Abstract
Assembly of a bipolar microtubule spindle is essential for accurate chromosome segregation. In somatic cells, spindle bipolarity is determined by the presence of exactly two centrosomes. Remarkably, mammalian oocytes do not contain canonical centrosomes. This study reveals that mouse oocytes assemble a bipolar spindle by fragmenting multiple acentriolar microtubule-organizing centres (MTOCs) into a high number of small MTOCs to be able to then regroup and merge them into two equal spindle poles. We show that MTOCs are fragmented in a three-step process. First, PLK1 triggers a decondensation of the MTOC structure. Second, BicD2-anchored dynein stretches the MTOCs into fragmented ribbons along the nuclear envelope. Third, KIF11 further fragments the MTOCs following nuclear envelope breakdown so that they can be evenly distributed towards the two spindle poles. Failure to fragment MTOCs leads to defects in spindle assembly, which delay chromosome individualization and congression, putting the oocyte at risk of aneuploidy.
Highlights
Of a bipolar microtubule spindle is essential for accurate chromosome segregation
To address how spindle bipolarity is achieved from multiple microtubule-organizing centres (MTOCs), we recorded high-resolution three-dimensional (3D) data sets of MTOCs during spindle assembly in live mouse oocytes
MTOCs were visualized with a tagged version of the pericentriolar material component Cep[192], which we found to be a bona fide marker for MTOCs as judged by colocalization with known MTOC components g-tubulin and Pericentrin (Supplementary Fig. 1)
Summary
Of a bipolar microtubule spindle is essential for accurate chromosome segregation. This study reveals that mouse oocytes assemble a bipolar spindle by fragmenting multiple acentriolar microtubule-organizing centres (MTOCs) into a high number of small MTOCs to be able to regroup and merge them into two equal spindle poles. Spindle microtubules are nucleated by multiple acentriolar microtubule-organizing centres (MTOCs)[7] These MTOCs contain many of the pericentriolar material components[8,9,10] of centrosomes; in contrast to centrosomes, they lack centriole pairs at their core[11]. Our data uncover a novel mechanism that facilitates spindle assembly in the absence of centrosomes: the MTOCs exhibit remarkable plasticity and undergo a three-step decondensation and fragmentation process, which facilitates the equal distribution of MTOC material between the two spindle poles. MTOC fragmentation is essential for accurate spindle assembly in the absence of centrosomes in mouse oocytes
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