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A prometaphase mechanism of securin destruction is essential for meiotic progression in mouse oocytes

Author

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  • Christopher Thomas

    (Biosciences Institute, Faculty of Medical Sciences, Newcastle University
    Max Planck Institute for Biophysical Chemistry)

  • Benjamin Wetherall

    (Biosciences Institute, Faculty of Medical Sciences, Newcastle University)

  • Mark D. Levasseur

    (Biosciences Institute, Faculty of Medical Sciences, Newcastle University)

  • Rebecca J. Harris

    (Biosciences Institute, Faculty of Medical Sciences, Newcastle University)

  • Scott T. Kerridge

    (Biosciences Institute, Faculty of Medical Sciences, Newcastle University)

  • Jonathan M. G. Higgins

    (Biosciences Institute, Faculty of Medical Sciences, Newcastle University)

  • Owen R. Davies

    (Biosciences Institute, Faculty of Medical Sciences, Newcastle University
    Institute of Cell Biology, University of Edinburgh, Michael Swann Building, Max Born Crescent)

  • Suzanne Madgwick

    (Biosciences Institute, Faculty of Medical Sciences, Newcastle University)

Abstract

Successful cell division relies on the timely removal of key cell cycle proteins such as securin. Securin inhibits separase, which cleaves the cohesin rings holding chromosomes together. Securin must be depleted before anaphase to ensure chromosome segregation occurs with anaphase. Here we find that in meiosis I, mouse oocytes contain an excess of securin over separase. We reveal a mechanism that promotes excess securin destruction in prometaphase I. Importantly, this mechanism relies on two phenylalanine residues within the separase-interacting segment (SIS) of securin that are only exposed when securin is not bound to separase. We suggest that these residues facilitate the removal of non-separase-bound securin ahead of metaphase, as inhibiting this period of destruction by mutating both residues causes the majority of oocytes to arrest in meiosis I. We further propose that cellular securin levels exceed the amount an oocyte is capable of removing in metaphase alone, such that the prometaphase destruction mechanism identified here is essential for correct meiotic progression in mouse oocytes.

Suggested Citation

  • Christopher Thomas & Benjamin Wetherall & Mark D. Levasseur & Rebecca J. Harris & Scott T. Kerridge & Jonathan M. G. Higgins & Owen R. Davies & Suzanne Madgwick, 2021. "A prometaphase mechanism of securin destruction is essential for meiotic progression in mouse oocytes," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-24554-2
    DOI: 10.1038/s41467-021-24554-2
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    References listed on IDEAS

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    1. Zhe Wei & Jessica Greaney & Chenxi Zhou & Hayden Homer, 2018. "Cdk1 inactivation induces post-anaphase-onset spindle migration and membrane protrusion required for extreme asymmetry in mouse oocytes," Nature Communications, Nature, vol. 9(1), pages 1-15, December.
    2. Frank Uhlmann & Friedrich Lottspeich & Kim Nasmyth, 1999. "Sister-chromatid separation at anaphase onset is promoted by cleavage of the cohesin subunit Scc1," Nature, Nature, vol. 400(6739), pages 37-42, July.
    3. William C. H. Chao & Kiran Kulkarni & Ziguo Zhang & Eric H. Kong & David Barford, 2012. "Structure of the mitotic checkpoint complex," Nature, Nature, vol. 484(7393), pages 208-213, April.
    4. Zhonghui Lin & Xuelian Luo & Hongtao Yu, 2016. "Structural basis of cohesin cleavage by separase," Nature, Nature, vol. 532(7597), pages 131-134, April.
    5. Leifu Chang & Ziguo Zhang & Jing Yang & Stephen H. McLaughlin & David Barford, 2014. "Molecular architecture and mechanism of the anaphase-promoting complex," Nature, Nature, vol. 513(7518), pages 388-393, September.
    6. Shukun Luo & Liang Tong, 2017. "Molecular mechanism for the regulation of yeast separase by securin," Nature, Nature, vol. 542(7640), pages 255-259, February.
    7. Suyang Zhang & Thomas Tischer & David Barford, 2019. "Cyclin A2 degradation during the spindle assembly checkpoint requires multiple binding modes to the APC/C," Nature Communications, Nature, vol. 10(1), pages 1-16, December.
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    Cited by:

    1. Devashish Dwivedi & Daniela Harry & Patrick Meraldi, 2023. "Mild replication stress causes premature centriole disengagement via a sub-critical Plk1 activity under the control of ATR-Chk1," Nature Communications, Nature, vol. 14(1), pages 1-16, December.

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