The structure of DNA-bound human topoisomerase II alpha: Conformational mechanisms for coordinating inter-subunit interactions with DNA cleavage

Journal of Molecular Biology

Volumn 424, Issue 3-4, 2012, Pages 109-124

  Wendorff, Timothy J ^a   Schmidt, Bryan H ^a   Heslop, Pauline ^b   Austin, Caroline A ^b   Berger, James M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

allostery; chemotherapeutics; double strand DNA breaks; protein drug interactions; type IIA topoisomerase

Indexed keywords

DNA TOPOISOMERASE (ATP HYDROLYSING); DNA TOPOISOMERASE 2 ALPHA; OLIGONUCLEOTIDE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DIMERIZATION; DNA BINDING; DNA CLEAVAGE; DNA DETERMINATION; DNA STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA INTERACTION;

EID: 84869097457     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2012.07.014     Document Type: Article

References (97)

1. A.J. Schoeffler, and J.M. Berger DNA topoisomerases: harnessing and constraining energy to govern chromosome topology Q. Rev. Biophys. 1 2008 41 101
2. J.E. Deweese, and N. Osheroff The DNA cleavage reaction of topoisomerase II: wolf in sheep's clothing Nucleic Acids Res. 37 2009 738 748
3. Y. Pommier, E. Leo, H. Zhang, and C. Marchand DNA topoisomerases and their poisoning by anticancer and antibacterial drugs Chem. Biol. 17 2010 421 433
4. J. Roca, and J.C. Wang 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 1992 833 840
5. J. Roca, and J.C. Wang DNA transport by a type II DNA topoisomerase: evidence in favor of a two-gate mechanism Cell 77 1994 609 616
6. J. Roca, J.M. Berger, S.C. Harrison, and J.C. Wang DNA transport by a type II two-gate mechanism topoisomerase: direct evidence for a two-gate mechanism Proc. Natl Acad. Sci. USA 93 1996 4057 4062 (Pubitemid 26144245)
7. N.L. Williams, and A. Maxwell Probing the two-gate mechanism of DNA gyrase using cysteine cross-linking Biochemistry 38 1999 13502 13511
8. D.B. Wigley, G.J. Davies, E.J. Dodson, A. Maxwell, and G. Dodson Crystal structure of an N-terminal fragment of the DNA gyrase B protein Nature 351 1991 624 629 (Pubitemid 21896650)
9. A. Morrison, and N.R. Cozzarelli Site-specific gyrase cleavage of DNA by E. coli DNA Cell 17 1979 175 184 (Pubitemid 9188221)
10. Y.C. Tse, K. Kirkegaard, and J.C. Wang Covalent bonds between protein and DNA. Formation of phosphotyrosine linkage between certain DNA topoisomerases and DNA J. Biol. Chem. 255 1980 5560 5565
11. C. Buhler, J.H. Lebbink, C. Bocs, R. Ladenstein, and P. Forterre DNA topoisomerase VI generates ATP-dependent double-strand breaks with two-nucleotide overhangs J. Biol. Chem. 276 2001 37215 37222
12. M. Gellert, K. Mizuuchi, M.H. O'Dea, and H.A. Nash DNA gyrase: an enzyme that introduces superhelical turns into DNA Proc. Natl Acad. Sci. USA 73 1976 3872 3876
13. L.F. Liu, C.-C. Liu, and B.M. Alberts T4 DNA topoisomerase: a new ATP-dependent enzyme essential for initiation of T4 bacteriophage DNA replication Nature 281 1979 456 461 (Pubitemid 10244266)
14. M.I. Baldi, P. Benedetti, E. Mattoccia, and G.P. Tocchini-Valentini In vitro catenation and decatenation of DNA and a novel eucaryotic ATP-dependent topoisomerase Cell 20 1980 461 467 (Pubitemid 10117762)
15. T. Goto, and J. Wang Yeast DNA topoisomerase II. An ATP-dependent type II topoisomerase that catalyzes the catenation, decatenation, unknotting, and relaxation of double-stranded DNA rings J. Biol. Chem. 257 1982 5866 5872
16. C.L. Baird, T.T. Harkins, S.K. Morris, and J.E. Lindsley Topoisomerase II drives DNA transport by hydrolyzing one ATP Proc. Natl Acad. Sci. USA 96 1999 13685 13690
17. T.T. Harkins, T.J. Lewis, and J.E. Lindsley 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 1998 7299 7312 (Pubitemid 28235213)
18. K.D. Corbett, P. Benedetti, and J.M. Berger Holoenzyme assembly and ATP-mediated conformational dynamics of topoisomerase VI Nat. Struct. Mol. Biol. 14 2007 611 619 (Pubitemid 47037071)
19. M. Graille, L. Cladiere, D. Durand, F. Lecointe, D. Gadelle, and S. Quevillon-Cheruel Crystal structure of an intact type II DNA topoisomerase: insights into DNA transfer mechanisms Structure 16 2008 360 370 (Pubitemid 351324114)
20. P. Forterre, S. Gribaldo, D. Gadelle, and M.-C. Serre Origin and evolution of DNA topoisomerases Biochimie 89 2007 427 446 (Pubitemid 46656307)
21. A.D. Bates, J.M. Berger, and A. Maxwell The ancestral role of ATP hydrolysis in type II topoisomerases: prevention of DNA double-strand breaks Nucleic Acids Res. 39 2011 6327 6339
22. J.M. Berger, S.J. Gamblin, S.C. Harrison, and J.C. Wang Structure and mechanism of DNA topoisomerase II Nature 379 1996 225 232 (Pubitemid 26025206)
23. M. Tsai-Pflugfelder, L.F. Liu, A.A. Liu, K.M. Tewey, J. Whang-Peng, and T. Knutsen Cloning and sequencing of cDNA encoding human DNA topoisomerase II and localization of the gene to chromosome region 17q21-22 Proc. Natl Acad. Sci. USA 85 1988 7177 7181
24. T.D. Chung, F.H. Drake, K.B. Tan, S.R. Per, S.T. Crooke, and C.K. Mirabelli Characterization and immunological identification of cDNA clones encoding two human DNA topoisomerase II isozymes Proc. Natl Acad. Sci. USA 86 1989 9431 9435 (Pubitemid 20010440)
25. C.A. Austin, and L.M. Fisher Isolation and characterization of a human cDNA clone encoding a novel DNA topoisomerase II homologue from HeLa cells FEBS Lett. 266 1990 115 117 (Pubitemid 20194187)
26. C.A. Austin, J.-H. Sng, S. Patel, and L.M. Fisher Novel HeLa topoisomerase II is the II beta isoform: complete coding sequence and homology with other type II topoisomerases Biochim. Biophys. Acta 1172 1993 283 291 (Pubitemid 23079954)
27. G. Capranico, S. Tinelli, C.A. Austin, M.L. Fisher, and F. Zunino Different patterns of gene expression of topoisomerase II isoforms in differentiated tissues during murine development Biochim. Biophys. Acta 1132 1992 43 48
28. K. Padget, A. Pearson, and C. Austin Quantitation of DNA topoisomerase IIalpha and beta in human leukaemia cells by immunoblot Leukemia 14 2005 1997 2005
29. K. Tsutsui, K. Tsutsui, S. Okada, M. Watanabe, T. Shohmori, S. Seki, and Y. Inoue Molecular cloning of partial cDNAs for rat DNA topoisomerase II isoforms and their differential expression in brain development J. Biol. Chem. 268 1993 19076 19083 (Pubitemid 23273863)
30. K. Tsutsui, K. Sano, A. Kikuchi, and A. Tokunaga Involvement of DNA topoisomerase IIbeta in neuronal differentiation J. Biol. Chem. 276 2001 5769 5778
31. Y.L. Lyu, and J.C. Wang Aberrant lamination in the cerebral cortex of mouse embryos lacking DNA topoisomerase IIbeta Proc. Natl Acad. Sci. USA 100 2003 7123 7128 (Pubitemid 36706403)
32. P. Grue, A. Grasser, M. Sehested, P.B. Jensen, A. Uhse, and T. Straub Essential mitotic functions of DNA topoisomerase IIalpha are not adopted by topoisomerase IIbeta in human H69 cells J. Biol. Chem. 273 1998 33660 33666
33. A. Niimi, N. Suka, M. Harata, A. Kikuchi, and S. Mizuno Co-localization of chicken DNA topoisomerase IIα, but not β, with sites of DNA replication and possible involvement of a C-terminal region of α through its binding to PCNA Chromosoma 110 2001 102 114 (Pubitemid 32529714)
34. B.-G. Ju, W. Lunyak, V. Perissi, I. Garcia-Bassets, D.W. Rose, C.K. Glass, and M.G. Rosenfeld A topoisomerase IIbeta-mediated dsDNA break required for regulated transcription Science 312 2006 1798 1802 (Pubitemid 43962898)
35. B. Perillo, M.N. Ombra, A. Bertoni, C. Cuozzo, S. Sacchetti, and A. Sasso DNA oxidation as triggered by H3K9me2 demethylation drives estrogen-induced gene expression Science 319 2008 202 206
36. S. McNamara, H. Wang, N. Hanna, and W.H. Miller Topoisomerase IIbeta negatively modulates retinoic acid receptor alpha function: a novel mechanism of retinoic acid resistance Mol. Cell. Biol. 28 2008 2066 2077 (Pubitemid 351342636)
37. A.M. Dingemans, H.M. Pinedo, and G. Giaccone Clinical resistance to topoisomerase-targeted drugs Biochim. Biophys. Acta 1400 1998 275 288 (Pubitemid 28475109)
38. A.M. Fry, C.M. Chresta, S.M. Davies, M.C. Walker, A.L. Harris, and J.A. Hartley Relationship between topoisomerase II Level and chemosensitivity in human tumor cell lines relationship between topoisomerase II level and chemosensitivity in human Cancer 1991 6592 6595
39. K. Kasahara, Y. Fujiwara, Y. Sugimoto, K. Nishio, T. Tamura, T. Matsuda, and N. Saijo Determinants of response to the DNA topoisomerase II inhibitors doxorubicin and etoposide in human lung cancer cell lines J. Natl Cancer Inst. 84 1992 113 118
40. F. Boege, A. Andersen, S. Jensen, R. Zeidler, and H. Kreipe Proliferation-associated nuclear antigen Ki-S1 is identical with topoisomerase IIalpha Am. J. Pathol. 146 1995 1302 1308
41. C. Felix Secondary leukemias induced by topoisomerase-targeted drugs Biochim. Biophys. Acta 1400 1998 233 255 (Pubitemid 28475107)
42. C. Felix Leukemias related to treatment with DNA topoisomerase II inhibitors Med. Pediatr. Oncol. 36 2001 525 535 (Pubitemid 32336557)
43. J. Pedersen-Bjergaard Genetic pathways in therapy-related myelodysplasia and acute myeloid leukemia Blood 99 2002 1909 1912 (Pubitemid 34525468)
44. A.M. Azarova, Y.L. Lyu, C.-P. Lin, Y.-C. Tsai, J.Y.-N. Lau, J.C. Wang, and L.F. Liu Roles of DNA topoisomerase II isozymes in chemotherapy and secondary malignancies Proc. Natl Acad. Sci. USA 104 2007 11014 11019 (Pubitemid 47175218)
45. Y.L. Lyu, J.E. Kerrigan, C.P. Lin, A.M. Azarova, Y.C. Tsai, Y. Ban, and L.F. Liu Topoisomerase IIbeta mediated DNA double-strand breaks: implications in doxorubicin cardiotoxicity and prevention by dexrazoxane Cancer Res. 67 2007 8839 8846 (Pubitemid 47437460)
46. M.C. Haffner, M.J. Aryee, A. Toubaji, D.M. Esopi, R. Albadine, and B. Gurel Androgen-induced TOP2B-mediated double-strand breaks and prostate cancer gene rearrangements Nat. Genet. 42 2010 668 675
47. I.G. Cowell, C. Sondka, K. Smith, K.C. Lee, C.M. Manville, and M. Sidorczuk-Lesthuruge A model for MLL translocations in therapy-related leukemia involving topoisomerase II-beta mediated DNA strand breaks and gene proximity Proc. Natl Acad. Sci. USA 109 2012 8989 8994
48. E. Toyoda, S. Kagaya, I.G. Cowell, A. Kurosawa, K. Kamoshita, and K. Nishikawa NK314, a topoisomerase II inhibitor that specifically targets the alpha isoform J. Biol. Chem. 283 2008 23711 23720
49. C.-C. Wu, T.-K. Li, L. Farh, L.-Y. Lin, T.-S. Lin, and Y.-J. Yu Structural basis of type II topoisomerase inhibition by the anticancer drug etoposide Science 333 2011 459 462
50. K.C. Dong, and J.M. Berger Structural basis for gate-DNA recognition and bending by type IIA topoisomerases Nature 450 2007 1201 1205
51. I. Laponogov, M.K. Sohi, D.A. Veselkov, X.S. Pan, R. Sawhney, and A.W. Thompson Structural insight into the quinolone-DNA cleavage complex of type IIA topoisomerases Nat. Struct. Mol. Biol. 16 2009 667 669
52. A. Wohlkonig, P.F. Chan, A.P. Fosberry, P. Homes, J. Huang, and M. Kranz Structural basis of quinolone inhibition of type IIA topoisomerases and target-mediated resistance Nat. Struct. Mol. Biol. 17 2010 1152 1153
53. B.H. Schmidt, A.B. Burgin, J.E. Deweese, N. Osheroff, and J.M. Berger A novel and unified two-metal mechanism for DNA cleavage by type II and IA topoisomerases Nature 465 2010 641 644
54. G. Charvin, T.R. Strick, D. Bensimon, and V. Croquette Topoisomerase IV bends and overtwists DNA upon binding Biophys. J. 89 2005 384 392 (Pubitemid 41098293)
55. A.H. Hardin, S.K. Sarkar, Y. Seol, G.F. Liou, N. Osheroff, and K.C. Neuman Direct measurement of DNA bending by type IIA topoisomerases: implications for non-equilibrium topology simplification Nucleic Acids Res. 39 2011 5729 5743
56. V.B. Chen, W.B. Arendall, J.J. Headd, D.A. Keedy, R.M. Immormino, and G.J. Kapral MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 12 21
57. I. Laponogov, X.S. Pan, D.A. Veselkov, K.E. McAuley, L.M. Fisher, and M.R. Sanderson Structural basis of gate-DNA breakage and resealing by type II topoisomerases PLoS One 5 2010 e11338
58. B.D. Bax, P.F. Chan, D.S. Eggleston, A. Fosberry, D.R. Gentry, and F. Gorrec Type IIA topoisomerase inhibition by a new class of antibacterial agents Nature 466 2010 935 940
59. J. Bachant, A. Alcasabas, Y. Blat, N. Kleckner, and S.J. Elledge The SUMO-1 isopeptidase Smt4 is linked to centromeric cohesion through SUMO-1 modification of DNA topoisomerase II Mol. Cell 9 2002 1169 1182 (Pubitemid 34722297)
60. M.M. Dawlaty, L. Malureanu, K.B. Jeganathan, E. Kao, C. Sustmann, and S. Tahk Resolution of sister centromeres requires RanBP2-mediated SUMOylation of topoisomerase IIalpha Cell 133 2008 103 115 (Pubitemid 351442988)
61. M.-T. Lee, and J. Bachant SUMO modification of DNA topoisomerase II: trying to get a CENse of it all DNA Repair 8 2009 557 568
62. H. Ryu, M. Furuta, D. Kirkpatrick, S.P. Gygi, and Y. Azuma PIASy-dependent SUMOylation regulates DNA topoisomerase IIalpha activity J. Cell Biol. 191 2010 783 794
63. M.S. Rodriguez, C. Dargemont, and R.T. Hay SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting J. Biol. Chem. 276 2001 12654 12659
64. R.T. Hay SUMO: a history of modification Mol. Cell 18 2005 1 12 (Pubitemid 40444643)
65. A.C. Gentry, S.L. Pitts, M.J. Jablonsky, C. Bailly, D.E. Graves, and N. Osheroff Interactions between the etoposide derivative F14512 and human type II topoisomerases: implications for the C4 spermine moiety in promoting enzyme-mediated DNA cleavage Biochemistry 50 2011 3240 3249
66. E. Willmore, A.J. Frank, K. Padget, M.J. Tilby, and C.A. Austin Etoposide targets topoisomerase IIalpha and IIbeta in leukemic cells: isoform-specific cleavable complexes visualized and quantified in situ by a novel immunofluorescence technique Mol. Pharmacol. 54 1998 78 85 (Pubitemid 28337589)
67. O.J. Bandele, and N. Osheroff The efficacy of topoisomerase II-targeted anticancer agents reflects the persistence of drug-induced cleavage complexes in cells Biochemistry 47 2008 11900 11908
68. P.C. Dedon, and R.F. Borch Characterization of the reactions of platinum antitumor agents with biological and nonbiological sulfur-containing nucleophiles Biochem. Pharmacol. 36 1987 1955 1964 (Pubitemid 17100217)
69. M.A. Fuertes, C. Alonso, and J.M. Pérez Biochemical modulation of cisplatin mechanisms of action: enhancement of antitumor activity and circumvention of drug resistance Chem. Rev. 103 2003 645 662
70. R.P. Bender, M.J. Jablonsky, M. Shadid, I. Romaine, N. Dunlap, and C. Anklin Substituents on etoposide that interact with human topoisomerase IIalpha in the binary enzyme-drug complex: contributions to etoposide binding and activity Biochemistry 47 2009 4501 4509 (Pubitemid 351522100)
71. A.M. Wilstermann, R.P. Bender, M. Godfrey, S. Choi, C. Anklin, and D.B. Berkowitz Topoisomerase II-drug interaction domains: identification of substituents on etoposide that interact with the enzyme Biochemistry 2007 8217 8225 (Pubitemid 47075961)
72. F.H. Drake, G.A. Hofmann, H.F. Bartus, M.R. Mattern, S.T. Crooke, and C.K. Mirabelli Biochemical and pharmacological properties of p170 and p180 forms of topoisomerase II Biochemistry 28 1989 8154 8160 (Pubitemid 19252897)
73. J.H. Morais Cabral, A.P. Jackson, C.V. Smith, N. Shikotra, A. Maxwell, and R.C. Liddington Crystal structure of the breakage-reunion domain of DNA gyrase Nature 388 1997 903 906 (Pubitemid 27377066)
74. D. Fass, C.E. Bogden, and J.M. Berger Quaternary changes in topoisomerase II may direct orthogonal movement of two DNA strands Nat. Struct. Mol. Biol. 6 1999 322 326 (Pubitemid 29166478)
75. K.D. Corbett, A.J. Schoeffler, N.D. Thomsen, and J.M. Berger The structural basis for substrate specificity in DNA topoisomerase IV J. Mol. Biol. 351 2005 545 561 (Pubitemid 41021940)
76. I. Laponogov, D.A. Veselkov, M.K. Sohi, X.S. Pan, A. Achari, and C. Yang Breakage-reunion domain of Streptococcus pneumoniae topoisomerase IV: crystal structure of a gram-positive quinolone target PLoS One 2 2007 e301
77. E.M. Tretter, A.J. Schoeffler, S.R. Weisfield, and J.M. Berger Crystal structure of the DNA gyrase GyrA N-terminal domain from Mycobacterium tuberculosis Proteins: Struct. Funct. Bioinf. 78 2010 492 495
78. A.J. Schoeffler, A.P. May, and J.M. Berger A domain insertion in Escherichia coli GyrB adopts a novel fold that plays a critical role in gyrase function Nucleic Acids Res. 38 2010 7830 7844
79. J. Roca The path of the DNA along the dimer interface of topoisomerase II J. Biol. Chem. 279 2004 25783 25788 (Pubitemid 38756842)
80. K.L. West, E.L. Meczes, R. Thorn, R.M. Turnbull, R. Marshall, and C.A. Austin Mutagenesis of E477 or K505 in the B′ domain of human topoisomerase II beta increases the requirement for magnesium ions during strand passage Biochemistry 39 2000 1223 1233 (Pubitemid 30090688)
81. C.G. Noble, and A. Maxwell The role of GyrB in the DNA cleavage-religation reaction of DNA gyrase: a proposed two metal-ion mechanism J. Mol. Biol. 318 2002 361 371 (Pubitemid 34734831)
82. J.E. Deweese, F.P. Guengerich, A.B. Burgin, and N. Osheroff Metal ion interactions in the DNA cleavage/ligation active site of human topoisomerase IIalpha Biochemistry 48 2009 8940 8947
83. W. Yang An equivalent metal ion in one- and two-metal-ion catalysis Nat. Struct. Mol. Biol. 15 2008 1228 1231
84. R.A. Wasserman, and J.C. Wang Mechanistic studies of amsacrine-resistant derivatives of DNA topoisomerase II. Implications in resistance to multiple antitumor drugs targeting the enzyme. J. Biol. Chem. 269 1994 20943 20951
85. J.E. Tropea, S. Cherry, and D.S. Waugh High throughput protein expression and purification Methods Mol. Biol. 498 2009 297 307
86. A. MacDowell, R.S. Celestre, M. Howells, W. McKinney, J. Krupnick, and D. Cambie Suite of three protein crystallography beamlines with single superconducting bend magnet as the source J. Synchrotron Radiat. 11 2004 447 455 (Pubitemid 40087583)
87. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 306 315
88. M.D. Winn, C.C. Ballard, K.D. Cowtan, E.J. Dodson, P. Emsley, and P.R. Evans Overview of the CCP4 suite and current developments Acta Crystallogr., Sect. D: Biol. Crystallogr. 67 2011 235 242
89. S.F. Altschul, J.C. Wootton, E.M. Gertz, R. Agarwala, A. Morgulis, A.A. Schaffer, and Y.K. Yu Protein database searches using compositionally adjusted substitution matrices FEBS J. 272 2005 5101 5109 (Pubitemid 41503143)
90. S.F. Altschul, T.L. Madden, A.A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D.J. Lipman Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res. 25 1997 3389 3402 (Pubitemid 27359211)
91. N. Stein CHAINSAW: a program for mutating pdb files used as templates in molecular replacement J. Appl. Crystallogr. 41 2008 641 643 (Pubitemid 351693895)
92. A.J. McCoy, R.W. Grosse-Kunstleve, P.D. Adams, M.D. Winn, L.C. Storoni, and R.J. Read Phaser crystallographic software J. Appl. Crystallogr. 40 2007 658 674 (Pubitemid 47080256)
93. P.D. Adams, P.V. Afonine, G. Bunkoczi, V.B. Chen, I.W. Davis, and N. Echols PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 213 221
94. P. Emsley, B. Lohkamp, W.G. Scott, and K. Cowtan Features and development of Coot Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 486 501
95. J. Painter, and E.A. Merritt Optimal description of a protein structure in terms of multiple groups undergoing TLS motion Acta Crystallogr., Sect. D: Biol. Crystallogr. 62 2006 439 450
96. J. Painter, and E.A. Merritt TLSMD web server for the generation of multi-group TLS models J. Appl. Crystallogr. 39 2006 109 111
97. The PyMOL Molecular Graphics System, Version 1.2r3pre, Schödinger, LLC.