Evidence for anaphase pulling forces during<i>C. elegans</i>meiosis

Danlasky, Brennan M; Panzica, Michelle T.; McNally, Karen Perry; Vargas, Elizabeth; Bailey, Cynthia; Li, Wenzhe; Gong, Ting; Fishman, Elizabeth S.; Jiang, Xueer; McNally, Francis J.

doi:10.1083/jcb.202005179

Cited by 30 publications

(25 citation statements)

References 71 publications

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“…Similar to mice and yeast, it is therefore likely that PP2A complexes at the chromosome control proper chromosome-spindle attachments. The alignment defects we observed upon PPTR-1/2 depletion (or in the LxxIxE motif mutant) resemble those reported in the absence of kinetochore proteins ( Danlasky et al, 2020 ; Dumont et al, 2010 ). Interestingly, PP2A:B56 complexes containing PPTR-1 and PPTR-2 are present at the meiotic kinetochore, and it is therefore possible that PP2A:B56 works in parallel to and/or regulates kinetochore protein(s).…”

Section: Discussionsupporting

confidence: 80%

“…Interestingly, PP2A:B56 complexes containing PPTR-1 and PPTR-2 are present at the meiotic kinetochore, and it is therefore possible that PP2A:B56 works in parallel to and/or regulates kinetochore protein(s). Furthermore, we detected GFP::PAA-1 on anaphase chromosomes, similar to kinetochore proteins ( Danlasky et al, 2020 ; Dumont et al, 2010 ; Hattersley et al, 2016 ).…”

Section: Discussionmentioning

confidence: 66%

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BUB-1 targets PP2A:B56 to regulate chromosome congression during meiosis I in C. elegans oocytes

Borja

Soubigou

Taylor

et al. 2020

eLife

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Protein Phosphatase 2A (PP2A) is a heterotrimer composed of scaffolding (A), catalytic (C), and regulatory (B) subunits. PP2A complexes with B56 subunits are targeted by Shugoshin and BUBR1 to protect centromeric cohesion and stabilise kinetochore–microtubule attachments in yeast and mouse meiosis. In Caenorhabditis elegans, the closest BUBR1 orthologue lacks the B56-interaction domain and Shugoshin is not required for meiotic segregation. Therefore, the role of PP2A in C. elegans female meiosis is unknown. We report that PP2A is essential for meiotic spindle assembly and chromosome dynamics during C. elegans female meiosis. BUB-1 is the main chromosome-targeting factor for B56 subunits during prometaphase I. BUB-1 recruits PP2A:B56 to the chromosomes via a newly identified LxxIxE motif in a phosphorylation-dependent manner, and this recruitment is important for proper chromosome congression. Our results highlight a novel mechanism for B56 recruitment, essential for recruiting a pool of PP2A involved in chromosome congression during meiosis I.

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Section: Discussionsupporting

confidence: 80%

Section: Discussionmentioning

confidence: 66%

BUB-1 targets PP2A:B56 to regulate chromosome congression during meiosis I in C. elegans oocytes

Borja

Soubigou

Taylor

et al. 2020

eLife

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“…Whether or not Naegleria has conventional kinetochores, spindle assembly and chromosome movement is well established to occur in the absence of kinetochores (Heald et al , 1996; Brunet et al , 1999). For example, in both mouse and C. elegans meiotic and human mitotic spindles, lateral interactions between microtubules and chromosomes drive chromosome congression, although chromosome-to-pole motion does require kinetochore-microtubule interactions (Kapoor et al , 2006; Mullen, Davis-Roca and Wignall, 2019; Danlasky et al , 2020).…”

Section: Discussionmentioning

confidence: 99%

Naegleria’smitotic spindles are built from unique tubulins and highlight core spindle features

Trupinić

Ivec

Swafford

et al. 2021

Preprint

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Naegleria gruberi is a unicellular eukaryote whose evolutionary distance from animals and fungi has made it useful for developing hypotheses about the last common eukaryotic ancestor. Naegleria amoebae lack a cytoplasmic microtubule cytoskeleton and assemble microtubules only during mitosis, and thus provides a unique system to study the evolution and functional specificity of mitotic tubulins and the resulting spindle. Previous studies showed that Naegleria amoebae express a divergent α-tubulin during mitosis and we now show that Naegleria amoebae express a second mitotic α- and two mitotic β-tubulins. The mitotic tubulins are evolutionarily divergent relative to typical α- and β- tubulins, contain residues that suggest distinct microtubule properties, and may represent drug targets for the "brain-eating amoeba" Naegleria fowleri. Using quantitative light microscopy, we find that Naegleria's mitotic spindle is a distinctive barrel-like structure built from a ring of microtubule bundles. Similar to those of other species, Naegleria's spindle is twisted and its length increases during mitosis suggesting that these aspects of mitosis are ancestral features. Because bundle numbers change during metaphase, we hypothesize that the initial bundles represent kinetochore fibers, and secondary bundles function as bridging fibers.

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“…For example, C. elegans female meiotic spindles appear to lack significant forces from astral regions. These spindles can move chromosomes in anaphase without kinetochores [ 92 ], though kinetochores are required to separate homologous chromosomes [ 93 ]. At later stages of anaphase in C. elegans female meiotic spindles, they lack kinetochore microtubules, laser ablation between chromosomes completely stops chromosome motion, and central spindle microtubules slide apart at the same speed as chromosomes [ 50 , 94 ].…”

Section: Mechanics Of Chromosome Segregationmentioning

confidence: 99%

Mechanical Mechanisms of Chromosome Segregation

Anjur-Dietrich

Kelleher

Needleman

2021

Cells

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Chromosome segregation—the partitioning of genetic material into two daughter cells—is one of the most crucial processes in cell division. In all Eukaryotes, chromosome segregation is driven by the spindle, a microtubule-based, self-organizing subcellular structure. Extensive research performed over the past 150 years has identified numerous commonalities and contrasts between spindles in different systems. In this review, we use simple coarse-grained models to organize and integrate previous studies of chromosome segregation. We discuss sites of force generation in spindles and fundamental mechanical principles that any understanding of chromosome segregation must be based upon. We argue that conserved sites of force generation may interact differently in different spindles, leading to distinct mechanical mechanisms of chromosome segregation. We suggest experiments to determine which mechanical mechanism is operative in a particular spindle under study. Finally, we propose that combining biophysical experiments, coarse-grained theories, and evolutionary genetics will be a productive approach to enhance our understanding of chromosome segregation in the future.

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Evidence for anaphase pulling forces duringC. elegansmeiosis

Cited by 30 publications

References 71 publications

BUB-1 targets PP2A:B56 to regulate chromosome congression during meiosis I in C. elegans oocytes

BUB-1 targets PP2A:B56 to regulate chromosome congression during meiosis I in C. elegans oocytes

Naegleria’smitotic spindles are built from unique tubulins and highlight core spindle features

Mechanical Mechanisms of Chromosome Segregation

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