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Mitotic chromosomes are self-entangled and disentangle through a Topoisomerase II-dependent two stage exit from mitosis

ABSTRACT: The topological state of chromosomes determines their mechanical properties, dynamics, and function. Recent work indicated that interphase chromosomes are largely free of entanglements. Here, we use Hi-C, polymer simulations and multi-contact 3C, and propose that, in contrast, mitotic chromosomes are self-entangled. We explore how a mitotic self-entangled state is converted into an unentangled interphase state during mitotic exit. Most mitotic entanglements are removed during anaphase/telophase, with remaining ones removed during early G1, in a Topoisomerase II-dependent process. Polymer models suggest a two-stage disentanglement pathway: first, decondensation of mitotic chromosomes with remaining condensin loops produces entropic forces that bias Topoisomerase II activity towards decatenation. At the second stage, the loops are released, and formation of new entanglements is prevented by lower Topoisomerase II activity, allowing the establishment of unentangled and territorial G1 chromosomes. When mitotic entanglements are not removed, in experiment and models, a normal interphase state cannot be acquired.

ORGANISM(S): Homo sapiens

PROVIDER: GSE198610 | GEO | 2024/03/07

REPOSITORIES: GEO

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Metaphase-Chromosome-Organization

Project description:Mitotic chromosomes are among the most recognizable structures in the cell, yet for over a century their internal organization remains largely unsolved. We applied chromosome conformation capture methods, 5C and Hi-C, across the cell cycle and revealed two alternative three-dimensional folding states of the human genome. We show that the highly compartmentalized and cell-type-specific organization described previously for non-synchronous cells is restricted to interphase. In metaphase, we identify a homogenous folding state, which is locus-independent, common to all chromosomes, and consistent among cell types, suggesting a general principle of metaphase chromosome organization. Using polymer simulations, we find that metaphase Hi-C data is inconsistent with classic hierarchical models, and is instead best described by a linearly-organized longitudinally compressed array of consecutive chromatin loops.

2013-11-05 | E-MTAB-1948 | biostudies-arrayexpress

Cohesin-dependent compaction of mitotic chromosomes in budding yeast

Project description:The extreme length of chromosomal DNA requires organizing mechanisms to both promote functional genetic interactions and ensure faithful chromosome segregation when cells divide. Microscopy and genome wide contact frequency (Hi-C) analyses indicate that intra-chromosomal looping of DNA is a primary pathway of chromosomal organization during all stages of the cell cycle (Dekker, J. & Mirny, L. . Cell 164, 1110–1121 (2016). Although the enzymatic pathways required for DNA loop formation are yet to be fully characterized, the activity of the SMC family of proteins has been consistently associated with this process in interphase and mitosis. Here we use Hi-C to study the reorganization of budding yeast chromosome conformation in early mitosis and the role of SMCs in this process. Using polymer simulations, we find that the differences between interphase and mitotic Hi-C maps can be explained by the formation of intra-chromosomal (cis-) loops in mitotic chromosomes. We demonstrate that mitotic SMC cohesin activity is required for formation of cis-loops, independently of sister-chromatid cohesion. In contrast, SMC condensin is not required for loop formation in these early mitotic cells. Rather condensin activity promotes distinct higher order structures in the chromosomes at centromeres and in the rDNA proximal regions. Thus we demonstrate that cohesin-dependent cis-loops provide the primary higher order organization of budding yeast mitotic chromosomes, independently of condensin and sister chromatid cohesion.

2017-03-22 | GSE87311 | GEO

Fission yeast condensin contributes to interphase chromatin organization and prevents transcription-coupled DNA damage

Project description:Background: Structural maintenance of chromosomes (SMC) complexes are central organizers of chromatin architecture throughout the cell cycle. The SMC family member condensin is best known for establishing long-range chromatin interactions in mitosis. These compact chromatin and create mechanically stable chromosomes. How condensin contributes to chromatin organization in interphase is less well understood. Results: Here, we use efficient conditional depletion of fission yeast condensin to determine its contribution to interphase chromatin organization. We deplete condensin in G2 arrested cells to preempt confounding effects from cell cycle progression without condensin. Genome-wide chromatin interaction mapping, using Hi-C, reveals condensin-mediated chromatin interactions in interphase that are qualitatively similar to those observed in mitosis, but quantitatively far less prevalent. Despite its low abundance, chromatin mobility tracking shows that condensin markedly confines interphase chromatin movements. Without condensin, chromatin behaves as an unconstrained Rouse polymer with excluded volume, while condensin constrains its mobility. Unexpectedly, we find that condensin is required during interphase to prevent ongoing transcription from eliciting a DNA damage response. Conclusions: In addition to establishing mitotic chromosome architecture, condensin-mediated long-range chromatin interactions contribute to shaping chromatin organization in interphase. The resulting structure confines chromatin mobility and protects the genome from transcription-induced DNA damage. This adds to the important roles of condensin in maintaining chromosome stability.

2020-09-14 | GSE143338 | GEO

Analysis of barley chromosomal proteome: a multiapproach exploration of flow cytometry-sorted mitotic chromosomes

Project description:Proteins contribute to the structure of chromatin and regulate its functions. The basic building block of chromatin in eukaryotes is the nucleosome containing histones. Structural maintenance of chromosomes complexes perform the assembly of genomic DNA into the higher organizational structures of interphase chromatin as well as the compact arrangement of dividing chromosomes. Here, proteins were extracted from flow cytometry-sorted barley mitotic chromosomes after a nuclease treatment to remove DNA. Peptides from tryptic protein digests were fractionated either on a cation exchanger or reversed-phase microgradient system prior to liquid chromatography coupled to tandem mass spectrometry. Nuclear and chromosomal proteins (almost 900 identifications) were then classified based on a combination of software prediction results, available database localization information, sequence homology, and domain representation. The degree of enrichment of the chromosome samples by chromosomal proteins was evaluated by comparing the results with controls (depleted flow cytometric fraction and initial cell lyzate). A biological context evaluation indicated the presence of several groups of abundant proteins including histone variants, topoisomerase 2, PARP2, Condensin complex subunits, and many proteins with chromatin-related functions. Interestingly, nucleolar proteins were found as wells as proteins documenting processes related to replication, transcription and DNA repair in barley mitotic chromosomes.

2021-07-21 | PXD024689 | Pride

The length and strength of compartmental interactions are modulated by condensin II activity [Hi-C]

Project description:Condensin II plays a crucial role in shaping chromosome structure throughout the cell cycle, but its specific functions during interphase have remained unclear. In this study, we utilized Oligopaints and Hi-C techniques to investigate how changes in condensin II levels affect chromosome organization across various length scales. Our findings reveal that condensin II has a significant impact on long-range interactions within chromosomes, which are essential for the organization of intrachromosomal compartments. Importantly, these effects occur independently of the chromatin state. Furthermore, overexpression of condensin II during interphase leads to the formation of "peri-centric super stripes" observed through Hi-C analysis, indicating a disruption of the boundary between heterochromatin and euchromatin on Drosophila chromosomes. Collectively, our results challenge the existing belief that compartments form without the involvement of a loop extruder and suggest that condensin II activity is a prerequisite for driving proximity between distal compartmental domains within chromosomes.

2023-09-03 | GSE242222 | GEO

The length and strength of compartmental interactions are modulated by condensin II activity [RNA-Seq]

2023-09-03 | GSE242223 | GEO

Condensin-mediated remodeling of the mitotic chromatin landscape in fission yeast

Project description:Chromatin fibres dynamically change their organisation during cell cycle. In interphase nucleus, chromatin fibres are evenly distributed whereas their spatial occupancy are reorganised to form condensed chromosomes in mitosis. This process called chromosome condensation is necessary for an accomplishment of faithful chromosome segregation. One of the Structural Maintenance of Chromosomes complexes, Condensin, is indispensable for chromosome condensation. It remains, however, unknown how Condensin plays its role in shaping mitotic chromosome. Here we show that chromatin fibres change their interacting partners; short-range contacts in interphase nucleus are converted into long-range interactions to shape condensed chromosomes. This conversion of interactions among chromatin fibres results in the formation of larger domains within mitotic chromosomes. Condensin is solely in charge of the conversion and large domain formation in fission yeast mitosis. Our results show how fission yeast Condensin is involved in shaping mitotic chromosomes.

2017-07-13 | GSE94475 | GEO

Condensin-mediated remodeling of the mitotic chromatin landscape in fission yeast

2017-07-13 | GSE94474 | GEO

RNA pol II transcript abundance controls condensin accumulation at mitotically upregulated and heat shock-inducible genes in fission yeast

Project description:Condensin plays fundamental roles in chromosome dynamics. In this study, we determined the binding sites of condensin on fission yeast (Schizosaccharomyces pombe) chromosomes at the level of nucleotide sequences using chromatin immunoprecipitation (ChIP) and ChIP-sequencing (ChIP-seq). We found that condensin binds to RNA polymerase I-, II- and III-transcribed genes during both mitosis and interphase, and we focused on pol II constitutive and inducible genes. Accumulation sites for condensin are distinct from those of cohesin and DNA topoisomerase II. Using cell cycle stage- and heat shock-inducible genes, we demonstrate that pol II-mediated transcripts cause condensin accumulation. First, condensin’s enrichment on mitotically activated genes was abolished by deleting the sep1+ gene that encodes an M-phase-specific forkhead transcription factor. Second, by raising the temperature, condensin accumulation was rapidly induced at heat shock protein genes in interphase and even during mid-mitosis. In interphase, condensin accumulates preferentially during the post-replicative phase. pol II-mediated transcription was neither repressed nor activated by condensin, as levels of transcripts per se did not change when mutant condensin failed to associate with chromosomal DNA. However, massive chromosome missegregation occurred, suggesting that abundant pol II transcription may require active condensin prior to proper chromosome segregation.

2015-04-15 | GSE65956 | GEO

Chip-chip from C-33 cells expressing FLAG-HPV1 E2 with FLAG-HPV1 E2

Project description:HPV1 E2 binds with Brd4 to host mitotic chromosomes. To identify the targets, chromatin was prepared from mitotic C-33 cells expressing HPV1 E2, and analyzed by ChIP-chip analysis for binding to a portion of the human genome. E2 and Brd4 bind to active promoters in interphase C-33 cells (Jang et al., 2009), however, in mitosis E2 was observed instead to bind to a few extremely broad peaks on several chromosomes. These peaks ranged in size from several hundred Kb to >1 Mb and, for the most part, overlapped coding regions. Signals of anti-FLAG E2 ChIP DNA from mitotic HPV1 E2 expressing C-33 cells

2014-04-14 | E-GEOD-52312 | biostudies-arrayexpress

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