Multiple motors cooperate to establish and maintain acentrosomal spindle bipolarity in C. elegans oocyte meiosis

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Abstract

While centrosomes organize spindle poles during mitosis, oocyte meiosis can occur in their absence. Spindles in human oocytes frequently fail to maintain bipolarity and consequently undergo chromosome segregation errors, making it important to understand mechanisms that promote acentrosomal spindle stability. To this end, we have optimized the auxin-inducible degron system in C. elegans to remove factors from pre-formed oocyte spindles within minutes and assess effects on spindle structure. This approach revealed that dynein is required to maintain the integrity of acentrosomal poles; removal of dynein from bipolar spindles caused pole splaying, and when coupled with a monopolar spindle induced by depletion of the kinesin-12 motor KLP-18, dynein depletion led to a complete dissolution of the monopole. Surprisingly, we went on to discover that following monopole disruption, individual chromosomes were able to reorganize local microtubules and re-establish a miniature bipolar spindle that mediated chromosome segregation. This revealed the existence of redundant microtubule sorting forces that are undetectable when KLP-18 and dynein are active. We found that the kinesin-5 family motor BMK-1 provides this force, uncovering the first evidence that kinesin-5 contributes to C. elegans meiotic spindle organization. Altogether, our studies have revealed how multiple motors are working synchronously to establish and maintain bipolarity in the absence of centrosomes.

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All data generated or analyzed in this study are included in the manuscript and supporting files. Source data files have been provided for Figure 2B, Figure 2 - figure supplement 1, Figure 2 - figure supplement 2, and Figure 4C.

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Gabriel Cavin-Meza

Department of Molecular Biosciences, Northwestern University, Evanston, United States

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-5820-4071
Michelle M Kwan

Department of Molecular Biosciences, Northwestern University, Evanston, United States

Competing interests
The authors declare that no competing interests exist.
Sarah Marie Wignall

Department of Molecular Biosciences, Northwestern University, Evanston, United States

For correspondence
s-wignall@northwestern.edu

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-9828-9356

Funding

National Institute of General Medical Sciences (R01GM124354)

Sarah Marie Wignall

National Cancer Institute (T32CA009560)

Gabriel Cavin-Meza

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.