on the manuscript.

Funding

This project was supported by Agriculture and Food Research Initiative Competitive Grant number OHOW-2020-02790 from the USDA National Institute of Food and Agriculture and Grant number 1R15HD110863 from NIH-NICHD.

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Authors and Affiliations

  1. Department of Biological Sciences, College of Natural Sciences and Mathematics, University of Toledo, Toledo, OH, 43607, USA

    Tomer Avidor-Reiss

  2. Department of Urology, College of Medicine and Life Sciences, University of Toledo, Toledo, OH, 43607, USA

    Tomer Avidor-Reiss

  3. Laboratory of Cell Biology and Electron Microscopy, Faculty of Medicine, University of Tours, 37032, Tours, France

    Rustem Uzbekov

  4. Faculty of Bioengineering and Bioinformatics, Moscow State University, 119992, Moscow, Russia

    Rustem Uzbekov

Authors
  1. Tomer Avidor-Reiss
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  2. Rustem Uzbekov
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Correspondence to Tomer Avidor-Reiss.

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The authors declare no competing interests.

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Highlights

• Most early embryonic centrioles are structurally atypical.

• The atypical spermatozoan distal centriole remains atypical in the embryo while “duplicating” new centrioles.

• The canonical spermatozoan proximal centriole changes in the embryo, sometimes acquiring an atypical structure.

• The first two new centrioles formed in the zygote are structurally atypical.

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Avidor-Reiss, T., Uzbekov, R. Revisiting the mystery of centrioles at the beginning of mammalian embryogenesis. J Assist Reprod Genet 40, 2539–2543 (2023). https://doi.org/10.1007/s10815-023-02927-4

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  • DOI: https://doi.org/10.1007/s10815-023-02927-4

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