Chromosomal Translocations in Human Cells Are Generated by Canonical Nonhomologous End-Joining

Molecular Cell

Volumn 55, Issue 6, 2014, Pages 829-842

  Ghezraoui, Hind ^a,b,c   Piganeau, Marion ^a,b,c   Renouf, Benjamin ^a,b,c   Renaud, Jean Baptiste ^a,b,c   Sallmyr, Annahita ^d   Ruis, Brian ^e   Oh, Sehyun ^e   Tomkinson, Alan E ^d   Hendrickson, Eric A ^e   Giovannangeli, Carine ^a,b,c   Jasin, Maria ^f   Brunet, Erika ^a,b,c  

^a MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

^b CNRS   (France)

^c INSERM   (France)

^d UNIVERSITY OF NEW MEXICO   (United States)

^e UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^f MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRISPR ASSOCIATED PROTEIN; DNA LIGASE IV; NUCLEASE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PROTEIN TALEN; PROTEIN ZFN; UNCLASSIFIED DRUG; XRCC4 PROTEIN; DEOXYRIBONUCLEASE; DNA BINDING PROTEIN; POLYDEOXYRIBONUCLEOTIDE SYNTHASE (ATP); XRCC4 PROTEIN, HUMAN;

ARTICLE; CARCINOGENESIS; CELL MUTANT; CHROMOSOME 19; CHROMOSOME 22; CHROMOSOME DELETION; CHROMOSOME REARRANGEMENT; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; DNA END JOINING REPAIR; DOUBLE STRANDED DNA BREAK; HUMAN; HUMAN CELL; HUMAN VERSUS ANIMAL COMPARISON; PHENOTYPE; PRE B LYMPHOCYTE; SEQUENCE HOMOLOGY; SPECIES DIFFERENCE; WILD TYPE; ANIMAL; GENE DELETION; GENE TRANSLOCATION; GENETICS; HUMAN CHROMOSOME; MOUSE; PHYSIOLOGY; TUMOR CELL CULTURE;

ANIMALS; CHROMOSOMES, HUMAN; DEOXYRIBONUCLEASES; DNA END-JOINING REPAIR; DNA LIGASES; DNA-BINDING PROTEINS; HUMANS; MICE; SEQUENCE DELETION; SPECIES SPECIFICITY; TRANSLOCATION, GENETIC; TUMOR CELLS, CULTURED;

EID: 84907976219     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2014.08.002     Document Type: Article

References (65)

1. Beamish H.J., Jessberger R., Riballo E., Priestley A., Blunt T., Kysela B., Jeggo P.A. The C-terminal conserved domain of DNA-PKcs, missing in the SCID mouse, is required for kinase activity. Nucleic Acids Res. 2000, 28:1506-1513.
2. Bennardo N., Cheng A., Huang N., Stark J.M. Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet. 2008, 4:e1000110.
3. Bétermier M., Bertrand P., Lopez B.S. Is non-homologous end-joining really an inherently error-prone process?. PLoS Genet. 2014, 10:e1004086.
4. Boboila C., Jankovic M., Yan C.T., Wang J.H., Wesemann D.R., Zhang T., Fazeli A., Feldman L., Nussenzweig A., Nussenzweig M., Alt F.W. 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.
5. Boboila C., Alt F.W., Schwer B. Classical and alternative end-joining pathways for repair of lymphocyte-specific and general DNA double-strand breaks. Adv. Immunol. 2012, 116:1-49.
6. Boubakour-Azzouz I., Bertrand P., Claes A., Lopez B.S., Rougeon F. Terminal deoxynucleotidyl transferase requires KU80 and XRCC4 to promote N-addition at non-V(D)J chromosomal breaks in non-lymphoid cells. Nucleic Acids Res. 2012, 40:8381-8391.
7. Brunet E., Simsek D., Tomishima M., DeKelver R., Choi V.M., Gregory P., Urnov F., Weinstock D.M., Jasin M. Chromosomal translocations induced at specified loci in human stem cells. Proc. Natl. Acad. Sci. USA 2009, 106:10620-10625.
8. Bryans M., Valenzano M.C., Stamato T.D. Absence of DNA ligase IV protein in XR-1 cells: evidence for stabilization by XRCC4. Mutat. Res. 1999, 433:53-58.
9. Carvalho C.M., Pehlivan D., Ramocki M.B., Fang P., Alleva B., Franco L.M., Belmont J.W., Hastings P.J., Lupski J.R. Replicative mechanisms for CNV formation are error prone. Nat. Genet. 2013, 45:1319-1326.
10. Choi P.S., Meyerson M. Targeted genomic rearrangements using CRISPR/Cas technology. Nat. Commun. 2014, 5:3728.
11. Cong L., Ran F.A., Cox D., Lin S., Barretto R., Habib N., Hsu P.D., Wu X., Jiang W., Marraffini L.A., Zhang F. Multiplex genome engineering using CRISPR/Cas systems. Science 2013, 339:819-823.
12. Cottarel J., Frit P., Bombarde O., Salles B., Négrel A., Bernard S., Jeggo P.A., Lieber M.R., Modesti M., Calsou P. A noncatalytic function of the ligation complex during nonhomologous end joining. J.Cell Biol. 2013, 200:173-186.
13. DelacÔte F., Han M., Stamato T.D., Jasin M., Lopez B.S. An xrcc4 defect or Wortmannin stimulates homologous recombination specifically induced by double-strand breaks in mammalian cells. Nucleic Acids Res. 2002, 30:3454-3463.
14. Deriano L., Roth D.B. Modernizing the nonhomologous end-joining repertoire: alternative and classical NHEJ share the stage. Annu. Rev. Genet. 2013, 47:433-455.
15. Fattah F., Lee E.H., Weisensel N., Wang Y., Lichter N., Hendrickson E.A. Ku regulates the non-homologous end joining pathway choice of DNA double-strand break repair in human somatic cells. PLoS Genet. 2010, 6:e1000855.
16. Finnie N.J., Gottlieb T.M., Blunt T., Jeggo P.A., Jackson S.P. DNA-dependent protein kinase activity is absent in xrs-6 cells: implications for site-specific recombination and DNA double-strand break repair. Proc. Natl. Acad. Sci. USA 1995, 92:320-324.
17. Fu Y., Foden J.A., Khayter C., Maeder M.L., Reyon D., Joung J.K., Sander J.D. High-frequency off-target mutagenesis induced by CRISPR-Cas nucleases in human cells. Nat. Biotechnol. 2013, 31:822-826.
18. Gaj T., Gersbach C.A., Barbas C.F. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol. 2013, 31:397-405.
19. Gillert E., Leis T., Repp R., Reichel M., Hösch A., Breitenlohner I., Angermüller S., Borkhardt A., Harbott J., Lampert F., et al. A DNA damage repair mechanism is involved in the origin of chromosomal translocations t(4;11) in primary leukemic cells. Oncogene 1999, 18:4663-4671.
20. Goodarzi A.A., Jeggo P.A. The repair and signaling responses to DNA double-strand breaks. Adv. Genet. 2013, 82:1-45.
21. Grawunder U., Zimmer D., Fugmann S., Schwarz K., Lieber M.R. DNA ligase IV is essential for V(D)J recombination and DNA double-strand break repair in human precursor lymphocytes. Mol. Cell 1998, 2:477-484.
22. Guirouilh-Barbat J., Rass E., Plo I., Bertrand P., Lopez B.S. Defects in XRCC4 and KU80 differentially affect the joining of distal nonhomologous ends. Proc. Natl. Acad. Sci. USA 2007, 104:20902-20907.
23. Hastings P.J., Ira G., Lupski J.R. A microhomology-mediated break-induced replication model for the origin of human copy number variation. PLoS Genet. 2009, 5:e1000327.
24. Jinek M., Chylinski K., Fonfara I., Hauer M., Doudna J.A., Charpentier E. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 2012, 337:816-821.
25. Kabotyanski E.B., Gomelsky L., Han J.O., Stamato T.D., Roth D.B. Double-strand break repair in Ku86- and XRCC4-deficient cells. Nucleic Acids Res. 1998, 26:5333-5342.
26. Langer T., Metzler M., Reinhardt D., Viehmann S., Borkhardt A., Reichel M., Stanulla M., Schrappe M., Creutzig U., Ritter J., et al. Analysis of t(9;11) chromosomal breakpoint sequences in childhood acute leukemia: almost identical MLL breakpoints in therapy-related AML after treatment without etoposides. Genes Chromosomes Cancer 2003, 36:393-401.
27. Li G., Nelsen C., Hendrickson E.A. Ku86 is essential in human somatic cells. Proc. Natl. Acad. Sci. USA 2002, 99:832-837.
28. Liang F., Jasin M. Ku80-deficient cells exhibit excess degradation of extrachromosomal DNA. J.Biol. Chem. 1996, 271:14405-14411.
29. Lieber M.R. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem. 2010, 79:181-211.
30. Lin C., Yang L., Tanasa B., Hutt K., Ju B.G., Ohgi K., Zhang J., Rose D.W., Fu X.D., Glass C.K., Rosenfeld M.G. Nuclear receptor-induced chromosomal proximity and DNA breaks underlie specific translocations in cancer. Cell 2009, 139:1069-1083.
31. Mali P., Aach J., Stranges P.B., Esvelt K.M., Moosburner M., Kosuri S., Yang L., Church G.M. CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat. Biotechnol. 2013, 31:833-838.
32. Mali P., Yang L., Esvelt K.M., Aach J., Guell M., DiCarlo J.E., Norville J.E., Church G.M. RNA-guided human genome engineering via Cas9. Science 2013, 339:823-826.
33. Mani R.S., Chinnaiyan A.M. Triggers for genomic rearrangements: insights into genomic, cellular and environmental influences. Nat. Rev. Genet. 2010, 11:819-829.
34. Mattarucchi E., Guerini V., Rambaldi A., Campiotti L., Venco A., Pasquali F., Lo Curto F., Porta G. Microhomologies and interspersed repeat elements at genomic breakpoints in chronic myeloid leukemia. Genes Chromosomes Cancer 2008, 47:625-632.
35. Meek K., Kienker L., Dallas C., Wang W., Dark M.J., Venta P.J., Huie M.L., Hirschhorn R., Bell T. SCID in Jack Russell terriers: a new animal model of DNA-PKcs deficiency. J.Immunol. 2001, 167:2142-2150.
36. Mitelman F., Johansson B., Mertens F. The impact of translocations and gene fusions on cancer causation. Nat. Rev. Cancer 2007, 7:233-245.
37. Nussenzweig A., Nussenzweig M.C. Origin of chromosomal translocations in lymphoid cancer. Cell 2010, 141:27-38.
38. Nussenzweig A., Chen C., da Costa Soares V., Sanchez M., Sokol K., Nussenzweig M.C., Li G.C. Requirement for Ku80 in growth and immunoglobulin V(D)J recombination. Nature 1996, 382:551-555.
39. O'Driscoll M., Cerosaletti K.M., Girard P.M., Dai Y., Stumm M., Kysela B., Hirsch B., Gennery A., Palmer S.E., Seidel J., et al. DNA ligase IV mutations identified in patients exhibiting developmental delay and immunodeficiency. Mol. Cell 2001, 8:1175-1185.
40. Oh S., Wang Y., Zimbric J., Hendrickson E.A. 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. 2013, 41:1734-1749.
41. Oh S., Harvey A., Zimbric J., Wang Y., Nguyen T., Jackson P.J., Hendrickson E.A. DNA ligase III and DNA ligase IV carry out genetically distinct forms of end joining in human somatic cells. DNA Repair (Amst). 2014, 21:97-110.
42. Pannunzio N.R., Li S., Watanabe G., Lieber M.R. Non-homologous end joining often uses microhomology: implications for alternative end joining. DNA Repair (Amst.) 2014, 17:74-80.
43. Piganeau M., Ghezraoui H., De Cian A., Guittat L., Tomishima M., Perrouault L., René O., Katibah G.E., Zhang L., Holmes M.C., et al. Cancer translocations in human cells induced by zinc finger and TALE nucleases. Genome Res. 2013, 23:1182-1193.
44. Ran F.A., Hsu P.D., Lin C.Y., Gootenberg J.S., Konermann S., Trevino A.E., Scott D.A., Inoue A., Matoba S., Zhang Y., Zhang F. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 2013, 154:1380-1389.
45. Reichel M., Gillert E., Nilson I., Siegler G., Greil J., Fey G.H., Marschalek R. Fine structure of translocation breakpoints in leukemic blasts with chromosomal translocation t(4;11): the DNA damage-repair model of translocation. Oncogene 1998, 17:3035-3044.
46. Roth D.B., Porter T.N., Wilson J.H. Mechanisms of nonhomologous recombination in mammalian cells. Mol. Cell. Biol. 1985, 5:2599-2607.
47. 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.
48. Simsek D., Brunet E., Wong S.Y., Katyal S., Gao Y., McKinnon P.J., Lou J., Zhang L., Li J., Rebar E.J., et al. DNA ligase III promotes alternative nonhomologous end-joining during chromosomal translocation formation. PLoS Genet. 2011, 7:e1002080.
49. Smith J., Riballo E., Kysela B., Baldeyron C., Manolis K., Masson C., Lieber M.R., Papadopoulo D., Jeggo P. Impact of DNA ligase IV on the fidelity of end joining in human cells. Nucleic Acids Res. 2003, 31:2157-2167.
50. Sobreira N.L., Gnanakkan V., Walsh M., Marosy B., Wohler E., Thomas G., Hoover-Fong J.E., Hamosh A., Wheelan S.J., Valle D. Characterization of complex chromosomal rearrangements by targeted capture and next-generation sequencing. Genome Res. 2011, 21:1720-1727.
51. Soni A., Siemann M., Grabos M., Murmann T., Pantelias G.E., Iliakis G. Requirement for Parp-1 and DNA ligases 1 or 3 but not of Xrcc1 in chromosomal translocation formation by backup end joining. Nucleic Acids Res. 2014, 42:6380-6392.
52. Taccioli G.E., Gottlieb T.M., Blunt T., Priestley A., Demengeot J., Mizuta R., Lehmann A.R., Alt F.W., Jackson S.P., Jeggo P.A. Ku80: product of the XRCC5 gene and its role in DNA repair and V(D)J recombination. Science 1994, 265:1442-1445.
53. Urnov F.D., Rebar E.J., Holmes M.C., Zhang H.S., Gregory P.D. Genome editing with engineered zinc finger nucleases. Nat. Rev. Genet. 2010, 11:636-646.
54. 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.
55. Wang Y., Ghosh G., Hendrickson E.A. Ku86 represses lethal telomere deletion events in human somatic cells. Proc. Natl. Acad. Sci. USA 2009, 106:12430-12435.
56. Weinstock D.M., Elliott B., Jasin M. A model of oncogenic rearrangements: differences between chromosomal translocation mechanisms and simple double-strand break repair. Blood 2006, 107:777-780.
57. Weinstock D.M., Brunet E., Jasin M. Formation of NHEJ-derived reciprocal chromosomal translocations does not require Ku70. Nat. Cell Biol. 2007, 9:978-981.
58. Windhofer F., Wu W., Iliakis G. Low levels of DNA ligases III and IV sufficient for effective NHEJ. J.Cell. Physiol. 2007, 213:475-483.
59. Woodbine L., Gennery A.R., Jeggo P.A. The clinical impact of deficiency in DNA non-homologous end-joining. DNA Repair (Amst.) 2014, 16:84-96.
60. 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.
61. Zhang Y., Strissel P., Strick R., Chen J., Nucifora G., Le Beau M.M., Larson R.A., Rowley J.D. Genomic DNA breakpoints in AML1/RUNX1 and ETO cluster with topoisomerase II DNA cleavage and DNase I hypersensitive sites in t(8;21) leukemia. Proc. Natl. Acad. Sci. USA 2002, 99:3070-3075.
62. Zhang Q., Wei F., Wang H.Y., Liu X., Roy D., Xiong Q.B., Jiang S., Medvec A., Danet-Desnoyers G., Watt C., et al. The potent oncogene NPM-ALK mediates malignant transformation of normal human CD4(+) T lymphocytes. Am. J. Pathol. 2013, 183:1971-1980.
63. Zhu C., Bogue M.A., Lim D.S., Hasty P., Roth D.B. Ku86-deficient mice exhibit severe combined immunodeficiency and defective processing of V(D)J recombination intermediates. Cell 1996, 86:379-389.
64. Zhu C., Mills K.D., Ferguson D.O., Lee C., Manis J., Fleming J., Gao Y., Morton C.C., Alt F.W. Unrepaired DNA breaks in p53-deficient cells lead to oncogenic gene amplification subsequent to translocations. Cell 2002, 109:811-821.
65. Zucman-Rossi J., Legoix P., Victor J.M., Lopez B., Thomas G. Chromosome translocation based on illegitimate recombination in human tumors. Proc. Natl. Acad. Sci. USA 1998, 95:11786-11791.