DNA double-strand break repair: How to fix a broken relationship

Cellular and Molecular Life Sciences

Volumn 66, Issue 6, 2009, Pages 1039-1056

  Pardo, B ^a   Gomez Gonzalez B ^a   Aguilera, A ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

Author keywords

Checkpoint; DNA repair; Genome stability; Homologous recombination; Nonhomologous end joining; Repair pathway choice

Indexed keywords

PROTEIN RAD9; POLYDEOXYRIBONUCLEOTIDE SYNTHASE;

APOPTOSIS; BASE PAIRING; CELL CYCLE; CELL CYCLE ARREST; DNA DAMAGE; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; EUKARYOTIC CELL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REVIEW; GENETIC RECOMBINATION; GENOMIC INSTABILITY; METABOLISM; PHYSIOLOGY;

EUKARYOTA;

CELL CYCLE; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA LIGASES; DNA REPAIR; DNA REPLICATION; GENOMIC INSTABILITY; RECOMBINATION, GENETIC;

EID: 62349103878     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-009-8740-3     Document Type: Review

References (167)

1. Rich, T., Allen, R. L. and Wyllie, A. H. (2000) Defying death after DNA damage. Nature 407, 777-783.
2. 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.
3. Keeney, S. and Neale, M. J. (2006) Initiation of meiotic recombination by formation of DNA double-strand breaks: mechanism and regulation. Biochem. Soc. Trans. 34, 523-525.
4. Soulas-Sprauel, P., Rivera-Munoz, P., Malivert, L., Le Guyader, G., Abramowski, V., Revy, P. and de Villartay, J. P. (2007) V(D)J and immunoglobulin class switch recombinations: a paradigm to study the regulation of DNA end-joining. Oncogene 26, 7780-7791.
5. Weinert, T. A. and Hartwell, L. H. (1988) The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science 241, 317-322.
6. Su, T. T. (2006) Cellular responses to DNA damage: one signal, multiple choices. Annu. Rev. Genet. 40, 187-208.
7. Chen, L., Trujillo, K., Ramos, W., Sung, P. and Tomkinson, A. E. (2001) Promotion of Dnl4-catalyzed DNA end-joining by the Rad50/Mre11/Xrs2 and Hdf1/Hdf2 complexes. Mol. Cell 8, 1105-1115.
8. Hopfner, K. P., Craig, L., Moncalian, G., Zinkel, R. A., Usui, T., Owen, B. A., Karcher, A., Henderson, B., Bodmer, J.L., McMurray, C.T. et al. (2002) The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair. Nature 418, 562-566.
9. Grenon, M., Gilbert, C. and Lowndes, N. F. (2001) Checkpoint activation in response to double-strand breaks requires the Mre11/Rad50/Xrs2 complex. Nat. Cell. Biol. 3, 844-847.
10. Lee, J. H. and Paull, T. T. (2005) ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 308, 551-554.
11. Paull, T. T. and Lee, J. H. (2005) The Mre11/Rad50/Nbs1 complex and its role as a DNA double-strand break sensor for ATM. Cell Cycle 4, 737-740.
12. Mantiero, D., Clerici, M., Lucchini, G. and Longhese, M. P. (2007) Dual role for Saccharomyces cerevisiae Tel1 in the checkpoint response to double-strand breaks. EMBO Rep. 8, 380-387.
13. Zou, L. and Elledge, S. J. (2003) Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300, 1542-1548.
14. Jazayeri, A., Falck, J., Lukas, C., Bartek, J., Smith, G. C., Lukas, J. and Jackson, S. P. (2006) ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat. Cell. Biol. 8, 37-45.
15. Adams, K. E., Medhurst, A. L., Dart, D. A. and Lakin, N. D. (2006) Recruitment of ATR to sites of ionising radiation-induced DNA damage requires ATM and components of the MRN protein complex. Oncogene 25, 3894-3904.
16. Dubrana, K., van Attikum, H., Hediger, F. and Gasser, S. M. (2007) The processing of double-strand breaks and binding of single-strand-binding proteins RPA and Rad51 modulate the formation of ATR-kinase foci in yeast. J. Cell. Sci. 120, 4209-4220.
17. Paciotti, V., Clerici, M., Lucchini, G. and Longhese, M. P. (2000) The checkpoint protein Ddc2, functionally related to S. pombe Rad26, interacts with Mec1 and is regulated by Mec1-dependent phosphorylation in budding yeast. Genes Dev. 14, 2046-2059.
18. Rouse, J. and Jackson, S. P. (2000) LCD1: an essential gene involved in checkpoint control and regulation of the MEC1 signalling pathway in Saccharomyces cerevisiae. EMBO J. 19, 5801-5812.
19. Melo, J. A., Cohen, J. and Toczyski, D. P. (2001) Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. Genes Dev. 15, 2809-2821.
20. Zou, L., Liu, D. and Elledge, S. J. (2003) Replication protein A-mediated recruitment and activation of Rad17 complexes. Proc. Natl. Acad. Sci. USA 100, 13827-13832.
21. Naiki, T., Shimomura, T., Kondo, T., Matsumoto, K. and Sugimoto, K. (2000) Rfc5, in cooperation with rad24, controls DNA damage checkpoints throughout the cell cycle in Saccharomyces cerevisiae. Mol. Cell. Biol. 20, 5888-5896.
22. Rogakou, E. P., Pilch, D.R., Orr, A. H., Ivanova, V. S. and Bonner, W. M. (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273, 5858-5868.
23. Stucki, M., Clapperton, J. A., Mohammad, D., Yaffe, M. B., Smerdon, S. J. and Jackson, S. P. (2005) MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 123, 1213-1226.
24. Celeste, A., Fernandez-Capetillo, O., Kruhlak, M. J., Pilch, D. R., Staudt, D. W., Lee, A., Bonner, R. F., Bonner, W. M. and Nussenzweig, A. (2003) Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat. Cell. Biol. 5, 675-679.
25. Downs, J. A., Lowndes, N. F. and Jackson, S. P. (2000) A role for Saccharomyces cerevisiae histone H2A in DNA repair. Nature 408, 1001-1004.
26. Morrison, A. J., Highland, J., Krogan, N. J., Arbel-Eden, A., Greenblatt, J. F., Haber, J. E. and Shen, X. (2004) INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 119, 767-775.
27. van Attikum, H., Fritsch, O., Hohn, B. and Gasser, S. M. (2004) Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119, 777-788.
28. Bao, Y. and Shen, X. (2007) Chromatin remodeling in DNA double-strand break repair. Curr. Opin. Genet. Dev. 17, 126-131.
29. Herzberg, K., Bashkirov, V.I., Rolfsmeier, M., Haghnazari, E., McDonald, W. H., Anderson, S., Bashkirova, E. V., Yates, J.R., 3rd and Heyer, W. D. (2006) Phosphorylation of Rad55 on serines 2, 8, and 14 is required for efficient homologous recombination in the recovery of stalled replication forks. Mol. Cell. Biol. 26, 8396-8409.
30. Ahnesorg, P. and Jackson, S. P. (2007) The non-homologous end-joining protein Nej1p is a target of the DNA damage checkpoint. DNA Repair (Amst) 6, 190-201.
31. Moore, J. K. and Haber, J. E. (1996) Cell cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae. Mol. Cell. Biol. 16, 2164-2173.
32. Wilson, T. E., Grawunder, U. and Lieber, M. R. (1997) Yeast DNA ligase IV mediates non-homologous DNA end joining. Nature 388, 495-498.
33. Wilson, T. E. and Lieber, M. R. (1999) Efficient processing of DNA ends during yeast nonhomologous end joining. Evidence for a DNA polymerase beta (Pol4)-dependent pathway. J. Biol. Chem. 274, 23599-23609.
34. Boulton, S. J. 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, 5093-5103.
35. Daley, J. M. and Wilson, T. E. (2005) Rejoining of DNA double-strand breaks as a function of overhang length. Mol. Cell. Biol. 25, 896-906.
36. Daley, J. M., Palmbos, P. L., Wu, D. and Wilson, T. E. (2005) Nonhomologous end joining in yeast. Annu. Rev. Genet. 39, 431-451.
37. Lisby, M., Barlow, J. H., Burgess, R. C. and Rothstein, R. (2004) Choreography of the DNA damage response: spatio-temporal relationships among checkpoint and repair proteins. Cell 118, 699-713.
38. Lisby, M., Antunez de Mayolo, A., Mortensen, U. H. and Rothstein, R. (2003) Cell cycle-regulated centers of DNA double-strand break repair. Cell Cycle 2, 479-483.
39. Lobachev, K., Vitriol, E., Stemple, J., Resnick, M. A. and Bloom, K. (2004) Chromosome fragmentation after induction of a double-strand break is an active process prevented by the RMX repair complex. Curr. Biol. 14, 2107-2112.
40. Moreau, S., Ferguson, J. R. and Symington, L. S. (1999) The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol. Cell. Biol. 19, 556-566.
41. Trujillo, K. M., Yuan, S. S., Lee, E. Y. and Sung, P. (1998) Nuclease activities in a complex of human recombination and DNA repair factors Rad50, Mre11, and p95. J. Biol. Chem. 273, 21447-21450.
42. Trujillo, K. M., Roh, D. H., Chen, L., Van Komen, S., Tomkinson, A. and Sung, P. (2003) Yeast xrs2 binds DNA and helps target rad50 and mre11 to DNA ends. J. Biol. Chem. 278, 48957-48964.
43. D'Amours, D. and Jackson, S. P. (2001) The yeast Xrs2 complex functions in S phase checkpoint regulation. Genes Dev. 15, 2238-2249.
44. Palmbos, P. L., Daley, J. M. and Wilson, T. E. (2005) Mutations of the Yku80 C terminus and Xrs2 FHA domain specifically block yeast nonhomologous end joining. Mol. Cell. Biol. 25, 10782-10790.
45. Gottlieb, T. M. and Jackson, S. P. (1993) The DNA-dependent protein kinase: requirement for DNA ends and association with Ku antigen. Cell 72, 131-142.
46. Spagnolo, L., Rivera-Calzada, A., Pearl, L. H. and Llorca, O. (2006) Three-dimensional structure of the human DNA-PKcs/Ku70/Ku80 complex assembled on DNA and its implications for DNA DSB repair. Mol. Cell 22, 511-519.
47. Ribes-Zamora, A., Mihalek, I., Lichtarge, O. and Bertuch, A. A. (2007) Distinct faces of the Ku heterodimer mediate DNA repair and telomeric functions. Nat. Struct. Mol. Biol. 14, 301-307.
48. Lee, S. E., Moore, J. K., Holmes, A., Umezu, K., Kolodner, R. D. and Haber, J. E. (1998) Saccharomyces Ku70, mre11/rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell 94, 399-409.
49. Zhang, Y., Hefferin, M. L., Chen, L., Shim, E. Y., Tseng, H. M., Kwon, Y., Sung, P., Lee, S. E. and Tomkinson, A. E. (2007) Role of Dnl4-Lif1 in nonhomologous end-joining repair complex assembly and suppression of homologous recombination. Nat. Struct. Mol. Biol. 14, 639-646.
50. Grawunder, U., Wilm, M., Wu, X., Kulesza, P., Wilson, T. E., Mann, M. and Lieber, M. R. (1997) Activity of DNA ligase IV stimulated by complex formation with XRCC4 protein in mammalian cells. Nature 388, 492-495.
51. Herrmann, G., Lindahl, T. and Schar, P. (1998) Saccharomyces cerevisiae LIF1: a function involved in DNA double-strand break repair related to mammalian XRCC4. EMBO J. 17, 4188-4198.
52. Sibanda, B. L., Critchlow, S. E., Begun, J., Pei, X. Y., Jackson, S. P., Blundell, T. L. and Pellegrini, L. (2001) Crystal structure of an Xrcc4-DNA ligase IV complex. Nat. Struct. Biol. 8, 1015-1019.
53. Ahnesorg, P., Smith, P. and Jackson, S. P. (2006) XLF interacts with the XRCC4-DNA ligase IV complex to promote DNA nonhomologous end-joining. Cell 124, 301-313.
54. Frank-Vaillant, M. and Marcand, S. (2001) NHEJ regulation by mating type is exercised through a novel protein, Lif2p, essential to the ligase IV pathway. Genes Dev. 15, 3005-3012.
55. Lu, H., Pannicke, U., Schwarz, K. and Lieber, M. R. (2007) Length-dependent binding of human XLF to DNA and stimulation of XRCC4.DNA ligase IV activity. J. Biol. Chem. 282, 11155-11162.
56. Gu, J., Lu, H., Tsai, A. G., Schwarz, K. and Lieber, M. R. (2007) Single-stranded DNA ligation and XLF-stimulated incompatible DNA end ligation by the XRCC4-DNA ligase IV complex: influence of terminal DNA sequence. Nucleic Acids Res. 35, 5755-5762.
57. Tsai, C. J., Kim, S. A. and Chu, G. (2007) Cernunnos/XLF promotes the ligation of mismatched and noncohesive DNA ends. Proc. Natl. Acad. Sci. USA 104, 7851-7856.
58. Chappell, C., Hanakahi, L.A., Karimi-Busheri, F., Weinfeld, M. and West, S. C. (2002) Involvement of human polynucleotide kinase in double-strand break repair by non-homologous end joining. EMBO J. 21, 2827-2832.
59. Koch, C. A., Agyei, R., Galicia, S., Metalnikov, P., O Donnell, P., Starostine, A., Weinfeld, M. and Durocher, D. (2004) Xrcc4 physically links DNA end processing by polynucleotide kinase to DNA ligation by DNA ligase IV. EMBO J. 23, 3874-3885.
60. Ahel, I., Rass, U., El-Khamisy, S. F., Katyal, S., Clements, P. M., McKinnon, P. J., Caldecott, K. W. and West, S. C. (2006) The neurodegenerative disease protein aprataxin resolves abortive DNA ligation intermediates. Nature 443, 713-716.
61. Clements, P. M., Breslin, C., Deeks, E. D., Byrd, P. J., Ju, L., Bieganowski, P., Brenner, C., Moreira, M. C., Taylor, A. M. and Caldecott, K. W. (2004) The ataxia-oculomotor apraxia 1 gene product has a role distinct from ATM and interacts with the DNA strand break repair proteins XRCC1 and XRCC4. DNA Repair (Amst) 3, 1493-1502.
62. Tseng, H. M. and Tomkinson, A. E. (2004) Processing and joining of DNA ends coordinated by interactions among Dnl4/Lif1, Pol4, and FEN-1. J. Biol. Chem. 279, 47580-47588.
63. Wu, X., Wilson, T. E. and Lieber, M. R. (1999) A role for FEN-1 in nonhomologous DNA end joining: the order of strand annealing and nucleolytic processing events. Proc. Natl. Acad. Sci. USA 96, 1303-1308.
64. Ma, Y., Pannicke, U., Schwarz, K. and Lieber, M. R. (2002) Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination. Cell 108, 781-794.
65. Niewolik, D., Pannicke, U., Lu, H., Ma, Y., Wang, L. C., Kulesza, P., Zandi, E., Lieber, M. R. and Schwarz, K. (2006) DNA-PKcs dependence of Artemis endonucleolytic activity, differences between hairpins and 5′ or 3′ overhangs. J. Biol. Chem. 281, 33900-33909.
66. Daley, J. M., Laan, R. L., Suresh, A. and Wilson, T.E. (2005) DNA joint dependence of pol X family polymerase action in nonhomologous end joining. J. Biol. Chem. 280, 29030-29037.
67. Lee, J. W., Blanco, L., Zhou, T., Garcia-Diaz, M., Bebenek, K., Kunkel, T. A., Wang, Z. and Povirk, L. F. (2004) Implication of DNA polymerase lambda in alignment-based gap filling for nonhomologous DNA end joining in human nuclear extracts. J. Biol. Chem. 279, 805-811.
68. Mahajan, K. N., Nick McElhinny, S. A., Mitchell, B. S. and Ramsden, D. A. (2002) Association of DNA polymerase mu (pol mu) with Ku and ligase IV: role for pol mu in end-joining double-strand break repair. Mol. Cell. Biol. 22, 5194-5202.
69. Moon, A. F., Garcia-Diaz, M., Batra, V. K., Beard, W. A., Bebenek, K., Kunkel, T. A., Wilson, S. H. and Pedersen, L. C. (2007) The X family portrait: structural insights into biological functions of X family polymerases. DNA Repair (Amst) 6, 1709-1725.
70. Nick McElhinny, S. A., Havener, J. M., Garcia-Diaz, M., Juarez, R., Bebenek, K., Kee, B. L., Blanco, L., Kunkel, T. A. and Ramsden, D. A. (2005) A gradient of template dependence defines distinct biological roles for family x polymerases in nonhomologous end joining. Mol. Cell 19, 357-366.
71. Pardo, B., Ma, E. and Marcand, S. (2006) Mismatch tolerance by DNA polymerase Pol4 in the course of nonhomologous end joining in Saccharomyces cerevisiae. Genetics 172, 2689-2694.
72. Ma, J. L., Kim, E. M., Haber, J. E. and Lee, S. E. (2003) Yeast Mre11 and Rad1 proteins define a Ku-independent mechanism to repair double-strand breaks lacking overlapping end sequences. Mol. Cell. Biol. 23, 8820-8828.
73. Decottignies, A. (2007) Microhomology-mediated end joining in fission yeast is repressed by pku70 and relies on genes involved in homologous recombination. Genetics 176, 1403-1415.
74. Katsura, Y., Sasaki, S., Sato, M., Yamaoka, K., Suzukawa, K., Nagasawa, T., Yokota, J. and Kohno, T. (2007) Involvement of Ku80 in microhomology- mediated end joining for DNA double-strand breaks in vivo. DNA Repair (Amst) 6, 639-648.
75. Lee, K. and Lee, S. E. (2007) Saccharomyces cerevisiae Sae2- and Tel1-dependent single-strand DNA formation at DNA break promotes microhomology-mediated end joining. Genetics 176, 2003-2014.
76. Krogh, B. O. and Symington, L. S. (2004) Recombination proteins in yeast. Annu. Rev. Genet. 38, 233-271.
77. Szostak, J. W., Orr-Weaver, T. L., Rothstein, R. J. and Stahl, F. W. (1983) The double-strand-break repair model for recombination. Cell 33, 25-35.
78. Sun, H., Treco, D. and Szostak, J. W. (1991) Extensive 3′-overhanging, single-stranded DNA associated with the meiosis-specific double-strand breaks at the ARG4 recombination initiation site. Cell 64, 1155-1161.
79. White, C. I. and Haber, J. E. (1990) Intermediates of recombination during mating type switching in Saccharomyces cerevisiae. EMBO J. 9, 663-673.
80. Bressan, D. A., Baxter, B. K. and Petrini, J. H. (1999) The Mre11-Rad50-Xrs2 protein complex facilitates homologous recombination-based double-strand break repair in Saccharomyces cerevisiae. Mol. Cell. Biol. 19, 7681-7687.
81. Johzuka, K. and Ogawa, H. (1995) Interaction of Mre11 and Rad50: two proteins required for DNA repair and meiosis-specific double-strand break formation in Saccharomyces cerevisiae. Genetics 139, 1521-1532.
82. Moreau, S., Morgan, E. A. and Symington, L. S. (2001) Overlapping functions of the Saccharomyces cerevisiae Mre11, Exo1 and Rad27 nucleases in DNA metabolism. Genetics 159, 1423-1433.
83. Llorente, B. and Symington, L. S. (2004) The Mre11 nuclease is not required for 5′ to 3′ resection at multiple HO-induced double-strand breaks. Mol. Cell. Biol. 24, 9682-9694.
84. Ivanov, E. L., Sugawara, N., White, C. I., Fabre, F. and Haber, J. E. (1994) Mutations in XRS2 and RAD50 delay but do not prevent mating-type switching in Saccharomyces cerevisiae. Mol. Cell. Biol. 14, 3414-3425.
85. McKee, A. H. and Kleckner, N. (1997) A general method for identifying recessive diploid-specific mutations in Saccharomyces cerevisiae, its application to the isolation of mutants blocked at intermediate stages of meiotic prophase and characterization of a new gene SAE2. Genetics 146, 797-816.
86. Sartori, A. A., Lukas, C., Coates, J., Mistrik, M., Fu, S., Bartek, J., Baer, R., Lukas, J. and Jackson, S. P. (2007) Human CtIP promotes DNA end resection. Nature 450, 509-514.
87. Lengsfeld, B. M., Rattray, A. J., Bhaskara, V., Ghirlando, R. and Paull, T. T. (2007) Sae2 Is an endonuclease that processes hairpin DNA cooperatively with the Mre11/Rad50/Xrs2 complex. Mol. Cell 28, 638-651.
88. Tsubouchi, H. and Ogawa, H. (2000) Exo1 roles for repair of DNA double-strand breaks and meiotic crossing over in Saccharomyces cerevisiae. Mol. Biol. Cell. 11, 2221-2233.
89. Song, B. and Sung, P. (2000) Functional interactions among yeast Rad51 recombinase, Rad52 mediator, and replication protein A in DNA strand exchange. J. Biol. Chem. 275, 15895-15904.
90. Alani, E., Thresher, R., Griffith, J. D. and Kolodner, R. D. (1992) Characterization of DNA-binding and strand-exchange stimulation properties of y-RPA, a yeast single-strand-DNA-binding protein. J. Mol. Biol. 227, 54-71.
91. Hays, S. L., Firmenich, A. A., Massey, P., Banerjee, R. and Berg, P. (1998) Studies of the interaction between Rad52 protein and the yeast single-stranded DNA binding protein RPA. Mol. Cell. Biol. 18, 4400-4406.
92. Symington, L. S. (2002) Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol. Mol. Biol. Rev. 66, 630-670, table of contents.
93. Davies, O. R. and Pellegrini, L. (2007) Interaction with the BRCA2 C terminus protects RAD51-DNA filaments from disassembly by BRC repeats. Nat. Struct. Mol. Biol. 14, 475-483.
94. Esashi, F., Galkin, V. E., Yu, X., Egelman, E. H. and West, S. C. (2007) Stabilization of RAD51 nucleoprotein filaments by the C-terminal region of BRCA2. Nat. Struct. Mol. Biol. 14, 468-474.
95. Sugawara, N., Wang, X. and Haber, J. E. (2003) In vivo roles of Rad52, Rad54, and Rad55 proteins in Rad51-mediated recombination. Mol. Cell 12, 209-219.
96. Sung, P. (1997) Yeast Rad55 and Rad57 proteins form a heterodimer that functions with replication protein A to promote DNA strand exchange by Rad51 recombinase. Genes Dev. 11, 1111-1121.
97. Bugreev, D. V., Hanaoka, F. and Mazin, A. V. (2007) Rad54 dissociates homologous recombination intermediates by branch migration. Nat. Struct. Mol. Biol. 14, 746-753.
98. Heyer, W. D., Li, X., Rolfsmeier, M. and Zhang, X. P. (2006) Rad54: the Swiss Army knife of homologous recombination? Nucleic Acids Res. 34, 4115-4125.
99. Ristic, D., Modesti, M., van der Heijden, T., van Noort, J., Dekker, C., Kanaar, R. and Wyman, C. (2005) Human Rad51 filaments on double- and single-stranded DNA: correlating regular and irregular forms with recombination function. Nucleic Acids Res. 33, 3292-3302.
100. Ira, G. and Haber, J. E. (2002) Characterization of RAD51-independent break-induced replication that acts preferentially with short homologous sequences. Mol. Cell. Biol. 22, 6384-6392.
101. Amitani, I., Baskin, R. J. and Kowalczykowski, S. C. (2006) Visualization of Rad54, a chromatin remodeling protein, translocating on single DNA molecules. Mol. Cell 23, 143-148.
102. Mortensen, U. H., Bendixen, C., Sunjevaric, I. and Rothstein, R. (1996) DNA strand annealing is promoted by the yeast Rad52 protein. Proc. Natl. Acad. Sci. USA 93, 10729-10734.
103. Ira, G., Malkova, A., Liberi, G., Foiani, M. and Haber, J. E. (2003) Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115, 401-411.
104. Robert, T., Dervins, D., Fabre, F. and Gangloff, S. (2006) Mrc1 and Srs2 are major actors in the regulation of spontaneous crossover. EMBO J. 25, 2837-2846.
105. Nassif, N., Penney, J., Pal, S., Engels, W. R. and Gloor, G. B. (1994) Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair. Mol. Cell. Biol. 14, 1613-1625.
106. Wu, L. and Hickson, I. D. (2003) The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426, 870-874.
107. Bugreev, D. V., Yu, X., Egelman, E. H. and Mazin, A. V. (2007) Novel pro- and anti-recombination activities of the Bloom's syndrome helicase. Genes Dev. 21, 3085-3094.
108. Veaute, X., Jeusset, J., Soustelle, C., Kowalczykowski, S. C., Le Cam, E. and Fabre, F. (2003) The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423, 309-312.
109. Dupaigne, P., Le Breton, C., Fabre, F., Gangloff, S., Le Cam, E. and Veaute, X. (2008) The Srs2 helicase activity is stimulated by Rad51 filaments on dsDNA: implications for crossover incidence during mitotic recombination. Mol. Cell 29, 243-254.
110. Liu, Y., Masson, J. Y., Shah, R., O'Regan, P. and West, S. C. (2004) RAD51C is required for Holliday junction processing in mammalian cells. Science 303, 243-246.
111. Wu, L., Bachrati, C. Z., Ou, J., Xu, C., Yin, J., Chang, M., Wang, W., Li, L., Brown, G. W. and Hickson, I. D. (2006) BLAP75/RMI1 promotes the BLM-dependent dissolution of homologous recombination intermediates. Proc. Natl. Acad. Sci. USA 103, 4068-4073.
112. Kaliraman, V., Mullen, J. R., Fricke, W. M., Bastin-Shanower, S. A. and Brill, S. J. (2001) Functional overlap between Sgs1-Top3 and the Mms4-Mus81 endonuclease. Genes Dev. 15, 2730-2740.
113. Mullen, J. R., Nallaseth, F. S., Lan, Y. Q., Slagle, C. E. and Brill, S. J. (2005) Yeast Rmi1/Nce4 controls genome stability as a subunit of the Sgs1-Top3 complex. Mol. Cell. Biol. 25, 4476-4487.
114. Fricke, W. M., Bastin-Shanower, S. A. and Brill, S. J. (2005) Substrate specificity of the Saccharomyces cerevisiae Mus81-Mms4 endonuclease. DNA Repair (Amst) 4, 243-251.
115. Osman, F., Dixon, J., Doe, C. L. and Whitby, M. C. (2003) Generating crossovers by resolution of nicked Holliday junctions: a role for Mus81-Eme1 in meiosis. Mol. Cell 12, 761-774.
116. Lundblad, V. and Blackburn, E. H. (1993) An alternative pathway for yeast telomere maintenance rescues est1- senescence. Cell 73, 347-360.
117. Morrow, D. M., Connelly, C. and Hieter, P. (1997) 'Break copy' duplication: a model for chromosome fragment formation in Saccharomyces cerevisiae. Genetics 147, 371-382.
118. Voelkel-Meiman, K. and Roeder, G. S. (1990) Gene conversion tracts stimulated by HOT1-promoted transcription are long and continuous. Genetics 126, 851-867.
119. Bosco, G. and Haber, J. E. (1998) Chromosome break-induced DNA replication leads to nonreciprocal translocations and telomere capture. Genetics 150, 1037-1047.
120. Smith, C. E., Llorente, B. and Symington, L. S. (2007) Template switching during break-induced replication. Nature 447, 102-105.
121. Davis, A. P. and Symington, L. S. (2004) RAD51-dependent break-induced replication in yeast. Mol. Cell. Biol. 24, 2344-2351.
122. Malkova, A., Naylor, M. L., Yamaguchi, M., Ira, G. and Haber, J. E. (2005) RAD51-dependent break-induced replication differs in kinetics and checkpoint responses from RAD51-mediated gene conversion. Mol. Cell. Biol. 25, 933-944.
123. Lydeard, J. R., Jain, S., Yamaguchi, M. and Haber, J. E. (2007) Break-induced replication and telomerase-independent telomere maintenance require Pol32. Nature 448, 820-823.
124. Malkova, A., Ivanov, E. L. and Haber, J. E. (1996) Double-strand break repair in the absence of RAD51 in yeast: a possible role for break-induced DNA replication. Proc. Natl. Acad. Sci. USA 93, 7131-7136.
125. Signon, L., Malkova, A., Naylor, M. L., Klein, H. and Haber, J. E. (2001) Genetic requirements for RAD51- and RAD54-independent break-induced replication repair of a chromosomal double-strand break. Mol. Cell. Biol. 21, 2048-2056.
126. VanHulle, K., Lemoine, F. J., Narayanan, V., Downing, B., Hull, K., McCullough, C., Bellinger, M., Lobachev, K., Petes, T. D. and Malkova, A. (2007) Inverted DNA repeats channel repair of distant double-strand breaks into chromatid fusions and chromosomal rearrangements. Mol. Cell. Biol. 27, 2601-2614.
127. Bai, Y. and Symington, L. S. (1996) A Rad52 homolog is required for RAD51-independent mitotic recombination in Saccharomyces cerevisiae. Genes Dev. 10, 2025-2037.
128. Kang, L. E. and Symington, L. S. (2000) Aberrant double-strand break repair in rad51 mutants of Saccharomyces cerevisiae. Mol. Cell. Biol. 20, 9162-9172.
129. Malagon, F. and Aguilera, A. (2001) Yeast spt6-140 mutation, affecting chromatin and transcription, preferentially increases recombination in which Rad51p-mediated strand exchange is dispensable. Genetics 158, 597-611.
130. Aguilera, A. (2001) Double-strand break repair: are Rad51/RecA-DNA joints barriers to DNA replication? Trends Genet. 17, 318-321.
131. Lin, F. L., Sperle, K. and Sternberg, N. (1984) Model for homologous recombination during transfer of DNA into mouse L cells: role for DNA ends in the recombination process. Mol. Cell. Biol. 4, 1020-1034.
132. Fishman-Lobell, J., Rudin, N. and Haber, J. E. (1992) Two alternative pathways of double-strand break repair that are kinetically separable and independently modulated. Mol. Cell. Biol. 12, 1292-1303.
133. Fishman-Lobell, J. and Haber, J. E. (1992) Removal of nonhomologous DNA ends in double-strand break recombination: the role of the yeast ultraviolet repair gene RAD1. Science 258, 480-484.
134. Flott, S., Alabert, C., Toh, G. W., Toth, R., Sugawara, N., Campbell, D. G., Haber, J.E., Pasero, P. and Rouse, J. (2007) Phosphorylation of Slx4 by Mec1 and Tel1 regulates the single-strand annealing mode of DNA repair in budding yeast. Mol. Cell. Biol. 27, 6433-6445.
135. Saparbaev, M., Prakash, L. and Prakash, S. (1996) Requirement of mismatch repair genes MSH2 and MSH3 in the RAD1-RAD10 pathway of mitotic recombination in Saccharomyces cerevisiae. Genetics 142, 727-736.
136. Schar, P., Herrmann, G., Daly, G. and Lindahl, T. (1997) A newly identified DNA ligase of Saccharomyces cerevisiae involved in RAD52-independent repair of DNA double-strand breaks. Genes Dev. 11, 1912-1924.
137. Siede, W., Friedl, A. A., Dianova, I., Eckardt-Schupp, F. and Friedberg, E. C. (1996) The Saccharomyces cerevisiae Ku autoantigen homologue affects radiosensitivity only in the absence of homologous recombination. Genetics 142, 91-102.
138. Frank-Vaillant, M. and Marcand, S. (2002) Transient stability of DNA ends allows nonhomologous end joining to precede homologous recombination. Mol. Cell 10, 1189-1199.
139. Aylon, Y., Liefshitz, B. and Kupiec, M. (2004) The CDK regulates repair of double-strand breaks by homologous recombination during the cell cycle. EMBO J. 23, 4868-4875.
140. Ira, G., Pellicioli, A., Balijja, A., Wang, X., Fiorani, S., Carotenuto, W., Liberi, G., Bressan, D., Wan, L., Hollingsworth, N. M., Haber, J. E. et al. (2004) DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 431, 1011-1017.
141. Ferreira, M. G. and Cooper, J. P. (2004) Two modes of DNA double-strand break repair are reciprocally regulated through the fission yeast cell cycle. Genes Dev. 18, 2249-2254.
142. Takata, M., Sasaki, M. S., Sonoda, E., Morrison, C., Hashimoto, M., Utsumi, H., Yamaguchi-Iwai, Y., Shinohara, A. and Takeda, S. (1998) Homologous recombination and nonhomologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J. 17, 5497-5508.
143. Astrom, S. U., Okamura, S. M. and Rine, J. (1999) Yeast cell-type regulation of DNA repair. Nature 397, 310.
144. Cortes-Ledesma, F. and Aguilera, A. (2006) Double-strand breaks arising by replication through a nick are repaired by cohesin-dependent sister-chromatid exchange. EMBO Rep. 7, 919-926.
145. Strom, L., Lindroos, H. B., Shirahige, K. and Sjogren, C. (2004) Postreplicative recruitment of cohesin to double-strand breaks is required for DNA repair. Mol. Cell 16, 1003-1015.
146. Unal, E., Arbel-Eden, A., Sattler, U., Shroff, R., Lichten, M., Haber, J. E. and Koshland, D. (2004) DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol. Cell 16, 991-1002.
147. Kim, J. S., Krasieva, T. B., LaMorte, V., Taylor, A. M. and Yokomori, K. (2002) Specific recruitment of human cohesin to laser-induced DNA damage. J. Biol. Chem. 277, 45149-45153.
148. Adachi, N., So, S. and Koyama, H. (2004) Loss of nonhomologous end joining confers camptothecin resistance in DT40 cells. Implications for the repair of topoisomerase I-mediated DNA damage. J. Biol. Chem. 279, 37343-37348.
149. Tercero, J. A. and Diffley, J. F. (2001) Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 412, 553-557.
150. Lopes, M., Cotta-Ramusino, C., Pellicioli, A., Liberi, G., Plevani, P., Muzi-Falconi, M., Newlon, C. S. and Foiani, M. (2001) The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412, 557-561.
151. Sogo, J. M., Lopes, M. and Foiani, M. (2002) Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297, 599-602.
152. Hanada, K., Budzowska, M., Davies, S. L., van Drunen, E., Onizawa, H., Beverloo, H. B., Maas, A., Essers, J., Hickson, I. D. and Kanaar, R. (2007) The structure-specific endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nat. Struct. Mol. Biol. 14, 1096-1104.
153. Hochegger, H., Dejsuphong, D., Fukushima, T., Morrison, C., Sonoda, E., Schreiber, V., Zhao, G. Y., Saberi, A., Masutani, M., Adachi, N. et al. (2006) Parp-1 protects homologous recombination from interference by Ku and Ligase IV in vertebrate cells. EMBO J. 25, 1305-1314.
154. Saberi, A., Hochegger, H., Szuts, D., Lan, L., Yasui, A., Sale, J. E., Taniguchi, Y., Murakawa, Y., Zeng, W., Yokomori, K. et al. (2007) RAD18 and poly(ADP-ribose) polymerase independently suppress the access of nonhomologous end joining to double-strand breaks and facilitate homologous recombination-mediated repair. Mol. Cell. Biol. 27, 2562-2571.
155. Mirzoeva, O. K. and Petrini, J. H. (2003) DNA replication-dependent nuclear dynamics of the Mre11 complex. Mol. Cancer. Res. 1, 207-218.
156. Esashi, F., Christ, N., Gannon, J., Liu, Y., Hunt, T., Jasin, M. and West, S. C. (2005) CDK-dependent phosphorylation of BRCA2 as a regulatory mechanism for recombinational repair. Nature 434, 598-604.
157. Limbo, O., Chahwan, C., Yamada, Y., de Bruin, R. A., Wittenberg, C. and Russell, P. (2007) Ctp1 is a cell-cycle-regulated protein that functions with Mre11 complex to control double-strand break repair by homologous recombination. Mol. Cell 28, 134-146.
158. Yu, X. and Baer, R. (2000) Nuclear localization and cell cycle-specific expression of CtIP, a protein that associates with the BRCA1 tumor suppressor. J. Biol. Chem. 275, 18541-9.
159. Li, S., Ting, N. S., Zheng, L., Chen, P. L., Ziv, Y., Shiloh, Y., Lee, E. Y. and Lee, W. H. (2000) Functional link of BRCA1 and ataxia telangiectasia gene product in DNA damage response. Nature 406, 210-215.
160. Wong, A. K., Ormonde, P. A., Pero, R., Chen, Y., Lian, L., Salada, G., Berry, S., Lawrence, Q., Dayananth, P., Ha, P. et al. (1998) Characterization of a carboxy-terminal BRCA1 interacting protein. Oncogene 17, 2279-2285.
161. Chen, L., Nievera, C., Lee, A. Y. and Wu, X. (2008) Cell cycle-dependent complex formation of BRCA1/CtIP/MRN is important for DNA double-strand break repair. J. Biol. Chem. 283, 7713-7720.
162. Orr-Weaver, T. L., Szostak, J. W. and Rothstein, R. J. (1981) Yeast transformation: a model system for the study of recombination. Proc. Natl. Acad. Sci. USA 78, 6354-6358.
163. Ip, S.C., Rass, U., Blanco, M.G., Flynn, H.R., Skehel, J.M. and West, S.C. (2008). Identification of Holliday junction resolvases from humans and yeast. Nature 456, 357-61.
164. Mimitou, E.P. and Symington, L.S. (2008). Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455, 770-4.
165. Zhu, Z., Chung, W.H., Shim, E.Y., Lee, S.E. and Ira, G. (2008). Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134, 981-94.
166. Gravel, S., Chapman, J.R., Magill, C. and Jackson, S.P. (2008). DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev. 22, 2767-72.
167. Huertas, P., Cortes-Ledesma, F., Sartori, A.A., Aguilera, A. and Jackson, S.P. (2008). CDK targets Sae2 to control DNA-end resection and homologous recombination. Nature 455, 689-92.