Biophysical Characterization of the Centromere-specific Nucleosome from Budding Yeast

Kingston, Isabel J.; Yung, Jasmine Sum Yee; Singleton, Martin R.

doi:10.1074/jbc.m110.189340

Cited by 84 publications

(103 citation statements)

References 23 publications

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“…These findings also speak to the current debate on whether CenH3-containing nucleosomes engender the normal left-handed, or the opposite right-handed DNA writhe (21)(22)(23). The in vivo topology of STB revealed in the present investigation and that of CEN deduced from an earlier study (21) are consistent with the right-handed writhe.…”

supporting

confidence: 75%

“…Experimental evidence in favor of a histone tetramer [hemisome; H2A/H2B/H4/(CenH3 = Cse4)] or a histone octamer (H2A/H2B/H4/CenH3/CenH3/H4/H2B/ H2A) has been reported (22,25,(28)(29)(30). The specter of an unusual hexameric nucleosome core, bereft of H2A and H2B, but including the Cse4-associated nonhistone protein Scm3 [H4/ Cse4/Cse4/H4-(Scm3)2], has also been raised (31).…”

Section: Discussionmentioning

confidence: 99%

“…Strikingly, in vitro assembled CENPA-containing nucleosomes induce the conventional negative writhe in DNA. Depending on assembly conditions, DNA can be wrapped in a left-or right-handed fashion around Cse4-containing nucleosomes in vitro (21,22).…”

Section: Discussionmentioning

confidence: 99%

“…The chiral ambiguities of in vitro assembled Cse4 nucleosomes (21,22) likely arise from conditions that induce alternative histone stoichiometries, modulate their stacking preferences, and promote DNA contacts that are permissive of either left-or right-handed DNA writhe. The deduced in vivo topologies, protected against such vagaries perhaps by the stabilizing influence of the kinetochore and plasmid partitioning complexes, are unlikely to distort the authentic chirality of CEN or STB chromatin.…”

Section: Coupling Between 2-μm Plasmid and Chromosome Segregationmentioning

confidence: 99%

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Histone H3-variant Cse4-induced positive DNA supercoiling in the yeast plasmid has implications for a plasmid origin of a chromosome centromere

Huang

Chang

Cui

et al. 2011

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

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The Saccharomyces cerevisiae 2-μm plasmid is a multicopy selfish genome that resides in the nucleus. The genetic organization of the plasmid is optimized for stable, high-copy propagation in hostcell populations. The plasmid's partitioning system poaches host factors, including the centromere-specific histone H3-variant Cse4 and the cohesin complex, enabling replicated plasmid copies to segregate equally in a chromosome-coupled fashion. We have characterized the in vivo chromatin topology of the plasmid partitioning locus STB in its Cse4-associated and Cse4-nonassociated states. We find that the occupancy of Cse4 at STB induces positive DNA supercoiling, with a linking difference (ΔLk) contribution estimated between +1 and +2 units. One plausible explanation for this contrary topology is the presence of a specialized Cse4-containing nucleosome with a right-handed DNA writhe at a functional STB, contrasted by a standard histone H3-containing nucleosome with a left-handed DNA writhe at a nonfunctional STB. The similarities between STB and centromere in their nucleosome signature and DNA topology would be consistent with the potential origin of the unusual point centromere of budding yeast chromosomes from the partitioning locus of an ancestral plasmid.CEN evolution | nucleosome topology | reversome T he 2-μm plasmid of Saccharomyces cerevisiae resides in the nucleus at 40 to 60 copies per cell, and propagates itself with nearly the same stability as chromosomes (1, 2). The plasmid is a benign selfish DNA element that seems to provide no advantage to its host, but poses, at its normal copy number, no serious disadvantage either. In haploid cells the plasmid is organized into a cluster of three to five foci, and segregates as a cluster (3). This effective reduction in copy number necessitates an active partitioning system, comprised of two plasmid-coded proteins, Rep1 and Rep2, and a cis-acting partitioning locus STB, to ensure equal or nearly equal plasmid segregation. A decline in plasmid copy number because of rare missegregation events is corrected via DNA amplification triggered by the Flp sitespecific recombination system harbored by the plasmid (4, 5). Positive and negative regulatory circuits implemented through the plasmid-coded Raf1 protein and the Rep proteins ensure quick amplification response without the danger of runaway increase in copy number (6-8).The Rep-STB system channels several host factors involved in chromosome segregation toward the execution of plasmid segregation. These factors include the mitotic spindle, the spindleassociated motor Kip1, the RSC2 chromatin-remodeling complex, the centromere-specific histone H3-variant Cse4 (CenH3), and the yeast cohesin complex (9-15). The de novo assembly of the plasmid-partitioning complex at STB during the G1-S window of each cell cycle (9,12,14,16) is reminiscent of the assembly of the kinetochore complex at centromeres. However, kinetochore components have not been detected at STB by ChIP (13).The assembly of the plasmid-partitioning complex culmin...

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supporting

confidence: 75%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Coupling Between 2-μm Plasmid and Chromosome Segregationmentioning

confidence: 99%

See 2 more Smart Citations

Histone H3-variant Cse4-induced positive DNA supercoiling in the yeast plasmid has implications for a plasmid origin of a chromosome centromere

Huang

Chang

Cui

et al. 2011

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

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“…Overexpression of CENP-A has recently been shown to cause CENP-A/H3.3 heterotypic octameric nucleosomes assembly on chromosomal arms (Lacoste et al 2014). However, as the predominant CENP-A nucleosome species at centromeres appears to be homotypic octamers, the functional relevance of heterotypic octamers remains unclear (Foltz et al 2006;Kingston et al 2011). Determining whether CENP-A nucleosomes change composition during the cell cycle and how those transitions occur is an important future goal.…”

Section: The Structure Of Cenp-a-containing Nucleosomesmentioning

confidence: 99%

The Centromere: Epigenetic Control of Chromosome Segregation during Mitosis

Westhorpe

Straight

2014

Cold Spring Harb Perspect Biol

143

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A fundamental challenge for the survival of all organisms is maintaining the integrity of the genome in all cells. Cells must therefore segregate their replicated genome equally during each cell division. Eukaryotic organisms package their genome into a number of physically distinct chromosomes, which replicate during S phase and condense during prophase of mitosis to form paired sister chromatids. During mitosis, cells form a physical connection between each sister chromatid and microtubules of the mitotic spindle, which segregate one copy of each chromatid to each new daughter cell. The centromere is the DNA locus on each chromosome that creates the site of this connection. In this review, we present a brief history of centromere research and discuss our current knowledge of centromere establishment, maintenance, composition, structure, and function in mitosis.

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Variations on a nucleosome theme: The structural basis of centromere function

Moreno-Moreno

Torras-Llort²,

Azorı́n³

2017

BioEssays

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The centromere is a specialized chromosomal structure that dictates kinetochore assembly and, thus, is essential for accurate chromosome segregation. Centromere identity is determined epigenetically by the presence of a centromere-specific histone H3 variant, CENP-A, that replaces canonical H3 in centromeric chromatin. Here, we discuss recent work by Roulland et al. that identifies structural elements of the nucleosome as essential determinants of centromere function. In particular, CENP-A nucleosomes have flexible DNA ends due to the short αN helix of CENP-A. The higher flexibility of the DNA ends of centromeric nucleosomes impairs binding of linker histones H1, while it facilitates binding of other essential centromeric proteins, such as CENP-C, and is required for mitotic fidelity. This work extends previous observations indicating that the differential structural properties of CENP-A nucleosomes are on the basis of its contribution to centromere identity and function. Here, we discuss the implications of this work and the questions arising from it.

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Biophysical Characterization of the Centromere-specific Nucleosome from Budding Yeast

Cited by 84 publications

References 23 publications

Histone H3-variant Cse4-induced positive DNA supercoiling in the yeast plasmid has implications for a plasmid origin of a chromosome centromere

Histone H3-variant Cse4-induced positive DNA supercoiling in the yeast plasmid has implications for a plasmid origin of a chromosome centromere

The Centromere: Epigenetic Control of Chromosome Segregation during Mitosis

Variations on a nucleosome theme: The structural basis of centromere function

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