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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.

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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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Model of cross-linking in the metaphase spindle apparatus. (A) Diagram of WT metaphase spindle structure and interactions. kMTs (light green) emanating from the spindle pole (dark green) are cross-linked via the kinesin 5 motor Cin8, whereas multiple nonlinear (looped) pericentric chromatin springs (CEN15 and CEN11) are cross-liked via condensin at the base and cohesin radially displaced (Stephens et al., 2011). Cross-links could occur through homotypic interaction or single complex (see Thadani et al. [2012] for condensin and Haering and Jessberger [2012] for cohesin). (B) Condensin functions as an axial cross-linker between compact pericentromeres of different chromosomes to correlate their movement during metaphase. Alternatively, condensin’s contributions to compaction, spring constant, or interactions with topoisomerase II could affect correlated motion. (C) Loss of condensin cross-links results in decreased correlated motion (smaller arrows; Fig. 1 F). (D) Cohesin functions primarily as a distal cross-linker between pericentromeres, resulting in coordinated stretching (double arrows). (E) Loss of pericentric cohesin results in pericentromeres stretching independently (one stretched and one compact; Fig. 2 G).
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fig5: Model of cross-linking in the metaphase spindle apparatus. (A) Diagram of WT metaphase spindle structure and interactions. kMTs (light green) emanating from the spindle pole (dark green) are cross-linked via the kinesin 5 motor Cin8, whereas multiple nonlinear (looped) pericentric chromatin springs (CEN15 and CEN11) are cross-liked via condensin at the base and cohesin radially displaced (Stephens et al., 2011). Cross-links could occur through homotypic interaction or single complex (see Thadani et al. [2012] for condensin and Haering and Jessberger [2012] for cohesin). (B) Condensin functions as an axial cross-linker between compact pericentromeres of different chromosomes to correlate their movement during metaphase. Alternatively, condensin’s contributions to compaction, spring constant, or interactions with topoisomerase II could affect correlated motion. (C) Loss of condensin cross-links results in decreased correlated motion (smaller arrows; Fig. 1 F). (D) Cohesin functions primarily as a distal cross-linker between pericentromeres, resulting in coordinated stretching (double arrows). (E) Loss of pericentric cohesin results in pericentromeres stretching independently (one stretched and one compact; Fig. 2 G).

Mentions: The resistive properties of the spring likely come from compaction and cross-linking of pericentromeres through condensin and cohesin (Fig. 5; Guacci et al., 1997; Lavoie et al., 2002, 2004; Lam et al., 2006; Heidinger-Pauli et al., 2010; Cuylen et al., 2011; Stephens et al., 2011, 2013). Condensin-dependent chromatin compaction is also critical for tension-sensing mechanisms (Yong-Gonzalez et al., 2007; Uchida et al., 2009). The segregation apparatus allows for a variable number of microtubule attachments by generating an interlinked network in the chromatin, critical for orienting and maintaining bioriented attachments and the kinetochore under tension.


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)

Model of cross-linking in the metaphase spindle apparatus. (A) Diagram of WT metaphase spindle structure and interactions. kMTs (light green) emanating from the spindle pole (dark green) are cross-linked via the kinesin 5 motor Cin8, whereas multiple nonlinear (looped) pericentric chromatin springs (CEN15 and CEN11) are cross-liked via condensin at the base and cohesin radially displaced (Stephens et al., 2011). Cross-links could occur through homotypic interaction or single complex (see Thadani et al. [2012] for condensin and Haering and Jessberger [2012] for cohesin). (B) Condensin functions as an axial cross-linker between compact pericentromeres of different chromosomes to correlate their movement during metaphase. Alternatively, condensin’s contributions to compaction, spring constant, or interactions with topoisomerase II could affect correlated motion. (C) Loss of condensin cross-links results in decreased correlated motion (smaller arrows; Fig. 1 F). (D) Cohesin functions primarily as a distal cross-linker between pericentromeres, resulting in coordinated stretching (double arrows). (E) Loss of pericentric cohesin results in pericentromeres stretching independently (one stretched and one compact; Fig. 2 G).
© Copyright Policy - openaccess
Related In: Results  -  Collection

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

fig5: Model of cross-linking in the metaphase spindle apparatus. (A) Diagram of WT metaphase spindle structure and interactions. kMTs (light green) emanating from the spindle pole (dark green) are cross-linked via the kinesin 5 motor Cin8, whereas multiple nonlinear (looped) pericentric chromatin springs (CEN15 and CEN11) are cross-liked via condensin at the base and cohesin radially displaced (Stephens et al., 2011). Cross-links could occur through homotypic interaction or single complex (see Thadani et al. [2012] for condensin and Haering and Jessberger [2012] for cohesin). (B) Condensin functions as an axial cross-linker between compact pericentromeres of different chromosomes to correlate their movement during metaphase. Alternatively, condensin’s contributions to compaction, spring constant, or interactions with topoisomerase II could affect correlated motion. (C) Loss of condensin cross-links results in decreased correlated motion (smaller arrows; Fig. 1 F). (D) Cohesin functions primarily as a distal cross-linker between pericentromeres, resulting in coordinated stretching (double arrows). (E) Loss of pericentric cohesin results in pericentromeres stretching independently (one stretched and one compact; Fig. 2 G).
Mentions: The resistive properties of the spring likely come from compaction and cross-linking of pericentromeres through condensin and cohesin (Fig. 5; Guacci et al., 1997; Lavoie et al., 2002, 2004; Lam et al., 2006; Heidinger-Pauli et al., 2010; Cuylen et al., 2011; Stephens et al., 2011, 2013). Condensin-dependent chromatin compaction is also critical for tension-sensing mechanisms (Yong-Gonzalez et al., 2007; Uchida et al., 2009). The segregation apparatus allows for a variable number of microtubule attachments by generating an interlinked network in the chromatin, critical for orienting and maintaining bioriented attachments and the kinetochore under tension.

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