Binding of two DNA molecules by type II topoisomerases for decatenation

Nucleic Acids Research

Volumn 40, Issue 21, 2012, Pages 10904-10915

  Kumar, Rupesh ^a   Riley, Jane E ^b   Parry, Damian ^b   Bates, Andrew D ^b   Nagaraja, Valakunja ^a,c  

^a INDIAN INSTITUTE OF SCIENCE   (India)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c JAWAHARLAL NEHRU CENTRE FOR ADVANCED SCIENTIFIC RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; ARGININE; BACTERIAL DNA; DNA TOPOISOMERASE (ATP HYDROLYSING); DNA TOPOISOMERASE (ATP HYDROLYSING) B; PROTEIN PARC; PROTEIN PARE;

AMINO ACID SUBSTITUTION; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING ASSAY; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DECANTENATION; ENZYME MODIFICATION; ENZYME STABILITY; ESCHERICHIA COLI; MYCOBACTERIUM SMEGMATIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN FUNCTION;

ADENOSINE TRIPHOSPHATASES; ARGININE; DNA; DNA GYRASE; DNA TOPOISOMERASE IV; DNA, CATENATED; ESCHERICHIA COLI; MYCOBACTERIUM SMEGMATIS; PROTEIN BINDING;

CORYNEBACTERINEAE; ESCHERICHIA COLI;

EID: 84870589738     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks843     Document Type: Article

References (63)

1. Akrigg, A. and Cook, P.R. (1980) DNA gyrase stimulates transcription. Nucleic Acids Res., 8, 845-854.
2. De Wyngaert, M. and Hinkle, D.C. (1979) Involvement of DNA gyrase in replication and transcription of bacteriophage T7 DNA. J. Virol., 29, 529-535. (Pubitemid 9098423)
3. Filutowicz, M. (1980) Requirement of DNA gyrase for the initiation of chromosome replication in Escherichia coli K-12. Mol. Gen. Genet., 177, 301-309.
4. Masse, E. and Drolet, M. (1999) Relaxation of transcription-induced negative supercoiling is an essential function of Escherichia coli DNA topoisomerase I. J. Biol. Chem., 274, 16654-16658.
5. 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.
6. Wang, J.C. (1996) DNA topoisomerases. Annu. Rev. Biochem., 65, 635-692. (Pubitemid 26250622)
7. Corbett, K.D. and Berger, J.M. (2004) Structure, molecular mechanisms, and evolutionary relationships in DNA topoisomerases. Annu. Rev. Biophys. Biomol. Struct., 33, 95-118. (Pubitemid 38829953)
8. Hande, K.R. (1998) Clinical applications of anticancer drugs targeted to topoisomerase II. Biochim. Biophys. Acta, 1400, 173-184. (Pubitemid 28475102)
9. Nitiss, J.L. (2002) DNA topoisomerases in cancer chemotherapy: using enzymes to generate selective DNA damage. Curr. Opin. Investig. Drugs, 3, 1512-1516.
10. Collin, F., Karkare, S. and Maxwell, A. (2011) Exploiting bacterial DNA gyrase as a drug target: current state and perspectives. Appl. Microbiol. Biotechnol., 92, 479-497.
11. Maxwell, A. (1999) DNA gyrase as a drug target. Biochem. Soc. Trans., 27, 48-53. (Pubitemid 29086006)
12. 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)
13. 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)
14. 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)
15. 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.
16. Liu, L.F. and Wang, J.C. (1987) Supercoiling of the DNA template during transcription. Proc. Natl Acad. Sci. USA, 84, 7024-7027.
17. Adams, D.E., Shekhtman, E.M., Zechiedrich, E.L., Schmid, M.B. and Cozzarelli, N.R. (1992) The role of topoisomerase IV in partitioning bacterial replicons and the structure of catenated intermediates in DNA replication. Cell, 71, 277-288.
18. Peng, H. and Marians, K.J. (1993) Escherichia coli topoisomerase IV. Purification, characterization, subunit structure, and subunit interactions. J. Biol. Chem., 268, 24481-24490. (Pubitemid 23335445)
19. Kato, J., Suzuki, H. and Ikeda, H. (1992) Purification and characterization of DNA topoisomerase IV in Escherichia coli. J. Biol. Chem., 267, 25676-25684. (Pubitemid 23013960)
20. Deibler, R.W., Rahmati, S. and Zechiedrich, E.L. (2001) Topoisomerase IV, alone, unknots DNA in E coli. Genes Dev., 15, 748-761. (Pubitemid 32244903)
21. Rodriguez-Campos, A. (1996) DNA knotting abolishes in vitro chromatin assembly. J. Biol. Chem., 271, 14150-14155. (Pubitemid 26190311)
22. Ullsperger, C. and Cozzarelli, N.R. (1996) Contrasting enzymatic activities of topoisomerase IV and DNA gyrase from Escherichia coli. J. Biol. Chem., 271, 31549-31555. (Pubitemid 26408614)
23. Champoux, J.J. (2001) DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem., 70, 369-413. (Pubitemid 32662215)
24. 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)
25. Corbett, K.D., Shultzaberger, R.K. and Berger, J.M. (2004) The C-terminal domain of DNA gyrase A adopts a DNA-bending beta-pinwheel fold. Proc. Natl Acad. Sci. USA, 101, 7293-7298. (Pubitemid 38638026)
26. Dong, K.C. and Berger, J.M. (2007) Structural basis for gate-DNA recognition and bending by type IIA topoisomerases. Nature, 450, 1201-1205.
27. Hsieh, T.J., Farh, L., Huang, W.M. and Chan, N.L. (2004) Structure of the topoisomerase IV C-terminal domain: a broken beta-propeller implies a role as geometry facilitator in catalysis. J. Biol. Chem., 279, 55587-55593. (Pubitemid 40066562)
28. Ruthenburg, A.J., Graybosch, D.M., Huetsch, J.C. and Verdine, G.L. (2005) A superhelical spiral in the Escherichia coli DNA gyrase A C-terminal domain imparts unidirectional supercoiling bias. J. Biol. Chem., 280, 26177-26184. (Pubitemid 41022213)
29. 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.
30. 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.
31. 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)
32. Bellon, S., Parsons, J.D., Wei, Y., Hayakawa, K., Swenson, L.L., Charifson, P.S., Lippke, J.A., Aldape, R. and Gross, C.H. (2004) Crystal structures of Escherichia coli topoisomerase IV ParE subunit (24 and 43 kilodaltons): a single residue dictates differences in novobiocin potency against topoisomerase IV and DNA gyrase. Antimicrob. Agents Chemother., 48, 1856-1864. (Pubitemid 38544398)
33. Brino, L., Urzhumtsev, A., Mousli, M., Bronner, C., Mitschler, A., Oudet, P. and Moras, D. (2000) Dimerization of Escherichia coli DNA-gyrase B provides a structural mechanism for activating the ATPase catalytic center. J. Biol. Chem., 275, 9468-9475. (Pubitemid 30185175)
34. 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)
35. 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)
36. Jain, P. and Nagaraja, V. (2005) An atypical type II topoisomerase from Mycobacterium smegmatis with positive supercoiling activity. Mol. Microbiol., 58, 1392-1405. (Pubitemid 41705417)
37. Gadelle, D., Filee, J., Buhler, C. and Forterre, P. (2003) Phylogenomics of type II DNA topoisomerases. Bioessays, 25, 232-242. (Pubitemid 36314110)
38. 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.
39. Manjunatha, U.H., Dalal, M., Chatterji, M., Radha, D.R., Visweswariah, S.S. and Nagaraja, V. (2002) Functional characterisation of mycobacterial DNA gyrase: an efficient decatenase. Nucleic Acids Res., 30, 2144-2153. (Pubitemid 34567935)
40. Aubry, A., Fisher, L.M., Jarlier, V. and Cambau, E. (2006) First functional characterization of a singly expressed bacterial type II topoisomerase: the enzyme from Mycobacterium tuberculosis. Biochem. Biophys. Res. Commun., 348, 158-165. (Pubitemid 44177674)
41. Maxwell, A. and Howells, A.J. (1999) Overexpression and purification of bacterial DNA gyrase. Methods Mol. Biol., 94, 135-144.
42. Kirsch, R.D. and Joly, E. (1998) An improved PCR-mutagenesis strategy for two-site mutagenesis or sequence swapping between related genes. Nucleic Acids Res., 26, 1848-1850. (Pubitemid 28291826)
43. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 72, 248-254.
44. Toth, J. and Biggin, M.D. (2000) The specificity of protein-DNA crosslinking by formaldehyde: in vitro and in drosophila embryos. Nucleic Acids Res., 28, e4.
45. Tamura, J.K. and Gellert, M. (1990) Characterization of the ATP binding site on Escherichia coli DNA gyrase. Affinity labeling of Lys-103 and Lys-110 of the B subunit by pyridoxal 5'-diphospho-5'-adenosine. J. Biol. Chem., 265, 21342-21349. (Pubitemid 120014159)
46. 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.
47. 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)
48. Gottler, T. and Klostermeier, D. (2007) Dissection of the nucleotide cycle of B. subtilis DNA gyrase and its modulation by DNA. J. Mol. Biol., 367, 1392-1404. (Pubitemid 46413271)
49. Maxwell, A. and Gellert, M. (1984) The DNA dependence of the ATPase activity of DNA gyrase. J. Biol. Chem., 259, 14472-14480. (Pubitemid 15222266)
50. Maxwell, A. (1997) DNA gyrase as a drug target. Trends Microbiol., 5, 102-109. (Pubitemid 27139470)
51. 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)
52. 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)
53. 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)
54. Charvin, G., Strick, T.R., Bensimon, D. and Croquette, V. (2005) Tracking topoisomerase activity at the single-molecule level. Annu. Rev. Biophys. Biomol. Struct., 34, 201-219. (Pubitemid 40847723)
55. 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)
56. Hsieh, T.J., Yen, T.J., Lin, T.S., Chang, H.T., Huang, S.Y., Hsu, C.H., Farh, L. and Chan, N.L. (2010) Twisting of the DNA-binding surface by a beta-strand-bearing proline modulates DNA gyrase activity. Nucleic Acids Res., 38, 4173-4181.
57. Campbell, S. and Maxwell, A. (2002) The ATP-operated clamp of human DNA topoisomerase IIalpha: hyperstimulation of ATPase by "piggy-back" binding. J. Mol. Biol., 320, 171-188. (Pubitemid 34722210)
58. Gardiner, L.P., Roper, D.I., Hammonds, T.R. and Maxwell, A. (1998) The N-terminal domain of human topoisomerase IIalpha is a DNA-dependent ATPase. Biochemistry, 37, 16997-17004. (Pubitemid 28566778)
59. Dar, A., Prusty, D., Mondal, N. and Dhar, S.K. (2009) A unique 45-amino-acid region in the toprim domain of Plasmodium falciparum gyrase B is essential for its activity. Eukaryot. Cell, 8, 1759-1769.
60. Zechiedrich, E.L. and Osheroff, N. (1990) Eukaryotic topoisomerases recognize nucleic acid topology by preferentially interacting with DNA crossovers. EMBO J., 9, 4555-4562. (Pubitemid 120026015)
61. Moore, C.L., Klevan, L., Wang, J.C. and Griffith, J.D. (1983) Gyrase. DNA complexes visualized as looped structures by electron microscopy. J. Biol. Chem., 258, 4612-4617.
62. Belotserkovskii, B.P., Arimondo, P.B. and Cozzarelli, N.R. (2006) Topoisomerase action on short DNA duplexes reveals requirements for gate and transfer DNA segments. J. Biol. Chem., 281, 25407-25415. (Pubitemid 44401929)
63. Espeli, O., Lee, C. and Marians, K.J. (2003) A physical and functional interaction between Escherichia coli FtsK and topoisomerase IV. J. Biol. Chem., 278, 44639-44644. (Pubitemid 37377219)