Hypersensitivity of Ku-deficient cells toward the DNA topoisomerase II inhibitor ICRF-193 suggests a novel role for Ku antigen during the G2 and M phases of the cell cycle

Molecular and Cellular Biology

Volumn 18, Issue 10, 1998, Pages 5797-5808

  Muñoz, Purificación ^a   Zdzienicka, Malgorzata Z ^b   Blanchard, Jean Marie ^a   Piette, Jacques ^a  

^a CNRS   (France)

^b LEIDEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

GYRASE INHIBITOR;

ANIMAL CELL; ANTIGEN RECOGNITION; ARTICLE; CELL CYCLE G2 PHASE; CELL MUTANT; CHINESE HAMSTER; DNA REPAIR; DNA REPLICATION; DNA STRUCTURE; ENZYME ACTIVITY; ENZYME INHIBITION; GENETIC COMPLEMENTATION; GENETIC RECOMBINATION; HYPERSENSITIVITY; NONHUMAN; PRIORITY JOURNAL; RECEPTOR GENE;

ANIMALIA; CRICETINAE; CRICETULUS GRISEUS;

EID: 0031656232     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.18.10.5797     Document Type: Article

References (77)

1. Adachi, Y., E. Kas, and U. K. Laemmli. 1989. Preferential, cooperative binding of DNA topoisomerase II to scaffold-associated regions. EMBO J. 8:3997-1006.
2. Adachi, Y., M. Luke, and U. K. Laemmli. 1991. Chromosome assembly in vitro: topoisomerase II is required for condensation. Cell 64:137-148.
3. Anderson, C. W., and S. P. Lees-Miller. 1992. The nuclear serine/threonine protein kinase DNA-PK. Crit. Rev. Eukaryot. Gene Expr. 2:283-314.
4. Anderson, H., and M. Roberge. 1996. Topoisomerase II inhibitors affect entry into mitosis and chromosome condensation in BHK cells. Cell Growth Differ. 7:83-90.
5. Andoh, T., M. Sato, T. Narita, and R. Ishida. 1993. Role of DNA topoisomerase II in chromosome dynamics in mammalian cells. Biotechnol. Appl. Biochem. 18:165-174.
6. Andreassen, P. R., F. B. Lacroix, and R. L. Margolis. 1997. Chromosomes with two intact axial cores are induced by G2 checkpoint override: evidence that DNA decatenation is not required to template the chromosome structure. J. Cell Biol. 136:29-43.
7. Blunt, T., N. J. Finnie, G. E. Taccioli, G. C. Smith, J. Demengeot, T. M. Gottlieb, R. Mizuta, A. J. Varghese, F. W. Alt, P. A. Jeggo, et al. 1995. Defective DNA-dependent protein kinase activity is linked to V(D)J recombination and DNA repair detects associated with the murine acid mutation. Cell 80:813-823.
8. Bosma, G. C., R. P. Custer, and M. J. Bosma. 1983. A severe combined immunodeficiency mutation in the mouse. Nature 301:527-530.
9. Boubnov, N. V., K. T. Hall, Z. Wills, S. E. Lee, D. M. He, D. M. Benjamin, C. R. Pulaski, H. Band, W. Reeves, E. A. Hendrickson, and D. T. Weaver. 1995. Complementation of the ionizing radiation sensitivity, DNA end binding and V(D)J recombination defects of double-strand break repair mutants by the p86 Ku autoantigen. Proc. Natl. Acad. Sci. USA 92:890-894.
10. Brush, G. S., C. W. Anderson, and T. J. Kelly. 1994. The DNA-activated protein kinase is required for the phosphorylation of replication protein A during simian virus 40 DNA replication. Proc. Natl. Acad. Sci. USA 91:12520-12524.
11. Cao, Q. P., S. Pitt, J. Leskyk, and E. F. Baril. 1994. DNA-dependent ATPase from HeLa cells is related to human Ku antigen. Biochemistry 33:8548-8557.
12. Carter, T., I. Vancurova, I. Sun, W. Lou, and S. DeLeon. 1990. A DNA-activated protein kinase from HeLa cell nuclei. Mol. Cell. Biol. 10:6460-6471.
13. Chaly, N., X. Chen, J. Dentry, and D. L. Brown. 1996. Organization of DNA topoisomerase II isotypes during the cell cycle of human lymphocytes and HeLa cells. Chromosome Res. 4:457-466.
14. Chen, A. Y., and L. F. Liu. 1994. DNA topoisomerase: essential enzymes and lethal targets. Annu. Rev. Pharmacol. Toxicol. 36:191-218.
15. Chen, F., S. R. Peterson, M. D. Story, and D. J. Chen. 1996. Disruption of DNA-PK in Ku80 mutant xrs-6 and the implications in DNA double-strand break repair. Mutat. Res. 362:9-19.
16. Chen, M., and W. T. Beck. 1993. Teniposide-resistant CEM cells, which express mutant DNA topoisomerase II alpha, when treated with non-complex-stabilizing inhibitors of the enzyme, display no cross-resistance and reveal aberrant functions of the mutant enzyme. Cancer Res. 53:5946-5953.
17. Clarke, D. J., R. T. Johnson, and C. S. Downes. 1993. Topoisomerase II inhibition prevents anaphase chromatid segregation in mammalian cells in-dependently of the generation of DNA strand breaks. J. Cell Sci. 105:563-569.
18. Cockerill, P. N., and W. T. Garrard. 1986. Chromosomal loop anchorage of the kappa immunoglobulin gene occurs next to the enhancer in a region containing topoisomerase II sites. Cell 44:273-282.
19. DeVore, R. F., A. H. Corbett, and N. Osheroff. 1992. Phosphorylation of topoisomerase II by casein kinase II and protein kinase C: effects on enzyme-mediated DNA cleavage/religation and sensitivity to the antineoplastic drugs etoposide and 4′-(9-acridinylamino)methane-sulfon-m-anisidide. Cancer Res. 52:2156-2161.
20. Dorr, R. T. 1992. Bleomycin pharmacology: mechanism of action and resistance, and clinical pharmacokinetics. Semin. Oncol. 19:3-8.
21. Downes, C. S., D. J. Clarke, A. M. Mullinger, J. F. Gimenez-Abian, A. M. Creighton, and R. T. Johnson. 1994. A topoisomerase II-dependent G2 cycle checkpoint in mammalian cells. Nature 372:467-470. (Erratum, 372:710.)
22. Dvir, A., S. R. Peterson, M. W. Knuth, H. Lu, and W. S. Dynan. 1992. Ku autoantigen is the regulatory component of a template-associated protein kinase that phosphorylates RNA polymerase II. P roc. Natl. Acad. Sci. USA 89:11920-11924.
23. Earnshaw, W. C., B. Halligan, C. A. Cooke, M. M. Heck, and L. F. Liu. 1985. Topoisomerase II is a structural component of mitotic chromosome scaffolds. J. Cell Biol. 100:1706-1715.
24. Errami, A., D. M. He, A. A. Friedl, W. J. I. Overkamp, B. Morolli, E. A. Hendrickson, F. Eekardt-Schupp, M. Oshimura, P. H. M. Lohman, S. P. Jackson, and M. Z. Zdzienicka. 1998. XR-C1, a new CHO cell mutant which is defective in DNA-PKcs, is impaired in both V(D)J coding and signal joint formation. Nucleic Acids Res. 26:3146-3153.
25. Errami, A., V. Smider, W. K. Rathmell, D. M. He, E. A. Hendrickson, M. Z. Zdzienicka, and G. Chu. 1996. Ku86 defines the genetic defect and restores X-ray resistance and V(D)J recombination to complementation group 5 hamster cell mutants. Mol. Cell. Biol. 16:1519-1526.
26. Gasser, S. M., T. Laroche, J. Falquet, E. Boy de la Tour, and U. K. Laemmli. 1986. Metaphase chromosome structure. Involvement of topoisomerase II. J. Mol. Biol. 188:613-629.
27. Giffin, W., J. Kwast-Welfeld, D. J. Rodda, G. G. Prefontaine, M. Traykova-Andonova, Y. Zhang, N. L. Weigel, Y. A. Lefebvre, and R. J. Hache. 1997. Sequence-specific DNA binding and transcription factor phosphorylation by Ku autoantigen/DNA-dependent protein kinase. Phosphorylation of Ser-527 of the rat glucocorticoid receptor. J. Biol. Chem. 272:5647-5658.
28. Gottlieb, T. M., and S. P. Jackson. 1993. The DNA-dependent protein kinase: requirement for DNA ends and association with Ku antigen. Cell 72:131-142.
29. He, D. M., S. E. Lee, and E. A. Hendrickson. 1996. Restoration of X-ray and etoposide resistance, Ku-end binding activity and V(D) J recombination to the Chinese hamster sxi-3 mutant by a hamster Ku86 cDNA. Mutat. Res. 363:43-56.
30. Hirano, T., and T. J. Mitchison. 1993. Topoisomerase II does not play a scaffolding role in the organization of mitotic chromosomes assembled in Xenopus egg extracts. J. Cell Biol. 120:601-612.
31. Holm, C., T. Goto, J. C. Wang, and D. Botstein. 1985. DNA topoisomerase II is required at the time of mitosis in yeast. Cell 41:553-563.
32. Huang, L. C., K. C. Clarkin, and G. M. Wahl. 1996. P53-dependent cell cycle arrests are preserved in DNA-activated protein kinase-deficient mouse fibroblasts. Cancer Res. 56:2940-2944.
33. Ishida, R., T. Miki, T. Narita, R. Yui, M. Sato, K. R. Utsumi, K. Tanabe, and T. Andoh. 1991. Inhibition of intracellular topoisomerase II by antitumor bis(2,6-dioxopiperazine) derivatives: mode of cell growth inhibition distinct from that of cleavable complex-forming type inhibitors. Cancer Res. 51:4909-4916.
34. Ishida, R., M. Sato, T. Narita, K. R. Utsumi, T. Nishimoto, T. Morita, H. Nagata, and T. Andoh. 1994. Inhibition of DNA topoisomerase II by ICRF-193 induces polyploidization by uncoupling chromosome dynamics from other cell cycle events. J. Cell Biol. 126:1341-1351.
35. Jackson, S. P., and P. A. Jeggo. 1995. DNA double-strand break repair and V(D)J recombination: involvement of DNA-PK. Trends Biochem. Sci. 20:412-115.
36. Jeggo, P. A., K. Caldecott, S. Pidsley, and G. R. Banks. 1989. Sensitivity of Chinese hamster ovary mutants defective in DNA double strand break repair to topoisomerase' II inhibitors. Cancer Res. 49:7057-7063.
37. Kimura, K., N. Nozaki, T. Enomoto, M. Tanaka, and A. Kikuchi. 1996. Analysis of M phase-specific phosphorylation of DNA topoisomerase II. J. Biol. Chem. 271:21439-21445.
38. Kimura, K., M. Saijo, M. Ui, and T. Enomoto. 1994. Growth state- and cell cycle-dependent fluctuation in the expression of two forms of DNA topoisomerase II and possible specific modification of the higher molecular weight form in the M phase. J. Biol. Chem. 269:1173-1176.
39. Kuhn, A., T. M. Gottlieb, S. P. Jackson, and I. Grummt. 1995. DNA-dependent protein kinase: a potent inhibitor of transcription by RNA polymerase I. Genes Dev. 9:193-203.
40. Kysela, B. P., B. D. Michael, and J. E. Arrand. 1993. Relative contributions of levels of initial DNA damage and repair of double strand breaks to the ionizing radiation-sensitive phenotype of the Chinese hamster cell mutant, XR-V15B. Pan I. X-rays. Int. J. Radiat. Biol. 63:609-616.
41. Labhart, P. 1995. DNA-dependent protein kinase specifically represses promoter-directed transcription initiation by RNA polymerase I. Proc. Natl. Acad. Sci. USA 92:2934-2938.
42. Lee, S. E., R. A. Mitchell, A. Cheng, and E. A. Hendrickson. 1997. Evidence for DNA-PK-dependent and -independent DNA double-strand break repair pathways in mammalian cells as a function of the cell cycle. Mol. Cell. Biol. 17:1425-1433.
43. Lees-Miller, S. P., Y. R. Chen, and C. W. Anderson. 1990. Human cells contain a DNA-activated protein kinase that phosphorylates simian virus 40 T antigen, mouse p53, and the human Ku autoantigen. Mol. Cell. Biol. 10:6472-6481.
44. Liu, L. F. 1989. DNA topoisomerase poisons as antitumor drugs. Annu. Rev. Biochem. 58:351-375.
45. Meyer, K. N., E. Kjeldsen, T. Straub, B. R. Knudsen, I. D. Hickson, A. Kikuchi, H. Kreipe, and F. Boege. 1997. Cell cycle-coupled relocation of types I and II topoisomerases and modulation of catalytic enzyme activities. J. Cell Biol. 136:775-788.
46. Mimori, T., and J. A. Hardin. 1986. Mechanism of interaction between Ku protein and DNA. J. Biol. Chem. 261:10375-10379.
47. Mimori, T., J. A. Hardin, and J. A. Steitz. 1986. Characterization of the DNA-binding protein antigen Ku recognized by autoantibodies from patients with rheumatic disorders. J. Biol. Chem. 261:2274-2278.
48. Morozov, V. E., M. Falzon, C. W. Anderson, and E. L. Kuff. 1994. DNA-dependent protein kinase is activated by nicks and larger single-stranded gaps. J. Biol. Chem. 269:16684-16688.
49. Newport, J. 1987. Nuclear reconstitution in vitro: stages of assembly around protein-free DNA. Cell 48:205-207.
50. Newport, J., and T. Spann. 1987. Disassembly of the nucleus in mitotic extracts: membrane vesicularization, lamin disassembly, and chromosome condensation are independent processes. Cell 48:219-230.
51. Nussenzweig, A., C. Chen, V. da Costa Soares, M. Sanchez, K. Sokol, M. C. Nussenzweig, and G. C. Li. 1996. Requirement for Ku80 in growth and immunoglobulin V(D)J recombination. Nature 382:551-555.
52. Pan, Z. Q., A. A. Amin, E. Gibbs, H. Niu, and J. Hurwitz. 1994. Phosphorylation of the p34 subunit of human single-stranded-DNA-binding protein in cyclin A-activated G1 extracts is catalyzed by cdk-cyclin A complex and DNA-dependent protein kinase. Proc. Natl. Acad. Sci. USA 91:8343-8347.
53. Pommier, Y., F. Leteurtre, M. R. Fesen, A. Fujimori, R. Bertrand, E. Solary, G. Kolhagen, and K. W. Kohn. 1994. Cellular determinants of sensitivity and resistance to DNA topoisomerase inhibitors. Cancer Investig. 12:530-542.
54. Roca, J., R. Ishida, J. M. Berger, T. Andoh, and J. C. Wang. 1994. Antitumor bisdioxopiperazines inhibit yeast DNA topoisomerase II by trapping the enzyme in the form of a closed protein clamp. Proc. Natl. Acad. Sci. USA 91:1781-1785.
55. Schwartz, J. L., J. M. Cowen, E. Moan, B. A. Sedita, J. Stephens, and A. T. Vaughan. 1993. Metaphase chromosome and nucleoid differences between CHO-K1 and its radiosensitive derivative xrs-5. Mutagenesis 8:105-108.
56. Sipley, J. U., J. C. Menninger, K. O. Hartley, D. C. Ward, S. P. Jackson, and C. W. Anderson. 1995. Gene for the catalytic subunit of the human DNA-activated protein kinase maps to the site of the XRCC7 gene on chromosome 8. Proc. Natl. Acad. Sci. USA 92:7515-7519.
57. Smider, V., W. K. Rathmell, M. R. Lieber, and G. Chu. 1994. Restoration of X-ray resistance and V(D)J recombination in mutant cells by Ku cDNA. Science 266:288-291.
58. Strick, R., and L. K. Laemmli. 1995. SARs are cis DNA elements of chromosome dynamics: synthesis of a SAR repressor protein. Cell 83:1137-1148.
59. Taccioli, G. E., T. M. Gottlieb, T. Blunt, A. Priestley, J. Demengeot, R. Mizuta, A. R. Lehmann, F. W. Alt, S. P. Jackson, and P. A. Jeggo. 1994. Ku80: product of the XRCC5 gene and its role in DNA repair and V(D)J recombination. Science 265:1442-1445.
60. Takano, H., K. Kohno, M. Ono, Y. Uchida, and M. Kuwano. 1991. Increased phosphorylation of DNA topoisomerase II by antitumor agents bis(2,6-dioxopiperazine) derivatives. Cancer Res. 51:3951-3957.
61. Tanabe, K., Y. Ikegami, R. Ishida, and T. Andoh. 1991. Inhibition of topoisomerase II by antitumor agents bis(2,6-dioxopiperazine) derivatives. Cancer Res. 51:4903-4908.
62. Tuteja, N., R. Tuteja, A. Ochem, P. Taneja, N. W. Huang, A. Simoncsits, S. Susic, K. Rahman, L. Marusic, J. Chen, J. Zhang, S. Wang, S. Pongor, and A. Falaschi. 1994. Human DNA helicase II: a novel DNA unwinding enzyme identified as the Ku autoantigen. EMBO J. 13:4991-5001.
63. Uemura, T., H. Ohkura, Y. Adachi, K. Morino, K. Shiozaki, and M. Yanagida. 1987. DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe. Cell 50:917-925.
64. Vassetzky, Y. S., Q. Dang, P. Benedetti, and S. M. Gasser. 1994. Topoisomerase II forms multimers in vitro: effects of metals, beta-glycerophosphate, and phosphorylation of its C-terminal domain. Mol. Cell. Biol. 14:6962-6974.
65. Wang, J. C. 1996. DNA topoisomerases. Annu. Rev. Biochem. 65:635-692.
66. Warters, R. L., B. W. Lyons, T. M. Li, and D. J. Chen. 1991. Topoisomerase II activity in DNA double-strand break repair deficient Chinese hamster ovary cell line. Mutat. Res. 254:167-174.
67. Watt, P. M., and I. D. Hickson. 1994. Structure and function of type II DNA topoisomerase. Biochem. J. 303:681-695.
68. Watt, P. M., E. J. Louis, R. H. Borts, and I. D. Hickson. 1995. Sgs1: a eukaryotic homolog of E. coli RecQ that interacts with topoisomerase II in vivo and is required for faithful chromosome segregation. Cell 81:253-260.
69. Weaver, D. T. 1996. Regulation and repair of double-strand DNA breaks. Crit. Rev. Eukaryot. Gene Expr. 6:345-375.
70. Wiler, R., R. Leber, B. B. Moore, L. F. Van Dyk, L. E. Ferryman, and K. Meek. 1995. Equine severe combined immunodeficiency: a defect in V(D)J recombination and DNA-dependent protein kinase activity. Proc. Natl. Acad. Sci. USA 92:11485-11489.
71. Woessner, R. D., M. R. Mattern, C. K. Mirabelli, R. K. Johnson, and F. H. Drake. 1991. Proliferation- and cell cycle-dependent differences in expression of the 170 kilodalton and 180 kilodalton forms of topoisomerase II in NIH-3T3 cells. Cell Growth Differ. 2:209-214.
72. Yasui, L. S., T. J. Fink, and A. M. Enrique. 1994. Nuclear scaffold organization in the X-ray sensitive Chinese hamster mutant cell line, xrs-5. Int. J. Radiat. Biol. 65:185-192.
73. Yasui, L. S., L. Ling-Indeck, B. Johnson-Wint, T. J. Fink, and D. Molsen. 1991. Changes in the nuclear structure in the radiation-sensitive CHO mutant cell, xrs-5. Radiat. Res. 127:269-277.
74. Yonish-Rouach, Y., J. Borde, M. Gotteland, Z. Mishal, A. Viron, and E. May. 1994. Induction of apoptosis by transiently transfected metabolically stable wt p53 in transformed cell lines. Cell Death Differ. 1:39-47.
75. Zdzienicka, M. Z. 1995. Mammalian mutants defective in the response to ionizing radiation-induced DNA damage. Mutat. Res. 336:203-213.
76. Zdzienicka, M. Z., Q. Tran, G. P. van der Schans, and J. W. Simons. 1988. Characterization of an X-ray-hypersensitive mutant of V79 Chinese hamster cells. Mutat. Res. 194:239-249.
77. Zhu, C., M. A. Bogue, D. S. Lim, P. Hasty, and D. B. Roth. 1996. Ku86-deficient mice exhibit severe combined immunodeficiency and defective processing of V(D)J recombination intermediates. Cell 86:379-389.