Local selection rules that can determine specific pathways of DNA unknotting by type II DNA topoisomerases

Nucleic Acids Research

Volumn 35, Issue 15, 2007, Pages 5223-5231

  Burnier, Yannis ^a,c   Weber, Cedric ^a,d   Flammini, Alessandro ^b   Stasiak, Andrzej ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b INDIANA UNIVERSITY   (United States)

^c EPFL   (Switzerland)

^d INSTITUT ROMAND DE RECHERCHE NUMÉRIQUE EN PHYSIQUE DES MATÉRIAUX IRRMA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

DNA TOPOISOMERASE (ATP HYDROLYSING);

ARTICLE; DNA CROSS LINKING; DNA STRAND BREAKAGE; DNA STRUCTURE; DNA TRANSPOSITION; GEOMETRY; PRIORITY JOURNAL; PROTEIN PROCESSING; SIMULATION; STRUCTURE ANALYSIS;

COMPUTER SIMULATION; DNA; DNA TOPOISOMERASES, TYPE II; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION;

EID: 34548576981     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkm532     Document Type: Article

References (51)

1. Maxwell,A., Costenaro,L., Mitelheiser,S. and Bates,A.D. (2005) Coupling ATP hydrolysis to DNA strand passage in type IIA DNA topoisomerases. Biochem. Soc. Trans., 33, 1460-1464.
2. Bates,A.D. and Maxwell,A. (2005) DNA Topology. Oxford University Press, Oxford.
3. Schvartzman,J.B. and Stasiak,A. (2004) A topological view of the replicon. EMBO Rep., 5, 256-261.
4. Portugal,J. and Rodriguez-Campos,A. (1996) T7 RNA polymerase cannot transcribe through a highly knotted DNA template. Nucleic Acids Res. 24, 4890-4894.
5. Olavarrieta,L., Martinez-Robles,M.L., Sogo,J.M., Stasiak,A., Hernandez,P., Krimer,D.B. and Schvartzman,J.B. (2002) Supercoiling, knotting and replication fork reversal in partially replicated plasmids. Nucleic Acids Res., 30, 656-666.
6. Rybenkov,V.V., Ullsperger,C., Vologodskii,A.V. and Cozzarelli,N.R. (1997) Simplification of DNA topology below equilibrium values by type II topoisomerases. Science, 277, 690-693.
7. Yan,J., Magnasco,M.O. and Marko,J.F. (1999) A kinetic proof-reading mechanism for disentanglement of DNA by topoisomerases. Nature, 401, 932-935.
8. Vologodskii,A.V., Zhang,W., Rybenkov,V.V., Podtelezhnikov,A.A., Subramanian,D., Griffith,J.D. and Cozzarelli,N.R. (2001) Mechanism of topology simplification by type II DNA topoisomerases. Proc. Natl Acad. Sci. USA, 98, 3045-3049.
9. Roca,J. (2001) Varying levels of positive and negative supercoiling differently affect the efficiency with which topoisomerase II catenates and decatenates DNA. J. Mol. Biol., 305, 441-450.
10. Klenin,K., Langowski,J. and Vologodskii,A. (2002) Computational analysis of the chiral action of type II DNA topoisomerases. J. Mol. Biol., 320, 359-367.
11. Trigueros,S., Salceda,J., Bermudez,I., Fernandez,X. and Roca,J. (2004) Asymmetric removal of supercoils suggests how topoisomerase II simplifies DNA topology. J. Mol. Biol., 335, 723-731.
12. Buck,G.R. and Zechiedrich,E.L. (2004) DNA disentangling by type-2 topoisomerases. J. Mol. Biol., 340, 933-939.
13. Liu,Z., Mann,J.K., Zechiedrich,E.L. and Chan,H.S. (2006) Topological information embodied in local juxtaposition geometry provides a statistical mechanical basis for unknotting by type-2 DNA topoisomerases. J. Mol. Biol., 361, 268-285.
14. Liu,Z., Zechiedrich,E.L. and Chan,H.S. (2006) Inferring global topology from local juxtaposition geometry: Interlinking polymer rings and ramifications for topoisomerase action. Biophys. J., 90, 2344-2355.
15. Janse van Rensburg,E.J. and Whittington,S.G. (1990) The knot probability in lattice polygons. J. Phys. A: Math. Gen., 23, 3573-3590.
16. Yao,A., Matsuda,H., Tsukahara,H., Shimamura,M.K. and Deguchi,T. (2001) On the dominance of trivial knots among SAPs on a cubic lattice. J. Phys. A: Math. Gen., 34, 7563-7577.
17. Rybenkov,V.V., Cozzarelli,N.R. and Vologodskii,A.V. (1993) Probability of DNA knotting and the effective diameter of the DNA double helix. Proc. Natl Acad. Sci. USA, 90, 5307-5311.
18. Shaw,S.Y. and Wang,J.C. (1993) Knotting of a DNA chain during ring closure. Science, 260, 533-536.
19. Adrian,M., Ten Heggeler-Bordier,B., Wahli,W., Stasiak,A.Z., Stasiak,A. and Dubochet,J. (1990) Direct visualization of super-coiled DNA molecules in solution. EMBO J., 9, 4551-4554.
20. Bednar,J., Furrer,P., Stasiak,A., Dubochet,J., Egelman,E.H. and Bates,A.D. (1994) The twist, writhe and overall shape of supercoiled DNA change during counterion-induced transition from a loosely to a tightly interwound superhelix. Possible implications for DNA structure in vivo. J. Mol. Biol., 235, 825-847.
21. Flammini,A., Maritan,A. and Stasiak,A. (2004) Simulations of action of DNA topoisomerases to investigate boundaries and shapes of spaces of knots. Biophys. J., 87, 2968-2975.
22. Hua,X., Nguyen,D., Raghavan,B., Arsuaga,J. and Vazquez,M. (2007) Random state transitions of knots: A first step towards modeling unknotting by type II topoisomerases. Topol. Appl., 154, 1381-1397.
23. Ewing,B. and Millett,K.C. (1996) Progress in Knot Theory and Related Topics Herman, Paris, Vol. 56, pp. 51-68.
24. Cloutier,T.E. and Widom,J. (2004) Spontaneous sharp bending of double-stranded DNA. Mol. Cell, 14, 355-362.
25. Du,Q., Smith,C., Shiffeldrim,N., Vologodskaia,M. and Vologodskii,A. (2005) Cyclization of short DNA fragments and bending fluctuations of the double helix. Proc. Natl Acad. Sci. USA, 102, 5397-5402.
26. Wiggins,P.A. and Nelson,P.C. (2006) Generalized theory of semiflexible polymers. Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 73, 031906.
27. Mann,J.K., Deibler,R.W., Sumners,D.W. and Zechiedrich,E.L. (2004) Unknotting by type II topoisomerases. Abstracts of papers presented to the American Mathematical Society, 25, 994-992-187.
28. Wasserman,S.A. and Cozzarelli,N.R. (1991) Supercoiled DNA-directed knotting by T4 topoisomerase. J. Biol. Chem., 266, 20567-20573.
29. Sogo,J.M., Stasiak,A., Martinez-Robles,M.L., Krimer,D.B., Hernandez,P. and Schvartzman,J.B. (1999) Formation of knots in partially replicated DNA molecules. J. Mol. Biol., 286, 637-643.
30. Flammini,A. and Stasiak,A. (2006) Natural classification of knots. Proc. R. Soc. A, 463, 569-582.
31. Katritch,V., Bednar,J., Michoud,D., Scharein,R.G., Dubochet,J. and Stasiak,A. (1996) Geometry and physics of knots. Nature, 384 142-145.
32. Cerf,C. and Stasiak,A. (2000) A topological invariant to predict the three-dimensional writhe of ideal configurations of knots and links. Proc. Natl Acad. Sci. USA, 97, 3795-3798.
33. Janse van Rensburg,E.J., Orlandini,E., Sumners,D.W., Tesi,M.C. and Whittington,S.G. (1997) The writhe of knots in the cubic lattice. J. Knot Theor., 5, 31-44.
34. Katritch,V., Olson,W.K., Pieranski,P., Dubochet,J. and Stasiak,A. (1997) Properties of ideal composite knots. Nature, 388, 148-151.
35. Plunkett,P., Piatek,M., Dobay,A., Kern,J., Millett,K.C., Stasiak,A. and Rawdon,E.J. (2007) Total curvature and total torsion of knotted polymers. Macromolecules, 40, 3860-3867.
36. Sundin,O. and Varshavsky,A. (1980) Terminal stages of SV40 DNA replication proceed via multiply intertwined catenated dimers. Cell 21, 103-114.
37. Peter,B.J., Ullsperger,C., Hiasa,H., Marians,K.J. and Cozzarelli,N.R. (1998) The structure of supercoiled intermediates in DNA replication. Cell, 94, 819-827.
38. Zechiedrich,E.L. and Cozzarelli,N.R. (1995) Roles of topoisomerase IV and DNA gyrase in DNA unlinking during replication in Escherichia coli. Genes Dev., 9, 2859-2869.
39. Deibler,R.W., Mann,J.K., Sumners,D.W. and Zechiedrich,L. (2007) Hin-mediated DNA knotting and recombining promote replicon dysfunction and mutation. BMC Mol. Biol., 8, 44.
40. Bates,A.D. and Maxwell,A. (2007) Energy coupling in type II topoisomerases: Why do they hydrolyze ATP? Biochemistry, 46, 7929-7941.
41. Osheroff,N., Shelton,E.R. and Brutlag,D.L. (1983) DNA topoisomerase II from Drosophila melanogaster. Relaxation of supercoiled DNA. J. Biol. Chem., 258, 9536-9543.
42. Williams,N.L., Howells,A.J. and Maxwell,A. (2001) Locking the ATP-operated clamp of DNA gyrase: Probing the mechanism of strand passage. J. Mol. Biol., 306, 969-984.
43. Roca,J. and Wang,J.C. (1994) DNA transport by a type II DNA topoisomerase: Evidence in favor of a two-gate mechanism. Cell, 77, 609-616.
44. Harkins,T.T., Lewis,T.J. and Lindsley,J.E. (1998) Pre-steady-state analysis of ATP hydrolysis by Saccharomyces cerevisiae DNA topoisomerase II. 2. Kinetic mechanism for the sequential hydrolysis of two ATP. Biochemistry, 37, 7299-7312.
45. Baird,C.L., Harkins,T.T., Morris,S.K. and Lindsley,J.E. (1999) Topoisomerase II drives DNA transport by hydrolyzing one ATP. Proc. Natl Acad. Sci. USA, 96, 13685-13690.
46. Sugino,A., Higgins,N.P., Brown,P.O., Peebles,C.L. and Cozzarelli,N.R. (1978) Energy coupling in DNA gyrase and the mechanism of action of novobiocin. Proc. Natl Acad. Sci. USA, 75, 4838-4842.
47. Rosselli,W. and Stasiak,A. (1990) Energetics of RecA-mediated recombination reactions. Without ATP hydrolysis RecA can mediate polar strand exchange but is unable to recycle. J. Mol. Biol., 216 335-352.
48. Rolfsen,D. (1976) Knots and links. Publish or Perish Press, Berkeley, CA.
49. Adams,C.C. (1994) The Knot Book. W.H. Freeman and Company, New York.
50. Darcy,I.K. and Sumners,D.W. (1997) In Suzuki,S. (ed), Knots '96: Proceedings of the Fifth International Research Institute of Mathematical Society of Japan. World Scientific, Singapore, pp. 267-278.
51. Darcy,I.K. and Sumners,D.W. (2000) Rational tangle distance on knots and links. Math. Proc. Cambridge Philos. Soc., 128, 497-510.