Effects of conditional depletion of topoisomerase II on cell cycle progression in mammalian cells

Cell Cycle

Volumn 10, Issue 20, 2011, Pages 3505-3514

  Gonzalez, Ruth E ^a,b   Lim, Chang Uk ^a,c   Cole, Kelly ^a   Bianchini, Christine Hanko ^a   Schools, Gary P ^a,c   Davis, Brian E ^a   Wada, Ikuo ^a   Roninson, Igor B ^a,c   Broude, Eugenia V ^a,c  

^a ORDWAY RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Conditional knockdown; Mitosis; Mitotic catastrophe; S phase; Topoisomerase II

Indexed keywords

DNA TOPOISOMERASE (ATP HYDROLYSING);

ARTICLE; CELL CYCLE G2 PHASE; CELL CYCLE PROGRESSION; CELL DEATH; CELL DIVISION; CHROMOSOME CONDENSATION; CONTROLLED STUDY; DNA REPLICATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IN VITRO STUDY; MAMMAL CELL; MITOSIS; PROTEIN EXPRESSION; SISTER CHROMATID;

MAMMALIA;

EID: 80055110142     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.10.20.17778     Document Type: Article

References (39)

1. Nitiss JL. DNA topoisomerase II and its growing repertoire of biological functions. Nat Rev Cancer 2009; 9:327-37; PMID:19377505; DOI:10.1038/nrc2608.
2. Holm C, Goto T, Wang JC, Botstein D. DNA topoisomerase II is required at the time of mitosis in yeast. Cell 1985; 41:553-63; PMID:2985283; DOI:10.1016/S0092-8674(85)80028-3.
3. Uemura T, Ohkura H, Adachi Y, Morino K, Shiozaki K, Yanagida M. DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe. Cell 1987; 50:917-25; PMID:3040264; DOI:10.1016/0092-8674(87)90518-6.
4. Gasser SM, Laroche T, Falquet J. Boy dlT, Laemmli UK. Metaphase chromosome structure. Involvement of topoisomerase II. J Mol Biol 1986; 188:613-29; PMID:3016287; DOI:10.1016/S0022-2836(86)80010-9.
5. Giménez-Abián JF, Clarke DJ, Devlin J, Giménez- AbiánMI, De la Torre C, Johnson RT, et al. Premitotic chromosome individualization in mammalian cells depends on topoisomerase II activity. Chromosoma 2000; 109:235-44; PMID:10968252; DOI:10.1007/s004120000065.
6. Tapia-Alveal C, Outwin EA, Trempolec N, Dziadkowiec D, Murray JM, O'Connell MJ. SMC complexes and topoisomerase II work together so that sister chromatids can work apart. Cell Cycle 2010; 9:2065-70; PMID:20495382; DOI:10.4161/cc.9.11.11734.
7. Baxter J, Diffley JF. Topoisomerase II inactivation prevents the completion of DNA replication in budding yeast. Mol Cell 2008; 30:790-802; PMID:18570880; DOI:10.1016/j.molcel.2008.04.019.
8. Li H, Wang Y, Liu X. Plk1-dependent phosphorylation regulates functions of DNA topoisomerase IIalpha in cell cycle progression. J Biol Chem 2008; 283:6209-21; PMID:18171681; DOI:10.1074/jbc.M709007200.
9. Downes CS, Clarke DJ, Mullinger AM, Gimenez-Abian JF, Creighton AM, Johnson RT. A topoisomerase II-dependent G2 cycle checkpoint in mammalian cells. Nature 1994; 372:467-70; PMID:7984241; DOI:10.1038/372467a0.
10. Deming PB, Cistulli CA, Zhao H, Graves PR, Piwnica- Worms H, Paules RS, et al. The human decatenation checkpoint. Proc Natl Acad Sci USA 2001; 98:12044-9; PMID:11593014; DOI:10.1073/pnas.221430898.
11. Skoufias DA, Lacroix FB, Andreassen PR, Wilson L, Margolis RL. Inhibition of DNA decatenation, but not DNA damage, arrests cells at metaphase. Mol Cell 2004; 15:977-90; PMID:15383286; DOI:10.1016/j.molcel.2004.08.018.
12. Luo K, Yuan J, Chen J, Lou Z. Topoisomerase IIalpha controls the decatenation checkpoint. Nat Cell Biol 2009; 11:204-10; PMID:19098900; DOI:10.1038/ncb1828.
13. Johnson M, Phua HH, Bennett SC, Spence JM, Farr CJ. Studying vertebrate topoisomerase 2 function using a conditional knockdown system in DT40 cells. Nucleic Acids Res 2009; 37:98; PMID:19494182; DOI:10.1093/nar/gkp480.
14. Bower JJ, Karaca GF, Zhou Y, Simpson DA, Cordeiro- Stone M, Kaufmann WK. Topoisomerase IIalpha maintains genomic stability through decatenation G(2) checkpoint signaling. Oncogene 2010; 29:4787-99; PMID:20562910; DOI:10.1038/onc.2010.232.
15. Nitiss JL. Targeting DNA topoisomerase II in cancer chemotherapy. Nat Rev Cancer 2009; 9:338-50; PMID:19377506; DOI:10.1038/nrc2607.
16. Larsen AK, Escargueil AE, Skladanowski A. Catalytic topoisomerase II inhibitors in cancer therapy. Pharmacol Ther 2003; 99:167-81; PMID:12888111; DOI:10.1016/S0163-7258(03)00058-5.
17. Hawtin RE, Stockett DE, Wong OK, Lundin C, Helleday T, Fox JA. Homologous recombination repair is essential for repair of vosaroxin-induced DNA double-strand breaks. Oncotarget 2010; 1:606-19; PMID:21317456.
18. Huang KC, Gao H, Yamasaki EF, Grabowski DR, Liu S, Shen LL, et al. Topoisomerase II poisoning by ICRF-193. J Biol Chem 2001; 276:44488-94; PMID:11577077; DOI:10.1074/jbc.M104383200.
19. 2/M transition by triggering the p38 MAPK checkpoint pathway. J Cell Biol 2004; 166:517-26; PMID:15302851; DOI:10.1083/jcb.200405167.
20. Carpenter AJ, Porter AC. Construction, characterization and complementation of a conditional-lethal DNA topoisomerase IIalpha mutant human cell line. Mol Biol Cell 2004; 15:5700-11; PMID:15456904; DOI:10.1091/mbc.E04- 08-0732.
21. Sakaguchi A, Kikuchi A. Functional compatibility between isoformalpha and beta of type II DNA topoisomerase. J Cell Sci 2004; 117:1047-54; PMID:14996935; DOI:10.1242/jcs.00977.
22. Toyoda Y, Yanagida M. Coordinated requirements of human topo II and cohesin for metaphase centromere alignment under Mad2-dependent spindle checkpoint surveillance. Mol Biol Cell 2006; 17:2287-302; PMID:16510521; DOI:10.1091/mbc.E05-11-1089.
23. Ossovskaya VS, Mazo IA, Chernov MV, Chernova OB, Strezoska Z, Kondratov R, et al. Use of genetic suppressor elements to dissect distinct biological effects of separate p53 domains. Proc Natl Acad Sci USA 1996; 93:10309-14; PMID:8816796; DOI:10.1073/pnas.93.19.10309.
24. Chang BD, Broude EV, Dokmanovic M, Zhu H, Ruth A, Xuan Y, et al. A senescence-like phenotype distinguishes tumor cells that undergo terminal proliferation arrest after exposure to anticancer agents. Cancer Res 1999; 59:3761-7; PMID:10446993.
25. Broude EV, Swift ME, Vivo C, Chang BD, Davis BM, Kalurupalle S, et al. p21(Waf1/Cip1/Sdi1) mediates retinoblastoma protein degradation. Oncogene 2007; 26:6954-8; PMID:17486059; DOI:10.1038/sj.onc.1210516.
26. Broude EV, Demidenko ZN, Vivo C, Swift ME, Davis BM, Blagosklonny MV, et al. p21 (CDKN1A) is a negative regulator of p53 stability. Cell Cycle 2007; 6:1468-71; PMID:17585201; DOI:10.4161/cc.6.12.4313.
27. Wiznerowicz M, Trono D. Conditional suppression of cellular genes: lentivirus vector-mediated drug-inducible RNA interference. J Virol 2003; 77:8957-61; PMID:12885912; DOI:10.1128/JVI.77.16.8957-1.2003.
28. Maliyekkel A, Davis BA, Roninson IB. Cell cycle arrest drastically extends the duration of gene silencing after transient expression of short hairpin RNA. Cell Cycle 2006; 5:2390-5; PMID:17102616; DOI:10.4161/cc.5.20.3363.
29. Shtutman M, Maliyekkel A, Shao Y, Carmack CS, Baig M, Warholic N, et al. Function-based gene identification using enzymatically generated normalized shRNA library and massive parallel sequencing. Proc Natl Acad Sci USA 2010; 107:7377-82; PMID:20368428; DOI:10.1073/pnas.1003055107.
30. Kinner A, Wu W, Staudt C, Iliakis G. Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res 2008; 36:5678-94; PMID:18772227; DOI:10.1093/nar/gkn550.
31. Buck JW, Dong W, Mueller DS. Effect of light exposure on in vitro germination and germ tube growth of eight species of rust fungi. Mycologia 2010; 102:1134-40; PMID:20943512; DOI:10.3852/09-283.
32. Rundle NT, Xu L, Andersen RJ, Roberge M. G2 DNA damage checkpoint inhibition and antimitotic activity of 13-hydroxy-15-oxozoapatlin. J Biol Chem 2001; 276:48231-6; PMID:11572854.
33. Ishida R, Sato M, Narita T, Utsumi KR, Nishimoto T, Morita T, et al. Inhibition of DNA topoisomerase II by ICRF-193 induces polyploidization by uncoupling chromosome dynamics from other cell cycle events. J Cell Biol 1994; 126:1341-51; PMID:8089169; DOI:10.1083/jcb.126.6.1341.
34. Iwai M, Hara A, Andoh T, Ishida R. ICRF-193, a catalytic inhibitor of DNA topoisomerase II, delays the cell cycle progression from metaphase, but not from anaphase to the G1 phase in mammalian cells. FEBS Lett 1997; 406:267-70; PMID:9136899; DOI:10.1016/S0014-5793(97)00282-2.
35. Vitale I, Senovilla L, Jemaa M, Michaud M, Galluzzi L, Kepp O, et al. Multipolar mitosis of tetraploid cells: inhibition by p53 and dependency on Mos. EMBO J 2010; 29:1272-84; PMID:20186124; DOI:10.1038/emboj.2010.11.
36. Broude EV, Loncarek J, Wada I, Cole K, Hanko C, Swift M, et al. Mitotic catastrophe in cancer therapy in Beyond Apoptosis: Cellular outcomes of cancer therapy (Roninson IB, Brown JM, Bredesen DE, Eds.). Informa Healthcare 2008; 307-20.
37. Tao Y, Leteur C, Calderaro J, Girdler F, Zhang P, Frascogna V, et al. The aurora B kinase inhibitor AZD1152 sensitizes cancer cells to fractionated irradiation and induces mitotic catastrophe. Cell Cycle 2009; 8:3172-81; PMID:19755861; DOI:10.4161/cc.8.19.9729.
38. waf1/cip1 in senescence-like terminal proliferation arrest induced in human tumor cells by chemotherapeutic drugs. Oncogene 1999; 18:4808-18; PMID:10490814; DOI:10.1038/sj.onc.1203078.
39. Rubinson DA, Dillon CP, Kwiatkowski AV, Sievers C, Yang L, Kopinja J, et al. A lentivirus-based system to functionally silence genes in primary mammalian cells, stem cells and transgenic mice by RNA interference. Nat Genet 2003; 33:401-6; PMID:12590264; DOI:10.1038/ng1117.