Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA

Science

Volumn 279, Issue 5356, 1998, Pages 1504-1513

  Redinbo, Matthew R ^a   Stewart, Lance ^a   Kuhn, Peter ^a   Champoux, James J ^a   Hol, Wim G J ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

CAMPTOTHECIN; DNA TOPOISOMERASE;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTAL STRUCTURE; DNA HELIX; DNA SEQUENCE; DNA STRAND BREAKAGE; DRUG DNA BINDING; ENZYME ACTIVE SITE; ENZYME STRUCTURE; HUMAN; HUMAN CELL; PRIORITY JOURNAL;

ANTINEOPLASTIC AGENTS, PHYTOGENIC; BINDING SITES; CAMPTOTHECIN; CRYSTALLOGRAPHY, X-RAY; DNA; DNA TOPOISOMERASES, TYPE I; DNA-BINDING PROTEINS; HOMEODOMAIN PROTEINS; HOST CELL FACTOR C1; HUMANS; HYDROGEN BONDING; INTEGRASES; MODELS, MOLECULAR; MUTATION; NUCLEIC ACID CONFORMATION; OCTAMER TRANSCRIPTION FACTOR-1; OLIGODEOXYRIBONUCLEOTIDES; PROTEIN CONFORMATION; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; TRANSCRIPTION FACTORS; TYROSINE;

EID: 0032489634     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.279.5356.1504     Document Type: Article

References (80)

1. J. J. Champoux, in DNA Topology and Its Biological Effects, J. C. Wang and N. R. Cozzarelli, Eds. (Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, 1990), pp. 217-242; J. C. Wang, Annu. Rev. Biochem. 65, 635 (1996); J. J. Champoux, Prog. Nucleic Acids Res. Mol. Biol., in press.
2. J. J. Champoux, in DNA Topology and Its Biological Effects, J. C. Wang and N. R. Cozzarelli, Eds. (Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, 1990), pp. 217-242; J. C. Wang, Annu. Rev. Biochem. 65, 635 (1996); J. J. Champoux, Prog. Nucleic Acids Res. Mol. Biol., in press.
3. J. J. Champoux, in DNA Topology and Its Biological Effects, J. C. Wang and N. R. Cozzarelli, Eds. (Cold Spring Harbor Laboratory, Cold Spring Harbor, NY, 1990), pp. 217-242; J. C. Wang, Annu. Rev. Biochem. 65, 635 (1996); J. J. Champoux, Prog. Nucleic Acids Res. Mol. Biol., in press.
4. N. Lue, A. Sharma, A. Mondragon, J. C. Wang, Structure 3, 1315 (1995).
5. A. Sharma, R. Hanai, A. Mondragon, ibid. 2, 767 (1994).
6. C. D. Lima, J. C. Wang, A. Mondragón, Nature 367, 138 (1994); J. M. Berger, S. J. Gamblin, S. C. Harrison, J. C. Wang, ibid. 380, 179 (1996).
7. C. D. Lima, J. C. Wang, A. Mondragón, Nature 367, 138 (1994); J. M. Berger, S. J. Gamblin, S. C. Harrison, J. C. Wang, ibid. 380, 179 (1996).
8. H.-K. Wang, S. L. Morris-Natschke, K.-H. Lee, Med. Res. Rev. 17, 367 (1997).
9. R. Shaffer and P. Traktman, J. Biol. Chem. 262, 9309 (1987).
10. S. Shuman and B. Moss, Proc. Natl. Acad. Sci. U.S.A. 84, 7478 (1987).
11. M. Gupta, A. Fujimori, Y. Pommier, Biochim. Biophys. Acta 1262, 1 (1995); P. R. Caron and J. C. Wang, Adv. Pharmacol. 29B, 271 (1994).
12. M. Gupta, A. Fujimori, Y. Pommier, Biochim. Biophys. Acta 1262, 1 (1995); P. R. Caron and J. C. Wang, Adv. Pharmacol. 29B, 271 (1994).
13. 2-terminal fragments of the enzyme that do not contain activesite residues or bound DNA.
14. P. D'Arpa et al., Proc. Natl. Acad. Sci. U.S.A. 85, 2543 (1988).
15. L. Stewart, G. C. Ireton, L. H. Parker, K. R. Madden, J. J. Champoux, J. Biol. Chem. 271, 7593 (1996).
16. L. Stewart, G. C. Ireton, J. J. Champoux, ibid., p. 7602.
17. J. Alsner, J. Q. Svejstrup, E. Kjeldsen, B. S. Sorensen, O. Westergaard, ibid. 267, 12408 (1992).
18. A. K. Bharti, M. O. Olson, D. W. Kufe, E. H. Rubin, ibid. 271, 1993 (1996).
19. K. R. Madden and J. J. Champoux, Cancer Res. 52, 525 (1992).
20. L. Stewart, G. C. Ireton, J. J. Champoux, J. Mol. Biol. 269, 355 (1997).
21. The reconstituted enzyme is more sensitive to ionic strength and more distributive in its mode of action than the full-length enzyme (16, 20).
22. M. D. Been, R. R. Burgess, J. J. Champoux, Nucleic Acids Res 12, 3097 (1984).
23. A. H. Andersen, E. Gocke, B. J. Bonven, O. F. Nielsen, O. Westergaard, ibid. 13, 1543 (1985).
24. L. Stewart, M. R. Redinbo, X. Qiu, W. G. J. Hol, J. J. Champoux, Science 279, 1534 (1998).
25. M, E. Wall et al., J. Am. Chem. 88, 3888 (1966); S. B. Horwitz, C. K. Chang, A. P. Grollman, Mol. Pharmacol. 7, 632 (1971).
26. M, E. Wall et al., J. Am. Chem. 88, 3888 (1966); S. B. Horwitz, C. K. Chang, A. P. Grollman, Mol. Pharmacol. 7, 632 (1971).
27. Y. H. Hsiang, R. Hertzberg, S. Hecht, L. F. Liu, J. Biol. Chem. 260, 14873 (1985).
28. M. A. Bjornsti, P. Benedetti, G. A. Viglianti, J. C. Wang, Cancer Res. 49, 6318 (1989).
29. R. P. Hertzberg et al., J. Med. Chem. 32, 715 (1989).
30. S. Sawada et al., Chem. Pharmacol. Bull. 39, 3183 (1991).
31. S. E. Porter and J. J. Champoux, Nucleic Acids Res. 17, 8521 (1989).
32. R. P. Hertzberg, M. J. Caranfa, S. M. Hecht, Biochemistry 28, 4629 (1989); J. Q. Svejstrup, K. Christiansen, I. I. Gromova, A. H. Andersen, O. Westergaard, J. Mol. Biol. 222, 669 (1991).
33. R. P. Hertzberg, M. J. Caranfa, S. M. Hecht, Biochemistry 28, 4629 (1989); J. Q. Svejstrup, K. Christiansen, I. I. Gromova, A. H. Andersen, O. Westergaard, J. Mol. Biol. 222, 669 (1991).
34. R. P. Hertzberg et al., J. Biol. Chem. 265, 19287 (1990).
35. C. Bendixen, B. Thomsen, J. Alsner, O. Westergaard, Biochemistry 29, 5613 (1990).
36. Y. H. Hsiang, M. G. Lihou, L. F. Liu, Cancer Res. 49, 5077 (1989).
37. P. Benedetti, P. Fiorani, L. Capuani, J. C. Wang, ibid. 53, 4343 (1993); A. M. Knab, J. Fertala, M. A. Bjornsti, J. Biol. Chem. 268, 22322 (1993); E. Rubin et al., ibid. 269, 2433 (1994); L. F. Wang et al., Cancer Res. 57, 1516 (1997); H. Tamura et al.. Nucleic Acids Res. 19, 69 (1991); A. Tanizawa etf al., J. Biol. Chem. 268, 25463 (1993); N. Kubota et al., Biochem. Biophys. Res. Commun. 188, 571 (1992); X. G. Li et al., Bioch. Pharmacol. 53, 1019 (1997).
38. P. Benedetti, P. Fiorani, L. Capuani, J. C. Wang, ibid. 53, 4343 (1993); A. M. Knab, J. Fertala, M. A. Bjornsti, J. Biol. Chem. 268, 22322 (1993); E. Rubin et al., ibid. 269, 2433 (1994); L. F. Wang et al., Cancer Res. 57, 1516 (1997); H. Tamura et al.. Nucleic Acids Res. 19, 69 (1991); A. Tanizawa etf al., J. Biol. Chem. 268, 25463 (1993); N. Kubota et al., Biochem. Biophys. Res. Commun. 188, 571 (1992); X. G. Li et al., Bioch. Pharmacol. 53, 1019 (1997).
39. P. Benedetti, P. Fiorani, L. Capuani, J. C. Wang, ibid. 53, 4343 (1993); A. M. Knab, J. Fertala, M. A. Bjornsti, J. Biol. Chem. 268, 22322 (1993); E. Rubin et al., ibid. 269, 2433 (1994); L. F. Wang et al., Cancer Res. 57, 1516 (1997); H. Tamura et al.. Nucleic Acids Res. 19, 69 (1991); A. Tanizawa etf al., J. Biol. Chem. 268, 25463 (1993); N. Kubota et al., Biochem. Biophys. Res. Commun. 188, 571 (1992); X. G. Li et al., Bioch. Pharmacol. 53, 1019 (1997).
40. P. Benedetti, P. Fiorani, L. Capuani, J. C. Wang, ibid. 53, 4343 (1993); A. M. Knab, J. Fertala, M. A. Bjornsti, J. Biol. Chem. 268, 22322 (1993); E. Rubin et al., ibid. 269, 2433 (1994); L. F. Wang et al., Cancer Res. 57, 1516 (1997); H. Tamura et al.. Nucleic Acids Res. 19, 69 (1991); A. Tanizawa etf al., J. Biol. Chem. 268, 25463 (1993); N. Kubota et al., Biochem. Biophys. Res. Commun. 188, 571 (1992); X. G. Li et al., Bioch. Pharmacol. 53, 1019 (1997).
41. P. Benedetti, P. Fiorani, L. Capuani, J. C. Wang, ibid. 53, 4343 (1993); A. M. Knab, J. Fertala, M. A. Bjornsti, J. Biol. Chem. 268, 22322 (1993); E. Rubin et al., ibid. 269, 2433 (1994); L. F. Wang et al., Cancer Res. 57, 1516 (1997); H. Tamura et al.. Nucleic Acids Res. 19, 69 (1991); A. Tanizawa etf al., J. Biol. Chem. 268, 25463 (1993); N. Kubota et al., Biochem. Biophys. Res. Commun. 188, 571 (1992); X. G. Li et al., Bioch. Pharmacol. 53, 1019 (1997).
42. P. Benedetti, P. Fiorani, L. Capuani, J. C. Wang, ibid. 53, 4343 (1993); A. M. Knab, J. Fertala, M. A. Bjornsti, J. Biol. Chem. 268, 22322 (1993); E. Rubin et al., ibid. 269, 2433 (1994); L. F. Wang et al., Cancer Res. 57, 1516 (1997); H. Tamura et al.. Nucleic Acids Res. 19, 69 (1991); A. Tanizawa etf al., J. Biol. Chem. 268, 25463 (1993); N. Kubota et al., Biochem. Biophys. Res. Commun. 188, 571 (1992); X. G. Li et al., Bioch. Pharmacol. 53, 1019 (1997).
43. P. Benedetti, P. Fiorani, L. Capuani, J. C. Wang, ibid. 53, 4343 (1993); A. M. Knab, J. Fertala, M. A. Bjornsti, J. Biol. Chem. 268, 22322 (1993); E. Rubin et al., ibid. 269, 2433 (1994); L. F. Wang et al., Cancer Res. 57, 1516 (1997); H. Tamura et al.. Nucleic Acids Res. 19, 69 (1991); A. Tanizawa etf al., J. Biol. Chem. 268, 25463 (1993); N. Kubota et al., Biochem. Biophys. Res. Commun. 188, 571 (1992); X. G. Li et al., Bioch. Pharmacol. 53, 1019 (1997).
44. P. Benedetti, P. Fiorani, L. Capuani, J. C. Wang, ibid. 53, 4343 (1993); A. M. Knab, J. Fertala, M. A. Bjornsti, J. Biol. Chem. 268, 22322 (1993); E. Rubin et al., ibid. 269, 2433 (1994); L. F. Wang et al., Cancer Res. 57, 1516 (1997); H. Tamura et al.. Nucleic Acids Res. 19, 69 (1991); A. Tanizawa etf al., J. Biol. Chem. 268, 25463 (1993); N. Kubota et al., Biochem. Biophys. Res. Commun. 188, 571 (1992); X. G. Li et al., Bioch. Pharmacol. 53, 1019 (1997).
45. F. Leteurtre et al., J. Biol. Chem. 269, 28702 (1994).
46. The reconstituted enzyme was prepared by incubating crude nuclear extracts containing the 58-kD core domain (expressed in insect cells) with the immobilized glutathione-S-transferase (GST)-COOH-terminal domain fusion protein (expressed in E. coli) (16). The reconstituted core plus COOH-terminal enzyme was liberated by factor Xa cleavage. The reconstituted human topo I was separated from factor Xa and any free GST or COOH-terminal domain by POROS SP20 chromatography as described (16). DNA oligonucleotides were synthesized by DNA express (Fort Collins, CO) and purified as described (11). Oligonucleotides that contained a 5′-bridging phosphorothioate linkage at the site of topo I cleavage were synthesized according to Burgin et al. (34), where 5′-(S-trityl)-mercapto-5′-deoxythymidine-3′-O-(2-cyanoethyl-N, N-diisopropylamino)phosphite was used for the synthesis of the +1 nucleotide in the cleaved strand of the high-affinity topo I binding site from T. thermophilus (79). Duplex oligonucleotides were prepared by mixing equimolar concentrations of complementary strands, each at a final concentration of 0.1 mM, in the presence of 6 mM NaCl. Annealing of the two strands was achieved by slow cooling from 8O°C to room temperature over a period of 8 hours.
47. A. B. Burgin Jr., B. N. Huizenga, H. A. Nash, Nucleic Acids Res. 23, 2973 (1995).
48. E. de La Fortelle and G. Bricogne, Methods Enzymol. 276, 472 (1997).
49. L. Holm and C. Sander, Nucleic Acids Res. 25, 231 (1997).
50. J. D. Klemm, M. A, Rould, R. Aurora, W. Herr, C. Pabo, Cell 77, 21 (1994).
51. A. B. Hickman, S. Waninger, J. J. Scocca, F. Dyda, ibid. 89, 227 (1997).
52. D. Esposito and J. J. Scocca, Nucleic Acids Res. 25, 3605 (1997); HP1 integrase also uses a transient 3′ -phosphate-tyrosine intermediate during its catalytic cycle of integration and excision of the phage DNA and is representative of the family of bacteriophage integrases.
53. C. Jaxel, K. W. Kohn, M. C. Wani, M. E. Wall, Y. Pommier, Cancer Res. 49, 1465 (1989); A. Tanizawa, K. W. Kohn, G. Kohlhagen, F. Leteurtre, Y. Pommier, Biochemistry 34, 7200 (1995).
54. C. Jaxel, K. W. Kohn, M. C. Wani, M. E. Wall, Y. Pommier, Cancer Res. 49, 1465 (1989); A. Tanizawa, K. W. Kohn, G. Kohlhagen, F. Leteurtre, Y. Pommier, Biochemistry 34, 7200 (1995).
55. R. T. Crow and D. M. Crothers, J. Med. Chem. 35, 4160 (1992).
56. M. E. Wall et al., ibid. 36, 2689 (1993).
57. K. Lackey et al., ibid. 38, 906 (1995); W. D. Kingsbury et al., ibid. 34, 98 (1991).
58. K. Lackey et al., ibid. 38, 906 (1995); W. D. Kingsbury et al., ibid. 34, 98 (1991).
59. A. Tanizawa, K. W. Kohn, Y. Pommier, Nucleic Acids Res. 21, 5157 (1993); E. Kjeldsen et al., J. Mol. Biol. 202, 333 (1988).
60. A. Tanizawa, K. W. Kohn, Y. Pommier, Nucleic Acids Res. 21, 5157 (1993); E. Kjeldsen et al., J. Mol. Biol. 202, 333 (1988).
61. Y. Pommier et al., Proc. Natl Acad. Sci. U.S.A. 92, 8861 (1995).
62. A. T. McPhail and G. A. Sim, J. Chem. Soc. B, 923 (1968).
63. Z. Otwinowski and W. Minor, Eds., Data Collection and Processing (Daresbury, UK, 1993).
64. Z. Otwinowski, in ibid., pp. 80-86.
65. K. Cowtan, Joint CCP4 and ESF-EACBM Newslett. Protein Crystallogr. 31, 34 (1994).
66. J. P. Abrahams and A. G. W. Leslie, Acte Crystallogr. D52, 30 (1996).
67. T. A. Jones, J.-Y. Zou, S. W. Cowan, ibid. A47, 110 (1991).
68. J. Navaza, ibid. A50, 157 (1994).
69. A. T. Brunger, X-PLOR (Version 3. 1): A System for X-ray Crystallography and NMR (Yale Univ. Press, New Haven, CT, 1993).
70. _, J, Mol. Biol. 203, 803 (1988).
71. _, Nature 355, 472 (1992).
72. R. J. Read, Acta Crystallogr. A42, 140 (1986).
73. J. M. Moore, W. J. Chazin, R. Powls, P. E. Wright, Biochemistry 27, 7806 (1988).
74. P. J. Kraulis, J. Appl. Crystallogr. 24, 946 (1991).
75. D. J. Bacon and W. F. Andersen, J. Mol. Graphics 6, 219 (1988); E. A. Merritt and M. E. P. Murphy, Acta Crystallogr. D50, 869 (1994).
76. D. J. Bacon and W. F. Andersen, J. Mol. Graphics 6, 219 (1988); E. A. Merritt and M. E. P. Murphy, Acta Crystallogr. D50, 869 (1994).
77. A. Nicholls, K. A. Sharp, B. Honig, Proteins Struct. Funct. Genet. 11, 282 (1991).
78. G. J. Barton, Protein Eng. 6, 37 (1993).
79. L. Joshua-Tor et al., J. Mol. Biol. 225, 397 (1992).
80. We thank S. Turley, E. Pohl, S. Suresh, B. Bernstein, A. Ævarsson, D. Chudzik, J. Yeh, F. Athappilly, F. van den Akker, C. Verlinde, and many other members of the Biomolecular Structure Center at the University of Washington for technical assistance and intellectual support. We also thank the staffs of the Stanford Synchrotron Radiation Laboratory, the Brookhaven National Laboratory, the Cornell High Energy Synchrotron Source, and the European Synchrotron Radiation Laboratory for their extensive support with data collection. Thanks are also due to A. Burgin for advice on the synthesis of oligonucleotides containing a 5′-bridging phosphorothioate, and to DNA Express (Fort Collins, CO) for conducting the syntheses. Supported by American Cancer Society grant PF-3905 (L.S.), grant GM49156 from the National Institutes of Health (J.J.C.), by a major equipment grant from the Murdock Charitable Trust to the Biomolecular Structure Center, and grant NCI CA65656 from the National Institutes of Health (W.G.J.H.). The Stanford Synchrotron Radiation Laboratory is founded by the Department of Energy (BES, OBER) and the NIH (NCRR).