Homologous recombination as a replication fork escort: Fork-protection and recovery

Biomolecules

Volumn 3, Issue 1, 2013, Pages 39-71

  Costes, Audrey ^a   Lambert, Sarah A E ^a  

^a CNRS   (France)

Author keywords

DNA repair; DNA replication; Fork stabilization; Fork repair; Fork restart; Homologous recombination

Indexed keywords

BRCA2 PROTEIN; DNA POLYMERASE; RAD51 PROTEIN; RECF PROTEIN; RECJ PROTEIN; RECN PROTEIN; RECO PROTEIN; RECOMBINASE; RECQ HELICASE; RECR PROTEIN; SINGLE STRANDED DNA;

DNA REPAIR; DNA REPLICATION; DNA SYNTHESIS; EUKARYOTE; GENETIC ANALYSIS; GENETIC VARIABILITY; HOMOLOGOUS RECOMBINATION; HUMAN; IMMUNOFLUORESCENCE; MINICHROMOSOME; NONHUMAN; PROTEIN PROTEIN INTERACTION; RECA GENE; RECOMBINATION REPAIR; REVIEW; SISTER CHROMATID; TWO DIMENSIONAL GEL ELECTROPHORESIS;

EID: 85016350382     PISSN: None     EISSN: 2218273X     Source Type: Journal    
DOI: 10.3390/biom3010039     Document Type: Review

References (189)

1. West, S.C. Molecular views of recombination proteins and their control. Natl. Rev. Mol. Cell Biol. 2003, 4, 435-445.
2. Cox, M.M. Regulation of bacterial reca protein function. Crit. Rev. Biochem. Mol. Biol. 2007, 42, 41-63.
3. Krejci, L.; Altmannova, V.; Spirek, M.; Zhao, X. Homologous recombination and its regulation. Nucleic Acids Res. 2012, 40, 5795-5818.
4. Deakyne, J.S.; Mazin, A.V. Fanconi anemia: At the crossroads of DNA repair. Biochem. Biokhimiia 2011, 76, 36-48.
5. Michel, B.; Boubakri, H.; Baharoglu, Z.; LeMasson, M.; Lestini, R. Recombination proteins and rescue of arrested replication forks. DNA Repair 2007, 6, 967-980.
6. Costanzo, V. Brca2, rad51 and mre11: Performing balancing acts on replication forks. DNA Repair 2011, 10, 1060-1065.
7. Courcelle, J.; Hanawalt, P.C. Reca-dependent recovery of arrested DNA replication forks. Annu. Rev. Genet. 2003, 37, 611-646.
8. Cox, M.M.; Goodman, M.F.; Kreuzer, K.N.; Sherratt, D.J.; Sandler, S.J.; Marians, K.J. The importance of repairing stalled replication forks. Nature 2000, 404, 37-41.
9. Heller, R.C.; Marians, K.J. Replication fork reactivation downstream of a blocked nascent leading strand. Nature 2006, 439, 557-562.
10. Heller, R.C.; Marians, K.J. Replisome assembly and the direct restart of stalled replication forks. Nat. Rev. Mol. Cell Biol. 2006, 7, 932-943.
11. Gabbai, C.B.; Marians, K.J. Recruitment to stalled replication forks of the pria DNA helicase and replisome-loading activities is essential for survival. DNA Repair 2010, 9, 202-209.
12. Heller, R.C.; Marians, K.J. The disposition of nascent strands at stalled replication forks dictates the pathway of replisome loading during restart. Mol. Cell 2005, 17, 733-743.
13. Kowalczykowski, S.C. Initiation of genetic recombination and recombination-dependent replication. Trends Biochem. Sci. 2000, 25, 156-165.
14. Lusetti, S.L.; Cox, M.M. The bacterial reca protein and the recombinational DNA repair of stalled replication forks. Annu. Rev. Biochem. 2002, 71, 71-100.
15. Kuzminov, A. DNA replication meets genetic exchange: Chromosomal damage and its repair by homologous recombination. Proc. Natl. Acad. Sci. USA 2001, 98, 8461-8468.
16. Liu, J.; Marians, K.J. Pria-directed assembly of a primosome on d loop DNA. J. Biol. Chem. 1999, 274, 25033-25041.
17. Ng, J.Y.; Marians, K.J. The ordered assembly of the phix174-type primosome. Ii. Preservation of primosome composition from assembly through replication. J. Biol. Chem. 1996, 271, 15649-15655.
18. Liu, J.; Nurse, P.; Marians, K.J. The ordered assembly of the phix174-type primosome. III Prib facilitates complex formation between pria and dnat.J. Biol. Chem. 1996, 271, 15656-15661.
19. Xu, L.; Marians, K.J. Pria mediates DNA replication pathway choice at recombination intermediates. Mol. Cell 2003, 11, 817-826.
20. Nurse, P.; Liu, J.; Marians, K.J. Two modes of pria binding to DNA. J. Biol. Chem. 1999, 274, 25026-25032.
21. McGlynn, P.; Al-Deib, A.A.; Liu, J.; Marians, K.J.; Lloyd, R.G. The DNA replication protein pria and the recombination protein recg bind d-loops. J. Mol. Biol. 1997, 270, 212-221.
22. Kowalczykowski, S.C.; Krupp, R.A. Effects of escherichia coli ssb protein on the single-stranded DNA-dependent atpase activity of escherichia coli reca protein. Evidence that ssb protein facilitates the binding of reca protein to regions of secondary structure within single-stranded DNA. J. Mol. Biol. 1987, 193, 97-113.
23. Roy, R.; Kozlov, A.G.; Lohman, T.M.; Ha, T. Ssb protein diffusion on single-stranded DNA stimulates reca filament formation. Nature 2009, 461, 1092-1097.
24. Umezu, K.; Kolodner, R.D. Protein interactions in genetic recombination in escherichia coli. Interactions involving reco and recr overcome the inhibition of reca by single-stranded DNA-binding protein. J. Biol. Chem. 1994, 269, 30005-30013.
25. Umezu, K.; Chi, N.W.; Kolodner, R.D. Biochemical interaction of the escherichia coli recf, reco, and recr proteins with reca protein and single-stranded DNA binding protein. Proc. Natl. Acad. Sci. USA 1993, 90, 3875-3879.
26. Beernink, H.T.; Morrical, S.W. Rmps: Recombination/replication mediator proteins. Trends Biochem. Sci. 1999, 24, 385-389.
27. Kuzminov, A.; Stahl, F.W. Double-strand end repair via the recbc pathway in escherichia coli primes DNA replication. Genes Dev. 1999, 13, 345-356.
28. Dillingham, M.S.; Kowalczykowski, S.C. Recbcd enzyme and the repair of double-stranded DNA breaks. Microbiol. Mol. Biol. Rev. 2008, 72, 642-671.
29. Yeeles, J.T.; Dillingham, M.S. The processing of double-stranded DNA breaks for recombinational repair by helicase-nuclease complexes. DNA Repair 2010, 9, 276-285.
30. Sakai, A.; Cox, M.M. Recfor and recor as distinct reca loading pathways. J. Biol. Chem. 2009, 284, 3264-3272.
31. Lovett, S.T.; Kolodner, R.D. Identification and purification of a single-stranded-DNA-specific exonuclease encoded by the recj gene of escherichia coli. Proc. Natl. Acad. Sci. USA 1989, 86, 2627-2631.
32. Umezu, K.; Nakayama, K.; Nakayama, H. Escherichia coli recq protein is a DNA helicase. Proc. Natl. Acad. Sci. USA 1990, 87, 5363-5367.
33. Tseng, Y.C.; Hung, J.L.; Wang, T.C. Involvement of recf pathway recombination genes in postreplication repair in uv-irradiated escherichia coli cells. Mut. Res.1994, 315, 1-9.
34. Courcelle, J.; Hanawalt, P.C. Recq and recj process blocked replication forks prior to the resumption of replication in uv-irradiated escherichia coli. Mol. Gen. Genet. 1999, 262, 543-551.
35. Webb, B.L.; Cox, M.M.; Inman, R.B. Recombinational DNA repair: The recf and recr proteins limit the extension of reca filaments beyond single-strand DNA gaps. Cell 1997, 91, 347-356.
36. Anderson, D.G.; Kowalczykowski, S.C. The translocating recbcd enzyme stimulates recombination by directing reca protein onto ssdna in a chi-regulated manner. Cell 1997, 90, 77-86.
37. Baharoglu, Z.; Petranovic, M.; Flores, M.J.; Michel, B. Ruvab is essential for replication forks reversal in certain replication mutants. EMBO J. 2006, 25, 596-604.
38. Flores, M.J.; Bierne, H.; Ehrlich, S.D.; Michel, B. Impairment of lagging strand synthesis triggers the formation of a ruvabc substrate at replication forks. EMBO J. 2001, 20, 619-629.
39. Michel, B.; Ehrlich, S.D.; Uzest, M. DNA double-strand breaks caused by replication arrest. EMBO J. 1997, 16, 430-438.
40. Grompone, G.; Seigneur, M.; Ehrlich, S.D.; Michel, B. Replication fork reversal in DNA polymerase III mutants of escherichia coli: A role for the beta clamp. Mol. Microbiol. 2002, 44, 1331-1339.
41. Pennington, J.M.; Rosenberg, S.M. Spontaneous DNA breakage in single living escherichia coli cells. Nat. Genet. 2007, 39, 797-802.
42. Seigneur, M.; Bidnenko, V.; Ehrlich, S.D.; Michel, B. Ruvab acts at arrested replication forks. Cell 1998, 95, 419-430.
43. Grompone, G.; Ehrlich, D.; Michel, B. Cells defective for replication restart undergo replication fork reversal. EMBO Rep. 2004, 5, 607-612.
44. De Septenville, A.L.; Duigou, S.; Boubakri, H.; Michel, B. Replication fork reversal after replication-transcription collision. PLoS Genet. 2012, 8, doi:10.1371/journal.pgen.1002622.
45. Seigneur, M.; Ehrlich, S.D.; Michel, B. Ruvabc-dependent double-strand breaks in dnabts mutants require reca. Mol. Microbiol. 2000, 38, 565-574.
46. McGlynn, P.; Lloyd, R.G. Genome stability and the processing of damaged replication forks by recg. Trends Genet. 2002, 18, 413-419.
47. McGlynn, P.; Lloyd, R.G.; Marians, K.J. Formation of holliday junctions by regression of nascent DNA in intermediates containing stalled replication forks: Recg stimulates regression even when the DNA is negatively supercoiled. Proc. Natl. Acad. Sci. USA 2001, 98, 8235-8240.
48. Robu, M.E.; Inman, R.B.; Cox, M.M. Reca protein promotes the regression of stalled replication forks in vitro. Proc. Natl. Acad. Sci. USA 2001, 98, 8211-8218.
49. Flores, M.J.; Bidnenko, V.; Michel, B. The DNA repair helicase uvrd is essential for replication fork reversal in replication mutants. EMBO Rep. 2004, 5, 983-988.
50. Flores, M.J.; Sanchez, N.; Michel, B. A fork-clearing role for uvrd. Mol. Microbiol. 2005, 57, 1664-1675.
51. Setlow, R.B. Cyclobutane-type pyrimidine dimers in polynucleotides. Science 1966, 153, 379-386.
52. Koehler, D.R.; Courcelle, J.; Hanawalt, P.C. Kinetics of pyrimidine(6-4)pyrimidone photoproduct repair in escherichia coli. J. Bacteriol. 1996, 178, 1347-1350.
53. Howard-Flanders, P.; Boyce, R.P.; Theriot, L. Three loci in escherichia coli k-12 that control the excision of pyrimidine dimers and certain other mutagen products from DNA. Genetics 1966, 53, 1119-1136.
54. Howard-Flanders, P.; Theriot, L. Mutants of escherichia coli k-12 defective in DNA repair and in genetic recombination. Genetics 1966, 53, 1137-1150.
55. Smith, D.W.; Hanawalt, P.C. Repair replication of DNA in ultraviolet irradiated mycoplasma laidlawii b. J. Mol. Biol. 1969, 46, 57-72.
56. Villani, G.; Spadari, S.; Boiteux, S.; Defais, M.; Caillet-Fauquet, P.; Radman, M. Replication of chemically modified DNA. Biochimie 1978, 60, 1145-1150.
57. Truglio, J.J.; Karakas, E.; Rhau, B.; Wang, H.; DellaVecchia, M.J.; Van Houten, B.; Kisker, C. Structural basis for DNA recognition and processing by uvrb. Nat. Struct. Mol. Biol. 2006, 13, 360-364.
58. Wang, T.C.; Smith, K.C. Mechanisms for recf-dependent and recb-dependent pathways of postreplication repair in uv-irradiated escherichia coli uvrb. J. Bacteriol. 1983, 156, 1093-1098.
59. Donaldson, J.R.; Courcelle, C.T.; Courcelle, J. Ruvabc is required to resolve holliday junctions that accumulate following replication on damaged templates in escherichia coli. J. Biol. Chem. 2006, 281, 28811-28821.
60. Rupp, W.D.; Wilde, C.E., III.; Reno, D.L.; Howard-Flanders, P. Exchanges between DNA strands in ultraviolet-irradiated escherichia coli. J. Mol. Biol. 1971, 61, 25-44.
61. Howard-Flanders, P.; Rupp, W.D. Recombinational repair in uv-irradiated escherichia coli. Johns Hopkins Med. J. 1972, 1, 212-225.
62. Pages, V.; Fuchs, R.P. Uncoupling of leading-and lagging-strand DNA replication during lesion bypass in vivo. Science 2003, 300, 1300-1303.
63. Higuchi, K.; Katayama, T.; Iwai, S.; Hidaka, M.; Horiuchi, T.; Maki, H. Fate of DNA replication fork encountering a single DNA lesion during oric plasmid DNA replication in vitro. Genes to Cells: Devoted to Molecular and Cellular Mechanisms 2003, 8, 437-449.
64. Yeeles, J.T.; Marians, K.J. The Escherichia coli replisome is inherently DNA damage tolerant. Science 2011, 334, 235-238.
65. Khidhir, M.A.; Casaregola, S.; Holland, I.B. Mechanism of transient inhibition of DNA synthesis in ultraviolet-irradiated E. coli: Inhibition is independent of reca whilst recovery requires reca protein itself and an additional, inducible sos function. Mol. Gen. Genet. 1985, 199, 133-140.
66. Courcelle, C.T.; Belle, J.J.; Courcelle, J. Nucleotide excision repair or polymerase v-mediated lesion bypass can act to restore uv-arrested replication forks in escherichia coli. J. Bacteriol. 2005, 187, 6953-6961.
67. Rudolph, C.J.; Upton, A.L.; Lloyd, R.G. Replication fork stalling and cell cycle arrest in uv-irradiated escherichia coli. Genes Dev. 2007, 21, 668-681.
68. Rudolph, C.J.; Upton, A.L.; Lloyd, R.G. Maintaining replication fork integrity in uv-irradiated escherichia coli cells. DNA Repair 2008, 7, 1589-1602.
69. Courcelle, J.; Carswell-Crumpton, C.; Hanawalt, P.C. Recf and recr are required for the resumption of replication at DNA replication forks in escherichia coli. Proc. Natl. Acad. Sci. USA 1997, 94, 3714-3719.
70. Courcelle, J.; Crowley, D.J.; Hanawalt, P.C. Recovery of DNA replication in uv-irradiated escherichia coli requires both excision repair and recf protein function. J. Bacteriol. 1999, 181, 916-922.
71. Chow, K.H.; Courcelle, J. Reco acts with recf and recr to protect and maintain replication forks blocked by uv-induced DNA damage in escherichia coli. J. Biol. Chem. 2004, 279, 3492-3496.
72. Courcelle, C.T.; Landstrom, A.J.; Anderson, B.; Courcelle, J. Cellular characterization of the primosome and rep helicase in processing and restoration of replication following arrest by uv-induced DNA damage in escherichia coli. J. Bacteriol. 2012, 194, 3977-3986.
73. Hishida, T.; Han, Y.W.; Shibata, T.; Kubota, Y.; Ishino, Y.; Iwasaki, H.; Shinagawa, H. Role of the escherichia coli recq DNA helicase in sos signaling and genome stabilization at stalled replication forks. Genes Dev. 2004, 18, 1886-1897.
74. McInerney, P.; O'Donnell, M. Replisome fate upon encountering a leading strand block and clearance from DNA by recombination proteins. J. Biol. Chem. 2007, 282, 25903-25916.
75. Courcelle, J.; Hanawalt, P.C. Participation of recombination proteins in rescue of arrested replication forks in uv-irradiated escherichia coli need not involve recombination. Proc. Natl. Acad. Sci. USA 2001, 98, 8196-8202.
76. Courcelle, J.; Ganesan, A.K.; Hanawalt, P.C. Therefore, what are recombination proteins there for? BioEssays 2001, 23, 463-470.
77. Al-Hadid, Q.; Ona, K.; Courcelle, C.T.; Courcelle, J. Reca433 cells are defective in recf-mediated processing of disrupted replication forks but retain recbcd-mediated functions. Mut. Res. 2008, 645, 19-26.
78. Renzette, N.; Gumlaw, N.; Nordman, J.T.; Krieger, M.; Yeh, S.P.; Long, E.; Centore, R.; Boonsombat, R.; Sandler, S.J. Localization of reca in escherichia coli k-12 using reca-gfp. Mol. Microbiol. 2005, 57, 1074-1085.
79. Simmons, L.A.; Grossman, A.D.; Walker, G.C. Replication is required for the reca localization response to DNA damage in bacillus subtilis. Proc. Natl. Acad. Sci. USA 2007, 104, 1360-1365.
80. Lecointe, F.; Serena, C.; Velten, M.; Costes, A.; McGovern, S.; Meile, J.C.; Errington, J.; Ehrlich, S.D.; Noirot, P.; Polard, P. Anticipating chromosomal replication fork arrest: Ssb targets repair DNA helicases to active forks. EMBO J. 2007, 26, 4239-4251.
81. Costes, A.; Lecointe, F.; McGovern, S.; Quevillon-Cheruel, S.; Polard, P. The c-terminal domain of the bacterial ssb protein acts as a DNA maintenance hub at active chromosome replication forks. PLoS Genet.2010, 6, doi:10.1371/journal.pgen.1001238.
82. Mechali, M. Eukaryotic DNA replication origins: Many choices for appropriate answers. Nat. Rev. Mol. Cell Biol. 2010, 11, 728-738.
83. Cayrou, C.; Coulombe, P.; Mechali, M. Programming DNA replication origins and chromosome organization. Chrom. Res. 2010, 18, 137-145.
84. Kelly, T.J.; Brown, G.W. Regulation of chromosome replication. Annu. Rev. Biochem. 2000, 69, 829-880.
85. Lambert, S.; Froget, B.; Carr, A.M. Arrested replication fork processing: Interplay between checkpoints and recombination. DNA Repair 2007, 6, 1042-1061.
86. Mirkin, E.V.; Mirkin, S.M. Replication fork stalling at natural impediments. Microbiol. Mol. Biol. Rev. 2007, 71, 13-35.
87. Szilard, R.; Jacques, P.; Laramée, L.; Cheng, B.; Galicia, S.; Bataille, A.; Yeung, M.; Mendez, M.; Bergeron, M.; Robert, F.; et al. Systematic identification of fragile sites via genome-wide location analysis of gamma-h2ax. Nat. Struct. Mol. Biol. 2010, 17, 299-305.
88. Helleday, T. Homologous recombination in cancer development, treatment and development of drug resistance. Carcinogenesis 2010, 31, 955-960.
89. Kawabata, T.; Luebben, S.W.; Yamaguchi, S.; Ilves, I.; Matise, I.; Buske, T.; Botchan, M.R.; Shima, N. Stalled fork rescue via dormant replication origins in unchallenged s phase promotes proper chromosome segregation and tumor suppression. Mol. Cell 2011, 41, 543-553.
90. Woodward, A.M.; Gohler, T.; Luciani, M.G.; Oehlmann, M.; Ge, X.; Gartner, A.; Jackson, D.A.; Blow, J.J. Excess mcm2-7 license dormant origins of replication that can be used under conditions of replicative stress. J. Cell Biol. 2006, 173, 673-683.
91. Ge, X.Q.; Jackson, D.A.; Blow, J.J. Dormant origins licensed by excess mcm2-7 are required for human cells to survive replicative stress. Genes Dev. 2007, 21, 3331-3341.
92. Le Tallec, B.; Dutrillaux, B.; Lachages, A.M.; Millot, G.A.; Brison, O.; Debatisse, M. Molecular profiling of common fragile sites in human fibroblasts. Nat. Struc. Mol. Biol. 2011, 18, 1421-1423.
93. Letessier, A.; Millot, G.A.; Koundrioukoff, S.; Lachages, A.M.; Vogt, N.; Hansen, R.S.; Malfoy, B.; Brison, O.; Debatisse, M. Cell-type-specific replication initiation programs set fragility of the fra3b fragile site. Nature 2011, 470, 120-123.
94. Daboussi, F.; Courbet, S.; Benhamou, S.; Kannouche, P.; Zdzienicka, M.Z.; Debatisse, M.; Lopez, B.S. A homologous recombination defect affects replication-fork progression in mammalian cells. J. Cell Sci. 2008, 121, 162-166.
95. Branzei, D.; Foiani, M. Maintaining genome stability at the replication fork. Nat. Rev. Mol. Cell Biol. 2010, 11, 208-219.
96. Katou, Y.; Kanoh, Y.; Bando, M.; Noguchi, H.; Tanaka, H.; Ashikari, T.; Sugimoto, K.; Shirahige, K. S-phase checkpoint proteins tof1 and mrc1 form a stable replication-pausing complex. Nature 2003, 424, 1078-1083.
97. De Piccoli, G.; Katou, Y.; Itoh, T.; Nakato, R.; Shirahige, K.; Labib, K. Replisome stability at defective DNA replication forks is independent of s phase checkpoint kinases. Mol. Cell 2012, 45, 696-704.
98. Cotta-Ramusino, C.; Fachinetti, D.; Lucca, C.; Doksani, Y.; Lopes, M.; Sogo, J.; Foiani, M. Exo1 processes stalled replication forks and counteracts fork reversal in checkpoint-defective cells. Mol. Cell 2005, 17, 153-159.
99. Froget, B.; Blaisonneau, J.; Lambert, S.; Baldacci, G. Cleavage of stalled forks by fission yeast mus81/eme1 in absence of DNA replication checkpoint. Mol. Biol. Cell 2008, 19, 445-456.
100. Kai, M.; Boddy, M.N.; Russell, P.; Wang, T.S. Replication checkpoint kinase cds1 regulates mus81 to preserve genome integrity during replication stress. Genes Dev. 2005, 19, 919-932.
101. Hu, J.; Sun, L.; Shen, F.; Chen, Y.; Hua, Y.; Liu, Y.; Zhang, M.; Hu, Y.; Wang, Q.; Xu, W.; et al. The intra-s phase checkpoint targets dna2 to prevent stalled replication forks from reversing. Cell 2012, 149, 1221-1232.
102. Nimonkar, A.V.; Sica, R.A.; Kowalczykowski, S.C. Rad52 promotes second-end DNA capture in double-stranded break repair to form complement-stabilized joint molecules. Proc. Natl. Acad. Sci. USA 2009, 106, 3077-3082.
103. McIlwraith, M.J.; West, S.C. DNA repair synthesis facilitates rad52-mediated second-end capture during dsb repair. Mol. Cell 2008, 29, 510-516.
104. Carreira, A.; Hilario, J.; Amitani, I.; Baskin, R.J.; Shivji, M.K.; Venkitaraman, A.R.; Kowalczykowski, S.C. The brc repeats of brca2 modulate the DNA-binding selectivity of rad51. Cell 2009, 136, 1032-1043.
105. Jensen, R.B.; Carreira, A.; Kowalczykowski, S.C. Purified human brca2 stimulates rad51-mediated recombination. Nature 2010, 467, 678-683.
106. Wray, J.; Liu, J.; Nickoloff, J.A.; Shen, Z. Distinct rad51 associations with rad52 and bccip in response to DNA damage and replication stress. Cancer Res. 2008, 68, 2699-2707.
107. Lisby, M.; Barlow, J.H.; Burgess, R.C.; Rothstein, R. Choreography of the DNA damage response: Spatiotemporal relationships among checkpoint and repair proteins. Cell 2004, 118, 699-713.
108. Sung, P. Yeast rad55 and rad57 proteins form a heterodimer that functions with replication protein a to promote DNA strand exchange by rad51 recombinase. Genes Dev. 1997, 11, 1111-1121.
109. Ward, J.D.; Barber, L.J.; Petalcorin, M.I.; Yanowitz, J.; Boulton, S.J. Replication blocking lesions present a unique substrate for homologous recombination. EMBO J. 2007, 26, 3384-3396.
110. Mankouri, H.W.; Ngo, H.P.; Hickson, I.D. Shu proteins promote the formation of homologous recombination intermediates that are processed by sgs1-rmi1-top3. Mol. Biol Cell 2007, 18, 4062-4073.
111. Shor, E.; Weinstein, J.; Rothstein, R. A genetic screen for top3 suppressors in saccharomyces cerevisiae identifies shu1, shu2, psy3 and csm2: Four genes involved in error-free DNA repair. Genetics 2005, 169, 1275-1289.
112. Ball, L.G.; Zhang, K.; Cobb, J.A.; Boone, C.; Xiao, W. The yeast shu complex couples error-free post-replication repair to homologous recombination. Mol. Microbiol. 2009, 73, 89-102.
113. Choi, K.; Szakal, B.; Chen, Y.H.; Branzei, D.; Zhao, X. The smc5/6 complex and esc2 influence multiple replication-associated recombination processes in saccharomyces cerevisiae. Mol. Biol Cell 2010, 21, 2306-2314.
114. Martin, V.; Chahwan, C.; Gao, H.; Blais, V.; Wohlschlegel, J.; Yates, J.R. III.; McGowan, C.H.; Russell, P. Sws1 is a conserved regulator of homologous recombination in eukaryotic cells. EMBO J. 2006, 25, 2564-2574.
115. Liu, J.; Renault, L.; Veaute, X.; Fabre, F.; Stahlberg, H.; Heyer, W.D. Rad51 paralogues rad55-rad57 balance the antirecombinase srs2 in rad51 filament formation. Nature 2011, 479, 245-248.
116. Papouli, E.; Chen, S.; Davies, A.A.; Huttner, D.; Krejci, L.; Sung, P.; Ulrich, H.D. Crosstalk between sumo and ubiquitin on pcna is mediated by recruitment of the helicase srs2p. Mol. Cell 2005, 19, 123-133.
117. Pfander, B.; Moldovan, G.L.; Sacher, M.; Hoege, C.; Jentsch, S. Sumo-modified pcna recruits srs2 to prevent recombination during s phase. Nature 2005, 436, 428-433.
118. Bashkirov, V.I.; King, J.S.; Bashkirova, E.V.; Schmuckli-Maurer, J.; Heyer, W.D. DNA repair protein rad55 is a terminal substrate of the DNA damage checkpoints. Mol. Cell. Biol. 2000, 20, 4393-4404.
119. Herzberg, K.; Bashkirov, V.I.; Rolfsmeier, M.; Haghnazari, E.; McDonald, W.H.; Anderson, S.; Bashkirova, E.V.; Yates, J.R., III.; Heyer, W.D. 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. 2006, 26, 8396-8409.
120. Haaf, T.; Golub, E.I.; Reddy, G.; Radding, C.M.; Ward, D.C. Nuclear foci of mammalian rad51 recombination protein in somatic cells after DNA damage and its localization in synaptonemal complexes. Proc. Natl. Acad. Sci. USA 1995, 92, 2298-2302.
121. Tashiro, S.; Kotomura, N.; Shinohara, A.; Tanaka, K.; Ueda, K.; Kamada, N. S phase specific formation of the human rad51 protein nuclear foci in lymphocytes. Oncogene 1996, 12, 2165-2170.
122. Golub, E.I.; Gupta, R.C.; Haaf, T.; Wold, M.S.; Radding, C.M. Interaction of human rad51 recombination protein with single-stranded DNA binding protein, rpa. Nucleic Acids Res. 1998, 26, 5388-5393.
123. Raderschall, E.; Golub, E.I.; Haaf, T. Nuclear foci of mammalian recombination proteins are located at single-stranded DNA regions formed after DNA damage. Proc. Natl. Acad. Sci. USA 1999, 96, 1921-1926.
124. Mizuta, R.; LaSalle, J.M.; Cheng, H.L.; Shinohara, A.; Ogawa, H.; Copeland, N.; Jenkins, N.A.; Lalande, M.; Alt, F.W. Rab22 and rab163/mouse brca2: Proteins that specifically interact with the rad51 protein. Proc. Natl. Acad. Sci. USA 1997, 94, 6927-6932.
125. Tashiro, S.; Walter, J.; Shinohara, A.; Kamada, N.; Cremer, T. Rad51 accumulation at sites of DNA damage and in postreplicative chromatin. J. Cell Biol. 2000, 150, 283-291.
126. Chen, J.; Silver, D.P.; Walpita, D.; Cantor, S.B.; Gazdar, A.F.; Tomlinson, G.; Couch, F.J.; Weber, B.L.; Ashley, T.; Livingston, D.M.; et al. Stable interaction between the products of the brca1 and brca2 tumor suppressor genes in mitotic and meiotic cells. Mol. Cell 1998, 2, 317-328.
127. Scully, R.; Chen, J.; Plug, A.; Xiao, Y.; Weaver, D.; Feunteun, J.; Ashley, T.; Livingston, D.M. Association of brca1 with rad51 in mitotic and meiotic cells. Cell 1997, 88, 265-275.
128. Scully, R.; Chen, J.; Ochs, R.L.; Keegan, K.; Hoekstra, M.; Feunteun, J.; Livingston, D.M. Dynamic changes of brca1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell 1997, 90, 425-435.
129. Meister, P.; Poidevin, M.; Francesconi, S.; Tratner, I.; Zarzov, P.; Baldacci, G. Nuclear factories for signalling and repairing DNA double strand breaks in living fission yeast. Nucleic Acids Res. 2003, 31, 5064-5073.
130. Lisby, M.; Rothstein, R.; Mortensen, U.H. Rad52 forms DNA repair and recombination centers during s phase. Proc. Natl. Acad. Sci. USA 2001, 98, 8276-8282.
131. Lambert, S.; Mizuno, K.; Blaisonneau, J.; Martineau, S.; Chanet, R.; Fréon, K.; Murray, J.M.; Carr, A.M.; Baldacci, G. Homologous recombination restarts blocked replication forks at the expense of genome rearrangements by template exchange. Mol. Cell 2010, 39, 346-359.
132. Lambert, S.; Watson, A.; Sheedy, D.M.; Martin, B.; Carr, A.M. Gross chromosomal rearrangements and elevated recombination at an inducible site-specific replication fork barrier. Cell 2005, 121, 689-702.
133. Mizuno, K.; Lambert, S.; Baldacci, G.; Murray, J.M.; Carr, A.M. Nearby inverted repeats fuse to generate acentric and dicentric palindromic chromosomes by a replication template exchange mechanism. Genes Dev. 2009, 23, 2876-2886.
134. Zou, H.; Rothstein, R. Holliday junctions accumulate in replication mutants via a reca homolog-independent mechanism. Cell 1997, 90, 87-96.
135. Tsang, E.; Carr, A. Replication fork arrest, recombination and the maintenance of ribosomal DNA stability. DNA Repair 2008, 7, 1613-1623.
136. Karanam, K.; Kafri, R.; Loewer, A.; Lahav, G. Quantitative live cell imaging reveals a gradual shift between DNA repair mechanisms and a maximal use of hr in mid s phase. Mol. Cell 2012, 47, 320-329.
137. Wong, J.M.; Ionescu, D.; Ingles, C.J. Interaction between brca2 and replication protein a is compromised by a cancer-predisposing mutation in brca2. Oncogene 2003, 22, 28-33.
138. Shukla, A.; Navadgi, V.M.; Mallikarjuna, K.; Rao, B.J. Interaction of hrad51 and hrad52 with mcm complex: A cross-talk between recombination and replication proteins. Biochem. Biophys. Res. Commun. 2005, 329, 1240-1245.
139. Bailis, J.M.; Luche, D.D.; Hunter, T.; Forsburg, S.L. Minichromosome maintenance proteins interact with checkpoint and recombination proteins to promote s-phase genome stability. Mol. Cell. Biol. 2008, 28, 1724-1738.
140. Oyola, S.O.; Bringaud, F.; Melville, S.E. A kinetoplastid brca2 interacts with DNA replication protein cdc45. Int. J. Parasitol. 2009, 39, 59-69.
141. Alabert, C.; Bianco, J.; Pasero, P. Differential regulation of homologous recombination at DNA breaks and replication forks by the mrc1 branch of the s-phase checkpoint. EMBO J. 2009, 28, 1131-1141.
142. Lopes, M.; Foiani, M.; Sogo, J.M. Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable uv lesions. Mol. Cell 2006, 21, 15-27.
143. Hashimoto, Y.; Ray Chaudhuri, A.; Lopes, M.; Costanzo, V. Rad51 protects nascent DNA from mre11-dependent degradation and promotes continuous DNA synthesis. Nat. Struc. Mol. Biol. 2010, 17, 1305-1311.
144. Liberi, G.; Maffioletti, G.; Lucca, C.; Chiolo, I.; Baryshnikova, A.; Cotta-Ramusino, C.; Lopes, M.; Pellicioli, A.; Haber, J.E.; Foiani, M. Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of blm recq helicase. Genes Dev. 2005, 19, 339-350.
145. Branzei, D.; Vanoli, F.; Foiani, M. Sumoylation regulates rad18-mediated template switch. Nature 2008, 456, 915-920.
146. Branzei, D.; Sollier, J.; Liberi, G.; Zhao, X.; Maeda, D.; Seki, M.; Enomoto, T.; Ohta, K.; Foiani, M. Ubc9-and mms21-mediated sumoylation counteracts recombinogenic events at damaged replication forks. Cell 2006, 127, 509-522.
147. Mankouri, H.W.; Ashton, T.M.; Hickson, I.D. Holliday junction-containing DNA structures persist in cells lacking sgs1 or top3 following exposure to DNA damage. Proc. Nat. Acad. Sci. USA 2011, 108, 4944-4949.
148. Branzei, D. Ubiquitin family modifications and template switching. FEBS Lett. 2011, 585, 2810-2817.
149. Vanoli, F.; Fumasoni, M.; Szakal, B.; Maloisel, L.; Branzei, D. Replication and recombination factors contributing to recombination-dependent bypass of DNA lesions by template switch. PLoS Genet. 2010, 6, doi:10.1371/journal.pgen.1001205.
150. Moriel-Carretero, M.; Aguilera, A. A postincision-deficient tfiih causes replication fork breakage and uncovers alternative rad51-or pol32-mediated restart mechanisms. Mol. Cell 2010, 37, 690-701.
151. Roseaulin, L.; Yamada, Y.; Tsutsui, Y.; Russell, P.; Iwasaki, H.; Arcangioli, B. Mus81 is essential for sister chromatid recombination at broken replication forks. EMBO J. 2008, 27, 1378-1387.
152. Hashimoto, Y.; Puddu, F.; Costanzo, V. Rad51-and mre11-dependent reassembly of uncoupled cmg helicase complex at collapsed replication forks. Nat. Struc. Mol. Biol. 2011, 19, 17-24.
153. Clemente-Ruiz, M.; Prado, F. Chromatin assembly controls replication fork stability. EMBO Rep. 2009, 10, 790-796.
154. Long, D.T.; Raschle, M.; Joukov, V.; Walter, J.C. Mechanism of rad51-dependent DNA interstrand cross-link repair. Science 2011, 333, 84-87.
155. Bjergbaek, L.; Cobb, J.A.; Tsai-Pflugfelder, M.; Gasser, S.M. Mechanistically distinct roles for sgs1p in checkpoint activation and replication fork maintenance. EMBO J. 2005, 24, 405-417.
156. Nakahara, M.; Sonoda, E.; Nojima, K.; Sale, J.E.; Takenaka, K.; Kikuchi, K.; Taniguchi, Y.; Nakamura, K.; Sumitomo, Y.; Bree, R.T.; et al. Genetic evidence for single-strand lesions initiating nbs1-dependent homologous recombination in diversification of ig v in chicken b lymphocytes. PLoS Genet. 2009, 5, doi:10.1371/journal.pgen.1000356.
157. Paek, A.L.; Kaochar, S.; Jones, H.; Elezaby, A.; Shanks, L.; Weinert, T. Fusion of nearby inverted repeats by a replication-based mechanism leads to formation of dicentric and acentric chromosomes that cause genome instability in budding yeast. Genes Dev. 2009, 23, 2861-2875.
158. Meister, P.; Taddei, A.; Vernis, L.; Poidevin, M.; Gasser, S.M.; Baldacci, G. Temporal separation of replication and recombination requires the intra-s checkpoint. J. Cell Biol. 2005, 168, 537-544.
159. Sorensen, C.S.; Hansen, L.T.; Dziegielewski, J.; Syljuasen, R.G.; Lundin, C.; Bartek, J.; Helleday, T. The cell-cycle checkpoint kinase chk1 is required for mammalian homologous recombination repair. Nat. Cell Biol. 2005, 7, 195-201.
160. Petermann, E.; Orta, M.L.; Issaeva, N.; Schultz, N.; Helleday, T. Hydroxyurea-stalled replication forks become progressively inactivated and require two different rad51-mediated pathways for restart and repair. Mol. Cell 2010, 37, 492-502.
161. Saintigny, Y.; Delacote, F.; Vares, G.; Petitot, F.; Lambert, S.; Averbeck, D.; Lopez, B.S. Characterization of homologous recombination induced by replication inhibition in mammalian cells. EMBO J. 2001, 20, 3861-3870.
162. Raveendranathan, M.; Chattopadhyay, S.; Bolon, Y.T.; Haworth, J.; Clarke, D.J.; Bielinsky, A.K. Genome-wide replication profiles of s-phase checkpoint mutants reveal fragile sites in yeast. EMBO J. 2006, 25, 3627-3639.
163. Hanada, K.; Budzowska, M.; Davies, S.L.; van Drunen, E.; Onizawa, H.; Beverloo, H.B.; Maas, A.; Essers, J.; Hickson, I.D.; Kanaar, R. The structure-specific endonuclease mus81 contributes to replication restart by generating double-strand DNA breaks. Nat. Struc. Mol. Biol. 2007, 14, 1096-1104.
164. Bosco, G.; Haber, J.E. Chromosome break-induced DNA replication leads to nonreciprocal translocations and telomere capture. Genetics 1998, 150, 1037-1047.
165. Llorente, B.; Smith, C.E.; Symington, L.S. Break-induced replication: What is it and what is it for? Cell Cycle 2008, 7, 859-864.
166. Kraus, E.; Leung, W.Y.; Haber, J.E. Break-induced replication: A review and an example in budding yeast. Proc. Natl. Acad. Sci. USA 2001, 98, 8255-8262.
167. Lydeard, J.R.; Jain, S.; Yamaguchi, M.; Haber, J.E. Break-induced replication and telomerase-independent telomere maintenance require pol32. Nature 2007, 448, 820-823.
168. Lydeard, J.R.; Lipkin-Moore, Z.; Sheu, Y.J.; Stillman, B.; Burgers, P.M.; Haber, J.E. Break-induced replication requires all essential DNA replication factors except those specific for pre-rc assembly. Genes Dev. 2010, 24, 1133-1144.
169. Deem, A.; Keszthelyi, A.; Blackgrove, T.; Vayl, A.; Coffey, B.; Mathur, R.; Chabes, A.; Malkova, A. Break-induced replication is highly inaccurate. PLoS Biol. 2011, 9, doi:10.1371/journal.pbio.1000594.
170. Iraqui, I.; Chekkal, Y.; Jmari, N.; Pietrobon, V.; Freon, K.; Costes, A.; Lambert, S.A. Recovery of arrested replication forks by homologous recombination is error-prone. PLoS Genet. 2012, 8, doi:10.1371/journal.pgen.1002976.
171. Mizuno, K.; Miyabe, I.; Schalbetter, S.A.; Carr, A.M.; Murray, J.M. Recombination-restarted replication makes inverted chromosome fusions at inverted repeats. Nature 2012, doi:10.1038/nature11676.
172. Stracker, T.H.; Petrini, J.H. The mre11 complex: Starting from the ends. Nat. Rev. Mol. Cell Biol. 2011, 12, 90-103.
173. Lomonosov, M.; Anand, S.; Sangrithi, M.; Davies, R.; Venkitaraman, A.R. Stabilization of stalled DNA replication forks by the brca2 breast cancer susceptibility protein. Genes Dev. 2003, 17, 3017-3022.
174. Schlacher, K.; Christ, N.; Siaud, N.; Egashira, A.; Wu, H.; Jasin, M. Double-strand break repair-independent role for brca2 in blocking stalled replication fork degradation by mre11. Cell 2011, 145, 529-542.
175. Schlacher, K.; Wu, H.; Jasin, M. A distinct replication fork protection pathway connects fanconi anemia tumor suppressors to rad51-brca1/2. Cancer Cell 2012, 22, 106-116.
176. Tinline-Purvis, H.; Savory, A.P.; Cullen, J.K.; Dave, A.; Moss, J.; Bridge, W.L.; Marguerat, S.; Bahler, J.; Ragoussis, J.; Mott, R.; et al. Failed gene conversion leads to extensive end processing and chromosomal rearrangements in fission yeast. EMBO J. 2009, 28, 3400-3412.
177. Sonoda, E.; Sasaki, M.S.; Buerstedde, J.M.; Bezzubova, O.; Shinohara, A.; Ogawa, H.; Takata, M.; Yamaguchi-Iwai, Y.; Takeda, S. Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J. 1998, 17, 598-608.
178. Venkitaraman, A.R. Chromosome stability, DNA recombination and the brca2 tumour suppressor. Curr. Opin. Cell Biol. 2001, 13, 338-343.
179. Fachinetti, D.; Bermejo, R.; Cocito, A.; Minardi, S.; Katou, Y.; Kanoh, Y.; Shirahige, K.; Azvolinsky, A.; Zakian, V.A.; Foiani, M. Replication termination at eukaryotic chromosomes is mediated by top2 and occurs at genomic loci containing pausing elements. Mol. Cell 2010, 39, 595-605.
180. Nitiss, J. DNA topoisomerase ii and its growing repertoire of biological functions. Natl. Rev. Cancer 2009, 9, 327-337.
181. Steinacher, R.; Osman, F.; Dalgaard, J.Z.; Lorenz, A.; Whitby, M.C. The DNA helicase pfh1 promotes fork merging at replication termination sites to ensure genome stability. Genes Dev. 2012, 26, 594-602.
182. Kojic, M.; Holloman, W.K. Brh2 domain function distinguished by differential cellular responses to DNA damage and replication stress. Mol. Microbiol. 2012, 83, 351-361.
183. Heyer, W.D.; Li, X.; Rolfsmeier, M.; Zhang, X.P. Rad54: The swiss army knife of homologous recombination? Nucleic Acids Res. 2006, 34, 4115-4125.
184. Lambert, S.; Lopez, B.S. Characterization of mammalian rad51 double strand break repair using non-lethal dominant-negative forms. EMBO J. 2000, 19, 3090-3099.
185. Liu, P.; Carvalho, C.M.; Hastings, P.; Lupski, J.R. Mechanisms for recurrent and complex human genomic rearrangements. Curr. Opin. Genet. Dev. 2012, 22, 211-220.
186. Halazonetis, T.D.; Gorgoulis, V.G.; Bartek, J. An oncogene-induced DNA damage model for cancer development. Science 2008, 319, 1352-1355.
187. Chabosseau, P.; Buhagiar-Labarchede, G.; Onclercq-Delic, R.; Lambert, S.; Debatisse, M.; Brison, O.; Amor-Gueret, M. Pyrimidine pool imbalance induced by blm helicase deficiency contributes to genetic instability in bloom syndrome. Nat. Commun. 2011, 2, 368.
188. Bester, A.C.; Roniger, M.; Oren, Y.S.; Im, M.M.; Sarni, D.; Chaoat, M.; Bensimon, A.; Zamir, G.; Shewach, D.S.; Kerem, B. Nucleotide deficiency promotes genomic instability in early stages of cancer development. Cell 2011, 145, 435-446.
189. Evers, B.; Helleday, T.; Jonkers, J. Targeting homologous recombination repair defects in cancer. Trends Pharmacol. Sci. 2010, 31, 372-380.