DNA Ligase IV and Artemis Act Cooperatively to Suppress Homologous Recombination in Human Cells: Implications for DNA Double-Strand Break Repair

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Kurosawa, Aya ^a   Saito, Shinta ^a   So, Sairei ^a   Hashimoto, Mitsumasa ^b   Iwabuchi, Kuniyoshi ^b   Watabe, Haruka ^a   Adachi, Noritaka ^a  

^a YOKOHAMA CITY UNIVERSITY   (Japan)

^b KANAZAWA MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARTEMIS PROTEIN; CELL PROTEIN; DNA TOPOISOMERASE (ATP HYDROLYSING); POLYDEOXYRIBONUCLEOTIDE SYNTHASE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE IV; UNCLASSIFIED DRUG;

ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DNA END JOINING REPAIR; DNA REPAIR; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; GENE INACTIVATION; GENE TARGETING; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; PROTEIN DEPLETION; PROTEIN PROTEIN INTERACTION; RADIATION DOSE; RADIATION INJURY; SIGNAL TRANSDUCTION;

CELL LINE; DNA BREAKS, DOUBLE-STRANDED; DNA END-JOINING REPAIR; DNA LIGASES; DNA REPLICATION; DNA TOPOISOMERASES, TYPE II; GENE KNOCKOUT TECHNIQUES; GENE TARGETING; HOMOLOGOUS RECOMBINATION; HUMANS; MUTATION; NUCLEAR PROTEINS; TOPOISOMERASE II INHIBITORS;

EID: 84881499062     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0072253     Document Type: Article

References (62)

1. O'Driscoll M, Jeggo PA, (2006) The role of double-strand break repair- insights from human genetics. Nature Rev Genet 7: 45-54.
2. Karpenshif Y, Bernstein KA, (2012) From yeast to mammals: Recent advances in genetic control of homologous recombination. DNA Repair (Amst) 11: 781-788.
3. Krejci L, Altmannova V, Spirek M, Zhao X, (2012) Homologous recombination and its regulation. Nucleic Acids Res 40: 5975-5818.
4. Kurosawa A, Adachi N, (2010) Functions and regulation of Artemis: a goddess in the maintenance of genome integrity. J Radiat Res 51: 503-509.
5. Lieber MR, (2010) The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu Rev Biochem 79: 181-211.
6. Kass EM, Jasin M, (2010) Collaboration and competition between DNA double-strand break repair pathways. FEBS Lett 584: 3703-3708.
7. Sekiguchi JM, Ferguson DO, (2006) DNA double-strand break repair: a relentless hunt uncovers new prey. Cell 124: 260-262.
8. Van Dyck E, Stasiak AZ, Stasiak A, West SC, (1999) Binding of double-strand breaks in DNA by human Rad52 protein. Nature 398: 728-731.
9. Bunting SF, Callen E, Wong N, Chen HT, Polato F, et al. (2010) 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 141: 243-254.
10. Jeggo PA, Geuting V, Lobrich M, (2011) The role of homologous recombination in radiation-induced double-strand break repair. Radiother oncol 101: 7-12.
11. Symington LS, Gautier J, (2011) Double-strand break end resection and repair pathway choice. Annu Rev Genet 45: 247-271.
12. Adachi N, So S, Iiizumi S, Nomura Y, Murai K, et al. (2006) The human pre-B cell line Nalm-6 is highly proficient in gene targeting by homologous recombination. DNA Cell Biol 25: 19-24.
13. Iiizumi S, Nomura Y, So S, Uegaki K, Aoki K, et al. (2006) Simple one-week method to construct gene-targeting vectors: application to production of human knockout cell lines. Biotechniques 41: 311-316.
14. Ceballos SJ, Heyer WD, (2011) Functions of the Snf2/Swi2 family Rad54 motor protein in homologous recombination. Biochim Biophys Acta 1809: 509-523.
15. 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.
16. Mills KD, Ferguson DO, Essers J, Eckersdorff M, Kanaar R, et al. (2004) Rad54 and DNA Ligase IV cooperate to maintain mammalian chromatid stability. Genes Dev 18: 1283-1292.
17. 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.
18. Adachi N, Ishino T, Ishii Y, Takeda S, Koyama H, (2001) DNA ligase IV-deficient cells are more resistant to ionizing radiation in the absence of Ku70: Implications for DNA double-strand break repair. Proc Natl Acad Sci U S A 98: 12109-12113.
19. Grawunder U, Zimmer D, Fugmann S, Schwarz K, Lieber MR, (1998) DNA ligase IV is essential for V(D)J recombination and DNA double-strand break repair in human precursor lymphocytes. Mol Cell 2: 477-484.
20. Karanjawala ZE, Adachi N, Irvine RA, Oh EK, Shibata D, et al. (2002) The embryonic lethality in DNA ligase IV-deficient mice is rescued by deletion of Ku: implications for unifying the heterogeneous phenotypes of NHEJ mutants. DNA Repair (Amst) 1: 1017-1026.
21. Ma Y, Pannicke U, Schwarz K, Lieber MR, (2002) Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination. Cell 108: 781-794.
22. Povirk LF, (2006) Biochemical mechanisms of chromosomal translocations resulting from DNA double-strand breaks. DNA Repair (Amst) 5: 1199-1212.
23. Iwabuchi K, Hashimoto M, Matsui T, Kurosawa A, Adachi N, et al. (2008) Cell sorting analysis of cell cycle-dependent X-ray sensitivity in end joining-deficient human cells. Biochem Biophys Res Commun 372: 662-667.
24. Nitiss JL, (2009) Targeting DNA topoisomease II in cancer chemotherapy. Nature Rev Cancer 9: 338-350.
25. Liu LF, (1989) DNA topoisomerase poisons as antitumor drugs. Annu Rev Biochem 58: 351-375.
26. Germe T, Hyrien O, (2005) Topoisomerase II-DNA complexes trapped by ICRF-193 perturb chromatin structure. EMBO Rep 6: 729-735.
27. Sabourin M, Nitiss JL, Nitiss KC, Tatebayashi K, Ikeda H, et al. (2003) Yeast recombination pathways triggered by topoisomerase II-mediated DNA breaks. Nucleic Acids Res 31: 4373-4384.
28. Adachi N, Suzuki H, Iiizumi S, 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.
29. Pommier Y, (2009) DNA topoisomerase I inhibitors: chemistry, biology, and interfacial inhibition. Chem Rev 109: 2894-2902.
30. Wang Z, Wang F, Tang T, Guo C, (2012) The role of PARP1 in the DNA damage response and its application in tumor therapy. Front Med 6: 156-164.
31. Shao RG, Cao CX, Zhang H, Kohn KW, Wold MS, et al. (1999) Replication-mediated DNA damage by camptothecin induces phosphorylation of RPA by DNA-dependent protein kinase and dissociates RPA:DNA-PK complexes. EMBO J 18: 1397-1406.
32. Furuta T, Takemura H, Liao ZY, Aune GJ, Redon C, et al. (2003) Phosphorylation of histone H2AX and activation of Mre11, Rad50, and Nbs1 in response to replication-dependent DNA double-strand breaks induced by mammalian DNA topoisomerase I cleavage complexes. J Biol Chem 278: 20303-20312.
33. Farmer H, McCabe N, Lord CJ, Tutt AN, Johnson DA, et al. (2005) Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434: 917-921.
34. Adachi N, So S, Koyama H, (2004) Loss of nonhomologous end joining confers camptothecin resistance in DT40 cells. Implications for the repair of topoisomerase I-mediated DNA damage. J Biol Chem 279: 37343-37348.
35. Soutoglou E, Misteli T, (2007) Mobility and immobility of chromatin in transcription and genome stability. Curr Opin Genet Dev 17: 435-442.
36. Soutoglou E, Dorn JF, Sengupta K, Jasin M, Nussenzweig A, et al. (2007) Positional stability of single double-strand breaks in mammalian cells. Nat Cell Biol 9: 675-682.
37. Yano K, Morotomi-Yano K, Wang SY, Uematsu N, Lee KJ, et al. (2008) Ku recruits XLF to DNA double-strand breaks. EMBO Rep 9: 91-96.
38. Saberi A, Hochegger H, Szuts D, Lan L, Yasui A, et al. (2007) RAD18 and poly(ADP-ribose) polymerase independently suppress the access of nonhomologous end joining to double-strand breaks and facilitate homologous recombination-mediated repair. Mol Cell Biol 27: 2562-2571.
39. Hochegger H, Dejsuphong D, Fukushima T, Morrison C, Sonoda E, et al. (2006) Parp-1 protects homologous recombination from interference by Ku and Ligase IV in vertebrate cells. EMBO J 25: 1305-1314.
40. Shibata A, Conrad S, Birraux J, Geuting V, Barton O, et al. (2011) Factors determining DNA double-strand break repair pathway choice in G2 phase. EMBO J 30: 1079.
41. Pannicke U, Ma Y, Hopfner KP, Niewolik D, Lieber MR, et al. (2004) Functional and biochemical dissection of the structure-specific nuclease ARTEMIS. EMBO J 23: 1987-1997.
42. Chen L, Morio T, Minegishi Y, Nakada S, Nagasawa M, et al. (2005) Ataxia-telangiectasia-mutated dependent phosphorylation of Artemis in response to DNA damage. Cancer Sci 96: 134-141.
43. Cui X, Yu Y, Gupta S, Cho YM, Lees-Miller SP, et al. (2005) Autophosphorylation of DNA-dependent protein kinase regulates DNA end processing and may also alter double-strand break repair pathway choice. Mol Cell Biol 25: 10842-10852.
44. Iiizumi S, Kurosawa A, So S, Ishii Y, Chikaraishi Y, et al. (2008) Impact of non-homologous end-joining deficiency on random and targeted DNA integration: implications for gene targeting. Nucleic Acids Res 36: 6333-6342.
45. Riballo E, Kuhne M, Rief N, Doherty A, Smith GC, et al. (2004) A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to gamma-H2AX foci. Mol Cell 16: 715-724.
46. Zhang X, Succi J, Feng Z, Prithivirajsingh S, Story MD, et al. (2004) Artemis is a phosphorylation target of ATM and ATR and is involved in the G2/M DNA damage checkpoint response. Mol Cell Biol 24: 9207-9220.
47. Lobrich M, Jeggo PA, (2005) Harmonising the response to DSBs: a new string in the ATM bow. DNA Repair (Amst) 4: 749-759.
48. Sekiguchi J, Ferguson DO, Chen HT, Yang EM, Earle J, et al. (2001) Genetic interactions between ATM and the nonhomologous end-joining factors in genomic stability and development. Proc Natl Acad Sci U S A 98: 3243-3248.
49. Chen BP, Uematsu N, Kobayashi J, Lerenthal Y, Krempler A, et al. (2007) Ataxia telangiectasia mutated (ATM) is essential for DNA-PKcs phosphorylations at the Thr-2609 cluster upon DNA double strand break. J Biol Chem 282: 6582-6587.
50. Tomimatsu N, Tahimic CG, Otsuki A, Burma S, Fukuhara A, et al. (2007) Ku70/80 modulates ATM and ATR signaling pathways in response to DNA double strand breaks. J Biol Chem 282: 10138-10145.
51. Li G, Nelsen C, Hendrickson EA, (2002) Ku86 is essential in human somatic cells. Proc Natl Acad Sci U S A 99: 832-837.
52. Uegaki K, Adachi N, So S, Iiizumi S, Koyama H, (2006) Heterozygous inactivation of human Ku70/Ku86 heterodimer does not affect cell growth, double-strand break repair, or genome integrity. DNA Repair (Amst) 5: 303-311.
53. Fattah FJ, Lichter NF, Fattah KR, Oh S, Hendrickson EA, (2008) Ku70, an essential gene, modulates the frequency of rAAV-mediated gene targeting in human somatic cells. Proc Natl Acad Sci U S A 105: 8703-8708.
54. Chapman JR, Taylor MR, Boulton SJ, (2012) Playing the end game: DNA double-strand break repair pathway choice. Mol Cell 47: 497-510.
55. Yamaguchi-Iwai Y, Sonoda E, Buerstedde JM, Bezzubova O, Morrison C, et al. (1998) Homologous recombination, but not DNA repair, is reduced in vertebrate cells deficient in RAD52. Mol Cell Biol 18: 6430-6435.
56. Toyoda E, Kagaya S, Cowell IG, Kurosawa A, kamoshita K, et al. (2008) NK314, a topoisomerase II inhibitor that specifically targets the alpha isoform. J Biol Chem 283: 23711-23720.
57. Iwabuchi K, Hashimoto M, Matsui T, Kurihara T, Shimizu H, et al. (2006) 53BP1 contributes to survival of cells irradiated with X-ray during G1 without Ku70 or Artemis. Genes Cells 11: 935-948.
58. Corneo B, Wendland RL, Deriano L, Cui X, Klein IA, et al. (2007) Rag mutations reveal robust alternative end joining. Nature 449: 483-486.
59. Simsek D, Brunet E, Wong SY, Katyal S, Gao Y, et al. (2011) DNA ligase III promotes alternative nonhomologous end-joining during chromosomal translocation formation. PLoS Genetics 7: e1002080.
60. Yan CT, Boboila C, Souza EK, Franco S, Hickernell TR, et al. (2007) IgH class switching and translocations use a robust non-classical end-joining pathway. Nature 449: 478-482.
61. Ma Y, Schwarz K, Lieber MR, (2005) The Artemis:DNA-PKcs endonuclease cleaves DNA loops, flaps, and gaps. DNA Repair (Amst) 4: 845-851.
62. Dobbs TA, Tainer JA, Lees-Miller SP, (2010) A structural model for regulation of NHEJ by DNA-PKcs autophosphorylation. DNA Repair (Amst) 9: 1307-1314.