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Individual pericentromeres display coordinated motion and stretching in the yeast spindle.

Stephens AD, Snider CE, Haase J, Haggerty RA, Vasquez PA, Forest MG, Bloom K - J. Cell Biol. (2013)

Bottom Line: By labeling several chromosomes, we find that pericentromeres display coordinated motion and stretching in metaphase.The pericentromeres of different chromosomes exhibit physical linkage dependent on centromere function and structural maintenance of chromosomes complexes.Coordinated motion is dependent on condensin and the kinesin motor Cin8, whereas coordinated stretching is dependent on pericentric cohesin and Cin8.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, 2 Department of Mathematics, and 3 Department Biomedical Engineering, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599.

ABSTRACT
The mitotic segregation apparatus composed of microtubules and chromatin functions to faithfully partition a duplicated genome into two daughter cells. Microtubules exert extensional pulling force on sister chromatids toward opposite poles, whereas pericentric chromatin resists with contractile springlike properties. Tension generated from these opposing forces silences the spindle checkpoint to ensure accurate chromosome segregation. It is unknown how the cell senses tension across multiple microtubule attachment sites, considering the stochastic dynamics of microtubule growth and shortening. In budding yeast, there is one microtubule attachment site per chromosome. By labeling several chromosomes, we find that pericentromeres display coordinated motion and stretching in metaphase. The pericentromeres of different chromosomes exhibit physical linkage dependent on centromere function and structural maintenance of chromosomes complexes. Coordinated motion is dependent on condensin and the kinesin motor Cin8, whereas coordinated stretching is dependent on pericentric cohesin and Cin8. Linking of pericentric chromatin through cohesin, condensin, and kinetochore microtubules functions to coordinate dynamics across multiple attachment sites.

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Simulation of cross-linking springs between pericentromeres recapitulates correlated movement and stretching. A mathematical model of spindle length force balance, including kMT dynamics and a nonlinear spring, was used to simulate the results of adding cross-linking springs between pericentromeres (Stephens et al., 2013). (A) Springs were added to cross-link neighbors or all pericentromeres into a network. (B and C) Graphs show cross-correlation of kMT plus-end movements (B) or coordinated stretching (C) upon increasing the cross-linking spring constant (kcross) relative to the pericentromere spring constant (kpericentromere; n = 500). All simulations had a 12 ± 2% single pericentromere stretching frequency (black line) similar to in vivo WT. Error bars represent standard deviations.
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fig3: Simulation of cross-linking springs between pericentromeres recapitulates correlated movement and stretching. A mathematical model of spindle length force balance, including kMT dynamics and a nonlinear spring, was used to simulate the results of adding cross-linking springs between pericentromeres (Stephens et al., 2013). (A) Springs were added to cross-link neighbors or all pericentromeres into a network. (B and C) Graphs show cross-correlation of kMT plus-end movements (B) or coordinated stretching (C) upon increasing the cross-linking spring constant (kcross) relative to the pericentromere spring constant (kpericentromere; n = 500). All simulations had a 12 ± 2% single pericentromere stretching frequency (black line) similar to in vivo WT. Error bars represent standard deviations.

Mentions: We used a mathematical model of the yeast spindle to query the extent that chromatin cross-links could increase correlated motion and stretching in the spindle (Stephens et al., 2013). Addition of cross-linking springs between pericentromeres and their two adjacent neighbors fractionally increases the cross-correlation of kMT plus ends (Fig. 3, A and B, blue). A network in which all pericentromeres were cross-linked to each other significantly increases correlated motion (Fig. 3, A and B, red). Interestingly, simulation of either type of cross-link leads to increased coordinated stretching that matches levels measured in WT cells (Fig. 3 C). Thus, chromatin-based cross-linking of all pericentromeres provides a mechanism for correlated movement and stretching observed in vivo.


Individual pericentromeres display coordinated motion and stretching in the yeast spindle.

Stephens AD, Snider CE, Haase J, Haggerty RA, Vasquez PA, Forest MG, Bloom K - J. Cell Biol. (2013)

Simulation of cross-linking springs between pericentromeres recapitulates correlated movement and stretching. A mathematical model of spindle length force balance, including kMT dynamics and a nonlinear spring, was used to simulate the results of adding cross-linking springs between pericentromeres (Stephens et al., 2013). (A) Springs were added to cross-link neighbors or all pericentromeres into a network. (B and C) Graphs show cross-correlation of kMT plus-end movements (B) or coordinated stretching (C) upon increasing the cross-linking spring constant (kcross) relative to the pericentromere spring constant (kpericentromere; n = 500). All simulations had a 12 ± 2% single pericentromere stretching frequency (black line) similar to in vivo WT. Error bars represent standard deviations.
© Copyright Policy - openaccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC3824013&req=5

fig3: Simulation of cross-linking springs between pericentromeres recapitulates correlated movement and stretching. A mathematical model of spindle length force balance, including kMT dynamics and a nonlinear spring, was used to simulate the results of adding cross-linking springs between pericentromeres (Stephens et al., 2013). (A) Springs were added to cross-link neighbors or all pericentromeres into a network. (B and C) Graphs show cross-correlation of kMT plus-end movements (B) or coordinated stretching (C) upon increasing the cross-linking spring constant (kcross) relative to the pericentromere spring constant (kpericentromere; n = 500). All simulations had a 12 ± 2% single pericentromere stretching frequency (black line) similar to in vivo WT. Error bars represent standard deviations.
Mentions: We used a mathematical model of the yeast spindle to query the extent that chromatin cross-links could increase correlated motion and stretching in the spindle (Stephens et al., 2013). Addition of cross-linking springs between pericentromeres and their two adjacent neighbors fractionally increases the cross-correlation of kMT plus ends (Fig. 3, A and B, blue). A network in which all pericentromeres were cross-linked to each other significantly increases correlated motion (Fig. 3, A and B, red). Interestingly, simulation of either type of cross-link leads to increased coordinated stretching that matches levels measured in WT cells (Fig. 3 C). Thus, chromatin-based cross-linking of all pericentromeres provides a mechanism for correlated movement and stretching observed in vivo.

Bottom Line: By labeling several chromosomes, we find that pericentromeres display coordinated motion and stretching in metaphase.The pericentromeres of different chromosomes exhibit physical linkage dependent on centromere function and structural maintenance of chromosomes complexes.Coordinated motion is dependent on condensin and the kinesin motor Cin8, whereas coordinated stretching is dependent on pericentric cohesin and Cin8.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biology, 2 Department of Mathematics, and 3 Department Biomedical Engineering, University of North Carolina at Chapel Hill, Chapel Hill, NC 27599.

ABSTRACT
The mitotic segregation apparatus composed of microtubules and chromatin functions to faithfully partition a duplicated genome into two daughter cells. Microtubules exert extensional pulling force on sister chromatids toward opposite poles, whereas pericentric chromatin resists with contractile springlike properties. Tension generated from these opposing forces silences the spindle checkpoint to ensure accurate chromosome segregation. It is unknown how the cell senses tension across multiple microtubule attachment sites, considering the stochastic dynamics of microtubule growth and shortening. In budding yeast, there is one microtubule attachment site per chromosome. By labeling several chromosomes, we find that pericentromeres display coordinated motion and stretching in metaphase. The pericentromeres of different chromosomes exhibit physical linkage dependent on centromere function and structural maintenance of chromosomes complexes. Coordinated motion is dependent on condensin and the kinesin motor Cin8, whereas coordinated stretching is dependent on pericentric cohesin and Cin8. Linking of pericentric chromatin through cohesin, condensin, and kinetochore microtubules functions to coordinate dynamics across multiple attachment sites.

Show MeSH
Related in: MedlinePlus