DNA double-strand breaks with 5′ adducts are efficiently channeled to the DNA2-mediated resection pathway

Nucleic Acids Research

Volumn 44, Issue 1, 2016, Pages 221-231

  Tammaro, Margaret ^a   Liao, Shuren ^a   Beeharry, Neil ^a   Yan, Hong ^a  

^a FOX CHASE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; DNA TOPOISOMERASE (ATP HYDROLYSING); DNA2 PROTEIN; ETOPOSIDE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; DNA ADDUCT; SINGLE STRANDED DNA;

5' ADDUCT; ANIMAL CELL; ARTICLE; CATALYSIS; CELL SURVIVAL; CHEMOSENSITIVITY; CONTROLLED STUDY; DNA END JOINING REPAIR; DNA REPAIR; DNA STRUCTURE; DNA2 MEDIATED RESECTION; DOUBLE STRANDED DNA BREAK; G2 PHASE CELL CYCLE CHECKPOINT; GENE SILENCING; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; S PHASE CELL CYCLE CHECKPOINT; XENOPUS; ANIMAL; CELL PROLIFERATION; DNA ADDUCT; DRUG EFFECTS; GENE EXPRESSION; GENETICS; METABOLISM; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; DNA ADDUCTS; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA TOPOISOMERASES, TYPE II; DNA, SINGLE-STRANDED; ETOPOSIDE; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; HUMANS; RNA, SMALL INTERFERING; XENOPUS;

EID: 84959543961     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv969     Document Type: Article

References (45)

1. Vilenchik,M.M. and Knudson,A.G. (2003) Endogenous DNA double-strand breaks: production, fidelity of repair, and induction of cancer. Proc. Natl. Acad. Sci. U.S.A., 100, 12871-12876.
2. O'Driscoll,M. and Jeggo,P.A. (2006) The role of double-strand break repair - insights from human genetics. Nat. Rev. Genet., 7, 45-54.
3. Friedberg,E., Walker,G.C., Siede,W., Wood,R.D., Schultz,R.A. and Ellenberger,T. (2006) DNA Repair and Mutagenesis. ASM Press, Washington, D.C.
4. Nussenzweig,A. and Nussenzweig,M.C. (2010) Origin of chromosomal translocations in lymphoid cancer. Cell, 141, 27-38.
5. Baumann,P. and West,S.C. (1998) Role of the human RAD51 protein in homologous recombination and double- stranded-break repair. Trends Biochem. Sci., 23, 247-251.
6. Karran,P. (2000) DNA double strand break repair in mammalian cells. Curr. Opin. Genet. Dev., 10, 144-150.
7. Pastink,A., Eeken,J.C. and Lohman,P.H. (2001) Genomic integrity and the repair of double-strand DNA breaks. Mutat. Res., 480-481, 37-50.
8. Symington,L.S. and Gautier,J. (2011) Double-strand break end resection and repair pathway choice. Annu. Rev. Genet., 45, 247-271.
9. Toczylowski,T. and Yan,H. (2006) Mechanistic analysis of a DNA end processing pathway mediated by the Xenopus Werner syndrome protein. J. Biol. Chem., 281, 33198-33205.
10. Gravel,S., Chapman,J.R., Magill,C. and Jackson,S.P. (2008) DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev., 22, 2767-2772.
11. Liao,S., Toczylowski,T. and Yan,H. (2008) Identification of the Xenopus DNA2 protein as a major nuclease for the 5′->3′ strand-specific processing of DNA ends. Nucleic Acids Res., 36, 6091-6100.
12. Mimitou,E.P. and Symington,L.S. (2008) Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature, 455, 770-774.
13. Zhu,Z., Chung,W.H., Shim,E.Y., Lee,S.E. and Ira,G. (2008) Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell, 134, 981-994.
14. Yan,H., Toczylowski,T., McCane,J., Chen,C. and Liao,S. (2011) Replication protein A promotes 5′->3′ end processing during homology-dependent DNA double-strand break repair. J. Cell Biol., 192, 251-261.
15. Liao,S., Toczylowski,T. and Yan,H. (2011) Mechanistic analysis of Xenopus EXO1's function in 5′-strand resection at DNA double-strand breaks. Nucleic Acids Res., 39, 5967-5977.
16. Jazayeri,A., Falck,J., Lukas,C., Bartek,J., Smith,G.C., Lukas,J. and Jackson,S.P. (2006) ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell Biol., 8, 37-45.
17. Sartori,A.A., Lukas,C., Coates,J., Mistrik,M., Fu,S., Bartek,J., Baer,R., Lukas,J. and Jackson,S.P. (2007) Human CtIP promotes DNA end resection. Nature, 450, 509-514.
18. You,Z., Shi,L.Z., Zhu,Q., Wu,P., Zhang,Y.W., Basilio,A., Tonnu,N., Verma,I.M., Berns,M.W. and Hunter,T. (2009) CtIP links DNA double-strand break sensing to resection. Mol. Cell, 36, 954-969.
19. Liao,S., Guay,C., Toczylowski,T. and Yan,H. (2012) Analysis of MRE11's function in the 5′->3′ processing of DNA double-strand breaks. Nucleic Acids Res., 40, 4496-4506.
20. Keeney,S., Giroux,C.N. and Kleckner,N. (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell, 88, 375-384.
21. Challberg,M.D., Ostrove,J.M. and Kelly,T.J. Jr (1982) Initiation of adenovirus DNA replication: detection of covalent complexes between nucleotide and the 80-kilodalton terminal protein. J. Virol., 41, 265-270.
22. Nitiss,J.L. (2009) Targeting DNA topoisomerase II in cancer chemotherapy. Nat. Rev. Cancer, 9, 338-350.
23. Pommier,Y. (2013) Drugging topoisomerases: lessons and challenges. ACS Chem. Biol., 8, 82-95.
24. Deweese,J.E. and Osheroff,N. (2009) The DNA cleavage reaction of topoisomerase II: wolf in sheep's clothing. Nucleic Acids Res., 37, 738-748.
25. Bromberg,K.D., Burgin,A.B. and Osheroff,N. (2003) A two-drug model for etoposide action against human topoisomerase IIalpha. J. Biol. Chem., 278, 7406-7412.
26. Tennyson,R.B. and Lindsley,J.E. (1997) Type II DNA topoisomerase from Saccharomyces cerevisiae is a stable dimer. Biochemistry, 36, 6107-6114.
27. Tammaro,M., Barr,P., Ricci,B. and Yan,H. (2013) Replication-dependent and transcription-dependent mechanisms of DNA double-strand break induction by the topoisomerase 2-targeting drug Etoposide. PLoS One, 8, e79202.
28. Mao,Y., Desai,S.D., Ting,C.Y., Hwang,J. and Liu,L.F. (2001) 26 S proteasome-mediated degradation of topoisomerase II cleavable complexes. J. Biol. Chem., 276, 40652-40658.
29. Xiao,H., Mao,Y., Desai,S.D., Zhou,N., Ting,C.Y., Hwang,J. and Liu,L.F. (2003) The topoisomerase IIbeta circular clamp arrests transcription and signals a 26S proteasome pathway. Proc. Natl. Acad. Sci. U.S.A., 100, 3239-3244.
30. Alchanati,I., Teicher,C., Cohen,G., Shemesh,V., Barr,H.M., Nakache,P., Ben-Avraham,D., Idelevich,A., Angel,I., Livnah,N. et al. (2009) The E3 ubiquitin-ligase Bmi1/Ring1A controls the proteasomal degradation of Top2alpha cleavage complex - a potentially new drug target. PLoS One, 4, e8104.
31. Cortes Ledesma,F., El Khamisy,S.F., Zuma,M.C., Osborn,K. and Caldecott,K.W. (2009) A human 5′-tyrosyl DNA phosphodiesterase that repairs topoisomerase-mediated DNA damage. Nature, 461, 674-678.
32. Gao,R., Schellenberg,M.J., Huang,S.Y., Abdelmalak,M., Marchand,C., Nitiss,K.C., Nitiss,J.L., Williams,R.S. and Pommier,Y. (2014) Proteolytic degradation of topoisomerase II (Top2) enables the processing of Top2.DNA and Top2.RNA covalent complexes by tyrosyl-DNA-phosphodiesterase 2 (TDP2). J. Biol. Chem., 289, 17960-17969.
33. Zeng,Z., Cortes-Ledesma,F., El Khamisy,S.F. and Caldecott,K.W. (2010) 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.
34. Cannavo,E. and Cejka,P. (2014) Sae2 promotes dsDNA endonuclease activity within Mre11-Rad50-Xrs2 to resect DNA breaks. Nature, 514, 122-125.
35. Gomez-Herreros,F., Romero-Granados,R., Zeng,Z., Alvarez-Quilon,A., Quintero,C., Ju,L., Umans,L., Vermeire,L., Huylebroeck,D., Caldecott,K.W. et al. (2013) TDP2-dependent non-homologous end-joining protects against topoisomerase II-induced DNA breaks and genome instability in cells and in vivo. PLoS Genet., 9, e1003226.
36. de Campos-Nebel,M., Larripa,I. and Gonzalez-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.
37. Smythe,C. and Newport,J.W. (1991) In: Hamkalo,BA and Elgin,SCR (eds). Methods Cell Biol. Academic Press, NY, Vol. 35, pp. 449-468.
38. Roca,J., Ishida,R., Berger,J.M., Andoh,T. and Wang,J.C. (1994) Antitumor bisdioxopiperazines inhibit yeast DNA topoisomerase II by trapping the enzyme in the form of a closed protein clamp. Proc. Natl. Acad. Sci. U.S.A., 91, 1781-1785.
39. Kao,G.D., McKenna,W.G., Guenther,M.G., Muschel,R.J., Lazar,M.A. and Yen,T.J. (2003) Histone deacetylase 4 interacts with 53BP1 to mediate the DNA damage response. J. Cell Biol., 160, 1017-1027.
40. Karanja,K.K., Cox,S.W., Duxin,J.P., Stewart,S.A. and Campbell,J.L. (2012) DNA2 and EXO1 in replication-coupled, homology-directed repair and in the interplay between HDR and the FA/BRCA network. Cell Cycle, 11, 3983-3996.
41. Peng,G., Dai,H., Zhang,W., Hsieh,H.J., Pan,M.R., Park,Y.Y., Tsai,R.Y., Bedrosian,I., Lee,J.S., Ira,G. et al. (2012) Human nuclease/helicase DNA2 alleviates replication stress by promoting DNA end resection. Cancer Res., 72, 2802-2813.
42. Sturzenegger,A., Burdova,K., Kanagaraj,R., Levikova,M., Pinto,C., Cejka,P. and Janscak,P. (2014) DNA2 cooperates with the WRN and BLM RecQ helicases to mediate long-range DNA-end resection in human cells. J. Biol. Chem., 289, 27314-27326.
43. Duxin,J.P., Dao,B., Martinsson,P., Rajala,N., Guittat,L., Campbell,J.L., Spelbrink,J.N. and Stewart,S.A. (2009) Human Dna2 is a nuclear and mitochondrial DNA maintenance protein. Mol. Cell. Biol., 29, 4274-4282.
44. Duxin,J.P., Moore,H.R., Sidorova,J., Karanja,K., Honaker,Y., Dao,B., Piwnica-Worms,H., Campbell,J.L., Monnat,R.J. Jr and Stewart,S.A. (2012) Okazaki fragment processing-independent role for human Dna2 enzyme during DNA replication. J. Biol. Chem., 287, 21980-21991.
45. Chen,L., Nievera,C.J., Lee,A.Y. and Wu,X. (2008) Cell cycle-dependent complex formation of BRCA1.CtIP.MRN is important for DNA double-strand break repair. J. Biol. Chem., 283, 7713-7720.