Assembly of Caenorhabditis elegans acentrosomal spindles occurs without evident microtubuleorganizing centers and requires microtubule sorting by KLP-18/kinesin-12 and MESP-1

Ian D. Wolff, Michael V. Tran, Timothy J. Mullen, Anne M. Villeneuve, Sarah M. Wignalla*

*Corresponding author for this work

Research output: Contribution to journalArticle

16 Scopus citations

Abstract

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 fnd 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 confguration in which minus ends are away from the chromosomes, enabling formation of nascent poles.

Original languageEnglish (US)
Pages (from-to)3122-3131
Number of pages10
JournalMolecular biology of the cell
Volume27
Issue number20
DOIs
StatePublished - Oct 15 2016

ASJC Scopus subject areas

  • Molecular Biology
  • Cell Biology

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