Mechanism of Topology Simplification by Type II DNA Topoisomerases

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2001 Mar 15

PMID 11248029

Citations 73

Authors

A V Vologodskii

W Zhang

V V Rybenkov

A A Podtelezhnikov

D Subramanian

J D Griffith

N R Cozzarelli

Affiliations

Soon will be listed here.

Abstract

Type II DNA topoisomerases actively reduce the fractions of knotted and catenated circular DNA below thermodynamic equilibrium values. To explain this surprising finding, we designed a model in which topoisomerases introduce a sharp bend in DNA. Because the enzymes have a specific orientation relative to the bend, they act like Maxwell's demon, providing unidirectional strand passage. Quantitative analysis of the model by computer simulations proved that it can explain much of the experimental data. The required sharp DNA bend was demonstrated by a greatly increased cyclization of short DNA fragments from topoisomerase binding and by direct visualization with electron microscopy.

Citing Articles

Osmotic disruption of chromatin induces Topoisomerase 2 activity at sites of transcriptional stress.

Gittens W, Allison R, Wright E, Brown G, Neale M Nat Commun. 2024; 15(1):10606.

PMID: 39639049 PMC: 11621772. DOI: 10.1038/s41467-024-54567-6.

Structural and functional insights into the T-even type bacteriophage topoisomerase II.

Xin Y, Xian R, Yang Y, Cong J, Rao Z, Li X Nat Commun. 2024; 15(1):8719.

PMID: 39379365 PMC: 11461880. DOI: 10.1038/s41467-024-53037-3.

What's on the Other Side of the Gate: A Structural Perspective on DNA Gate Opening of Type IA and IIA DNA Topoisomerases.

Vidmar V, Vayssieres M, Lamour V Int J Mol Sci. 2023; 24(4).

PMID: 36835394 PMC: 9960139. DOI: 10.3390/ijms24043986.

DNA-Stimulated Liquid-Liquid phase separation by eukaryotic topoisomerase ii modulates catalytic function.

Jeong J, Lee J, Carcamo C, Parker M, Berger J Elife. 2022; 11.

PMID: 36342377 PMC: 9674351. DOI: 10.7554/eLife.81786.

Kinetics of DNA looping by Anabaena sensory rhodopsin transducer (ASRT) by using DNA cyclization assay.

Lee J, Kim S, Lee K, Chuon K, Jung K, Kim D Sci Rep. 2021; 11(1):23721.

PMID: 34887464 PMC: 8660804. DOI: 10.1038/s41598-021-03148-4.

References

Yan J, Magnasco M, Marko J . A kinetic proofreading mechanism for disentanglement of DNA by topoisomerases. Nature. 1999; 401(6756):932-5. DOI: 10.1038/44872. View

Wang J . Moving one DNA double helix through another by a type II DNA topoisomerase: the story of a simple molecular machine. Q Rev Biophys. 1998; 31(2):107-44. DOI: 10.1017/s0033583598003424. View

Podtelezhnikov A, Mao C, Seeman N, Vologodskii A . Multimerization-cyclization of DNA fragments as a method of conformational analysis. Biophys J. 2000; 79(5):2692-704. PMC: 1301149. DOI: 10.1016/S0006-3495(00)76507-6. View

Griffith J, Christiansen G . Electron microscope visualization of chromatin and other DNA-protein complexes. Annu Rev Biophys Bioeng. 1978; 7:19-35. DOI: 10.1146/annurev.bb.07.060178.000315. View

Ulanovsky L, Bodner M, Trifonov E, Choder M . Curved DNA: design, synthesis, and circularization. Proc Natl Acad Sci U S A. 1986; 83(4):862-6. PMC: 322970. DOI: 10.1073/pnas.83.4.862. View

Taylor W, Hagerman P . Application of the method of phage T4 DNA ligase-catalyzed ring-closure to the study of DNA structure. II. NaCl-dependence of DNA flexibility and helical repeat. J Mol Biol. 1990; 212(2):363-76. DOI: 10.1016/0022-2836(90)90131-5. View

Crothers D, DRAK J, Kahn J, Levene S . DNA bending, flexibility, and helical repeat by cyclization kinetics. Methods Enzymol. 1992; 212:3-29. DOI: 10.1016/0076-6879(92)12003-9. View

Roca J, Wang J . The capture of a DNA double helix by an ATP-dependent protein clamp: a key step in DNA transport by type II DNA topoisomerases. Cell. 1992; 71(5):833-40. DOI: 10.1016/0092-8674(92)90558-t. View

Rybenkov V, Cozzarelli N, Vologodskii A . Probability of DNA knotting and the effective diameter of the DNA double helix. Proc Natl Acad Sci U S A. 1993; 90(11):5307-11. PMC: 46705. DOI: 10.1073/pnas.90.11.5307. View

10.

Roca J, Wang J . DNA transport by a type II DNA topoisomerase: evidence in favor of a two-gate mechanism. Cell. 1994; 77(4):609-16. DOI: 10.1016/0092-8674(94)90222-4. View

11.

Roca J, Berger J, Harrison S, Wang J . DNA transport by a type II topoisomerase: direct evidence for a two-gate mechanism. Proc Natl Acad Sci U S A. 1996; 93(9):4057-62. PMC: 39486. DOI: 10.1073/pnas.93.9.4057. View

12.

Berger J, Wang J . Recent developments in DNA topoisomerase II structure and mechanism. Curr Opin Struct Biol. 1996; 6(1):84-90. DOI: 10.1016/s0959-440x(96)80099-6. View

13.

Wang J . DNA topoisomerases. Annu Rev Biochem. 1996; 65:635-92. DOI: 10.1146/annurev.bi.65.070196.003223. View

14.

Ullsperger C, Cozzarelli N . Contrasting enzymatic activities of topoisomerase IV and DNA gyrase from Escherichia coli. J Biol Chem. 1996; 271(49):31549-55. DOI: 10.1074/jbc.271.49.31549. View

15.

Roca J, Wang J . The probabilities of supercoil removal and decatenation by yeast DNA topoisomerase II. Genes Cells. 1996; 1(1):17-27. DOI: 10.1046/j.1365-2443.1996.01001.x. View

16.

Rybenkov V, Vologodskii A, Cozzarelli N . The effect of ionic conditions on the conformations of supercoiled DNA. II. Equilibrium catenation. J Mol Biol. 1997; 267(2):312-23. DOI: 10.1006/jmbi.1996.0877. View

17.

Rybenkov V, Ullsperger C, Vologodskii A, Cozzarelli N . Simplification of DNA topology below equilibrium values by type II topoisomerases. Science. 1997; 277(5326):690-3. DOI: 10.1126/science.277.5326.690. View

18.

Pulleyblank D . Of topo and Maxwell's dream. Science. 1997; 277(5326):648-9. DOI: 10.1126/science.277.5326.648. View

19.

Morais Cabral J, Jackson A, Smith C, Shikotra N, Maxwell A, Liddington R . Crystal structure of the breakage-reunion domain of DNA gyrase. Nature. 1997; 388(6645):903-6. DOI: 10.1038/42294. View

20.

BAIRD C, Harkins T, Morris S, Lindsley J . Topoisomerase II drives DNA transport by hydrolyzing one ATP. Proc Natl Acad Sci U S A. 1999; 96(24):13685-90. PMC: 24125. DOI: 10.1073/pnas.96.24.13685. View