Abstract
The meiotic spindle is formed without centrosomes in a large volume of oocytes. Local activation of crucial spindle proteins around chromosomes is important for formation and maintenance of a bipolar spindle in oocytes. We found that phosphodocking 14-3-3 proteins stabilize spindle bipolarity in Drosophila melanogaster oocytes. A critical 14-3-3 target is the minus end-directed motor Ncd (human HSET; kinesin-14), which has well-documented roles in stabilizing a bipolar spindle in oocytes. Phospho docking by 14-3-3 inhibits the microtubule binding activity of the nonmotor Ncd tail. Further phosphorylation by Aurora B kinase can release Ncd from this inhibitory effect of 14-3-3. As Aurora B localizes to chromosomes and spindles, 14-3-3 facilitates specific association of Ncd with spindle microtubules by preventing Ncd from binding to nonspindle microtubules in oocytes. Therefore, 14-3-3 translates a spatial cue provided by Aurora B to target Ncd selectively to the spindle within the large volume of oocytes.
Highlights
Meiotic spindle formation in oocytes faces two challenges, lack of centrosomes and a large cytoplasmic volume in oocytes (Ohkura, 2015)
14-3-3 regulates the meiotic spindle in oocytes
Depletion of 14-3-3ε by expressing either of two non-overlapping short-hairpin RNAs in the female germline resulted in similar abnormal spindle morphologies (Fig 1A-C,S1)
Summary
Meiotic spindle formation in oocytes faces two challenges, lack of centrosomes and a large cytoplasmic volume in oocytes (Ohkura, 2015). It has been proposed that, in addition to Ran, chromatin-bound Aurora B provides a critical spatial cue for bipolar spindle assembly in oocytes (Sampath et al, 2004; Colombié et al, 2008; Radford et al, 2012b), but little is yet known about how this signal is translated into spindle morphogenesis, except that it inhibits the microtubule depolymerase kinesin-13 (Ohi et al, 2004). Drosophila provides an advantage in defining in vivo roles of 14-3-3 It has revealed roles in development (Chang and Rubin, 1997; Kockel et al, 1997; Benton et al, 2002), but a role in the meiotic spindles has not been established before. In response to the spatial cue provided by Aurora B, 14-3-3 promotes Ncd binding to spindle microtubules by preventing it from binding other microtubules in the large cytoplasmic volume of oocytes
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