Replication fork reversal in eukaryotes: from dead end to dynamic response (original) (raw)

• Higgins, N. P., Kato, K. & Strauss, B. A model for replication repair in mammalian cells. J. Mol. Biol. 101, 417–425 (1976).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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). The direct visualization of fork reversal and restart in the bacteriophage T4 system illustrated the dynamics of strand exchange and protein turnover at the replication fork.
  Article CAS PubMed Google Scholar
• De Septenville, A. L., Duigou, S., Boubakri, H. & Michel, B. Replication fork reversal after replication-transcription collision. PLoS Genet. 8, e1002622 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Atkinson, J. & McGlynn, P. Replication fork reversal and the maintenance of genome stability. Nucleic Acids Res. 37, 3475–3492 (2009). This is an excellent overview of replication fork reversal in prokaryotic and eukaryotic cells.
  Article CAS PubMed PubMed Central Google Scholar
• Branzei, D. & Foiani, M. Maintaining genome stability at the replication fork. Nature Rev. Mol. Cell. Biol. 11, 208–219 (2010).
  Article CAS Google Scholar
• Saugar, I., Ortiz-Bazán, M. Á. & Tercero, J. A. Tolerating DNA damage during eukaryotic chromosome replication. Exp. Cell Res. 329, 170–177 (2014).
  Article CAS PubMed Google Scholar
• Lopes, M. et al. The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412, 557–561 (2001).
  Article CAS PubMed Google Scholar
• 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). This is the first visualization of reversed replication forks in S. cerevisiae , linking fork reversal with checkpoint defects.
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Bermejo, R. et al. The replication checkpoint protects fork stability by releasing transcribed genes from nuclear pores. Cell 146, 233–246 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Ray Chaudhuri, A. et al. Topoisomerase I poisoning results in PARP-mediated replication fork reversal. Nature Struct. Mol. Biol. 19, 417–423 (2012). This paper shows that topoisomerase inhibition promotes fork reversal in yeast and higher eukaryotes, and provides the first evidence for fork reversal in metazoans.
  Article CAS Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Hu, J. et al. The intra-S phase checkpoint targets Dna2 to prevent stalled replication forks from reversing. Cell 149, 1221–1232 (2012).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Olavarrieta, L. et al. Supercoiling, knotting and replication fork reversal in partially replicated plasmids. Nucleic Acids Res. 30, 656–666 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article PubMed PubMed Central Google Scholar
• 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).
  Article PubMed Google Scholar
• Giannattasio, M. et al. Visualization of recombination-mediated damage bypass by template switching. Nature Struct. Mol. Biol. 21, 884–892 (2014).
  Article CAS Google Scholar
• 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).
• Pommier, Y. Topoisomerase I inhibitors: camptothecins and beyond. Nature Rev. Cancer 6, 789–802 (2006).
  Article CAS Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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). This paper elucidates the mechanism by which RECQ1 and PARP1 cooperatively regulate fork restart.
  Article CAS Google Scholar
• 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). This paper shows that RAD51-dependent replication fork reversal is a global response to a wide variety of replication perturbations.
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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). This paper shows that oncogenes that deregulate DNA replication cause fork reversal, and that the cleavage of reversed forks contributes to oncogene-induced genome instability.
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Räschle, M. et al. Mechanism of replication-coupled DNA interstrand crosslink repair. Cell 134, 969–980 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Huang, J. et al. The DNA translocase FANCM/MHF promotes replication traverse of DNA interstrand crosslinks. Mol. Cell 52, 434–446 (2013). This paper shows that ICLs in chromosomal DNA do not block replication fork progression, but are frequently 'traversed' by the fork.
  Article CAS PubMed Google Scholar
• McMurray, C. T. Mechanisms of trinucleotide repeat instability during human development. Nature Rev. Genet. 11, 786–799 (2010).
  Article CAS PubMed Google Scholar
• Mirkin, S. M. Expandable DNA repeats and human disease. Nature 447, 932–940 (2007).
  Article CAS PubMed Google Scholar
• Couch, F. B. et al. ATR phosphorylates SMARCAL1 to prevent replication fork collapse. Genes Dev. 27, 1610–1623 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Bester, A. C. et al. Nucleotide deficiency promotes genomic instability in early stages of cancer development. Cell 145, 435–446 (2011).
  Article CAS PubMed PubMed Central Google Scholar
• Jones, R. M. et al. Increased replication initiation and conflicts with transcription underlie cyclin E-induced replication stress. Oncogene 32, 3744–3753 (2013).
  Article CAS PubMed Google Scholar
• 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).
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS Google Scholar
• Fugger, K. et al. Human Fbh1 helicase contributes to genome maintenance via pro- and anti-recombinase activities. J. Cell Biol. 186, 655–663 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Adelman, C. A. et al. HELQ promotes RAD51 paralogue-dependent repair to avert germ cell loss and tumorigenesis. Nature 502, 381–384 (2013).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Kim, H. & D'Andrea, A. D. Regulation of DNA cross-link repair by the Fanconi anemia/BRCA pathway. Genes Dev. 26, 1393–1408 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• Popuri, V. et al. The human RecQ helicases, BLM and RECQ1, display distinct DNA substrate specificities. J. Biol. Chem. 283, 17766–17776 (2008).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Cotta-Ramusino, C. et al. Exo1 processes stalled replication forks and counteracts fork reversal in checkpoint-defective cells. Mol. Cell 17, 153–159 (2005).
  Article CAS PubMed Google Scholar
• 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).
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS Google Scholar
• Murfuni, I. et al. The WRN and MUS81 proteins limit cell death and genome instability following oncogene activation. Oncogene 32, 610–620 (2012).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS Google Scholar
• 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).
  Article CAS Google Scholar
• Pepe, A. & West, S. C. MUS81-EME2 promotes replication fork restart. Cell Rep. 7, 1048–1055 (2014).
  Article CAS PubMed PubMed Central Google Scholar
• Boddy, M. N. et al. Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107, 537–548 (2001).
  Article CAS PubMed Google Scholar
• Chen, X. B. et al. Human Mus81-associated endonuclease cleaves Holliday junctions in vitro. Mol. Cell 8, 1117–1127 (2001).
  Article CAS PubMed Google Scholar
• 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).
  Article PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Pepe, A. & West, S. C. Substrate specificity of the MUS81-EME2 structure selective endonuclease. Nucleic Acids Res. 42, 3833–3845 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Rass, U. Resolving branched DNA intermediates with structure-specific nucleases during replication in eukaryotes. Chromosoma 122, 499–515 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Fekairi, S. et al. Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell 138, 78–89 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Svendsen, J. M. et al. Mammalian BTBD12/SLX4 assembles a Holliday junction resolvase and is required for DNA repair. Cell 138, 63–77 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Larsen, N. B. & Hickson, I. D. RecQ helicases: conserved guardians of genomic integrity. Adv. Exp. Med. Biol. 767, 161–184 (2013).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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). This study provides the first biochemical evidence that post-replication repair proteins catalyse fork reversal.
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article PubMed PubMed Central Google Scholar
• Bétous, R. et al. Substrate-selective repair and restart of replication forks by DNA translocases. Cell Rep. 3, 1958–1969 (2013). This study biochemically investigates the fork reversal activity of the annealing helicase SMARCAL1 and illustrates the importance of RPA.
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article PubMed PubMed Central Google Scholar
• 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).
  Article PubMed PubMed Central Google Scholar
• Petukhova, G., Stratton, S. & Sung, P. Catalysis of homologous DNA pairing by yeast Rad51 and Rad54 proteins. Nature 393, 91–94 (1998).
  Article CAS PubMed Google Scholar
• Bugreev, D. V., Mazina, O. M. & Mazin, A. V. Rad54 protein promotes branch migration of Holliday junctions. Nature 442, 590–593 (2006). This study describes RAD51 and RAD54 as the first eukaryotic proteins involved in branch migration.
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Yusufzai, T. & Kadonaga, J. T. HARP is an ATP-driven annealing helicase. Science 322, 748–750 (2008). This study characterizes SMARCAL1 — the first annealing helicase.
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Yuan, J., Ghosal, G. & Chen, J. The annealing helicase HARP protects stalled replication forks. Genes Dev. 23, 2394–2399 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Carroll, C. et al. Phosphorylation of a C-terminal auto-inhibitory domain increases SMARCAL1 activity. Nucleic Acids Res. 42, 918–925 (2013).
  Article CAS PubMed PubMed Central Google Scholar
• Ciccia, A. et al. Polyubiquitinated PCNA recruits the ZRANB3 translocase to maintain genomic integrity after replication stress. Mol. Cell 47, 396–409 (2012).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Whitby, M. C. The FANCM family of DNA helicases/translocases. DNA Repair 9, 224–236 (2010).
  Article CAS PubMed Google Scholar
• 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). This study describes fork reversal by FANCM — the first catalytic activity attributed to a Fanconi anaemia protein.
  Article CAS PubMed Google Scholar
• 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).
  Article PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Zhao, Q. et al. The MHF complex senses branched DNA by binding a pair of crossover DNA duplexes. Nature Commun. 5, 2987 (2014).
  Article CAS Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Blackford, A. N. et al. The DNA translocase activity of FANCM protects stalled replication forks. Hum. Mol. Genet. 21, 2005–2016 (2012).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Alver, R. C. & Bielinsky, A.-K. Termination at sTop2. Mol. Cell 39, 487–489 (2010).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Wendel, B. M., Courcelle, C. T. & Courcelle, J. Completion of DNA replication in Escherichia coli. Proc. Natl Acad. Sci. USA 111, 16454–16459 (2014). This study shows that replication termination in E. coli depends on DSB-processing factors and RecG, and involves over-replication of the termination sequence.
  Article CAS PubMed PubMed Central Google Scholar
• Bastia, D. & Mohanty, B. K. DNA Replication in Eukaryotic Cells 177–215 (Cold Spring Harbor Lab. Press, 1996).
  Google Scholar
• Bussiere, D. E. & Bastia, D. Termination of DNA replication of bacterial and plasmid chromosomes. Mol. Microbiol. 31, 1611–1618 (1999).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Longhese, M. P., Anbalagan, S., Martina, M. & Bonetti, D. The role of shelterin in maintaining telomere integrity. Front. Biosci. 17, 1715–1728 (2012).
  Article CAS Google Scholar
• 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).
  Article CAS Google Scholar
• 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).
  Article CAS PubMed PubMed Central Google Scholar
• Arias, E. E. & Walter, J. C. Strength in numbers: preventing rereplication via multiple mechanisms in eukaryotic cells. Genes Dev. 21, 497–518 (2007).
  Article CAS PubMed Google Scholar
• Alabert, C. & Groth, A. Chromatin replication and epigenome maintenance. Nature Rev. Mol. Cell. Biol. 13, 153–167 (2012).
  Article CAS Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• 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).
  Article CAS PubMed Google Scholar
• Deans, A. J. & West, S. C. DNA interstrand crosslink repair and cancer. Nature Rev. Cancer 11, 467–480 (2011).
  Article CAS Google Scholar