How are nucleosomes disrupted during transcription elongation?

Zlatanova, Jordanka; Victor, Jean–Marc

doi:10.2976/1.3249971

Cited by 11 publications

(11 citation statements)

References 19 publications

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“…Topo I is a rapid, processive, torque-sensitive enzyme with low activity on nucleosomal templates [45–46] that is well-evolved to act ahead of elongating RNA polymerase where accumulated positive torsional stress and histone modifications mobilize nucleosomes [47]. Inhibiting Topo I slows elongation in vivo [5].…”

Section: Discussionmentioning

confidence: 99%

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Transcription-dependent dynamic supercoiling is a short-range genomic force

Kouzine

Gupta

Baranello

et al. 2013

Nat Struct Mol Biol

287

327

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Transcription has the capacity to modify mechanically DNA topology, DNA structure, and nucleosome arrangement. Resulting from ongoing transcription, these modifications in turn, may provide instant feedback to the transcription machinery. To substantiate the connection between transcription and DNA dynamics, we charted an ENCODE map of transcription-dependent dynamic supercoiling in human Burkitt lymphoma cells using psoralen photobinding to probe DNA topology in vivo. Dynamic supercoils spread ~1.5 kb upstream of the start sites of active genes. Low and high output promoters handle this torsional stress differently as shown using inhibitors of transcription and topoisomerases, and by chromatin immunoprecipation of RNA polymerase and topoisomerases I and II. Whereas lower outputs are managed adequately by topoisomerase I, high output promoters additionally require topoisomerase II. The genome-wide coupling between transcription and DNA topology emphasizes the importance of dynamic supercoiling for gene regulation.

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Section: Discussionmentioning

confidence: 99%

“…In vitro studies functionally couple chromatin structure with DNA topology [47]. DNA supercoiling may assist chromatin remodeling, influence chromatin and DNA structure, and modify DNA-transcription factor interactions [1].…”

Section: Discussionmentioning

confidence: 99%

Transcription-dependent dynamic supercoiling is a short-range genomic force

Kouzine

Gupta

Baranello

et al. 2013

Nat Struct Mol Biol

287

327

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“…However, this and other proposals have only considered events around the TSS, whereas our study is unique in observing features of paused genes throughout gene bodies. One proposal for the immediate disruption of downstream nucleosomes at the 87A Hsp70 locus during heat shock (Petesch and Lis 2008) is that the sudden acceleration of Pol II transit elicits a wave of positive supercoiling ahead that causes nucleosomes to unwrap before the topoisomerase swivel can relieve the strain (Zlatanova and Victor 2009). The fact that ordinary genes show high nucleosome occupancy when they are active (Cui et al 2010) suggests that transcriptional elongation has evolved such that eviction of nucleosomes upon sudden acceleration of RNA polymerases is minimized.…”

Section: Discussionmentioning

confidence: 99%

Heat shock reduces stalled RNA polymerase II and nucleosome turnover genome-wide

Teves¹,

Henikoff²

2011

Genes Dev.

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Heat shock rapidly induces expression of a subset of genes while globally repressing transcription, making it an attractive system to study alterations in the chromatin landscape that accompany changes in gene regulation. We characterized these changes in Drosophila cells by profiling classical low-salt-soluble chromatin, RNA polymerase II (Pol II), and nucleosome turnover dynamics at single-base-pair resolution. With heat shock, low-salt-soluble chromatin and stalled Pol II levels were found to decrease within gene bodies, but no overall changes were detected at transcriptional start sites. Strikingly, nucleosome turnover decreased genome-wide within gene bodies upon heat shock in a pattern similar to that observed with inhibition of Pol II elongation, especially at genes involved in the heat-shock response. Relatively high levels of nucleosome turnover were also observed throughout the bodies of genes with paused Pol II. These observations suggest that down-regulation of transcription during heat shock involves reduced nucleosome mobility and that this process has evolved to promote heat-shock gene regulation. Our ability to precisely map both nucleosomal and subnucleosomal particles directly from low-saltsoluble chromatin extracts to assay changes in the chromatin landscape provides a simple general strategy for epigenome characterization.

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“…Consequently, it was suggested that at each round of transcription, the positive supercoiling is pushed ahead of RNA polymerase. Accumulated positive torsional stress induces structural modification of nucleosomes and creates conditions in which polymerase efficiently elongates through the nucleosomal array [44,68]. Negative stress in the wake of the transcription machinery facilitates rapid re-formation of nucleosomes behind the elongating complex.…”

Section: Dna Supercoiling In Regulatory Pathwaysmentioning

confidence: 99%

The importance of being supercoiled: How DNA mechanics regulate dynamic processes

Baranello

Levens

Gupta

et al. 2012

Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanism

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Through dynamic changes in structure resulting from DNA-protein interactions and constraints given by the structural features of the double helix, chromatin accommodates and regulates different DNA-dependent processes. All DNA transactions (such as transcription, DNA replication and chromosomal segregation) are necessarily linked to strong changes in the topological state of the double helix known as torsional stress or supercoiling. As virtually all DNA transactions are in turn affected by the torsional state of DNA, these changes have the potential to serve as regulatory signals detected by protein partners. This two-way relationship indicates that DNA dynamics may contribute to the regulation of many events occurring during cell life. In this review we will focus on the role of DNA supercoiling in the cellular processes, with particular emphasis on transcription. Besides giving an overview on the multiplicity of factors involved in the generation and dissipation of DNA torsional stress, we will discuss recent studies which give new insight into the way cells use DNA dynamics to perform functions otherwise not achievable.

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How are nucleosomes disrupted during transcription elongation?

Cited by 11 publications

References 19 publications

Transcription-dependent dynamic supercoiling is a short-range genomic force

Transcription-dependent dynamic supercoiling is a short-range genomic force

Heat shock reduces stalled RNA polymerase II and nucleosome turnover genome-wide

The importance of being supercoiled: How DNA mechanics regulate dynamic processes

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