Maintaining genome stability at the replication fork
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Schwob, E. Flexibility and governance in eukaryotic DNA replication. Curr. Opin. Microbiol. 7, 680–690 (2004).
Kearsey, S. E. & Cotterill, S. Enigmatic variations: divergent modes of regulating eukaryotic DNA replication. Mol. Cell 12, 1067–1075 (2003).
Zegerman, P. & Diffley, J. F. DNA replication as a target of the DNA damage checkpoint. DNA Repair (Amst.) 8, 1077–1088 (2009).
Yabuki, N., Terashima, H. & Kitada, K. Mapping of early firing origins on a replication profile of budding yeast. Genes Cells 7, 781–789 (2002).
Wyrick, J. J. et al. Genome-wide distribution of ORC and MCM proteins in S. cerevisiae: high-resolution mapping of replication origins. Science 294, 2357–2360 (2001). References 5 and 6 map replication origins and identify their replication time.
Dershowitz, A. & Newlon, C. S. The effect on chromosome stability of deleting replication origins. Mol. Cell. Biol. 13, 391–398 (1993). Analyzes the consequences of ablating origins and suggests that origins are present in excess.
Woodward, A. M. et al. Excess Mcm2–7 license dormant origins of replication that can be used under conditions of replicative stress. J. Cell Biol. 173, 673–683 (2006).
Ibarra, A., Schwob, E. & Mendez, J. Excess MCM proteins protect human cells from replicative stress by licensing backup origins of replication. Proc. Natl Acad. Sci. USA 105, 8956–8961 (2008).
Okuno, Y., McNairn, A. J., den Elzen, N., Pines, J. & Gilbert, D. M. Stability, chromatin association and functional activity of mammalian pre-replication complex proteins during the cell cycle. EMBO J. 20, 4263–4277 (2001).
Laskey, R. A. & Harland, R. M. Replication origins in the eukaryotic chromosome. Cell 24, 283–284 (1981).
Ivessa, A. S. et al. The Saccharomyces cerevisiae helicase Rrm3p facilitates replication past nonhistone protein-DNA complexes. Mol. Cell 12, 1525–1536 (2003).
Cha, R. S. & Kleckner, N. ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science 297, 602–606 (2002). Shows the crucial role of the replication checkpoint in preventing breakage at replication slow zones.
Ivessa, A. S., Zhou, J. Q., Schulz, V. P., Monson, E. K. & Zakian, V. A. Saccharomyces Rrm3p, a 5′ to 3′ DNA helicase that promotes replication fork progression through telomeric and subtelomeric DNA. Genes Dev. 16, 1383–1396 (2002).
Ivessa, A. S., Zhou, J. Q. & Zakian, V. A. The Saccharomyces Pif1p DNA helicase and the highly related Rrm3p have opposite effects on replication fork progression in ribosomal DNA. Cell 100, 479–489 (2000).
Shore, D. & Bianchi, A. Telomere length regulation: coupling DNA end processing to feedback regulation of telomerase. EMBO J. 28, 2309–2322 (2009).
Dulev, S. et al. Essential global role of CDC14 in DNA synthesis revealed by chromosome underreplication unrecognized by checkpoints in cdc14 mutants. Proc. Natl Acad. Sci. USA 106, 14466–14471 (2009).
Aguilera, A. & Gomez-Gonzalez, B. Genome instability: a mechanistic view of its causes and consequences. Nature Rev. Genet. 9, 204–217 (2008).
Kolodner, R. D., Putnam, C. D. & Myung, K. Maintenance of genome stability in Saccharomyces cerevisiae. Science 297, 552–557 (2002).
Bochman, M. L. & Schwacha, A. The Mcm2–7 complex has in vitro helicase activity. Mol. Cell 31, 287–293 (2008).
Labib, K., Tercero, J. A. & Diffley, J. F. Uninterrupted MCM2–7 function required for DNA replication fork progression. Science 288, 1643–1647 (2000).
Dowell, S. J., Romanowski, P. & Diffley, J. F. Interaction of Dbf4, the Cdc7 protein kinase regulatory subunit, with yeast replication origins in vivo. Science 265, 1243–1246 (1994).
Bell, S. P. Eukaryotic replicators and associated protein complexes. Curr. Opin. Genet. Dev. 5, 162–167 (1995).
Aparicio, O. M., Weinstein, D. M. & Bell, S. P. Components and dynamics of DNA replication complexes in S. cerevisiae: redistribution of MCM proteins and Cdc45p during S phase. Cell 91, 59–69 (1997).
Toone, W. M., Aerne, B. L., Morgan, B. A. & Johnston, L. H. Getting started: regulating the initiation of DNA replication in yeast. Annu. Rev. Microbiol 51, 125–149 (1997).
Gambus, A. et al. GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks. Nature Cell Biol. 8, 358–366 (2006).
Katou, Y. et al. S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 424, 1078–1083 (2003).
Cobb, J. A., Bjergbaek, L., Shimada, K., Frei, C. & Gasser, S. M. DNA polymerase stabilization at stalled replication forks requires Mec1 and the RecQ helicase Sgs1. EMBO J. 22, 4325–4336 (2003).
Lucca, C. et al. Checkpoint-mediated control of replisome-fork association and signalling in response to replication pausing. Oncogene 23, 1206–1213 (2004).
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).
Wang, J. C. Cellular roles of DNA topoisomerases: a molecular perspective. Nature Rev. Mol. Cell. Biol. 3, 430–440 (2002).
Bermejo, R. et al. Top1- and Top2-mediated topological transitions at replication forks ensure fork progression and stability and prevent DNA damage checkpoint activation. Genes Dev. 21, 1921–1936 (2007).
Fields-Berry, S. C. & DePamphilis, M. L. Sequences that promote formation of catenated intertwines during termination of DNA replication. Nucleic Acids Res. 17, 3261–3273 (1989).
Mirkin, E. V. & Mirkin, S. M. Replication fork stalling at natural impediments. Microbiol Mol. Biol. Rev. 71, 13–35 (2007). A comprehensive review on the natural elements that lead to RF stalling.
Casper, A. M., Nghiem, P., Arlt, M. F. & Glover, T. W. ATR regulates fragile site stability. Cell 111, 779–789 (2002). Documents the role of the replication checkpoint in preventing the expression of fragile sites.
Deshpande, A. M. & Newlon, C. S. DNA replication fork pause sites dependent on transcription. Science 272, 1030–1033 (1996). Shows that tRNA transcription causes RF pausing.
Azvolinsky, A., Giresi, P. G., Lieb, J. D. & Zakian, V. A. Highly transcribed RNA polymerase II genes are impediments to replication fork progression in Saccharomyces cerevisiae. Mol. Cell 34, 722–734 (2009). Provides a genome-wide analysis of replication pausing elements.
Olavarrieta, L., Hernandez, P., Krimer, D. B. & Schvartzman, J. B. DNA knotting caused by head-on collision of transcription and replication. J. Mol. Biol. 322, 1–6 (2002). Documents the topological consequences of RFs clashing with transcription units.
Tuduri, S. et al. Topoisomerase I suppresses genomic instability by preventing interference between replication and transcription. Nature Cell Biol. 11, 1315–1324 (2009).
Bermejo, R. et al. Genome-organizing factors Top2 and Hmo1 prevent chromosome fragility at sites of S phase transcription. Cell 138, 870–884 (2009).
Mirkin, S. M. DNA structures, repeat expansions and human hereditary disorders. Curr. Opin. Struct. Biol. 16, 351–358 (2006).
Lόpez Castel, A., Cleary, J. D & Pearson, C. E. Repeat instability as the basis for human diseases and as a potential target for therapy. Nature Rev. Mol. Cell Biol. 11, 165–170 (2010).
Sutherland, G. R. Fragile sites on human chromosomes: demonstration of their dependence on the type of tissue culture medium. Science 197, 265–266 (1977).
Roeder, G. S. & Fink, G. R. DNA rearrangements associated with a transposable element in yeast. Cell 21, 239–249 (1980).
Argueso, J. L. et al. Double-strand breaks associated with repetitive DNA can reshape the genome. Proc. Natl Acad. Sci. USA 105, 11845–11850 (2008).
Lemoine, F. J., Degtyareva, N. P., Lobachev, K. & Petes, T. D. Chromosomal translocations in yeast induced by low levels of DNA polymerase a model for chromosome fragile sites. Cell 120, 587–598 (2005). Shows that limiting the amounts of DNA polymerases can lead to fragile site expression.
Admire, A. et al. Cycles of chromosome instability are associated with a fragile site and are increased by defects in DNA replication and checkpoint controls in yeast. Genes Dev. 20, 159–173 (2006).
Peter, B. J., Ullsperger, C., Hiasa, H., Marians, K. J. & Cozzarelli, N. R. The structure of supercoiled intermediates in DNA replication. Cell 94, 819–827 (1998).
Trinh, T. Q. & Sinden, R. R. Preferential DNA secondary structure mutagenesis in the lagging strand of replication in E. coli. Nature 352, 544–547 (1991).
Rosche, W. A., Trinh, T. Q. & Sinden, R. R. Differential DNA secondary structure-mediated deletion mutation in the leading and lagging strands. J. Bacteriol. 177, 4385–4391 (1995).
Hansen, R. S., Canfield, T. K., Lamb, M. M., Gartler, S. M. & Laird, C. D. Association of fragile X syndrome with delayed replication of the FMR1 gene. Cell 73, 1403–1409 (1993).
Lu, J., Kobayashi, R. & Brill, S. J. Characterization of a high mobility group 1/2 homolog in yeast. J. Biol. Chem. 271, 33678–33685 (1996).
Kim, H. & Livingston, D. M. Suppression of a DNA polymerase δ mutation by the absence of the high mobility group protein Hmo1 in Saccharomyces cerevisiae. Curr. Genet. 55, 127–138 (2009).
Prado, F. & Aguilera, A. Impairment of replication fork progression mediates RNA polII transcription-associated recombination. EMBO J. 24, 1267–1276 (2005).
Pomerantz, R. T. & O'Donnell, M. The replisome uses mRNA as a primer after colliding with RNA polymerase. Nature 456, 762–766 (2008). In vitro study proposing that mRNAs can be used as primers by the leading-strand polymerase.
Dalgaard, J. Z. & Klar, A. J. A DNA replication-arrest site RTS1 regulates imprinting by determining the direction of replication at mat1 in S. pombe. Genes Dev. 15, 2060–2068 (2001).
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 121, 689–702 (2005). Describes the consequences of RF collapse in the triggering of recombination and genome instability.
Inagawa, T. et al. Schizosaccharomyces pombe Rtf2 mediates site-specific replication termination by inhibiting replication restart. Proc. Natl Acad. Sci. USA 106, 7927–7932 (2009).
Doe, C. L. & Whitby, M. C. The involvement of Srs2 in post-replication repair and homologous recombination in fission yeast. Nucleic Acids Res. 32, 1480–1491 (2004).
Fabre, F., Chan, A., Heyer, W. D. & Gangloff, S. Alternate pathways involving Sgs1/Top3, Mus81/Mms4, and Srs2 prevent formation of toxic recombination intermediates from single-stranded gaps created by DNA replication. Proc. Natl Acad. Sci. USA 99, 16887–16892 (2002).
Pfander, B., Moldovan, G. L., Sacher, M., Hoege, C. & Jentsch, S. SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature 436, 428–433 (2005).
Papouli, E. et al. Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. Mol. Cell 19, 123–133 (2005).
Branzei, D., Vanoli, F. & Foiani, M. SUMOylation regulates Rad18-mediated template switch. Nature 456, 915–920 (2008). Provides physical evidence for a role of the Rad18 pathway in promoting recombination structures that involve sister chromatids during replication of damaged templates.
Branzei, D. et al. Ubc9- and Mms21-mediated sumoylation counteracts recombinogenic events at damaged replication forks. Cell 127, 509–522 (2006). Documents the role of sumoylation in the resolution of recombination intermediates formed during the replication of damaged templates.
Zhao, X. & Blobel, G. A SUMO ligase is part of a nuclear multiprotein complex that affects DNA repair and chromosomal organization. Proc. Natl Acad. Sci. USA 102, 4777–4782 (2005).
Sollier, J. et al. The Saccharomyces cerevisiae Esc2 and Smc5–6 proteins promote sister chromatid junction-mediated intra-S repair. Mol. Biol. Cell 20, 1671–1682 (2009).
Stegmeier, F. & Amon, A. Closing mitosis: the functions of the Cdc14 phosphatase and its regulation. Annu. Rev. Genet. 38, 203–232 (2004).
Lopes, M. et al. The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412, 557–561 (2001).
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). References 73 and74 document the role of the replication checkpoint in preventing the regression of stalled RFs.
Doksani, Y., Bermejo, R., Fiorani, S., Haber, J. E. & Foiani, M. Replicon dynamics, dormant origin firing, and terminal fork integrity after double-strand break formation. Cell 137, 247–258 (2009). Addresses the consequences of RFs encountering DSBs, and the pathways promoting the integrity of such terminal RFs.
Lahiri, M., Gustafson, T. L., Majors, E. R. & Freudenreich, C. H. Expanded CAG repeats activate the DNA damage checkpoint pathway. Mol. Cell 15, 287–293 (2004).
Freudenreich, C. H. & Lahiri, M. Structure-forming CAG/CTG repeat sequences are sensitive to breakage in the absence of Mrc1 checkpoint function and S-phase checkpoint signaling: implications for trinucleotide repeat expansion diseases. Cell Cycle 3, 1370–1374 (2004).
Voineagu, I., Narayanan, V., Lobachev, K. S. & Mirkin, S. M. Replication stalling at unstable inverted repeats: interplay between DNA hairpins and fork stabilizing proteins. Proc. Natl Acad. Sci. USA 105, 9936–9941 (2008).
Voineagu, I., Surka, C. F., Shishkin, A. A., Krasilnikova, M. M. & Mirkin, S. M. Replisome stalling and stabilization at CGG repeats, which are responsible for chromosomal fragility. Nature Struct. Mol. Biol. 16, 226–228 (2009).
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). In vitro study showing that RF reversal can be induced by positive supercoiling.
Fierro-Fernandez, M., Hernandez, P., Krimer, D. B., Stasiak, A. & Schvartzman, J. B. Topological locking restrains replication fork reversal. Proc. Natl Acad. Sci. USA 104, 1500–1505 (2007).
Cotta-Ramusino, C. et al. Exo1 processes stalled replication forks and counteracts fork reversal in checkpoint-defective cells. Mol. Cell 17, 153–159 (2005).
Feng, W. et al. Genomic mapping of single-stranded DNA in hydroxyurea-challenged yeasts identifies origins of replication. Nature Cell Biol. 8, 148–155 (2006).
Alcasabas, A. A. et al. Mrc1 transduces signals of DNA replication stress to activate Rad53. Nature Cell Biol. 3, 958–965 (2001).
Osborn, A. J. & Elledge, S. J. Mrc1 is a replication fork component whose phosphorylation in response to DNA replication stress activates Rad53. Genes Dev. 17, 1755–1767 (2003).
Foss, E. J. Tof1p regulates DNA damage responses during S phase in Saccharomyces cerevisiae. Genetics 157, 567–577 (2001).
Branzei, D. & Foiani, M. The checkpoint response to replication stress. DNA Repair (Amst.) 8, 1038–1046 (2009).
Shishkin, A. A. et al. Large-scale expansions of Friedreich's ataxia GAA repeats in yeast. Mol. Cell 35, 82–92 (2009).
Kai, M. & Wang, T. S. Checkpoint activation regulates mutagenic translesion synthesis. Genes Dev. 17, 64–76 (2003).
Sabbioneda, S. et al. The 9-1-1 checkpoint clamp physically interacts with polζ and is partially required for spontaneous polζ-dependent mutagenesis in Saccharomyces cerevisiae. J. Biol. Chem. 280, 38657–38665 (2005).
Liberi, G. et al. Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes Dev. 19, 339–350 (2005).
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). Shows physical evidence that gaps form during DNA replication without affecting RF progression.
Sancar, A., Lindsey-Boltz, L. A., Unsal-Kacmaz, K. & Linn., S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73, 39–85 (2004).
Higgins, N. P., Kato, K. & Strauss, B. A model for replication repair in mammalian cells. J. Mol. Biol. 101, 417–425 (1976).
Heller, R. C. & Marians, K. J. Replication fork reactivation downstream of a blocked nascent leading strand. Nature 439, 557–562 (2006). In vitro study showing that leading strands can also restart by re-priming downstream of the blocking lesions.
Amado, L. & Kuzminov, A. The replication intermediates in Escherichia coli are not the product of DNA processing or uracil excision. J. Biol. Chem. 281, 22635–22646 (2006).
Kogoma, T. Stable DNA replication: interplay between DNA replication, homologous recombination, and transcription. Microbiol Mol. Biol. Rev. 61, 212–238 (1997). Comprehensive review on the DNA metabolism processes operating during DNA replication.
Barbour, L., Ball, L. G., Zhang, K. & Xiao, W. DNA damage checkpoints are involved in postreplication repair. Genetics 174, 1789–1800 (2006).
Paulovich, A. G., Margulies, R. U., Garvik, B. M. & Hartwell, L. H. RAD9, RAD17, and RAD24 are required for S phase regulation in Saccharomyces cerevisiae in response to DNA damage. Genetics 145, 45–62 (1997).
Kai, M., Furuya, K., Paderi, F., Carr, A. M. & Wang, T. S. Rad3-dependent phosphorylation of the checkpoint clamp regulates repair-pathway choice. Nature Cell Biol. 9, 691–697 (2007).
Prakash, L. Characterization of postreplication repair in Saccharomyces cerevisiae and effects of rad6, rad18, rev3 and rad52 mutations. Mol. Gen. Genet. 184, 471–478 (1981).
Zhang, H. & Lawrence, C. W. The error-free component of the RAD6/RAD18 DNA damage tolerance pathway of budding yeast employs sister-strand recombination. Proc. Natl Acad. Sci. USA 102, 15954–15959 (2005).
Gangavarapu, V., Prakash, S. & Prakash, L. Requirement of RAD52 group genes for postreplication repair of UV-damaged DNA in Saccharomyces cerevisiae. Mol. Cell. Biol. 27, 7758–7764 (2007).
Hoege, C., Pfander, B., Moldovan, G. L., Pyrowolakis, G. & Jentsch, S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419, 135–141 (2002). This study was the first to identify PCNA modifications by ubiquitin and SUMO, and to suggest their role in DNA repair.
Stelter, P. & Ulrich, H. D. Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature 425, 188–191 (2003).
Kannouche, P. L., Wing, J. & Lehmann, A. R. Interaction of human DNA polymerase ɛ with monoubiquitinated PCNA: a possible mechanism for the polymerase switch in response to DNA damage. Mol. Cell 14, 491–500 (2004).
Torres-Ramos, C. A., Prakash, S. & Prakash, L. Requirement of RAD5 and MMS2 for postreplication repair of UV-damaged DNA in Saccharomyces cerevisiae. Mol. Cell. Biol. 22, 2419–2426 (2002).
Haracska, L., Torres-Ramos, C. A., Johnson, R. E., Prakash, S. & Prakash, L. Opposing effects of ubiquitin conjugation and SUMO modification of PCNA on replicational bypass of DNA lesions in Saccharomyces cerevisiae. Mol. Cell. Biol. 24, 4267–4274 (2004).
Falbo, K. B. et al. Involvement of a chromatin remodeling complex in damage tolerance during DNA replication. Nature Struct. Mol. Biol. 16, 1167–1172 (2009).
Wu, L. & Hickson, I. D. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426, 870–874 (2003).
Mankouri, H. W. & Hickson, I. D. Top3 processes recombination intermediates and modulates checkpoint activity after DNA damage. Mol. Biol. Cell 17, 4473–4483 (2006).
Mankouri, H. W., Ngo, H. P. & Hickson, I. D. Esc2 and Sgs1 act in functionally distinct branches of the homologous recombination repair pathway in Saccharomyces cerevisiae. Mol. Biol. Cell 20, 1683–1694 (2009).
Goldfless, S. J., Morag, A. S., Belisle, K. A., Sutera, V. A., Jr. & Lovett, S. T. DNA repeat rearrangements mediated by DnaK-dependent replication fork repair. Mol. Cell 21, 595–604 (2006).
Johnson, R. E. et al. Saccharomyces cerevisiae RAD5-encoded DNA repair protein contains DNA helicase and zinc-binding sequence motifs and affects the stability of simple repetitive sequences in the genome. Mol. Cell. Biol. 12, 3807–3818 (1992).
Branzei, D. & Foiani, M. Template switching: from replication fork repair to genome rearrangements. Cell 131, 1228–1230 (2007).
Lee, J. A., Carvalho, C. M. & Lupski, J. R. A DNA replication mechanism for generating nonrecurrent rearrangements associated with genomic disorders. Cell 131, 1235–1247 (2007). Proposes that template switching involving microhomology elements and different RFs is responsible for the complex genome rearrangements associated with certain genomic disorders.
Paek, A. L. et al. 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. 23, 2861–2875 (2009).
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. 23, 2876–2886 (2009). References 117 and 118 propose that template switching at nearby inverted repeats generates dicentric chromosomes without a DSB intermediate.
Scharer, O. D. DNA interstrand crosslinks: natural and drug-induced DNA adducts that induce unique cellular responses. Chembiochem 6, 27–32 (2005).
Niedzwiedz, W. et al. The Fanconi anaemia gene FANCC promotes homologous recombination and error-prone DNA repair. Mol. Cell 15, 607–620 (2004).
Wang, W. Emergence of a DNA-damage response network consisting of Fanconi anaemia and BRCA proteins. Nature Rev. Genet. 8, 735–748 (2007).
Sobeck, A. et al. Fanconi anemia proteins are required to prevent accumulation of replication-associated DNA double-strand breaks. Mol. Cell. Biol. 26, 425–437 (2006).
Meetei, A. R., Yan, Z. & Wang, W. FANCL replaces BRCA1 as the likely ubiquitin ligase responsible for FANCD2 monoubiquitination. Cell Cycle 3, 179–181 (2004).
Smogorzewska, A. et al. Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell 129, 289–301 (2007).
Ciccia, A. et al. Identification of FAAP24, a Fanconi anemia core complex protein that interacts with FANCM. Mol. Cell 25, 331–343 (2007).
Xia, B. et al. Fanconi anemia is associated with a defect in the BRCA2 partner PALB2. Nature Genet. 39, 159–161 (2007).
Sung, P. & Klein, H. Mechanism of homologous recombination: mediators and helicases take on regulatory functions. Nature Rev. Mol. Cell Biol. 7, 739–750 (2006).
Litman, R. et al. BACH1 is critical for homologous recombination and appears to be the Fanconi anemia gene product FANCJ. Cancer Cell 8, 255–265 (2005).
Nojima, K. et al. Multiple repair pathways mediate tolerance to chemotherapeutic cross-linking agents in vertebrate cells. Cancer Res. 65, 11704–11711 (2005).
Gari, K., Decaillet, 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).
Gari, K., Decaillet, 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).
Sun, W. et al. The FANCM ortholog Fml1 promotes recombination at stalled replication forks and limits crossing over during DNA double-strand break repair. Mol. Cell 32, 118–128 (2008).
Chen, Y. H. et al. Interplay between the Smc5/6 complex and the Mph1 helicase in recombinational repair. Proc. Natl Acad. Sci. USA 106, 21252–21257 (2009).
Raschle, M. et al. Mechanism of replication-coupled DNA interstrand crosslink repair. Cell 134, 969–980 (2008).
Knipscheer, P. et al. The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair. Science 326, 1698–1701 (2009). References 134 and 135 propose, based on in vitro studies, a new mechanism through which Fanconi anaemia proteins promote ICL repair.
Lou, Z., Minter-Dykhouse, K. & Chen, J. BRCA1 participates in DNA decatenation. Nature Struct. Mol. Biol. 12, 589–593 (2005).
Andreassen, P. R., D'Andrea, A. D. & Taniguchi, T. ATR couples FANCD2 monoubiquitination to the DNA-damage response. Genes Dev. 18, 1958–1963 (2004).
Luke-Glaser, S., Luke, B., Grossi, S. & Constantinou, A. FANCM regulates DNA chain elongation and is stabilized by S-phase checkpoint signalling. EMBO J. 10 Dec 2009 (doi: 10.1038/emboj.2009.371).
Koster, D. A., Palle, K., Bot., E. S., Bjornsti, M. A. & Dekker, N. H. Antitumour drugs impede DNA uncoiling by topoisomerase I. Nature 448, 213–217 (2007).
Branzei, D. & Foiani, M. Regulation of DNA repair throughout the cell cycle. Nature Rev. Mol. Cell Biol. 9, 297–308 (2008).
Sonoda, E., Hochegger, H., Saberi, A., Taniguchi, Y. & Takeda, S. Differential usage of non-homologous end-joining and homologous recombination in double strand break repair. DNA Repair (Amst.) 5, 1021–1029 (2006).
Tsao, Y. P., Russo, A., Nyamuswa, G., Silber, R. & Liu, L. F. Interaction between replication forks and topoisomerase I-DNA cleavable complexes: studies in a cell-free SV40 DNA replication system. Cancer Res. 53, 5908–5914 (1993).
Bartek, J. & Lukas, J. DNA damage checkpoints: from initiation to recovery or adaptation. Curr. Opin. Cell Biol. 19, 238–245 (2007).
Segurado, M. & Diffley, J. F. Separate roles for the DNA damage checkpoint protein kinases in stabilizing DNA replication forks. Genes Dev. 22, 1816–1827 (2008).
Champoux, J. J. DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem. 70, 369–413 (2001).
Geiss-Friedlander, R. & Melchior, F. Concepts in sumoylation: a decade on. Nature Rev. Mol. Cell Biol. 8, 947–956 (2007).
Mimura, S., Komata, M., Kishi, T., Shirahige, K. & Kamura, T. SCFDia2 regulates DNA replication forks during S-phase in budding yeast. EMBO J. 28, 3693–3705 (2009).
Morohashi, H., Maculins, T. & Labib, K. The amino-terminal TPR domain of Dia2 tethers SCF(Dia2) to the replisome progression complex. Curr. Biol. 19, 1943–1949 (2009). References 148 and 149 identifiy the replisome components Mrc1 and Ctf4 as targets for the F-box ubiquitin ligase Dia2.
Zhong, W., Feng, H., Santiago, F. E. & Kipreos, E. T. CUL-4 ubiquitin ligase maintains genome stability by restraining DNA-replication licensing. Nature 423, 885–889 (2003).
Zhang, Y. W. et al. Genotoxic stress targets human Chk1 for degradation by the ubiquitin-proteasome pathway. Mol. Cell 19, 607–618 (2005).
Leung-Pineda, V., Huh, J. & Piwnica-Worms, H. DDB1 targets Chk1 to the Cul4 E3 ligase complex in normal cycling cells and in cells experiencing replication stress. Cancer Res. 69, 2630–2637 (2009).
Whitcomb, E. A., Dudek, E. J., Liu, Q. & Taylor, A. Novel control of S phase of the cell cycle by ubiquitin-conjugating enzyme H7. Mol. Biol. Cell 20, 1–9 (2009).
Taniguchi, T. et al. S-phase-specific interaction of the Fanconi anemia protein, FANCD2, with BRCA1 and RAD51. Blood 100, 2414–2420 (2002).