Nucleosome Chiral Transition under Positive Torsional Stress in Single Chromatin Fibers

Bancaud, Aurélien; Wagner, Gaudeline; Silva, Natalia Conde e; Lavelle, Christophe; Wong, Hua; Mozziconacci, Julien; Barbi, Maria; Sivolob, Andrei; Cam, Eric Le; Mouawad, Liliane; Viovy, Jean‐Louis; Victor, Jean–Marc; Prunell, Ariel

doi:10.1016/j.molcel.2007.05.037

Cited by 131 publications

(159 citation statements)

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“…Right-handed DNA writhe observed in (H3-H4) 2 tetrasomes in vitro (45,46) suggests a mechanism for the entrapment of a metastable right-handed turn per "reversome" particle in nucleosome arrays subjected to large positive torsional stress (47,48). In vivo, compensatory positive supercoils generated, for example, as a result of transcription could potentially trigger the flip from nucleosome to reversome.…”

Section: Coupling Between 2-μm Plasmid and Chromosome Segregationmentioning

confidence: 97%

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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Section: Coupling Between 2-μm Plasmid and Chromosome Segregationmentioning

confidence: 97%

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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“…It is reasonable to speculate that when this action of condensin is compromised, catenanes between sister DNAs fail to be removed completely, thereby causing defects in sister chromatid resolution and segregation in anaphase (e.g., Coelho et al 2003;Hudson et al 2003;D'Ambrosio et al 2008a). In the future, it will be important to address how positive superhelical tension imposed by condensin might alter nucleosome structures (Bancaud et al 2007) and how topo II might act on such nucleosome templates (Roca 2009).…”

Section: Supercoiling and Decatenating Dsdnamentioning

confidence: 99%

Condensins: universal organizers of chromosomes with diverse functions

2012

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Condensins are multisubunit protein complexes that play a fundamental role in the structural and functional organization of chromosomes in the three domains of life. Most eukaryotic species have two different types of condensin complexes, known as condensins I and II, that fulfill nonoverlapping functions and are subjected to differential regulation during mitosis and meiosis. Recent studies revealed that the two complexes contribute to a wide variety of interphase chromosome functions, such as gene regulation, recombination, and repair. Also emerging are their cell type- and tissue-specific functions and relevance to human disease. Biochemical and structural analyses of eukaryotic and bacterial condensins steadily uncover the mechanisms of action of this class of highly sophisticated molecular machines. Future studies on condensins will not only enhance our understanding of chromosome architecture and dynamics, but also help address a previously underappreciated yet profound set of questions in chromosome biology.

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“…Recently, reversomes (for reverse nucleosomes, built on a righthanded tetrasome) were proposed to form under the action of a DNA supercoiling wave pushed in front of the RNA polymerase (Lavelle and Prunell 2007). The nucleosome reversome would facilitate transcription elongation by giving the RNA polymerase a lever to break the docking of the H2A-H2B dimers, which otherwise exerts a stringent blocking against transcription in absence of other factors (Bancaud et al 2007). By a dynamical domino-like effect, the elongation process of compact regularly spaced nucleosomal intragenic arrays might result in a reversome wave that would progress faster than the RNA polymerase.…”

Section: Proof Onlymentioning

confidence: 99%

Thermodynamics of Intragenic Nucleosome Ordering

et al. 2009

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Numerous AU2studies of chromatin structure showed that nucleosome free regions (NFRs) located at 59 gene ends contribute to transcription initiation regulation. Here, we determine the role of intragenic chromatin structure on gene expression regulation. We show that, along Saccharomyces cerevisiae genes, nucleosomes are highly organized following two types of architecture that depend only on the distance between the NFRs located at the 59 and 39 gene ends. In the first type, this distance constrains in vivo the positioning of n nucleosomes regularly organized in a ''crystal-like'' array. In the second type, this distance is such that the corresponding genes can accommodate either n or (n + 1) nucleosomes, thereby displaying two possible crystal-like arrays of n weakly compacted or n + 1 highly compacted nucleosomes. This adaptability confers ''bistable'' properties to chromatin and is a key to its dynamics. Compared to crystal-like genes, bi-stable genes present higher transcriptional plasticity, higher sensitivity to chromatin regulators, higher H3 turnover rate, and lower H2A.Z enrichment. The results strongly suggest that transcription elongation is facilitated by higher chromatin compaction. The data allow us to propose a new paradigm of transcriptional control mediated by the stability and the level of compaction of the intragenic chromatin architecture and open new ways for investigating eukaryotic gene expression regulation.

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Nucleosome Chiral Transition under Positive Torsional Stress in Single Chromatin Fibers

Cited by 131 publications

References 50 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

Condensins: universal organizers of chromosomes with diverse functions

Thermodynamics of Intragenic Nucleosome Ordering

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