Processing of DNA double strand breaks by alternative non-homologous end-joining in hyperacetylated chromatin

Genome Integrity

Volumn 3, Issue , 2012, Pages

  Manova, Vasilissa ^a,b   Singh, Satyendra K ^a   Iliakis, George ^a  

^a UNIVERSITY OF ESSEN MEDICAL SCHOOL   (Germany)

^b INSTITUTE OF PHYSIOLOGY   (Bulgaria)

Author keywords

Chromatin; Chromatin acetylation; DNA Double strand breaks (DSB); HDAC; Ionizing radiation (IR); NHEJ

Indexed keywords

CELL PROTEIN; DNA; HISTONE DEACETYLASE 2; PROTEIN LIG4; SMALL INTERFERING RNA; TRICHOSTATIN A; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CYCLE PHASE; CELL STRAIN HCT116; CHROMATIN; CHROMATIN ACETYLATION; CHROMATIN DEACETYLATION; CHROMATIN HYPERACETYLATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; DNA END JOINING REPAIR; DNA REPAIR; DOUBLE STRANDED DNA BREAK; EMBRYO; ENZYME INHIBITION; FIBROBLAST CULTURE; GENE; GENE SILENCING; GENETIC REGULATION; GLIOMA CELL; HDAC2 GENE; HISTONE ACETYLATION; HUMAN; HUMAN CELL; IONIZING RADIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE;

EID: 84867621675     PISSN: None     EISSN: 20419414     Source Type: Journal    
DOI: 10.1186/2041-9414-3-4     Document Type: Article

References (72)

1. McVey M, Lee SE. MMEJ repair of double-strand breaks (director's cut): deleted sequences and alternative endings. Trends Genet 2008, 24:529-538. 10.1016/j.tig.2008.08.007, 18809224.
2. Lieber MR. The Mechanism of Double-Strand DNA Break Repair by the Nonhomologous DNA End-Joining Pathway. Annu Rev Biochem 2010, 79:1.1-1.31.
3. Mladenov E, Iliakis G. Induction and repair of DNA double strand breaks: the increasing spectrum of non-homologous end joining pathways. Mutat Res Fundam Mol Mech Mutagen 2011, 711:61-72.
4. Iliakis G. Backup pathways of NHEJ in cells of higher eukaryotes: cell cycle dependence. Radiother Oncol 2009, 92:310-315. 10.1016/j.radonc.2009.06.024, 19604590.
5. Iliakis G, Wang H, Perrault AR, Boecker W, Rosidi B, Windhofer F, Wu W, Guan J, Terzoudi G, Pantelias G. Mechanisms of DNA double strand break repair and chromosome aberration formation. Cytogenet Genome Res 2004, 104:14-20. 10.1159/000077461, 15162010.
6. Iliakis G, Wu W, Wang M, Terzoudi GI, Pantelias GE. Backup Pathways of Nonhomologous End Joining May Have a Dominant Role in the Formation of Chromosome Aberrations. Chromosomal Alterations 2007, 67-85. Springer Verlag, Berlin, Obe G, Vijayalaxmi S, [Repair/NHEJ/Reviews SD (Series Editor).
7. Audebert M, Salles B, Calsou P. Involvement of Poly(ADP-ribose) Polymerase-1 and XRCC1/DNA Ligase III in an Alternative Route for DNA Double-strand Breaks Rejoining. J Biol Chem 2004, 279:55117-55126. 10.1074/jbc.M404524200, 15498778.
8. Wang H, Rosidi B, Perrault R, Wang M, Zhang L, Windhofer F, Iliakis G. DNA Ligase III as a Candidate Component of Backup Pathways of Nonhomologous End Joining. Cancer Res 2005, 65:4020-4030. 10.1158/0008-5472.CAN-04-3055, 15899791.
9. Simsek D, Brunet E, Wong SY-W, Katyal S, Gao Y, McKinnon PJ, Lou J, Zhang L, Li J, Rebar EJ, et al. DNA Ligase III Promotes Alternative Nonhomologous End-Joining during Chromosomal Translocation Formation. PLoS Genet 2011, 7:e1002080. 10.1371/journal.pgen.1002080, 3107202, 21655080.
10. Cotner-Gohara E, Kim I-K, Hammel M, Tainer JA, Tomkinson AE, Ellenberger T. Human DNA Ligase III Recognizes DNA Ends by Dynamic Switching between Two DNA-Bound States. Biochemistry 2010, 49:6165-6176. 10.1021/bi100503w, 2922849, 20518483.
11. Liang L, Deng L, Nguyen SC, Zhao X, Maulion CD, Shao C, Tischfield JA. Human DNA ligases I and III, but not ligase IV, are required for microhomology-mediated end joining of DNA double-strand breaks. Nucleic Acids Res 2008, 36:3297-3310. 10.1093/nar/gkn184, 2425475, 18440984.
12. Rosidi B, Wang M, Wu W, Sharma A, Wang H, Iliakis G. Histone H1 functions as a stimulatory factor in backup pathways of NHEJ. Nucleic Acids Res 2008, 36:1610-1623. 10.1093/nar/gkn013, 2275134, 18250087.
13. Poplawski T, Blasiak J. BCR/ABL downregulates DNA-PKCS-dependent and upregulates backup non-homologous end joining in leukemic cells. Mol Biol Rep 2010, 37:2309-2315. 10.1007/s11033-009-9730-0, 19697154.
14. Sallmyr A, Tomkinson AE, Rassool FV. Up-regulation of WRN and DNA ligase IIIα in chronic myeloid leukemia: consequences for the repair of DNA double-strand breaks. Blood 2008, 112:1413-1423. 10.1182/blood-2007-07-104257, 2967309, 18524993.
15. Rass E, Grabarz A, Plo I, Gautier J, Bertrand P, Lopez BS. Role of Mre11 in chromosomal nonhomologous end joining in mammalian cells. Nat Struct Mol Biol 2009, 16:819-825. 10.1038/nsmb.1641, 19633668.
16. Deriano L, Stracker TH, Baker A, Petrini JHJ, Roth DB. Roles for NBS1 in Alternative Nonhomologous End-Joining of V(D)J Recombination Intermediates. Mol Cell 2009, 34:13-25. 10.1016/j.molcel.2009.03.009, 2704125, 19362533.
17. Boboila C, Jankovic M, Yan CT, Wang JH, Wesemann DR, Zhang T, Fazeli A, Feldman L, Nussenzweig A, Nussenzweig M, Alt FW. Alternative end-joining catalyzes robust IgH locus deletions and translocations in the combined absence of ligase 4 and Ku70. Proc Natl Acad Sci USA 2010, 107:3034-3039. 10.1073/pnas.0915067107, 2840344, 20133803.
18. Boboila C, Yan C, Wesemann DR, Jankovic M, Wang JH, Manis J, Nussenzweig A, Nussenzweig M, Alt FW. Alternative end-joining catalyzes class switch recombination in the absence of both Ku70 and DNA ligase 4. J Exp Med 2010, 207:417-427. 10.1084/jem.20092449, 2822597, 20142431.
19. Simsek D, Jasin M. Alternative end-joining is suppressed by the canonical NHEJ component Xrcc4-ligase IV during chromosomal translocation formation. Nat Struct Mol Biol 2010, 17:410-416. 10.1038/nsmb.1773, 20208544.
20. Zhang Y, Jasin M. An essential role for CtIP in chromosomal translocation formation through an alternative end-joining pathway. Nat Struct Mol Biol 2011, 18:80-84. 10.1038/nsmb.1940, 3261752, 21131978.
21. Yan CT, Boboila C, Souza EK, Franco S, Hickernell TR, Murphy M, Gumaste S, Geyer M, Zarrin AA, Manis JP, et al. IgH class switching and translocations use a robust non-classical end-joining pathway. Nature 2007, 449:478-482. 10.1038/nature06020, 17713479.
22. Soulas-Sprauel P, Le Guyader G, Rivera-Munoz P, Abramowski V, Olivier-Martin C, Goujet-Zalc C, Charneau P, de Villartay J-P. Role for DNA repair factor XRCC4 in immunoglobulin class switch recombination. J Exp Med 2007, 204:1717-1727. 10.1084/jem.20070255, 2118634, 17606631.
23. Corneo B, Wendland RL, Deriano L, Cui X, Klein IA, Wong S-Y, Arnal S, Holub AJ, Weller GR, Pancake BA, et al. Rag mutations reveal robust alternative end joining. Nature 2007, 449:483-486. 10.1038/nature06168, 17898768.
24. Rai R, Zheng H, He H, Luo Y, Multani A, Carpenter PB, Chang S. The function of classical and alternative non-homologous end-joining pathways in the fusion of dysfunctional telomeres. EMBO J 2010, 29:2598-2610. 10.1038/emboj.2010.142, 2928694, 20588252.
25. Wu W, Wang M, Wu W, Singh SK, Mussfeldt T, Iliakis G. Repair of radiation induced DNA double strand breaks by backup NHEJ is enhanced in G2. DNA Repair (Amst) 2008, 7:329-338.
26. Wu W, Wang M, Mussfeldt T, Iliakis G. Enhanced Use of Backup Pathways of NHEJ in G2 in Chinese Hamster Mutant Cells with Defects in the Classical Pathway of NHEJ. Radiat Res 2008, 170:512-520. 10.1667/RR1456.1, 19024658.
27. Windhofer F, Wu W, Wang M, Singh SK, Saha J, Rosidi B, Iliakis G. Marked dependence on growth state of backup pathways of NHEJ. Int J Radiat Oncol Biol Phys 2007, 68:1462-1470. 10.1016/j.ijrobp.2007.04.038, 17674976.
28. Singh SK, Wu W, Zhang L, Klammer H, Wang M, Iliakis G. Widespread dependence of backup NHEJ on growth state: ramifications for the use of DNA-PK Inhibitors. Int J Radiat Oncol Biol Phys 2011, 79:540-548. 10.1016/j.ijrobp.2010.08.018, 20950945.
29. Singh SK, Bednar T, Zhang L, Wu W, Mladenov E, Iliakis G. Inhibition of B-NHEJ in Plateau-Phase Cells Is Not a Direct Consequence of Suppressed Growth Factor Signaling. Int J Radiat Oncol Biol Phys 2012, 84:e237-e243.. 10.1016/j.ijrobp.2012.03.060, 22658216.
30. Karagiannis TC, El-Osta A. Chromatin modifications and DNA double-strand breaks: the current state of play. Leukemia 2007, 21:195-200. 10.1038/sj.leu.2404478, 17151702.
31. Karagiannis TC, KN H, El-Osta A. Disparity of histone deacetylase inhibition on repair of radiation-induced DNA damage on euchromatin and constitutive heterochromatin compartments. Oncogene 2007, 26:3963-3971. 10.1038/sj.onc.1210174, 17213813.
32. McBlane F, Boyes J. Stimulation of V(D)J recombination by histone acetylation. Curr Biol 2000, 10:483-486. 10.1016/S0960-9822(00)00449-8, 10801420.
33. Miller KM, Tjeertes JV, Coates J, Legube G, Polo SE, Britton S, Jackson SP. Human HDAC1 and HDAC2 function in the DNA-damage response to promote DNA nonhomologous end-joining. Nat Struct Mol Biol 2010, 17:1144-1151. 10.1038/nsmb.1899, 3018776, 20802485.
34. Downs JA, Nussenzweig MC, Nussenzweig A. Chromatin dynamics and the preservation of genetic information. Nature 2007, 447:951-958. 10.1038/nature05980, 17581578.
35. Kinner A, Wu W, Staudt C, Iliakis G. γ-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res 2008, 36:5678-5694. 10.1093/nar/gkn550, 2553572, 18772227.
36. Groth A, Rocha W, Verreault A, Almouzni G. Chromatin challenges during DNA replication and repair. Cell 2007, 128:721-733. 10.1016/j.cell.2007.01.030, 17320509.
37. Misteli T, Soutoglou E. The emerging role of nuclear architecture in DNA repair and genome maintenance. Nat Rev Mol Cell Biol 2009, 10:243-254. 10.1038/nrm2651, 19277046.
38. Woodbine L, Brunton H, Goodarzi AA, Shibata A, Jeggo PA. Endogenously induced DNA double strand breaks arise in heterochromatic DNA regions and require ataxia telangiectasia mutated and Artemis for their repair. Nucleic Acids Res 2011, 39:6986-6997. 10.1093/nar/gkr331, 3167608, 21596788.
39. Goodarzi AA, Jeggo P, Lobrich M. The influence of heterochromatin on DNA double strand break repair: Getting the strong, silent type to relax. DNA Repair (Amst) 2010, 9:1273-1282.
40. Goodarzi AA, Noon AT, Deckbar D, Ziv Y, Shiloh Y, Löbrich M, Jeggo PA. ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol Cell 2008, 31:167-177. 10.1016/j.molcel.2008.05.017, 18657500.
41. Kouzarides T. Chromatin modifications and their function. Cell 2007, 128:693-705. 10.1016/j.cell.2007.02.005, 17320507.
42. Glozak MA, Seto E. Histone deacetylases and cancer. Oncogene 2007, 26:5420-5432. 10.1038/sj.onc.1210610, 17694083.
43. Yang X-J, Seto E. The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat Rev Mol Cell Biol 2008, 9:206-218. 10.1038/nrm2346, 2667380, 18292778.
44. de Ruijter AJ, van Gennip AH, Caron HN, Kemp S, van Kuilenburg AB. Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem J 2003, 370:737-749. 10.1042/BJ20021321, 1223209, 12429021.
45. Göttlicher M, Minucci S, Zhu P, Kramer OH, Schimpf A, Giavara S, Sleeman JP, Lo Coco F, Nervi C, Pelicci PG, Heinzel T. Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J 2001, 20:6969-6978. 10.1093/emboj/20.24.6969, 125788, 11742974.
46. Marchion DC, Bicaku E, Daud AI, Sullivan DM, Munster PN. Valproic Acid Alters Chromatin Structure by Regulation of Chromatin Modulation Proteins. Cancer Res 2005, 65:3815-3822. 10.1158/0008-5472.CAN-04-2478, 15867379.
47. Kim DH, Kim M, Kwon HJ. Histone deacetylase in carcinogenesis and its inhibitors as anti-cancer agents. J Biochem Mol Biol 2003, 36:110-119. 10.5483/BMBRep.2003.36.1.110, 12542981.
48. Tóth KF, Knoch TA, Wachsmuth M, Frank-Stöhr M, Stöhr M, Bacher CP, Müller G, Rippe K. Trichostatin A-induced histone acetylation causes decondensation of interphase chromatin. J Cell Sci 2004, 117:4277-4287. 10.1242/jcs.01293, 15292402.
49. Koeller KM, Haggarty SJ, Perkins BD, Leykin I, Wong JC, Kao M-CJ, Schreiber SL. Chemical genetic modifier screens: small molecule trichostatin suppressors as probes of intracellular histone and tubulin acetylation. Chem Biol 2003, 10:397-410. 10.1016/S1074-5521(03)00093-0, 12770822.
50. Murr R, Loizou JI, Yang Y-G, Cuenin C, Li H, Wang Z-Q, Herceg Z. Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nat Cell Biol 2006, 8:91-99. 10.1038/ncb1343, 16341205.
51. Karagiannis TC, El-Osta A. Modulation of cellular radiation responses by histone deacetylase inhibitors. Oncogene 2006, 25:3885-3893. 10.1038/sj.onc.1209417, 16462761.
52. Koprinarova M, Botev P, Russev G. Histone deacetylase inhibitor sodium butyrate enhances cellular radiosensitivity by inhibiting both DNA nonhomologous end joining and homologous recombination. DNA Repair (Amst) 2011, 10:970-977.
53. Green CM, Almouzni G. When repair meets chromatin - First in series on chromatin dynamics. EMBO Rep 2002, 31:28-33.
54. Kanaar R, Hoeijmakers JHJ, van Gent DC. Molecular mechanisms of DNA double-strand break repair. Trends Cell Biol 1998, 8:483-489. 10.1016/S0962-8924(98)01383-X, 9861670.
55. Rief N, Löbrich M. Efficient Rejoining of Radiation-induced DNA Double-strand Breaks in Centromeric DNA of Human Cells. J Biol Chem 2002, 277:20572-20582. 10.1074/jbc.M200265200, 11927583.
56. Sak A, Stuschke M. Repair of ionizing radiation induced DNA double-strand breaks (dsb) at the c-myc locus in comparison to the overall genome. Int J Radiat Biol 1998, 73:35-43. 10.1080/095530098142680, 9464475.
57. Goodarzi AA, Noon AT, Jeggo PA. The impact of heterochromatin on DSB repair. Biochem Soc Trans 2009, 37:569-576. 10.1042/BST0370569, 19442252.
58. Iliakis GE, Cicilioni O, Metzger L. Measurement of DNA double strand breaks in CHO cells at various stages of the cell cycle using pulsed field gel electrophoresis: Calibrations by means of 125I decay. Int J Radiat Biol 1991, 59:343-357. 10.1080/09553009114550321, 1671686.
59. Su H, Altucci L, You Q. Competitive or noncompetitive, that's the question: research toward histone deacetylase inhibitors. Mol Cancer Ther 2008, 7:1007-1012. 10.1158/1535-7163.MCT-07-2289, 18483291.
60. Marchion DC, Bicaku E, Turner JG, Schmitt ML, Morelli DR, Munster PN. HDAC2 regulates chromatin plasticity and enhances DNA vulnerability. Mol Cancer Ther 2009, 8:794-801. 10.1158/1535-7163.MCT-08-0985, 19372552.
61. Storch K, Eke I, Borgmann K, Krause M, Richter C, Becker K, Schrock E, Cordes N. Three-Dimensional Cell Growth Confers Radioresistance by Chromatin Density Modification. Cancer Res 2010, 70:3925-3934. 10.1158/0008-5472.CAN-09-3848, 20442295.
62. Schrump DS. Cytotoxicity Mediated by Histone Deacetylase Inhibitors in Cancer Cells: Mechanisms and Potential Clinical Implications. Clin Cancer Res 2009, 15:3947-3957. 10.1158/1078-0432.CCR-08-2787, 19509170.
63. Moreira J, Scheipers P, Sorensen P. The histone deacetylase inhibitor Trichostatin A modulates CD4+ T cell responses. BMC Cancer 2003, 3:30. 10.1186/1471-2407-3-30, 280656, 14606959.
64. Choi YH. Induction of apoptosis by trichostatin A, a histone deacetylase inhibitor, is associated with inhibition of cyclooxygenase-2 activity in human non-small cell lung cancer cells. Int J Oncol 2005, 27:473-479.
65. Singh SK, Wu W, Wu W, Wang M, Iliakis G. Extensive Repair of DNA Double-Strand Breaks in Cells Deficient in the DNA-PK Dependent Pathway of NHEJ after Exclusion of Heat-Labile Sites. Radiat Res 2009, 172:152-164. 10.1667/RR1745.1, 19630520.
66. Stoilov L, Darroudi F, Meschini R, van der Schans G, Mullenders LHF, Natarajan AT. Inhibition of repair of X-ray-induced DNA double-strand breaks in human lymphocytes exposed to sodium butyrate. Int J Radiat Biol 2000, 76:1485-1491. 10.1080/09553000050176243, 11098851.
67. Xu Y, Price BD. Chromatin dynamics and the repair of DNA double strand breaks. Cell Cycle 2011, 10:261-267. 10.4161/cc.10.2.14543, 3048797, 21212734.
68. Frank KM, Sharpless NE, Gao Y, Sekiguchi JM, Fergson DO, Zhu C, Manis JP, Horner J, DePinho RA, Alt FW. DNA ligase IV deficiency in mice leads to defective neurogenesis and embryonic lethality via the p53 pathway. Mol Cell 2000, 5:993-1002. 10.1016/S1097-2765(00)80264-6, 10911993.
69. Allalunis-Turner MJ, Barron GM, Day RS, Dobler KD, Mirzayans R. Isolation of two cell lines from a human malignant glioma specimen differing in sensitivity to radiation and chemotherapeutic drugs. Radiat Res 1993, 134:349-354. 10.2307/3578196, 8316628.
70. Fattah F, Lee EH, Weisensel N, Wang Y, Lichter N, Hendrickson EA. Ku Regulates the Non-Homologous End Joining Pathway Choice of DNA Double-Strand Break Repair in Human Somatic Cells. PLoS Genet 2010, 6:e1000855. 10.1371/journal.pgen.1000855, 2829059, 20195511.
71. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29:2002-2007.
72. DiBiase SJ, Zeng Z-C, Chen R, Hyslop T, Curran WJ, Iliakis G. DNA-dependent protein kinase stimulates an independently active, nonhomologous, end-joining apparatus. Cancer Res 2000, 60:1245-1253.