The Why and How of DNA Unlinking

Overview

Journal Nucleic Acids Res

Publisher Oxford University Press

Specialty Biochemistry

Date 2009 Feb 26

PMID 19240147

Citations 50

Authors

Zhirong Liu

Richard W Deibler

Hue Sun Chan

Lynn Zechiedrich

Affiliations

Soon will be listed here.

Abstract

The nucleotide sequence of DNA is the repository of hereditary information. Yet, it is now clear that the DNA itself plays an active role in regulating the ability of the cell to extract its information. Basic biological processes, including control of gene transcription, faithful DNA replication and segregation, maintenance of the genome and cellular differentiation are subject to the conformational and topological properties of DNA in addition to the regulation imparted by the sequence itself. How do these DNA features manifest such striking effects and how does the cell regulate them? In this review, we describe how misregulation of DNA topology can lead to cellular dysfunction. We then address how cells prevent these topological problems. We close with a discussion on recent theoretical advances indicating that the topological problems, themselves, can provide the cues necessary for their resolution by type-2 topoisomerases.

Citing Articles

Concise Overview of Methodologies Employed in the Study of Bacterial DNA Replication.

Maciag-Dorszynska M, Morcinek-Orlowska J, Baranska S Int J Mol Sci. 2025; 26(2).

PMID: 39859162 PMC: 11764726. DOI: 10.3390/ijms26020446.

Interactions between Zoliflodacin and Gyrase and Topoisomerase IV: Enzymological Basis for Cellular Targeting.

Collins J, Basarab G, Chibale K, Osheroff N ACS Infect Dis. 2024; 10(8):3071-3082.

PMID: 39082980 PMC: 11320581. DOI: 10.1021/acsinfecdis.4c00438.

Interactions between Gepotidacin and Gyrase and Topoisomerase IV: Genetic and Biochemical Evidence for Well-Balanced Dual-Targeting.

Oviatt A, Gibson E, Huang J, Mattern K, Neuman K, Chan P ACS Infect Dis. 2024; 10(4):1137-1151.

PMID: 38606465 PMC: 11015057. DOI: 10.1021/acsinfecdis.3c00346.

Target-Mediated Fluoroquinolone Resistance in : Actions of Ciprofloxacin against Gyrase and Topoisomerase IV.

Collins J, Oviatt A, Chan P, Osheroff N ACS Infect Dis. 2024; 10(4):1351-1360.

PMID: 38606464 PMC: 11015056. DOI: 10.1021/acsinfecdis.4c00041.

Gyrase and Topoisomerase IV: Recycling Old Targets for New Antibacterials to Combat Fluoroquinolone Resistance.

Collins J, Osheroff N ACS Infect Dis. 2024; 10(4):1097-1115.

PMID: 38564341 PMC: 11019561. DOI: 10.1021/acsinfecdis.4c00128.

References

Corbett A, Zechiedrich E, Osheroff N . A role for the passage helix in the DNA cleavage reaction of eukaryotic topoisomerase II. A two-site model for enzyme-mediated DNA cleavage. J Biol Chem. 1992; 267(2):683-6. View

Baxter J, Diffley J . Topoisomerase II inactivation prevents the completion of DNA replication in budding yeast. Mol Cell. 2008; 30(6):790-802. DOI: 10.1016/j.molcel.2008.04.019. View

Bao X, Lee H, Quake S . Behavior of complex knots in single DNA molecules. Phys Rev Lett. 2004; 91(26 Pt 1):265506. DOI: 10.1103/PhysRevLett.91.265506. View

Benjamin K, Abola A, Kanaar R, Cozzarelli N . Contributions of supercoiling to Tn3 resolvase and phage Mu Gin site-specific recombination. J Mol Biol. 1996; 256(1):50-65. DOI: 10.1006/jmbi.1996.0067. View

Maritan A, Micheletti C, Trovato A, Banavar J . Optimal shapes of compact strings. Nature. 2000; 406(6793):287-90. DOI: 10.1038/35018538. View

Moore C, Klevan L, Wang J, Griffith J . Gyrase . DNA complexes visualized as looped structures by electron microscopy. J Biol Chem. 1983; 258(7):4612-7. View

Schoeffler A, Berger J . DNA topoisomerases: harnessing and constraining energy to govern chromosome topology. Q Rev Biophys. 2008; 41(1):41-101. DOI: 10.1017/S003358350800468X. View

Bliska J, Cozzarelli N . Use of site-specific recombination as a probe of DNA structure and metabolism in vivo. J Mol Biol. 1987; 194(2):205-18. DOI: 10.1016/0022-2836(87)90369-x. View

Baaklini I, Usongo V, Nolent F, Sanscartier P, Hraiky C, Drlica K . Hypernegative supercoiling inhibits growth by causing RNA degradation. J Bacteriol. 2008; 190(22):7346-56. PMC: 2576660. DOI: 10.1128/JB.00680-08. View

10.

Postow L, Hardy C, Arsuaga J, Cozzarelli N . Topological domain structure of the Escherichia coli chromosome. Genes Dev. 2004; 18(14):1766-79. PMC: 478196. DOI: 10.1101/gad.1207504. View

11.

Deibler R, Mann J, Sumners D, Zechiedrich L . Hin-mediated DNA knotting and recombining promote replicon dysfunction and mutation. BMC Mol Biol. 2007; 8:44. PMC: 1904230. DOI: 10.1186/1471-2199-8-44. View

12.

Andrews C, Vas A, Meier B, Gimenez-Abian J, Diaz-Martinez L, Green J . A mitotic topoisomerase II checkpoint in budding yeast is required for genome stability but acts independently of Pds1/securin. Genes Dev. 2006; 20(9):1162-74. PMC: 1472475. DOI: 10.1101/gad.1367206. View

13.

Travers A, Muskhelishvili G . A common topology for bacterial and eukaryotic transcription initiation?. EMBO Rep. 2007; 8(2):147-51. PMC: 1796767. DOI: 10.1038/sj.embor.7400898. View

14.

Hickford J, Jones R, Courrech du Pont S, Eggers J . Knotting probability of a shaken ball-chain. Phys Rev E Stat Nonlin Soft Matter Phys. 2007; 74(5 Pt 1):052101. DOI: 10.1103/PhysRevE.74.052101. View

15.

. DNA knotting abolishes in vitro chromatin assembly. J Biol Chem. 1996; 271(24):14150-5. DOI: 10.1074/jbc.271.24.14150. View

16.

Burnier Y, Weber C, Flammini A, Stasiak A . Local selection rules that can determine specific pathways of DNA unknotting by type II DNA topoisomerases. Nucleic Acids Res. 2007; 35(15):5223-31. PMC: 1976442. DOI: 10.1093/nar/gkm532. View

17.

Masliah G, Rene B, Zargarian L, Fermandjian S, Mauffret O . Identification of intrinsic dynamics in a DNA sequence preferentially cleaved by topoisomerase II enzyme. J Mol Biol. 2008; 381(3):692-706. DOI: 10.1016/j.jmb.2008.06.024. View

18.

Adams D, SHEKHTMAN E, Zechiedrich E, Schmid M, Cozzarelli N . The role of topoisomerase IV in partitioning bacterial replicons and the structure of catenated intermediates in DNA replication. Cell. 1992; 71(2):277-88. DOI: 10.1016/0092-8674(92)90356-h. View

19.

Wang X, Reyes-Lamothe R, Sherratt D . Modulation of Escherichia coli sister chromosome cohesion by topoisomerase IV. Genes Dev. 2008; 22(17):2426-33. PMC: 2532930. DOI: 10.1101/gad.487508. View

20.

Sinden R, Carlson J, PETTIJOHN D . Torsional tension in the DNA double helix measured with trimethylpsoralen in living E. coli cells: analogous measurements in insect and human cells. Cell. 1980; 21(3):773-83. DOI: 10.1016/0092-8674(80)90440-7. View