Abstract

Mammalian oocytes assemble a bipolar acentriolar microtubule spindle to segregate chromosomes during asymmetric division. There is increasing evidence that actin in the spindle interior not only participates in spindle migration and positioning but also protects oocytes from chromosome segregation errors leading to aneuploidy. Here we show that actin is an integral component of the meiotic machinery that closely interacts with microtubules during all major events of human oocyte maturation from the time point of spindle assembly till polar body extrusion and metaphase arrest. With the aid of drugs selectively affecting cytoskeleton dynamics and transiently disturbing the integrity of the two cytoskeleton systems, we identify interdependent structural rearrangements indicative of a close communication between actin and microtubules as fundamental feature of human oocytes. Our data support a model of actin-microtubule interplay that is essential for bipolar spindle assembly and correct partitioning of the nuclear genome in human oocyte meiosis.

Highlights

  • Mammalian oocytes assemble a bipolar acentriolar microtubule spindle to segregate chromosomes during asymmetric division

  • We set-up an experimental strategy based on multi-color 3Dfluorescence microscopy that allowed us to monitor the spatiotemporal organization of actin and microtubules simultaneously, starting from NEBD till the stage of metaphase II (MII) arrest

  • We established that actin is an essential component of the human oocyte spindle throughout the entire oocyte maturation process, where it accompanies microtubule dynamics during spindle formation and asymmetric division in meiosis I, and during the subsequent stages of spindle decomposition and spindle reconstruction in meiosis II

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Summary

Introduction

Mammalian oocytes assemble a bipolar acentriolar microtubule spindle to segregate chromosomes during asymmetric division. A number of studies mainly conducted with the mouse oocyte model show that actin is crucial for spindle migration and anchorage[13], but it protects the maturing oocyte from chromosome segregation errors by promoting the formation of kinetochore-fibers that mediate stable microtubule-chromosome attachments[14]. This mechanism is thought to reduce the frequency of erroneous chromosome movements that are responsible for misdistributions leading to aneuploidy. Using drug treatments to disrupt the microtubule and actin spindles, we identify an important role of actin for microtubule-based spindle organization in human oocytes

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