Structure of a topoisomerase II-DNA-nucleotide complex reveals a new control mechanism for ATPase activity

Nature Structural and Molecular Biology

Volumn 19, Issue 11, 2012, Pages 1147-1154

  Schmidt, Bryan H ^a   Osheroff, Neil ^b   Berger, James M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DNA; DNA TOPOISOMERASE (ATP HYDROLYSING);

ARTICLE; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME STRUCTURE; HYDROLYSIS; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

ADENYLYL IMIDODIPHOSPHATE; AMINO ACID SEQUENCE; ANTIGENS, NEOPLASM; CHROMATOGRAPHY, GEL; CRYSTALLIZATION; DIMERIZATION; DNA; DNA TOPOISOMERASES, TYPE II; DNA-BINDING PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; PROTEIN CONFORMATION; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE;

EID: 84869094439     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2388     Document Type: Article

References (67)

1. Bustamante, C., Cheng, W. & Mejia, Y.X. Revisiting the central dogma one molecule at a time. Cell 144, 480-497 (2011).
2. Schoeffler, A.J. & Berger, J.M. DNA topoisomerases: harnessing and constraining energy to govern chromosome topology. Q. Rev. Biophys. 41, 41-101 (2008).
3. 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).
4. Roca, J., Berger, J.M., Harrison, S.C. & Wang, J.C. DNA transport by a type II topoisomerase: direct evidence for a two-gate mechanism. Proc. Natl. Acad. Sci. USA 93, 4057-4062 (1996). (Pubitemid 26144245)
5. Wigley, D.B., Davies, G.J., Dodson, E.J., Maxwell, A. & Dodson, G. Crystal structure of an N-terminal fragment of the DNA gyrase B protein. Nature 351, 624-629 (1991). (Pubitemid 21896650)
6. Berger, J.M., Gamblin, S.J., Harrison, S.C. & Wang, J.C. Structure and mechanism of DNA topoisomerase II. Nature 379, 225-232 (1996). (Pubitemid 26025206)
7. Morais Cabral, J.H. et al. Crystal structure of the breakage-reunion domain of DNA gyrase. Nature 388, 903-906 (1997). (Pubitemid 27377066)
8. 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).
9. Worland, S.T. & Wang, J.C. Inducible overexpression, purification, and active site mapping of DNA topoisomerase II from the yeast Saccharomyces cerevisiae. J. Biol. Chem. 264, 4412-4416 (1989). (Pubitemid 19081341)
10. Tse, Y.C., Kirkegaard, K. & Wang, J.C. Covalent bonds between protein and DNA. Formation of phosphotyrosine linkage between certain DNA topoisomerases and DNA. J. Biol. Chem. 255, 5560-5565 (1980).
11. 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). (Pubitemid 28418379)
12. Lindsley, J.E. & Wang, J.C. Study of allosteric communication between protomers by immunotagging. Nature 361, 749-750 (1993). (Pubitemid 23070487)
13. Gellert, M., Fisher, L.M. & O'Dea, M.H. DNA gyrase: purification and catalytic properties of a fragment of gyrase B protein. Proc. Natl. Acad. Sci. USA 76, 6289-6293 (1979). (Pubitemid 10163386)
14. Brown, P.O., Peebles, C.L. & Cozzarelli, N.R. A topoisomerase from Escherichia coli related to DNA gyrase. Proc. Natl. Acad. Sci. USA 76, 6110-6114 (1979). (Pubitemid 10165364)
15. Williams, N.L. & Maxwell, A. Locking the DNA gate of DNA gyrase: investigating the effects on DNA cleavage and ATP hydrolysis. Biochemistry 38, 14157-14164 (1999).
16. Williams, N.L. & Maxwell, A. Probing the two-gate mechanism of DNA gyrase using cysteine cross-linking. Biochemistry 38, 13502-13511 (1999).
17. Classen, S., Olland, S. & Berger, J.M. 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 (2003). (Pubitemid 37140080)
18. Mizuuchi, K., O'Dea, M.H. & Gellert, M. DNA gyrase: subunit structure and ATPase activity of the purified enzyme. Proc. Natl. Acad. Sci. USA 75, 5960-5963 (1978). (Pubitemid 9093640)
19. 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). (Pubitemid 23120392)
20. Osheroff, N., Shelton, E.R. & Brutlag, D.L. DNA topoisomerase II from Drosophila melanogaster. Relaxation of supercoiled DNA. J. Biol. Chem. 258, 9536-9543 (1983).
21. 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). (Pubitemid 28235213)
22. Dutta, R. & Inouye, M. GHKL, an emergent ATPase/kinase superfamily. Trends Biochem. Sci. 25, 24-28 (2000). (Pubitemid 30060426)
23. Laponogov, I. et al. Structural basis of gate-DNA breakage and resealing by type II topoisomerases. PLoS ONE 5, e11338 (2010).
24. Laponogov, I. et al. Structural insight into the quinolone-DNA cleavage complex of type IIA topoisomerases. Nat. Struct. Mol. Biol. 16, 667-669 (2009).
25. Wohlkonig, A. et al. Structural basis of quinolone inhibition of type IIA topoisomerases and target-mediated resistance. Nat. Struct. Mol. Biol. 17, 1152-1153 (2010).
26. Bax, B.D. et al. Type IIA topoisomerase inhibition by a new class of antibacterial agents. Nature 466, 935-940 (2010).
27. Schmidt, B.H., Burgin, A.B., Deweese, J.E., Osheroff, N. & Berger, J.M. A novel and unified two-metal mechanism for DNA cleavage by type II and IA topoisomerases. Nature 465, 641-644 (2010).
28. Wu, C.C. et al. Structural basis of type II topoisomerase inhibition by the anticancer drug etoposide. Science 333, 459-462 (2011).
29. Wendorff, T.J., Schmidt, B.H., Heslop, P., Austin, C.A. & Berger, J.M. The structure of DNA-bound human topoisomerase II alpha: conformational mechanisms for coordinating inter-subunit interactions with DNA cleavage. J. Mol. Biol. published online, doi:10.1016/j.jmb.2012.07.014 (25 July 2012).
30. 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). (Pubitemid 29354805)
31. Schultz, P., Olland, S., Oudet, P. & Hancock, R. Structure and conformational changes of DNA topoisomerase II visualized by electron microscopy. Proc. Natl. Acad. Sci. USA 93, 5936-5940 (1996). (Pubitemid 26190780)
32. 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). (Pubitemid 34952456)
33. Brino, L. et al. Dimerization of Escherichia coli DNA-gyrase B provides a structural mechanism for activating the ATPase catalytic center. J. Biol. Chem. 275, 9468-9475 (2000). (Pubitemid 30185175)
34. 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). (Pubitemid 41587788)
35. Bjergbaek, L. et al. Communication between the ATPase and cleavage/religation domains of human topoisomerase IIα. J. Biol. Chem. 275, 13041-13048 (2000). (Pubitemid 30241465)
36. Liu, L.F., Liu, C.C. & Alberts, B.M. Type II DNA topoisomerases: enzymes that can unknot a topologically knotted DNA molecule via a reversible double-strand break. Cell 19, 697-707 (1980). (Pubitemid 10134849)
37. Marini, J.C., Miller, K.G. & Englund, P.T. Decatenation of kinetoplast DNA by topoisomerases. J. Biol. Chem. 255, 4976-4979 (1980).
38. Osheroff, N. & Zechiedrich, E.L. Calcium-promoted DNA cleavage by eukaryotic topoisomerase II: trapping the covalent enzyme-DNA complex in an active form. Biochemistry 26, 4303-4309 (1987).
39. Lindsley, J.E. Use of a real-time, coupled assay to measure the ATPase activity of DNA topoisomerase II. Methods Mol. Biol. 95, 57-64 (2001).
40. Tamura, J.K. & Gellert, M. 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 (1990). (Pubitemid 120014159)
41. Maxwell, A. & Gellert, M. The DNA dependence of the ATPase activity of DNA gyrase. J. Biol. Chem. 259, 14472-14480 (1984). (Pubitemid 15222266)
42. Hammonds, T.R. & Maxwell, A. The DNA dependence of the ATPase activity of human DNA topoisomerase IIα. J. Biol. Chem. 272, 32696-32703 (1997). (Pubitemid 28011962)
43. West, K.L., Turnbull, R.M., Willmore, E., Lakey, J.H. & Austin, C.A. Characterisation of the DNA-dependent ATPase activity of human DNA topoisomerase IIbeta: mutation of Ser165 in the ATPase domain reduces the ATPase activity and abolishes the in vivo complementation ability. Nucleic Acids Res. 30, 5416-5424 (2002). (Pubitemid 36113919)
44. Mueller-Planitz, F. & Herschlag, D. DNA topoisomerase II selects DNA cleavage sites based on reactivity rather than binding affinity. Nucleic Acids Res. 35, 3764-3773 (2007). (Pubitemid 47244669)
45. Shiozaki, K. & Yanagida, M. Functional dissection of the phosphorylated termini of fission yeast DNA topoisomerase II. J. Cell Biol. 119, 1023-1036 (1992).
46. Cardenas, M.E., Dang, Q., Glover, C.V. & Gasser, S.M. Casein kinase II phosphorylates the eukaryote-specific C-terminal domain of topoisomerase II in vivo. EMBO J. 11, 1785-1796 (1992).
47. McClendon, A.K. et al. Bimodal recognition of DNA geometry by human topoisomerase II α: preferential relaxation of positively supercoiled DNA requires elements in the C-terminal domain. Biochemistry 47, 13169-13178 (2008).
48. Caron, P.R., Watt, P. & Wang, J.C. The C-terminal domain of Saccharomyces cerevisiae DNA topoisomerase II. Mol. Cell. Biol. 14, 3197-3207 (1994). (Pubitemid 24132733)
49. Roca, J. The path of the DNA along the dimer interface of topoisomerase II. J. Biol. Chem. 279, 25783-25788 (2004). (Pubitemid 38756842)
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. Osheroff, N. Eukaryotic topoisomerase II. Characterization of enzyme turnover. J. Biol. Chem. 261, 9944-9950 (1986). (Pubitemid 17214132)
52. 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). (Pubitemid 27007889)
53. Li, W. & Wang, J.C. Footprinting of yeast DNA topoisomerase II lysyl side chains involved in substrate binding and interdomainal interactions. J. Biol. Chem. 272, 31190-31195 (1997). (Pubitemid 27527570)
54. Choudhary, C. et al. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325, 834-840 (2009).
55. Bates, A.D., Berger, J.M. & Maxwell, A. The ancestral role of ATP hydrolysis in type II topoisomerases: prevention of DNA double-strand breaks. Nucleic Acids Res. 39, 6327-6339 (2011).
56. Ali, M.M. et al. Crystal structure of an Hsp90-nucleotide-p23/Sba1 closed chaperone complex. Nature 440, 1013-1017 (2006).
57. 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).
58. Lee, S. et al. DNA cleavage and opening reactions of human topoisomerase IIα are regulated via Mg2+-mediated dynamic bending of gate-DNA. Proc. Natl. Acad. Sci. USA 109, 2925-2930 (2012).
59. Skouboe, C. et al. A human topoisomerase II α heterodimer with only one ATP binding site can go through successive catalytic cycles. J. Biol. Chem. 278, 5768-5774 (2003). (Pubitemid 36800822)
60. Göttler, T. & Klostermeier, D. Dissection of the nucleotide cycle of B. subtilis DNA gyrase and its modulation by DNA. J. Mol. Biol. 367, 1392-1404 (2007). (Pubitemid 46413271)
61. Deweese, J.E., Burgin, A.B. & Osheroff, N. Using 3′-bridging phosphorothiolates to isolate the forward DNA cleavage reaction of human topoisomerase IIα. Biochemistry 47, 4129-4140 (2008). (Pubitemid 351458127)
62. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (1997). (Pubitemid 27085611)
63. McCoy, A.J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007). (Pubitemid 47080256)
64. Emsley, P., Lohkamp, B., Scott, W.G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
65. Adams, P.D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221 (2010).
66. Chen, V.B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21 (2010).
67. The PyMOL Molecular Graphics System. Version 1.5.0.1 Schrödinger, LLC.