TDP2-Dependent Non-Homologous End-Joining Protects against Topoisomerase II-Induced DNA Breaks and Genome Instability in Cells and In Vivo

PLoS Genetics

Volumn 9, Issue 3, 2013, Pages

  Gómez Herreros, Fernando ^a   Romero Granados, Rocío ^b   Zeng, Zhihong ^a   Álvarez Quilón, Alejandro ^b   Quintero, Cristina ^b   Ju, Limei ^a   Umans, Lieve ^c   Vermeire, Liesbeth ^c   Huylebroeck, Danny ^c   Caldecott, Keith W ^a   Cortés Ledesma, Felipe ^b  

^a UNIVERSITY OF SUSSEX   (United Kingdom)

^b UNIVERSITY OF SEVILLE   (Spain)

^c UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

DNA TOPOISOMERASE (ATP HYDROLYSING); PHOSPHODIESTERASE; TDP2 PROTEIN; UNCLASSIFIED DRUG;

ACCURACY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW; CANCER CHEMOTHERAPY; CONTROLLED STUDY; CYTOTOXICITY; DNA END JOINING REPAIR; DOUBLE STRANDED DNA BREAK; FEMALE; GENE DELETION; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; IN VIVO STUDY; INTESTINE INJURY; LYMPHOID TISSUE; MALE; MOUSE; NONHUMAN; PROTEIN FUNCTION; TDP2 GENE;

ANIMALS; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA END-JOINING REPAIR; DNA REPAIR; DNA TOPOISOMERASES, TYPE II; GENOMIC INSTABILITY; MICE; PHOSPHORIC DIESTER HYDROLASES; RECOMBINATION, GENETIC; TUMOR NECROSIS FACTOR RECEPTOR-ASSOCIATED PEPTIDES AND PROTEINS;

MUS;

EID: 84875992493     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003226     Document Type: Article

References (51)

1. Champoux JJ, (2001) DNA topoisomerases: structure, function, and mechanism. Annu Rev Biochem 70: 369-413 doi:10.1146/annurev.biochem.70.1.369.
2. Wang JC, (2002) Cellular roles of DNA topoisomerases: a molecular perspective. Nat Rev Mol Cell Biol 3: 430-440 doi:10.1038/nrm831.
3. Nitiss JL, (2009) DNA topoisomerase II and its growing repertoire of biological functions. Nat Rev Cancer 9: 327-337 doi:10.1038/nrc2608.
4. Deweese JE, Osheroff N, (2009) The DNA cleavage reaction of topoisomerase II: wolf in sheep's clothing. Nucleic Acids Res 37: 738-748 doi:10.1093/nar/gkn937.
5. Nitiss JL, (2009) Targeting DNA topoisomerase II in cancer chemotherapy. Nat Rev Cancer 9: 338-350 doi:10.1038/nrc2607.
6. Anderson RD, Berger NA, (1994) International Commission for Protection Against Environmental Mutagens and Carcinogens. Mutagenicity and carcinogenicity of topoisomerase-interactive agents. Mutat Res 309: 109-142.
7. Felix CA, Kolaris CP, Osheroff N, (2006) Topoisomerase II and the etiology of chromosomal translocations. DNA Repair (Amst) 5: 1093-1108 doi:10.1016/j.dnarep.2006.05.031.
8. Povirk LF, (2006) Biochemical mechanisms of chromosomal translocations resulting from DNA double-strand breaks. DNA Repair (Amst) 5: 1199-1212 doi:10.1016/j.dnarep.2006.05.016.
9. Albain KS, Le Beau MM, Ullirsch R, Schumacher H, (1990) Implication of prior treatment with drug combinations including inhibitors of topoisomerase II in therapy-related monocytic leukemia with a 9;11 translocation. Gene Chromosome Canc 2: 53-58.
10. Ahuja HG, Felix CA, Aplan PD, (2000) Potential role for DNA topoisomerase II poisons in the generation of t(11;20)(p15;q11) translocations. Gene Chromosome Canc 29: 96-105.
11. Andersen MK, Christiansen DH, Jensen BA, Ernst P, Hauge G, et al. (2001) Therapy-related acute lymphoblastic leukaemia with MLL rearrangements following DNA topoisomerase II inhibitors, an increasing problem: report on two new cases and review of the literature since 1992. Br J Haematol 114: 539-543.
12. Lovett BD, Lo Nigro L, Rappaport EF, Blair IA, Osheroff N, et al. (2001) Near-precise interchromosomal recombination and functional DNA topoisomerase II cleavage sites at MLL and AF-4 genomic breakpoints in treatment-related acute lymphoblastic leukemia with t(4;11) translocation. Proc Natl Acad Sci USA 98: 9802-9807 doi:10.1073/pnas.171309898.
13. Whitmarsh RJ, Saginario C, Zhuo Y, Hilgenfeld E, Rappaport EF, et al. (2003) Reciprocal DNA topoisomerase II cleavage events at 5"-TATTA-3" sequences in MLL and AF-9 create homologous single-stranded overhangs that anneal to form der(11) and der(9) genomic breakpoint junctions in treatment-related AML without further processing. Oncogene 22: 8448-8459 doi:10.1038/sj.onc.1207052.
14. Mistry AR, Felix CA, Whitmarsh RJ, Mason A, Reiter A, et al. (2005) DNA topoisomerase II in therapy-related acute promyelocytic leukemia. N Engl J Med 352: 1529-1538 doi:10.1056/NEJMoa042715.
15. Giguère A, Hébert J, (2011) Microhomologies and topoisomerase II consensus sequences identified near the breakpoint junctions of the recurrent t(7;21)(p22;q22) translocation in acute myeloid leukemia. Gene Chromosome Canc 50: 228-238 doi:10.1002/gcc.20848.
16. Le H, Singh S, Shih S-J, Du N, Schnyder S, et al. (2009) Rearrangements of the MLL gene are influenced by DNA secondary structure, potentially mediated by topoisomerase II binding. Gene Chromosome Canc 48: 806-815 doi:10.1002/gcc.20685.
17. Mirault M-E, Boucher P, Tremblay A, (2006) Nucleotide-resolution mapping of topoisomerase-mediated and apoptotic DNA strand scissions at or near an MLL translocation hotspot. Am J Hum Genet 79: 779-791 doi:10.1086/507791.
18. Connelly JC, Leach DRF, (2004) Repair of DNA covalently linked to protein. Mol Cell 13: 307-316.
19. Kurosawa A, Koyama H, Takayama S, Miki K, Ayusawa D, et al. (2008) The requirement of Artemis in double-strand break repair depends on the type of DNA damage. DNA Cell Biol 27: 55-61 doi:10.1089/dna.2007.0649.
20. Sartori AA, Lukas C, Coates J, Mistrik M, Fu S, et al. (2007) Human CtIP promotes DNA end resection. Nature 450: 509-514 doi:10.1038/nature06337.
21. Quennet V, Beucher A, Barton O, Takeda S, Löbrich M, (2011) CtIP and MRN promote non-homologous end-joining of etoposide-induced DNA double-strand breaks in G1. Nucleic Acids Res 39: 2144-2152 doi:10.1093/nar/gkq1175.
22. Cortes Ledesma F, Khamisy El SF, Zuma MC, Osborn K, Caldecott KW, (2009) A human 5′-tyrosyl DNA phosphodiesterase that repairs topoisomerase-mediated DNA damage. Nature 461: 674-678 doi:10.1038/nature08444.
23. Pype S, Declercq W, Ibrahimi A, Michiels C, Van Rietschoten JG, et al. (2000) TTRAP, a novel protein that associates with CD40, tumor necrosis factor (TNF) receptor-75 and TNF receptor-associated factors (TRAFs), and that inhibits nuclear factor-kappa B activation. J Biol Chem 275: 18586-18593 doi:10.1074/jbc.M000531200.
24. Pei H, Yordy JS, Leng Q, Zhao Q, Watson DK, et al. (2003) EAPII interacts with ETS1 and modulates its transcriptional function. Oncogene 22: 2699-2709 doi:10.1038/sj.onc.1206374.
25. Zeng Z, Cortes Ledesma F, Khamisy El SF, Caldecott KW, (2011) TDP2/TTRAP is the major 5′-tyrosyl DNA phosphodiesterase activity in vertebrate cells and is critical for cellular resistance to topoisomerase II-induced DNA damage. J Biol Chem 286: 403-409 doi:10.1074/jbc.M110.181016.
26. Shrivastav M, De Haro LP, Nickoloff JA, (2008) Regulation of DNA double-strand break repair pathway choice. Cell Res 18: 134-147 doi:10.1038/cr.2007.111.
27. Murai J, Huang S-YN, Das BB, Dexheimer TS, Takeda S, et al. (2012) Tyrosyl-DNA phosphodiesterase 1 (TDP1) repairs DNA damage induced by topoisomerases I and II and base alkylation in vertebrate cells. J Biol Chem 287: 12848-12857 doi:10.1074/jbc.M111.333963.
28. Baumann P, West SC, (1998) DNA end-joining catalyzed by human cell-free extracts. Proc Natl Acad Sci USA 95: 14066-14070.
29. Löbrich M, Shibata A, Beucher A, Fisher A, Ensminger M, et al. (2010) gammaH2AX foci analysis for monitoring DNA double-strand break repair: strengths, limitations and optimization. Cell Cycle 9: 662-669.
30. Huertas P, (2010) DNA resection in eukaryotes: deciding how to fix the break. Nat Struct Mol Biol 17: 11-16 doi:10.1038/nsmb.1710.
31. Sonoda E, Sasaki MS, Morrison C, Yamaguchi-Iwai Y, Takata M, et al. (1999) Sister chromatid exchanges are mediated by homologous recombination in vertebrate cells. Mol Cell Biol 19: 5166-5169.
32. Takahashi N, Kadota T, Kawano S, Ishikawa K, Kuroyanagi K, et al. (1986) [Toxicity studies of VP 16-213 (I)-Acute toxicity in mice, rats and rabbits]. J Toxicol Sci 11 Suppl 1: 1-16.
33. Li C, Sun S-Y, Khuri FR, Li R, (2011) Pleiotropic functions of EAPII/TTRAP/TDP2: cancer development, chemoresistance and beyond. Cell Cycle 10: 3274-3283 doi:10.4161/cc.10.19.17763.
34. Barthelmes HU, Habermeyer M, Christensen MO, Mielke C, Interthal H, et al. (2004) TDP1 overexpression in human cells counteracts DNA damage mediated by topoisomerases I and II. J Biol Chem 279: 55618-55625 doi:10.1074/jbc.M405042200.
35. Nitiss KC, Malik M, He X, White SW, Nitiss JL, (2006) Tyrosyl-DNA phosphodiesterase (Tdp1) participates in the repair of TOP2-mediated DNA damage. Proc Natl Acad Sci USA 103: 8953-8958 doi:10.1073/pnas.0603455103.
36. Zeng Z, Sharma A, Ju L, Murai J, Umans L, et al. (2012) TDP2 promotes repair of topoisomerase I-mediated DNA damage in the absence of TDP1. Nucleic Acids Res doi:10.1093/nar/gks622.
37. Symington LS, Gautier J, (2011) Double-strand break end resection and repair pathway choice. Annu Rev Genet 45: 247-271 doi:10.1146/annurev-genet-110410-132435.
38. de Campos-Nebel M, Larripa I, González-Cid M, (2010) Topoisomerase II-mediated DNA damage is differently repaired during the cell cycle by non-homologous end joining and homologous recombination. PLoS ONE 5: e12541 doi:10.1371/journal.pone.0012541.
39. Li GC, Ouyang H, Li X, Nagasawa H, Little JB, et al. (1998) Ku70: a candidate tumor suppressor gene for murine T cell lymphoma. Mol Cell 2: 1-8.
40. Pierce AJ, Hu P, Han M, Ellis N, Jasin M, (2001) Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev 15: 3237-3242 doi:10.1101/gad.946401.
41. Saintigny Y, Delacôte F, Boucher D, Averbeck D, Lopez BS, (2007) XRCC4 in G1 suppresses homologous recombination in S/G2, in G1 checkpoint-defective cells. Oncogene 26: 2769-2780 doi:10.1038/sj.onc.1210075.
42. Cortes Ledesma F, Prado F, Aguilera A (2007) Sister chromatid recombination. In: Aguilera A, Rothstein R, editors. Top Curr Genet 17 (Molecular Genetics of Recombination). Berlin Heidelberg: Springer-Verlag. pp. 363-380.
43. Li C, Fan S, Owonikoko TK, Khuri FR, Sun S-Y, et al. (2011) Oncogenic role of EAPII in lung cancer development and its activation of the MAPK-ERK pathway. Oncogene 30: 3802-3812 doi:10.1038/onc.2011.94.
44. Do PM, Varanasi L, Fan S, Li C, Kubacka I, et al. (2012) Mutant p53 cooperates with ETS2 to promote etoposide resistance. Genes Dev 26: 830-845 doi:10.1101/gad.181685.111.
45. Wolff SN, Hainsworth JD, Greco FA, (2008) High-dose etoposide: from phase I to a component of curative therapy. J Clin Oncol 26: 5310-5312 doi:10.1200/JCO.2008.19.0892.
46. Langer T, Metzler M, Reinhardt D, Viehmann S, Borkhardt A, et al. (2003) Analysis of t(9;11) chromosomal breakpoint sequences in childhood acute leukemia: almost identical MLL breakpoints in therapy-related AML after treatment without etoposides. Gene Chromosome Canc 36: 393-401 doi:10.1002/gcc.10167.
47. Haffner MC, Aryee MJ, Toubaji A, Esopi DM, Albadine R, et al. (2010) Androgen-induced TOP2B-mediated double-strand breaks and prostate cancer gene rearrangements. Nat Genet 42: 668-675 doi:10.1038/ng.613.
48. Takata M, Sasaki MS, Sonoda E, Morrison C, Hashimoto M, et al. (1998) Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J 17: 5497-5508 doi:10.1093/emboj/17.18.5497.
49. Beucher A, Birraux J, Tchouandong L, Barton O, Shibata A, et al. (2009) ATM and Artemis promote homologous recombination of radiation-induced DNA double-strand breaks in G2. EMBO J 28: 3413-3427 doi:10.1038/emboj.2009.276.
50. Sáenz Robles MT, Symonds H, Chen J, Van Dyke T, (1994) Induction versus progression of brain tumor development: differential functions for the pRB- and p53-targeting domains of simian virus 40 T antigen. Mol Cell Biol 14: 2686-2698.
51. Seluanov A, Mittelman D, Pereira-Smith OM, Wilson JH, Gorbunova V, (2004) DNA end joining becomes less efficient and more error-prone during cellular senescence. Proc Natl Acad Sci USA 101: 7624-7629 doi:10.1073/pnas.0400726101.