Holoenzyme assembly and ATP-mediated conformational dynamics of topoisomerase VI (original) (raw)

References

1. Champoux, J.J. DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem. 70, 369–413 (2001).
   Article CAS PubMed Google Scholar
2. Wang, J.C. Cellular roles of topoisomerases: a molecular perspective. Nat. Rev. Mol. Cell Biol. 3, 430–440 (2002).
   Article CAS PubMed Google Scholar
3. Wang, J.C. 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 (1998).
   Article CAS PubMed Google Scholar
4. Corbett, K.D. & Berger, J.M. Structure, molecular mechanisms, and evolutionary relationships in DNA topoisomerases. Annu. Rev. Biophys. Biomol. Struct. 33, 95–118 (2004).
   Article CAS PubMed Google Scholar
5. Gadelle, D., Filee, J., Buhler, C. & Forterre, P. Phylogenomics of type II DNA topoisomerases. Bioessays 25, 232–242 (2003).
   Article CAS PubMed Google Scholar
6. Bergerat, A. et al. An atypical topoisomerase II from archaea with implications for meiotic recombination. Nature 386, 414–417 (1997).
   Article CAS PubMed Google Scholar
7. Keeney, S., Giroux, C.N. & Kleckner, N. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88, 375–384 (1997).
   Article CAS PubMed Google Scholar
8. Nichols, M.D., DeAngelis, K., Keck, J.L. & Berger, J.M. Structure and function of an archaeal topoisomerase VI subunit with homology to the meiotic recombination factor Spo11. EMBO J. 18, 6177–6188 (1999).
   Article CAS PubMed PubMed Central Google Scholar
9. Aravind, L., Leipe, D.D. & Koonin, E.V. 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 (1998).
   Article CAS PubMed PubMed Central Google Scholar
10. Dutta, R. & Inouye, M. GHKL, an emergent ATPase/kinase superfamily. Trends Biochem. Sci. 25, 24–28 (2000).
    Article CAS PubMed Google Scholar
11. Wigley, D.B., Davies, G.J., Dodson, E.J., Maxwell, A. & Dodson, G. Crystal structure of an amino-terminal fragment of the DNA gyrase B protein. Nature 351, 624–629 (1991).
    Article CAS PubMed Google Scholar
12. Corbett, K.D. & Berger, J.M. Structural dissection of ATP turnover in the prototypical GHL ATPase topo VI. Structure 13, 873–882 (2005).
    Article CAS PubMed Google Scholar
13. Corbett, K.D. & Berger, J.M. Structure of the topoisomerase VI B subunit: implications for type II topoisomerase mechanism and evolution. EMBO J. 22, 151–163 (2003).
    Article CAS PubMed PubMed Central Google Scholar
14. Roca, J. & Wang, J.C. 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 (1992).
    Article CAS PubMed Google Scholar
15. Buhler, C., Lebbink, J.H.G., Bocs, C., Ladenstein, R. & Forterre, P. DNA topoisomerase VI generates ATP-dependent double-strand breaks with two-nucleotide overhangs. J. Biol. Chem. 276, 37215–37222 (2001).
    Article CAS PubMed Google Scholar
16. Baird, C.L., Harkins, T.T., Morris, S.K. & Lindsley, J.E. Topoisomerase II drives DNA transport by hydrolyzing one ATP. Proc. Natl. Acad. Sci. USA 96, 13685–13690 (1999).
    Article CAS PubMed PubMed Central Google Scholar
17. Roca, J. & Wang, J.C. DNA transport by a type II DNA topoisomerase: evidence in favor of a two-gate mechanism. Cell 77, 609–616 (1994).
    Article CAS PubMed Google Scholar
18. Berger, J.M., Gamblin, S.J., Harrison, S.C. & Wang, J.C. Structure and mechanism of DNA topoisomerase II. Nature 379, 225–232 (1996).
    Article CAS PubMed Google Scholar
19. Bork, P., Holm, L. & Sander, C. The immunoglobulin fold. Structural classification, sequence patterns and common core. J. Mol. Biol. 242, 309–320 (1994).
    CAS PubMed Google Scholar
20. Xu, G.Y. et al. Solution structure of a cellulose-binding domain from Cellulomonas fimi by nuclear magnetic resonance spectroscopy. Biochemistry 34, 6993–7009 (1995).
    Article CAS PubMed Google Scholar
21. Jenner, L., Husted, L., Thirup, S., Sottrup-Jensen, L. & Nyborg, J. Crystal structure of the receptor-binding domain of a 2-macroglobulin. Structure 6, 595–604 (1998).
    Article CAS PubMed Google Scholar
22. Reece, R.J. & Maxwell, A. The C-terminal domain of the Escherichia coli DNA gyrase A subunit is a DNA-binding protein. Nucleic Acids Res. 19, 1399–1405 (1991).
    Article CAS PubMed PubMed Central Google Scholar
23. Corbett, K.D., Schoeffler, A.J., Thomsen, N.D. & Berger, J.M. The structural basis for substrate specificity in DNA topoisomerase IV. J. Mol. Biol. 351, 545–561 (2005).
    Article CAS PubMed Google Scholar
24. Corbett, K.D., Shultzaberger, R.K. & Berger, J.M. The C-terminal domain of DNA gyrase A adopts a DNA-bending β-pinwheel fold. Proc. Natl. Acad. Sci. USA 101, 7293–7298 (2004).
    Article CAS PubMed PubMed Central Google Scholar
25. Ward, D. & Newton, A. Requirement of topoisomerase IV parC and parE genes for cell cycle progression and developmental regulation in Caulobacter crescentus. Mol. Microbiol. 26, 897–910 (1997).
    Article CAS PubMed Google Scholar
26. Crisona, N.J., Strick, T.R., Bensimon, D., Croquette, V. & Cozzarelli, N.R. Preferential relaxation of positively supercoiled DNA by E. coli topoisomerase IV in single-molecule and ensemble measurements. Genes Dev. 14, 2881–2892 (2000).
    Article CAS PubMed PubMed Central Google Scholar
27. Peng, H. & Marians, K.J. The interaction of Escherichia coli topoisomerase IV with DNA. J. Biol. Chem. 270, 25286–25290 (1995).
    Article CAS PubMed Google Scholar
28. Wang, S.C. & Shapiro, L. The topoisomerase IV ParC subunit colocalizes with the Caulobacter replisome and is required for polar localization of replication origins. Proc. Natl. Acad. Sci. USA 101, 9251–9256 (2004).
    Article CAS PubMed PubMed Central Google Scholar
29. Espeli, O., Lee, C. & Marians, K.J. A physical and functional interaction between Escherichia coli FtsK and topoisomerase IV. J. Biol. Chem. 278, 44639–44644 (2003).
    Article CAS PubMed Google Scholar
30. Svergun, D.I. & Koch, M.H.J. Small-angle scattering studies of biological macromolecules in solution. Rep. Prog. Phys. 66, 1735–1782 (2003).
    Article CAS Google Scholar
31. Svergun, D.I. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Cryst. 25, 495–503 (1992).
    Article CAS Google Scholar
32. Svergun, D.I. Restoring low resolution structure of biological macromolecules from solution scattering using simulated annealing. Biophys. J. 76, 2879–2886 (1999).
    Article CAS PubMed PubMed Central Google Scholar
33. Kozin, M.B. & Svergun, D.I. Automated matching of high- and low-resolution structural models. J. Appl. Cryst. 34, 33–41 (2001).
    Article CAS Google Scholar
34. Svergun, D.I., Barberato, C. & Koch, M.H.J. CRYSOL - a program to evaluate x-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Cryst. 28, 768–773 (1995).
    Article CAS Google Scholar
35. Konarev, P.V., Volkov, V.V., Sokolova, A.V., Koch, M.H.J. & Svergun, D.I. PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Cryst. 36, 1277–1282 (2003).
    Article CAS Google Scholar
36. Buhler, C., Gadelle, D., Forterre, P., Wang, J.C. & Bergerat, A. Reconstitution of DNA topoisomerase VI of the thermophilic archaeon Sulfolobus shibatae from subunits separately overexpressed in Escherichia coli. Nucleic Acids Res. 26, 5157–5162 (1998).
    Article CAS PubMed PubMed Central Google Scholar
37. Morais Cabral, J.H. et al. Crystal structure of the breakage-reunion domain of DNA gyrase. Nature 388, 903–906 (1997).
    Article CAS PubMed Google Scholar
38. Tingey, A.P. & Maxwell, A. Probing the role of the ATP-operated clamp in the strand-passage reaction of DNA gyrase. Nucleic Acids Res. 24, 4868–4873 (1996).
    Article CAS PubMed PubMed Central Google Scholar
39. Williams, N.L., Howells, A.J. & Maxwell, A. Locking the ATP-operated clamp of DNA gyrase: probing the mechanism of strand passage. J. Mol. Biol. 306, 969–984 (2001).
    Article CAS PubMed Google Scholar
40. Lamour, V., Hoermann, L., Jeltsch, J-M., Oudet, P. & Moras, D. An open conformation of the Thermus thermophilus gyrase B ATP-binding domain. J. Biol. Chem. 277, 18947–18953 (2002).
    Article CAS PubMed Google Scholar
41. Wei, H., Ruthenburg, A.J., Bechis, S.K. & Verdine, G.L. Nucleotide-dependent domain movement in the ATPase domain of a human type IIA DNA topoisomerase. J. Biol. Chem. 280, 37041–37047 (2005).
    Article CAS PubMed Google Scholar
42. Morrison, A. & Cozzarelli, N.R. Site-specific cleavage of DNA by E. coli DNA gyrase. Cell 17, 175–184 (1979).
    Article CAS PubMed Google Scholar
43. Sander, M. & Hsieh, T. Double strand DNA cleavage by type II DNA topoisomerase from Drosophila melanogaster. J. Biol. Chem. 258, 8421–8428 (1983).
    CAS PubMed Google Scholar
44. Roca, J. The path of the DNA along the dimer interface of topoisomerase II. J. Biol. Chem. 279, 25783–25788 (2004).
    Article CAS PubMed Google Scholar
45. Trigueros, S., Salceda, J., Bermudez, I., Fernandez, X. & Roca, J. Asymmetric removal of supercoils suggests how topoisomerase II simplifies DNA topology. J. Mol. Biol. 335, 723–731 (2004).
    Article CAS PubMed Google Scholar
46. Rybenkov, V.V., Ullsperger, C., Vologodskii, A.V. & Cozzarelli, N.R. Simplification of DNA topology below equilibrium values by type II topoisomerases. Science 277, 690–693 (1997).
    Article CAS PubMed Google Scholar
47. Keeney, S. & Neale, M.J. Initiation of meiotic recombination by formation of DNA double-strand breaks: mechanism and regulation. Biochem. Soc. Trans. 34, 523–525 (2006).
    Article CAS PubMed Google Scholar
48. Nag, D.K., Pata, J.D., Sironi, M., Flood, D.R. & Hart, A.M. Both conserved and non-conserved regions of Spo11 are essential for meiotic recombination initiation in yeast. Mol. Genet. Genomics 276, 313–321 (2006).
    Article CAS PubMed Google Scholar
49. Tan, S. A modular polycistronic expression system for overexpressing protein complexes in Escherichia coli. Protein Expr. Purif. 21, 224–234 (2001).
    Article CAS PubMed Google Scholar
50. Kapust, R.B. & Waugh, D.S. Escherichia coli maltose-binding protein is uncommonly effective at promoting the solubility of polypeptides to which it is fused. Protein Sci. 8, 1668–1674 (1999).
    Article CAS PubMed PubMed Central Google Scholar
51. MacDowell, A.A. et al. Suite of three protein crystallography beamlines with single superconducting bend magnet as the source. J. Synchrotron Radiat. 11, 447–455 (2004).
    Article CAS PubMed Google Scholar
52. Benedetti, P., Silvestri, A., Fiorani, P. & Wang, J.C. Study of yeast DNA topoisomerase II and its truncation derivatives by transmission electron microscopy. J. Biol. Chem. 272, 12132–12137 (1997).
    Article CAS PubMed Google Scholar
53. Kirchhausen, T., Wang, J.C. & Harrison, S.C. DNA gyrase and its complexes with DNA: direct observation by electron microscopy. Cell 41, 933–943 (1985).
    Article CAS PubMed Google Scholar
54. Tyler, J.M. & Branton, D. Rotary shadowing of extended molecules dried from glycerol. J. Ultrastruct. Res. 71, 95–102 (1980).
    Article CAS PubMed Google Scholar

Download references