Erratum: Complex Breakpoints and Template Switching Associated with Non-canonical Termination of Homologous Recombination in Mammalian Cells (PLoS Genetics (2016) 12:11 (e1006410) DOI: 10.1371/journal.pgen.1006410);Complex Breakpoints and Template Switching Associated with Non-canonical Termination of Homologous Recombination in Mammalian Cells

PLoS Genetics

Volumn 12, Issue 11, 2016, Pages

  Hartlerode, Andrea J ^a,c   Willis, Nicholas A ^a   Rajendran, Anbazhagan ^a   Manis, John P ^b   Scully, Ralph ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ARTICLE; CHROMOSOME BREAKAGE; COMPLEX FORMATION; CONTROLLED STUDY; GENE; GENE CONVERSION; GENE FUNCTION; GENE IDENTIFICATION; GENE SWITCHING; HOMOLOGOUS RECOMBINATION; LONG TRACT GENE CONVERSION; MAMMAL CELL; MOLECULAR DYNAMICS; NONHUMAN; STRUCTURE ANALYSIS; XRCC4 GENE; ANIMAL; BREAST TUMOR; CHROMATID; DNA END JOINING REPAIR; FEMALE; GENETICS; GENOMIC INSTABILITY; HUMAN; MOUSE; MOUSE EMBRYONIC STEM CELL; OVARY TUMOR; PATHOLOGY;

BRCA1 PROTEIN; BRCA2 PROTEIN; BRCA2 PROTEIN, HUMAN; DNA BINDING PROTEIN; XRCC4 PROTEIN, MOUSE;

ANIMALS; BRCA1 PROTEIN; BRCA2 PROTEIN; BREAST NEOPLASMS; CHROMATIDS; DNA END-JOINING REPAIR; DNA-BINDING PROTEINS; FEMALE; GENE CONVERSION; GENOMIC INSTABILITY; HOMOLOGOUS RECOMBINATION; HUMANS; MICE; MOUSE EMBRYONIC STEM CELLS; OVARIAN NEOPLASMS;

EID: 85000605739     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/JOURNAL.PGEN.1006509     Document Type: Erratum

References (66)

1. Ciccia A, Elledge SJ, The DNA damage response: making it safe to play with knives. Mol Cell. 2010;40(2):179–204. Epub 2010/10/23. S1097-2765(10)00747-1 [pii] doi: 10.1016/j.molcel.2010.09.01920965415.
2. Hartlerode AJ, Scully R, Mechanisms of double-strand break repair in somatic mammalian cells. Biochem J. 2009;423(2):157–68. 19772495; doi: 10.1042/BJ20090942
3. Alt FW, Zhang Y, Meng FL, Guo C, Schwer B, Mechanisms of programmed DNA lesions and genomic instability in the immune system. Cell. 2013;152(3):417–29. Epub 2013/02/05. doi: 10.1016/j.cell.2013.01.007 S0092-8674(13)00009-3 [pii]. 23374339.
4. Cox MM, Goodman MF, Kreuzer KN, Sherratt DJ, Sandler SJ, Marians KJ, The importance of repairing stalled replication forks. Nature. 2000;404(6773):37–41. doi: 10.1038/3500350110716434
5. Lambert S, Watson A, Sheedy DM, Martin B, Carr AM, Gross chromosomal rearrangements and elevated recombination at an inducible site-specific replication fork barrier. Cell. 2005;121(5):689–702. 15935756. doi: 10.1016/j.cell.2005.03.022
6. Knipscheer P, Raschle M, Smogorzewska A, Enoiu M, Ho TV, Scharer OD, et al. The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair. Science. 2009;326(5960):1698–701. Epub 2009/12/08. doi: 10.1126/science.118237219965384.
7. Chan KL, Hickson ID, New insights into the formation and resolution of ultra-fine anaphase bridges. Seminars in cell & developmental biology. 2011;22(8):906–12. Epub 2011/07/26. doi: 10.1016/j.semcdb.2011.07.001 S1084-9521(11)00087-5 [pii]. 21782962.
8. Duxin JP, Walter JC, What is the DNA repair defect underlying Fanconi anemia?Current opinion in cell biology. 2015;37:49–60. doi: 10.1016/j.ceb.2015.09.00226512453.
9. Moynahan ME, Jasin M, Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat Rev Mol Cell Biol. 2010;11(3):196–207. Epub 2010/02/24. doi: 10.1038/nrm2851 nrm2851 [pii]. 20177395.
10. Nagaraju G, Scully R, Minding the gap: the underground functions of BRCA1 and BRCA2 at stalled replication forks. DNA Repair (Amst). 2007;6(7):1018–31. doi: 10.1016/j.dnarep.2007.02.02017379580.
11. Carr AM, Lambert S, Replication Stress-Induced Genome Instability: The Dark Side of Replication Maintenance by Homologous Recombination. J Mol Biol. 2013. Epub 2013/05/07. S0022-2836(13)00271-4 [pii] doi: 10.1016/j.jmb.2013.04.02323643490.
12. Lambert S, Mizuno K, Blaisonneau J, Martineau S, Chanet R, Freon K, et al. Homologous recombination restarts blocked replication forks at the expense of genome rearrangements by template exchange. Mol Cell. 2010;39(3):346–59. Epub 2010/08/14. doi: 10.1016/j.molcel.2010.07.01520705238.
13. Scully R, Livingston DM, In search of the tumour-suppressor functions of BRCA1 and BRCA2. Nature. 2000;408(6811):429–32. doi: 10.1038/3504400011100717
14. Walsh T, King MC, Ten genes for inherited breast cancer. Cancer Cell. 2007;11(2):103–5. 17292821. doi: 10.1016/j.ccr.2007.01.010
15. Venkitaraman AR, Cancer susceptibility and the functions of BRCA1 and BRCA2. Cell. 2002;108(2):171–82. 11832208.
16. McVey M, Lee SE, MMEJ repair of double-strand breaks (director's cut): deleted sequences and alternative endings. Trends in genetics: TIG. 2008;24(11):529–38. 18809224. doi: 10.1016/j.tig.2008.08.007
17. Truong LN, Li Y, Shi LZ, Hwang PY, He J, Wang H, et al. Microhomology-mediated End Joining and Homologous Recombination share the initial end resection step to repair DNA double-strand breaks in mammalian cells. Proc Natl Acad Sci U S A. 2013;110(19):7720–5. Epub 2013/04/24. doi: 10.1073/pnas.1213431110 1213431110 [pii]. 23610439.
18. Bignell GR, Santarius T, Pole JC, Butler AP, Perry J, Pleasance E, et al. Architectures of somatic genomic rearrangement in human cancer amplicons at sequence-level resolution. Genome research. 2007;17(9):1296–303. 17675364. doi: 10.1101/gr.6522707
19. Stephens PJ, McBride DJ, Lin ML, Varela I, Pleasance ED, Simpson JT, et al. Complex landscapes of somatic rearrangement in human breast cancer genomes. Nature. 2009;462(7276):1005–10. Epub 2009/12/25. nature08645 [pii] doi: 10.1038/nature0864520033038.
20. Malhotra A, Lindberg M, Faust GG, Leibowitz ML, Clark RA, Layer RM, et al. Breakpoint profiling of 64 cancer genomes reveals numerous complex rearrangements spawned by homology-independent mechanisms. Genome research. 2013;23(5):762–76. doi: 10.1101/gr.143677.11223410887.
21. Willis NA, Rass E, Scully R, Deciphering the Code of the Cancer Genome: Mechanisms of Chromosome Rearrangement. Trends Cancer. 2015;1(4):217–30. doi: 10.1016/j.trecan.2015.10.00726726318.
22. Paques F, Haber JE, Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiology and molecular biology reviews: MMBR. 1999;63(2):349–404. 10357855.
23. Elliott B, Richardson C, Winderbaum J, Nickoloff JA, Jasin M, Gene conversion tracts from double-strand break repair in mammalian cells. Mol Cell Biol. 1998;18(1):93–101. 9418857
24. Sweetser DB, Hough H, Whelden JF, Arbuckle M, Nickoloff JA, Fine-resolution mapping of spontaneous and double-strand break-induced gene conversion tracts in Saccharomyces cerevisiae reveals reversible mitotic conversion polarity. Mol Cell Biol. 1994;14(6):3863–75. 8196629
25. Taghian DG, Nickoloff JA, Chromosomal double-strand breaks induce gene conversion at high frequency in mammalian cells. Mol Cell Biol. 1997;17(11):6386–93. 9343400
26. Johnson RD, Jasin M, Sister chromatid gene conversion is a prominent double-strand break repair pathway in mammalian cells. Embo J. 2000;19(13):3398–407. doi: 10.1093/emboj/19.13.339810880452
27. Puget N, Knowlton M, Scully R, Molecular analysis of sister chromatid recombination in mammalian cells. DNA Repair (Amst). 2005;4(2):149–61. 15590323. doi: 10.1016/j.dnarep.2004.08.010
28. Nagaraju G, Odate S, Xie A, Scully R, Differential regulation of short- and long-tract gene conversion between sister chromatids by Rad51C. Mol Cell Biol. 2006;26(21):8075–86. 16954385. doi: 10.1128/MCB.01235-06
29. Chandramouly G, Kwok A, Huang B, Willis NA, Xie A, Scully R, BRCA1 and CtIP suppress long-tract gene conversion between sister chromatids. Nat Commun. 2013;4:2404. Epub 2013/09/03. doi: 10.1038/ncomms3404 ncomms3404 [pii]. 23994874.
30. Willis NA, Chandramouly G, Huang B, Kwok A, Follonier C, Deng C, et al. BRCA1 controls homologous recombination at Tus/Ter-stalled mammalian replication forks. Nature. 2014;510(7506):556–9. doi: 10.1038/nature1329524776801.
31. Brenneman MA, Wagener BM, Miller CA, Allen C, Nickoloff JA, XRCC3 controls the fidelity of homologous recombination: roles for XRCC3 in late stages of recombination. Molecular Cell. 2002;10(2):387–95. 12191483
32. Tauchi H, Kobayashi J, Morishima K, van Gent DC, Shiraishi T, Verkaik NS, et al. Nbs1 is essential for DNA repair by homologous recombination in higher vertebrate cells. Nature. 2002;420(6911):93–8. doi: 10.1038/nature0112512422221
33. Saleh-Gohari N, Helleday T, Strand invasion involving short tract gene conversion is specifically suppressed in BRCA2-deficient hamster cells. Oncogene. 2004;23(56):9136–41. Epub 2004/10/14. 1208178 [pii] doi: 10.1038/sj.onc.120817815480413.
34. Nagaraju G, Hartlerode A, Kwok A, Chandramouly G, Scully R, XRCC2 and XRCC3 regulate the balance between short- and long-tract gene conversion between sister chromatids. Mol Cell Biol. 2009. 19470754. doi: 10.1128/MCB.01406-08
35. Anand RP, Lovett ST, Haber JE, Break-induced DNA replication. Cold Spring Harb Perspect Biol. 2013;5(12). Epub 2013/07/25. doi: 10.1101/cshperspect.a010397 a010397 [pii] cshperspect.a010397 [pii]. 23881940.
36. Malkova A, Haber JE, Mutations arising during repair of chromosome breaks. Annual review of genetics. 2012;46:455–73. Epub 2012/11/14. doi: 10.1146/annurev-genet-110711-15554723146099.
37. Llorente B, Smith CE, Symington LS, Break-induced replication: what is it and what is it for?Cell Cycle. 2008;7(7):859–64. 18414031. doi: 10.4161/cc.7.7.5613
38. Donnianni RA, Symington LS, Break-induced replication occurs by conservative DNA synthesis. Proc Natl Acad Sci U S A. 2013;110(33):13475–80. Epub 2013/07/31. doi: 10.1073/pnas.130980011023898170.
39. Saini N, Ramakrishnan S, Elango R, Ayyar S, Zhang Y, Deem A, et al. Migrating bubble during break-induced replication drives conservative DNA synthesis. Nature. 2013;502(7471):389–92. Epub 2013/09/13. doi: 10.1038/nature12584 nature12584 [pii]. 24025772.
40. Wilson MA, Kwon Y, Xu Y, Chung WH, Chi P, Niu H, et al. Pif1 helicase and Poldelta promote recombination-coupled DNA synthesis via bubble migration. Nature. 2013;502(7471):393–6. Epub 2013/09/13. doi: 10.1038/nature12585 nature12585 [pii]. 24025768.
41. Smith CE, Llorente B, Symington LS, Template switching during break-induced replication. Nature. 2007;447(7140):102–5. 17410126. doi: 10.1038/nature05723
42. Yim E, O'Connell KE, St Charles J, Petes TD, High-resolution mapping of two types of spontaneous mitotic gene conversion events in Saccharomyces cerevisiae. Genetics. 2014;198(1):181–92. doi: 10.1534/genetics.114.16739524990991.
43. Richardson C, Jasin M, Coupled homologous and nonhomologous repair of a double-strand break preserves genomic integrity in mammalian cells. Molecular & Cellular Biology. 2000;20(23):9068–75.
44. Costantino L, Sotiriou SK, Rantala JK, Magin S, Mladenov E, Helleday T, et al. Break-induced replication repair of damaged forks induces genomic duplications in human cells. Science. 2014;343(6166):88–91. doi: 10.1126/science.124321124310611.
45. Yu AM, McVey M, Synthesis-dependent microhomology-mediated end joining accounts for multiple types of repair junctions. Nucleic Acids Res. 2010;38(17):5706–17. doi: 10.1093/nar/gkq37920460465.
46. Chan SH, Yu AM, McVey M, Dual roles for DNA polymerase theta in alternative end-joining repair of double-strand breaks in Drosophila. PLoS genetics. 2010;6(7):e1001005. doi: 10.1371/journal.pgen.100100520617203.
47. Xie A, Hartlerode A, Stucki M, Odate S, Puget N, Kwok A, et al. Distinct roles of chromatin-associated proteins MDC1 and 53BP1 in mammalian double-strand break repair. Mol Cell. 2007;28(6):1045–57. 18158901. doi: 10.1016/j.molcel.2007.12.005
48. Yan CT, Boboila C, Souza EK, Franco S, Hickernell TR, Murphy M, et al. IgH class switching and translocations use a robust non-classical end-joining pathway. Nature. 2007;449(7161):478–82. 17713479. doi: 10.1038/nature06020
49. Xie A, Puget N, Shim I, Odate S, Jarzyna I, Bassing CH, et al. Control of sister chromatid recombination by histone H2AX. Mol Cell. 2004;16(6):1017–25. 15610743. doi: 10.1016/j.molcel.2004.12.007
50. Gao Y, Sun Y, Frank KM, Dikkes P, Fujiwara Y, Seidl KJ, et al. A critical role for DNA end-joining proteins in both lymphogenesis and neurogenesis. Cell. 1998;95(7):891–902. 9875844.
51. Ferguson DO, Sekiguchi JM, Chang S, Frank KM, Gao Y, DePinho RA, et al. The nonhomologous end-joining pathway of DNA repair is required for genomic stability and the suppression of translocations. Proc Natl Acad Sci U S A. 2000;97(12):6630–3. 10823907. doi: 10.1073/pnas.110152897
52. Simsek D, Jasin M, Alternative end-joining is suppressed by the canonical NHEJ component Xrcc4-ligase IV during chromosomal translocation formation. Nature structural & molecular biology. 2010;17(4):410–6. doi: 10.1038/nsmb.177320208544.
53. Scully R, Chen J, Plug A, Xiao Y, Weaver D, Feunteun J, et al. Association of BRCA1 with Rad51 in mitotic and meiotic cells. Cell. 1997;88(2):265–75. 9008167
54. Anand RP, Tsaponina O, Greenwell PW, Lee CS, Du W, Petes TD, et al. Chromosome rearrangements via template switching between diverged repeated sequences. Genes Dev. 2014;28(21):2394–406. doi: 10.1101/gad.250258.11425367035.
55. Hastings PJ, Ira G, Lupski JR, A microhomology-mediated break-induced replication model for the origin of human copy number variation. PLoS genetics. 2009;5(1):e1000327. Epub 2009/01/31. doi: 10.1371/journal.pgen.100032719180184.
56. Lee JA, Carvalho CM, Lupski JR, A DNA replication mechanism for generating nonrecurrent rearrangements associated with genomic disorders. Cell. 2007;131(7):1235–47. doi: 10.1016/j.cell.2007.11.03718160035.
57. McVey M, Adams M, Staeva-Vieira E, Sekelsky JJ, Evidence for multiple cycles of strand invasion during repair of double-strand gaps in Drosophila. Genetics. 2004;167(2):699–705. 15238522. doi: 10.1534/genetics.103.025411
58. Sakofsky CJ, Ayyar S, Deem AK, Chung WH, Ira G, Malkova A, Translesion Polymerases Drive Microhomology-Mediated Break-Induced Replication Leading to Complex Chromosomal Rearrangements. Mol Cell. 2015;60(6):860–72. doi: 10.1016/j.molcel.2015.10.04126669261.
59. Foster SS, Balestrini A, Petrini JH, Functional interplay of the Mre11 nuclease and Ku in the response to replication-associated DNA damage. Mol Cell Biol. 2011;31(21):4379–89. Epub 2011/08/31. doi: 10.1128/MCB.05854-11 MCB.05854-11 [pii]. 21876003.
60. Shima N, Munroe RJ, Schimenti JC, The mouse genomic instability mutation chaos1 is an allele of Polq that exhibits genetic interaction with Atm. Mol Cell Biol. 2004;24(23):10381–9. doi: 10.1128/MCB.24.23.10381-10389.200415542845.
61. Roerink SF, van Schendel R, Tijsterman M, Polymerase theta-mediated end joining of replication-associated DNA breaks in C. elegans. Genome research. 2014;24(6):954–62. doi: 10.1101/gr.170431.11324614976.
62. Yousefzadeh MJ, Wood RD, DNA polymerase POLQ and cellular defense against DNA damage. DNA Repair (Amst). 2013;12(1):1–9. doi: 10.1016/j.dnarep.2012.10.00423219161.
63. Yousefzadeh MJ, Wyatt DW, Takata K, Mu Y, Hensley SC, Tomida J, et al. Mechanism of suppression of chromosomal instability by DNA polymerase POLQ. PLoS genetics. 2014;10(10):e1004654. doi: 10.1371/journal.pgen.100465425275444.
64. Wyatt DW, Feng W, Conlin MP, Yousefzadeh MJ, Roberts SA, Mieczkowski P, et al. Essential Roles for Polymerase theta-Mediated End Joining in the Repair of Chromosome Breaks. Mol Cell. 2016. doi: 10.1016/j.molcel.2016.06.02027453047.
65. Mayle R, Campbell IM, Beck CR, Yu Y, Wilson M, Shaw CA, et al. Mus81 and converging forks limit the mutagenicity of replication fork breakage. Science. 2015;349(6249):742–7. doi: 10.1126/science.aaa839126273056.
66. Xie A, Kwok A, Scully R, Role of mammalian Mre11 in classical and alternative nonhomologous end joining. Nature structural & molecular biology. 2009;16(8):814–8. 19633669. doi: 10.1038/nsmb.1640