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F-actin patches nucleated on chromosomes coordinate capture by microtubules in oocyte meiosis

Mariia Burdyniuk, Andrea Callegari, Masashi Mori, Francois Nedelec, Peter Lenart

Posted on: 20 February 2018

Preprint posted on 13 February 2018

Article now published in The Journal of Cell Biology at http://dx.doi.org/10.1083/jcb.201802080

When actin buys you time - a new preprint shows that large oocytes assemble actin on chromosomes to postpone their capture by microtubules. This gives them enough time to transport all of their chromosomes to the spindle before they are segregated.

Selected by Binyam Mogessie

Background. Chromosome segregation is conserved throughout eukaryotes – a spindle machinery that is assembled from microtubules aligns and equally partitions chromosomes into daughter cells. When disintegration of the nucleus at the start of cell division releases its contents into the cytoplasm, microtubules promptly capture the chromosomes. However, microtubules are not always capable of collecting all the chromosomes for segregation. For example, in large starfish oocytes, a contractile network of actin has to first deliver the chromosomes to microtubules before they can be segregated.

Key findings. How actin-driven collection of scattered chromosomes is coordinated with their capture by microtubules has remained unclear. Burdyniuk et al. now show that in starfish oocytes, actin shields chromosomes from premature attachment to microtubules until all chromosomes have been collected near the assembling spindle. Once all chromosomes have been transported, actin patches on the chromosomes are disassembled to allow their attachment to microtubules. This actin-dependent delay in chromosome capture ensures that no chromosome is left behind when segregation begins – in essence, it buys these large cells enough time to gather even those chromosomes that have scattered farthest away from probing microtubule plus ends.

What I like about this work. My own lab is interested in actin-dependent mechanisms of chromosome segregation in mammalian oocytes – we recently showed that actin filaments prevent aneuploidy in mouse eggs by efficiently bundling spindle microtubules. We have since set out on a quest to discover whether chromosome-mediated assembly of actin filaments reinforces the spindle machinery of mammalian eggs. The revelation that actin is nucleated on starfish oocyte chromosomes particularly strengthens our hypothesis, and indeed we may not be far from the truth. However, I have not selected this preprint solely because it complements our own studies. The work of Burdyniuk et al. goes well beyond confirming suspicions: it defines a previously unknown function of actin in preventing untimely chromosome-microtubule interactions that could otherwise lead to aneuploidy in eggs.

Future directions. Some immediate questions that deserve deeper mechanistic investigation arise from the work of Burdyniuk and colleagues. It remains unclear which mechanisms sense completion of chromosome gathering and selectively disassemble chromosome-associated actin filaments. The authors propose steric blockage of microtubule-chromosome interactions as one possible mechanism for delaying capture. Could actin also accomplish this task by directly binding the chromosomes’ kinetochores to render microtubule binding sites inaccessible? Finally, it will be important to examine whether this mechanism of ensuring timely chromosome-microtubule attachment is conserved in oocytes of other species, including mice and humans.

Tags: actin, aneuploidy, cell division, chromosome segregation, kinetochore, meiosis, microtubule, oocyte

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