scholarly journals Spherical Spindle Shape Promotes Perpendicular Cortical Orientation by Preventing Isometric Cortical Pulling on both Spindle Poles during C. elegans Female Meiosis

2019 ◽  
Author(s):  
Elizabeth Vargas ◽  
Karen P. McNally ◽  
Daniel B. Cortes ◽  
Michelle T. Panzica ◽  
Amy Shaub-Maddox ◽  
...  
Keyword(s):  
Polar Body ◽  
Spherical Shape ◽  
Viscous Drag ◽  
Female Meiosis ◽  
C Elegans ◽  
Microtubule Severing ◽  
Perpendicular Orientation ◽  
Spindle Poles ◽  
Meiotic Spindles ◽  
Segregation Of Chromosomes

AbstractMeiotic spindles are positioned perpendicular to the oocyte cortex to facilitate segregation of chromosomes into a large egg and a tiny polar body. In C. elegans, spindles are initially ellipsoid and parallel to the cortex before shortening to a spherical shape and rotating to the perpendicular orientation by dynein-driven cortical pulling. The mechanistic connection between spindle shape and rotation has remained elusive. Here we used mutants of the microtubule-severing protein katanin to manipulate spindle shape without eliminating cortical pulling. In a katanin mutant, spindles remained ellipsoid, had pointed poles and became trapped in either a diagonal or a parallel orientation. Results indicated that astral microtubules emanating from both spindle poles initially engage in cortical pulling until microtubules emanating from one pole detach from the cortex allowing pivoting of the spindle. The lower viscous drag experienced by spherical spindles prevented recapture of the cortex by astral microtubules emanating from the detached pole. In addition, maximizing contact between pole dynein and cortical dynein stabilizes round poles in a perpendicular orientation. Spherical spindle shape can thus promote perpendicular orientation by two distinct mechanisms.

scholarly journals CDK-1 inhibits meiotic spindle shortening and dynein-dependent spindle rotation in C. elegans

2011 ◽  
Vol 193 (7) ◽  
pp. 1229-1244 ◽  
Author(s):  
Marina L. Ellefson ◽  
Francis J. McNally
Keyword(s):  
Polar Body ◽  
Spindle Pole ◽  
Cyclin B ◽  
Meiotic Spindle ◽  
Anaphase Promoting Complex ◽  
C Elegans ◽  
Perpendicular Orientation ◽  
Spindle Poles ◽  
Spindle Rotation ◽  
Chromosome Separation

In animals, the female meiotic spindle is positioned at the egg cortex in a perpendicular orientation to facilitate the disposal of half of the chromosomes into a polar body. In Caenorhabditis elegans, the metaphase spindle lies parallel to the cortex, dynein is dispersed on the spindle, and the dynein activators ASPM-1 and LIN-5 are concentrated at spindle poles. Anaphase-promoting complex (APC) activation results in dynein accumulation at spindle poles and dynein-dependent rotation of one spindle pole to the cortex, resulting in perpendicular orientation. To test whether the APC initiates spindle rotation through cyclin B–CDK-1 inactivation, separase activation, or degradation of an unknown dynein inhibitor, CDK-1 was inhibited with purvalanol A in metaphase-I–arrested, APC-depleted embryos. CDK-1 inhibition resulted in the accumulation of dynein at spindle poles and dynein-dependent spindle rotation without chromosome separation. These results suggest that CDK-1 blocks rotation by inhibiting dynein association with microtubules and with LIN-5–ASPM-1 at meiotic spindle poles and that the APC promotes spindle rotation by inhibiting CDK-1.

scholarly journals Katanin controls mitotic and meiotic spindle length

2006 ◽  
Vol 175 (6) ◽  
pp. 881-891 ◽  
Author(s):  
Karen McNally ◽  
Anjon Audhya ◽  
Karen Oegema ◽  
Francis J. McNally
Keyword(s):  
Chromosome Segregation ◽  
Eukaryotic Cell ◽  
Meiotic Spindle ◽  
Mitotic Spindles ◽  
Wild Type ◽  
Female Meiosis ◽  
C Elegans ◽  
Microtubule Severing ◽  
Spindle Poles ◽  
Type C

Accurate control of spindle length is a conserved feature of eukaryotic cell division. Lengthening of mitotic spindles contributes to chromosome segregation and cytokinesis during mitosis in animals and fungi. In contrast, spindle shortening may contribute to conservation of egg cytoplasm during female meiosis. Katanin is a microtubule-severing enzyme that is concentrated at mitotic and meiotic spindle poles in animals. We show that inhibition of katanin slows the rate of spindle shortening in nocodazole-treated mammalian fibroblasts and in untreated Caenorhabditis elegans meiotic embryos. Wild-type C. elegans meiotic spindle shortening proceeds through an early katanin-independent phase marked by increasing microtubule density and a second, katanin-dependent phase that occurs after microtubule density stops increasing. In addition, double-mutant analysis indicated that γ-tubulin–dependent nucleation and microtubule severing may provide redundant mechanisms for increasing microtubule number during the early stages of meiotic spindle assembly.

scholarly journals Mixing and Matching Chromosomes during Female Meiosis

Cells ◽  
2020 ◽  
Vol 9 (3) ◽  
pp. 696
Author(s):  
Thomas Rubin ◽  
Nicolas Macaisne ◽  
Jean-René Huynh
Keyword(s):  
Female Meiosis ◽  
Homologous Chromosomes ◽  
C Elegans ◽  
Similarities And Differences ◽  
Segregation Of Chromosomes

Meiosis is a key event in the manufacturing of an oocyte. During this process, the oocyte creates a set of unique chromosomes by recombining paternal and maternal copies of homologous chromosomes, and by eliminating one set of chromosomes to become haploid. While meiosis is conserved among sexually reproducing eukaryotes, there is a bewildering diversity of strategies among species, and sometimes within sexes of the same species, to achieve proper segregation of chromosomes. Here, we review the very first steps of meiosis in females, when the maternal and paternal copies of each homologous chromosomes have to move, find each other and pair. We explore the similarities and differences observed in C. elegans, Drosophila, zebrafish and mouse females.

scholarly journals Spherical spindle shape promotes perpendicular cortical orientation by preventing isometric cortical pulling on both spindle poles during C. elegans female meiosis

Development ◽  
2019 ◽  
Vol 146 (20) ◽  
pp. dev178863 ◽  
Author(s):  
Elizabeth Vargas ◽  
Karen P. McNally ◽  
Daniel B. Cortes ◽  
Michelle T. Panzica ◽  
Brennan M. Danlasky ◽  
...  
Keyword(s):  
Female Meiosis ◽  
C Elegans ◽  
Spindle Poles

scholarly journals Dynactin-dependent cortical dynein and spherical spindle shape correlate temporally with meiotic spindle rotation in Caenorhabditis elegans

2015 ◽  
Vol 26 (17) ◽  
pp. 3030-3046 ◽  
Author(s):  
Marina E. Crowder ◽  
Jonathan R. Flynn ◽  
Karen P. McNally ◽  
Daniel B. Cortes ◽  
Kari L. Price ◽  
...  
Keyword(s):  
Caenorhabditis Elegans ◽  
Spherical Shape ◽  
Nematode Species ◽  
Meiotic Spindle ◽  
Present Evidence ◽  
Basic Domain ◽  
C Elegans ◽  
Polar Bodies ◽  
Spindle Rotation ◽  
Meiotic Spindles

Oocyte meiotic spindles orient with one pole juxtaposed to the cortex to facilitate extrusion of chromosomes into polar bodies. In Caenorhabditis elegans, these acentriolar spindles initially orient parallel to the cortex and then rotate to the perpendicular orientation. To understand the mechanism of spindle rotation, we characterized events that correlated temporally with rotation, including shortening of the spindle in the pole-to pole axis, which resulted in a nearly spherical spindle at rotation. By analyzing large spindles of polyploid C. elegans and a related nematode species, we found that spindle rotation initiated at a defined spherical shape rather than at a defined spindle length. In addition, dynein accumulated on the cortex just before rotation, and microtubules grew from the spindle with plus ends outward during rotation. Dynactin depletion prevented accumulation of dynein on the cortex and prevented spindle rotation independently of effects on spindle shape. These results support a cortical pulling model in which spindle shape might facilitate rotation because a sphere can rotate without deforming the adjacent elastic cytoplasm. We also present evidence that activation of spindle rotation is promoted by dephosphorylation of the basic domain of p150 dynactin.

scholarly journals Microtubule re-organization during female meiosis in C elegans

eLife ◽  
2021 ◽  
Vol 10 ◽  
Author(s):  
Ina Lantzsch ◽  
Che-Hang Yu ◽  
Yu-Zen Chen ◽  
Vitaly Zimyanin ◽  
Hossein Yazdkhasti ◽  
...  
Keyword(s):  
Large Scale ◽  
Electron Tomography ◽  
Morphological Changes ◽  
Average Length ◽  
Close Contact ◽  
Length Distribution ◽  
C Elegans ◽  
Microtubule Severing ◽  
Meiotic Spindles ◽  
Turn Over

The female meiotic spindles of most animals are acentrosomal and undergo striking morphological changes while transitioning from metaphase to anaphase. The ultra-structure of acentrosomal spindles, and how changes to this structure correlate with such dramatic spindle rearrangements remains largely unknown. To address this, we applied light microscopy, large-scale electron tomography and mathematical modeling of female meiotic C. elegans spindles undergoing the transition from metaphase to anaphase. Combining these approaches, we find that meiotic spindles are dynamic arrays of short microtubules that turn over on second time scales. The results show that the transition from metaphase to anaphase correlates with an increase in the number of microtubules and a decrease in their average length. Detailed analysis of the tomographic data revealed that the length of microtubules changes significantly during the metaphase-to-anaphase transition. This effect is most pronounced for those microtubules located within 150 nm of the chromosome surface. To understand the mechanisms that drive this transition, we developed a mathematical model for the microtubule length distribution that considers microtubule growth, catastrophe, and severing. Using Bayesian inference to compare model predictions and data, we find that microtubule turn-over is the major driver of the observed large-scale reorganizations. Our data suggest that in metaphase only a minor fraction of microtubules, those that are closest to the chromosomes, are severed. The large majority of microtubules, which are not in close contact with chromosomes, do not undergo severing. Instead, their length distribution is fully explained by growth and catastrophe alone. In anaphase, even microtubules close to the chromosomes show no signs of cutting. This suggests that the most prominent drivers of spindle rearrangements from metaphase to anaphase are changes in nucleation and catastrophe rate. In addition, we provide evidence that microtubule severing is dependent on the presence of katanin.

scholarly journals Localization of the mei-1 gene product of Caenorhaditis elegans, a meiotic-specific spindle component.

1994 ◽  
Vol 126 (1) ◽  
pp. 199-209 ◽  
Author(s):  
S Clark-Maguire ◽  
P E Mains
Keyword(s):  
Regulatory Network ◽  
Meiotic Spindle ◽  
Loss Of Function ◽  
Wild Type ◽  
Female Meiosis ◽  
Gain Of Function ◽  
Spindle Poles ◽  
Meiotic Spindles ◽  
Female Germline ◽  
Meiosis I

Genetic evidence suggests that the product of the mei-1 gene of Caenorhabditis elegans is specifically required for meiosis in the female germline. Loss-of-function mei-1 mutations block meiotic spindle formation while a gain-of-function allele instead results in spindle defects during the early mitotic cleavages. In this report, we use immunocytochemistry to examine the localization of the mei-1 product in wild-type and mutant embryos. During metaphase of meiosis I in wild-type embryos, mei-1 protein was found throughout the spindle but was more concentrated toward the poles. At telophase I, mei-1 product colocalized with the chromatin at the spindle poles. The pattern was repeated during meiosis II but no mei-1 product was visible during the subsequent mitotic cleavages. The mei-1 gain-of-function allele resulted in ectopic mei-1 staining in the centers of the microtubule-organizing centers during interphase and in the spindles during the early cleavages. This aberrant localization is probably responsible for the poorly formed and misoriented cleavage spindles characteristic of the mutation. We also examined the localization of mei-1(+) product in the presence of mutations of genes that genetically interact with mei-1 alleles. mei-2 is apparently required to localize mei-1 product to the spindle during meiosis while mel-26 acts as a postmeiotic inhibitor. We conclude that mei-1 encodes a novel spindle component, one that is specialized for the acentriolar meiotic spindles unique to female meiosis. The genes mei-2 and mel-26 are part of a regulatory network that confines mei-1 activity to meiosis.

scholarly journals Evidence for anaphase pulling forces during C. elegans meiosis

2020 ◽  
Vol 219 (12) ◽  
Author(s):  
Brennan M. Danlasky ◽  
Michelle T. Panzica ◽  
Karen P. McNally ◽  
Elizabeth Vargas ◽  
Cynthia Bailey ◽  
...  
Keyword(s):  
Spindle Pole ◽  
Outer Face ◽  
Chromosome Movement ◽  
Female Meiosis ◽  
Homologous Chromosomes ◽  
C Elegans ◽  
Spindle Poles ◽  
Pulling Forces ◽  
Spindle Elongation ◽  
Anaphase B

Anaphase chromosome movement is thought to be mediated by pulling forces generated by end-on attachment of microtubules to the outer face of kinetochores. However, it has been suggested that during C. elegans female meiosis, anaphase is mediated by a kinetochore-independent pushing mechanism with microtubules only attached to the inner face of segregating chromosomes. We found that the kinetochore proteins KNL-1 and KNL-3 are required for preanaphase chromosome stretching, suggesting a role in pulling forces. In the absence of KNL-1,3, pairs of homologous chromosomes did not separate and did not move toward a spindle pole. Instead, each homolog pair moved together with the same spindle pole during anaphase B spindle elongation. Two masses of chromatin thus ended up at opposite spindle poles, giving the appearance of successful anaphase.

scholarly journals A novel chromosome segregation mechanism during female meiosis

2016 ◽  
Vol 27 (16) ◽  
pp. 2576-2589 ◽  
Author(s):  
Karen Perry McNally ◽  
Michelle T. Panzica ◽  
Taekyung Kim ◽  
Daniel B. Cortes ◽  
Francis J. McNally
Keyword(s):  
Chromosome Segregation ◽  
Meiotic Chromosome ◽  
Spindle Pole ◽  
Chromosome Movement ◽  
Female Meiosis ◽  
Spindle Poles ◽  
Wide Range ◽  
Chromosome Separation ◽  
Meiotic Spindles ◽  
Anaphase B

In a wide range of eukaryotes, chromosome segregation occurs through anaphase A, in which chromosomes move toward stationary spindle poles, anaphase B, in which chromosomes move at the same velocity as outwardly moving spindle poles, or both. In contrast, Caenorhabditis elegans female meiotic spindles initially shorten in the pole-to-pole axis such that spindle poles contact the outer kinetochore before the start of anaphase chromosome separation. Once the spindle pole-to-kinetochore contact has been made, the homologues of a 4-μm-long bivalent begin to separate. The spindle shortens an additional 0.5 μm until the chromosomes are embedded in the spindle poles. Chromosomes then separate at the same velocity as the spindle poles in an anaphase B–like movement. We conclude that the majority of meiotic chromosome movement is caused by shortening of the spindle to bring poles in contact with the chromosomes, followed by separation of chromosome-bound poles by outward sliding.

Chromosome Segregation in C. Elegans Female Meiosis is Accompanied by a Switch in Lateral to End-On Microtubule Orientation

2018 ◽  
Author(s):  
Stefanie Redemann ◽  
Ina Lantzsch ◽  
Norbert Lindow ◽  
Steffen Prohaska ◽  
Martin Srayko ◽  
...  
Keyword(s):  
Chromosome Segregation ◽  
Female Meiosis ◽  
Microtubule Orientation ◽  
C Elegans
Sign in / Sign up

Export Citation Format

Share Document