ATP binding controls distinct structural transitions of Escherichia coli DNA gyrase in complex with DNA

Nature Structural and Molecular Biology

Volumn 19, Issue 5, 2012, Pages 538-546

  Basu, Aakash ^a,b   Schoeffler, Allyn J ^c   Berger, James M ^c   Bryant, Zev ^b,d  

^a STANFORD UNIVERSITY   (United States)

^b Stanford University   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; BACTERIAL DNA; DNA TOPOISOMERASE (ATP HYDROLYSING);

ARTICLE; DNA SUPERCOILING; ENERGY TRANSFER; ENZYME CONFORMATION; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING;

ADENOSINE TRIPHOSPHATE; DNA GYRASE; DNA, BACTERIAL; DNA, SUPERHELICAL; ESCHERICHIA COLI; KINETICS; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN CONFORMATION;

ESCHERICHIA COLI;

EID: 84860751723     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2278     Document Type: Article

References (60)

1. Wang, J.C. Cellular roles of DNA topoisomerases: a molecular perspective. Nat. Rev. Mol. Cell Biol. 3, 430-440 (2002).
2. Peter, B.J. et al. Genomic transcriptional response to loss of chromosomal supercoiling in Escherichia coli. Genome Biol. 5, R87 (2004).
3. Vijayan, V., Zuzow, R. & O'Shea, E.K. Oscillations in supercoiling drive circadian gene expression in cyanobacteria. Proc. Natl. Acad. Sci. USA 106, 22564-22568 (2009).
4. Thomsen, N.D. & Berger, J.M. Structural frameworks for considering microbial protein-and nucleic acid-dependent motor ATPases. Mol. Microbiol. 69, 1071-1090 (2008).
5. Saraste, M., Sibbald, P.R. & Wittinghofer, A. The P-loop-a common motif in ATP-and GTP-binding proteins. Trends Biochem. Sci. 15, 430-434 (1990).
6. Pommier, Y., Leo, E., Zhang, H. & Marchand, C. DNA topoisomerases and their poisoning by anticancer and antibacterial drugs. Chem. Biol. 17, 421-433 (2010).
7. Kim, Y.S. et al. Update on Hsp90 inhibitors in clinical trial. Curr. Top. Med. Chem. 9, 1479-1492 (2009).
8. Wang, J.C. DNA topoisomerases. Annu. Rev. Biochem. 65, 635-692 (1996).
9. Schoeffler, A.J. & Berger, J.M. Recent advances in understanding structure-function relationships in the type II topoisomerase mechanism. Biochem. Soc. Trans. 33, 1465-1470 (2005).
10. Gellert, M., Mizuuchi, K., O'Dea, M.H. & Nash, H.A. DNA gyrase: an enzyme that introduces superhelical turns into DNA. Proc. Natl. Acad. Sci. USA 73, 3872-3876 (1976).
11. Liu, L.F. & Wang, J.C. DNA-DNA gyrase complex: the wrapping of the DNA duplex outside the enzyme. Cell 15, 979-984 (1978).
12. Brown, P.O. & Cozzarelli, N.R. A sign inversion mechanism for enzymatic supercoiling of DNA. Science 206, 1081-1083 (1979).
13. Liu, L.F. & Wang, J.C. Micrococcus luteus DNA gyrase: active components and a model for its supercoiling of DNA. Proc. Natl. Acad. Sci. USA 75, 2098-2102 (1978).
14. Kampranis, S.C., Bates, A.D. & Maxwell, A. A model for the mechanism of strand passage by DNA gyrase. Proc. Natl. Acad. Sci. USA 96, 8414-8419 (1999).
15. Orphanides, G. & Maxwell, A. Evidence for a conformational change in the DNA gyrase-DNA complex from hydroxyl radical footprinting. Nucleic Acids Res. 22, 1567-1575 (1994).
16. Kirkegaard, K. & Wang, J.C. Mapping the topography of DNA wrapped around gyrase by nucleolytic and chemical probing of complexes of unique DNA sequences. Cell 23, 721-729 (1981).
17. Lee, M.P., Sander, M. & Hsieh, T. Nuclease protection by Drosophila DNA topoisomerase II. Enzyme/DNA contacts at the strong topoisomerase II cleavage sites. J. Biol. Chem. 264, 21779-21787 (1989).
18. Luger, K., Mader, A.W., Richmond, R.K., Sargent, D.F. & Richmond, T.J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389, 251-260 (1997).
19. Kampranis, S.C. & Maxwell, A. Conversion of DNA gyrase into a conventional type II topoisomerase. Proc. Natl. Acad. Sci. USA 93, 14416-14421 (1996).
20. Corbett, K.D., Shultzaberger, R.K. & Berger, J.M. The C-terminal domain of DNA gyrase A adopts a DNA-bending beta-pinwheel fold. Proc. Natl. Acad. Sci. USA 101, 7293-7298 (2004).
21. Ruthenburg, A.J., Graybosch, D.M., Huetsch, J.C. & Verdine, G.L. A superhelical spiral in the Escherichia coli DNA gyrase A C-terminal domain imparts unidirectional supercoiling bias. J. Biol. Chem. 280, 26177-26184 (2005).
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).
23. Dong, K.C. & Berger, J.M. Structural basis for gate-DNA recognition and bending by type IIA topoisomerases. Nature 450, 1201-1205 (2007).
24. Bax, B.D. et al. Type IIA topoisomerase inhibition by a new class of antibacterial agents. Nature 466, 935-940 (2010).
25. Laponogov, I. et al. Structural insight into the quinolone-DNA cleavage complex of type IIA topoisomerases. Nat. Struct. Mol. Biol. 16, 667-669 (2009).
26. Yasuda, R., Noji, H., Yoshida, M., Kinosita, K. Jr. & Itoh, H. Resolution of distinct rotational substeps by submillisecond kinetic analysis of F1-ATPase. Nature 410, 898-904 (2001).
27. Adachi, K. et al. Coupling of rotation and catalysis in F1-ATPase revealed by single-molecule imaging and manipulation. Cell 130, 309-321 (2007).
28. Bryant, Z. et al. Structural transitions and elasticity from torque measurements on DNA. Nature 424, 338-341 (2003).
29. Gore, J. et al. Mechanochemical analysis of DNA gyrase using rotor bead tracking. Nature 439, 100-104 (2006).
30. Bates, A.D. DNA topoisomerases: single gyrase caught in the act. Curr. Biol. 16, R204-R206 (2006).
31. Cozzarelli, N.R. DNA gyrase and the supercoiling of DNA. Science 207, 953-960 (1980).
32. Nöllmann, M., Crisona, N.J. & Arimondo, P.B. Thirty years of Escherichia coli DNA gyrase: from in vivo function to single-molecule mechanism. Biochimie 89, 490-499 (2007).
33. Rief, M. et al. Myosin-V stepping kinetics: a molecular model for processivity. Proc. Natl. Acad. Sci. USA 97, 9482-9486 (2000).
34. Harkins, T.T., Lewis, T.J. & Lindsley, J.E. 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 (1998).
35. Ali, J.A., Orphanides, G. & Maxwell, A. Nucleotide binding to the 43-kilodalton N-terminal fragment of the DNA gyrase B protein. Biochemistry 34, 9801-9808 (1995).
36. Ali, J.A., Jackson, A.P., Howells, A.J. & Maxwell, A. The 43-kilodalton N-terminal fragment of the DNA gyrase-B protein hydrolyzes ATP and binds coumarin drugs. Biochemistry 32, 2717-2724 (1993).
37. Nöllmann, M. et al. Multiple modes of Escherichia coli DNA gyrase activity revealed by force and torque. Nat. Struct. Mol. Biol. 14, 264-271 (2007).
38. Heddle, J.G., Mitelheiser, S., Maxwell, A. & Thomson, N.H. Nucleotide binding to DNA gyrase causes loss of DNA wrap. J. Mol. Biol. 337, 597-610 (2004).
39. 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).
40. Costenaro, L., Grossmann, J.G., Ebel, C. & Maxwell, A. Small-angle X-ray scattering reveals the solution structure of the full-length DNA gyrase A subunit. Structure 13, 287-296 (2005).
41. Baker, N.M., Weigand, S., Maar-Mathias, S. & Mondragon, A. Solution structures of DNA-bound gyrase. Nucleic Acids Res. 39, 755-766 (2011).
42. Huang, B., Wang, W., Bates, M. & Zhuang, X. Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science 319, 810-813 (2008).
43. Vologodskii, A. Determining protein-induced DNA bending in force-extension experiments: theoretical analysis. Biophys. J. 96, 3591-3599 (2009).
44. Li, J.Y., Nelson, P.C. & Betterton, M.D. Entropic elasticity of DNA with a permanent kink. Macromolecules 39, 8816-8821 (2006).
45. Gubaev, A. & Klostermeier, D. DNA-induced narrowing of the gyrase N-gate coordinates T-segment capture and strand passage. Proc. Natl. Acad. Sci. USA 108, 14085-14090 (2011).
46. Elting, M.W., Bryant, Z., Liao, J.C. & Spudich, J.A. Detailed tuning of structure and intramolecular communication are dispensable for processive motion of myosin VI. Biophys. J. 100, 430-439 (2011).
47. Sugino, A., Higgins, N.P., Brown, P.O., Peebles, C.L. & Cozzarelli, N.R. Energy coupling in DNA gyrase and the mechanism of action of novobiocin. Proc. Natl. Acad. Sci. USA 75, 4838-4842 (1978).
48. 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).
49. Lanz, M.A. & Klostermeier, D. Guiding strand passage: DNA-induced movement of the gyrase C-terminal domains defines an early step in the supercoiling cycle. Nucleic Acids Res. 39, 9681-9694 (2011).
50. 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).
51. Lindsley, J.E. & Wang, J.C. On the coupling between ATP usage and DNA transport by yeast DNA topoisomerase II. J. Biol. Chem. 268, 8096-8104 (1993).
52. Sugino, A. & Cozzarelli, N.R. The intrinsic ATPase of DNA gyrase. J. Biol. Chem. 255, 6299-6306 (1980).
53. Bates, A.D., O'Dea, M.H. & Gellert, M. Energy coupling in Escherichia coli DNA gyrase: the relationship between nucleotide binding, strand passage, and DNA supercoiling. Biochemistry 35, 1408-1416 (1996).
54. Mickler, M., Hessling, M., Ratzke, C., Buchner, J. & Hugel, T. The large conformational changes of Hsp90 are only weakly coupled to ATP hydrolysis. Nat. Struct. Mol. Biol. 16, 281-286 (2009).
55. Kampranis, S.C. & Maxwell, A. The DNA gyrase-quinolone complex. ATP hydrolysis and the mechanism of DNA cleavage. J. Biol. Chem. 273, 22615-22626 (1998).
56. Pato, M.L., Howe, M.M. & Higgins, N.P.A. DNA gyrase-binding site at the center of the bacteriophage Mu genome is required for efficient replicative transposition. Proc. Natl. Acad. Sci. USA 87, 8716-8720 (1990).
57. Schoeffler, A.J., May, A.P. & Berger, J.M. A domain insertion in Escherichia coli GyrB adopts a novel fold that plays a critical role in gyrase function. Nucleic Acids Res. 38, 7830-7844 (2010).
58. Tokunaga, M., Imamoto, N. & Sakata-Sogawa, K. Highly inclined thin illumination enables clear single-molecule imaging in cells. Nat. Methods 5, 159-161 (2008).
59. Sun, Y., McKenna, J.D., Murray, J.M., Ostap, E.M. & Goldman, Y.E. Parallax: high accuracy three-dimensional single molecule tracking using split images. Nano Lett. 9, 2676-2682 (2009).
60. Gore, J. Single-Molecule Studies of DNA Twist Mechanics and Gyrase Mechanochemistry. Thesis, Univ. California, Berkeley (2005).