“Breaking Up Is Hard to Do”: The Formation and Resolution of Sister Chromatid Intertwines

Baxter, Jonathan

doi:10.1016/j.jmb.2014.08.022

Journal of Molecular Biology

2015

DOI: 10.1016/j.jmb.2014.08.022

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“Breaking Up Is Hard to Do”: The Formation and Resolution of Sister Chromatid Intertwines

Jonathan Baxter

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Cited by 22 publications

(40 citation statements)

References 110 publications

(141 reference statements)

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“…These intertwines are subsequently resolved by the action of type II topoisomerases. If type II topoisomerases do not completely resolve either the precatenanes or the full DNA catenanes formed at the completion of replication, the unresolved intertwines will cause chromosome bridging, nondisjunction, and aneuploidy (5). Fork rotation and DNA precatenation appear to be the primary pathway of unlinking when forks come together at the termination of DNA replication (6,7).…”

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confidence: 99%

“…However, unlike viral replisomes and replication complexes established in in vitro systems, the eukaryotic replisome holoenzyme is composed of a far greater number of proteins and activities. These factors are thought to facilitate replication through the highly variable eukaryotic genomic landscape and coordinate DNA synthesis with other chromatid maturation processes such as chromatin assembly and cohesion establishment (5). These latter processes act on the same newly replicated DNA potentially braided by precatenation.…”

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confidence: 99%

“…These latter processes act on the same newly replicated DNA potentially braided by precatenation. How these activities occurring in the wake of the fork may be impeded by precatenation is unexplored (5).…”

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confidence: 99%

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Fork rotation and DNA precatenation are restricted during DNA replication to prevent chromosomal instability

Schalbetter

Mansoubi

Chambers

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

106

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Faithful genome duplication and inheritance require the complete resolution of all intertwines within the parental DNA duplex. This is achieved by topoisomerase action ahead of the replication fork or by fork rotation and subsequent resolution of the DNA precatenation formed. Although fork rotation predominates at replication termination, in vitro studies have suggested that it also occurs frequently during elongation. However, the factors that influence fork rotation and how rotation and precatenation may influence other replication-associated processes are unknown. Here we analyze the causes and consequences of fork rotation in budding yeast. We find that fork rotation and precatenation preferentially occur in contexts that inhibit topoisomerase action ahead of the fork, including stable protein-DNA fragile sites and termination. However, generally, fork rotation and precatenation are actively inhibited by Timeless/Tof1 and Tipin/Csm3. In the absence of Tof1/Timeless, excessive fork rotation and precatenation cause extensive DNA damage following DNA replication. With Tof1, damage related to precatenation is focused on the fragile protein-DNA sites where fork rotation is induced. We conclude that although fork rotation and precatenation facilitate unwinding in hard-to-replicate contexts, they intrinsically disrupt normal chromosome duplication and are therefore restricted by Timeless/Tipin.uring DNA replication, it is essential to completely unwind and remove all of the intertwining between the two strands of the template DNA double helix. This is achieved by the combined action of replicative helicases and topoisomerases. During elongation, replicative helicases force the strands apart, generating compensatory topological overwinding stress in the unreplicated region ahead of the fork. If overwinding accumulates, it prevents further DNA replication (1, 2). Relaxation of the stress is achieved either by topoisomerase action ahead of the fork, directly on the overwound region, or by coupling helicase action with rotation of the whole fork relative to the unreplicated DNA (Fig. S1). This latter pathway relaxes topological stress ahead of the fork at the expense of generating double-stranded intertwines behind the fork, often referred to as DNA precatenanes (3, 4). These intertwines are subsequently resolved by the action of type II topoisomerases. If type II topoisomerases do not completely resolve either the precatenanes or the full DNA catenanes formed at the completion of replication, the unresolved intertwines will cause chromosome bridging, nondisjunction, and aneuploidy (5). Fork rotation and DNA precatenation appear to be the primary pathway of unlinking when forks come together at the termination of DNA replication (6, 7). In addition, fork rotation appears to be a frequent event during elongation in vitro; it can support ongoing replication, and extensive precatenation is observed behind elongating forks (8-10). Therefore, the prevailing view is that the topological stress caused by DNA unwinding is reso...

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confidence: 99%

mentioning

confidence: 99%

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Fork rotation and DNA precatenation are restricted during DNA replication to prevent chromosomal instability

Schalbetter

Mansoubi

Chambers

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

106

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“…It was hypothesized that the connections might be resolved by introducing transitory breaks in the strands, but one had to wait 30 years for these enzymes to be identified (see review, Ref. [1]). …”

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confidence: 99%

“…Here, we are particularly delighted to present seven comprehensive reviews [1][2][3][4][5][6][7], one perspective [8] and one communication [9] that altogether report the latest developments in the field of genome biology. Recent research revealed an intricate nuclear organization and a high level of hierarchy in its architecture.…”

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confidence: 99%

Why Is Nuclear Organization Dynamic, Hierarchical and Intricate? Implications for Gene Regulation, Cellular Differentiation and Disease

Ostankovitch¹,

Soutoglou

2015

Journal of Molecular Biology

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The Localization and Action of Topoisomerase IV in Escherichia coli Chromosome Segregation Is Coordinated by the SMC Complex, MukBEF

et al. 2015

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SummaryThe type II topoisomerase TopoIV, which has an essential role in Escherichia coli chromosome decatenation, interacts with MukBEF, an SMC (structural maintenance of chromosomes) complex that acts in chromosome segregation. We have characterized the intracellular dynamics of individual TopoIV molecules and the consequences of their interaction with MukBEF clusters by using photoactivated-localization microscopy. We show that ∼15 TopoIV molecules per cell are associated with MukBEF clusters that are preferentially localized to the replication origin region (ori), close to the long axis of the cell. A replication-dependent increase in the fraction of immobile molecules, together with a proposed catalytic cycle of ∼1.8 s, is consistent with the majority of active TopoIV molecules catalyzing decatenation, with a minority maintaining steady-state DNA supercoiling. Finally, we show that the MukB-ParC interaction is crucial for timely decatenation and segregation of newly replicated ori DNA.

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“Breaking Up Is Hard to Do”: The Formation and Resolution of Sister Chromatid Intertwines

Cited by 22 publications

References 110 publications

Fork rotation and DNA precatenation are restricted during DNA replication to prevent chromosomal instability

Fork rotation and DNA precatenation are restricted during DNA replication to prevent chromosomal instability

Why Is Nuclear Organization Dynamic, Hierarchical and Intricate? Implications for Gene Regulation, Cellular Differentiation and Disease

The Localization and Action of Topoisomerase IV in Escherichia coli Chromosome Segregation Is Coordinated by the SMC Complex, MukBEF

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