The ancestral role of ATP hydrolysis in type II topoisomerases: Prevention of DNA double-strand breaks

Nucleic Acids Research

Volumn 39, Issue 15, 2011, Pages 6327-6339

  Bates, Andrew D ^a   Berger, James M ^b   Maxwell, Anthony ^c  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c JOHN INNES CENTRE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; ADENYLYLIMIDODIPHOSPHATE; DNA TOPOISOMERASE (ATP HYDROLYSING); SPO11 PROTEIN; DEOXYRIBONUCLEASE; MEIOTIC RECOMBINATION PROTEIN SPO11;

CONFORMATIONAL TRANSITION; DIMERIZATION; DNA CLEAVAGE; DNA GATE; DNA PROTEIN COMPLEX; DNA RECOMBINATION; DNA SUPERCOILING; DOUBLE STRANDED DNA BREAK; ENERGY TRANSFER; HYDROLYSIS; ILLEGITIMATE RECOMBINATION; MEIOSIS; MEIOTIC RECOMBINATION; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; THERMODYNAMICS; CHEMISTRY; EVOLUTION; GENETIC RECOMBINATION; GENETICS; METABOLISM;

HARNESS;

ADENOSINE TRIPHOSPHATE; BIOLOGICAL EVOLUTION; DNA BREAKS, DOUBLE-STRANDED; DNA GYRASE; DNA TOPOISOMERASES, TYPE II; ENDODEOXYRIBONUCLEASES; HYDROLYSIS; MEIOSIS; RECOMBINATION, GENETIC;

EID: 80055065448     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr258     Document Type: Review

References (153)

1. Wang,J.C. (1998) Moving one DNA double helix through another by a type II DNA topoisomerase: the story of a simple molecular machine. Q. Rev. Biophys., 31, 107-144. (Pubitemid 28448731)
2. Bates,A.D. and Maxwell,A. (2005) DNA Topology. Oxford University Press, Oxford.
3. Schoeffler,A.J. and Berger,J.M. (2008) DNA topoisomerases: harnessing and constraining energy to govern chromosome topology. Q. Rev. Biophys., 41, 41-101.
4. Wang,J.C. (1996) DNA topoisomerases. Annu. Rev. Biochem., 65, 635-692. (Pubitemid 26250622)
5. Postow,L., Crisona,N.J., Peter,B.J., Hardy,C.D. and Cozzarelli,N.R. (2001) Topological challenges to DNA replication: conformations at the fork. Proc. Natl Acad. Sci. USA, 98, 8219-8226. (Pubitemid 32678016)
6. Wang,J.C. (2002) Cellular roles of DNA topoisomerases: a molecular perspective. Nat. Rev. Mol. Cell Biol., 3, 430-440. (Pubitemid 34685700)
7. Liu,Z., Deibler,R.W., Chan,H.S. and Zechiedrich,L. (2009) The why and how of DNA unlinking. Nucleic Acids Res., 37, 661-671.
8. Aravind,L., Leipe,D.D. and Koonin,E.V. (1998) Toprim - a conserved catalytic domain in type IA and II topoisomerases, DnaG-type primases, OLD family nucleases and RecR proteins. Nucleic Acids Res., 26, 4205-4213. (Pubitemid 28418379)
9. Bergerat,A., de Massy,B., Gadelle,D., Varoutas,P.C., Nicolas,A. and Forterre,P. (1997) An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature, 386, 414-417. (Pubitemid 27154484)
10. Corbett,K.D. and Berger,J.M. (2003) Structure of the topoisomerase VI-B subunit: implications for type II topoisomerase mechanism and evolution. EMBO J., 22, 151-163. (Pubitemid 36091278)
11. Nichols,M.D., DeAngelis,K., Keck,J.L. and Berger,J.M. (1999) Structure and function of an archaeal topoisomerase VI subunit with homology to the meiotic recombination factor Spo 11. Embo J., 18, 6177-6188. (Pubitemid 29515692)
12. Gadelle,D., Filee,J., Buhler,C. and Forterre,P. (2003) Phylogenomics of type II DNA topoisomerases. Bioessays, 25, 232-242. (Pubitemid 36314110)
13. Forterre,P. and Gadelle,D. (2009) Phylogenomics of DNA topoisomerases: their origin and putative roles in the emergence of modern organisms. Nucleic Acids Res., 37, 679-692.
14. Gellert,M., Mizuuchi,K., O'Dea,M.H. and Nash,H.A. (1976) DNA gyrase: an enzyme that introduces superhelical turns into DNA. Proc. Natl Acad. Sci. USA, 73, 3872-3876.
15. Bates,A.D., O'Dea,M.H. and Gellert,M. (1996) Energy coupling in Escherichia coli DNA gyrase: the relationship between nucleotide binding, strand passage, and DNA supercoiling. (Pubitemid 26055276)
16. Dong,K.C. and Berger,J.M. (2007) Structural basis for gate-DNA recognition and bending by type IIA topoisomerases. Nature, 450, 1201-1205.
17. Laponogov, I., Sohi, M.K., Veselkov, D.A., Pan, X.-S., Sawhney, R., Thompson, A.W., McAuley, K.E., Fisher, L.M. and Sanderson, M.R. (2009) Structural insight into the quinolone-DNA cleavage complex of type IIA topoisomerases 16, 667-669.
18. 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. (Pubitemid 32220796)
19. Sander, M. and Hsieh, T. (1983) Double strand DNA cleavage by type II DNA topoisomerase from Drosophila melanogaster. J. Biol. Chem., 258, 8421-8428.
20. Roca, J., Berger, J.M., Harrison, S.C. and Wang, J.C. (1996) DNA transport by a type II topoisomerase: direct evidence for a two-gate mechanism. Proc. Natl Acad. Sci. USA, 93, 4057-4062. (Pubitemid 26144245)
21. Williams, N.L. and Maxwell, A. (1999) Probing the two-gate mechanism of DNA gyrase using cysteine cross-linking.
22. Baird, C.L., Gordon, M.S., Andrenyak, D.M., Marecek, J.F. and Lindsley, J.E. (2001) The ATPase reaction cycle of yeast DNA topoisomerase II. Slow rates of ATP resynthesis and P(i) release. J. Biol. Chem., 276, 27893-27898.
23. 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.
24. Brown, P.O. and Cozzarelli, N.R. (1979) A sign inversion mechanism for enzymatic supercoiling of DNA. Science, 206, 1081-1083. (Pubitemid 10208881)
25. Mizuuchi, K., Fisher, M., O'Dea, M. and Gellert, M. (1980) DNA gyrase action involves the introduction of transient double-strand breaks into DNA. Proc. Natl Acad. Sci. USA, 77, 1847-1851. (Pubitemid 10089564)
26. Wang, J.C., Gumport, R.I., Javaherian, K., Kirkegaard, K., Klevan, L., Kotewicz, M.L. and Tse, Y.-C. (1980) In Alberts, B. and Fox, C.F. (eds), Mechanistic Studies of DNA Replication and Genetic Recombination. Academic Press, NY, pp. 769-784.
27. Berger, J.M., Gamblin, S.J., Harrison, S.C. and Wang, J.C. (1996) Structure and mechanism of DNA topoisomerase II. Nature, 379, 225-232. (Pubitemid 26025206)
28. Morais Cabral, J.H., Jackson, A.P., Smith, C.V., Shikotra, N., Maxwell, A. and Liddington, R.C. (1997) Crystal structure of the breakage-reunion domain of DNA gyrase. Nature, 388, 903-906. (Pubitemid 27377066)
29. 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.
30. Brown, P.O. and Cozzarelli, N.R. (1981) Catenation and knotting of duplex DNA by type I topoisomerases: A mechanistic parallel with type II topoisomerases. Proc. Natl Acad. Sci. USA, 78, 843-847. (Pubitemid 11159522)
31. Tse, Y.-C. and Wang, J.C. (1980) E. coli and M. luteus DNA topoisomerase I can catalyse catenation or decatenation of double-stranded DNA rings. Cell, 22, 269-276. (Pubitemid 11226448)
32. Lindsley, J.E. (1996) Intradimerically tethered DNA topoisomerase II is catalytically active in DNA transport. Proc. Natl Acad. Sci. USA, 93, 2975-2980. (Pubitemid 26114348)
33. Roca, J., Berger, J.M., Harrison, S.C. and Wang, J.C. (1996) DNA transport by a type II topoisomerase: direct evidence for a two-gate mechanism. Proc. Natl Acad. Sci. USA, 93, 4057-4062. (Pubitemid 26144245)
34. Roca, J. and Wang, J.C. (1992) 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, 71, 833-840.
35. Buhler, C., Lebbink, J.H., Bocs, C., Ladenstein, R. and Forterre, P. (2001) DNA topoisomerase VI generates ATP-dependent double-strand breaks with two-nucleotide overhangs. J. Biol. Chem., 276, 37215-37222.
36. Corbett, K.D., Benedetti, P. and Berger, J.M. (2007) Holoenzyme assembly and ATP-mediated conformational dynamics of topoisomerase VI 14, 611-619. (Pubitemid 47037071)
37. Fisher, L.M., Mizuuchi, K., O'Dea, M.H., Ohmori, H. and Gellert, M. (1981) Site-specific interaction of DNA gyrase with DNA. Proc. Natl Acad. Sci. USA, 78, 4165-4169.
38. Kirkegaard, K. and Wang, J.C. (1981) Mapping the topography of DNA wrapped around gyrase by nucleolytic and chemical probing of complexes of unique DNA sequences. Cell, 23, 721-729. (Pubitemid 11156983)
39. Liu, L. and Wang, J. (1978) Micrococcus luteus DNA gyrase: Active components and a model for its supercoiling of DNA. Proc. Natl Acad. Sci. USA, 75, 2098-2102.
40. Liu, L.F. and Wang, J.C. (1978) DNA-DNA gyrase complex: the wrapping of the DNA duplex outside the enzyme. Cell, 15, 979-984.
41. Morrison, A. and Cozzarelli, N.R. (1981) Contacts between DNA gyrase and its binding site on DNA: features of symmetry and asymmetry revealed by protection from nucleases. Proc. Natl Acad. Sci. USA, 78, 1416-1420.
42. Orphanides, G. and Maxwell, A. (1994) Evidence for a conformational change in the DNA gyrase-DNA complex from hydroxyl radical footprinting. Nucleic Acids Res., 22, 1567-1575. (Pubitemid 24155808)
43. Rau, D.C., Gellert, M., Thoma, F. and Maxwell, A. (1987) Structure of the DNA gyrase-DNA complex as revealed by transient electric dichroism, J. Mol. Biol., 193, 555-569. (Pubitemid 17025289)
44. Heddle, J.G., Mitelheiser, S., Maxwell, A. and Thomson, N.H. (2004) Nucleotide binding to DNA gyrase causes loss of DNA wrap, J. Mol. Biol., 337, 597-610. (Pubitemid 38326880)
45. Kampranis, S.C. and Maxwell, A. (1996) Conversion of DNA gyrase into a conventional type II topoisomerase. Proc. Natl Acad. Sci. USA, 93, 14416-14421. (Pubitemid 26418981)
46. Corbett, K.D., Schoeffler, A.J., Thomsen, N.D. and Berger, J.M. (2005) The structural basis for substrate specificity in DNA topoisomerase IV, J. Mol. Biol., 351, 545-561. (Pubitemid 41021940)
47. Zechiedrich, E.L., Khodursky, A.B. and Cozzarelli, N.R. (1997) Topoisomerase IV, not gyrase, decatenates products of site-specific recombination in Escherichia coli. Genes Dev., 11, 2580-2592. (Pubitemid 27438838)
48. Deweese, J.E. and Osheroff, N. (2009) The DNA cleavage reaction of topoisomerase II: wolf in sheep's clothing. Nucleic Acids Res., 37, 738-748.
49. Tse-Dinh, Y.C. (2007) Exploring DNA topoisomerases as targets of novel therapeutic agents in the treatment of infectious diseases. Infect. Disord. Drug Targets, 7, 3-9.
50. Buhler, C., Gadelle, D., Forterre, P., Wang, J.C. and Bergerat, A. (1998) Reconstitution of DNA topoisomerase VI of the thermophilic archaeon Sulfolobus shibatae from subunits separately overexpressed in Escherichia coli. Nucleic Acids Res., 26, 5157-5162. (Pubitemid 28517573)
51. Kampranis, S.C., Bates, A.D. and Maxwell, A. (1999) A model for the mechanism of strand passage by DNA gyrase. Proc. Natl Acad. Sci. USA, 96, 8414-8419. (Pubitemid 29354805)
52. Morrison, A., Higgins, N.P. and Cozzarelli, N.R. (1980) Interaction between DNA gyrase and its cleavage site on DNA. J. Biol. Chem., 255, 2211-2219.
53. Sander, M. and Hsieh, T. (1983) Double strand DNA cleavage by type II DNA topoisomerase from Drosophila melanogaster. J. Biol. Chem., 258, 8421-8428.
54. Fortune, J.M., Dickey, J.S., Lavrukhin, O.V., Van Etten, J.L., Lloyd, R.S. and Osheroff, N. (2002) Site-specific DNA cleavage by Chlorella virus topoisomerase II. Biochemistry, 41, 11761-11769
55. Fortune, J.M., Lavrukhin, O.V., Gurnon, J.R., Van Etten, J.L., Lloyd, R.S. and Osheroff, N. (2001) Topoisomerase II from Chlorella virus PBCV-1 has an exceptionally high DNA cleavage activity. J. Biol. Chem., 276, 24401-24408.
56. Dickey, J.S., Choi, T.J., Van Etten, J.L. and Osheroff, N. (2005) Chlorella virus Marburg topoisomerase II: high DNA cleavage activity as a characteristic of Chlorella virus type II enzymes. Biochemistry, 44, 3899-3908. (Pubitemid 40358041)
57. Noble, C.G. and Maxwell, A. (2002) The role of GyrB in the DNA cleavage-religation reaction of DNA gyrase: a proposed two-metal-ion mechanism, J. Mol. Biol., 318, 361-371. (Pubitemid 34734831)
58. Wang, J.C. (1998) Moving one DNA double helix through another by a type II DNA topoisomerase: the story of a simple molecular machine.Quart. Rev. Biophys., 31, 107-144. (Pubitemid 28448731)
59. Smiley, R.D., Collins, T.R., Hammes, G.G. and Hsieh, T.S. (2007) Single-molecule measurements of the opening and closing of the DNA gate by eukaryotic topoisomerase II. Proc. Natl Acad. Sci. USA, 104, 4840-4845. (Pubitemid 47186138)
60. Gubaev, A., Hilbert, M. and Klostermeier, D. (2009) The DNA-gate of Bacillus subtilis gyrase is predominantly in the closed conformation during the DNA supercoiling reaction. Proc. Natl Acad. Sci. USA, 106, 13278-13283.
61. Corbett, A.H., Zechiedrich, E.L. and Osheroff, N. (1992) A role for the passage helix in the DNA cleavage reaction of eukaryotic topoisomerase II. J. Biol. Chem., 267, 683-686.
62. Fu, G., Wu, J., Liu, W., Zhu, D., Hu, Y., Deng, J., Zhang, X.E., Bi, L. and Wang, D.C. (2009) Crystal structure of DNA gyrase B' domain sheds lights on the mechanism for T-segment navigation. Nucleic Acids Res., 37, 5908-5916.
63. Roca, J. (2004) The path of the DNA along the dimer interface of topoisomerase II. J. Biol. Chem., 279, 25783-25788. (Pubitemid 38756842)
64. Osheroff, N., Shelton, E.R. and Brutlag, D.L. (1983) DNA topoisomerase II from Drosophila melangaster. Relaxation of supercoiled DNA. J. Biol. Chem., 258, 9536-9543.
65. 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. (Pubitemid 9048630)
66. Classen, S., Olland, S. and Berger, J.M. (2003) Structure of the topoisomerase II ATPase region and its mechanism of inhibition by the chemotherapeutic agent ICRF-187. Proc. Natl Acad. Sci. USA, 100, 10629-10634. (Pubitemid 37140080)
67. Wei, H., Ruthenburg, A.J., Bechis, S.K. and Verdine, G.L. (2005) Nucleotide-dependent domain movement in the ATPase domain of a human type IIA DNA topoisomerase. J. Biol. Chem., 280, 37041-37047. (Pubitemid 41587788)
68. Sugino, A. and Cozzarelli, N.R. (1980) The intrinsic ATPase of DNA gyrase. J. Biol. Chem., 255, 6299-6306.
69. Tingey, A.P. and Maxwell, A. (1996) Probing the role of the ATP-operated clamp in the strand-passage reaction of DNA gyrase. Nucleic Acids Res., 24, 4868-4873. (Pubitemid 27007889)
70. 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. (Pubitemid 33029999)
71. Lamour, V., Hoermann, L., Jeltsch, J.M., Oudet, P. and Moras, D. (2002) An open conformation of the Thermus thermophilus gyrase B ATP-binding domain. J. Biol. Chem., 277, 18947-18953. (Pubitemid 34952456)
72. Corbett, K.D. and Berger, J.M. (2005) Structural dissection of ATP turnover in the prototypical GHL ATPase TopoVI. Structure, 13, 873-882. (Pubitemid 40804390)
73. 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. (Pubitemid 27373915)
74. Deibler, R.W., Mann, J.K., Sumners de, W.L. and Zechiedrich, L. (2007) Hin-mediated DNA knotting and recombining promote replicon dysfunction and mutation. BMC Mol. Biol., 8, 44.
75. Portugal, J. and Rodr?íguez-Campos, A. (1996) T7 RNA polymerase cannot transcribe through a highly knotted DNA template. Nucleic Acids Res., 24, 4890-4894. (Pubitemid 27007892)
76. Bates, A.D. and Maxwell, A. (2007) Energy coupling in type II topoisomerases: why do they hydrolyze ATP? Biochemistry, 46, 7929-7941. (Pubitemid 47053858)
77. Buck, G.R. and Zechiedrich, E.L. (2004) DNA disentangling by type-2 topoisomerases, J. Mol. Biol., 340, 933-939. (Pubitemid 38968692)
78. 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. (Pubitemid 44092778)
79. Stuchinskaya, T., Mitchenall, L.A., Schoeffler, A.J., Corbett, K.D., Berger, J.M., Bates, A.D. and Maxwell, A. (2009) How do type II topoisomerases use ATP hydrolysis to simplify DNA topology beyond equilibrium? Investigating the relaxation reaction of nonsupercoiling type II topoisomerases, J. Mol. Biol., 385, 1397-1408.
80. Bates, A.D. and Maxwell, A. (2010) The role of ATP in the reactions of type II DNA topoisomerases. Biochem. Soc. Trans., 38, 438-442.
81. Holm, C. (1994) Coming undone: how to untangle a chromosome. Cell, 77, 955-957. (Pubitemid 24208853)
82. Holmes, V.F. and Cozzarelli, N.R. (2000) Closing the ring: links between SMC proteins and chromosome partitioning, condensation, and supercoiling. Proc. Natl Acad. Sci. USA, 97, 1322-1324. (Pubitemid 30118433)
83. Martinez-Robles, M.L., Witz, G., Hernandez, P., Schvartzman, J.B., Stasiak, A. and Krimer, D.B. (2009) Interplay of DNA supercoiling and catenation during the segregation of sister duplexes. Nucleic Acids Res., 37, 5126-5137.
84. Vologodskii, A. (2010) DNA supercoiling helps to unlink sister duplexes after replication. Bioessays, 32, 9-12.
85. Burnier, Y., Dorier, J. and Stasiak, A. (2008) DNA supercoiling inhibits DNA knotting. Nucleic Acids Res., 36, 4956-4963.
86. Baxter, J., Sen, N., Martinez, V.L., De Carandini, M.E., Schvartzman, J.B., Diffley, J.F. and Aragon, L. (2011) Positive supercoiling of mitotic DNA drives decatenation by topoisomerase II in eukaryotes. Science, 331, 1328-1332.
87. Delagoutte, E. and von Hippel, P.H. (2003) Helicase mechanisms and the coupling of helicases within macromolecular machines. Part II: Integration of helicases into cellular processes. Q. Rev. Biophys., 36, 1-69. (Pubitemid 36313959)
88. Muller, U.F. (2006) Re-creating an RNA world. Cell Mol. Life Sci., 63, 1278-1293. (Pubitemid 43939013)
89. Gellert, M. (1981) DNA Gyrase and other type II topoismerases. The Enzymes, XIV, 345-366.
90. Wang, J.C. (1994) DNA topoisomerases as targets of therapeutics: an overview. Adv. Pharmacol., 29A, 1-19.
91. Wang, J.C., Caron, P.R. and Kim, R.A. (1990) The role of DNA topoisomerases in recombination and genome stability: a double-edged sword? Cell, 62, 403-406.
92. Roca, J. (2009) Topoisomerase II: a fitted mechanism for the chromatin landscape. Nucleic Acids Res., 37, 721-730.
93. Kouzine, F., Sanford, S., Elisha-Feil, Z. and Levens, D. (2008) The functional response of upstream DNA to dynamic supercoiling in vivo Nat. Struct. Mol. Biol., 15, 146-154. (Pubitemid 351207509)
94. Williams, N.L. and Maxwell, A. (1999) Locking the DNA gate of DNA gyrase: investigating the effects on DNA cleavage and ATP hydrolysis. Biochemistry, 38, 14157-14164.
95. Wilstermann, A.M. and Osheroff, N. (2003) Stabilization of eukaryotic topoisomerase II-DNA cleavage complexes. Curr. Top. Med. Chem., 3, 321-338.
96. Krissinel, E. and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state, J. Mol. Biol. 372, 774-797. (Pubitemid 47321791)
97. 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. (Pubitemid 32220796)
98. Sikorav, J.L. and Jannink, G. (1994) Kinetics of chromosome condensation in the presence of topoisomerases: a phantom chain model. Biophys. J., 66, 827-837. (Pubitemid 24083003)
99. Gellert, M., Mizuuchi, K., O'Dea, M.H., Itoh, T. and Tomizawa, J. (1977) Nalidixic acid resistance: a second genetic character involved in DNA gyrase activity. Proc. Natl Acad. Sci. USA, 74, 4772-4776. (Pubitemid 8227005)
100. Sugino, A., Peebles, C.L., Kruezer, K.N. and Cozzarelli, N.R. (1977) Mechanism of action of nalidixic acid: purification of Escherichia coli nalA gene product and its relationship to DNA gyrase and a novel nicking-closing enzyme. Proc. Natl Acad. Sci. USA, 74, 4767-4771. (Pubitemid 8227004)
101. Wigley, D.B., Davies, G.J., Dodson, E.J., Maxwell, A. and Dodson, G. (1991) Crystal structure of an N-terminal fragment of the DNA gyrase B protein. Nature, 351, 624-629. (Pubitemid 21896650)
102. Dutta, R. and Inouye, M. (2000) GHKL, an emergent ATPase/ kinase superfamily. Trends Biochem. Sci., 25, 24-28. (Pubitemid 30060426)
103. Forterre, P., Gribaldo, S., Gadelle, D. and Serre, M.C. (2007) Origin and evolution of DNA topoisomerases. Biochimie, 89, 427-446. (Pubitemid 46656307)
104. Nollmann, M., Stone, M.D., Bryant, Z., Gore, J., Crisona, N.J., Hong, S.C., Mitelheiser, S., Maxwell, A., Bustamante, C. and Cozzarelli, N.R. (2007) Multiple modes of Escherichia coli DNA gyrase activity revealed by force and torque. Nat. Struct. Mol. Biol., 14, 264-271. (Pubitemid 46608338)
105. Wang, J.C. (2002) Cellular roles of DNA topoisomerases: a molecular perspective. Nat. Rev. Mol. Cell Biol., 3, 430-440. (Pubitemid 34685700)
106. Bennett, B.D., Kimball, E.H., Gao, M., Osterhout, R., Van Dien, S.J. and Rabinowitz, J.D. (2009) Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat. Chem. Biol., 5, 593-599.
107. Liu, L.F., Liu, C.-C. and Alberts, B.M. (1980) Type II DNA topoisomerases: enzymes that can unknot a topologically knotted DNA molecule via a reversible double-strand break. Cell, 19, 697-707. (Pubitemid 10134849)
108. Bates, A.D. and Maxwell, A. (1989) DNA gyrase can supercoil DNA circles as small as 174 base pairs. EMBO J., 8, 1861-1866. (Pubitemid 19274391)
109. Cullis, P.M., Maxwell, A. and Weiner, D.P. (1992) Energy coupling in DNA gyrase: a thermodynamic limit to the extent of DNA supercoiling. Biochemistry, 31, 9642-9646.
110. Maxwell, A. and Gellert, M. (1986) Mechanistic aspects of DNA topoisomerases. Adv. Prot. Chem., 38, 69-107.
111. Westerhoff, H.V., O'Dea, M.H., Maxwell, A. and Gellert, M. (1988) DNA supercoiling by DNA gyrase. A static head analysis. Cell Biophys., 12, 157-181.
112. Ikeda, H., Shiraishi, K. and Ogata, Y. (2004) Illegitimate recombination mediated by double-strand break and end-joining in Escherichia coli. Adv. Biophys., 38, 3-20. (Pubitemid 39186709)
113. Ikeda, H., Moriya, K. and Matsumoto, T. (1981) In vitro study of illegitimate recombination: Involvement of DNA gyrase. Cold Spring Harbor Symp. Quant. Biol., 45, 399-408. (Pubitemid 11026017)
114. Ikeda, H., Aoki, K. and Naito, A. (1982) Illegitimate recombination mediated in vitro by DNA gyrase of Escherichia coli: structure of recombinant DNA molecules. Proc. Natl Acad. Sci. USA, 7, 3724-3728.
115. Ikeda, H. (1994) DNA topoisomerase-mediated illegitimate recombination Adv. Pharmacol., 29A, 147-165.
116. Ashizawa, Y., Yokochi, T., Ogata, Y., Shobuike, Y., Kato, J. and Ikeda, H. (1999) Mechanism of DNA gyrase-mediated illegitimate recombination: characterization of Escherichia coli gyrA mutations that confer hyper-recombination phenotype J. Mol. Biol., 289, 447-458. (Pubitemid 29295116)
117. Chiba, M., Shimizu, H., Fujimoto, A., Nashimoto, H. and Ikeda, H. (1989) Common sites for recombination and cleavage mediated by bacteriophage T4 DNA topoisomerase in vitro. J. Biol. Chem., 264, 12785-12790. (Pubitemid 19194845)
118. Ikeda, H. (1986) Illegitimate recombination mediated by T4 DNA topoisomerase in vitro. Mol. Gen. Genet., 1986, 518-520.
119. Ikeda, H. (1986) Bacteriophage T4 DNA topoisomerase mediates illegitimate recombination in vitro. Proc. Natl Acad. Sci. USA, 83, 922-926.
120. Bae, Y.-S., Kawsaki, I., Ikeda, H. and Liu, L.F. (1988) Illegitimate recombination mediated by calf thymus DNA topoisomerase II in vitro. Proc. Natl Acad. Sci. USA., 85, 2076-2080. (Pubitemid 24315831)
121. Asami, Y., Jia, D.W., Tatebayashi, K., Yamagata, K., Tanokura, M. and Ikeda, H. (2002) Effect of the DNA topoisomerase II inhibitor VP-16 on illegitimate recombination in yeast chromosomes. Gene, 291, 251-257. (Pubitemid 34722395)
122. Keeney, S., Giroux, C.N. and Kleckner, N. (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell, 88, 375-384. (Pubitemid 27131379)
123. Keeney, S. (2001) Mechanism and control of meiotic recombination initiation. Curr. Top. Dev. Biol., 52, 1-53. (Pubitemid 33804625)
124. Neale, M.J. and Keeney, S. (2006) Clarifying the mechanics of DNA strand exchange in meiotic recombination. Nature, 442, 153-158. (Pubitemid 44086556)
125. Keeney, S. and Neale, M.J. (2006) Initiation of meiotic recombination by formation of DNA double-strand breaks: mechanism and regulation. Biochem. Soc. Trans., 34, 523-525. (Pubitemid 44230753)
126. Hirano, T. (2006) At the heart of the chromosome: SMC proteins in action. Nat. Rev. Mol. Cell Biol., 7, 311-322.
127. Nasmyth, K. and Haering, C.H. (2005) The structure and function of SMC and kleisin complexes. Annu. Rev. Biochem., 74, 595-648. (Pubitemid 40995519)
128. Lim, J.H. and Oh, B.H. (2009) Structural and functional similarities between two bacterial chromosome compacting machineries. Biochem. Biophys. Res. Commun., 386, 415-419.
129. Yamazoe, M., Onogi, T., Sunako, Y., Niki, H., Yamanaka, K., Ichimura, T. and Hiraga, S. (1999) Complex formation of MukB, MukE and MukF proteins involved in chromosome partitioning in Escherichia coli. EMBO J., 18, 5873-5884. (Pubitemid 29515664)
130. Cobbe, N. and Heck, M.M. (2004) The evolution of SMC proteins: phylogenetic analysis and structural implications. Mol. Biol. Evol., 21, 332-347. (Pubitemid 38314622)
131. Woo, J.S., Lim, J.H., Shin, H.C., Suh, M.K., Ku, B., Lee, K.H., Joo, K., Robinson, H., Lee, J., Park, S.Y. et al. (2009) Structural studies of a bacterial condensin complex reveal ATP-dependent disruption of intersubunit interactions. Cell, 136, 85-96.
132. Fennell-Fezzie, R., Gradia, S.D., Akey, D. and Berger, J.M. (2005) The MukF subunit of Escherichia coli condensin: architecture and functional relationship to kleisins. Embo J., 24, 1921-1930. (Pubitemid 40896164)
133. Hopfner, K.P., Karcher, A., Shin, D.S., Craig, L., Arthur, L.M., Carney, J.P. and Tainer, J.A. (2000) Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell, 101, 789-800.
134. Thomsen, N.D. and Berger, J.M. (2008) Structural frameworks for considering microbial protein- and nucleic acid-dependent motor ATPases. Mol. Microbiol., 69, 1071-1090.
135. Haering, C.H., Schoffnegger, D., Nishino, T., Helmhart, W., Nasmyth, K. and Lowe, J. (2004) Structure and stability of cohesin's Smc1-kleisin interaction. Mol. Cell, 15, 951-964. (Pubitemid 39277991)
136. She, W., Wang, Q., Mordukhova, E.A. and Rybenkov, V.V. (2007) MukEF Is required for stable association of MukB with the chromosome. J. Bacteriol., 189, 7062-7068. (Pubitemid 47525451)
137. Gruber, S., Arumugam, P., Katou, Y., Kuglitsch, D., Helmhart, W., Shirahige, K. and Nasmyth, K. (2006) Evidence that loading of cohesin onto chromosomes involves opening of its SMC hinge. Cell, 127, 523-537. (Pubitemid 44647422)
138. Moreno-Herrero, F., de Jager, M., Dekker, N.H., Kanaar, R., Wyman, C. and Dekker, C. (2005) Mesoscale conformational changes in the DNA-repair complex Rad50/Mre11/Nbs1 upon binding DNA. Nature, 437, 440-443. (Pubitemid 41613509)
139. Kunkel, T.A. and Erie, D.A. (2005) DNA mismatch repair. Annu. Rev. Biochem., 74, 681-710. (Pubitemid 40995521)
140. Lamers, M.H., Perrakis, A., Enzlin, J.H., Winterwerp, H.H., de Wind, N. and Sixma, T.K. (2000) The crystal structure of DNA mismatch repair protein MutS binding to a G x T mismatch. Nature, 407, 711-717.
141. Obmolova, G., Ban, C., Hsieh, P. and Yang, W. (2000) Crystal structures of mismatch repair protein MutS and its complex with a substrate DNA. Nature, 407, 703-710.
142. Ban, C., Junop, M. and Yang, W. (1999) Transformation of MutL by ATP binding and hydrolysis: a switch in DNA mismatch repair. Cell, 97, 85-97. (Pubitemid 29165892)
143. Ban, C. and Yang, W. (1998) Crystal structure and ATPase activity of MutL: implications for DNA repair and mutagenesis. Cell, 95, 541-552. (Pubitemid 28533310)
144. Kadyrov, F.A., Holmes, S.F., Arana, M.E., Lukianova, O.A., O'Donnell, M., Kunkel, T.A. and Modrich, P. (2007) Saccharomyces cerevisiae MutLalpha is a mismatch repair endonuclease. J. Biol. Chem., 282, 37181-37190.
145. Kadyrov, F.A., Dzantiev, L., Constantin, N. and Modrich, P. (2006) Endonucleolytic function of MutLalpha in human mismatch repair. Cell, 126, 297-308. (Pubitemid 44092957)
146. Bose, D., Joly, N., Pape, T., Rappas, M., Schumacher, J., Buck, M. and Zhang, X. (2008) Dissecting the ATP hydrolysis pathway of bacterial enhancer-binding proteins. Biochem. Soc. Trans., 36, 83-88. (Pubitemid 351269627)
147. Erzberger, J.P. and Berger, J.M. (2006) Evolutionary relationships and structural mechanisms of AAA+proteins. Annu. Rev. Biophys. Biomol. Struct., 35, 93-114. (Pubitemid 43877371)
148. Schumacher, J., Joly, N., Rappas, M., Zhang, X. and Buck, M. (2006) Structures and organisation of AAA+enhancer binding proteins in transcriptional activation. J. Struct. Biol., 156, 190-199. (Pubitemid 44486050)
149. Chen, B., Sysoeva, T.A., Chowdhury, S. and Nixon, B.T. (2008) Regulation and action of the bacterial enhancer-binding protein AAA+domains. Biochem. Soc. Trans., 36, 89-93. (Pubitemid 351269628)
150. Bramhill, D. and Kornberg, A. (1988) A model for initiation at origins of DNA replication. Cell, 54, 915-918.
151. Erzberger, J.P., Mott, M.L. and Berger, J.M. (2006) Structural basis for ATP-dependent DnaA assembly and replication-origin remodeling 13, 676-683. (Pubitemid 44175159)
152. Margulies, C. and Kaguni, J.M. (1996) Ordered and sequential binding of DnaA protein to oriC, the chromosomal origin of Escherichia coli. J. Biol. Chem., 271, 17035-17040. (Pubitemid 26244249)
153. Leonard, A.C. and Grimwade, J.E. (2005) Building a bacterial orisome: emergence of new regulatory features for replication origin unwinding. Mol. Microbiol., 55, 978-985. (Pubitemid 40299170)