Unlinking of Supercoiled DNA Catenanes by Type IIA Topoisomerases

Vologodskii, Alexander

doi:10.1016/j.bpj.2011.08.011

Cited by 13 publications

(11 citation statements)

References 49 publications

(73 reference statements)

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“…Although efficient resolution of cen-UFBs is mediated primarily by TOP2A, it is facilitated by PICH and TOP3A (96,132). Since the decatenation activity of TOP2 has been proposed to be most efficient on positively supercoiled catenanes, there is the intriguing possibility that PICH and TOP3A catalyze positive supercoiling in order to facilitate the rapid decatenation of cen-UFBs through stimulation of TOP2A (135)(136)(137). In this context and by analogy with the function of prokaryotic Reverse-gyrases critical to protect DNA against thermal denaturation (38,97,138), the positive supercoiling activity of the PICH-TOP3A complex might also contribute to protecting DNA against denaturation when exposed to mitotic spindle forces (139).…”

Section: Roles Of Top3a At Ultra-fine Anaphase Bridgesmentioning

confidence: 99%

The many lives of type IA topoisomerases

Bizard

Hickson

2020

Journal of Biological Chemistry

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The double helical structure of genomic DNA is both elegant and functional in that it serves both to protect vulnerable DNA bases and to facilitate DNA replication and compaction. However, these design advantages come at the cost of having to evolve and maintain a cellular machinery that can manipulate a long polymeric molecule that readily becomes topologically entangled whenever it has to open for translation, replication, or repair. If such a machinery fails to eliminate detrimental topological entanglements, utilization of the information stored in the DNA double helix is compromised. As a consequence, the use of Bform DNA as the carrier of genetic information must have co-evolved with a means to manipulate its complex topology. This duty is performed by DNA topoisomerases, which therefore are, unsurprisingly, ubiquitous in all kingdoms of life. In this review, we focus on how DNA topoisomerases catalyze their impressive range of DNA-conjuring tricks, with a particular emphasis on DNA topoisomerase III (TOP3). Once thought to be the most unremarkable of topoisomerases, the many lives of these type IA topoisomerases are now being progressively revealed. This research interest is driven by a realization that their substrate versatility and their ability to engage in intimate collaborations with translocases and other DNA-processing enzymes are far more extensive and impressive than was thought hitherto. This, coupled with the recent associations of TOP3s with developmental and neurological pathologies in humans, is clearly making us reconsider their undeserved reputation as being unexceptional enzymes.

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Section: Roles Of Top3a At Ultra-fine Anaphase Bridgesmentioning

confidence: 99%

The many lives of type IA topoisomerases

Bizard

Hickson

2020

Journal of Biological Chemistry

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“…Understanding the interplay between supercoiling and pre-catenation in partially replicated molecules is hindered, though, by the fact that DNA conformation is disturbed during sample preparation. On the other hand, several studies convincingly proved that computer simulation can give a very accurate description of the DNA properties that are difficult to address experimentally (Martinez-Robles et al, 2009;Rawdon et al, 2016;Vologodskii, 2011;Vologodskii and Rybenkov, 2009;Vologodskii and Cozzarelli, 1993;Witz and Stasiak, 2010). For all these reasons, here we used the worm-like chain (WLC) model in combination with Metropolis Monte Carlo (MC) numerical simulation to study the dynamics of DNA topology in partially replicated plasmid DNA molecules, once these RIs are isolated in vitro.…”

Section: Introductionmentioning

confidence: 99%

Distribution of torsional stress between the un-replicated and replicated regions in partially replicated molecules

López‐Martínez

Schaerer

Hernández

et al. 2020

Journal of Biomolecular Structure and Dynamics

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DNA topology changes continuously as replication proceeds. Unwinding of the DNA duplex by helicases is favored by negative supercoiling but it causes the progressive accumulation of positive supercoiling ahead of the fork. This torsional stress must be removed for the fork to keep advancing. Elimination of this positive torsional stress may be accomplished by topoisomerases acting solely ahead of the fork or simultaneously in the un-replicated and replicated regions after diffusion of some positive torsional strain from the un-replicated to the replicated regions by swivelling of the replication forks. In any case, once replication is completed fully replicated molecules are known to be heavily catenated and this catenation derives from pre-catenanes formed during replication. Although there is still controversy as to whether fork swiveling redistributes this positive torsional stress continuously or only as termination approaches, the forces that cause fork rotation and the generation of precatenanes are still poorly characterized. Here we used a numerical simulation, based on the worm-like chain model and the Metropolis Monte Carlo method, to study the interchange of supercoiling and pre-catenation in a naked circular DNA molecule of 4,440 bp partially replicated in vivo and in vitro. We propose that a dynamic gradient of torsional stress between the un-replicated and replicated regions drives fork swiveling allowing the interchange of supercoiling and pre-catenation.

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“…Curiously, in Saccharomyces cerevisiae , fully replicated catenanes were found to be transiently positively supercoiled (Figure 9B) during mitosis (76). Computer simulations showed that positive supercoiling of individual DNA circles in catenanes with right-handed crossings makes these catenanes more likely to undergo decatenation by type II DNA topoisomerases as compared to right-handed catenanes composed of negative supercoiled DNA circles (98).…”

Section: Introductionmentioning

confidence: 99%

Closing the DNA replication cycle: from simple circular molecules to supercoiled and knotted DNA catenanes

Schvartzman

Hernández

Krimer

et al. 2019

Nucleic Acids Research

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Due to helical structure of DNA, massive amounts of positive supercoils are constantly introduced ahead of each replication fork. Positive supercoiling inhibits progression of replication forks but various mechanisms evolved that permit very efficient relaxation of that positive supercoiling. Some of these mechanisms lead to interesting topological situations where DNA supercoiling, catenation and knotting coexist and influence each other in DNA molecules being replicated. Here, we first review fundamental aspects of DNA supercoiling, catenation and knotting when these qualitatively different topological states do not coexist in the same circular DNA but also when they are present at the same time in replicating DNA molecules. We also review differences between eukaryotic and prokaryotic cellular strategies that permit relaxation of positive supercoiling arising ahead of the replication forks. We end our review by discussing very recent studies giving a long-sought answer to the question of how slow DNA topoisomerases capable of relaxing just a few positive supercoils per second can counteract the introduction of hundreds of positive supercoils per second ahead of advancing replication forks.

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Unlinking of Supercoiled DNA Catenanes by Type IIA Topoisomerases

Cited by 13 publications

References 49 publications

The many lives of type IA topoisomerases

The many lives of type IA topoisomerases

Distribution of torsional stress between the un-replicated and replicated regions in partially replicated molecules

Closing the DNA replication cycle: from simple circular molecules to supercoiled and knotted DNA catenanes

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