Cohesin, condensin, and the intramolecular centromere loop together generate the mitotic chromatin spring

Stephens, Andrew D.; Haase, Julian; Vicci, Leandra; Taylor, Russell M.; Bloom, Kerry

doi:10.1083/jcb.201103138

Cited by 132 publications

(258 citation statements)

References 68 publications

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“…Such increase is in agreement with the role of condensin in forming a “spring” of chromatin at pericentromeric regions at the metaphase‐to‐anaphase transition (Stephens et al , 2011). Surprisingly, a peculiar loop pattern appears on chr12 in cdc15 ‐arrested cells, bridging the centromere and the centromere–proximal left flanking region of the rDNA cluster (see pink arrowheads in Fig 4F, G and H).…”

Section: Resultssupporting

confidence: 83%

“…Cohesins, such as Scc1, promote SC cohesion during DNA replication (Blat & Kleckner, 1999; Glynn et al , 2004) and get cleaved at the metaphase‐to‐anaphase transition (Uhlmann et al , 1999). At the same time, condensins such as Smc2 are loaded onto SCs to facilitate their segregation (Renshaw et al , 2010; Stephens et al , 2011; Hirano, 2012). In fission yeast, the binding of SMCs modifies the level of chromosome compaction defined as the ratio between long (> 10 kb)‐ and short‐range (< 10 kb) contacts at specific loci (Mizuguchi et al , 2014; Kim et al , 2016).…”

Section: Introductionmentioning

confidence: 99%

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Cohesins and condensins orchestrate the 4D dynamics of yeast chromosomes during the cell cycle

et al. 2017

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Duplication and segregation of chromosomes involves dynamic reorganization of their internal structure by conserved architectural proteins, including the structural maintenance of chromosomes (SMC) complexes cohesin and condensin. Despite active investigation of the roles of these factors, a genome‐wide view of dynamic chromosome architecture at both small and large scale during cell division is still missing. Here, we report the first comprehensive 4D analysis of the higher‐order organization of the Saccharomyces cerevisiae genome throughout the cell cycle and investigate the roles of SMC complexes in controlling structural transitions. During replication, cohesion establishment promotes numerous long‐range intra‐chromosomal contacts and correlates with the individualization of chromosomes, which culminates at metaphase. In anaphase, mitotic chromosomes are abruptly reorganized depending on mechanical forces exerted by the mitotic spindle. Formation of a condensin‐dependent loop bridging the centromere cluster with the rDNA loci suggests that condensin‐mediated forces may also directly facilitate segregation. This work therefore comprehensively recapitulates cell cycle‐dependent chromosome dynamics in a unicellular eukaryote, but also unveils new features of chromosome structural reorganization during highly conserved stages of cell division.

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Section: Resultssupporting

confidence: 83%

Section: Introductionmentioning

confidence: 99%

Cohesins and condensins orchestrate the 4D dynamics of yeast chromosomes during the cell cycle

et al. 2017

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“…Sgo1 can recruit condensin to chromosomes and has the capability to dephosphorylate cohesin, both of which contribute to chromosome structure and organization (Peplowska et al, 2014;Stephens et al, 2011;Verzijlbergen et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

Sgo1 recruits PP2A to chromosomes to ensure sister chromatid bi-orientation in mitosis

Eshleman

Morgan

2014

Journal of Cell Science

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Sister chromatid bi-orientation on the mitotic spindle is essential for proper chromosome segregation. Defects in bi-orientation are sensed and corrected to prevent chromosome mis-segregation and aneuploidy. This response depends on the adaptor protein Sgo1, which associates with pericentromeric chromatin in mitosis. The mechanisms underlying Sgo1 function and regulation are unclear. Here, we show that Sgo1 is an anaphase-promoting complex/cyclosome (APC/C) substrate in budding yeast (Saccharomyces cerevisiae), and that its mitotic destruction depends on an unusual D-box-related sequence motif near its Cterminus. We find that the removal of Sgo1 from chromosomes before anaphase is not dependent on its destruction, but rather on other mechanisms responsive to tension between sister chromatids. Additionally, we find that Sgo1 recruits the protein phosphatase 2A (PP2A) isoform containing Rts1 to the pericentromeric region prior to bi-orientation, and that artificial recruitment of Rts1 to this region of a single chromosome is sufficient to perform the function of Sgo1 on that chromosome. We conclude that in early mitosis, Sgo1 associates transiently with pericentromeric chromatin to promote biorientation, in large part by recruiting the Rts1 isoform of PP2A.

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“…For the much larger (and more easily manipulable) system of eukaryotic chromosomes and spindles, a combination of biophysical and biochemical methods has begun to unravel their micromechanical properties (20)(21)(22). In contrast, despite some of the earlier pioneering biophysical work (23), experimental progress for bacterial chromosomes has lagged behind, because of compound experimental difficulties (ı.e., small in size but complex in molecular and biochemical detail).…”

mentioning

confidence: 99%

Physical manipulation of the Escherichia coli chromosome reveals its soft nature

Pelletier

Halvorsen

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

187

270

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Replicating bacterial chromosomes continuously demix from each other and segregate within a compact volume inside the cell called the nucleoid. Although many proteins involved in this process have been identified, the nature of the global forces that shape and segregate the chromosomes has remained unclear because of limited knowledge of the micromechanical properties of the chromosome. In this work, we demonstrate experimentally the fundamentally soft nature of the bacterial chromosome and the entropic forces that can compact it in a crowded intracellular environment. We developed a unique "micropiston" and measured the force-compression behavior of single Escherichia coli chromosomes in confinement. Our data show that forces on the order of 100 pN and free energies on the order of 10 5 k B T are sufficient to compress the chromosome to its in vivo size. For comparison, the pressure required to hold the chromosome at this size is a thousand-fold smaller than the surrounding turgor pressure inside the cell. Furthermore, by manipulation of molecular crowding conditions (entropic forces), we were able to observe in real time fast (approximately 10 s), abrupt, reversible, and repeatable compaction-decompaction cycles of individual chromosomes in confinement. In contrast, we observed much slower dissociation kinetics of a histone-like protein HU from the whole chromosome during its in vivo to in vitro transition. These results for the first time provide quantitative, experimental support for a physical model in which the bacterial chromosome behaves as a loaded entropic spring in vivo.chromosome segregation | depletion forces | polymer physics | mother machine | optical trap

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Cohesin, condensin, and the intramolecular centromere loop together generate the mitotic chromatin spring

Abstract: During mitosis, spindle microtubule force is balanced by the combined activities of the cohesin and condensin SMC complexes and intramolecular pericentric chromatin loops.

Cited by 132 publications

References 68 publications

Cohesins and condensins orchestrate the 4D dynamics of yeast chromosomes during the cell cycle

Cohesins and condensins orchestrate the 4D dynamics of yeast chromosomes during the cell cycle

Sgo1 recruits PP2A to chromosomes to ensure sister chromatid bi-orientation in mitosis

Physical manipulation of the Escherichia coli chromosome reveals its soft nature

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