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

Wolff, Ian D.; Tran, Michael V.; Mullen, Timothy J.; Villeneuve, Anne M.; Wignall, Sarah M.

doi:10.1091/mbc.e16-05-0291

Cited by 51 publications

(102 citation statements)

References 51 publications

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“…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: 91%

“…We then analyzed nuclear envelope breakdown (NEBD) and meiotic spindle assembly in control and KLP-7-depleted oocytes during both meiotic divisions in utero in immobilized worms expressing GFP-tagged β-tubulin or the microtubule minus-end and spindle pole marker protein Abnormal spindle protein 1 (ASPM-1) and mCherry-tagged histone 2B (H2B) (van der Voet et al, 2009). Spindle assembly can be separated into four distinct phases (Wolff et al, 2016). In both control and KLP-7-depleted oocytes before NEBD, microtubules were excluded from the nucleus (Fig.…”

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

confidence: 95%

“…This second step is likely to be under the control of microtubule motors previously implicated in successful meiotic divisions, such as dynein, the two redundant kinesin-14 family members KLP-15/16 (orthologs of NCD) and the kinesin-12 family member KLP-18 (ortholog of XKLP2 or KIF15) (Dernburg et al, 2000;Piano et al, 2000;Colaiacovo et al, 2002;Segbert et al, 2003;Wolff et al, 2016). We found that in the absence of a nuclear cloud of microtubules in KLP-7-depleted oocytes, the ectopic perinuclear microtubules are instead bundled and coalesce around chromosomes to form a seemingly normal multipolar spindle.…”

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

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

confidence: 91%

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

confidence: 95%

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

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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“…Thus, it appears in mouse, and also pig oocytes (Sun, et al 2001), that chromosomes organize microtubules, but other nuclear factors may also be critical for spindle assembly (Polanski, et al 2005). In C. elegans , meiosis I oocyte spindle assembly appears to initiate with a microtubule “cage” that forms on the inside of the nuclear envelope (Wolff, et al 2016) (although at meiosis II, the microtubules assemble closely around the chromosomes like the other systems). Observations like these raise the possibility that spindle assembly is coupled to the release of nuclear factors caused by disassembly of the nuclear envelope.…”

Section: Oocyte Spindle Assembly Is Dominated By Chromosome-based Mecmentioning

confidence: 99%

“…Much like Drosophila , at least conceptually, there is a ring containing the CPC and a motor protein (KLP-19, a kinesin-4) that forms around the chromosomes during metaphase I (Wignall and Villeneuve 2009). C. elegans KLP-18 may have a role like kinesin-5 and enforce bipolarity by sliding microtubules and sorting the minus ends towards the poles (Wolff, et al 2016). …”

Section: Bipolarity Is Established Through a Central Spindlementioning

confidence: 99%

The chromosomal basis of meiotic acentrosomal spindle assembly and function in oocytes

et al. 2016

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Several aspects of meiosis are impacted by the absence of centrosomes in oocytes. Here we review four aspects of meiosis I that are significantly affected by the absence of centrosomes in oocyte spindles. One, microtubules tend to assemble around the chromosomes. Two, the organization of these microtubules into a bipolar spindle is directed by the chromosomes. Three, chromosome bi-orientation and attachment to microtubules from the correct pole require modification of the mechanisms used in mitotic cells. Four, chromosome movement to the poles at anaphase cannot rely on polar anchoring of spindle microtubules by centrosomes. Overall, the chromosomes are more active participants during acentrosomal spindle assembly in oocytes, compared to mitotic and male meiotic divisions where centrosomes are present. The chromosomes are endowed with information that can direct the meiotic divisions and dictate their own behavior in oocytes. Processes beyond those known from mitosis appear to be required for their bi-orientation at meiosis I. As mitosis occurs without centrosomes in many systems other than oocytes, including all plants, the concepts discussed here may not be not limited to oocytes. The study of meiosis in oocytes has revealed mechanisms that are operating in mitosis and will probably continue to do so.

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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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Assembly ofCaenorhabditis elegansacentrosomal spindles occurs without evident microtubule-organizing centers and requires microtubule sorting by KLP-18/kinesin-12 and MESP-1

Cited by 51 publications

References 51 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

The chromosomal basis of meiotic acentrosomal spindle assembly and function in oocytes

Microtubule length correlates with spindle length in C. elegans meiosis

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