Sister chromatid telomere fusions, but not NHEJmediated inter-chromosomal telomere fusions, occur independently of DNA ligases 3 and 4

Genome Research

Volumn 26, Issue 5, 2016, Pages 588-600

  Liddiard, Kate ^a   Ruis, Brian ^b   Takasugi, Taylor ^b   Harvey, Adam ^b   Ashelford, Kevin E ^a   Hendrickson, Eric A ^b   Baird, Duncan M ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA LIGASE; DNA LIGASE 3; DNA LIGASE 4; PROTEIN P53; UNCLASSIFIED DRUG; ATP DEPENDENT DNA LIGASE; LIG4 PROTEIN, HUMAN; TP53 PROTEIN, HUMAN;

ARTICLE; CHROMOSOMES AND CHROMOSOMAL PHENOMENA; CONTROLLED STUDY; DNA END JOINING REPAIR; DOUBLE STRANDED DNA BREAK; GENE INACTIVATION; GENE LOCUS; GENETIC CODE; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; HUMAN GENOME; INTER CHROMOSOMAL TELOMERE FUSION; PRIORITY JOURNAL; SISTER CHROMATID; SISTER CHROMATID TELOMERE FUSION; TELOMERE; CHROMATID; GENE DELETION; GENETICS; HUMAN CHROMOSOME; METABOLISM; NEOPLASM; TUMOR CELL LINE;

CELL LINE, TUMOR; CHROMATIDS; CHROMOSOMES, HUMAN; DNA BREAKS, DOUBLE-STRANDED; DNA END-JOINING REPAIR; DNA LIGASE ATP; GENE DELETION; HUMANS; NEOPLASMS; TELOMERE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84964961415     PISSN: 10889051     EISSN: 15495469     Source Type: Journal    
DOI: 10.1101/gr.200840.115     Document Type: Article

References (75)

1. Abu-Odeh M, Salah Z, Herbel C, Hofmann TG, Aqeilan RI. 2014. WWOX, the common fragile site FRA16D gene product, regulates ATMactivation and the DNA damage response. Proc Natl Acad Sci 111: E4716-E4725.
2. Akyüz N, Boehden GS, Süsse S, Rimek A, Preuss U, Scheidtmann KH, Wiesmüller L. 2002. DNA substrate dependence of p53-mediated regulation of double-strand break repair. Mol Cell Biol 22: 6306-6317.
3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. 1990. Basic local alignment search tool. J Mol Biol 215: 403-410.
4. Arakawa H, Bednar T, Wang M, Paul K, Mladenov E, Bencsik-Theilen AA, Iliakis G. 2012. Functional redundancy between DNA ligases I and III in DNA replication in vertebrate cells. Nucleic Acids Res 40: 2599-2610.
5. Baird DM, Rowson J, Wynford-Thomas D, Kipling D. 2003. Extensive allelic variation and ultrashort telomeres in senescent human cells. Nat Genet 33: 203-207.
6. Boboila C, Alt FW, Schwer B. 2012. Classical and alternative end-joining pathways for repair of lymphocyte-specific and general DNA doublestrand breaks. Adv Immunol 116: 1-49.
7. Britt-Compton B, Rowson J, Locke M, Mackenzie I, Kipling D, Baird DM. 2006. Structural stability and chromosome-specific telomere length is governed by cis-acting determinants in humans. Hum Mol Genet 15: 725-733.
8. Bunz F, Dutriaux A, Lengauer C, Waldman T, Zhou S, Brown JP, Sedivy JM, KinzlerKW, Vogelstein B. 1998. Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282: 1497-1501.
9. Capper R, Britt-Compton B, Tankimanova M, Rowson J, Letsolo B, Man S, Haughton M, Baird DM. 2007. The nature of telomere fusion and a definition of the critical telomere length in human cells. Genes Dev 21: 2495-2508.
10. Ceccaldi R, Liu JC, Amunugama R, Hajdu I, Primack B, Petalcorin MI, O'Connor KW, Konstantinopoulos PA, Elledge SJ, Boulton SJ, et al. 2015. Homologous-recombination-deficient tumours are dependent on PolΘ-mediated repair. Nature 518: 258-262.
11. Cer RZ, Donohue DE, Mudunuri US, Temiz NA, Loss MA, Starner NJ, Halusa GN, Volfovsky N, Yi M, Luke BT, et al. 2013. Non-B DB v2.0: a database of predicted non-B DNA-forming motifs and its associated tools. Nucleic Acids Res 41: D94-D100.
12. Chebel A, Rouault JP, Urbanowicz I, Baseggio L, Chien WW, Salles G, Ffrench M. 2009. Transcriptional activation of hTERT, the human telomerase reverse transcriptase, by nuclear factor of activated T cells. J Biol Chem 284: 35725-35734.
13. Chow TT, Zhao Y, Mak SS, Shay JW, Wright WE. 2012. Early and late steps in telomere overhang processing in normal human cells: The position of the final RNA primer drives telomere shortening. Genes Dev 26: 1167-1178.
14. Cohanim AB, Haran TE. 2009. The coexistence of the nucleosome positioning code with the genetic code on eukaryotic genomes. Nucleic Acids Res 37: 6466-6476.
15. Cooper DN, Bacolla A, Férec C, Vasquez KM, Kehrer-Sawatzki H, Chen JM. 2011. On the sequence-directed nature of human gene mutation: the role of genomic architecture and the local DNA sequence environment in mediating gene mutations underlying human inherited disease. Hum Mutat 32: 1075-1099.
16. Costantini M, Clay O, Auletta F, Bernardi G. 2006. An isochore map of human chromosomes. Genome Res 16: 536-541.
17. Counter CM, Avilion AA, LeFeuvre CE, Stewart NG, GreiderCW, Harley CB, Bacchetti S. 1992. Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J 11: 1921-1929.
18. Cowell JK, Miller OJ. 1983. Occurrence and evolution of homogeneously staining regions may be due to breakage-fusion-bridge cycles following telomere loss. Chromosoma 88: 216-221.
19. Cunningham F, Amode MR, Barrell D, Beal K, Billis K, Brent S, Carvalho- Silva D, Clapham P, Coates G, Fitzgerald S, et al. 2015. Ensembl 2015. Nucleic Acids Res 43: D662-D669.
20. Cuthbert AP, Bond J, Trott DA, Gill S, Broni J, Marriott A, Khoudoli G, Parkinson EK, Cooper CS, Newbold RF. 1999. Telomerase repressor sequences on chromosome 3 and induction of permanent growth arrest in human breast cancer cells. J Natl Cancer Inst 91: 37-45.
21. Davoli T, Denchi EL, de Lange T. 2010. Persistent telomere damage induces bypass of mitosis and tetraploidy. Cell 141: 81-93.
22. de Lange T. 2005. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev 19: 2100-2110.
23. Doyle EL, Booher NJ, Standage DS, Voytas DF, Brendel VP, Vandyk JK, Bogdanove AJ. 2012. TAL Effector-Nucleotide Targeter (TALE-NT) 2.0: tools for TAL effector design and target prediction. Nucleic Acids Res 40: W117-W122.
24. Escribano-Díaz C, Orthwein A, Fradet-Turcotte A, Xing M, Young JT, Tkáč J, Cook MA, Rosebrock AP, Munro M, Canny MD, et al. 2013. A cell cycledependent regulatory circuit composed of 53BP1-RIF1 and BRCA1-CtIP controls DNA repair pathway choice. Mol Cell 49: 872-883.
25. Farré M, Robinson TJ, Ruiz-Herrera A. 2015. An Integrative Breakage Model of genome architecture, reshuffling and evolution: the Integrative Breakage Model of genome evolution, a novel multidisciplinary hypothesis for the study of genome plasticity. Bioessays 37: 479-488.
26. Fernandez-Vidal A, Guitton-Sert L, Cadoret JC, Drac M, Schwob E, Baldacci G, Cazaux C, Hoffmann JS. 2014. A role for DNA polymerase Θ in the timing of DNA replication. Nat Commun 5: 4285.
27. Ghezraoui H, Piganeau M, Renouf B, Renaud JB, Sallmyr A, Ruis B, Oh S, Tomkinson AE, Hendrickson EA, Giovannangeli C, et al. 2014. Chromosomal translocations in human cells are generated by canonical nonhomologous end-joining. Mol Cell 55: 829-842.
28. Gu S, Yuan B, Campbell IM, Beck CR, Carvalho CM, Nagamani SC, Erez A, Patel A, Bacino CA, Shaw CA, et al. 2015. Alu-mediated diverse and complex pathogenic copy-number variants within human chromosome 17 at p13.3. Hum Mol Genet 24: 4061-4077.
29. Hartwell L. 1992. Defects in a cell cycle checkpoint may be responsible for the genomic instability of cancer cells. Cell 71: 543-546.
30. Hayashi MT, Cesare AJ, Rivera T, Karlseder J. 2015. Cell death during crisis is mediated by mitotic telomere deprotection. Nature 522: 492-496.
31. Hoffmeyer K, Raggioli A, Rudloff S, Anton R, Hierholzer A, Del Valle I, Hein K, Vogt R, Kemler R. 2012. Wnt/ß-catenin signaling regulates telomerase in stem cells and cancer cells. Science 336: 1549-1554.
32. Johnson RE, Klassen R, Prakash L, Prakash S. 2015. A major role of DNA polymerase δ in replication of both the leading and lagging DNA strands. Mol Cell 59: 163-175.
33. Jones RE, Oh S, Grimstead JW, Zimbric J, Roger L, Heppel NH, Ashelford KE, Liddiard K, Hendrickson EA, Baird DM. 2014. Escape from telomeredriven crisis is DNA ligase III dependent. Cell Rep 8: 1063-1076.
34. Kent WJ, SugnetCW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D. 2002. The human genome browser at UCSC. Genome Res 12: 996-1006.
35. Khan IF, Hirata RK, Russell DW. 2011. AAV-mediated gene targeting methods for human cells. Nat Protoc 6: 482-501.
36. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA. 2009. Circos: an information aesthetic for comparative genomics. Genome Res 19: 1639-1645.
37. Kyo S, Takakura M, Taira T, Kanaya T, Itoh H, Yutsudo M, Ariga H, Inoue M. 2000. Sp1 cooperates with c-Myc to activate transcription of the human telomerase reverse transcriptase gene (hTERT). Nucleic Acids Res 28: 669-677.
38. Letsolo BT, Rowson J, Baird DM. 2010. Fusion of short telomeres in human cells is characterized by extensive deletion and microhomology, and can result in complex rearrangements. Nucleic Acids Res 38: 1841-1852.
39. Li H. 2014. Toward better understanding of artifacts in variant calling from high-coverage samples. Bioinformatics 30: 2843-2851.
40. Li Q, Yoshioka N, Yutsudo M, Inafuku S, Aozasa K, Kitamura Y, Aizawa S, Nishimune Y, Hakura A, Kondoh G. 1998. Human papillomavirus-induced carcinogenesis with p53 deficiency in mouse: novel lymphomagenesis in HPV16E6E7 transgenic mice mimicking p53 defect. Virology 252: 28-33.
41. Li AY, Lin HH, Kuo CY, Shih HM, Wang CC, Yen Y, Ann DK. 2011. Highmobility group A2 protein modulates hTERT transcription to promote tumorigenesis. Mol Cell Biol 31: 2605-2617.
42. Lin TT, Norris K, Heppel NH, Pratt G, Allan JM, Allsup DJ, Bailey J, Cawkwell L, Hills R, Grimstead JW, et al. 2014. Telomere dysfunction accurately predicts clinical outcome in chronic lymphocytic leukaemia, even in patients with early stage disease. Br J Haematol 167: 214-223.
43. Lormand JD, Buncher N, Murphy CT, Kaur P, Lee MY, Burgers P, Wang H, Kunkel TA, Opresko PL. 2013. DNA polymerase δ stalls on telomeric lagging strand templates independently from G-quadruplex formation. Nucleic Acids Res 41: 10323-10333.
44. Lowden MR, Flibotte S, Moerman DG, Ahmed S. 2011. DNA synthesis generates terminal duplications that seal end-to-end chromosome fusions. Science 332: 468-471.
45. Lu G, Duan J, Shu S, Wang X, Gao L, Guo J, Zhang Y. 2016. Ligase I and ligase III mediate the DNA double-strand break ligation in alternative end-joining. Proc Natl Acad Sci 113: 1256-1260.
46. Lujan SA, Williams JS, Pursell ZF, Abdulovic-Cui AA, Clark AB, Nick McElhinny SA, Kunkel TA. 2012. Mismatch repair balances leading and lagging strand DNA replication fidelity. PLoS Genet 8: e1003016.
47. Luo Y, Hermetz KE, Jackson JM, Mulle JG, Dodd A, Tsuchiya KD, Ballif BC, Shaffer LG, Cody JD, Ledbetter DH, et al. 2011. Diverse mutational mechanisms cause pathogenic subtelomeric rearrangements. Hum Mol Genet 20: 3769-3778.
48. Ma X, Rogacheva MV, Nishant KT, Zanders S, Bustamante CD, Alani E. 2012. Mutation hot spots in yeast caused by long-range clustering of homopolymeric sequences. Cell Rep 1: 36-42.
49. Mateos-Gomez PA, Gong F, Nair N, Miller KM, Lazzerini-Denchi E, Sfeir A. 2015. Mammalian polymerase Θ promotes alternative NHEJ and suppresses recombination. Nature 518: 254-257.
50. Miller D, Reynolds GE, Mejia R, Stark JM, Murnane JP. 2011. Subtelomeric regions inmammalian cells are deficient in DNA double-strand break repair. DNA Repair 10: 536-544.
51. Minca EC, Kowalski D. 2011. Replication fork stalling by bulky DNA damage: localization at active origins and checkpoint modulation. Nucleic Acids Res 39: 2610-2623.
52. Mizuno K, Miyabe I, Schalbetter SA, Carr AM, Murray JM. 2013. Recombination-restarted replication makes inverted chromosome fusions at inverted repeats. Nature 493: 246-249.
53. Muraki K, Han L, Miller D, Murnane JP. 2015. Processing by MRE11 is involved in the sensitivity of subtelomeric regions to DNA double-strand breaks. Nucleic Acids Res 43: 7911-7930.
54. Murnane JP. 2010. Telomere loss as a mechanism for chromosome instability in human cancer. Cancer Res 70: 4255-4259.
55. Nick McElhinny SA, Havener JM, Garcia-Diaz M, Juárez R, Bebenek K, Kee BL, Blanco L, Kunkel TA, Ramsden DA. 2005. A gradient of template dependence defines distinct biological roles for family X polymerases in nonhomologous end joining. Mol Cell 19: 357-66.
56. Nick McElhinny SA, Gordenin DA, Stith CM, Burgers PM, Kunkel TA. 2008. Division of labor at the eukaryotic replication fork. Mol Cell 30: 137-144.
57. Oh S, Wang Y, Zimbric J, Hendrickson EA. 2013. Human LIGIV is synthetically lethal with the loss of Rad54B-dependent recombination and is required for certain chromosome fusion events induced by telomere dysfunction. Nucleic Acids Res 41: 1734-1749.
58. Oh S, Harvey A, Zimbric J, Wang Y, Nguyen T, Jackson PJ, Hendrickson EA. 2014. DNA ligase III and DNA ligase IV carry out genetically distinct forms of end joining in human somatic cells. DNA Repair 21: 97-110.
59. Ozeri-Galai E, Lebofsky R, Rahat A, Bester AC, Bensimon A, Kerem B. 2011. Failure of origin activation in response to fork stalling leads to chromosomal instability at fragile sites. Mol Cell 43: 122-131.
60. Pascal JM, Ellenberger T. 2015. The rise and fall of poly(ADP-ribose): an enzymatic perspective. DNA Repair 32: 10-16.
61. Pratto F, Brick K, Khil P, Smagulova F, Petukhova GV, Camerini-Otero RD. 2014. DNA recombination. Recombination initiation maps of individual human genomes. Science 346: 1256442.
62. Pruitt KD, Brown GR, Hiatt SM, Thibaud-Nissen F, Astashyn A, Ermolaeva O, Farrell CM, Hart J, Landrum MJ, McGarvey KM, et al. 2014. RefSeq: an update on mammalian reference sequences. Nucleic Acids Res 42: D756-D763.
63. Rai R, Zheng H, He H, Luo Y, Multani A, Carpenter PB, Chang S. 2010. The function of classical and alternative non-homologous end-joining pathways in the fusion of dysfunctional telomeres. EMBO J 29: 2598-2610.
64. Reijns MA, Kemp H, Ding J, de Procé SM, Jackson AP, Taylor MS. 2015. Lagging-strand replication shapes the mutational landscape of the genome. Nature 518: 502-506.
65. Shay JW, Wright WE, Brasiskyte D, Van der Haegen BA. 1993. E6 of human papillomavirus type 16 can overcome the M1 stage of immortalization in human mammary epithelial cells but not in human fibroblasts. Oncogene 8: 1407-1413.
66. Shibata A, Conrad S, Birraux J, Geuting V, Barton O, Ismail A, Kakarougkas A, Meek K, Taucher-Scholz G, Löbrich M, et al. 2011. Factors determining DNA double-strand break repair pathway choice in G2 phase. EMBO J 30: 1079-1092.
67. Stamatoyannopoulos JA, Adzhubei I, Thurman RE, Kryukov GV, Mirkin SM, Sunyaev SR. 2009. Human mutation rate associated with DNA replication timing. Nat Genet 41: 393-395.
68. Stith CM, Sterling J, Resnick MA, Gordenin DA, Burgers PM. 2008. Flexibility of eukaryotic Okazaki fragment maturation through regulated strand displacement synthesis. J Biol Chem 283: 34129-34140.
69. Stohr BA, Xu L, Blackburn EH. 2010. The terminal telomeric DNA sequence determines the mechanism of dysfunctional telomere fusion. Mol Cell 39: 307-314.
70. Stong N, Deng Z, Gupta R, Hu S, Paul S, Weiner AK, Eichler EE, Graves T, Fronick CC, Courtney L, et al. 2014. Subtelomeric CTCF and cohesin binding site organization using improved subtelomere assemblies and a novel annotation pipeline. Genome Res 24: 1039-1050.
71. Supek F, Lehner B. 2015. Differential DNA mismatch repair underlies mutation rate variation across the human genome. Nature 521: 81-84.
72. Thys RG, Lehman CE, Pierce LC, Wang YH. 2015. DNA secondary structure at chromosomal fragile sites in human disease. Curr Genomics 16: 60-70.
73. Tutton S, Azzam GA, Stong N, Vladimirova O, Wiedmer A, Monteith JA, Beishline K, Wang Z, Deng Z, Riethman H, et al. 2015. Subtelomeric p53 binding prevents accumulation of DNA damage at human telomeres. EMBO J 35: 193-207.
74. Vissers LE, Bhatt SS, Janssen IM, Xia Z, Lalani SR, Pfundt R, Derwinska K, de Vries BB, Gilissen C, Hoischen A, et al. 2009. Rare pathogenic microdeletions and tandem duplications are microhomology-mediated and stimulated by local genomic architecture. Hum Mol Genet 18: 3579-3593.
75. Yousefzadeh MJ, Wyatt DW, Takata K, Mu Y, Hensley SC, Tomida J, Bylund GO, Doublié S, Johansson E, Ramsden DA, et al. 2014. Mechanism of suppression of chromosomal instability by DNA polymerase POLQ. PLoS Genet 10: e1004654.