KLP-7 acts through the Ndc80 complex to limit pole number in <i>C. elegans</i> oocyte meiotic spindle assembly

Connolly, Amy A.; Sugioka, Kenji; Chuang, Chien-Hui; Lowry, Josh; Bowerman, Bruce

doi:10.1083/jcb.201412010

Cited by 49 publications

(70 citation statements)

References 74 publications

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“…2C). In agreement with a previous study and with our in utero analysis, we found that spindles assembled in KLP-7-depleted oocytes were multipolar (Connolly et al, 2015) ( Fig. 2D).…”

Section: In Utero Imaging Reveals That Klp-7 Is Required For the Initsupporting

confidence: 82%

“…In the C. elegans oocyte, KLP-7 has been proposed to limit metaphase spindle pole numbers by correcting improper kinetochore-microtubule attachments, but its precise function throughout the two meiotic divisions remains elusive (Connolly et al, 2015;Han et al, 2015). Here, we show the crucial meiotic function of KLP-7 in preventing ectopic microtubule assembly that otherwise leads to spindle disorganization and chromosome segregation defects.…”

Section: Introductionmentioning

confidence: 84%

“…6E). Previous studies of meiotic spindle assembly in the C. elegans oocyte have been performed at relatively low spatial and temporal resolutions, did not provide temporal information and/or missed the very early steps of spindle assembly (Yang et al, 2003;Connolly et al, 2015;Wolff et al, 2016). Here, we provide a precise quantitative picture covering the full time window of interest and the first time-resolved analysis of the entire process of meiotic spindle formation in this system.…”

Section: Klp-7 Is Globally Required For Normal Microtubule Dynamics Dmentioning

confidence: 95%

“…S1C, Movie 3). Progressive microtubule bundling and crosslinking led to the formation of a multipolar spindle with several ASPM-1 foci around chromosomes (Connolly et al, 2015). GFP:: KLP-7 also concentrated on these multiple poles (Fig.…”

Section: In Utero Imaging Reveals That Klp-7 Is Required For the Initmentioning

confidence: 99%

“…A recent study analyzing feeding RNAi-mediated depletion of KLP-7 or a KLP-7 temperature-sensitive loss-of-function mutant showed that the multipolar spindle phenotype observed when KLP-7 activity is decreased could be rescued upon co-depletion of the NDC-80 kinetochore component (Connolly et al, 2015). That study concluded that KLP-7 is involved in destabilizing improper kinetochore-microtubule attachments established during early prometaphase, similar to the function of its vertebrate ortholog MCAK during mitosis.…”

Section: Klp-7 Prevents the Formation Of Ectopic Cortical Microtubulementioning

confidence: 99%

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Inhibition of ectopic microtubule assembly by the kinesin-13 KLP-7 prevents chromosome segregation and cytokinesis defects in oocytes

Gigant¹,

Stefanutti²,

Laband³

et al. 2017

Journal of Cell Science

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In most species, oocytes lack centrosomes. Accurate meiotic spindle assembly and chromosome segregation -essential to prevent miscarriage or developmental defects -thus occur through atypical mechanisms that are not well characterized. Using quantitative in vitro and in vivo functional assays in the C. elegans oocyte, we provide novel evidence that the kinesin-13 KLP-7 promotes destabilization of the whole cellular microtubule network. By counteracting ectopic microtubule assembly and disorganization of the microtubule network, this function is strictly required for spindle organization, chromosome segregation and cytokinesis in meiotic cells. Strikingly, when centrosome activity was experimentally reduced, the absence of KLP-7 or the mammalian kinesin-13 protein MCAK (KIF2C) also resulted in ectopic microtubule asters during mitosis in C. elegans zygotes or HeLa cells, respectively. Our results highlight the general function of kinesin-13 microtubule depolymerases in preventing ectopic, spontaneous microtubule assembly when centrosome activity is defective or absent, which would otherwise lead to spindle microtubule disorganization and aneuploidy.

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“…2C). In agreement with a previous study and with our in utero analysis, we found that spindles assembled in KLP-7-depleted oocytes were multipolar (Connolly et al, 2015) ( Fig. 2D).…”

Section: In Utero Imaging Reveals That Klp-7 Is Required For the Initsupporting

confidence: 82%

Section: Introductionmentioning

confidence: 84%

Section: Klp-7 Is Globally Required For Normal Microtubule Dynamics Dmentioning

confidence: 95%

Section: In Utero Imaging Reveals That Klp-7 Is Required For the Initmentioning

confidence: 99%

Section: Klp-7 Prevents the Formation Of Ectopic Cortical Microtubulementioning

confidence: 99%

See 3 more Smart Citations

Inhibition of ectopic microtubule assembly by the kinesin-13 KLP-7 prevents chromosome segregation and cytokinesis defects in oocytes

Gigant¹,

Stefanutti²,

Laband³

et al. 2017

Journal of Cell Science

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RNF20 Regulates Oocyte Meiotic Spindle Assembly by Recruiting TPM3 to Centromeres and Spindle Poles

Wang,

Liu,

et al. 2024

Advanced Science

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Previously a ring finger protein 20 (RNF20) is found to be essential for meiotic recombination and mediates H2B ubiquitination during spermatogenesis. However, its role in meiotic division is still unknown. Here, it is shown that RNF20 is localized at both centromeres and spindle poles, and it is required for oocyte acentrosomal spindle organization and female fertility. RNF20‐depleted oocytes exhibit severely abnormal spindle and chromosome misalignment caused by defective bipolar organization. Notably, it is found that the function of RNF20 in spindle assembly is not dependent on its E3 ligase activity. Instead, RNF20 regulates spindle assembly by recruiting tropomyosin3 (TPM3) to both centromeres and spindle poles with its coiled‐coil motif. The RNF20‐TPM3 interaction is essential for acentrosomal meiotic spindle assembly. Together, the studies uncover a novel function for RNF20 in mediating TPM3 recruitment to both centromeres and spindle poles during oocyte spindle assembly.

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Microtubule length correlates with spindle length in C. elegans meiosis

Zimyanin,

Redemann

2024

Cytoskeleton

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The accurate segregation of chromosomes during female meiosis relies on the precise assembly and function of the meiotic spindle, a dynamic structure primarily composed of microtubules. Despite the crucial role of microtubule dynamics in this process, the relationship between microtubule length and spindle size remains elusive. Leveraging Caenorhabditis elegans as a model system, we combined electron tomography and live imaging to investigate this correlation. Our analysis revealed significant changes in spindle length throughout meiosis, coupled with alterations in microtubule length. Surprisingly, while spindle size decreases during the initial stages of anaphase, the size of antiparallel microtubule overlap decreased as well. Detailed electron tomography shows a positive correlation between microtubule length and spindle size, indicating a role of microtubule length in determining spindle dimensions. Notably, microtubule numbers displayed no significant association with spindle length, highlighting the dominance of microtubule length regulation in spindle size determination. Depletion of the microtubule depolymerase KLP‐7 led to elongated metaphase spindles with increased microtubule length, supporting the link between microtubule length and spindle size. These findings underscore the pivotal role of regulating microtubule dynamics, and thus microtubule length, in governing spindle rearrangements during meiotic division, shedding light on fundamental mechanisms dictating spindle architecture.

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KLP-7 acts through the Ndc80 complex to limit pole number in C. elegans oocyte meiotic spindle assembly

Abstract: KLP-7/MCAK regulates kinetochore–microtubule attachment and spindle tension to promote the coalescence of early spindle pole foci, which produces a bipolar structure during the acentrosomal process of oocyte meiotic spindle assembly in C. elegans.

Cited by 49 publications

References 74 publications

Inhibition of ectopic microtubule assembly by the kinesin-13 KLP-7 prevents chromosome segregation and cytokinesis defects in oocytes

Inhibition of ectopic microtubule assembly by the kinesin-13 KLP-7 prevents chromosome segregation and cytokinesis defects in oocytes

RNF20 Regulates Oocyte Meiotic Spindle Assembly by Recruiting TPM3 to Centromeres and Spindle Poles

Microtubule length correlates with spindle length in C. elegans meiosis

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