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Cohesin-dependent chromosome loop extrusion is limited by transcription and stalled replication forks [Hi-C]

ABSTRACT: Genome function depends on regulated chromosome folding, and loop extrusion by the protein complex cohesin is essential for this multilayered organization. The chromosomal positioning of cohesin is controlled by transcription, and the complex also localizes to stalled replication forks. However, the role of transcription and replication in chromosome looping remains unclear. Here, we show that reduction of chromosome-bound RNA polymerase weakens normal cohesin loop extrusion boundaries, allowing cohesin to form new long-range chromosome cis interactions. Stress response genes activated by transcription inhibition are also shown to act as new loop extrusion boundaries. Furthermore, cohesin loop extrusion during early S-phase is jointly controlled by transcription and replication units. Together, the results reveal that replication and transcription machineries are chromosome folding regulators that block the progression of loop-extruding cohesin, opening for new perspectives on cohesin’s roles in genome function and stability.

ORGANISM(S): Saccharomyces cerevisiae

PROVIDER: GSE162193 | GEO | 2022/06/15

REPOSITORIES: GEO

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Cohesin-dependent chromosome loop extrusion is limited by transcription and stalled replication forks [RNA-seq]

Project description:Genome function depends on regulated chromosome folding, and loop extrusion by the protein complex cohesin is essential for this multilayered organization. The chromosomal positioning of cohesin is controlled by transcription, and the complex also localizes to stalled replication forks. However, the role of transcription and replication in chromosome looping remains unclear. Here, we show that reduction of chromosome-bound RNA polymerase weakens normal cohesin loop extrusion boundaries, allowing cohesin to form new long-range chromosome cis interactions. Stress response genes activated by transcription inhibition are also shown to act as new loop extrusion boundaries. Furthermore, cohesin loop extrusion during early S-phase is jointly controlled by transcription and replication units. Together, the results reveal that replication and transcription machineries are chromosome folding regulators that block the progression of loop-extruding cohesin, opening for new perspectives on cohesin’s roles in genome function and stability.

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Cohesin-dependent chromosome loop extrusion is limited by transcription and stalled replication forks [ChIP-seq]

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Loop-extruding Smc5/6 organizes transcription-induced positive DNA supercoils [RNA-seq]

Project description:The Structural Maintenance of Chromosome (SMC) protein complexes cohesin, condensin and the Smc5/6 complex (Smc5/6) are essential for chromosome function. At the molecular level, these complexes fold DNA by loop extrusion. Accordingly, cohesin creates chromosome loops in interphase, and condensin compacts mitotic chromosomes. However, the role of Smc5/6’s recently discovered DNA loop extrusion activity is unknown. Here, we uncover that Smc5/6 controls the spatial organization of supercoiled chromosomal regions. The results show that Smc5/6 associates with transcription-induced positively supercoiled chromosomal DNA at cohesin-dependent chromosome loop boundaries. Mechanistically, single-molecule imaging reveals that dimers of Smc5/6 specifically recognize the tip of positively supercoiled DNA plectonemes, and efficiently initiates loop extrusion to gather the supercoiled DNA into a large plectonemic loop. Finally, Hi-C analysis shows that Smc5/6 links chromosomal regions containing transcription-induced positive supercoiling in cis. Altogether, our findings indicate that Smc5/6 controls the three-dimensional organization of chromosomes by recognizing and initiating loop extrusion on positively supercoiled DNA.

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A cohesin traffic pattern genetically linked to gene regulation [Hi-C]

Project description:Cohesin-mediated loop extrusion folds interphase chromosomes at the ten to hundreds kilobases scale. This process produces structural features such as loops and topologically associating domains. We identify three types of cis-elements that define the chromatin folding landscape generated by loop extrusion. First, CTCF sites form boundaries by stalling extruding cohesin, as shown before. Second, transcription termination sites form boundaries by acting as cohesin unloading sites. RNA polymerase II contributes to boundary formation at transcription termination sites. Third, transcription start sites form boundaries that are mostly independent of cohesin, but are sites where cohesin can pause. Together with cohesin loading at enhancers, and possibly other cis-elements, these loci create a dynamic pattern of cohesin traffic along the genome that guides enhancer-promoter interactions. Disturbing this traffic pattern, by removing CTCF barriers, makes cells sensitive to deletion of genes involved in transcription initiation, such as the SAGA and TFIID complexes, and RNA processing such DEAD-Box RNA helicases. In the absence of CTCF, several of these factors fail to be efficiently recruited to active promoters. We propose that the complex pattern of cohesin movement along chromatin contributes to appropriate promoter-enhancer interactions and localization of transcription and RNA processing factors to active genes.

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Cohesin-dependent chromosome loop extrusion is limited by transcription and stalled replication forks

Project description:Cohesin-dependent chromosome loop extrusion is limited by transcription and stalled replication forks

| PRJNA680814 | ENA

Cohesin chromatin loop formation by an extrinsic motor (Micro-C)

Project description:The ring-shaped cohesin complex topologically entraps two DNAs to establish sister chromatid cohesion. Cohesin also shapes the interphase chromatin landscape, with wide-ranging implications for gene regulation, which cohesin is thought to achieve by actively extruding DNA loops without topologically entrapping DNA. The ‘loop extrusion’ model find motivation from in vitro observations - whether this process indeed underlies chromatin loop formation in vivo remains untested. Here, using the budding yeast S. cerevisiae, we generate cohesin variants that have lost their ability to extrude DNA loops but retain their ability to topologically entrap DNA. Analysis of these variants suggests that in vivo chromatin loops form independently of loop extrusion. Instead, we find that transcription promotes loop formation, likely by generating DNA substrates for topological loop capture. Transcription furthermore acts as an extrinsic motor that, by pushing cohesin along transcription units, extends chromatin loops and defines their ultimate positions. Our results necessitate a re-evaluation of the loop extrusion hypothesis and point to an alternative mechanism for cohesin-dependent chromatin organisation. Loop formation by DNA-DNA capture, akin to sister chromatid cohesion establishment at replication forks, unifies cohesin’s two roles in chromosome segregation and interphase genome organisation.

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