Construction, characterization, and complementation of a conditional-lethal DNA topoisomerase IIα mutant human cell line

Molecular Biology of the Cell

Volumn 15, Issue 12, 2004, Pages 5700-5711

  Carpenter, Adam J ^a   Porter, Andrew C G ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA TOPOISOMERASE (ATP HYDROLYSING); GREEN FLUORESCENT PROTEIN; GYRASE INHIBITOR; TETRACYCLINE;

ANAPHASE; ARTICLE; CELL MUTANT; CHROMOSOME CONDENSATION; CHROMOSOME SEGREGATION; CHROMOSOME STRUCTURE; CONTROLLED STUDY; CYTOKINESIS; GENE SILENCING; GENETIC COMPLEMENTATION; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; MITOSIS; POLYMERASE CHAIN REACTION; POLYPLOIDY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RIBONUCLEASE PROTECTION ASSAY; RNA INTERFERENCE;

ANTIGENS, NEOPLASM; APOPTOSIS; CELL LINE; CELL NUCLEUS; CHROMOSOMES, HUMAN; DNA TOPOISOMERASES, TYPE II, EUKARYOTIC; DNA-BINDING PROTEINS; DOXYCYCLINE; GENE DELETION; GENES, LETHAL; GENETIC COMPLEMENTATION TEST; HUMANS; MITOSIS; MUTATION; PHOSPHORYLATION; POLYPLOIDY; SERINE; TYROSINE;

MAMMALIA;

EID: 9444229370     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-08-0732     Document Type: Article

References (64)

1. Adachi, N., Suzuki, H., Iiizumi, S., and Koyama, H. (2003). Hypersensitivity of nonhomologous DNA end-joining mutants to VP-16 and ICRF-193, implications for the repair of topoisomerase II-mediated DNA damage. J. Biol. Chem. 278, 35897-35902.
2. Adachi, Y., Luke, M., and Laemmli, U.K. (1991). Chromosome assembly in vitro: topoisomerase II is required for condensation. Cell 64, 137-148.
3. Agostinho, M., Rino, J., Braga, J., Ferreira, F., Steffensen, S., and Ferreira, J. (2004). Human topoisomerase IIalpha: targeting to subchromosomal sites of activity during interphase and mitosis. Mol. Biol. Cell 15, 2388-2400.
4. Akimitsu, N., Adachi, N., Hirai, H., Hossain, M.S., Hamamoto, H., Kobayashi, M., Aratani, Y., Koyama, H., and Sekimizu, K. (2003). Enforced cytokinesis without complete nuclear division in embryonic cells depleting the activity of DNA topoisomerase IIalpha. Genes Cells 8, 393-402.
5. Andersen, C.L., Wandall, A., Kjeldsen, E., Mielke, C., and Koch, J. (2002). Active, but not inactive, human centromeres display topoisomerase II activity in vivo. Chromosome Res. 10, 305-312.
6. Andoh, T., Sato, M., Narita, T., and Ishida, R. (1993). Role of DNA topoisomerase II in chromosome dynamics in mammalian cells. Biotechnol. Appl. Biochem. 18, 165-174.
7. Andreassen, P.R., Lacroix, F.B., and Margolis, R.L. (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.
8. Bachant, J., Alcasabas, A., Blat, Y., Kleckner, N., and Elledge, S.J. (2002). The SUMO-1 isopeptidase Smt4 is linked to centromeric cohesion through SUMO-1 modification of DNA topoisomerase II. Mol. Cell 9, 1169-1182.
9. Bernard, P., and Allshire, R. (2002). Centromeres become unstuck without heterochromatin. Trends Cell Biol. 12, 419-424.
10. Chang, C.J., Goulding, S., Earnshaw, W.C., and Carmena, M. (2003). RNAi analysis reveals an unexpected role for topoisomerase II in chromosome arm congression to a metaphase plate. J. Cell Sci. 116, 4715-4726.
11. Chikamori, K., et al. (2003). Phosphorylation of serine 1106 in the catalytic domain of topoisomerase II alpha regulates enzymatic activity and drug sensitivity. J. Biol. Chem. 278, 12696-12702.
12. Christensen, M.O., et al. (2002). Dynamics of human DNA topoisomerases IIalpha and IIbeta in living cells. J. Cell Biol. 157, 31-44.
13. Crosio, C., Fimia, G.M., Loury, R., Kimura, M., Okano, Y., Zhou, H., Sen, S., Allis, C.D., and Sassone-Corsi, P. (2002). Mitotic phosphorylation of histone H3, spatio-temporal regulation by mammalian Aurora kinases. Mol. Cell. Biol. 22, 874-885.
14. Deming, P.B., Cistulli, C.A., Zhao, H., Graves, P.R., Piwnica-Worms, H., Paules, R.S., Downes, C.S., and Kaufmann, W.K. (2001). The human decatenation checkpoint. Proc. Natl. Acad. Sci. USA 98, 12044-12049.
15. Downes, C.S., Clarke, D.J., Mullinger, A.M., Gimenez-Abian, J.F., Creighton, A.M., and Johnson, R.T. (1994). A topoisomerase II-dependent G2 cycle checkpoint in mammalian cells. Nature 372, 467-470.
16. Downes, C.S., Mullinger, A.M., and Johnson, R.T. (1991). Inhibitors of DNA topoisomerase II prevent chromatid separation in mammalian cells but do not prevent exit from mitosis. Proc. Natl. Acad. Sci. USA 88, 8895-8899.
17. Floridia, G., Zatterale, A., Zuffardi, O., and Tyler-Smith, C. (2000). Mapping of a human centromere onto the DNA by topoisomerase II cleavage. EMBO Rep. 1,489-493.
18. Gimenez-Abian, J.F., Clarke, D.J., Devlin, J., Gimenez-Abian, M.I., De la Torre, C., Johnson, R.T., Mullinger, A.M., and Downes, C.S. (2000). Premitotic chromosome individualization in mammalian cells depends on topoisomerase II activity. Chromosoma 109, 235-244.
19. Gimenez-Abian, J.F., Clarke, D.J., Mullinger, A.M., Downes, C.S., and Johnson, R.T. (1995). A postprophase topoisomerase II-dependent chromatid core separation step in the formation of metaphase chromosomes. J. Cell Biol. 131, 7-17.
20. Gorbsky, G.J. (1994). Cell cycle progression and chromosome segregation in mammalian cells cultured in the presence of the topoisomerase II inhibitors ICRF-187 [(+)-1,2-bis(3,5-dioxopiperazinyl-1-yl)propane; ADR-529] and ICRF-159 (Razoxane). Cancer Res. 54, 1042-1048.
21. Gossen, M., Bonin, A.L., Freundlieb, S., and Bujard, H. (1994). Inducible gene expression systems for higher eukaryotic cells. Curr. Opin. Biotechnol. 5, 516-520.
22. Haraguchi, T., et al. (2000). Live fluorescence imaging reveals early recruitment of emerin, LBR, RanBP2, and Nup153 to reforming functional nuclear envelopes. J. Cell Sci. 113, 779-794.
23. Hart, C.M., and Laemmli, U.K. (1998). Facilitation of chromatin dynamics by SARs. Curr. Opin. Genet. Dev. 8, 519-525.
24. Hirano, T. (2000). Chromosome cohesion, condensation, and separation. Annu. Rev. Biochem. 69, 115-144.
25. Hirano, T., and Mitchison, T.J. (1991). Cell cycle control of higher-order chromatin assembly around naked DNA in vitro. J. Cell Biol. 115, 1479-1489.
26. Hirano, T., and Mitchison, T.J. (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.
27. Holm, C., Goto, T., Wang, J.C., and Botstein, D. (1985). DNA topoisomerase II is required at the time of mitosis in yeast. Cell 41, 553-563.
28. Huang, K.C., Gao, H., Yamasaki, E.F., Grabowski, D.R., Liu, S., Shen, L.L., Chan, K.K., Ganapathi, R., and Snapka, R.M. (2001). Topoisomerase II poisoning by ICRF-193. J. Biol. Chem. 276, 44488-44494.
29. Hudson, D.F., Morrison, C., Ruchaud, S., and Earnshaw, W.C. (2002). Reverse genetics of essential genes in tissue-culture cells: 'dead cells talking'. Trends Cell Biol. 12, 281-287.
30. Hudson, D.F., Vagnarelli, P., Gassmann, R., and Earnshaw, W.C. (2003). Condensin is required for nonhistone protein assembly and structural integrity of vertebrate mitotic chromosomes. Dev. Cell. 5, 323-336.
31. Isaacs, R.J., Davies, S.L., Sandri, M.I., Redwood, C., Wells, N.J., and Hickson, I.D. (1998). Physiological regulation of eukaryotic topoisomerase II. Biochim. Biophys. Acta 1400, 121-137.
32. Ishida, R., Miki, T., Narita, T., Yui, R., Sato, M., Utsumi, K.R., Tanabe, K., and Andoh, T. (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.
33. Ishida, R., Sato, M., Narita, T., Utsumi, K.R., Nishimoto, T., Morita, T., Nagata, H., and Andoh, T. (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.
34. Itzhaki, J.E., Gilbert, C.S., and Porter, A.C.G. (1997). Construction by gene targeting in human cells of a 'conditional' CDC2 mutant that rereplicates its DNA. Nat. Genet. 15, 258-265.
35. Itzhaki, J.E., and Porter, A.C.G. (1991). Targeted disruption of a human interferon-inducible gene detected by secretion of human growth hormone. Nucleic Acids Res. 19, 3835-3842.
36. Jensen, S., Redwood, C.S., Jenkins, J.R., Andersen, A.H., and Hickson, I.D. (1996). Human DNA topoisomerases II alpha and II beta can functionally substitute for yeast TOP2 in chromosome segregation and recombination. Mol. Gen. Genet. 252, 79-86.
37. Khelifa, T., Casabianca-Pignede, M.R., Rene, B., and Jacquemin-Sablon, A. (1994). Expression of topoisomerases II alpha and beta in Chinese hamster lung cells resistant to topoisomerase II inhibitors. Mol. Pharmacol. 46, 323-328.
38. Kobayashi, M., Adachi, N., Aratani, Y., Kikuchi, A., and Koyama, H. (2001). Decreased topoisomerase IIalpha expression confers increased resistance to ICRF-193 as well as VP-16 in mouse embryonic stem cells. Cancer Lett. 166, 71-77.
39. Koshland, D., and Strunnikov, A. (1996). Mitotic chromosome condensation. Annu. Rev. Cell Dev. Biol. 12, 305-333.
40. Lavoie, B.D., Hogan, E., and Koshland, D. (2002). In vivo dissection of the chromosome condensation machinery: reversibility of condensation distinguishes contributions of condensin and cohesin. J. Cell Biol. 156, 805-815.
41. Losada, A., and Hirano, T. (2001). Shaping the metaphase chromosome: coordination of cohesion and condensation. Bioessays 23, 924-935.
42. Mirkovitch, J., Gasser, S.M., and Laemmli, U.K. (1988). Scaffold attachment of DNA loops in metaphase chromosomes. J. Mol. Biol. 200, 101-109.
43. Nasmyth, K. (2002). Segregating sister genomes: the molecular biology of chromosome separation. Science 297, 559-565.
44. Newport, J., and Spann, T. (1987). Disassembly of the nucleus in mitotic extracts: membrane vesicularization, lamin disassembly, and chromosome condensation are independent processes. Cell 48, 219-230.
45. Porter, A. (1998). Controlling your losses: conditional gene silencing in mammals. Trends Genet. 14, 73-79.
46. Porter, A.C.G., Chernajovsky, Y., Dale, T.C., Gilbert, C.S., Stark, G.R., and Kerr, I.M. (1988). Interferon response element of the human gene 6-16. EMBO J. 7, 85-92.
47. Rattner, J.B., Hendzel, M.J., Furbee, C.S., Muller, M.T., and Bazett-Jones, D.P. (1996). Topoisomerase II alpha is associated with the mammalian centromere in a cell cycle- and species-specific manner and is required for proper centromere/kinetochore structure. J. Cell Biol. 134, 1097-1107.
48. Sakaguchi, A., and Kikuchi, A. (2004). Functional compatibility between isoform alpha and beta of type II DNA topoisomerase. J. Cell Sci. 117, 1047-1054.
49. Sarkaria, J.N., Busby, E.C., Tibbetts, R.S., Roos, P., Taya, Y., Karnitz, L.M., and Abraham, R.T. (1999). Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res. 59, 4375-4382.
50. Spence, J.M., Critcher, R., Ebersole, T.A., Valdivia, M.M., Earnshaw, W.C., Fukagawa, T., and Farr, C.J. (2002). Co-localization of centromere activity, proteins and topoisomerase II within a subdomain of the major human X alpha-satellite array. EMBO J. 21, 5269-5280.
51. Sumner, A.T. (1996). The distribution of topoisomerase II on mammalian chromosomes. Chromosome Res. 4, 5-14.
52. Swedlow, J.R., and Hirano, T. (2003). The making of the mitotic chromosome: modern insights into classical questions. Mol. Cell 11, 557-569.
53. Tavormina, P.A., Come, M.G., Hudson, J.R., Mo, Y.Y., Beck, W.T., and Gorbsky, G.J. (2002). Rapid exchange of mammalian topoisomerase II alpha at kinetochores and chromosome arms in mitosis. J. Cell Biol. 158, 23-29.
54. Tse, Y., and Wang, J.C. (1980). E. coli and M. luteus DNA topoisomerase I can catalyze catenation of decatenation of double-stranded DNA rings. Cell 22, 269-276.
55. Uemura, T., Ohkura, H., Adachi, Y., Morino, K., Shiozaki, K., and Yanagida, M. (1987). DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe. Cell 50, 917-925.
56. Uemura, T., and Yanagida, M. (1986). Mitotic spindle pulls but fails to separate chromosomes in type II DNA topoisomerase mutants: uncoordinated mitosis. EMBO J. 5, 1003-1010.
57. van Hille, B., Clerc, X., Creighton, A.M., and Hill, B.T. (1999). Differential expression of topoisomerase I and RAD52 protein in yeast reveals new facets of the mechanism of action of bisdioxopiperazine compounds. Br. J. Cancer 81, 800-807.
58. Wang, J.C. (2002). Cellular roles of DNA topoisomerases: a molecular perspective. Nat. Rev. Mol. Cell. Biol. 3, 430-440.
59. Wang, L., and Eastmond, D.A. (2002). Catalytic inhibitors of topoisomerase II are DNA-damaging agents: induction of chromosomal damage by merbarone and ICRF-187. Environ. Mol. Mutagen. 39, 348-356.
60. Watt, P.M., and Hickson, I.D. (1994). Structure and function of type II DNA topoisomerases. Biochem. J. 303, 681-695.
61. Wells, N.J., and Hickson, I.D. (1995). Human topoisomerase II alpha is phosphorylated in a cell-cycle phase-dependent manner by a proline-directed kinase. Eur. J. Biochem. 231, 491-497.
62. Yanagida, M. (1998). Fission yeast cut mutations revisited: control of anaphase. Trends Cell. Biol. 8, 144-149.
63. Yáñez, R.J., and Porter, A.C.G. (1999). Gene targeting is enhanced in human cells overexpressing hRAD51. Gene Ther. 6, 1282-1290.
64. Yang, X., Li, W., Prescott, E.D., Burden, S.J., and Wang, J.C. (2000). DNA topoisomerase IIbeta and neural development. Science 287, 131-134.