Tension-dependent nucleosome remodeling at the pericentromere in yeast

Abstract

Dynamics of histones under tension in the pericentromere depends on RSC and ISW2 chromatin remodeling. The underlying pericentromeric chromatin forms a platform that is required to maintain kinetochore structure when under spindle-based tension.

Kinetochore Function and Chromosome Segregation Rely on Critical Residues in Histones H3 and H4 in Budding Yeast

“…An attractive hypothesis is that the DNA at the entry/exit site of the nucleosome may come under tension when kinetochores biorient, thus signaling to the cell that the kinetochores have achieved biorientation. Consistent with this, tension-dependent changes in budding yeast pericentromeric chromatin structure have been observed by microscopy (Haase et al 2012;Verdaasdonk et al 2012). The localization of Sgo1 to this region may therefore be coupled to its ability to trigger the spindle checkpoint when the pericentromeric chromatin is not under tension.…”

“…In addition, evidence suggests that the pericentromeric chromatin adopts a specialized intramolecular structure that is organized by Sgo1 and facilitates biorientation in budding yeast (Yeh et al 2008;Haase et al 2012). Consistent with this, changes in pericentromeric chromatin composition lead to defects in the organization of inner kinetochore proteins and chromosome segregation (Chambers et al 2012;Verdaasdonk et al 2012).…”

The Composition, Functions, and Regulation of the Budding Yeast Kinetochore

“…Although H3 was also reported to localize to centromeres in budding yeast (Lochmann and Ivanov 2012), the region of DNA analyzed was large enough to contain two nucleosomes so the H3 detected may be in the neighboring nucleosome rather than the centromeric nucleosome. Consistent with this, depletion of H3 in budding yeast has little effect on kinetochore function compared to H4 depletion or H2A mutations that lead to defects in kinetochore-microtubule attachments (Pinto and Winston 2000;Bouck and Bloom 2007;Verdaasdonk et al 2012). Together, these data suggest that H3 does not reside at the point centromere, although it is important for accurate segregation through its role in recruiting Sgo1 to the pericentromere and facilitating inner kinetochore function (Luo et al 2010;Verdaasdonk et al 2012).…”

“…Consistent with this, depletion of H3 in budding yeast has little effect on kinetochore function compared to H4 depletion or H2A mutations that lead to defects in kinetochore-microtubule attachments (Pinto and Winston 2000;Bouck and Bloom 2007;Verdaasdonk et al 2012). Together, these data suggest that H3 does not reside at the point centromere, although it is important for accurate segregation through its role in recruiting Sgo1 to the pericentromere and facilitating inner kinetochore function (Luo et al 2010;Verdaasdonk et al 2012). Finally, it was argued that Cse4 is part of an octameric nucleosome at the centromere based on sequential immunoprecipitation experiments, but the starting material for these experiments was not pure mononucleosomes (Camahort et al 2009).…”

“…Consistent with this, the geometry and elasticity of the pericentromere and inner kinetochore can change in response to alterations in microtubule dynamics (Haase et al 2012;Stephens et al 2013). These properties are regulated by the Bub1 and Sgo1 proteins as well as various chromatin-remodeling complexes (Haase et al 2012;Verdaasdonk et al 2012). While heterochromatin recruits pericentric cohesin in some organisms (Bernard et al 2001;Fukagawa et al 2004), components of the kinetochore itself direct cohesion enrichment in budding yeast (Megee et al 1999;Tanaka et al 1999;Weber et al 2004;Eckert et al 2007;Fernius and Marston 2009;Ng et al 2009;Fernius et al 2013).…”