Literature DB >> 35147496

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

Gabriel Cavin-Meza1, Michelle M Kwan1, Sarah M Wignall1.   

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 the mechanisms that promote acentrosomal spindle stability. To this end, we have optimized the auxin-inducible degron system in Caenorhabditis elegans to remove the factors from pre-formed oocyte spindles within minutes and assess the 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.
© 2022, Cavin-Meza et al.

Entities:  

Keywords:  C. elegans; acentrosomal; cell biology; genetics; genomics; meiosis; microtubule; motor; oocyte; spindle

Mesh:

Substances:

Year:  2022        PMID: 35147496      PMCID: PMC8963883          DOI: 10.7554/eLife.72872

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.713


  64 in total

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Journal:  Curr Biol       Date:  2001-11-27       Impact factor: 10.834

4.  Kinesin-12 differentially affects spindle assembly depending on its microtubule substrate.

Authors:  Emma G Sturgill; Ryoma Ohi
Journal:  Curr Biol       Date:  2013-06-20       Impact factor: 10.834

5.  Kif15 cooperates with eg5 to promote bipolar spindle assembly.

Authors:  Marvin E Tanenbaum; Libor Macůrek; Aniek Janssen; Erica F Geers; Mónica Alvarez-Fernández; René H Medema
Journal:  Curr Biol       Date:  2009-10-08       Impact factor: 10.834

6.  Methods for Rapid Protein Depletion in C. elegans using Auxin-Inducible Degradation.

Authors:  Nikita S Divekar; Hannah E Horton; Sarah M Wignall
Journal:  Curr Protoc       Date:  2021-02

7.  Functional analysis of kinetochore assembly in Caenorhabditis elegans.

Authors:  K Oegema; A Desai; S Rybina; M Kirkham; A A Hyman
Journal:  J Cell Biol       Date:  2001-06-11       Impact factor: 10.539

8.  Excess crossovers impede faithful meiotic chromosome segregation in C. elegans.

Authors:  Jeremy A Hollis; Marissa L Glover; Aleesa J Schlientz; Cori K Cahoon; Bruce Bowerman; Sarah M Wignall; Diana E Libuda
Journal:  PLoS Genet       Date:  2020-09-04       Impact factor: 5.917

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Authors:  Sarah M Wignall; Anne M Villeneuve
Journal:  Nat Cell Biol       Date:  2009-06-14       Impact factor: 28.824

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Authors:  Federico Pelisch; Triin Tammsalu; Bin Wang; Ellis G Jaffray; Anton Gartner; Ronald T Hay
Journal:  Mol Cell       Date:  2016-12-08       Impact factor: 19.328

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