Inherent Instability of Correct Kinetochore-Microtubule Attachments during Meiosis I in Oocytes

•Correct KT-MT attachments on stretched bivalents are unstable in oocytes•Aurora B/C is located close to KT-MT attachment sites on stretched bivalents•Aurora B/C facilitates incorrect KT-MT attachment on stretched bivalents•Oocyte MI lacks coordination of bivalent stretching and KT phosphoregulation

SummaryA model for mitosis suggests that correct kinetochore-microtubule (KT-MT) attachments are stabilized by spatial separation of the attachment sites from Aurora B kinase through sister KT stretching. However, the spatiotemporal regulation of attachment stability during meiosis I (MI) in oocytes remains unclear. Here, we found that in mouse oocytes, Aurora B and C (B/C) are located in close proximity to KT-MT attachment sites after bivalent stretching due to an intrinsic property of the MI chromosomes. The Aurora B/C activity destabilizes correct attachments while allowing a considerable amount of incorrect attachments to form. KT-MT attachments are eventually stabilized through KT dephosphorylation by PP2A-B56 phosphatase, which is progressively recruited to KTs depending on the BubR1 phosphorylation resulting from the timer Cdk1 and independent of bivalent stretching. Thus, oocytes lack a mechanism for coordinating bivalent stretching and KT phosphoregulation during MI, which may explain the high frequency of KT-MT attachment errors.

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