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Prc1-rich kinetochores are required for error-free acentrosomal spindle bipolarization during meiosis I in mouse oocytes

Author

Listed:
  • Shuhei Yoshida

    (RIKEN Center for Biosystems Dynamics Research (BDR))

  • Sui Nishiyama

    (RIKEN Center for Biosystems Dynamics Research (BDR)
    Kyoto University)

  • Lisa Lister

    (Biosciences Institute, Newcastle University, Centre for Life, Times Square
    Newcastle Fertility Centre, Centre for Life, Times Square)

  • Shu Hashimoto

    (RIKEN Center for Biosystems Dynamics Research (BDR)
    Osaka City University
    IVF Namba Clinic)

  • Tappei Mishina

    (RIKEN Center for Biosystems Dynamics Research (BDR))

  • Aurélien Courtois

    (RIKEN Center for Biosystems Dynamics Research (BDR))

  • Hirohisa Kyogoku

    (RIKEN Center for Biosystems Dynamics Research (BDR))

  • Takaya Abe

    (Laboratory for Animal Resources and Genetic Engineering, RIKEN Center for Biosystems Dynamics Research (BDR))

  • Aki Shiraishi

    (Laboratory for Animal Resources and Genetic Engineering, RIKEN Center for Biosystems Dynamics Research (BDR))

  • Meenakshi Choudhary

    (Biosciences Institute, Newcastle University, Centre for Life, Times Square
    Newcastle Fertility Centre, Centre for Life, Times Square)

  • Yoshiharu Nakaoka

    (IVF Namba Clinic)

  • Mary Herbert

    (Biosciences Institute, Newcastle University, Centre for Life, Times Square
    Newcastle Fertility Centre, Centre for Life, Times Square)

  • Tomoya S. Kitajima

    (RIKEN Center for Biosystems Dynamics Research (BDR)
    Kyoto University)

Abstract

Acentrosomal meiosis in oocytes represents a gametogenic challenge, requiring spindle bipolarization without predefined bipolar cues. While much is known about the structures that promote acentrosomal microtubule nucleation, less is known about the structures that mediate spindle bipolarization in mammalian oocytes. Here, we show that in mouse oocytes, kinetochores are required for spindle bipolarization in meiosis I. This process is promoted by oocyte-specific, microtubule-independent enrichment of the antiparallel microtubule crosslinker Prc1 at kinetochores via the Ndc80 complex. In contrast, in meiosis II, cytoplasm that contains upregulated factors including Prc1 supports kinetochore-independent pathways for spindle bipolarization. The kinetochore-dependent mode of spindle bipolarization is required for meiosis I to prevent chromosome segregation errors. Human oocytes, where spindle bipolarization is reportedly error prone, exhibit no detectable kinetochore enrichment of Prc1. This study reveals an oocyte-specific function of kinetochores in acentrosomal spindle bipolarization in mice, and provides insights into the error-prone nature of human oocytes.

Suggested Citation

  • Shuhei Yoshida & Sui Nishiyama & Lisa Lister & Shu Hashimoto & Tappei Mishina & Aurélien Courtois & Hirohisa Kyogoku & Takaya Abe & Aki Shiraishi & Meenakshi Choudhary & Yoshiharu Nakaoka & Mary Herbe, 2020. "Prc1-rich kinetochores are required for error-free acentrosomal spindle bipolarization during meiosis I in mouse oocytes," Nature Communications, Nature, vol. 11(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:11:y:2020:i:1:d:10.1038_s41467-020-16488-y
    DOI: 10.1038/s41467-020-16488-y
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    Cited by:

    1. Jurica Matković & Subhadip Ghosh & Mateja Ćosić & Susana Eibes & Marin Barišić & Nenad Pavin & Iva M. Tolić, 2022. "Kinetochore- and chromosome-driven transition of microtubules into bundles promotes spindle assembly," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    2. Shuwen He & John P. Gillies & Juliana L. Zang & Carmen M. Córdoba-Beldad & Io Yamamoto & Yasuhiro Fujiwara & Julie Grantham & Morgan E. DeSantis & Hiroki Shibuya, 2023. "Distinct dynein complexes defined by DYNLRB1 and DYNLRB2 regulate mitotic and male meiotic spindle bipolarity," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

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