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Review

Rescue from replication stress during mitosis

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Pages 613-633 | Received 11 Nov 2016, Accepted 24 Jan 2017, Published online: 27 Feb 2017

References

  • Sirbu BM, Cortez D. DNA damage response: three levels of DNA repair regulation. Cold Spring Harb Perspect Biol 2013; 5(8):a012724; PMID:23813586; http://dx.doi.org/10.1101/cshperspect.a012724
  • Zeman MK, Cimprich KA. Causes and consequences of replication stress. Nat Cell Biol 2014; 16(1):2-9; PMID:24366029; http://dx.doi.org/10.1038/ncb2897
  • Zou L, Elledge SJ. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 2003; 300(5625):1542-8; PMID:12791985; http://dx.doi.org/10.1126/science.1083430
  • Branzei D, Foiani M. The checkpoint response to replication stress. DNA Repair (Amst) 2009; 8(9):1038-46; PMID:19482564; http://dx.doi.org/10.1016/j.dnarep.2009.04.014
  • Jossen R, Bermejo R. The DNA damage checkpoint response to replication stress: A Game of Forks. Front Genet 2013; 4, 26; PMID:23493417; http://dx.doi.org/10.3389/fgene.2013.00026
  • Bergoglio V, Boyer AS, Walsh E, Naim V, Legube G, Lee MY, Rey L, Rosselli F, Cazaux C, Eckert KA, et al. DNA synthesis by Pol eta promotes fragile site stability by preventing under-replicated DNA in mitosis. J Cell Biol 2013; 201(3):395-408; PMID:23609533; http://dx.doi.org/10.1083/jcb.201207066
  • Le Beau MM, Rassool FV, Neilly ME, Espinosa R 3rd, Glover TW, Smith DI, McKeithan TW. Replication of a common fragile site, FRA3B, occurs late in S phase and is delayed further upon induction: implications for the mechanism of fragile site induction. Hum Mol Genet 1998; 7(4):755-61; PMID:9499431; http://dx.doi.org/10.1093/hmg/7.4.755
  • Widrow RJ, Hansen RS, Kawame H, Gartler SM, Laird CD. Very late DNA replication in the human cell cycle. Proc Natl Acad Sci U S A 1998; 95(19):11246-50; PMID:9736721; http://dx.doi.org/10.1073/pnas.95.19.11246
  • Hirano T. Chromosome Dynamics during Mitosis. Cold Spring Harb Perspect Biol 2015; 7(6):1–14; PMID:25722466; http://dx.doi.org/10.1101/cshperspect.a015792
  • Tanaka K, Hirota T. Chromosomal instability: A common feature and a therapeutic target of cancer. Biochim Biophys Acta 2016; 1866(1):64-75; PMID:27345585
  • Bakhoum SF, Silkworth WT, Nardi IK, Nicholson JM, Compton DA, Cimini D. The mitotic origin of chromosomal instability. Curr Biol 2014; 24(4):R148-9; PMID:24556433; http://dx.doi.org/10.1016/j.cub.2014.01.019
  • Naim V, Rosselli F. The FANC pathway and BLM collaborate during mitosis to prevent micro-nucleation and chromosome abnormalities. Nat Cell Biol 2009; 11(6):761-8; PMID:19465921; http://dx.doi.org/10.1038/ncb1883
  • Chan KL, Palmai-Pallag T, Ying S, Hickson ID. Replication stress induces sister-chromatid bridging at fragile site loci in mitosis. Nat Cell Biol 2009; 11(6):753-60; PMID:19465922; http://dx.doi.org/10.1038/ncb1882
  • Burrell RA, McClelland SE, Endesfelder D, Groth P, Weller MC, Shaikh N, Domingo E, Kanu N, Dewhurst SM, Gronroos E, et al. Replication stress links structural and numerical cancer chromosomal instability. Nature 2013; 494(7438):492-6; PMID:23446422; http://dx.doi.org/10.1038/nature11935
  • Naim V, Rosselli F. The FANC pathway and mitosis: a replication legacy. Cell Cycle 2009; 8(18):2907-11; PMID:19729998; http://dx.doi.org/10.4161/cc.8.18.9538
  • Chan KL, North PS, Hickson ID. BLM is required for faithful chromosome segregation and its localization defines a class of ultrafine anaphase bridges. EMBO J 2007; 26(14):3397-409; PMID:17599064; http://dx.doi.org/10.1038/sj.emboj.7601777
  • Lukas C, Savic V, Bekker-Jensen S, Doil C, Neumann B, Pedersen RS, Grøfte M, Chan KL, Hickson ID, Bartek J, et al. 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat Cell Biol 2011; 13(3):243-53; PMID:21317883; http://dx.doi.org/10.1038/ncb2201
  • Harrigan JA, Belotserkovskaya R, Coates J, Dimitrova DS, Polo SE, Bradshaw CR, Fraser P, Jackson SP. Replication stress induces 53BP1-containing OPT domains in G1 cells. J Cell Biol 2011; 193(1):97-108; PMID:21444690; http://dx.doi.org/10.1083/jcb.201011083
  • Baumann C, Körner R, Hofmann K, Nigg EA. PICH, a centromere-associated SNF2 family ATPase, is regulated by Plk1 and required for the spindle checkpoint. Cell 2007; 128(1):101-14; PMID:17218258; http://dx.doi.org/10.1016/j.cell.2006.11.041
  • 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. Nat Cell Biol 2013; 15(8):1008-15; PMID:23811686; http://dx.doi.org/10.1038/ncb2793
  • Ying S, Minocherhomji S, Chan KL, Palmai-Pallag T, Chu WK, Wass T, Mankouri HW, Liu Y, Hickson ID. MUS81 promotes common fragile site expression. Nat Cell Biol 2013; 15(8):1001-7; PMID:23811685; http://dx.doi.org/10.1038/ncb2773
  • Minocherhomji S, Ying S, Bjerregaard VA, Bursomanno S, Aleliunaite A, Wu W, Mankouri HW, Shen H, Liu Y, Hickson ID. Replication stress activates DNA repair synthesis in mitosis. Nature 2015; 528(7581):286-90; PMID:26633632; http://dx.doi.org/10.1038/nature16139
  • Pedersen RT, Kruse T, Nilsson J, Oestergaard VH, Lisby M. TopBP1 is required at mitosis to reduce transmission of DNA damage to G1 daughter cells. J Cell Biol 2015; 210(4):565-82; PMID:26283799; http://dx.doi.org/10.1083/jcb.201502107
  • Wild P, Matos J. Cell cycle control of DNA joint molecule resolution. Curr Opin Cell Biol 2016; 40, 74-80; PMID:26970388; http://dx.doi.org/10.1016/j.ceb.2016.02.018
  • Fragkos M, Ganier O, Coulombe P, Méchali M. DNA replication origin activation in space and time. Nat Rev Mol Cell Biol 2015; 16(6):360-74; PMID:25999062; http://dx.doi.org/10.1038/nrm4002
  • Shima N, Alcaraz A, Liachko I, Buske TR, Andrews CA, Munroe RJ, Hartford SA, Tye BK, Schimenti JC. A viable allele of Mcm4 causes chromosome instability and mammary adenocarcinomas in mice. Nat Genet 2007; 39(1):93-8; PMID:17143284; http://dx.doi.org/10.1038/ng1936
  • Kawabata T, Luebben SW, Yamaguchi S, Ilves I, Matise I, Buske T, Botchan MR, Shima N. Stalled fork rescue via dormant replication origins in unchallenged S phase promotes proper chromosome segregation and tumor suppression. Mol Cell 2011; 41(5):543-53; PMID:21362550; http://dx.doi.org/10.1016/j.molcel.2011.02.006
  • Letessier A, Millot GA, Koundrioukoff S, Lachagès AM, Vogt N, Hansen RS, Malfoy B, Brison O, Debatisse M. Cell-type-specific replication initiation programs set fragility of the FRA3B fragile site. Nature 2011; 470(7332):120-3; PMID:21258320; http://dx.doi.org/10.1038/nature09745
  • Ozeri-Galai E, Lebofsky R, Rahat A, Bester AC, Bensimon A, Kerem B. Failure of origin activation in response to fork stalling leads to chromosomal instability at fragile sites. Mol Cell 2011; 43(1):122-31; PMID:21726815; http://dx.doi.org/10.1016/j.molcel.2011.05.019
  • Aparicio OM. Location, location, location: it's all in the timing for replication origins. Genes Dev 2013; 27(2):117-28; PMID:23348837; http://dx.doi.org/10.1101/gad.209999.112
  • Toledo LI, Altmeyer M, Rask MB, Lukas C, Larsen DH, Povlsen LK, Bekker-Jensen S, Mailand N, Bartek J, Lukas J. ATR prohibits replication catastrophe by preventing global exhaustion of RPA. Cell 2013; 155(5):1088-103; PMID:24267891; http://dx.doi.org/10.1016/j.cell.2013.10.043
  • Magdalou I, Lopez BS, Pasero P, Lambert SA. The causes of replication stress and their consequences on genome stability and cell fate. Semin Cell Dev Biol 2014; 30, 154-64; PMID:24818779; http://dx.doi.org/10.1016/j.semcdb.2014.04.035
  • Blow JJ, Ge XQ, Jackson DA. How dormant origins promote complete genome replication. Trends Biochem Sci 2011; 36(8):405-14; PMID:21641805; http://dx.doi.org/10.1016/j.tibs.2011.05.002
  • Ge XQ, Jackson DA, Blow JJ. Dormant origins licensed by excess Mcm2-7 are required for human cells to survive replicative stress. Genes Dev 2007; 21(24):3331-41; PMID:18079179; http://dx.doi.org/10.1101/gad.457807
  • Woodward AM, Göhler T, Luciani MG, Oehlmann M, Ge X, Gartner A, Jackson DA, Blow JJ. Excess Mcm2-7 license dormant origins of replication that can be used under conditions of replicative stress. J Cell Biol 2006; 173(5):673-83; PMID:16754955; http://dx.doi.org/10.1083/jcb.200602108
  • Ibarra A, Schwob E, Méndez J. Excess MCM proteins protect human cells from replicative stress by licensing backup origins of replication. Proc Natl Acad Sci U S A 2008; 105(26):8956-61; PMID:18579778; http://dx.doi.org/10.1073/pnas.0803978105
  • Anglana M, Apiou F, Bensimon A, Debatisse M. Dynamics of DNA replication in mammalian somatic cells: nucleotide pool modulates origin choice and interorigin spacing. Cell 2003; 114(3):385-94; PMID:12914702; http://dx.doi.org/10.1016/S0092-8674(03)00569-5
  • Rybak P, Waligórska A, Bujnowicz Ł, Hoang A, Dobrucki JW. Activation of new replication foci under conditions of replication stress. Cell Cycle 2015; 14(16):2634-47; PMID:26212617; http://dx.doi.org/10.1080/15384101.2015.1064566
  • Cortez D. Preventing replication fork collapse to maintain genome integrity. DNA Repair (Amst) 2015; 32, 149-57; PMID:25957489; http://dx.doi.org/10.1016/j.dnarep.2015.04.026
  • Branzei D, Foiani M. Interplay of replication checkpoints and repair proteins at stalled replication forks. DNA Repair (Amst) 2007; 6(7):994-1003; PMID:17382606; http://dx.doi.org/10.1016/j.dnarep.2007.02.018
  • Paulsen RD, Cimprich KA. The ATR pathway: fine-tuning the fork. DNA Repair (Amst) 2007; 6(7):953-66; PMID:17531546; http://dx.doi.org/10.1016/j.dnarep.2007.02.015
  • Berti M, Vindigni A. Replication stress: getting back on track. Nat Struct Mol Biol 2016; 23(2):103-9; PMID:26840898; http://dx.doi.org/10.1038/nsmb.3163
  • Lehmann AR. Replication of UV-damaged DNA: new insights into links between DNA polymerases, mutagenesis and human disease. Gene 2000; 253(1):1-12; PMID:10925197; http://dx.doi.org/10.1016/S0378-1119(00)00250-X
  • Ward IM, Minn K, Chen J. UV-induced ataxia-telangiectasia-mutated and Rad3-related (ATR) activation requires replication stress. J Biol Chem 2004; 279(11):9677-80; PMID:14742437; http://dx.doi.org/10.1074/jbc.C300554200
  • Glover TW, Berger C, Coyle J, Echo B. DNA polymerase alpha inhibition by aphidicolin induces gaps and breaks at common fragile sites in human chromosomes. Hum Genet 1984; 67(2):136-42; PMID:6430783; http://dx.doi.org/10.1007/BF00272988
  • Byrnes JJ. Structural and functional properties of DNA polymerase delta from rabbit bone marrow. Mol Cell Biochem 1984; 62(1):13-24; PMID:6330522; http://dx.doi.org/10.1007/BF00230073
  • Cheng CH, Kuchta RD. DNA polymerase epsilon: aphidicolin inhibition and the relationship between polymerase and exonuclease activity. Biochemistry 1993; 32(33):8568-74; PMID:8395209; http://dx.doi.org/10.1021/bi00084a025
  • Takeuchi R, Oshige M, Uchida M, Ishikawa G, Takata K, Shimanouchi K, Kanai Y, Ruike T, Morioka H, Sakaguchi K. Purification of Drosophila DNA polymerase zeta by REV1 protein-affinity chromatography. Biochem J 2004; 382(Pt 2):535-43; PMID:15175013; http://dx.doi.org/10.1042/BJ20031833
  • Poli J, Tsaponina O, Crabbé L, Keszthelyi A, Pantesco V, Chabes A, Lengronne A, Pasero P. dNTP pools determine fork progression and origin usage under replication stress. EMBO J 2012; 31(4):883-94; PMID:22234185; http://dx.doi.org/10.1038/emboj.2011.470
  • Petermann E, Orta ML, 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(4):492-502; PMID:20188668; http://dx.doi.org/10.1016/j.molcel.2010.01.021
  • Aparicio JG, Viggiani CJ, Gibson DG, Aparicio OM. The Rpd3-Sin3 histone deacetylase regulates replication timing and enables intra-S origin control in Saccharomyces cerevisiae. Mol Cell Biol 2004; 24(11):4769-80; PMID:15143171; http://dx.doi.org/10.1128/MCB.24.11.4769-4780.2004
  • Bickmore WA, Carothers AD. Factors affecting the timing and imprinting of replication on a mammalian chromosome. J Cell Sci 1995; 108 ( Pt 8):2801-9; PMID:7593321
  • Pommier Y. Topoisomerase I inhibitors: camptothecins and beyond. Nat Rev Cancer 2006; 6(10):789-802; PMID:16990856; http://dx.doi.org/10.1038/nrc1977
  • Lambert S, Carr AM. Impediments to replication fork movement: stabilisation, reactivation and genome instability. Chromosoma 2013; 122(1-2):33-45; PMID:23446515; http://dx.doi.org/10.1007/s00412-013-0398-9
  • Tarsounas M, Tijsterman M. Genomes and G-quadruplexes: for better or for worse. J Mol Biol 2013; 425(23):4782-9; PMID:24076189; http://dx.doi.org/10.1016/j.jmb.2013.09.026
  • Mendoza O, Bourdoncle A, Boulé JB, Brosh RM Jr, Mergny JL. G-quadruplexes and helicases. Nucleic Acids Res 2016; 44(5):1989-2006; PMID:26883636; http://dx.doi.org/10.1093/nar/gkw079
  • Branzei D, Foiani M. Maintaining genome stability at the replication fork. Nat Rev Mol Cell Biol 2010; 11(3):208-19; PMID:20177396; http://dx.doi.org/10.1038/nrm2852
  • Martinez P, Blasco MA. Replicating through telomeres: a means to an end. Trends Biochem Sci 2015; 40(9):504-15; PMID:26188776; http://dx.doi.org/10.1016/j.tibs.2015.06.003
  • Zimmer J, Tacconi EM, Folio C, Badie S, Porru M, Klare K, Tumiati M, Markkanen E, Halder S, Ryan A, et al. Targeting BRCA1 and BRCA2 Deficiencies with G-Quadruplex-Interacting Compounds. Mol Cell 2016; 61(3):449-60; PMID:26748828; http://dx.doi.org/10.1016/j.molcel.2015.12.004
  • Sfeir A, Kosiyatrakul ST, Hockemeyer D, MacRae SL, Karlseder J, Schildkraut CL, de Lange T. Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell 2009; 138(1):90-103; PMID:19596237; http://dx.doi.org/10.1016/j.cell.2009.06.021
  • Vannier JB, Pavicic-Kaltenbrunner V, Petalcorin MI, Ding H, Boulton SJ. RTEL1 dismantles T loops and counteracts telomeric G4-DNA to maintain telomere integrity. Cell 2012; 149(4):795-806; PMID:22579284; http://dx.doi.org/10.1016/j.cell.2012.03.030
  • Aguilera A, Garcia-Muse T. Causes of genome instability. Annu Rev Genet 2013; 47, 1-32; PMID:23909437; http://dx.doi.org/10.1146/annurev-genet-111212-133232
  • Lebofsky R, Bensimon A. DNA replication origin plasticity and perturbed fork progression in human inverted repeats. Mol Cell Biol 2005; 25(15):6789-97; PMID:16024811; http://dx.doi.org/10.1128/MCB.25.15.6789-6797.2005
  • Akamatsu Y, Kobayashi T. The Human RNA Polymerase I Transcription Terminator Complex Acts as a Replication Fork Barrier That Coordinates the Progress of Replication with rRNA Transcription Activity. Mol Cell Biol 2015; 35(10):1871-81; PMID:25776556; http://dx.doi.org/10.1128/MCB.01521-14
  • Brewer BJ, Fangman WL. A replication fork barrier at the 3′ end of yeast ribosomal RNA genes. Cell 1988; 55(4):637-43; PMID:3052854; http://dx.doi.org/10.1016/0092-8674(88)90222-X
  • Kobayashi T, Horiuchi T. A yeast gene product, Fob1 protein, required for both replication fork blocking and recombinational hotspot activities. Genes Cells 1996; 1(5):465-74; PMID:9078378; http://dx.doi.org/10.1046/j.1365-2443.1996.d01-256.x
  • Linskens MH, Huberman JA. Organization of replication of ribosomal DNA in Saccharomyces cerevisiae. Mol Cell Biol 1988; 8(11):4927-35; PMID:3062373; http://dx.doi.org/10.1128/MCB.8.11.4927
  • Lopez-estrano C, Schvartzman JB, Krimer DB, Hernández P. Co-localization of polar replication fork barriers and rRNA transcription terminators in mouse rDNA. J Mol Biol 1998; 277(2):249-56; PMID:9514756; http://dx.doi.org/10.1006/jmbi.1997.1607
  • Gerber JK, Gögel E, Berger C, Wallisch M, Müller F, Grummt I, Grummt F. Termination of mammalian rDNA replication: polar arrest of replication fork movement by transcription termination factor TTF-I. Cell 1997; 90(3):559-67; PMID:9267035; http://dx.doi.org/10.1016/S0092-8674(00)80515-2
  • Probst AV, Almouzni G. Pericentric heterochromatin: dynamic organization during early development in mammals. Differentiation 2008; 76(1):15-23; PMID:17825083; http://dx.doi.org/10.1111/j.1432-0436.2007.00220.x
  • Porter AC, Farr CJ. Topoisomerase II: untangling its contribution at the centromere. Chromosome Res 2004; 12(6):569-83; PMID:15289664; http://dx.doi.org/10.1023/B:CHRO.0000036608.91085.d1
  • Rouzeau S, Cordelières FP, Buhagiar-Labarchède G, Hurbain I, Onclercq-Delic R, Gemble S, Magnaghi-Jaulin L, Jaulin C, Amor-Guéret M. Bloom's syndrome and PICH helicases cooperate with topoisomerase IIalpha in centromere disjunction before anaphase. PLoS One 2012; 7(4):e33905; PMID:22563370; http://dx.doi.org/10.1371/journal.pone.0033905
  • Azvolinsky A, Dunaway S, Torres JZ, Bessler JB, Zakian VA. The S. cerevisiae Rrm3p DNA helicase moves with the replication fork and affects replication of all yeast chromosomes. Genes Dev 2006; 20(22):3104-16; PMID:17114583; http://dx.doi.org/10.1101/gad.1478906
  • Gorgoulis VG, Vassiliou LV, Karakaidos P, Zacharatos P, Kotsinas A, Liloglou T, Venere M, Ditullio RA Jr, Kastrinakis NG, Levy B, et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 2005; 434(7035):907-13; PMID:15829965; http://dx.doi.org/10.1038/nature03485
  • Halazonetis TD, Gorgoulis VG, Bartek J. An oncogene-induced DNA damage model for cancer development. Science 2008; 319(5868):1352-5; PMID:18323444; http://dx.doi.org/10.1126/science.1140735
  • Maya-Mendoza A, Ostrakova J, Kosar M, Hall A, Duskova P, Mistrik M, Merchut-Maya JM, Hodny Z, Bartkova J, Christensen C, et al. Myc and Ras oncogenes engage different energy metabolism programs and evoke distinct patterns of oxidative and DNA replication stress. Mol Oncol 2015; 9(3):601-16; PMID:25435281; http://dx.doi.org/10.1016/j.molonc.2014.11.001
  • Tsantoulis PK, Kotsinas A, Sfikakis PP, Evangelou K, Sideridou M, Levy B, Mo L, Kittas C, Wu XR, Papavassiliou AG, et al. Oncogene-induced replication stress preferentially targets common fragile sites in preneoplastic lesions. A genome-wide study. Oncogene 2008; 27(23):3256-64
  • Bartkova J, Horejsí Z, Koed K, Krämer A, Tort F, Zieger K, Guldberg P, Sehested M, Nesland JM, Lukas C. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 2005; 434(7035):864-70; PMID:15829956; http://dx.doi.org/10.1038/nature03482
  • Bartkova J, Rezaei N, Liontos M, Karakaidos P, Kletsas D, Issaeva N, Vassiliou LV, Kolettas E, Niforou K, Zoumpourlis VC, et al. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 2006; 444(7119):633-7; PMID:17136093; http://dx.doi.org/10.1038/nature05268
  • Suram A, Kaplunov J, Patel PL, Ruan H, Cerutti A, Boccardi V, Fumagalli M, Di Micco R, Mirani N, Gurung RL. Oncogene-induced telomere dysfunction enforces cellular senescence in human cancer precursor lesions. EMBO J 2012; 31(13):2839-51; PMID:22569128; http://dx.doi.org/10.1038/emboj.2012.132
  • Di Micco R, Fumagalli M, Cicalese A, Piccinin S, Gasparini P, Luise C, Schurra C, Garre′ M, Nuciforo PG, Bensimon A, et al. Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 2006; 444(7119):638-42; PMID:17136094; http://dx.doi.org/10.1038/nature05327
  • Hills SA, Diffley JF. DNA replication and oncogene-induced replicative stress. Curr Biol 2014; 24(10):R435-44; PMID:24845676; http://dx.doi.org/10.1016/j.cub.2014.04.012
  • Ekholm-Reed S, Méndez J, Tedesco D, Zetterberg A, Stillman B, Reed SI. Deregulation of cyclin E in human cells interferes with prereplication complex assembly. J Cell Biol 2004; 165(6):789-800; PMID:15197178; http://dx.doi.org/10.1083/jcb.200404092
  • Jones RM, Mortusewicz O, Afzal I, Lorvellec M, García P, Helleday T, Petermann E. Increased replication initiation and conflicts with transcription underlie Cyclin E-induced replication stress. Oncogene 2013; 32(32):3744-53; PMID:22945645; http://dx.doi.org/10.1038/onc.2012.387
  • Bester AC, Roniger M, Oren YS, Im MM, Sarni D, Chaoat M, Bensimon A, Zamir G, Shewach DS, Kerem B. Nucleotide deficiency promotes genomic instability in early stages of cancer development. Cell 2011; 145(3):435-46; PMID:21529715; http://dx.doi.org/10.1016/j.cell.2011.03.044
  • Xie M, Yen Y, Owonikoko TK, Ramalingam SS, Khuri FR, Curran WJ, Doetsch PW, Deng X. Bcl2 induces DNA replication stress by inhibiting ribonucleotide reductase. Cancer Res 2014; 74(1):212-23; PMID:24197132; http://dx.doi.org/10.1158/0008-5472.CAN-13-1536-T
  • Burhans WC, Weinberger M. DNA replication stress, genome instability and aging. Nucleic Acids Res 2007; 35(22):7545-56; PMID:18055498; http://dx.doi.org/10.1093/nar/gkm1059
  • Ogrunc M, Di Micco R, Liontos M, Bombardelli L, Mione M, Fumagalli M, Gorgoulis VG, d'Adda di Fagagna F. Oncogene-induced reactive oxygen species fuel hyperproliferation and DNA damage response activation. Cell Death Differ 2014; 21(6):998-1012; PMID:24583638; http://dx.doi.org/10.1038/cdd.2014.16
  • Wilhelm T, Ragu S, Magdalou I, Machon C, Dardillac E, Técher H, Guitton J, Debatisse M, Lopez BS. Slow Replication Fork Velocity of Homologous Recombination-Defective Cells Results from Endogenous Oxidative Stress. PLoS Genet 2016; 12(5):e1006007; PMID:27135742; http://dx.doi.org/10.1371/journal.pgen.1006007
  • Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, Casero RA, Shi Y. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 2004; 119(7):941-53; PMID:15620353; http://dx.doi.org/10.1016/j.cell.2004.12.012
  • Brooks PJ, Theruvathu JA. DNA adducts from acetaldehyde: implications for alcohol-related carcinogenesis. Alcohol 2005; 35(3):187-93; PMID:16054980; http://dx.doi.org/10.1016/j.alcohol.2005.03.009
  • Garaycoechea JI, Patel KJ. Why does the bone marrow fail in Fanconi anemia? Blood 2014; 123(1):26-34; PMID:24200684; http://dx.doi.org/10.1182/blood-2013-09-427740
  • McClendon AK, Rodriguez AC, Osheroff N. Human topoisomerase IIalpha rapidly relaxes positively supercoiled DNA: implications for enzyme action ahead of replication forks. J Biol Chem 2005; 280(47):39337-45; PMID:16188892; http://dx.doi.org/10.1074/jbc.M503320200
  • Groth A, Rocha W, Verreault A, Almouzni G. Chromatin challenges during DNA replication and repair. Cell 2007; 128(4):721-33; PMID:17320509; http://dx.doi.org/10.1016/j.cell.2007.01.030
  • Clemente-Ruiz M, Prado F. Chromatin assembly controls replication fork stability. EMBO Rep 2009; 10(7):790-6; PMID:19465889; http://dx.doi.org/10.1038/embor.2009.67
  • Mejlvang J, et al. New histone supply regulates replication fork speed and PCNA unloading. J Cell Biol 2014; 204(1):29-43; http://dx.doi.org/10.1083/jcb.201305017
  • Nikolov I, Taddei A. Linking replication stress with heterochromatin formation. Chromosoma 2016; 125(3):523-33; http://dx.doi.org/10.1007/s00412-015-0545-6
  • Tabancay AP, Jr., Forsburg SL. Eukaryotic DNA replication in a chromatin context. Curr Top Dev Biol 76, 129-84; PMID:17118266
  • Wei X, Samarabandu J, Devdhar RS, Siegel AJ, Acharya R, Berezney R. (1998) Segregation of transcription and replication sites into higher order domains. Science 2006; 281(5382):1502-6; PMID:9727975; http://dx.doi.org/10.1126/science.281.5382.1502
  • Gottipati P, Cassel TN, Savolainen L, Helleday T. Transcription-associated recombination is dependent on replication in Mammalian cells. Mol Cell Biol 2008; 28(1):154-64; PMID:17967877; http://dx.doi.org/10.1128/MCB.00816-07
  • Poli J, Gerhold CB, Tosi A, Hustedt N, Seeber A, Sack R, Herzog F, Pasero P, Shimada K, Hopfner KP, et al. Mec1, INO80, and the PAF1 complex cooperate to limit transcription replication conflicts through RNAPII removal during replication stress. Genes Dev 2016; 30(3):337-54; PMID:26798134; http://dx.doi.org/10.1101/gad.273813.115
  • Lafon A, Taranum S, Pietrocola F, Dingli F, Loew D, Brahma S, Bartholomew B, Papamichos-Chronakis M. INO80 Chromatin Remodeler Facilitates Release of RNA Polymerase II from Chromatin for Ubiquitin-Mediated Proteasomal Degradation. Mol Cell 2015; 60(5):784-96; PMID:26656161; http://dx.doi.org/10.1016/j.molcel.2015.10.028
  • Poveda AM, Le Clech M, Pasero P. Transcription and replication: breaking the rules of the road causes genomic instability. Transcription 2010; 1(2):99-102; PMID:21326900; http://dx.doi.org/10.4161/trns.1.2.12665
  • Santos-Pereira JM, Aguilera A. R loops: new modulators of genome dynamics and function. Nat Rev Genet 2015; 16(10):583-97; PMID:26370899; http://dx.doi.org/10.1038/nrg3961
  • Sollier J, Stork CT, García-Rubio ML, Paulsen RD, Aguilera A, Cimprich KA. Transcription-coupled nucleotide excision repair factors promote R-loop-induced genome instability. Mol Cell 2014; 56(6):777-85; PMID:25435140; http://dx.doi.org/10.1016/j.molcel.2014.10.020
  • Alzu A, Bermejo R, Begnis M, Lucca C, Piccini D, Carotenuto W, Saponaro M, Brambati A, Cocito A, Foiani M, et al. Senataxin associates with replication forks to protect fork integrity across RNA-polymerase-II-transcribed genes. Cell 2012; 151(4):835-46; PMID:23141540; http://dx.doi.org/10.1016/j.cell.2012.09.041
  • Li X, Manley JL. Cotranscriptional processes and their influence on genome stability. Genes Dev 2006; 20(14):1838-47; PMID:16847344; http://dx.doi.org/10.1101/gad.1438306
  • Gomez-Gonzalez B, García-Rubio M, Bermejo R, Gaillard H, Shirahige K, Marín A, Foiani M, Aguilera A. Genome-wide function of THO/TREX in active genes prevents R-loop-dependent replication obstacles. EMBO J 2011; 30(15):3106-19; PMID:21701562; http://dx.doi.org/10.1038/emboj.2011.206
  • Stirling PC, Chan YA, Minaker SW, Aristizabal MJ, Barrett I, Sipahimalani P, Kobor MS, Hieter P. R-loop-mediated genome instability in mRNA cleavage and polyadenylation mutants. Genes Dev 2012; 26(2):163-75; PMID:22279048; http://dx.doi.org/10.1101/gad.179721.111
  • Wahba L, Gore SK, Koshland D. The homologous recombination machinery modulates the formation of RNA-DNA hybrids and associated chromosome instability. Elife 2, e00505; PMID:23795288; http://dx.doi.org/10.7554/eLife.00505
  • Ginno PA, Lim YW, Lott PL, Korf I, Chédin F. ( 2013) GC skew at the 5′ and 3′ ends of human genes links R-loop formation to epigenetic regulation and transcription termination. Genome Res 2013; 23(10):1590-600; PMID:23868195; http://dx.doi.org/10.1101/gr.158436.113
  • Aguilera A, Garcia-Muse T. R loops: from transcription byproducts to threats to genome stability. Mol Cell 2012; 46(2):115-24; PMID:22541554; http://dx.doi.org/10.1016/j.molcel.2012.04.009
  • Tuduri S, Crabbé L, Conti C, Tourrière H, Holtgreve-Grez H, Jauch A, Pantesco V, De Vos J, Thomas A, Theillet C, et al. Topoisomerase I suppresses genomic instability by preventing interference between replication and transcription. Nat Cell Biol 2009; 11(11):1315-24; PMID:19838172; http://dx.doi.org/10.1038/ncb1984
  • Bermejo R, Capra T, Gonzalez-Huici V, Fachinetti D, Cocito A, Natoli G, Katou Y, Mori H, Kurokawa K, Shirahige K, et al. Genome-organizing factors Top2 and Hmo1 prevent chromosome fragility at sites of S phase transcription. Cell 2009; 138(5):870-84; PMID:19737516; http://dx.doi.org/10.1016/j.cell.2009.06.022
  • Bermejo R, Capra T, Jossen R, Colosio A, Frattini C, Carotenuto W, Cocito A, Doksani Y, Klein H, Gómez-González B, et al. The replication checkpoint protects fork stability by releasing transcribed genes from nuclear pores. Cell 2011; 146(2):233-46; PMID:21784245; http://dx.doi.org/10.1016/j.cell.2011.06.033
  • Durkin SG, Glover TW. Chromosome fragile sites. Annu Rev Genet 41, 169-92; PMID:17608616; http://dx.doi.org/10.1146/annurev.genet.41.042007.165900
  • Sutherland GR ( 1977) Fragile sites on human chromosomes: demonstration of their dependence on the type of tissue culture medium. Science 2007; 197(4300):265-6; PMID:877551; http://dx.doi.org/10.1126/science.877551
  • Sutherland GR. The role of nucleotides in human fragile site expression. Mutat Res 1988; 200(1-2):207-13; PMID:3292907; http://dx.doi.org/10.1016/0027-5107(88)90084-X
  • Jiang Y, Lucas I, Young DJ, Davis EM, Karrison T, Rest JS, Le Beau MM. Common fragile sites are characterized by histone hypoacetylation. Hum Mol Genet 2009; 18(23):4501-12; PMID:19717471; http://dx.doi.org/10.1093/hmg/ddp410
  • Becker NA, Thorland EC, Denison SR, Phillips LA, Smith DI. Evidence that instability within the FRA3B region extends four megabases. Oncogene 2002; 21(57):8713-22; PMID:12483524; http://dx.doi.org/10.1038/sj.onc.1205950
  • Smith DI, Zhu Y, McAvoy S, Kuhn R. Common fragile sites, extremely large genes, neural development and cancer. Cancer Lett 2006; 232(1):48-57; PMID:16221525; http://dx.doi.org/10.1016/j.canlet.2005.06.049
  • Debatisse M, Le Tallec B, Letessier A, Dutrillaux B, Brison O. Common fragile sites: mechanisms of instability revisited. Trends Genet 2012; 28(1):22-32; PMID:22094264; http://dx.doi.org/10.1016/j.tig.2011.10.003
  • Le Tallec B, Koundrioukoff S, Wilhelm T, Letessier A, Brison O, Debatisse M. Updating the mechanisms of common fragile site instability: how to reconcile the different views? Cell Mol Life Sci 2014; 71(23):4489-94; PMID:25248392; http://dx.doi.org/10.1007/s00018-014-1720-2
  • Ozeri-Galai E, Tur-Sinai M, Bester AC, Kerem B. Interplay between genetic and epigenetic factors governs common fragile site instability in cancer. Cell Mol Life Sci 2014; 71(23):4495-506; PMID:25297918; http://dx.doi.org/10.1007/s00018-014-1719-8
  • Sarni D, Kerem B. The complex nature of fragile site plasticity and its importance in cancer. Curr Opin Cell Biol 40, 131-6; PMID:27062332; http://dx.doi.org/10.1016/j.ceb.2016.03.017
  • Miotto B, Ji Z, Struhl K. ( 2016) Selectivity of ORC binding sites and the relation to replication timing, fragile sites, and deletions in cancers. Proc Natl Acad Sci U S A 2016; 113(33):E4810-9; PMID:27436900; http://dx.doi.org/10.1073/pnas.1609060113
  • Helmrich A, Ballarino M, Tora L. Collisions between replication and transcription complexes cause common fragile site instability at the longest human genes. Mol Cell 2011; 44(6):966-77; PMID:22195969; http://dx.doi.org/10.1016/j.molcel.2011.10.013
  • Wilson TE, Arlt MF, Park SH, Rajendran S, Paulsen M, Ljungman M, Glover TW. Large transcription units unify copy number variants and common fragile sites arising under replication stress. Genome Res 2015; 25(2):189-200; PMID:25373142; http://dx.doi.org/10.1101/gr.177121.114
  • Gros J, Kumar C, Lynch G, Yadav T, Whitehouse I, Remus D. Post-licensing Specification of Eukaryotic Replication Origins by Facilitated Mcm2-7 Sliding along DNA. Mol Cell 2015; 60(5):797-807; PMID:26656162; http://dx.doi.org/10.1016/j.molcel.2015.10.022
  • Snyder M, Sapolsky RJ, Davis RW. Transcription interferes with elements important for chromosome maintenance in Saccharomyces cerevisiae. Mol Cell Biol 1988; 8(5):2184-94; PMID:3290652; http://dx.doi.org/10.1128/MCB.8.5.2184
  • Looke M, Reimand J, Sedman T, Sedman J, Järvinen L, Värv S, Peil K, Kristjuhan K, Vilo J, Kristjuhan A. Relicensing of transcriptionally inactivated replication origins in budding yeast. J Biol Chem 2010; 285(51):40004-11; PMID:20962350; http://dx.doi.org/10.1074/jbc.M110.148924
  • Miron K, Golan-Lev T, Dvir R, Ben-David E, Kerem B. Oncogenes create a unique landscape of fragile sites. Nat Commun 2015; 6, 7094; PMID:25959793; http://dx.doi.org/10.1038/ncomms8094
  • Miron K, Kerem B. To break or not to break - context matters. Mol Cell Oncol 2016; 3(1):e1072657; PMID:27308576; http://dx.doi.org/10.1080/23723556.2015.1072657
  • Barlow JH, Faryabi RB, Callén E, Wong N, Malhowski A, Chen HT, Gutierrez-Cruz G, Sun HW, McKinnon P, Wright G, et al. Identification of early replicating fragile sites that contribute to genome instability. Cell 2013; 152(3):620-32; PMID:23352430; http://dx.doi.org/10.1016/j.cell.2013.01.006
  • Koundrioukoff S, Carignon S, Técher H, Letessier A, Brison O, Debatisse M. Stepwise activation of the ATR signaling pathway upon increasing replication stress impacts fragile site integrity. PLoS Genet 2013; 9(7):e1003643; PMID:23874235; http://dx.doi.org/10.1371/journal.pgen.1003643
  • Magiera MM, Gueydon E, Schwob E. DNA replication and spindle checkpoints cooperate during S phase to delay mitosis and preserve genome integrity. J Cell Biol 2014; 204(2):165-75; PMID:24421333; http://dx.doi.org/10.1083/jcb.201306023
  • Mankouri HW, Huttner D, Hickson ID. How unfinished business from S-phase affects mitosis and beyond. EMBO J 2013; 32(20):2661-71; PMID:24065128; http://dx.doi.org/10.1038/emboj.2013.211
  • Hossain M, Stillman B. Meier-Gorlin syndrome mutations disrupt an Orc1 CDK inhibitory domain and cause centrosome reduplication. Genes Dev 2012; 26(16):1797-810; PMID:22855792; http://dx.doi.org/10.1101/gad.197178.112
  • Laulier C, Cheng A, Stark JM. The relative efficiency of homology-directed repair has distinct effects on proper anaphase chromosome separation. Nucleic Acids Res 2011; 39(14):5935-44; PMID:21459848; http://dx.doi.org/10.1093/nar/gkr187
  • Wilhelm T, Magdalou I, Barascu A, Técher H, Debatisse M, Lopez BS. Spontaneous slow replication fork progression elicits mitosis alterations in homologous recombination-deficient mammalian cells. Proc Natl Acad Sci U S A 2014; 111(2):763-8; PMID:24347643; http://dx.doi.org/10.1073/pnas.1311520111
  • Gelot C, Magdalou I, Lopez BS. Replication stress in Mammalian cells and its consequences for mitosis. Genes (Basel) 2015; 6(2):267-98; PMID:26010955
  • Kramer A, Mailand N, Lukas C, Syljuåsen RG, Wilkinson CJ, Nigg EA, Bartek J, Lukas J. Centrosome-associated Chk1 prevents premature activation of cyclin-B-Cdk1 kinase. Nat Cell Biol 2004; 6(9):884-91; PMID:15311285; http://dx.doi.org/10.1038/ncb1165
  • Chan KL, Hickson ID. New insights into the formation and resolution of ultra-fine anaphase bridges. Semin Cell Dev Biol 2011; 22(8):906-12; PMID:21782962; http://dx.doi.org/10.1016/j.semcdb.2011.07.001
  • Biebricher A, Hirano S, Enzlin JH, Wiechens N, Streicher WW, Huttner D, Wang LH, Nigg EA, Owen-Hughes T, Liu Y, et al. PICH: a DNA translocase specially adapted for processing anaphase bridge DNA. Mol Cell 2013; 51(5):691-701; PMID:23973328; http://dx.doi.org/10.1016/j.molcel.2013.07.016
  • Germann SM, Schramke V, Pedersen RT, Gallina I, Eckert-Boulet N, Oestergaard VH, Lisby M. TopBP1/Dpb11 binds DNA anaphase bridges to prevent genome instability. J Cell Biol 2014; 204(1):45-59; PMID:24379413; http://dx.doi.org/10.1083/jcb.201305157
  • Liu Y, Nielsen CF, Yao Q, Hickson ID. The origins and processing of ultra fine anaphase DNA bridges. Curr Opin Genet Dev 2014; 26, 1-5; PMID:24795279; http://dx.doi.org/10.1016/j.gde.2014.03.003
  • Nasmyth K, Haering CH. Cohesin: its roles and mechanisms. Annu Rev Genet 2009; 43, 525-58; PMID:19886810; http://dx.doi.org/10.1146/annurev-genet-102108-134233
  • Wang LH, Schwarzbraun T, Speicher MR, Nigg EA. Persistence of DNA threads in human anaphase cells suggests late completion of sister chromatid decatenation. Chromosoma 2008; 117(2):123-35; PMID:17989990; http://dx.doi.org/10.1007/s00412-007-0131-7
  • Wang LH, Mayer B, Stemmann O, Nigg EA. Centromere DNA decatenation depends on cohesin removal and is required for mammalian cell division. J Cell Sci 2010; 123(Pt 5):806-13; PMID:20144989; http://dx.doi.org/10.1242/jcs.058255
  • Barefield C, Karlseder J. The BLM helicase contributes to telomere maintenance through processing of late-replicating intermediate structures. Nucleic Acids Res 2012; 40(15):7358-67; PMID:22576367; http://dx.doi.org/10.1093/nar/gks407
  • d'Alcontres MS, Palacios JA, Mejias D, Blasco MA. TopoIIalpha prevents telomere fragility and formation of ultra thin DNA bridges during mitosis through TRF1-dependent binding to telomeres. Cell Cycle 2014; 13(9):1463-81; PMID:24626180; http://dx.doi.org/10.4161/cc.28419
  • Nera B, Huang HS, Lai T, Xu L. Elevated levels of TRF2 induce telomeric ultrafine anaphase bridges and rapid telomere deletions. Nat Commun 2015; 6, 10132; PMID:26640040; http://dx.doi.org/10.1038/ncomms10132
  • Zaaijer S, Shaikh N, Nageshan RK, Cooper JP. Rif1 Regulates the Fate of DNA Entanglements during Mitosis. Cell Rep 2016; 16(1):148-60; PMID:27320927; http://dx.doi.org/10.1016/j.celrep.2016.05.077
  • Sofueva S, Osman F, Lorenz A, Steinacher R, Castagnetti S, Ledesma J, Whitby MC. Ultrafine anaphase bridges, broken DNA and illegitimate recombination induced by a replication fork barrier. Nucleic Acids Res 2011; 39(15):6568-84; PMID:21576223; http://dx.doi.org/10.1093/nar/gkr340
  • Martinez P, Thanasoula M, Muñoz P, Liao C, Tejera A, McNees C, Flores JM, Fernández-Capetillo O, Tarsounas M, Blasco MA. Increased telomere fragility and fusions resulting from TRF1 deficiency lead to degenerative pathologies and increased cancer in mice. Genes Dev 2009; 23(17):2060-75; PMID:19679647; http://dx.doi.org/10.1101/gad.543509
  • Ke Y, Huh JW, Warrington R, Li B, Wu N, Leng M, Zhang J, Ball HL, Li B, Yu H. PICH and BLM limit histone association with anaphase centromeric DNA threads and promote their resolution. EMBO J 2011; 30(16):3309-21; PMID:21743438; http://dx.doi.org/10.1038/emboj.2011.226
  • Kaulich M, Cubizolles F, Nigg EA. On the regulation, function, and localization of the DNA-dependent ATPase PICH. Chromosoma 2012; 121(4):395-408; PMID:22527115; http://dx.doi.org/10.1007/s00412-012-0370-0
  • Nielsen CF, Huttner D, Bizard AH, Hirano S, Li TN, Palmai-Pallag T, Bjerregaard VA, Liu Y, Nigg EA, Wang LH. PICH promotes sister chromatid disjunction and co-operates with topoisomerase II in mitosis. Nat Commun 2015; 6, 8962; PMID:26643143; http://dx.doi.org/10.1038/ncomms9962
  • Nielsen CF, Hickson ID. PICH promotes mitotic chromosome segregation: Identification of a novel role in rDNA disjunction. Cell Cycle 2016; 15(20):2704-11; PMID:27565185; http://dx.doi.org/10.1080/15384101.2016.1222336
  • Broderick R, Nieminuszczy J, Blackford AN, Winczura A, Niedzwiedz W. TOPBP1 recruits TOP2A to ultra-fine anaphase bridges to aid in their resolution. Nat Commun 2015; 6, 6572; PMID:25762097; http://dx.doi.org/10.1038/ncomms7572
  • Vinciguerra P, Godinho SA, Parmar K, Pellman D, D'Andrea AD. Cytokinesis failure occurs in Fanconi anemia pathway-deficient murine and human bone marrow hematopoietic cells. J Clin Invest 2010; 120(11):3834-42; PMID:20921626; http://dx.doi.org/10.1172/JCI43391
  • Mattarocci S, Hafner L, Lezaja A, Shyian M, Shore D. Rif1: A Conserved Regulator of DNA Replication and Repair Hijacked by Telomeres in Yeasts. Front Genet 2016; 7, 45; PMID:27066066; http://dx.doi.org/10.3389/fgene.2016.00045
  • Hengeveld RC, de Boer HR, Schoonen PM, de Vries EG, Lens SM, van Vugt MA. Rif1 Is Required for Resolution of Ultrafine DNA Bridges in Anaphase to Ensure Genomic Stability. Dev Cell 2015; 34(4):466-74; PMID:26256213; http://dx.doi.org/10.1016/j.devcel.2015.06.014
  • Rodrigue A, Coulombe Y, Jacquet K, Gagné JP, Roques C, Gobeil S, Poirier G, Masson JY. The RAD51 paralogs ensure cellular protection against mitotic defects and aneuploidy. J Cell Sci 2013; 126(Pt 1):348-59; PMID:23108668; http://dx.doi.org/10.1242/jcs.114595
  • Galgoczy DJ, Toczyski DP. Checkpoint adaptation precedes spontaneous and damage-induced genomic instability in yeast. Mol Cell Biol 2001; 21(5):1710-8; PMID:11238908; http://dx.doi.org/10.1128/MCB.21.5.1710-1718.2001
  • Syljuasen RG, Jensen S, Bartek J, Lukas J. Adaptation to the ionizing radiation-induced G2 checkpoint occurs in human cells and depends on checkpoint kinase 1 and Polo-like kinase 1 kinases. Cancer Res 2006; 66(21):10253-7; PMID:17079442; http://dx.doi.org/10.1158/0008-5472.CAN-06-2144
  • Yoo HY, Kumagai A, Shevchenko A, Shevchenko A, Dunphy WG. Adaptation of a DNA replication checkpoint response depends upon inactivation of Claspin by the Polo-like kinase. Cell 2004; 117(5):575-88; PMID:15163406; http://dx.doi.org/10.1016/S0092-8674(04)00417-9
  • Eykelenboom JK, Harte EC, Canavan L, Pastor-Peidro A, Calvo-Asensio I, Llorens-Agost M, Lowndes NF. ATR activates the S-M checkpoint during unperturbed growth to ensure sufficient replication prior to mitotic onset. Cell Rep 2013; 5(4):1095-107; PMID:24268773; http://dx.doi.org/10.1016/j.celrep.2013.10.027
  • Torres-Rosell J, De Piccoli G, Cordon-Preciado V, Farmer S, Jarmuz A, Machin F, Pasero P, Lisby M, Haber JE, Aragón L. Anaphase onset before complete DNA replication with intact checkpoint responses. Science 2007; 315(5817):1411-5; PMID:17347440; http://dx.doi.org/10.1126/science.1134025
  • Bogliolo M, Surralles J. Fanconi anemia: a model disease for studies on human genetics and advanced therapeutics. Curr Opin Genet Dev 2015; 33, 32-40; PMID:26254775; http://dx.doi.org/10.1016/j.gde.2015.07.002
  • Ceccaldi R, Sarangi P, D'Andrea AD. The Fanconi anaemia pathway: new players and new functions. Nat Rev Mol Cell Biol 2016; 17(6):337-49; PMID:27145721; http://dx.doi.org/10.1038/nrm.2016.48
  • Bluteau D, Masliah-Planchon J, Clairmont C, Rousseau A, Ceccaldi R, Dubois d'Enghien C, Bluteau O, Cuccuini W, Gachet S, Peffault de Latour R, et al. Biallelic inactivation of REV7 is associated with Fanconi anemia. J Clin Invest 2016; 126(9):3580-4; PMID:27500492; http://dx.doi.org/10.1172/JCI88010
  • 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(1):106-16; PMID:22789542; http://dx.doi.org/10.1016/j.ccr.2012.05.015
  • Lossaint G, Larroque M, Ribeyre C, Bec N, Larroque C, Décaillet C, Gari K, Constantinou A. FANCD2 binds MCM proteins and controls replisome function upon activation of s phase checkpoint signaling. Mol Cell 2013; 51(5):678-90; PMID:23993743; http://dx.doi.org/10.1016/j.molcel.2013.07.023
  • Sirbu BM, McDonald WH, Dungrawala H, Badu-Nkansah A, Kavanaugh GM, Chen Y, Tabb DL, Cortez D. Identification of proteins at active, stalled, and collapsed replication forks using isolation of proteins on nascent DNA (iPOND) coupled with mass spectrometry. J Biol Chem 2013; 288(44):31458-67; PMID:24047897; http://dx.doi.org/10.1074/jbc.M113.511337
  • Chen YH, Jones MJ, Yin Y, Crist SB, Colnaghi L, Sims RJ 3rd, Rothenberg E, Jallepalli PV, Huang TT. ATR-mediated phosphorylation of FANCI regulates dormant origin firing in response to replication stress. Mol Cell 2015; 58(2):323-38; PMID:25843623; http://dx.doi.org/10.1016/j.molcel.2015.02.031
  • Shigechi T, Tomida J, Sato K, Kobayashi M, Eykelenboom JK, Pessina F, Zhang Y, Uchida E, Ishiai M, Lowndes NF, et al. ATR-ATRIP kinase complex triggers activation of the Fanconi anemia DNA repair pathway. Cancer Res 2012; 72(5):1149-56; PMID:22258451; http://dx.doi.org/10.1158/0008-5472.CAN-11-2904
  • Tomida J, Itaya A, Shigechi T, Unno J, Uchida E, Ikura M, Masuda Y, Matsuda S, Adachi J, Kobayashi M, et al. A novel interplay between the Fanconi anemia core complex and ATR-ATRIP kinase during DNA cross-link repair. Nucleic Acids Res 2013; 41(14):6930-41; PMID:23723247; http://dx.doi.org/10.1093/nar/gkt467
  • Stirling PC, Hieter P. Canonical DNA Repair Pathways Influence R-Loop-Driven Genome Instability. J Mol Biol 2016; in press; PMID:27452366
  • Hatchi E, Skourti-Stathaki K, Ventz S, Pinello L, Yen A, Kamieniarz-Gdula K, Dimitrov S, Pathania S, McKinney KM, Eaton ML, et al. BRCA1 recruitment to transcriptional pause sites is required for R-loop-driven DNA damage repair. Mol Cell 2015; 57(4):636-47; PMID:25699710; http://dx.doi.org/10.1016/j.molcel.2015.01.011
  • Bhatia V, Barroso SI, García-Rubio ML, Tumini E, Herrera-Moyano E, Aguilera A. BRCA2 prevents R-loop accumulation and associates with TREX-2 mRNA export factor PCID2. Nature 2014; 511(7509):362-5; PMID:24896180; http://dx.doi.org/10.1038/nature13374
  • Garcia-Rubio ML, Pérez-Calero C, Barroso SI, Tumini E, Herrera-Moyano E, Rosado IV, Aguilera A. The Fanconi Anemia Pathway Protects Genome Integrity from R-loops. PLoS Genet 2015; 11(11):e1005674; PMID:26584049; http://dx.doi.org/10.1371/journal.pgen.1005674
  • Schwab RA, Nieminuszczy J, Shah F, Langton J, Lopez Martinez D, Liang CC, Cohn MA, Gibbons RJ, Deans AJ, Niedzwiedz W. The Fanconi Anemia Pathway Maintains Genome Stability by Coordinating Replication and Transcription. Mol Cell 2015; 60(3):351-61; PMID:26593718; http://dx.doi.org/10.1016/j.molcel.2015.09.012
  • Howlett NG, Taniguchi T, Durkin SG, D'Andrea AD, Glover TW. The Fanconi anemia pathway is required for the DNA replication stress response and for the regulation of common fragile site stability. Hum Mol Genet 2005; 14(5):693-701; PMID:15661754; http://dx.doi.org/10.1093/hmg/ddi065
  • Madireddy A, Kosiyatrakul ST, Boisvert RA, Herrera-Moyano E, García-Rubio ML, Gerhardt J, Vuono EA, Owen N, Yan Z, Olson S, et al. FANCD2 Facilitates Replication through Common Fragile Sites. Mol Cell 2016; 64(2):388-404; PMID:27768874; http://dx.doi.org/10.1016/j.molcel.2016.09.017
  • Pichierri P, Franchitto A, Rosselli F. BLM and the FANC proteins collaborate in a common pathway in response to stalled replication forks. EMBO J 2004; 23(15):3154-63; PMID:15257300; http://dx.doi.org/10.1038/sj.emboj.7600277
  • Chaudhury I, Sareen A, Raghunandan M, Sobeck A. FANCD2 regulates BLM complex functions independently of FANCI to promote replication fork recovery. Nucleic Acids Res 2013; 41(13):6444-59; PMID:23658231; http://dx.doi.org/10.1093/nar/gkt348
  • Deans AJ, West SC. FANCM connects the genome instability disorders Bloom's Syndrome and Fanconi Anemia. Mol Cell 2009; 36(6):943-53; PMID:20064461; http://dx.doi.org/10.1016/j.molcel.2009.12.006
  • Ciccia A, McDonald N, West SC. Structural and functional relationships of the XPF/MUS81 family of proteins. Annu Rev Biochem 2008; 77, 259-87; PMID:18518821; http://dx.doi.org/10.1146/annurev.biochem.77.070306.102408
  • Hanada K, Budzowska M, Davies SL, van Drunen E, Onizawa H, Beverloo HB, Maas A, Essers J, Hickson ID, Kanaar R. The structure-specific endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nat Struct Mol Biol 2007; 14(11):1096-104; PMID:17934473; http://dx.doi.org/10.1038/nsmb1313
  • Guervilly JH, Takedachi A, Naim V, Scaglione S, Chawhan C, Lovera Y, Despras E, Kuraoka I, Kannouche P, Rosselli F, et al. The SLX4 complex is a SUMO E3 ligase that impacts on replication stress outcome and genome stability. Mol Cell 2015; 57(1):123-37; PMID:25533188; http://dx.doi.org/10.1016/j.molcel.2014.11.014
  • Ouyang J, Garner E, Hallet A, Nguyen HD, Rickman KA, Gill G, Smogorzewska A, Zou L. Noncovalent interactions with SUMO and ubiquitin orchestrate distinct functions of the SLX4 complex in genome maintenance. Mol Cell 2015; 57(1):108-22; PMID:25533185; http://dx.doi.org/10.1016/j.molcel.2014.11.015
  • Kim Y. Nuclease delivery: versatile functions of SLX4/FANCP in genome maintenance. Mol Cells 2014; 37(8):569-74; http://dx.doi.org/10.14348/molcells.2014.0118
  • Bhat A, et al. Rev3, the catalytic subunit of Polzeta, is required for maintaining fragile site stability in human cells. Nucleic Acids Res 2013; 41(4):2328-39; http://dx.doi.org/10.1093/nar/gks1442
  • Luebben SW, Kawabata T, Johnson CS, O'Sullivan MG, Shima N. A concomitant loss of dormant origins and FANCC exacerbates genome instability by impairing DNA replication fork progression. Nucleic Acids Res 2014; 42(9):5605-15; PMID:24589582; http://dx.doi.org/10.1093/nar/gku170
  • Gemble S, Ahuja A, Buhagiar-Labarchède G, Onclercq-Delic R, Dairou J, Biard DS, Lambert S, Lopes M, Amor-Guéret M. Pyrimidine Pool Disequilibrium Induced by a Cytidine Deaminase Deficiency Inhibits PARP-1 Activity, Leading to the Under Replication of DNA. PLoS Genet 2015; 11(7):e1005384; PMID:26181065; http://dx.doi.org/10.1371/journal.pgen.1005384
  • Malkova A, Ira G. Break-induced replication: functions and molecular mechanism. Curr Opin Genet Dev 2013; 23(3):271-9; PMID:23790415; http://dx.doi.org/10.1016/j.gde.2013.05.007
  • Anand RP, Lovett ST, Haber JE. Break-induced DNA replication. Cold Spring Harb Perspect Biol 2013; 5(12):a010397; PMID:23881940; http://dx.doi.org/10.1101/cshperspect.a010397
  • Lydeard JR, Jain S, Yamaguchi M, Haber JE. Break-induced replication and telomerase-independent telomere maintenance require Pol32. Nature 2007; 448(7155):820-3; PMID:17671506; http://dx.doi.org/10.1038/nature06047
  • Costantino L, Sotiriou SK, Rantala JK, Magin S, Mladenov E, Helleday T, Haber JE, Iliakis G, Kallioniemi OP, Halazonetis TD. Break-induced replication repair of damaged forks induces genomic duplications in human cells. Science 2014; 343(6166):88-91; PMID:24310611; http://dx.doi.org/10.1126/science.1243211
  • Lahkim Bennani-Belhaj K, Rouzeau S, Buhagiar-Labarchède G, Chabosseau P, Onclercq-Delic R, Bayart E, Cordelières F, Couturier J, Amor-Guéret M. The Bloom syndrome protein limits the lethality associated with RAD51 deficiency. Mol Cancer Res 2010; 8(3):385-94; PMID:20215422; http://dx.doi.org/10.1158/1541-7786.MCR-09-0534
  • Heijink AM, Krajewska M, van Vugt MA. The DNA damage response during mitosis. Mutat Res 2013; 750(1-2):45-55; PMID:23880065; http://dx.doi.org/10.1016/j.mrfmmm.2013.07.003
  • Giunta S, Belotserkovskaya R, Jackson SP. DNA damage signaling in response to double-strand breaks during mitosis. J Cell Biol 2010; 190(2):197-207; PMID:20660628; http://dx.doi.org/10.1083/jcb.200911156
  • Orthwein A, Fradet-Turcotte A, Noordermeer SM, Canny MD, Brun CM, Strecker J, Escribano-Diaz C, Durocher D. Mitosis inhibits DNA double-strand break repair to guard against telomere fusions. Science 2014; 344(6180):189-93; PMID:24652939; http://dx.doi.org/10.1126/science.1248024
  • 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(5):690-701; PMID:20227372; http://dx.doi.org/10.1016/j.molcel.2010.02.008
  • Matos J, West SC. Holliday junction resolution: regulation in space and time. DNA Repair (Amst) 2014; 19, 176-81; PMID:24767945; http://dx.doi.org/10.1016/j.dnarep.2014.03.013
  • Neelsen KJ, Zanini IM, Herrador R, Lopes M. Oncogenes induce genotoxic stress by mitotic processing of unusual replication intermediates. J Cell Biol 2013; 200(6):699-708; PMID:23479741; http://dx.doi.org/10.1083/jcb.201212058
  • Pardo B, Aguilera A. Complex chromosomal rearrangements mediated by break-induced replication involve structure-selective endonucleases. PLoS Genet 2012; 8(9):e1002979; PMID:23071463; http://dx.doi.org/10.1371/journal.pgen.1002979
  • Ho CK, Mazón G, Lam AF, Symington LS. Mus81 and Yen1 promote reciprocal exchange during mitotic recombination to maintain genome integrity in budding yeast. Mol Cell 2010; 40(6):988-1000; PMID:21172663; http://dx.doi.org/10.1016/j.molcel.2010.11.016
  • Mayle R, et al. DNA REPAIR. Mus81 and converging forks limit the mutagenicity of replication fork breakage. Science 2015; 349(6249):742-7
  • Guervilly JH, Gaillard PH. SLX4 gains weight with SUMO in genome maintenance. Mol Cell Oncol 2016; 3(2):e1008297; PMID:27308578; http://dx.doi.org/10.1080/23723556.2015.1008297
  • Knipscheer P, Räschle M, Smogorzewska A, Enoiu M, Ho TV, Schärer OD, Elledge SJ, Walter JC. The Fanconi anemia pathway promotes replication-dependent DNA interstrand cross-link repair. Science 2009; 326(5960):1698-701; PMID:19965384; http://dx.doi.org/10.1126/science.1182372
  • Waters LS, Minesinger BK, Wiltrout ME, D'Souza S, Woodruff RV, Walker GC. Eukaryotic translesion polymerases and their roles and regulation in DNA damage tolerance. Microbiol Mol Biol Rev 2009; 73(1):134-54; PMID:19258535; http://dx.doi.org/10.1128/MMBR.00034-08
  • Friedberg EC. Suffering in silence: the tolerance of DNA damage. Nat Rev Mol Cell Biol 2005; 6(12):943-53; PMID:16341080; http://dx.doi.org/10.1038/nrm1781
  • Branzei D, Szakal B. DNA damage tolerance by recombination: Molecular pathways and DNA structures. DNA Repair (Amst) 2016; 44, 68-75; PMID:27236213; http://dx.doi.org/10.1016/j.dnarep.2016.05.008
  • Goodman MF, Woodgate R. Translesion DNA polymerases. Cold Spring Harb Perspect Biol 2013; 5(10):a010363; PMID:23838442; http://dx.doi.org/10.1101/cshperspect.a010363
  • Kannouche PL, Wing J, Lehmann AR. Interaction of human DNA polymerase eta with monoubiquitinated PCNA: a possible mechanism for the polymerase switch in response to DNA damage. Mol Cell 2004; 14(4):491-500; PMID:15149598; http://dx.doi.org/10.1016/S1097-2765(04)00259-X
  • Chen X, Bosques L, Sung P, Kupfer GM. A novel role for non-ubiquitinated FANCD2 in response to hydroxyurea-induced DNA damage. Oncogene 2016; 35(1):22-34; PMID:25893307; http://dx.doi.org/10.1038/onc.2015.68
  • Gallina I, Christiansen SK, Pedersen RT, Lisby M, Oestergaard VH. TopBP1-mediated DNA processing during mitosis. Cell Cycle 2016; 15(2):176-83; PMID:26701150; http://dx.doi.org/10.1080/15384101.2015.1128595
  • Boyer AS, Grgurevic S, Cazaux C, Hoffmann JS. The human specialized DNA polymerases and non-B DNA: vital relationships to preserve genome integrity. J Mol Biol 2013; 425(23):4767-81; PMID:24095858; http://dx.doi.org/10.1016/j.jmb.2013.09.022
  • Baranovskiy AG, Lada AG, Siebler HM, Zhang Y, Pavlov YI, Tahirov TH. DNA polymerase delta and zeta switch by sharing accessory subunits of DNA polymerase delta. J Biol Chem 2012; 287(21):17281-7; PMID:22465957; http://dx.doi.org/10.1074/jbc.M112.351122
  • Johnson RE, Prakash L, Prakash S. Pol31 and Pol32 subunits of yeast DNA polymerase delta are also essential subunits of DNA polymerase zeta. Proc Natl Acad Sci U S A 2012; 109(31):12455-60; PMID:22711820; http://dx.doi.org/10.1073/pnas.1206052109
  • Makarova AV, Stodola JL, Burgers PM. A four-subunit DNA polymerase zeta complex containing Pol delta accessory subunits is essential for PCNA-mediated mutagenesis. Nucleic Acids Res 2012; 40(22):11618-26; PMID:23066099; http://dx.doi.org/10.1093/nar/gks948
  • Sakofsky CJ, Ayyar S, Deem AK, Chung WH, Ira G, Malkova A. Translesion Polymerases Drive Microhomology-Mediated Break-Induced Replication Leading to Complex Chromosomal Rearrangements. Mol Cell 2015; 60(6):860-72; PMID:26669261; http://dx.doi.org/10.1016/j.molcel.2015.10.041
  • Casper AM, Nghiem P, Arlt MF, Glover TW. ATR regulates fragile site stability. Cell 2002; 111(6):779-89; PMID:12526805; http://dx.doi.org/10.1016/S0092-8674(02)01113-3
  • Hu CM, Chang ZF. Mitotic control of dTTP pool: a necessity or coincidence? J Biomed Sci 2007; 14(4):491-7; PMID:17525869; http://dx.doi.org/10.1007/s11373-007-9175-1
  • Harris SL, Levine AJ. The p53 pathway: positive and negative feedback loops. Oncogene 2005; 24(17):2899-908; PMID:15838523; http://dx.doi.org/10.1038/sj.onc.1208615
  • Yaswen P, Campisi J. Oncogene-induced senescence pathways weave an intricate tapestry. Cell 2007; 128(2):233-4; PMID:17254959; http://dx.doi.org/10.1016/j.cell.2007.01.005
  • Vitale I, Galluzzi L, Castedo M, Kroemer G. Mitotic catastrophe: a mechanism for avoiding genomic instability. Nat Rev Mol Cell Biol 2011; 12(6):385-92; PMID:21527953; http://dx.doi.org/10.1038/nrm3115
  • Fukasawa K. Oncogenes and tumour suppressors take on centrosomes. Nat Rev Cancer 2007; 7(12):911-24; PMID:18004399; http://dx.doi.org/10.1038/nrc2249
  • Fragkos M, Beard P. Mitotic catastrophe occurs in the absence of apoptosis in p53-null cells with a defective G1 checkpoint. PLoS One 2011; 6(8):e22946; PMID:21853057; http://dx.doi.org/10.1371/journal.pone.0022946
  • Moreno A, Carrington JT, Albergante L, Al Mamun M, Haagensen EJ, Komseli ES, Gorgoulis VG, Newman TJ, Blow JJ. Unreplicated DNA remaining from unperturbed S phases passes through mitosis for resolution in daughter cells. Proc Natl Acad Sci U S A 2016; 113(39):E5757-64; PMID:27516545; http://dx.doi.org/10.1073/pnas.1603252113
  • Ganem NJ, Pellman D. Linking abnormal mitosis to the acquisition of DNA damage. J Cell Biol 2012; 199(6):871-81; PMID:23229895; http://dx.doi.org/10.1083/jcb.201210040
  • Zimmermann M, de Lange T. 53BP1: pro choice in DNA repair. Trends Cell Biol 2014; 24(2):108-17; PMID:24094932; http://dx.doi.org/10.1016/j.tcb.2013.09.003
  • Janssen A, van der Burg M, Szuhai K, Kops GJ, Medema RH. Chromosome segregation errors as a cause of DNA damage and structural chromosome aberrations. Science 2011; 333(6051):1895-8; PMID:21960636; http://dx.doi.org/10.1126/science.1210214
  • Passerini V, Ozeri-Galai E, de Pagter MS, Donnelly N, Schmalbrock S, Kloosterman WP, Kerem B, Storchová Z. The presence of extra chromosomes leads to genomic instability. Nat Commun 2016; 7, 10754; PMID:26876972; http://dx.doi.org/10.1038/ncomms10754
  • Ohashi A, Ohori M, Iwai K, Nakayama Y, Nambu T, Morishita D, Kawamoto T, Miyamoto M, Hirayama T, Okaniwa M, et al. Aneuploidy generates proteotoxic stress and DNA damage concurrently with p53-mediated post-mitotic apoptosis in SAC-impaired cells. Nat Commun 2015; 6, 7668; PMID:26144554; http://dx.doi.org/10.1038/ncomms8668
  • Donnelly N, Storchova Z. Aneuploidy and proteotoxic stress in cancer. Mol Cell Oncol 2015; 2(2):e976491; PMID:27308438; http://dx.doi.org/10.4161/23723556.2014.976491
  • Nicholson JM, Cimini D. Link between aneuploidy and chromosome instability. Int Rev Cell Mol Biol 2015; 315, 299-317; PMID:25708466
  • Fenech M. The in vitro micronucleus technique. Mutat Res 2000; 455(1-2):81-95; PMID:11113469; http://dx.doi.org/10.1016/S0027-5107(00)00065-8
  • Crasta K, Ganem NJ, Dagher R, Lantermann AB, Ivanova EV, Pan Y, Nezi L, Protopopov A, Chowdhury D, Pellman D. DNA breaks and chromosome pulverization from errors in mitosis. Nature 2012; 482(7383):53-8; PMID:22258507; http://dx.doi.org/10.1038/nature10802
  • Norden C, Mendoza M, Dobbelaere J, Kotwaliwale CV, Biggins S, Barral Y. The NoCut pathway links completion of cytokinesis to spindle midzone function to prevent chromosome breakage. Cell 2006; 125(1):85-98; PMID:16615892; http://dx.doi.org/10.1016/j.cell.2006.01.045
  • Mendoza M, Norden C, Durrer K, Rauter H, Uhlmann F, Barral Y. A mechanism for chromosome segregation sensing by the NoCut checkpoint. Nat Cell Biol 2009; 11(4):477-83; PMID:19270692; http://dx.doi.org/10.1038/ncb1855
  • Steigemann P, Wurzenberger C, Schmitz MH, Held M, Guizetti J, Maar S, Gerlich DW. Aurora B-mediated abscission checkpoint protects against tetraploidization. Cell 2009; 136(3):473-84; PMID:19203582; http://dx.doi.org/10.1016/j.cell.2008.12.020
  • Amaral N, Vendrell A, Funaya C, Idrissi FZ, Maier M, Kumar A, Neurohr G, Colomina N, Torres-Rosell J, Geli MI, et al. The Aurora-B-dependent NoCut checkpoint prevents damage of anaphase bridges after DNA replication stress. Nat Cell Biol 2016; 18(5):516-26; PMID:27111841; http://dx.doi.org/10.1038/ncb3343
  • Amaral N, et al. DNA Replication Stress: NoCut to the rescue. Cell Cycle 2017; 16(3):233-234
  • Pampalona J, Roscioli E, Silkworth WT, Bowden B, Genescà A, Tusell L, Cimini D. Chromosome Bridges Maintain Kinetochore-Microtubule Attachment throughout Mitosis and Rarely Break during Anaphase. PLoS One 2016; 11(1):e0147420; PMID:26784746; http://dx.doi.org/10.1371/journal.pone.0147420
  • Shimizu N, Shingaki K, Kaneko-Sasaguri Y, Hashizume T, Kanda T. When, where and how the bridge breaks: anaphase bridge breakage plays a crucial role in gene amplification and HSR generation. Exp Cell Res 2005; 302(2):233-43; PMID:15561104; http://dx.doi.org/10.1016/j.yexcr.2004.09.001
  • Mackay DR, Ullman KS. ATR and a Chk1-Aurora B pathway coordinate postmitotic genome surveillance with cytokinetic abscission. Mol Biol Cell 2015; 26(12):2217-26; PMID:25904336; http://dx.doi.org/10.1091/mbc.E14-11-1563
  • Jasencakova Z, Groth A. Replication stress, a source of epigenetic aberrations in cancer? Bioessays 2010; 32(10):847-55; PMID:20726011; http://dx.doi.org/10.1002/bies.201000055
  • Jasencakova Z, Groth A. Restoring chromatin after replication: how new and old histone marks come together. Semin Cell Dev Biol 2010; 21(2):231-7; PMID:19815085; http://dx.doi.org/10.1016/j.semcdb.2009.09.018
  • Dabin J, Fortuny A, Polo SE. Epigenome Maintenance in Response to DNA Damage. Mol Cell 2016; 62(5):712-27; PMID:27259203; http://dx.doi.org/10.1016/j.molcel.2016.04.006
  • Alabert C, Groth A. Chromatin replication and epigenome maintenance. Nat Rev Mol Cell Biol 2012; 13(3):153-67; PMID:22358331; http://dx.doi.org/10.1038/nrm3288
  • Khurana S, Oberdoerffer P. Replication Stress: A Lifetime of Epigenetic Change. Genes (Basel) 2015; 6(3):858-77; PMID:26378584
  • Sarkies P, Reams C, Simpson LJ, Sale JE. Epigenetic instability due to defective replication of structured DNA. Mol Cell 2010; 40(5):703-13; PMID:21145480; http://dx.doi.org/10.1016/j.molcel.2010.11.009
  • Jasencakova Z, Scharf AN, Ask K, Corpet A, Imhof A, Almouzni G, Groth A. Replication stress interferes with histone recycling and predeposition marking of new histones. Mol Cell 2010; 37(5):736-43; PMID:20227376; http://dx.doi.org/10.1016/j.molcel.2010.01.033
  • Saveliev A, Everett C, Sharpe T, Webster Z, Festenstein R. DNA triplet repeats mediate heterochromatin-protein-1-sensitive variegated gene silencing. Nature 2003; 422(6934):909-13; PMID:12712207; http://dx.doi.org/10.1038/nature01596
  • Nyce J, Liu L, Jones PA. Variable effects of DNA-synthesis inhibitors upon DNA methylation in mammalian cells. Nucleic Acids Res 1986; 14(10):4353-67; PMID:3086840; http://dx.doi.org/10.1093/nar/14.10.4353
  • Tran V, Lim C, Xie J, Chen X, et al. Asymmetric division of Drosophila male germline stem cell shows asymmetric histone distribution. Science 2012; 338(6107):679-82; PMID:23118191; http://dx.doi.org/10.1126/science.1226028
  • Gaillard H, García-Muse T, Aguilera A, et al. Replication stress and cancer. Nat Rev Cancer 2015; 15(5):276-89; PMID:25907220; http://dx.doi.org/10.1038/nrc3916
  • Burrow AA, Williams LE, Pierce LC, Wang YH, et al. Over half of breakpoints in gene pairs involved in cancer-specific recurrent translocations are mapped to human chromosomal fragile sites. BMC Genomics 2009; 10, 59; PMID:19183484; http://dx.doi.org/10.1186/1471-2164-10-59
  • Bignell GR, Greenman CD, Davies H, Butler AP, Edkins S, Andrews JM, Buck G, Chen L, Beare D, Latimer C, et al. Signatures of mutation and selection in the cancer genome. Nature 2010; 463(7283):893-8; PMID:20164919; http://dx.doi.org/10.1038/nature08768
  • Le Tallec B, Millot GA, Blin ME, Brison O, Dutrillaux B, Debatisse M. Common fragile site profiling in epithelial and erythroid cells reveals that most recurrent cancer deletions lie in fragile sites hosting large genes. Cell Rep 2013; 4(3):420-8; PMID:23911288; http://dx.doi.org/10.1016/j.celrep.2013.07.003
  • Macheret M, Halazonetis TD. DNA replication stress as a hallmark of cancer. Annu Rev Pathol 2015; 10, 425-48; PMID:25621662; http://dx.doi.org/10.1146/annurev-pathol-012414-040424
  • Ma K, Qiu L, Mrasek K, Zhang J, Liehr T, Quintana LG, Li Z. Common fragile sites: genomic hotspots of DNA damage and carcinogenesis. Int J Mol Sci 2012; 13(9):11974-99; PMID:23109895; http://dx.doi.org/10.3390/ijms130911974
  • Gao G, Smith DI. Very large common fragile site genes and their potential role in cancer development. Cell Mol Life Sci 2014; 71(23):4601-15; PMID:25300511; http://dx.doi.org/10.1007/s00018-014-1753-6
  • Ohta M, Inoue H, Cotticelli MG, Kastury K, Baffa R, Palazzo J, Siprashvili Z, Mori M, McCue P, Druck T, et al. The FHIT gene, spanning the chromosome 3p14.2 fragile site and renal carcinoma-associated t(3;8) breakpoint, is abnormal in digestive tract cancers. Cell 1996; 84(4):587-97; PMID:8598045; http://dx.doi.org/10.1016/S0092-8674(00)81034-X
  • Waters CE, Saldivar JC, Hosseini SA, Huebner K. The FHIT gene product: tumor suppressor and genome “caretaker.” Cell Mol Life Sci 2014; 71(23):4577-87; PMID:25283145; http://dx.doi.org/10.1007/s00018-014-1722-0
  • Bednarek AK, Keck-Waggoner CL, Daniel RL, Laflin KJ, Bergsagel PL, Kiguchi K, Brenner AJ, Aldaz CM. WWOX, the FRA16D gene, behaves as a suppressor of tumor growth. Cancer Res 2001; 61(22):8068-73; PMID:11719429
  • Aqeilan RI, Croce CM. WWOX in biological control and tumorigenesis. J Cell Physiol 2007; 212(2):307-10; PMID:17458891; http://dx.doi.org/10.1002/jcp.21099
  • Cesari R, Martin ES, Calin GA, Pentimalli F, Bichi R, McAdams H, Trapasso F, Drusco A, Shimizu M, Masciullo V, et al. Parkin, a gene implicated in autosomal recessive juvenile parkinsonism, is a candidate tumor suppressor gene on chromosome 6q25-q27. Proc Natl Acad Sci U S A 2003; 100(10):5956-61; PMID:12719539; http://dx.doi.org/10.1073/pnas.0931262100
  • Gong Y, Zack TI, Morris LG, Lin K, Hukkelhoven E, Raheja R, Tan IL, Turcan S, Veeriah S, Meng S, et al. Pan-cancer genetic analysis identifies PARK2 as a master regulator of G1/S cyclins. Nat Genet 2014; 46(6):588-94; PMID:24793136; http://dx.doi.org/10.1038/ng.2981
  • Coquelle A, Pipiras E, Toledo F, Buttin G, Debatisse M. Expression of fragile sites triggers intrachromosomal mammalian gene amplification and sets boundaries to early amplicons. Cell 1997; 89(2):215-25; PMID:9108477; http://dx.doi.org/10.1016/S0092-8674(00)80201-9
  • Ciullo M, Debily MA, Rozier L, Autiero M, Billault A, Mayau V, El Marhomy S, Guardiola J, Bernheim A, Coullin P, et al. Initiation of the breakage-fusion-bridge mechanism through common fragile site activation in human breast cancer cells: the model of PIP gene duplication from a break at FRA7I. Hum Mol Genet 2002; 11(23):2887-94; PMID:12393800; http://dx.doi.org/10.1093/hmg/11.23.2887
  • Hellman A, Zlotorynski E, Scherer SW, Cheung J, Vincent JB, Smith DI, Trakhtenbrot L, Kerem B. A role for common fragile site induction in amplification of human oncogenes. Cancer Cell 2002; 1(1):89-97; PMID:12086891; http://dx.doi.org/10.1016/S1535-6108(02)00017-X
  • Mazouzi A, Velimezi G, Loizou JI. DNA replication stress: causes, resolution and disease. Exp Cell Res 2014; 329(1):85-93; PMID:25281304; http://dx.doi.org/10.1016/j.yexcr.2014.09.030
  • Constantinou A. Rescue of replication failure by Fanconi anaemia proteins. Chromosoma 2012; 121(1):21-36; PMID:22057367; http://dx.doi.org/10.1007/s00412-011-0349-2
  • Porfirio B, Smeets D, Beckers L, Caporossi D, Tedeschi B, Vernole P, Joenje H, Nicoletti B, Dallapiccola B. Fragile sites and chromosome instability: the distribution of breaks induced by cis-diamine-dichloro-platinum (II) in Fanconi anemia lymphocyte cultures. Hum Genet 1991; 86(3):256-60; PMID:1997377; http://dx.doi.org/10.1007/BF00202404
  • Fundia A, Gorla N, Larripa I. Spontaneous chromosome aberrations in Fanconi's anemia patients are located at fragile sites and acute myeloid leukemia breakpoints. Hereditas 1994; 120(1):47-50; PMID:8206783; http://dx.doi.org/10.1111/j.1601-5223.1994.00047.x
  • Schoder C, Liehr T, Velleuer E, Wilhelm K, Blaurock N, Weise A, Mrasek K. New aspects on chromosomal instability: chromosomal break-points in Fanconi anemia patients co-localize on the molecular level with fragile sites. Int J Oncol 2010; 36(2):307-12; PMID:20043063
  • Filipovic J, Joksić G, Vujić D, Joksić I, Mrasek K, Weise A, Liehr T. First molecular-cytogenetic characterization of Fanconi anemia fragile sites in primary lymphocytes of FA-D2 patients in different stages of the disease. Mol Cytogenet 2016; 9(1):70; PMID:27625703; http://dx.doi.org/10.1186/s13039-016-0280-6
  • Pawlikowska P, Fouchet P, Vainchenker W, Rosselli F, Naim V. Defective endomitosis during megakaryopoiesis leads to thrombocytopenia in Fanca-/- mice. Blood 2014; 124(24):3613-23; PMID:25261197; http://dx.doi.org/10.1182/blood-2014-01-551457
  • Mohaghegh P, Hickson ID. DNA helicase deficiencies associated with cancer predisposition and premature ageing disorders. Hum Mol Genet 2001; 10(7):741-6; PMID:11257107; http://dx.doi.org/10.1093/hmg/10.7.741
  • Pirzio LM, Pichierri P, Bignami M, Franchitto A. Werner syndrome helicase activity is essential in maintaining fragile site stability. J Cell Biol 2008; 180(2):305-14; PMID:18209099; http://dx.doi.org/10.1083/jcb.200705126
  • Wei PC, Chang AN, Kao J, Du Z, Meyers RM, Alt FW, Schwer B. Long Neural Genes Harbor Recurrent DNA Break Clusters in Neural Stem/Progenitor Cells. Cell 2016; 164(4):644-55; PMID:26871630; http://dx.doi.org/10.1016/j.cell.2015.12.039
  • Yuce O, West SC. Senataxin, defective in the neurodegenerative disorder ataxia with oculomotor apraxia 2, lies at the interface of transcription and the DNA damage response. Mol Cell Biol 2013; 33(2):406-17; PMID:23149945; http://dx.doi.org/10.1128/MCB.01195-12
  • Andriani GA, Vijg J, Montagna C. Mechanisms and consequences of aneuploidy and chromosome instability in the aging brain. Mech Ageing Dev 2016; in press; PMID:27013377