Topoisomerase 1 activity during mitotic transcription favors the transition from mitosis to G1

Wiegard, Anika; Kuzin, Vladislav; Cameron, Donald P.; Grosser, Jan; Ceribelli, Michele; Mehmood, Rashid; Ballarino, Roberto; Valant, Francesco; Grochowski, Radosław; Karabogdan, Ivana; Crosetto, Nicola; Lindqvist, Arne; Bizard, Anna H.; Kouzine, Fedor; Natsume, Toyoaki; Baranello, Laura

doi:10.1016/j.molcel.2021.10.015

Cited by 19 publications

(17 citation statements)

References 96 publications

(137 reference statements)

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“…Chromatin immunoprecipitation of GapR combined with high-throughput sequencing was used to generate maps of positive supercoiling in bacteria and yeast [ 97 ]. Detection of topoisomerase activity sites (Middle panel) and non-B DNA structures (Bottom panel) are also powerful methods to predict DNA supercoiling in vivo [ 71 , 132 , 146 ]. There has been considerable concordance between the studies supporting the main prophecies of the twin-supercoiled domain model: negative torsional stress accumulated at the upstream promoter region of the active genes, while positive torsional stress accrues in a transcription-dependent manner in gene bodies and downstream to the 3’ ends of genes.…”

Section: Overviewmentioning

confidence: 99%

“…If the genomic distribution of positive supercoiling is disturbed, the next cell cycle is impaired. The study shows that during mitotic transcription [ 131 ], Pol II and Top1 coordinate their activities [ 132 ]. Deregulated Pol II-Top1 coordination or acute degradation of Top1 cause mitotic defects, cell cycle delays, and impaired transcription in the following cell cycle.…”

Section: Mechanical Epigeneticsmentioning

confidence: 99%

“…This preference indicates that positive supercoiling acquired in TADs and loops during the cell cycle is important for appropriate condensin function. If the required level of positive supercoiling is lost because of excessive annihilating negative supercoiling generated by mitotic transcription, the transition to the new cell cycle is delayed and the daughter cells experience a ‘temporal amnesia’ [ 132 ].…”

Section: Mechanical Epigeneticsmentioning

confidence: 99%

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Mechanical determinants of chromatin topology and gene expression

Jha

Levens

Kouzine

2022

Nucleus

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The compaction of linear DNA into micrometer-sized nuclear boundaries involves the establishment of specific three-dimensional (3D) DNA structures complexed with histone proteins that form chromatin. The resulting structures modulate essential nuclear processes such as transcription, replication, and repair to facilitate or impede their multi-step progression and these contribute to dynamic modification of the 3D-genome organization. It is generally accepted that protein–protein and protein–DNA interactions form the basis of 3D-genome organization. However, the constant generation of mechanical forces, torques, and other stresses produced by various proteins translocating along DNA could be playing a larger role in genome organization than currently appreciated. Clearly, a thorough understanding of the mechanical determinants imposed by DNA transactions on the 3D organization of the genome is required. We provide here an overview of our current knowledge and highlight the importance of DNA and chromatin mechanics in gene expression.

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Section: Overviewmentioning

confidence: 99%

Section: Mechanical Epigeneticsmentioning

confidence: 99%

Section: Mechanical Epigeneticsmentioning

confidence: 99%

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Mechanical determinants of chromatin topology and gene expression

Jha

Levens

Kouzine

2022

Nucleus

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“…The nuclear membrane also loses its continuity in mitotic cells and no longer serves as a tight barrier between the cytoplasm and chromatin (3). Given that transcription is rapidly re-established after cell division (2, 4), mechanisms must exist to facilitate the precise and accurate reestablishment of gene expression after mitosis (5). One proposed mechanism, termed mitotic bookmarking, suggests that the binding of proteins, mainly transcription factors (TFs), to specific genomic loci during mitosis marks genes for rapid activation after cell division (6).…”

Section: Introductionmentioning

confidence: 99%

Distinct modes of heat shock transcription factor interactions with mitotic chromosomes

Price

Budzyński

Shen

et al. 2022

Preprint

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A large number of transcription factors have been shown to bind and interact with mitotic chromosomes, which may promote the efficient reactivation of transcriptional programs following cell division. Although the DNA-binding domain (DBD) contributes strongly to TF behavior, TFs from the same DBD family can display distinct binding behaviors during mitosis. To define the mechanisms governing TF behavior during mitosis in mouse embryonic stem cells, we examined two related TFs: Heat Shock Factor 1 and 2 (HSF1 and HSF2). We found that HSF2 maintains site-specific binding genome-wide during mitosis, whereas HSF1 binding is globally decreased. Surprisingly, live-cell imaging shows that both factors appear excluded from mitotic chromosomes, and are similarly more dynamic in mitosis than in interphase. Exclusion from mitotic DNA is not due to extrinsic factors like nuclear import and export mechanisms. Rather, we found that the HSF2 DBD alone can coat mitotic chromosomes, but is insufficient to promote HSF1 coating. These data further confirm that site-specific binding and chromosome coating are independent properties, and that for some TFs, mitotic behavior is largely determined by the non-DBD regions.

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“…Studies in human cells proposed that the transcription termination Factor 2 (TTF2) drives the removal of active PolII in mitosis (Liu et al , 1998) whereas the transcription initiation inhibitor Gdown1 was shown to gain access to chromatin solely during mitosis to repress mitotic transcription (Ball et al , 2022). Recent studies have also proposed that specific mechanisms ensure promoter clearance upon mitotic entry, mediated by PolII-mediated activation of Top1, to release topological stress (Wiegard et al , 2021) or hyperactivation of P-TEFb, to enhance transcriptional elongation (Liang et al , 2015).…”

Section: Introductionmentioning

confidence: 99%

An SNF2 helicase-like protein links mitotic transcription termination to sister chromatid resolution

Carmo

Coelho

Silva

et al. 2022

Preprint

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Mitotic chromatin is largely assumed incompatible with transcription due to changes in the transcription machinery and chromosome architecture. However, the mechanisms of mitotic transcriptional inactivation and their interplay with chromosome assembly remain largely unknown. By monitoring ongoing transcription in Drosophila early embryos, we reveal that eviction of nascent mRNAs from mitotic chromatin occurs after substantial chromosome compaction and is not promoted by condensin I. Instead, we show that the timely removal of transcripts from mitotic chromatin is driven by the SNF2 helicase-like protein Lodestar (Lds), identified here as a modulator of sister chromatid cohesion defects. In addition to transcriptional termination, we uncovered that Lds cooperates with Topoisomerase 2 to ensure efficient sister chromatid resolution and mitotic fidelity. We conclude that mitotic transcriptional termination is not a passive consequence of cell cycle progression and/or chromosome compaction but occurs via dedicated mechanisms with functional parallelisms to sister chromatid resolution.

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Topoisomerase 1 activity during mitotic transcription favors the transition from mitosis to G1

Cited by 19 publications

References 96 publications

Mechanical determinants of chromatin topology and gene expression

Mechanical determinants of chromatin topology and gene expression

Distinct modes of heat shock transcription factor interactions with mitotic chromosomes

An SNF2 helicase-like protein links mitotic transcription termination to sister chromatid resolution

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