Abstract
In many species, oocyte meiosis is carried out in the absence of centrioles. As a result, microtubule organization, spindle assembly, and chromosome segregation proceed by unique mechanisms. Here, we report insights into the principles underlying this specialized form of cell division, through studies of C. elegans KLP-15 and KLP-16, two highly homologous members of the kinesin-14 family of minus-end-directed kinesins. These proteins localize to the acentriolar oocyte spindle and promote microtubule bundling during spindle assembly; following KLP-15/16 depletion, microtubule bundles form but then collapse into a disorganized array. Surprisingly, despite this defect we found that during anaphase, microtubules are able to reorganize into a bundled array that facilitates chromosome segregation. This phenotype therefore enabled us to identify factors promoting microtubule organization during anaphase, whose contributions are normally undetectable in wild-type worms; we found that SPD-1 (PRC1) bundles microtubules and KLP-18 (kinesin-12) likely sorts those bundles into a functional orientation capable of mediating chromosome segregation. Therefore, our studies have revealed an interplay between distinct mechanisms that together promote spindle formation and chromosome segregation in the absence of structural cues such as centrioles.
Highlights
During mitosis, centriole-containing centrosomes duplicate and move to opposite ends of the cell where they nucleate microtubules and form the spindle poles
Using C. elegans oocyte meiosis as a model, we recently found that acentriolar spindle assembly in this system proceeds by: 1) formation of a cage-like structure comprised of prominent bundles of microtubules that are constrained by the disassembling nuclear envelope, 2) reorganization of this structure such that the microtubule minus-ends are sorted away from the chromosomes to the periphery of the array where they are focused into multiple nascent poles, and 3) coalescence of these poles until bipolarity is achieved [2]
We have identified KLP-15 and KLP-16, members of the conserved kinesin-14 family of minus-end-directed kinesins [21], as factors required for microtubule bundling and organization during acentriolar spindle assembly in C. elegans oocytes; in the absence of these proteins, spindles are unable to maintain stable microtubule bundles and as a result are severely aberrant at metaphase and early anaphase
Summary
Centriole-containing centrosomes duplicate and move to opposite ends of the cell where they nucleate microtubules and form the spindle poles. Using C. elegans oocyte meiosis as a model, we recently found that acentriolar spindle assembly in this system proceeds by: 1) formation of a cage-like structure comprised of prominent bundles of microtubules that are constrained by the disassembling nuclear envelope, 2) reorganization of this structure such that the microtubule minus-ends are sorted away from the chromosomes to the periphery of the array where they are focused into multiple nascent poles, and 3) coalescence of these poles until bipolarity is achieved [2] During this process, the microtubule bundles project into the space near the homologous chromosome pairs (bivalents) and begin to form lateral associations with them, an interaction that is maintained through anaphase. These rings localize to chromosomes during spindle formation [3] and are removed from chromosomes in anaphase, remaining in the channels in the center of the spindle [8]
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