Journal
MOLECULAR BIOLOGY OF THE CELL
Volume 27, Issue 20, Pages 3122-3131Publisher
AMER SOC CELL BIOLOGY
DOI: 10.1091/mbc.E16-05-0291
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Funding
- National Institutes of Health Office of Research Infrastructure Programs [P40 OD010440]
- Chicago Biomedical Consortium
- Searle Funds at the Chicago Community Trust
- American Cancer Society, Illinois Division [253551]
- American Cancer Society Grant [ACS-IRG 93-037-18]
- National Institutes of Health/National Institute of General Medical Sciences Training Grant [T32GM008382]
- National Institutes of Health/National Cancer Institute Training Grant [T32CA009560]
- National Institutes of Health Grant [RO1 GM53804]
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Although centrosomes contribute to spindle formation in most cell types, oocytes of many species are acentrosomal and must organize spindles in their absence. Here we investigate this process in Caenorhabditis elegans, detailing how acentrosomal spindles form and revealing mechanisms required to establish bipolarity. Using high-resolution imaging, we find that in meiosis I, microtubules initially form a cage-like structure inside the disassembling nuclear envelope. This structure reorganizes so that minus ends are sorted to the periphery of the array, forming multiple nascent poles that then coalesce until bipolarity is achieved. In meiosis II, microtubules nucleate in the vicinity of chromosomes but then undergo similar sorting and pole formation events. We further show that KLP-18/kinesin-12 and MESP-1, previously shown to be required for spindle bipolarity, likely contribute to bipolarity by sorting microtubules. After their depletion, minus ends are not sorted outward at the early stages of spindle assembly and instead converge. These proteins colocalize on microtubules, are interdependent for localization, and can interact, suggesting that they work together. We propose that KLP-18/kinesin-12 and MESP-1 form a complex that functions to sort microtubules of mixed polarity into a configuration in which minus ends are away from the chromosomes, enabling formation of nascent poles.
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