Dynamics of double strand breaks and chromosomal translocations

Molecular Cancer

Volumn 13, Issue 1, 2014, Pages

  Iarovaia, Olga V ^a,c   Rubtsov, Mikhail ^c,d   Ioudinkova, Elena ^a,c   Tsfasman, Tatiana ^b,c   Razin, Sergey V ^a,c,d   Vassetzky, Yegor S ^b,c,d  

^a INSTITUTE OF GENE BIOLOGY   (Russian Federation)

^b UMR 8126   (France)

^c LIA1066   (France)

^d MOSCOW STATE UNIVERSITY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; DNA TOPOISOMERASE (ATP HYDROLYSING); DOUBLE STRANDED DNA; GYRASE INHIBITOR; HISTONE H2A; HISTONE H2AX; RAG1 PROTEIN; RAG2 PROTEIN;

CARCINOGENESIS; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME TRANSLOCATION; DNA END JOINING REPAIR; DNA REPAIR; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; EUKARYOTE; GENE REARRANGEMENT; HUMAN; IONIZING RADIATION; MEIOTIC RECOMBINATION; MOLECULAR MECHANICS; NONHUMAN; OXIDATIVE STRESS; PROTEIN PROCESSING; RECIPROCAL CHROMOSOME TRANSLOCATION; RECOMBINATION REPAIR; REVIEW; SOMATIC MUTATION; SPECIES DIFFERENCE; VDJ RECOMBINATION; VIRUS INFECTION; YEAST CELL;

EID: 84928801909     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-13-249     Document Type: Review

References (99)

1. Boveri T: Concerning the origin of malignant tumours by Theodor Boveri. Translated and annotated by Henry Harris. J Cell Sci 1914,121(Suppl 1):1-84.
2. Lieber MR: Pathological and physiological double-strand breaks: roles in cancer, aging, and the immune system. Am J Pathol 1, 153:1323-1332. 10.1016/S0002-9440(10)65716-1
3. Meaburn KJ, Misteli T, Soutoglou E: Spatial genome organization in the formation of chromosomal translocations. Semin Cancer Biol 1, 17:80-90. 10.1016/j.semcancer.2006.10.008
4. Nikiforova MN, Stringer JR, Blough R, Medvedovic M, Fagin JA, Nikiforov YE: Proximity of chromosomal loci that participate in radiation-induced rearrangements in human cells. Science 1, 290:138-141. 10.1126/science.290.5489.138
5. Osborne CS, Chakalova L, Mitchell JA, Horton A, Wood AL, Bolland DJ, Corcoran AE, Fraser P: Myc dynamically and preferentially relocates to a transcription factory occupied by Igh . PLoS Biol 1, 5:e192. 10.1371/journal.pbio.0050192
6. Falk M, Lukasova E, Kozubek S: Higher-order chromatin structure in DSB induction, repair and misrepair. Mutat Res 1, 704:88-100. 10.1016/j.mrrev.2010.01.013
7. Razin SV, Petrov A, Hair A, Vassetzky YS: Chromatin domains and territories: flexibly rigid. Crit Rev Eukaryot Gene Expr 1, 14:79-88. 10.1615/CritRevEukaryotGeneExpr.v14.i12.50
8. Glukhov SI, Rubtsov MA, Alexeyevsky DA, Alexeevski AV, Razin SV, Iarovaia OV: The broken MLL gene is frequently located outside the inherent chromosome territory in human lymphoid cells treated with DNA topoisomerase II poison etoposide. PLoS One 1, 8:e75871. 10.1371/journal.pone.0075871
9. Pfeiffer P, Goedecke W, Obe G: Mechanisms of DNA double-strand break repair and their potential to induce chromosomal aberrations. Mutagenesis 1, 15:289-302. 10.1093/mutage/15.4.289
10. Maizels N: Immunoglobulin gene diversification. Annu Rev Genet 1, 39:23-46. 10.1146/annurev.genet.39.073003.110544
11. Weitzman MD, Lilley CE, Chaurushiya MS: Genomes in conflict: maintaining genome integrity during virus infection. Annu Rev Microbiol 1, 64:61-81. 10.1146/annurev.micro.112408.134016
12. Keeney S, Neale MJ: Initiation of meiotic recombination by formation of DNA double-strand breaks: mechanism and regulation. Biochem Soc Trans 1, 34:523-525. 10.1042/BST0340523
13. Brugmans L, Kanaar R, Essers J: Analysis of DNA double-strand break repair pathways in mice. Mutat Res 1, 614:95-108. 10.1016/j.mrfmmm.2006.01.022
14. Lieber MR: The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu Rev Biochem 1, 79:181-211. 10.1146/annurev.biochem.052308.093131
15. Alt FW, Zhang Y, Meng FL, Guo C, Schwer B: Mechanisms of programmed DNA lesions and genomic instability in the immune system. Cell 1, 152:417-429. 10.1016/j.cell.2013.01.007
16. Gostissa M, Alt FW, Chiarle R: Mechanisms that promote and suppress chromosomal translocations in lymphocytes. Annu Rev Immunol 1, 29:319-350. 10.1146/annurev-immunol-031210-101329
17. Kruhlak MJ, Celeste A, Dellaire G, Fernandez-Capetillo O, Muller WG, McNally JG, Bazett-Jones DP, Nussenzweig A: Changes in chromatin structure and mobility in living cells at sites of DNA double-strand breaks. J Cell Biol 1, 172:823-834. 10.1083/jcb.200510015
18. Falk M, Lukasova E, Gabrielova B, Ondrej V, Kozubek S: Chromatin dynamics during DSB repair. Biochim Biophys Acta 1, 1773:1534-1545. 10.1016/j.bbamcr.2007.07.002
19. Jakob B, Splinter J, Durante M, Taucher-Scholz G: Live cell microscopy analysis of radiation-induced DNA double-strand break motion. Proc Natl Acad Sci U S A 1, 106:3172-3177. 10.1073/pnas.0810987106
20. Nelms BE, Maser RS, MacKay JF, Lagally MG, Petrini JH: In situ visualization of DNA double-strand break repair in human fibroblasts. Science 1, 280:590-592. 10.1126/science.280.5363.590
21. Soutoglou E, Dorn JF, Sengupta K, Jasin M, Nussenzweig A, Ried T, Danuser G, Misteli T: Positional stability of single double-strand breaks in mammalian cells. Nat Cell Biol 1, 9:675-682. 10.1038/ncb1591
22. Dion V, Kalck V, Horigome C, Towbin BD, Gasser SM: Increased mobility of double-strand breaks requires Mec1, Rad9 and the homologous recombination machinery. Nat Cell Biol 2012, 14:502-509. 10.1038/ncb2465
23. Aten JA, Stap J, Krawczyk PM, Van Oven CH, Hoebe RA, Essers J, Kanaar R: Dynamics of DNA double-strand breaks revealed by clustering of damaged chromosome domains. Science 1, 303:92-95. 10.1126/science.1088845
24. Mine-Hattab J, Rothstein R: Increased chromosome mobility facilitates homology search during recombination. Nat Cell Biol 1, 14:510-517. 10.1038/ncb2472
25. Soutoglou E, Misteli T: Mobility and immobility of chromatin in transcription and genome stability. Curr Opin Genet Dev 1, 17:435-442. 10.1016/j.gde.2007.08.004
26. Mine-Hattab J, Rothstein R: DNA in motion during double-strand break repair. Trends Cell Biol 1, 23:529-536. 10.1016/j.tcb.2013.05.006
27. Foray N, Colin C: Relationship between radiosensitivity, initial DNA damage, apoptosis and gene expression: between reproducible works and technical artefacts. Breast 1, 22:185. 10.1016/j.breast.2013.01.008
28. Prise KM, Ahnstrom G, Belli M, Carlsson J, Frankenberg D, Kiefer J, Lobrich M, Michael BD, Nygren J, Simone G, Stenerlow B: A review of dsb induction data for varying quality radiations. Int J Radiat Biol 1, 74:173-184. 10.1080/095530098141564
29. Krawczyk PM, Stap J, Hoebe RA, Van Oven CH, Kanaar R, Aten JA: Analysis of the mobility of DNA double-strand break-containing chromosome domains in living mammalian cells. Methods Mol Biol 1, 463:309-320. 10.1007/978-1-59745-406-3_19
30. Roukos V, Voss TC, Schmidt CK, Lee S, Wangsa D, Misteli T: Spatial dynamics of chromosome translocations in living cells. Science 1, 341:660-664. 10.1126/science.1237150
31. Henikoff S: Conspiracy of silence among repeated transgenes. Bioessays 1, 20:532-535. 10.1002/(SICI)1521-1878(199807)20:7<532::AID-BIES3>3.0.CO;2-M
32. Dubarry M, Loiodice I, Chen CL, Thermes C, Taddei A: Tight protein-DNA interactions favor gene silencing. Genes Dev 1, 25:1365-1370. 10.1101/gad.611011
33. Lisby M, Mortensen UH, Rothstein R: Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat Cell Biol 1, 5:572-577. 10.1038/ncb997
34. Oza P, Peterson CL: Opening the DNA repair toolbox: localization of DNA double strand breaks to the nuclear periphery. Cell Cycle 1, 9:43-49. 10.4161/cc.9.1.10317
35. Therizols P, Fairhead C, Cabal GG, Genovesio A, Olivo-Marin JC, Dujon B, Fabre E: Telomere tethering at the nuclear periphery is essential for efficient DNA double strand break repair in subtelomeric region. J Cell Biol 1, 172:189-199. 10.1083/jcb.200505159
36. Taddei A, Van Houwe G, Hediger F, Kalck V, Cubizolles F, Schober H, Gasser SM: Nuclear pore association confers optimal expression levels for an inducible yeast gene. Nature 1, 441:774-778. 10.1038/nature04845
37. Oza P, Jaspersen SL, Miele A, Dekker J, Peterson CL: Mechanisms that regulate localization of a DNA double-strand break to the nuclear periphery. Genes Dev 1, 23:912-927. 10.1101/gad.1782209
38. Falk M, Lukasova E, Stefancikova L, Baranova E, Falkova I, Jezkova L, Davidkova M, Bacikova A, Vachelova J, Michaelidesova A, Kozubek S: Heterochromatinization associated with cell differentiation as a model to study DNA double strand break induction and repair in the context of higher-order chromatin structure. Appl Radiat Isot 2014, 83 Pt B:177-185.
39. Kaye JA, Melo JA, Cheung SK, Vaze MB, Haber JE, Toczyski DP: DNA breaks promote genomic instability by impeding proper chromosome segregation. Curr Biol 1, 14:2096-2106. 10.1016/j.cub.2004.10.051
40. Lobachev K, Vitriol E, Stemple J, Resnick MA, Bloom K: Chromosome fragmentation after induction of a double-strand break is an active process prevented by the RMX repair complex. Curr Biol 1, 14:2107-2112. 10.1016/j.cub.2004.11.051
41. Nakai W, Westmoreland J, Yeh E, Bloom K, Resnick MA: Chromosome integrity at a double-strand break requires exonuclease 1 and MRX. DNA Repair (Amst) 1, 10:102-110. 10.1016/j.dnarep.2010.10.004
42. Krawczyk PM, Stap J, Van Oven C, Hoebe R, Aten JA: Clustering of double strand break-containing chromosome domains is not inhibited by inactivation of major repair proteins. Radiat Prot Dosimetry 2006, 122:150-153.
43. Huertas P: DNA resection in eukaryotes: deciding how to fix the break. Nat Struct Mol Biol 1, 17:11-16. 10.1038/nsmb.1710
44. Krejci L, Altmannova V, Spirek M, Zhao X: Homologous recombination and its regulation. Nucleic Acids Res 1, 40:5795-5818. 10.1093/nar/gks270
45. Bao Y: Chromatin response to DNA double-strand break damage. Epigenomics 1, 3:307-321. 10.2217/epi.11.14
46. Shi L, Oberdoerffer P: Chromatin dynamics in DNA double-strand break repair. Biochim Biophys Acta 1819, 2012:811-819.
47. Seeber A, Hauer M, Gasser SM: Nucleosome remodelers in double-strand break repair. Curr Opin Genet Dev 1, 23:174-184. 10.1016/j.gde.2012.12.008
48. Xu Y, Price BD: Chromatin dynamics and the repair of DNA double strand breaks. Cell Cycle 1, 10:261-267. 10.4161/cc.10.2.14543
49. Gospodinov A, Herceg Z: Chromatin structure in double strand break repair. DNA Repair (Amst) 1, 12:800-810. 10.1016/j.dnarep.2013.07.006
50. Neumann FR, Dion V, Gehlen LR, Tsai-Pflugfelder M, Schmid R, Taddei A, Gasser SM: Targeted INO80 enhances subnuclear chromatin movement and ectopic homologous recombination. Genes Dev 1, 26:369-383. 10.1101/gad.176156.111
51. Xu Y, Sun Y, Jiang X, Ayrapetov MK, Moskwa P, Yang S, Weinstock DM, Price BD: The p400 ATPase regulates nucleosome stability and chromatin ubiquitination during DNA repair. J Cell Biol 1, 191:31-43. 10.1083/jcb.201001160
52. Sun Y, Jiang X, Price BD: Tip60: connecting chromatin to DNA damage signaling. Cell Cycle 1, 9:930-936. 10.4161/cc.9.5.10931
53. Zhu Q, Wani AA: Histone modifications: crucial elements for damage response and chromatin restoration. J Cell Physiol 2010, 223:283-288.
54. Smeenk G, Van Attikum H: The chromatin response to DNA breaks: leaving a mark on genome integrity. Annu Rev Biochem 1, 82:55-80. 10.1146/annurev-biochem-061809-174504
55. Downs JA, Lowndes NF, Jackson SP: A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature 1, 408:1001-1004. 10.1038/35050000
56. Kalocsay M, Hiller NJ, Jentsch S: Chromosome-wide Rad51 spreading and SUMO-H2A.Z-dependent chromosome fixation in response to a persistent DNA double-strand break. Mol Cell 1, 33:335-343. 10.1016/j.molcel.2009.01.016
57. Robinson PJ, An W, Routh A, Martino F, Chapman L, Roeder RG, Rhodes D: 30 nm chromatin fibre decompaction requires both H4-K16 acetylation and linker histone eviction. J Mol Biol 1, 381:816-825. 10.1016/j.jmb.2008.04.050
58. Krawczyk PM, Borovski T, Stap J, Cijsouw T, Ten Cate R, Medema JP, Kanaar R, Franken NA, Aten JA: Chromatin mobility is increased at sites of DNA double-strand breaks. J Cell Sci 1, 125:2127-2133. 10.1242/jcs.089847
59. Razin SV, Iarovaia OV, Sjakste N, Sjakste T, Bagdoniene L, Rynditch AV, Eivazova ER, Lipinski M, Vassetzky YS: Chromatin domains and regulation of transcription. J Mol Biol 1, 369:597-607. 10.1016/j.jmb.2007.04.003
60. Razin SV, Iarovaia OV, Vassetzky YS: A requiem to the nuclear matrix: from a controversial concept to 3D organization of the nucleus. Chromosoma 2014., 123: doi:10.1007/s00412-00014-00459-00418
61. Guelen L, Pagie L, Brasset E, Meuleman W, Faza MB, Talhout W, Eussen BH, De Klein A, Wessels L, De Laat W, Van Steensel B: Domain organization of human chromosomes revealed by mapping of nuclear lamina interactions. Nature 1, 453:948-951. 10.1038/nature06947
62. Lieberman-Aiden E, Van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie BR, Sabo PJ, Dorschner MO, Sandstrom R, Bernstein B, Bender MA, Groudine M, Gnirke A, Stamatoyannopoulos J, Mirny LA, Lander ES, Dekker J: Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 1, 326:289-293. 10.1126/science.1181369
63. Mirny LA: The fractal globule as a model of chromatin architecture in the cell. Chromosome Res 2011, 19:37-51.
64. Phillips JE, Corces VG: CTCF: master weaver of the genome. Cell 1, 137:1194-1211. 10.1016/j.cell.2009.06.001
65. Millau JF, Gaudreau L: CTCF, cohesin, and histone variants: connecting the genome. Biochem Cell Biol 1, 89:505-513. 10.1139/o11-052
66. Feinauer CJ, Hofmann A, Goldt S, Liu L, Mate G, Heermann DW: Zinc finger proteins and the 3D organization of chromosomes. Adv Protein Chem Struct Biol 2013, 90:67-117.
67. Dowen JM, Young RA: SMC complexes link gene expression and genome architecture. Curr Opin Genet Dev 2014, 25C:131-137.
68. Mahen R, Hattori H, Lee M, Sharma P, Jeyasekharan AD, Venkitaraman AR: A-type lamins maintain the positional stability of DNA damage repair foci in mammalian nuclei. PLoS One 1, 8:e61893. 10.1371/journal.pone.0061893
69. Burden DA, Osheroff N: Mechanism of action of eukaryotic topoisomerase II and drugs targeted to the enzyme. Biochim Biophys Acta 1, 1400:139-154. 10.1016/S0167-4781(98)00132-8
70. Austin CA, Marsh KL: Eukaryotic DNA topoisomerase II beta. Bioessays 1, 20:215-226. 10.1002/(SICI)1521-1878(199803)20:3<215::AID-BIES5>3.0.CO;2-Q
71. Fortune JM, Osheroff N: Topoisomerase II as a target for anticancer drugs: when enzymes stop being nice. Prog Nucleic Acid Res Mol Biol 2000, 64:221-253.
72. Wilstermann AM, Osheroff N: Stabilization of eukaryotic topoisomerase II-DNA cleavage complexes. Curr Top Med Chem 1, 3:321-338. 10.2174/1568026033452519
73. Montecucco A, Biamonti G: Cellular response to etoposide treatment. Cancer Lett 1, 252:9-18. 10.1016/j.canlet.2006.11.005
74. Pui CH, Relling MV: Topoisomerase II inhibitor-related acute myeloid leukaemia. Br J Haematol 1, 109:13-23. 10.1046/j.1365-2141.2000.01843.x
75. Ezoe S: Secondary leukemia associated with the anti-cancer agent, etoposide, a topoisomerase II inhibitor. Int J Environ Res Public Health 1, 9:2444-2453. 10.3390/ijerph9072444
76. Cowell IG, Austin CA: Mechanism of generation of therapy related leukemia in response to anti-topoisomerase II agents. Int J Environ Res Public Health 1, 9:2075-2091. 10.3390/ijerph9062075
77. Aplan PD, Chervinsky DS, Stanulla M, Burhans WC: Site-specific DNA cleavage within the MLL breakpoint cluster region induced by topoisomerase II inhibitors. Blood 1996, 87:2649-2658.
78. Bystritskiy AA, Razin SV: Breakpoint clusters: reason or consequence? Crit Rev Eukaryot Gene Expr 1, 14:65-77. 10.1615/CritRevEukaryotGeneExpr.v14.i12.40
79. Hawtin RE, Stockett DE, Wong OK, Lundin C, Helleday T, Fox JA: Homologous recombination repair is essential for repair of vosaroxin-induced DNA double-strand breaks. Oncotarget 2010, 1:606-619.
80. Heisig P: Type II topoisomerases-inhibitors, repair mechanisms and mutations. Mutagenesis 1, 24:465-469. 10.1093/mutage/gep035
81. Yang Z, Waldman AS, Wyatt MD: Expression and regulation of RAD51 mediate cellular responses to chemotherapeutics. Biochem Pharmacol 1, 83:741-746. 10.1016/j.bcp.2011.12.022
82. Kantidze OL, Razin SV: Chemotherapy-related secondary leukemias: a role for DNA repair by error-prone non-homologous end joining in topoisomerase II - Induced chromosomal rearrangements. Gene 1, 391:76-79. 10.1016/j.gene.2006.12.006
83. Iliakis G: Backup pathways of NHEJ in cells of higher eukaryotes: cell cycle dependence. Radiother Oncol 1, 92:310-315. 10.1016/j.radonc.2009.06.024
84. Umanskaya ON, Lebedeva SS, Gavrilov AA, Bystritskiy AA, Razin SV: Inhibition of DNA topoisomerase II may trigger illegitimate recombination in living cells: Experiments with a model system. J Cell Biochem 1, 99:598-608. 10.1002/jcb.20938
85. Rowley JD, Olney HJ: International workshop on the relationship of prior therapy to balanced chromosome aberrations in therapy-related myelodysplastic syndromes and acute leukemia: overview report. Genes Chromosomes Cancer 1, 33:331-345. 10.1002/gcc.10040
86. Felix CA: Secondary leukemias induced by topoisomerase-targeted drugs. Biochim Biophys Acta 1, 1400:233-255. 10.1016/S0167-4781(98)00139-0
87. Rubtsov MA, Terekhov SM, Razin SV, Iarovaia OV: Repositioning of ETO gene in cells treated with VP-1, an inhibitor of DNA-topoisomerase II. J Cell Biochem 2008, 104:692-699. 10.1002/jcb.21656
88. Smith KA, Cowell IG, Zhang Y, Sondka Z, Austin CA: The role of topoisomerase II beta on breakage and proximity of RUNX1 to partner alleles RUNX1T1 and EVI1. Genes Chromosomes Cancer 1, 53:117-128. 10.1002/gcc.22124
89. Gue M, Sun JS, Boudier T: Simultaneous localization of MLL, AF4 and ENL genes in interphase nuclei by 3D-FISH: MLL translocation revisited. BMC Cancer 1, 6:20. 10.1186/1471-2407-6-20
90. Cowell IG, Sondka Z, Smith K, Lee KC, Manville CM, Sidorczuk-Lesthuruge M, Rance HA, Padget K, Jackson GH, Adachi N, Austin CA: Model for MLL translocations in therapy-related leukemia involving topoisomerase IIbeta-mediated DNA strand breaks and gene proximity. Proc Natl Acad Sci U S A 1, 109:8989-8994. 10.1073/pnas.1204406109
91. Do TU, Ho B, Shih SJ, Vaughan A: Zinc finger nuclease induced DNA double stranded breaks and rearrangements in MLL. Mutat Res 1, 740:34-42. 10.1016/j.mrfmmm.2012.12.006
92. Xiao H, Mao Y, Desai SD, Zhou N, Ting CY, Hwang J, Liu LF: The topoisomerase IIbeta circular clamp arrests transcription and signals a 26S proteasome pathway. Proc Natl Acad Sci U S A 1, 100:3239-3244. 10.1073/pnas.0736401100
93. Zhang A, Lyu YL, Lin CP, Zhou N, Azarova AM, Wood LM, Liu LF: A protease pathway for the repair of topoisomerase II-DNA covalent complexes. J Biol Chem 1, 281:35997-36003. 10.1074/jbc.M604149200
94. Mirault ME, Boucher P, Tremblay A: Nucleotide-resolution mapping of topoisomerase-mediated and apoptotic DNA strand scissions at or near an MLL translocation hotspot. Am J Hum Genet 1, 79:779-791. 10.1086/507791
95. Meyer C, Hofmann J, Burmeister T, Groger D, Park TS, Emerenciano M, Pombo De Oliveira M, Renneville A, Villarese P, Macintyre E, Cavé H, Clappier E, Mass-Malo K, Zuna J, Trka J, De Braekeleer E, De Braekeleer M, Oh SH, Tsaur G, Fechina L, van der Velden VH, van Dongen JJ, Delabesse E, Binato R, Silva ML, Kustanovich A, Aleinikova O, Harris MH, Lund-Aho T, Juvonen V: The MLL recombinome of acute leukemias in 2013. Leukemia 1, 27:2165-2176. 10.1038/leu.2013.135
96. Mitelman F, Johansson B, Mertens F: The impact of translocations and gene fusions on cancer causation. Nat Rev Cancer 1, 7:233-245. 10.1038/nrc2091
97. Ali H, Daser A, Dear P, Wood H, Rabbitts P, Rabbitts T: Nonreciprocal chromosomal translocations in renal cancer involve multiple DSBs and NHEJ associated with breakpoint inversion but not necessarily with transcription. Genes Chromosomes Cancer 1, 52:402-409. 10.1002/gcc.22038
98. Artandi SE, Chang S, Lee SL, Alson S, Gottlieb GJ, Chin L, DePinho RA: Telomere dysfunction promotes non-reciprocal translocations and epithelial cancers in mice. Nature 1, 406:641-645. 10.1038/35020592
99. Anderson RM, Stevens DL, Goodhead DT: M-FISH analysis shows that complex chromosome aberrations induced by alpha -particle tracks are cumulative products of localized rearrangements. Proc Natl Acad Sci U S A 1, 99:12167-12172. 10.1073/pnas.182426799