Replication fork reversal in eukaryotes: From dead end to dynamic response

Nature Reviews Molecular Cell Biology

Volumn 16, Issue 4, 2015, Pages 207-220

  Neelsen, Kai J ^a,b   Lopes, Massimo ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b University of Copenhagen   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

DNA TOPOISOMERASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE INHIBITOR; RECQ HELICASE; CHROMATIN;

CELL SURVIVAL; CHROMOSOME BREAKAGE; CHROMOSOME REARRANGEMENT; DNA CROSS LINKING; DNA DAMAGE; DNA DAMAGE CHECKPOINT; DNA REPLICATION; DNA STRUCTURE; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; EUKARYOTE; EUKARYOTIC CELL; GEL ELECTROPHORESIS; GENETIC CONSERVATION; GENOME; HOMOLOGOUS RECOMBINATION; HUMAN; IN VIVO STUDY; NONHUMAN; PHASE 3 CLINICAL TRIAL (TOPIC); PRIORITY JOURNAL; PROKARYOTE; PROTEIN DEPLETION; REPLICATION FORK REVERSAL; REPLISOME; REVIEW; TRINUCLEOTIDE REPEAT; ANIMAL; CHROMATIN; PHYSIOLOGY;

EUKARYOTA; METAZOA; PROKARYOTA;

ANIMALS; CHROMATIN; DNA DAMAGE; DNA REPLICATION; HUMANS;

EID: 84926226900     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm3935     Document Type: Review

References (142)

1. Higgins, N. P., Kato, K. & Strauss, B. A model for replication repair in mammalian cells. J. Mol. Biol. 101, 417-425 (1976).
2. Tatsumi, K. & Strauss, B. Production of DNA bifilarly substituted with bromodeoxyuridine in the first round of synthesis: branch migration during isolation of cellular DNA. Nucleic Acids Res. 5, 331-347 (1978).
3. Manosas, M., Perumal, S. K., Croquette, V. & Benkovic, S. J. Direct observation of stalled fork restart via fork regression in the T4 replication system. Science 338, 1217-1220 (2012).
4. De Septenville, A. L., Duigou, S., Boubakri, H. & Michel, B. Replication fork reversal after replication-transcription collision. PLoS Genet. 8, e1002622 (2012).
5. Nelson, S. W. & Benkovic, S. J. Response of the bacteriophage T4 replisome to noncoding lesions and regression of a stalled replication fork. J. Mol. Biol. 401, 743-756 (2010).
6. Atkinson, J. & McGlynn, P. Replication fork reversal and the maintenance of genome stability. Nucleic Acids Res. 37, 3475-3492 (2009).
7. Branzei, D. & Foiani, M. Maintaining genome stability at the replication fork. Nature Rev. Mol. Cell. Biol. 11, 208-219 (2010).
8. Saugar, I., Ortiz-Bazán, M. Á. & Tercero, J. A. Tolerating DNA damage during eukaryotic chromosome replication. Exp. Cell Res. 329, 170-177 (2014).
9. Lopes, M. et al. The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412, 557-561 (2001).
10. Sogo, J. M., Lopes, M. & Foiani, M. Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297, 599-602 (2002).
11. Bermejo, R., Lai, M. S. & Foiani, M. Preventing replication stress to maintain genome stability: resolving conflicts between replication and transcription. Mol. Cell 45, 710-718 (2012).
12. Bermejo, R. et al. The replication checkpoint protects fork stability by releasing transcribed genes from nuclear pores. Cell 146, 233-246 (2011).
13. 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 19, 445-456 (2008).
14. Lambert, S. et al. Homologous recombination restarts blocked replication forks at the expense of genome rearrangements by template exchange. Mol. Cell 39, 346-359 (2010).
15. Lopes, M., Foiani, M. & Sogo, J. M. Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions. Mol. Cell 21, 15-27 (2006).
16. Mojas, N., Lopes, M. & Jiricny, J. Mismatch repair-dependent processing of methylation damage gives rise to persistent single-stranded gaps in newly replicated DNA. Genes Dev. 21, 3342-3355 (2007).
17. Ray Chaudhuri, A. et al. Topoisomerase I poisoning results in PARP-mediated replication fork reversal. Nature Struct. Mol. Biol. 19, 417-423 (2012).
18. Redon, C. et al. Yeast histone 2A serine 129 is essential for the efficient repair of checkpoint-blind DNA damage. EMBO Rep. 4, 678-684 (2003).
19. Hu, J. et al. The intra-S phase checkpoint targets Dna2 to prevent stalled replication forks from reversing. Cell 149, 1221-1232 (2012).
20. Postow, L. et al. Positive torsional strain causes the formation of a four-way junction at replication forks. J. Biol. Chem. 276, 2790-2796 (2001).
21. Olavarrieta, L. et al. Supercoiling, knotting and replication fork reversal in partially replicated plasmids. Nucleic Acids Res. 30, 656-666 (2002).
22. Long, D. T. & Kreuzer, K. N. Regression supports two mechanisms of fork processing in phage T4. Proc. Natl Acad. Sci. USA 105, 6852-6857 (2008).
23. Fierro-Fernández, M., Hernández, P., Krimer, D. B. & Schvartzman, J. B. Replication fork reversal occurs spontaneously after digestion but is constrained in supercoiled domains. J. Biol. Chem. 282, 18190-18196 (2007).
24. Giannattasio, M. et al. Visualization of recombination-mediated damage bypass by template switching. Nature Struct. Mol. Biol. 21, 884-892 (2014).
25. Fumasoni, M., Zwicky, K., Vanoli, F., Lopes, M. & Branzei, D. Error-free DNA damage tolerance and sister chromatid proximity during DNA replication rely on the Pola/primase/Ctf4 complex. Mol. Cell http:// dx.doi.org/10.1016/j.molcel.2014.12.038 (2015).
26. Pommier, Y. Topoisomerase I inhibitors: camptothecins and beyond. Nature Rev. Cancer 6, 789-802 (2006).
27. Ge, X. Q. & Blow, J. J. Chk1 inhibits replication factory activation but allows dormant origin firing in existing factories. J. Cell Biol. 191, 1285-1297 (2010).
28. O'Connell, B. C. et al. A genome-wide camptothecin sensitivity screen identifies a mammalian MMS22L- NFKBIL2 complex required for genomic stability. Mol. Cell 40, 645-657 (2010).
29. Berti, M. et al. Human RECQ1 promotes restart of replication forks reversed by DNA topoisomerase I inhibition. Nature Struct. Mol. Biol. 20, 347-354 (2013).
30. Zellweger, R. et al. Rad51-mediated replication fork reversal is a general response to genotoxic treatments in human cells. J. Cell Biol. http://dx.doi.org/10.1083/ jcb.201406099 (2015).
31. Ray Chaudhuri, A., Ahuja, A. K., Herrador, R. & Lopes, M. Poly(ADP-ribosyl)gycohydrolase (PARG) prevents the accumulation of unusual replication structures during unperturbed S phase. Mol Cell. Biol. 35, 856-865 (2015).
32. Neelsen, K. J., Zanini, I. M. Y., Herrador, R. & Lopes, M. Oncogenes induce genotoxic stress by mitotic processing of unusual replication intermediates. J. Cell Biol. 200, 699-708 (2013).
33. Follonier, C., Oehler, J., Herrador, R. & Lopes, M. Friedreich's ataxia-associated GAA repeats induce replication-fork reversal and unusual molecular junctions. Nature Struct. Mol. Biol. 20, 486-494 (2013).
34. Neelsen, K. J. et al. Deregulated origin licensing leads to chromosomal breaks by rereplication of a gapped DNA template. Genes Dev. 27, 2537-2542 (2013).
35. Räschle, M. et al. Mechanism of replication-coupled DNA interstrand crosslink repair. Cell 134, 969-980 (2008).
36. Huang, J. et al. The DNA translocase FANCM/MHF promotes replication traverse of DNA interstrand crosslinks. Mol. Cell 52, 434-446 (2013).
37. McMurray, C. T. Mechanisms of trinucleotide repeat instability during human development. Nature Rev. Genet. 11, 786-799 (2010).
38. Mirkin, S. M. Expandable DNA repeats and human disease. Nature 447, 932-940 (2007).
39. Couch, F. B. et al. ATR phosphorylates SMARCAL1 to prevent replication fork collapse. Genes Dev. 27, 1610-1623 (2013).
40. León-Ortiz, A. M., Svendsen, J. & Boulton, S. J. Metabolism of DNA secondary structures at the eukaryotic replication fork. DNA Repair 19, 152-162 (2014).
41. Bester, A. C. et al. Nucleotide deficiency promotes genomic instability in early stages of cancer development. Cell 145, 435-446 (2011).
42. Jones, R. M. et al. Increased replication initiation and conflicts with transcription underlie cyclin E-induced replication stress. Oncogene 32, 3744-3753 (2013).
43. Fugger, K. et al. FBH1 catalyzes regression of stalled replication forks. Cell Rep. http://dx.doi.org/10.1016/j. celrep.2015.02.028 (2015).
44. Lorenz, A., Osman, F., Folkyte, V., Sofueva, S. & Whitby, M. C. Fbh1 limits Rad51-dependent recombination at blocked replication forks. Mol. Cell. Biol. 29, 4742-4756 (2009).
45. Chiolo, I. et al. The human F-Box DNA helicase FBH1 faces Saccharomyces cerevisiae Srs2 and postreplication repair pathway roles. Mol. Cell. Biol. 27, 7439-7450 (2007).
46. Fugger, K. et al. FBH1 co-operates with MUS81 in inducing DNA double-strand breaks and cell death following replication stress. Nature Commun. 4, 1423 (2013).
47. Fugger, K. et al. Human Fbh1 helicase contributes to genome maintenance via pro- and anti-recombinase activities. J. Cell Biol. 186, 655-663 (2009).
48. Masuda-Ozawa, T., Hoang, T., Seo, Y.-S., Chen, L.-F. & Spies, M. Single-molecule sorting reveals how ubiquitylation affects substrate recognition and activities of FBH1 helicase. Nucleic Acids Res. 41, 3576-3587 (2013).
49. Adelman, C. A. et al. HELQ promotes RAD51 paralogue-dependent repair to avert germ cell loss and tumorigenesis. Nature 502, 381-384 (2013).
50. Hashimoto, Y., Ray Chaudhuri, A., Lopes, M. & Costanzo, V. Rad51 protects nascent DNA from Mre11-dependent degradation and promotes continuous DNA synthesis. Nature Struct. Mol. Biol. 17, 1305-1311 (2010).
51. Schlacher, K. et al. Double-strand break repair-independent role for BRCA2 in blocking stalled replication fork degradation by MRE11. Cell 145, 529-542 (2011).
52. Schlacher, K., Wu, H. & Jasin, M. A distinct replication fork protection pathway connects Fanconi anemia tumor suppressors to RAD51-BRCA1/2. Cancer Cell 22, 106-116 (2012).
53. 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 37, 492-502 (2010).
54. 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. 329, 1240-1245 (2005).
55. 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. 28, 1724-1738 (2008).
56. Kim, H. & D'Andrea, A. D. Regulation of DNA cross-link repair by the Fanconi anemia/BRCA pathway. Genes Dev. 26, 1393-1408 (2012).
57. Popuri, V. et al. The human RecQ helicases, BLM and RECQ1, display distinct DNA substrate specificities. J. Biol. Chem. 283, 17766-17776 (2008).
58. LeRoy, G., Carroll, R., Kyin, S., Seki, M. & Cole, M. D. Identification of RecQL1 as a Holliday junction processing enzyme in human cell lines. Nucleic Acids Res. 33, 6251-6257 (2005).
59. Sharma, S. et al. Biochemical analysis of the DNA unwinding and strand annealing activities catalyzed by human RECQ1. J. Biol. Chem. 280, 28072-28084 (2005).
60. Cotta-Ramusino, C. et al. Exo1 processes stalled replication forks and counteracts fork reversal in checkpoint-defective cells. Mol. Cell 17, 153-159 (2005).
61. Thangavel, S. et al. DNA2 drives processing and restart of reversed replication forks in human cells. J. Cell Biol. http://dx.doi.org/10.1083/jcb.201406100 (2015).
62. Carr, A. M. & Lambert, S. Replication stress-induced genome instability: the dark side of replication maintenance by homologous recombination. J. Mol. Biol. 425, 4733-4744 (2013).
63. Hanada, K. et al. The structure-specific endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nature Struct. Mol. Biol. 14, 1096-1104 (2007).
64. Murfuni, I. et al. The WRN and MUS81 proteins limit cell death and genome instability following oncogene activation. Oncogene 32, 610-620 (2012).
65. Matos, J., Blanco, M. G., Maslen, S., Skehel, J. M. & West, S. C. Regulatory control of the resolution of DNA recombination intermediates during meiosis and mitosis. Cell 147, 158-172 (2011).
66. Matos, J., Blanco, M. G. & West, S. C. Cell-cycle kinases coordinate the resolution of recombination intermediates with chromosome segregation. Cell Rep. 4, 76-86 (2013).
67. Naim, V., Wilhelm, T., Debatisse, M. & Rosselli, F. ERCC1 and MUS81-EME1 promote sister chromatid separation by processing late replication intermediates at common fragile sites during mitosis. Nature Cell Biol. 15, 1-8 (2013).
68. Dehé, P.-M. et al. Regulation of Mus81-Eme1 Holliday junction resolvase in response to DNA damage. Nature Struct. Mol. Biol. 20, 598-603 (2013).
69. Pepe, A. & West, S. C. MUS81-EME2 promotes replication fork restart. Cell Rep. 7, 1048-1055 (2014).
70. Boddy, M. N. et al. Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107, 537-548 (2001).
71. Chen, X. B. et al. Human Mus81-associated endonuclease cleaves Holliday junctions in vitro. Mol. Cell 8, 1117-1127 (2001).
72. Whitby, M. C., Osman, F. & Dixon, J. Cleavage of model replication forks by fission yeast Mus81-Eme1 and budding yeast Mus81-Mms4. J. Biol. Chem. 278, 6928-6935 (2002).
73. Constantinou, A., Chen, X.-B., McGowan, C. H. & West, S. C. Holliday junction resolution in human cells: two junction endonucleases with distinct substrate specificities. EMBO J. 21, 5577-5585 (2002).
74. Pepe, A. & West, S. C. Substrate specificity of the MUS81-EME2 structure selective endonuclease. Nucleic Acids Res. 42, 3833-3845 (2013).
75. Amangyeld, T., Shin, Y.-K., Lee, M., Kwon, B. & Seo, Y.-S. Human MUS81-EME2 can cleave a variety of DNA structures including intact Holliday junction and nicked duplex. Nucleic Acids Res. 42, 5846-5862 (2014).
76. Rass, U. Resolving branched DNA intermediates with structure-specific nucleases during replication in eukaryotes. Chromosoma 122, 499-515 (2013).
77. Fekairi, S. et al. Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/ recombination endonucleases. Cell 138, 78-89 (2009).
78. Svendsen, J. M. et al. Mammalian BTBD12/SLX4 assembles a Holliday junction resolvase and is required for DNA repair. Cell 138, 63-77 (2009).
79. Larsen, N. B. & Hickson, I. D. RecQ helicases: conserved guardians of genomic integrity. Adv. Exp. Med. Biol. 767, 161-184 (2013).
80. Croteau, D. L., Popuri, V., Opresko, P. L. & Bohr, V. A. Human RecQ helicases in DNA repair, recombination, and replication. Annu. Rev. Biochem. 83, 519-552 (2014).
81. Ammazzalorso, F., Pirzio, L. M., Bignami, M., Franchitto, A. & Pichierri, P. ATR and ATM differently regulate WRN to prevent DSBs at stalled replication forks and promote replication fork recovery. EMBO J. 29, 3156-3169 (2010).
82. Rodríguez-López, A. M., Jackson, D. A., Iborra, F. & Cox, L. S. Asymmetry of DNA replication fork progression in Werner's syndrome. Aging Cell 1, 30-39 (2002).
83. Kanagaraj, R., Saydam, N., Garcia, P. L., Zheng, L. & Janscak, P. Human RECQ5 helicase promotes strand exchange on synthetic DNA structures resembling a stalled replication fork. Nucleic Acids Res. 34, 5217-5231 (2006).
84. Machwe, A., Xiao, L., Groden, J. & Orren, D. K. The Werner and Bloom syndrome proteins catalyze regression of a model replication fork. Biochemistry 45, 13939-13946 (2006).
85. Ralf, C., Hickson, I. D. & Wu, L. The Bloom's syndrome helicase can promote the regression of a model replication fork. J. Biol. Chem. 281, 22839-22846 (2006).
86. Machwe, A., Karale, R., Xu, X., Liu, Y. & Orren, D. K. The Werner and Bloom syndrome proteins help resolve replication blockage by converting (regressed) holliday junctions to functional replication forks. Biochemistry 50, 6774-6788 (2011).
87. Machwe, A., Lozada, E., Wold, M. S., Li, G.-M. & Orren, D. K. Molecular cooperation between the Werner syndrome protein and replication protein A in relation to replication fork blockage. J. Biol. Chem. 286, 3497-3508 (2011).
88. Davies, S. L., North, P. S., Dart, A., Lakin, N. D. & Hickson, I. D. Phosphorylation of the Bloom's syndrome helicase and its role in recovery from S-phase arrest. Mol. Cell. Biol. 24, 1279-1291 (2004).
89. Davies, S. L., North, P. S. & Hickson, I. D. Role for BLM in replication-fork restart and suppression of origin firing after replicative stress. Nature Struct. Mol. Biol. 14, 677-679 (2007).
90. Machwe, A., Xiao, L., Lloyd, R. G., Bolt, E. & Orren, D. K. Replication fork regression in vitro by the Werner syndrome protein (WRN): Holliday junction formation, the effect of leading arm structure and a potential role for WRN exonuclease activity. Nucleic Acids Res. 35, 5729-5747 (2007).
91. Flaus, A., Martin, D. M. A., Barton, G. J. & Owen-Hughes, T. Identification of multiple distinct Snf2 subfamilies with conserved structural motifs. Nucleic Acids Res. 34, 2887-2905 (2006).
92. Blastyák, A. et al. Yeast rad5 protein required for postreplication repair has a DNA helicase activity specific for replication fork regression. Mol. Cell 28, 167-175 (2007).
93. Unk, I. et al. Human HLTF functions as a ubiquitin ligase for proliferating cell nuclear antigen polyubiquitination. Proc. Natl Acad. Sci. USA 105, 3768-3773 (2008).
94. Bétous, R. et al. Substrate-selective repair and restart of replication forks by DNA translocases. Cell Rep. 3, 1958-1969 (2013).
95. Unk, I., Hajdu, I., Blastyák, A. & Haracska, L. Role of yeast Rad5 and its human orthologs, HLTF and SHPRH in DNA damage tolerance. DNA Repair 9, 257-267 (2010).
96. Blastyák, A., Hajdu, I., Unk, I. & Haracska, L. Role of double-stranded DNA translocase activity of human HLTF in replication of damaged DNA. Mol. Cell. Biol. 30, 684-693 (2010).
97. Burkovics, P., Sebesta, M., Balogh, D., Haracska, L. & Krejci, L. Strand invasion by HLTF as a mechanism for template switch in fork rescue. Nucleic Acids Res. 42, 1711-1720 (2013).
98. Achar, Y. J., Balogh, D. & Haracska, L. Coordinated protein and DNA remodeling by human HLTF on stalled replication fork. Proc. Natl Acad. Sci. USA 108, 14073-14078 (2011).
99. Motegi, A. et al. Polyubiquitination of proliferating cell nuclear antigen by HLTF and SHPRH prevents genomic instability from stalled replication forks. Proc. Natl Acad. Sci. USA 105, 12411-12416 (2008).
100. Petukhova, G., Stratton, S. & Sung, P. Catalysis of homologous DNA pairing by yeast Rad51 and Rad54 proteins. Nature 393, 91-94 (1998).
101. Bugreev, D. V., Mazina, O. M. & Mazin, A. V. Rad54 protein promotes branch migration of Holliday junctions. Nature 442, 590-593 (2006).
102. Bugreev, D. V., Rossi, M. J. & Mazin, A. V. Cooperation of RAD51 and RAD54 in regression of a model replication fork. Nucleic Acids Res. 39, 2153-2164 (2011).
103. Gonzalez-Prieto, R., Munoz-Cabello, A. M., Cabello-Lobato, M. J. & Prado, F. Rad51 replication fork recruitment is required for DNA damage tolerance. EMBO J. 32, 1307-1321 (2013).
104. Yusufzai, T. & Kadonaga, J. T. HARP is an ATP-driven annealing helicase. Science 322, 748-750 (2008).
105. Yusufzai, T. & Kadonaga, J. T. Annealing helicase 2 (AH2), a DNA-rewinding motor with an HNH motif. Proc. Natl Acad. Sci. USA 107, 20970-20973 (2010).
106. Betous, R. et al. SMARCAL1 catalyzes fork regression and Holliday junction migration to maintain genome stability during DNA replication. Genes Dev. 26, 151-162 (2012).
107. Yusufzai, T., Kong, X., Yokomori, K. & Kadonaga, J. T. The annealing helicase HARP is recruited to DNA repair sites via an interaction with RPA. Genes Dev. 23, 2400-2404 (2009).
108. Yuan, J., Ghosal, G. & Chen, J. The annealing helicase HARP protects stalled replication forks. Genes Dev. 23, 2394-2399 (2009).
109. Bansbach, C. E., Betous, R., Lovejoy, C. A., Glick, G. G. & Cortez, D. The annealing helicase SMARCAL1 maintains genome integrity at stalled replication forks. Genes Dev. 23, 2405-2414 (2009).
110. Ciccia, A. et al. The SIOD disorder protein SMARCAL1 is an RPA-interacting protein involved in replication fork restart. Genes Dev. 23, 2415-2425 (2009).
111. Postow, L., Woo, E. M., Chait, B. T. & Funabiki, H. Identification of SMARCAL1 as a component of the DNA damage response. J. Biol. Chem. 284, 35951-35961 (2009).
112. Carroll, C. et al. Phosphorylation of a C-terminal auto-inhibitory domain increases SMARCAL1 activity. Nucleic Acids Res. 42, 918-925 (2013).
113. Ciccia, A. et al. Polyubiquitinated PCNA recruits the ZRANB3 translocase to maintain genomic integrity after replication stress. Mol. Cell 47, 396-409 (2012).
114. Weston, R., Peeters, H. & Ahel, D. ZRANB3 is a structure-specific ATP-dependent endonuclease involved in replication stress response. Genes Dev. 26, 1558-1572 (2012).
115. Yuan, J., Ghosal, G. & Chen, J. The HARP-like domain-containing protein AH2/ZRANB3 binds to PCNA and participates in cellular response to replication stress. Mol. Cell 47, 410-421 (2012).
116. Whitby, M. C. The FANCM family of DNA helicases/ translocases. DNA Repair 9, 224-236 (2010).
117. Gari, K., D., Ecaillet, C., Stasiak, A. Z., Stasiak, A. & Constantinou, A. The Fanconi anemia protein FANCM can promote branch migration of Holliday junctions and replication forks. Mol. Cell 29, 141-148 (2008).
118. Gari, K., D., Ecaillet, C., Delannoy, M., Wu, L. & Constantinou, A. Remodeling of DNA replication structures by the branch point translocase FANCM. Proc. Natl Acad. Sci. USA 105, 16107-16112 (2008).
119. Xue, Y., Li, Y., Guo, R., Ling, C. & Wang, W. FANCM of the Fanconi anemia core complex is required for both monoubiquitination and DNA repair. Hum. Mol. Genet. 17, 1641-1652 (2008).
120. Fox, D. et al. The histone-fold complex MHF is remodeled by FANCM to recognize branched DNA and protect genome stability. Cell Res. 24, 560-575 (2014).
121. Zhao, Q. et al. The MHF complex senses branched DNA by binding a pair of crossover DNA duplexes. Nature Commun. 5, 2987 (2014).
122. Yan, Z. et al. A histone-fold complex and FANCM form a conserved DNA-remodeling complex to maintain genome stability. Mol. Cell 37, 865-878 (2010).
123. Luke-Glaser, S., Luke, B., Grossi, S. & Constantinou, A. FANCM regulates DNA chain elongation and is stabilized by S-phase checkpoint signalling. EMBO J. 29, 795-805 (2009).
124. Schwab, R. A., Blackford, A. N. & Niedzwiedz, W. ATR activation and replication fork restart are defective in FANCM-deficient cells. EMBO J. 29, 806-818 (2010).
125. Blackford, A. N. et al. The DNA translocase activity of FANCM protects stalled replication forks. Hum. Mol. Genet. 21, 2005-2016 (2012).
126. Collis, S. J. et al. FANCM and FAAP24 function in ATR-mediated checkpoint signaling independently of the Fanconi anemia core complex. Mol. Cell 32, 313-324 (2008).
127. Fachinetti, D. et al. Replication termination at eukaryotic chromosomes is mediated by Top2 and occurs at genomic loci containing pausing elements. Mol. Cell 39, 595-605 (2010).
128. Alver, R. C. & Bielinsky, A.-K. Termination at sTop2. Mol. Cell 39, 487-489 (2010).
129. Maric, M., Maculins, T., De Piccoli, G. & Labib, K. Cdc48 and a ubiquitin ligase drive disassembly of the CMG helicase at the end of DNA replication. Science 346, 1253596 (2014).
130. Moreno, S. P., Bailey, R., Campion, N., Herron, S. & Gambus, A. Polyubiquitylation drives replisome disassembly at the termination of DNA replication. Science 346, 477-481 (2014).
131. Wendel, B. M., Courcelle, C. T. & Courcelle, J. Completion of DNA replication in Escherichia coli. Proc. Natl Acad. Sci. USA 111, 16454-16459 (2014).
132. Bastia, D. & Mohanty, B. K. DNA Replication in Eukaryotic Cells 177-215 (Cold Spring Harbor Lab. Press, 1996).
133. Bussiere, D. E. & Bastia, D. Termination of DNA replication of bacterial and plasmid chromosomes. Mol. Microbiol. 31, 1611-1618 (1999).
134. Duggin, I. G., Wake, R. G., Bell, S. D. & Hill, T. M. The replication fork trap and termination of chromosome replication. Mol. Microbiol. 70, 1323-1333 (2008).
135. Longhese, M. P., Anbalagan, S., Martina, M. & Bonetti, D. The role of shelterin in maintaining telomere integrity. Front. Biosci. 17, 1715-1728 (2012).
136. Rouleau, M., Patel, A., Hendzel, M. J., Kaufmann, S. H. & Poirier, G. G. PARP inhibition: PARP1 and beyond. Nature Rev. Cancer 10, 293-301 (2010).
137. Postow, L., Crisona, N. J., Peter, B. J., Hardy, C. D. & Cozzarelli, N. R. Topological challenges to DNA replication: conformations at the fork. Proc. Natl Acad. Sci. USA 98, 8219-8226 (2001).
138. Arias, E. E. & Walter, J. C. Strength in numbers: preventing rereplication via multiple mechanisms in eukaryotic cells. Genes Dev. 21, 497-518 (2007).
139. Alabert, C. & Groth, A. Chromatin replication and epigenome maintenance. Nature Rev. Mol. Cell. Biol. 13, 153-167 (2012).
140. Schvartzman, J. B., Martínez-Robles, M.-L., López, V., Hernández, P. & Krimer, D. B. 2D gels and their third-dimension potential. Methods 57, 170-178 (2012).
141. Neelsen, K. J., Ray Chaudhuri, A., Follonier, C., Herrador, R. & Lopes, M. Visualization and interpretation of eukaryotic DNA replication intermediates in vivo by electron microscopy. Methods Mol. Biol. 1094, 177-208 (2014).
142. Deans, A. J. & West, S. C. DNA interstrand crosslink repair and cancer. Nature Rev. Cancer 11, 467-480 (2011).