Alternative end-joining mechanisms: A historical perspective

Frontiers in Genetics

Volumn 4, Issue APR, 2013, Pages

  Decottignies, Anabelle ^a  

^a DE DUVE INSTITUTE   (Belgium)

Author keywords

Alternative end joining; Chromosomal translocation; Double strand break; Ku70 ku80; Microhomology mediated end joining; Non homologous end joining; Single strand annealing; Telomere fusion

Indexed keywords

MAMMALIA;

EID: 84876161358     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2013.00048     Document Type: Review

References (53)

1. Audebert, M., Salles, B., and Calsou, P. (2004). 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. 279, 55117-55126.
2. Bae, N. S., and Baumann, P. (2007). A RAP1/TRF2 complex inhibits non-homologous end-joining at human telomeric DNA ends. Mol. Cell 26, 323-334.
3. Baumann, P., and Cech, T. R. (2000). Protection of telomeres by the Ku protein in fission yeast. Mol. Biol. Cell 11,3265-3275.
4. Bennardo, N., Cheng, A., Huang, N., and Stark, J. M. (2008). Altemative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet. 4:e1000110. doi:10.1371/journal. pgen. 1000110
5. Bentley, J., Diggle, C. P., Harnden, P., Knowles, M. A., and Kiltie, A. E. (2004). DNA double strand break repair in human bladder cancer is error prone and involves microhomology-associated end-joining. Nucleic Acids Res. 32, 5249-5259.
6. Boboila, C., Yan, C., Wesemann, D. R., Jankovic, M., Wang, J. H., Manis, J., et al. (2010a). Alternative end-joining catalyzes class switch recombination in the absence of both Ku70 and DNA ligase 4. J. Exp. Med. 207, 417-427.
7. Boboila, C., Jankovic, M., Yan, C. T., Wang, J. H., Wesemann, D. R., Zhang, T., et al. (2010b). Alternative end-joining catalyzes robust IgH locus deletions and translocations in the combined absence of ligase 4 and Ku70. Proc. Natl.AcadSci. U.S.A. 107, 3034-3039.
8. Boboila, C., Oksenych, V., Gostissa, M., Wang, J. H., Zha, S., Zhang, Y., et al. (2012). Robust chromosomal DNA repair via alternative end-joining in the absence of X-ray repair cross-complementing protein 1 (XRCC1). Proc. Natl. Acad Sci. U.S.A. 109, 2473-2478.
9. Boulton, S., and Jackson, S. P. (1996). Saccharomyces cerevisiae Ku70 potentiates illegitimate DNA double-strand break repair and serves as a barrier to error-prone DNA repair pathways. EMBO J. 15, 5083-5103.
10. Capper, R., Britt-Compton, B., Tankimanova, M., Rowson, J., Letsolo, B., Man, S., et al. (2007). The nature of telomere fusion and a definition of the critical telomere length in human cells. Genes Dev. 21, 2495-2508.
11. Chapman, J. R., Taylor, M. R. G., and Boulton, S. J. (2012). Playing the end game: DNA double-strand break repair pathway choice. Mol. Cell 47, 497-510.
12. Chapman, J. R., Barral, P., Vannier, J. B., Borel, V., Steger, M., Tomas-Loba, A., et al. (2013). RIF1 is essential for 53BP1-dependent nonhomologous end joining and suppression of DNA double-strand break resection. Mol. Cell 49, 858-871.
13. Decottignies, A. (2005). Capture of extranuclear DNA at fission yeast double-strand breaks. Genetics 171, 1535-1548.
14. Decottignies, A. (2007). Micro-homology-mediated end joining in fission yeast is repressed by Pku70 and relies on genes involved in homologous recombination. Genetics 176, 1403-1415.
15. Delia-Maria, J., Zhou, Y., Tsai, M.-S., Kuhnlein, J., Carney, J. P., Paull, T. T., et al. (2011). Human Mre1 1/Human Rad50/Nbs1 and DNA Ligase IIIa/XRCCl protein complexes act together in an alternative nonhomologous end joining pathway. J. Biol. Chem. 286, 33845-33853.
16. Di Virgilio, M., Callen, E., Yamane, A., Zhang, W., Jankovic, M., Gitlin, A. D., et al. (2013). Rif1 prevents resection of DNA breaks and promote immunoglobulin class switching. Science 339, 711-715.
17. Escribano-Diaz, C., Orthwein, A., Fradet-Turcotte, A., Xing, M., Young, J. T., Tkác, J., et al. (2013). A cell cycle-dependent regulatory circuit composed of 53BP1-RIF1 and BRCA1-CtIP controls DNA repair pathway choice. Mol. Cell 49, 872-883.
18. Feldmann, E., Schmiemann, V., Goedecke, W., Reichenberger, S., and Pfeiffer, P. (2000). DNA double-strand break repair in cell-free extracts from Ku80-deficient cells: implications for Ku serving as an alignment factor in non-homologous DNA end joining. Nucleic Acids Res. 32,2585-2596.
19. Gottlich, B., Reichenberger, S., Feldmann, E., and Pfeiffer, P. (1998). Rejoining of DNA double-strand breaks in vitro by single-strand annealing. Eur. J. Biochem. 258, 387-395.
20. Heacock, M., Idol, R. A., Friesner, J. D., Britt, A. B., and Shippen, D. E. (2007). Telomere dynamics and fusion of critically shortened telomeres in plants lacking DNA ligase IV. Nucleic Acids Res. 35, 6490-6500.
21. Heacock, M., Spangler, E., Riha, K., Puizina, J., and Shippen, D. E. (2004). Molecular analysis of telomere fusions in Arabidopsis: multiple pathways for chromosome end-joining. EMBO J. 23, 2304-2313.
22. Kabotyanski, E. B., Gomelsky, L., Han, J.-O., Stamato, T. D., and Roth, D. B. (1998). Double-strand break repair in Ku86- and XRCC4-deficient cells. Nucleic Acids Res. 26, 5333-5342.
23. Kramer, K. M., Brock, J. A., Bloom, K., Moore, J. K., and Haber, J. E. (1994). Two different types of double-strand breaks in Saccha-romyces cerevisiae are repaired by similar RAD52-independent, non-homologous recombination events. Mol. Cell. Biol. 14,1293-1301.
24. Letsolo, B. T., Rowson, J., and Baird, D. M. (2010). Fusion of short telomeres in human cells is characterized by extensive deletion and microho-mology, and can result in complex rearrangements. Nucleic Acids Res. 38,1841-1852.
25. Liang, L., Deng, L., Nguyen, S. C., Zhao, X., Maulion, C. D., Shao, C., et al. (2008). 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. 36, 3297-3310.
26. Ma, J.-L., Kim, E. M., Haber, J. E., and Lee, S. E. (2003). Yeast Mre 11 and Rad 1 proteins define a Ku-independent mechanism to repair double-strand breaks lacking overlapping end sequences. Mol. Cell. Biol. 23, 8820-8828.
27. Mason, R. M., Thacker, J., and Fairman, M. P. (1996). The joining of non-complementary DNA double-strand breaks by mammalian extracts. Nucleic Acids Res. 24, 4946-4953.
28. Mieczkowski, P. A., Mieczkowska, J. O., Dominaska, M., and Petes, T. D. (2003). Genetic regulation of telomere-telomere fusions in the yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U.S.A. 100, 10854-10859.
29. Paques, F., and Haber, J. E. (1999). Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63, 349-404.
30. Pierce, A. J., Hu, P., Han, M., Ellis, N., and Jasin, M. (2001). Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev. 15, 3237-3242.
31. Rai, R., Zheng, H., He, H., Luo, Y., Multani, A., Carpenter, P. B., et al. (2010). The function of classical and alternative non-homologous end-joining pathways in the fusion of dysfunctional telomeres. EMBO J. 29, 2598-2610.
32. Riha, K., and Shippen, D. E. (2003). Ku is required for telomeric C-rich strand maintenance, but not for end-to-end chromosome fusions in Ara-bidopsis. Proc. Natl. Acad. Sci. U.S.A. 100,611-615.
33. Rijkers, T., Van Den Ouwenland, J., Morolli, B., Rolink, A. G., Baarends, W. M., Van Sloun, P. P. H., et al. (1998). Targeted inactivation of mouse RAD52 reduces homologous recombination but not resistance to ionizing radiation. Mol. Cell. Biol. 18, 6423-6429.
34. Roth, D. B., Porter, T. N., and Wilson, J. H. (1985). Mechanisms of non-homologous recombination in mammalian cells. Mol. Cell. Biol. 5, 2599-2607.
35. Roth, D. B., and Wilson, J. H. (1986). Nonhomologous recombination in mammalian cells: role for short sequence homologies in the joining reaction. Mol. Cell. Biol. 6, 4295-4304.
36. Sfeir, A., and de Lange, T. (2012). Removal of shelterin reveals the telomere end-protection problem. Science 336, 593-597.
37. Sharpless, N. E., Ferguson, D. O., O'Hagan, R. C., Castrillon, D. H., Lee, C., Farazi, P. A., et al. (2001). Impaired nonhomologous end-joining provokes soft tissue sarcomas harboring chromosomal translocations, amplifications, and deletions. Mol. Cell 8, 1187-1196.
38. Simsek, D., Brunet, E., Wong, S. Y-W., Katyal, S., Gao, Y., McKinnon, P. J., et al. (2011). DNA Ligase III promotes alternative nonhomologous end-joining during chromosomal translocation formation. PLoS Genet. 7:el002080. doi:10.1371/jour-nal.pgen.1002080
39. Smogorzewska, A., and de Lange, T. (2002). Different telomere damage signaling pathways in human and mouse cells. EMBO J. 21, 4338-4348.
40. Soulas-Sprauel, P., Le Guyader, G., Rivera-Munoz, P., Abramowski, V., Olivier-Martin, C., Goujet-Zalc, C., et al. (2007). Role for DNA repair factor XRCC4 in immunoglobulin class switch recombination. J. Exp. Med. 204, 1717-1727.
41. Stark, J. M., Pierce, A. J., Oh, J., Pastink, A., and Jasin, M. (2004). Genetic steps of mammalian homologous repair with distinct mutagenic consequences. Mol. Cell. Biol. 24, 9305-9316.
42. Sugawara, N., Ira, G., and Haber, J. E. (2000). DNA length dependence of the single-strand annealing pathway and the role of Saccharomyces cerevisiae RAD59 in double-strand break repair. Mol. Cell. Biol. 20, 5300-5309.
43. Symington, L. S., and Gautier, J. (2011). Double-strand break resection and repair pathway choice. Annu. Rev. Genet. 45,247-271.
44. Tankimanova, M., Capper, R., Letsolo, B. T., Rowson, J., Jones, R. E., Britt-Compton, B., et al. (2012). Mre11 modulates the fidelity of fusion between short telomeres in human cells. Nucleic Acids Res. 40, 2518-2526.
45. van Steensel, B., Smogorzewska, A., and de Lange, T. (1998). TRF2 protects human telomeres from end-to-end fusions. Cell 92, 401-413.
46. Wang, H., Perrault, A. R., Takeda, Y., Qin, W., Wang, H., and Iliakis, G. (2003). Biochemical evidence for Ku-independent backup pathways of NHEJ. Nucleic Acids Res. 31, 5377-5388.
47. Wang, H., Rosidi, B., Perrault, R., Wang, M., Zhang, L., Windhofer, F., et al. (2005). DNA Ligase III as a candidate component of backup pathways of nonhomologous end joining. Cancer Res. 65, 4020-4030.
48. Wang, J. H., Alt, E W., Gostissa, M., Datta, A., Murphy, M., Alimzhanov, M. B., et al. (2008). Oncogenic transformation in the absence of Xrcc4 targets peripheral B cells that have undergone editing and switching. J. Exp. Med. 205, 3079-3080.
49. Weterings, E., and Chen, D. J. (2008). The endless tale of non-homologous end-joining. Cell Res. 18, 114-124.
50. Yan, C. T., Boboila, C., Souza, E. K., Franco, S., Hickernell, T. R., Murphy, M., et al. (2007). IgH class switching and translocations use a robust non-classical end-joining pathway. Nature 449, 478-482.
51. Yu, X., and Gabriel, A. (2003). Ku-dependent and Ku-independent end-joining pathways lead to chromosomal rearrangements during double-strand break repair in Saccharomyces cerevisiae. Genetics 163, 843-856.
52. Zhu, C., Mills, K. D., Ferguson, D. O., Lee, C., Manis, J., Fleming, J., et al. (2002). Unrepaired DNA breaks in p53-deficient cells lead to oncogenic gene amplification subsequent to translocations. Cell 109, 811-821.
53. Zimmermann, M., Lottersberger, F., Buonomo, S. B., Sfeir, A., and de Lange, T. (2013). 53BP1 regulates DSB repair using Rif1 to control 5' end resection. Science 339, 700-704.