ATR-Mediated Global Fork Slowing and Reversal Assist Fork Traverse and Prevent Chromosomal Breakage at DNA Interstrand Cross-Links

Interstrand cross-links (ICLs) are toxic DNA lesions interfering with DNA metabolism that are induced by widely used anticancer drugs. They have long been considered absolute roadblocks for replication forks, implicating complex DNA repair processes at stalled or converging replication forks. Recent...

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Published in:Cell reports (Cambridge) Vol. 24; no. 10; pp. 2629 - 2642.e5
Main Authors: Mutreja, Karun, Krietsch, Jana, Hess, Jeannine, Ursich, Sebastian, Berti, Matteo, Roessler, Fabienne K., Zellweger, Ralph, Patra, Malay, Gasser, Gilles, Lopes, Massimo
Format: Journal Article
Language:English
Published: United States Elsevier Inc 04.09.2018
Cell Press
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ISSN:2211-1247, 2211-1247
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Abstract Interstrand cross-links (ICLs) are toxic DNA lesions interfering with DNA metabolism that are induced by widely used anticancer drugs. They have long been considered absolute roadblocks for replication forks, implicating complex DNA repair processes at stalled or converging replication forks. Recent evidence challenged this view, proposing that single forks traverse ICLs by yet elusive mechanisms. Combining ICL immunolabeling and single-molecule approaches in human cells, we now show that ICL induction leads to global replication fork slowing, involving forks not directly challenged by ICLs. Active fork slowing is linked to rapid recruitment of RAD51 to replicating chromatin and to RAD51/ZRANB3-mediated fork reversal. This global modulation of fork speed and architecture requires ATR activation, promotes single-fork ICL traverse—here, directly visualized by electron microscopy—and prevents chromosomal breakage by untimely ICL processing. We propose that global fork slowing by remodeling provides more time for template repair and promotes bypass of residual lesions, limiting fork-associated processing. [Display omitted] •Fork slowing and reversal are also observed at forks not directly challenged by ICLs•Fork reversal assists ICL traverse and limits DSBs associated with ICL unhooking•ICL traverse can be directly visualized in human cells by electron microscopy•ATR mediates global fork slowing and reversal upon different genotoxic treatments Replication-coupled repair of DNA interstrand cross-links (ICLs) promotes resistance to chemotherapeutic treatments. Visualizing individual lesions and replication intermediates, Mutreja et al. report that forks slow down and reverse both at ICLs and away from lesions. This ATR-mediated response assists lesion bypass during replication and limits chromosomal breakage by fork-associated processing.
AbstractList Graphical Abstract Highlights d Fork slowing and reversal are also observed at forks not directly challenged by ICLs d Fork reversal assists ICL traverse and limits DSBs associated with ICL unhooking d ICL traverse can be directly visualized in human cells by electron microscopy d ATR mediates global fork slowing and reversal upon different genotoxic treatments In Brief Replication-coupled repair of DNA interstrand cross-links (ICLs) promotes resistance to chemotherapeutic treatments. Visualizing individual lesions and replication intermediates, Mutreja et al. report that forks slow down and reverse both at ICLs and away from lesions. This ATR-mediated response assists lesion bypass during replication and limits chromosomal breakage by fork-associated processing.
Interstrand cross-links (ICLs) are toxic DNA lesions interfering with DNA metabolism that are induced by widely used anticancer drugs. They have long been considered absolute roadblocks for replication forks, implicating complex DNA repair processes at stalled or converging replication forks. Recent evidence challenged this view, proposing that single forks traverse ICLs by yet elusive mechanisms. Combining ICL immunolabeling and single-molecule approaches in human cells, we now show that ICL induction leads to global replication fork slowing, involving forks not directly challenged by ICLs. Active fork slowing is linked to rapid recruitment of RAD51 to replicating chromatin and to RAD51/ZRANB3-mediated fork reversal. This global modulation of fork speed and architecture requires ATR activation, promotes single-fork ICL traverse—here, directly visualized by electron microscopy—and prevents chromosomal breakage by untimely ICL processing. We propose that global fork slowing by remodeling provides more time for template repair and promotes bypass of residual lesions, limiting fork-associated processing. : Replication-coupled repair of DNA interstrand cross-links (ICLs) promotes resistance to chemotherapeutic treatments. Visualizing individual lesions and replication intermediates, Mutreja et al. report that forks slow down and reverse both at ICLs and away from lesions. This ATR-mediated response assists lesion bypass during replication and limits chromosomal breakage by fork-associated processing. Keywords: DNA replication, DNA replication stress response, replication fork reversal, fork traverse, DNA interstrand crosslinks, ATR checkpoint, global fork slowing, electron microscopy, ICL immunolabeling
Interstrand cross-links (ICLs) are toxic DNA lesions interfering with DNA metabolism that are induced by widely used anticancer drugs. They have long been considered absolute roadblocks for replication forks, implicating complex DNA repair processes at stalled or converging replication forks. Recent evidence challenged this view, proposing that single forks traverse ICLs by yet elusive mechanisms. Combining ICL immunolabeling and single-molecule approaches in human cells, we now show that ICL induction leads to global replication fork slowing, involving forks not directly challenged by ICLs. Active fork slowing is linked to rapid recruitment of RAD51 to replicating chromatin and to RAD51/ZRANB3-mediated fork reversal. This global modulation of fork speed and architecture requires ATR activation, promotes single-fork ICL traverse—here, directly visualized by electron microscopy—and prevents chromosomal breakage by untimely ICL processing. We propose that global fork slowing by remodeling provides more time for template repair and promotes bypass of residual lesions, limiting fork-associated processing. • Fork slowing and reversal are also observed at forks not directly challenged by ICLs • Fork reversal assists ICL traverse and limits DSBs associated with ICL unhooking • ICL traverse can be directly visualized in human cells by electron microscopy • ATR mediates global fork slowing and reversal upon different genotoxic treatments Replication-coupled repair of DNA interstrand cross-links (ICLs) promotes resistance to chemotherapeutic treatments. Visualizing individual lesions and replication intermediates, Mutreja et al. report that forks slow down and reverse both at ICLs and away from lesions. This ATR-mediated response assists lesion bypass during replication and limits chromosomal breakage by fork-associated processing.
Interstrand cross-links (ICLs) are toxic DNA lesions interfering with DNA metabolism that are induced by widely used anticancer drugs. They have long been considered absolute roadblocks for replication forks, implicating complex DNA repair processes at stalled or converging replication forks. Recent evidence challenged this view, proposing that single forks traverse ICLs by yet elusive mechanisms. Combining ICL immunolabeling and single-molecule approaches in human cells, we now show that ICL induction leads to global replication fork slowing, involving forks not directly challenged by ICLs. Active fork slowing is linked to rapid recruitment of RAD51 to replicating chromatin and to RAD51/ZRANB3-mediated fork reversal. This global modulation of fork speed and architecture requires ATR activation, promotes single-fork ICL traverse—here, directly visualized by electron microscopy—and prevents chromosomal breakage by untimely ICL processing. We propose that global fork slowing by remodeling provides more time for template repair and promotes bypass of residual lesions, limiting fork-associated processing. [Display omitted] •Fork slowing and reversal are also observed at forks not directly challenged by ICLs•Fork reversal assists ICL traverse and limits DSBs associated with ICL unhooking•ICL traverse can be directly visualized in human cells by electron microscopy•ATR mediates global fork slowing and reversal upon different genotoxic treatments Replication-coupled repair of DNA interstrand cross-links (ICLs) promotes resistance to chemotherapeutic treatments. Visualizing individual lesions and replication intermediates, Mutreja et al. report that forks slow down and reverse both at ICLs and away from lesions. This ATR-mediated response assists lesion bypass during replication and limits chromosomal breakage by fork-associated processing.
Interstrand cross-links (ICLs) are toxic DNA lesions interfering with DNA metabolism that are induced by widely used anticancer drugs. They have long been considered absolute roadblocks for replication forks, implicating complex DNA repair processes at stalled or converging replication forks. Recent evidence challenged this view, proposing that single forks traverse ICLs by yet elusive mechanisms. Combining ICL immunolabeling and single-molecule approaches in human cells, we now show that ICL induction leads to global replication fork slowing, involving forks not directly challenged by ICLs. Active fork slowing is linked to rapid recruitment of RAD51 to replicating chromatin and to RAD51/ZRANB3-mediated fork reversal. This global modulation of fork speed and architecture requires ATR activation, promotes single-fork ICL traverse-here, directly visualized by electron microscopy-and prevents chromosomal breakage by untimely ICL processing. We propose that global fork slowing by remodeling provides more time for template repair and promotes bypass of residual lesions, limiting fork-associated processing.Interstrand cross-links (ICLs) are toxic DNA lesions interfering with DNA metabolism that are induced by widely used anticancer drugs. They have long been considered absolute roadblocks for replication forks, implicating complex DNA repair processes at stalled or converging replication forks. Recent evidence challenged this view, proposing that single forks traverse ICLs by yet elusive mechanisms. Combining ICL immunolabeling and single-molecule approaches in human cells, we now show that ICL induction leads to global replication fork slowing, involving forks not directly challenged by ICLs. Active fork slowing is linked to rapid recruitment of RAD51 to replicating chromatin and to RAD51/ZRANB3-mediated fork reversal. This global modulation of fork speed and architecture requires ATR activation, promotes single-fork ICL traverse-here, directly visualized by electron microscopy-and prevents chromosomal breakage by untimely ICL processing. We propose that global fork slowing by remodeling provides more time for template repair and promotes bypass of residual lesions, limiting fork-associated processing.
Interstrand cross-links (ICLs) are toxic DNA lesions interfering with DNA metabolism that are induced by widely used anticancer drugs. They have long been considered absolute roadblocks for replication forks, implicating complex DNA repair processes at stalled or converging replication forks. Recent evidence challenged this view, proposing that single forks traverse ICLs by yet elusive mechanisms. Combining ICL immunolabeling and single-molecule approaches in human cells, we now show that ICL induction leads to global replication fork slowing, involving forks not directly challenged by ICLs. Active fork slowing is linked to rapid recruitment of RAD51 to replicating chromatin and to RAD51/ZRANB3-mediated fork reversal. This global modulation of fork speed and architecture requires ATR activation, promotes single-fork ICL traverse-here, directly visualized by electron microscopy-and prevents chromosomal breakage by untimely ICL processing. We propose that global fork slowing by remodeling provides more time for template repair and promotes bypass of residual lesions, limiting fork-associated processing.
Author Mutreja, Karun
Krietsch, Jana
Hess, Jeannine
Roessler, Fabienne K.
Ursich, Sebastian
Zellweger, Ralph
Gasser, Gilles
Lopes, Massimo
Patra, Malay
Berti, Matteo
AuthorAffiliation 3 Department of Chemistry, University of Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland
1 Institute of Molecular Cancer Research, University of Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland
2 Center for Microscopy and Image Analysis, University of Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland
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Cites_doi 10.1038/nature09373
10.1016/j.tibs.2013.05.004
10.1016/j.molcel.2010.07.005
10.1126/science.1204258
10.15252/embr.201541455
10.1083/jcb.201406099
10.1016/j.molcel.2013.07.023
10.1128/MCB.26.8.3319-3326.2006
10.1016/j.molcel.2008.10.014
10.1016/j.molcel.2005.11.015
10.1016/j.molcel.2014.11.014
10.1016/j.molcel.2015.05.013
10.1038/nrm3935
10.1038/nsmb.2956
10.1038/nature10192
10.1016/j.molcel.2013.09.021
10.1242/jcs.053702
10.1038/nsmb.3163
10.1038/nature09377
10.1021/bc060309t
10.1016/j.dnarep.2014.03.018
10.1128/MCB.01521-12
10.1126/science.aad5634
10.1016/j.molcel.2017.11.022
10.1101/gad.2029711
10.1016/j.cell.2016.09.008
10.1038/nsmb.2501
10.1101/gad.214080.113
10.1128/MCB.02278-06
10.1016/j.celrep.2018.05.061
10.1126/science.1074023
10.1016/j.cell.2013.10.043
10.1021/ac801520m
10.15252/embj.201796664
10.3109/10409238.2012.655374
10.1038/nrm.2016.48
10.1016/j.cell.2008.08.030
10.1016/j.molcel.2012.05.024
10.1016/j.molcel.2014.03.015
10.1016/S1097-2765(02)00799-2
10.1038/nature11863
10.1073/pnas.1005031107
10.1016/j.molcel.2017.08.010
10.1021/bi00625a005
10.1083/jcb.201406100
10.1021/jm301859s
10.1073/pnas.0809350106
10.1083/jcb.201404111
10.1038/emboj.2009.385
10.1016/j.molcel.2014.08.012
10.1126/science.aao3172
10.1016/j.molcel.2012.05.025
10.1016/j.molcel.2014.12.003
10.1016/j.celrep.2015.03.038
10.1038/nrc3088
10.1038/nature09350
10.1007/978-1-4939-7306-4_19
10.1002/ejoc.200300663
10.1016/j.molcel.2007.11.032
10.1038/nrm.2017.67
10.1038/nsmb.2258
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Issue 10
Keywords DNA replication stress response
DNA replication
fork traverse
electron microscopy
ATR checkpoint
replication fork reversal
global fork slowing
DNA interstrand crosslinks
ICL immunolabeling
Language English
License This is an open access article under the CC BY-NC-ND license.
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content type line 23
Lead Contact
Present address: Chimie ParisTech, PSL University, Laboratory for Inorganic Chemical Biology, F-75005 Paris, France
Present address: Department of Chemistry, University of Cambridge, Lensfield Road, Cambridge CB2 1EW, United Kingdom
ORCID 0000-0002-4244-5097
OpenAccessLink https://doaj.org/article/88ea27e76737405085db695ef0f4991f
PMID 30184498
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PublicationCentury 2000
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PublicationDateYYYYMMDD 2018-09-04
PublicationDate_xml – month: 09
  year: 2018
  text: 2018-09-04
  day: 04
PublicationDecade 2010
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PublicationTitle Cell reports (Cambridge)
PublicationTitleAlternate Cell Rep
PublicationYear 2018
Publisher Elsevier Inc
Cell Press
Elsevier
Publisher_xml – name: Elsevier Inc
– name: Cell Press
– name: Elsevier
References Amunugama, Willcox, Wu, Abdullah, El-Sagheer, Brown, McHugh, Griffith, Walter (bib3) 2018; 23
Costanzo, Shechter, Lupardus, Cimprich, Gottesman, Gautier (bib10) 2003; 11
Vassin, Anantha, Sokolova, Kanner, Borowiec (bib54) 2009; 122
Huang, Liu, Bellani, Thazhathveetil, Ling, de Winter, Wang, Wang, Seidman (bib19) 2013; 52
Langevin, Crossan, Rosado, Arends, Patel (bib28) 2011; 475
Saldivar, Cortez, Cimprich (bib42) 2017; 18
Lai, Cao, Hearst, Corash, Luo, Wang (bib27) 2008; 80
Liu, Takeda, Kumar, Westergard, Brown, Pandita, Cheng, Hsieh (bib29) 2010; 467
Petermann, Maya-Mendoza, Zachos, Gillespie, Jackson, Caldecott (bib37) 2006; 26
Semlow, Zhang, Budzowska, Drohat, Walter (bib46) 2016; 167
Braun, Hartnagel, Ravanelli, Schade, Böttcher, Vostrowsky, Hirsch (bib6) 2004; 2004
Somyajit, Basavaraju, Scully, Nagaraju (bib48) 2013; 33
Williams, Gottesman, Gautier (bib56) 2013; 38
Long, Räschle, Joukov, Walter (bib30) 2011; 333
Long, Joukov, Budzowska, Walter (bib31) 2014; 56
Räschle, Knipscheer, Enoiu, Angelov, Sun, Griffith, Ellenberger, Schärer, Walter, Walter (bib40) 2008; 134
Ciccia, Nimonkar, Hu, Hajdu, Achar, Izhar, Petit, Adamson, Yoon, Kowalczykowski (bib8) 2012; 47
Isaacs, Shen, Hearst, Rapoport (bib20) 1977; 16
Zhang, Walter (bib61) 2014; 19
Petermann, Woodcock, Helleday (bib38) 2010; 107
Klein Douwel, Boonen, Long, Szypowska, Räschle, Walter, Knipscheer (bib24) 2014; 54
Ahlskog, Larsen, Achanta, Sørensen (bib2) 2016; 17
Murphy, Fitzgerald, Ro, Kim, Rabinowitsch, Chowdhury, Schildkraut, Borowiec (bib35) 2014; 206
Abdullah, McGouran, Brolih, Ptchelkine, El-Sagheer, Brown, McHugh (bib1) 2017; 36
Thangavel, Berti, Levikova, Pinto, Gomathinayagam, Vujanovic, Zellweger, Moore, Lee, Hendrickson (bib50) 2015; 208
Kottemann, Smogorzewska (bib25) 2013; 493
Schmid, Berti, Walser, Raso, Schmid, Krietsch, Zwicky, Ursich, Freire, Lopes (bib43) 2018; 56
Toledo, Altmeyer, Rask, Lukas, Larsen, Povlsen, Bekker-Jensen, Mailand, Bartek, Lukas (bib53) 2013; 155
Errico, Costanzo (bib13) 2012; 47
Lopez-Mosqueda, Maas, Jonsson, Defazio-Eli, Wohlschlegel, Toczyski (bib33) 2010; 467
Neelsen, Lopes (bib36) 2015; 16
Yuan, Ghosal, Chen (bib57) 2012; 47
Katsuno, Suzuki, Sugimura, Okumura, Zineldeen, Shimada, Niida, Mizuno, Hanaoka, Nakanishi (bib22) 2009; 106
Kile, Chavez, Bacal, Eldirany, Korzhnev, Bezsonova, Eichman, Cimprich (bib23) 2015; 58
Lossaint, Larroque, Ribeyre, Bec, Larroque, Décaillet, Gari, Constantinou (bib34) 2013; 51
Quinet, Lemaçon, Vindigni (bib39) 2017; 68
Berti, Ray Chaudhuri, Thangavel, Gomathinayagam, Kenig, Vujanovic, Odreman, Glatter, Graziano, Mendoza-Maldonado (bib5) 2013; 20
Guervilly, Takedachi, Naim, Scaglione, Chawhan, Lovera, Despras, Kuraoka, Kannouche, Rosselli, Gaillard (bib16) 2015; 57
Thazhathveetil, Liu, Indig, Seidman (bib51) 2007; 18
Lopes, Foiani, Sogo (bib32) 2006; 21
Karnani, Dutta (bib21) 2011; 25
Zellweger, Lopes (bib59) 2018; 1672
Ceccaldi, Sarangi, D’Andrea (bib7) 2016; 17
Gari, Décaillet, Stasiak, Stasiak, Constantinou (bib15) 2008; 29
Zhang, Dewar, Budzowska, Motnenko, Cohn, Walter (bib62) 2015; 22
Vujanovic, Krietsch, Raso, Terraneo, Zellweger, Schmid, Taglialatela, Huang, Holland, Zwicky (bib55) 2017; 67
Zellweger, Dalcher, Mutreja, Berti, Schmid, Herrador, Vindigni, Lopes (bib60) 2015; 208
Berti, Vindigni (bib4) 2016; 23
Collis, Ciccia, Deans, Horejsí, Martin, Maslen, Skehel, Elledge, West, Boulton (bib9) 2008; 32
Lachaud, Moreno, Marchesi, Toth, Blow, Rouse (bib26) 2016; 351
Guo, Kumagai, Schlacher, Shevchenko, Shevchenko, Dunphy (bib17) 2015; 57
Ray Chaudhuri, Hashimoto, Herrador, Neelsen, Fachinetti, Bermejo, Cocito, Costanzo, Lopes (bib41) 2012; 19
Tian, Paramasivam, Ghosal, Chen, Shen, Huang, Akhter, Legerski, Chen, Seidman (bib52) 2015; 10
Sogo, Lopes, Foiani (bib47) 2002; 297
Zegerman, Diffley (bib58) 2010; 467
Huang, Kim, Shiotani, Yang, Zou, D’Andrea (bib18) 2010; 39
Seiler, Conti, Syed, Aladjem, Pommier (bib45) 2007; 27
Foote, Blades, Cronin, Fillery, Guichard, Hassall, Hickson, Jacq, Jewsbury, McGuire (bib14) 2013; 56
Somyajit, Gupta, Sedlackova, Neelsen, Ochs, Rask, Choudhary, Lukas (bib49) 2017; 358
Schwab, Blackford, Niedzwiedz (bib44) 2010; 29
Couch, Bansbach, Driscoll, Luzwick, Glick, Bétous, Carroll, Jung, Qin, Cimprich, Cortez (bib11) 2013; 27
Deans, West (bib12) 2011; 11
Ciccia (10.1016/j.celrep.2018.08.019_bib8) 2012; 47
Foote (10.1016/j.celrep.2018.08.019_bib14) 2013; 56
Berti (10.1016/j.celrep.2018.08.019_bib5) 2013; 20
Huang (10.1016/j.celrep.2018.08.019_bib19) 2013; 52
Long (10.1016/j.celrep.2018.08.019_bib31) 2014; 56
Saldivar (10.1016/j.celrep.2018.08.019_bib42) 2017; 18
Thazhathveetil (10.1016/j.celrep.2018.08.019_bib51) 2007; 18
Zellweger (10.1016/j.celrep.2018.08.019_bib59) 2018; 1672
Somyajit (10.1016/j.celrep.2018.08.019_bib49) 2017; 358
Berti (10.1016/j.celrep.2018.08.019_bib4) 2016; 23
Petermann (10.1016/j.celrep.2018.08.019_bib37) 2006; 26
Kile (10.1016/j.celrep.2018.08.019_bib23) 2015; 58
Lopez-Mosqueda (10.1016/j.celrep.2018.08.019_bib33) 2010; 467
Collis (10.1016/j.celrep.2018.08.019_bib9) 2008; 32
Thangavel (10.1016/j.celrep.2018.08.019_bib50) 2015; 208
Tian (10.1016/j.celrep.2018.08.019_bib52) 2015; 10
Costanzo (10.1016/j.celrep.2018.08.019_bib10) 2003; 11
Huang (10.1016/j.celrep.2018.08.019_bib18) 2010; 39
Lai (10.1016/j.celrep.2018.08.019_bib27) 2008; 80
Lopes (10.1016/j.celrep.2018.08.019_bib32) 2006; 21
Petermann (10.1016/j.celrep.2018.08.019_bib38) 2010; 107
Long (10.1016/j.celrep.2018.08.019_bib30) 2011; 333
Errico (10.1016/j.celrep.2018.08.019_bib13) 2012; 47
Vujanovic (10.1016/j.celrep.2018.08.019_bib55) 2017; 67
Yuan (10.1016/j.celrep.2018.08.019_bib57) 2012; 47
Ceccaldi (10.1016/j.celrep.2018.08.019_bib7) 2016; 17
Zhang (10.1016/j.celrep.2018.08.019_bib61) 2014; 19
Somyajit (10.1016/j.celrep.2018.08.019_bib48) 2013; 33
Williams (10.1016/j.celrep.2018.08.019_bib56) 2013; 38
Langevin (10.1016/j.celrep.2018.08.019_bib28) 2011; 475
Amunugama (10.1016/j.celrep.2018.08.019_bib3) 2018; 23
Seiler (10.1016/j.celrep.2018.08.019_bib45) 2007; 27
Neelsen (10.1016/j.celrep.2018.08.019_bib36) 2015; 16
Karnani (10.1016/j.celrep.2018.08.019_bib21) 2011; 25
Murphy (10.1016/j.celrep.2018.08.019_bib35) 2014; 206
Semlow (10.1016/j.celrep.2018.08.019_bib46) 2016; 167
Deans (10.1016/j.celrep.2018.08.019_bib12) 2011; 11
Quinet (10.1016/j.celrep.2018.08.019_bib39) 2017; 68
Schwab (10.1016/j.celrep.2018.08.019_bib44) 2010; 29
Zegerman (10.1016/j.celrep.2018.08.019_bib58) 2010; 467
Katsuno (10.1016/j.celrep.2018.08.019_bib22) 2009; 106
Zellweger (10.1016/j.celrep.2018.08.019_bib60) 2015; 208
Gari (10.1016/j.celrep.2018.08.019_bib15) 2008; 29
Zhang (10.1016/j.celrep.2018.08.019_bib62) 2015; 22
Räschle (10.1016/j.celrep.2018.08.019_bib40) 2008; 134
Sogo (10.1016/j.celrep.2018.08.019_bib47) 2002; 297
Guervilly (10.1016/j.celrep.2018.08.019_bib16) 2015; 57
Schmid (10.1016/j.celrep.2018.08.019_bib43) 2018; 56
Kottemann (10.1016/j.celrep.2018.08.019_bib25) 2013; 493
Toledo (10.1016/j.celrep.2018.08.019_bib53) 2013; 155
Lachaud (10.1016/j.celrep.2018.08.019_bib26) 2016; 351
Ray Chaudhuri (10.1016/j.celrep.2018.08.019_bib41) 2012; 19
Isaacs (10.1016/j.celrep.2018.08.019_bib20) 1977; 16
Lossaint (10.1016/j.celrep.2018.08.019_bib34) 2013; 51
Vassin (10.1016/j.celrep.2018.08.019_bib54) 2009; 122
Liu (10.1016/j.celrep.2018.08.019_bib29) 2010; 467
Klein Douwel (10.1016/j.celrep.2018.08.019_bib24) 2014; 54
Abdullah (10.1016/j.celrep.2018.08.019_bib1) 2017; 36
Couch (10.1016/j.celrep.2018.08.019_bib11) 2013; 27
Guo (10.1016/j.celrep.2018.08.019_bib17) 2015; 57
Braun (10.1016/j.celrep.2018.08.019_bib6) 2004; 2004
Ahlskog (10.1016/j.celrep.2018.08.019_bib2) 2016; 17
21719678 - Science. 2011 Jul 1;333(6038):84-7
22324461 - Crit Rev Biochem Mol Biol. 2012 May-Jun;47(3):222-35
16387650 - Mol Cell. 2006 Jan 6;21(1):15-27
21406556 - Genes Dev. 2011 Mar 15;25(6):621-33
24726325 - Mol Cell. 2014 May 8;54(3):460-71
20057355 - EMBO J. 2010 Feb 17;29(4):806-18
26840898 - Nat Struct Mol Biol. 2016 Feb;23(2):103-9
25533188 - Mol Cell. 2015 Jan 8;57(1):123-37
28886337 - Mol Cell. 2017 Sep 7;67(5):882-890.e5
12142537 - Science. 2002 Jul 26;297(5581):599-602
30122534 - Mol Cell. 2018 Jul 24;:null
24207054 - Mol Cell. 2013 Nov 7;52(3):434-46
23993743 - Mol Cell. 2013 Sep 12;51(5):678-90
26797144 - Science. 2016 Feb 19;351(6275):846-9
23830640 - Trends Biochem Sci. 2013 Aug;38(8):386-93
23873943 - Genes Dev. 2013 Jul 15;27(14):1610-23
18995830 - Mol Cell. 2008 Nov 7;32(3):313-24
25113031 - J Cell Biol. 2014 Aug 18;206(4):493-507
19843584 - J Cell Sci. 2009 Nov 15;122(Pt 22):4070-80
20805465 - Proc Natl Acad Sci U S A. 2010 Sep 14;107(37):16090-5
27145721 - Nat Rev Mol Cell Biol. 2016 Jun;17(6):337-49
18805090 - Cell. 2008 Sep 19;134(6):969-80
18206976 - Mol Cell. 2008 Jan 18;29(1):141-8
29220651 - Mol Cell. 2017 Dec 7;68(5):830-833
25643322 - Nat Struct Mol Biol. 2015 Mar;22(3):242-7
24768452 - DNA Repair (Amst). 2014 Jul;19:135-42
25219499 - Mol Cell. 2014 Oct 2;56(1):174-85
22388737 - Nat Struct Mol Biol. 2012 Mar 04;19(4):417-23
27693351 - Cell. 2016 Oct 6;167(2):498-511.e14
29043630 - Methods Mol Biol. 2018;1672:261-294
20818375 - Nature. 2010 Sep 16;467(7313):343-6
17373769 - Bioconjug Chem. 2007 Mar-Apr;18(2):431-7
20865002 - Nature. 2010 Sep 23;467(7314):479-83
29924986 - Cell Rep. 2018 Jun 19;23(12):3419-3428
18947205 - Anal Chem. 2008 Nov 15;80(22):8790-8
23325218 - Nature. 2013 Jan 17;493(7432):356-63
16581803 - Mol Cell Biol. 2006 Apr;26(8):3319-26
849407 - Biochemistry. 1977 Mar 22;16(6):1058-64
19221029 - Proc Natl Acad Sci U S A. 2009 Mar 3;106(9):3184-9
20670894 - Mol Cell. 2010 Jul 30;39(2):259-68
23396353 - Nat Struct Mol Biol. 2013 Mar;20(3):347-54
20835227 - Nature. 2010 Sep 23;467(7314):474-8
21734703 - Nature. 2011 Jul 06;475(7354):53-8
25557548 - Mol Cell. 2015 Feb 5;57(3):492-505
22704558 - Mol Cell. 2012 Aug 10;47(3):396-409
29123070 - Science. 2017 Nov 10;358(6364):797-802
17515603 - Mol Cell Biol. 2007 Aug;27(16):5806-18
25733714 - J Cell Biol. 2015 Mar 2;208(5):563-79
23394205 - J Med Chem. 2013 Mar 14;56(5):2125-38
27113759 - EMBO Rep. 2016 May;17(5):671-81
12535533 - Mol Cell. 2003 Jan;11(1):203-13
21701511 - Nat Rev Cancer. 2011 Jun 24;11(7):467-80
22705370 - Mol Cell. 2012 Aug 10;47(3):410-21
25733713 - J Cell Biol. 2015 Mar 2;208(5):545-62
25714681 - Nat Rev Mol Cell Biol. 2015 Apr;16(4):207-20
28607004 - EMBO J. 2017 Jul 14;36(14):2047-2060
26051180 - Mol Cell. 2015 Jun 18;58(6):1090-100
23438602 - Mol Cell Biol. 2013 May;33(9):1830-44
28811666 - Nat Rev Mol Cell Biol. 2017 Oct;18(10):622-636
24267891 - Cell. 2013 Nov 21;155(5):1088-103
25818288 - Cell Rep. 2015 Mar 31;10(12):1957-66
References_xml – volume: 467
  start-page: 343
  year: 2010
  end-page: 346
  ident: bib29
  article-title: Phosphorylation of MLL by ATR is required for execution of mammalian S-phase checkpoint
  publication-title: Nature
– volume: 21
  start-page: 15
  year: 2006
  end-page: 27
  ident: bib32
  article-title: Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions
  publication-title: Mol. Cell
– volume: 29
  start-page: 806
  year: 2010
  end-page: 818
  ident: bib44
  article-title: ATR activation and replication fork restart are defective in FANCM-deficient cells
  publication-title: EMBO J.
– volume: 67
  start-page: 882
  year: 2017
  end-page: 890.e5
  ident: bib55
  article-title: Replication fork slowing and reversal upon DNA damage require PCNA polyubiquitination and ZRANB3 DNA translocase activity
  publication-title: Mol. Cell
– volume: 47
  start-page: 396
  year: 2012
  end-page: 409
  ident: bib8
  article-title: Polyubiquitinated PCNA recruits the ZRANB3 translocase to maintain genomic integrity after replication stress
  publication-title: Mol. Cell
– volume: 57
  start-page: 492
  year: 2015
  end-page: 505
  ident: bib17
  article-title: Interaction of Chk1 with Treslin negatively regulates the initiation of chromosomal DNA replication
  publication-title: Mol. Cell
– volume: 23
  start-page: 3419
  year: 2018
  end-page: 3428
  ident: bib3
  article-title: Replication fork reversal during DNA interstrand crosslink repair requires CMG unloading
  publication-title: Cell Rep.
– volume: 52
  start-page: 434
  year: 2013
  end-page: 446
  ident: bib19
  article-title: The DNA translocase FANCM/MHF promotes replication traverse of DNA interstrand crosslinks
  publication-title: Mol. Cell
– volume: 493
  start-page: 356
  year: 2013
  end-page: 363
  ident: bib25
  article-title: Fanconi anaemia and the repair of Watson and Crick DNA crosslinks
  publication-title: Nature
– volume: 27
  start-page: 1610
  year: 2013
  end-page: 1623
  ident: bib11
  article-title: ATR phosphorylates SMARCAL1 to prevent replication fork collapse
  publication-title: Genes Dev.
– volume: 33
  start-page: 1830
  year: 2013
  end-page: 1844
  ident: bib48
  article-title: ATM- and ATR-mediated phosphorylation of XRCC3 regulates DNA double-strand break-induced checkpoint activation and repair
  publication-title: Mol. Cell. Biol.
– volume: 208
  start-page: 563
  year: 2015
  end-page: 579
  ident: bib60
  article-title: Rad51-mediated replication fork reversal is a global response to genotoxic treatments in human cells
  publication-title: J. Cell Biol.
– volume: 22
  start-page: 242
  year: 2015
  end-page: 247
  ident: bib62
  article-title: DNA interstrand cross-link repair requires replication-fork convergence
  publication-title: Nat. Struct. Mol. Biol.
– volume: 32
  start-page: 313
  year: 2008
  end-page: 324
  ident: bib9
  article-title: FANCM and FAAP24 function in ATR-mediated checkpoint signaling independently of the Fanconi anemia core complex
  publication-title: Mol. Cell
– volume: 297
  start-page: 599
  year: 2002
  end-page: 602
  ident: bib47
  article-title: Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects
  publication-title: Science
– volume: 155
  start-page: 1088
  year: 2013
  end-page: 1103
  ident: bib53
  article-title: ATR prohibits replication catastrophe by preventing global exhaustion of RPA
  publication-title: Cell
– volume: 23
  start-page: 103
  year: 2016
  end-page: 109
  ident: bib4
  article-title: Replication stress: getting back on track
  publication-title: Nat. Struct. Mol. Biol.
– volume: 467
  start-page: 479
  year: 2010
  end-page: 483
  ident: bib33
  article-title: Damage-induced phosphorylation of Sld3 is important to block late origin firing
  publication-title: Nature
– volume: 29
  start-page: 141
  year: 2008
  end-page: 148
  ident: bib15
  article-title: The Fanconi anemia protein FANCM can promote branch migration of Holliday junctions and replication forks
  publication-title: Mol. Cell
– volume: 333
  start-page: 84
  year: 2011
  end-page: 87
  ident: bib30
  article-title: Mechanism of RAD51-dependent DNA interstrand cross-link repair
  publication-title: Science
– volume: 39
  start-page: 259
  year: 2010
  end-page: 268
  ident: bib18
  article-title: The FANCM/FAAP24 complex is required for the DNA interstrand crosslink-induced checkpoint response
  publication-title: Mol. Cell
– volume: 58
  start-page: 1090
  year: 2015
  end-page: 1100
  ident: bib23
  article-title: HLTF’s ancient HIRAN domain binds 3′ DNA ends to drive replication fork reversal
  publication-title: Mol. Cell
– volume: 80
  start-page: 8790
  year: 2008
  end-page: 8798
  ident: bib27
  article-title: Quantitative analysis of DNA interstrand cross-links and monoadducts formed in human cells induced by psoralens and UVA irradiation
  publication-title: Anal. Chem.
– volume: 47
  start-page: 410
  year: 2012
  end-page: 421
  ident: bib57
  article-title: The HARP-like domain-containing protein AH2/ZRANB3 binds to PCNA and participates in cellular response to replication stress
  publication-title: Mol. Cell
– volume: 56
  start-page: 2125
  year: 2013
  end-page: 2138
  ident: bib14
  article-title: Discovery of 4-4-[(3
  publication-title: J. Med. Chem.
– volume: 16
  start-page: 1058
  year: 1977
  end-page: 1064
  ident: bib20
  article-title: Synthesis and characterization of new psoralen derivatives with superior photoreactivity with DNA and RNA
  publication-title: Biochemistry
– volume: 51
  start-page: 678
  year: 2013
  end-page: 690
  ident: bib34
  article-title: FANCD2 binds MCM proteins and controls replisome function upon activation of S phase checkpoint signaling
  publication-title: Mol. Cell
– volume: 10
  start-page: 1957
  year: 2015
  end-page: 1966
  ident: bib52
  article-title: UHRF1 contributes to DNA damage repair as a lesion recognition factor and nuclease scaffold
  publication-title: Cell Rep.
– volume: 475
  start-page: 53
  year: 2011
  end-page: 58
  ident: bib28
  article-title: Fancd2 counteracts the toxic effects of naturally produced aldehydes in mice
  publication-title: Nature
– volume: 56
  start-page: 92
  year: 2018
  end-page: 101
  ident: bib43
  article-title: Histone ubiquitination by the DNA damage response is Histone ubiquitination by the DNA damage response is required for efficient DNA replication in unperturbed S-phase
  publication-title: Mol. Cell
– volume: 122
  start-page: 4070
  year: 2009
  end-page: 4080
  ident: bib54
  article-title: Human RPA phosphorylation by ATR stimulates DNA synthesis and prevents ssDNA accumulation during DNA-replication stress
  publication-title: J. Cell Sci.
– volume: 467
  start-page: 474
  year: 2010
  end-page: 478
  ident: bib58
  article-title: Checkpoint-dependent inhibition of DNA replication initiation by Sld3 and Dbf4 phosphorylation
  publication-title: Nature
– volume: 36
  start-page: 2047
  year: 2017
  end-page: 2060
  ident: bib1
  article-title: RPA activates the XPF-ERCC1 endonuclease to initiate processing of DNA interstrand crosslinks
  publication-title: EMBO J.
– volume: 11
  start-page: 203
  year: 2003
  end-page: 213
  ident: bib10
  article-title: An ATR- and Cdc7-dependent DNA damage checkpoint that inhibits initiation of DNA replication
  publication-title: Mol. Cell
– volume: 17
  start-page: 337
  year: 2016
  end-page: 349
  ident: bib7
  article-title: The Fanconi anaemia pathway: new players and new functions
  publication-title: Nat. Rev. Mol. Cell Biol.
– volume: 38
  start-page: 386
  year: 2013
  end-page: 393
  ident: bib56
  article-title: The differences between ICL repair during and outside of S phase
  publication-title: Trends Biochem. Sci.
– volume: 17
  start-page: 671
  year: 2016
  end-page: 681
  ident: bib2
  article-title: ATM/ATR-mediated phosphorylation of PALB2 promotes RAD51 function
  publication-title: EMBO Rep.
– volume: 134
  start-page: 969
  year: 2008
  end-page: 980
  ident: bib40
  article-title: Mechanism of replication-coupled DNA interstrand crosslink repair
  publication-title: Cell
– volume: 167
  start-page: 498
  year: 2016
  end-page: 511.e14
  ident: bib46
  article-title: Replication-dependent unhooking of DNA interstrand cross-links by the NEIL3 glycosylase
  publication-title: Cell
– volume: 1672
  start-page: 261
  year: 2018
  end-page: 294
  ident: bib59
  article-title: Dynamic architecture of eukaryotic DNA replication forks in vivo, visualized by electron microscopy
  publication-title: Methods Mol. Biol.
– volume: 106
  start-page: 3184
  year: 2009
  end-page: 3189
  ident: bib22
  article-title: Cyclin A-Cdk1 regulates the origin firing program in mammalian cells
  publication-title: Proc. Natl. Acad. Sci. USA
– volume: 26
  start-page: 3319
  year: 2006
  end-page: 3326
  ident: bib37
  article-title: Chk1 requirement for high global rates of replication fork progression during normal vertebrate S phase
  publication-title: Mol. Cell. Biol.
– volume: 68
  start-page: 830
  year: 2017
  end-page: 833
  ident: bib39
  article-title: Replication fork reversal: players and guardians
  publication-title: Mol. Cell
– volume: 47
  start-page: 222
  year: 2012
  end-page: 235
  ident: bib13
  article-title: Mechanisms of replication fork protection: a safeguard for genome stability
  publication-title: Crit. Rev. Biochem. Mol. Biol.
– volume: 107
  start-page: 16090
  year: 2010
  end-page: 16095
  ident: bib38
  article-title: Chk1 promotes replication fork progression by controlling replication initiation
  publication-title: Proc. Natl. Acad. Sci. USA
– volume: 11
  start-page: 467
  year: 2011
  end-page: 480
  ident: bib12
  article-title: DNA interstrand crosslink repair and cancer
  publication-title: Nat. Rev. Cancer
– volume: 27
  start-page: 5806
  year: 2007
  end-page: 5818
  ident: bib45
  article-title: The intra-S-phase checkpoint affects both DNA replication initiation and elongation: single-cell and -DNA fiber analyses
  publication-title: Mol. Cell. Biol.
– volume: 57
  start-page: 123
  year: 2015
  end-page: 137
  ident: bib16
  article-title: The SLX4 complex is a SUMO E3 ligase that impacts on replication stress outcome and genome stability
  publication-title: Mol. Cell
– volume: 20
  start-page: 347
  year: 2013
  end-page: 354
  ident: bib5
  article-title: Human RECQ1 promotes restart of replication forks reversed by DNA topoisomerase I inhibition
  publication-title: Nat. Struct. Mol. Biol.
– volume: 208
  start-page: 545
  year: 2015
  end-page: 562
  ident: bib50
  article-title: DNA2 drives processing and restart of reversed replication forks in human cells
  publication-title: J. Cell Biol.
– volume: 18
  start-page: 431
  year: 2007
  end-page: 437
  ident: bib51
  article-title: Psoralen conjugates for visualization of genomic interstrand cross-links localized by laser photoactivation
  publication-title: Bioconjug. Chem.
– volume: 25
  start-page: 621
  year: 2011
  end-page: 633
  ident: bib21
  article-title: The effect of the intra-S-phase checkpoint on origins of replication in human cells
  publication-title: Genes Dev.
– volume: 358
  start-page: 797
  year: 2017
  end-page: 802
  ident: bib49
  article-title: Redox-sensitive alteration of replisome architecture safeguards genome integrity
  publication-title: Science
– volume: 206
  start-page: 493
  year: 2014
  end-page: 507
  ident: bib35
  article-title: Phosphorylated RPA recruits PALB2 to stalled DNA replication forks to facilitate fork recovery
  publication-title: J. Cell Biol.
– volume: 56
  start-page: 174
  year: 2014
  end-page: 185
  ident: bib31
  article-title: BRCA1 promotes unloading of the CMG helicase from a stalled DNA replication fork
  publication-title: Mol. Cell
– volume: 19
  start-page: 417
  year: 2012
  end-page: 423
  ident: bib41
  article-title: Topoisomerase I poisoning results in PARP-mediated replication fork reversal
  publication-title: Nat. Struct. Mol. Biol.
– volume: 351
  start-page: 846
  year: 2016
  end-page: 849
  ident: bib26
  article-title: Ubiquitinated Fancd2 recruits Fan1 to stalled replication forks to prevent genome instability
  publication-title: Science
– volume: 18
  start-page: 622
  year: 2017
  end-page: 636
  ident: bib42
  article-title: The essential kinase ATR: ensuring faithful duplication of a challenging genome
  publication-title: Nat. Rev. Mol. Cell Biol.
– volume: 2004
  start-page: 1983
  year: 2004
  end-page: 2001
  ident: bib6
  article-title: Amphiphilic [5:1]- and [3:3]-hexakisadducts of C60
  publication-title: Eur. J. Org. Chem.
– volume: 54
  start-page: 460
  year: 2014
  end-page: 471
  ident: bib24
  article-title: XPF-ERCC1 acts in unhooking DNA interstrand crosslinks in cooperation with FANCD2 and FANCP/SLX4
  publication-title: Mol. Cell
– volume: 19
  start-page: 135
  year: 2014
  end-page: 142
  ident: bib61
  article-title: Mechanism and regulation of incisions during DNA interstrand cross-link repair
  publication-title: DNA Repair (Amst.)
– volume: 16
  start-page: 207
  year: 2015
  end-page: 220
  ident: bib36
  article-title: Replication fork reversal in eukaryotes: from dead end to dynamic response
  publication-title: Nat. Rev. Mol. Cell Biol.
– volume: 467
  start-page: 474
  year: 2010
  ident: 10.1016/j.celrep.2018.08.019_bib58
  article-title: Checkpoint-dependent inhibition of DNA replication initiation by Sld3 and Dbf4 phosphorylation
  publication-title: Nature
  doi: 10.1038/nature09373
– volume: 56
  start-page: 92
  year: 2018
  ident: 10.1016/j.celrep.2018.08.019_bib43
  article-title: Histone ubiquitination by the DNA damage response is Histone ubiquitination by the DNA damage response is required for efficient DNA replication in unperturbed S-phase
  publication-title: Mol. Cell
– volume: 38
  start-page: 386
  year: 2013
  ident: 10.1016/j.celrep.2018.08.019_bib56
  article-title: The differences between ICL repair during and outside of S phase
  publication-title: Trends Biochem. Sci.
  doi: 10.1016/j.tibs.2013.05.004
– volume: 39
  start-page: 259
  year: 2010
  ident: 10.1016/j.celrep.2018.08.019_bib18
  article-title: The FANCM/FAAP24 complex is required for the DNA interstrand crosslink-induced checkpoint response
  publication-title: Mol. Cell
  doi: 10.1016/j.molcel.2010.07.005
– volume: 333
  start-page: 84
  year: 2011
  ident: 10.1016/j.celrep.2018.08.019_bib30
  article-title: Mechanism of RAD51-dependent DNA interstrand cross-link repair
  publication-title: Science
  doi: 10.1126/science.1204258
– volume: 17
  start-page: 671
  year: 2016
  ident: 10.1016/j.celrep.2018.08.019_bib2
  article-title: ATM/ATR-mediated phosphorylation of PALB2 promotes RAD51 function
  publication-title: EMBO Rep.
  doi: 10.15252/embr.201541455
– volume: 208
  start-page: 563
  year: 2015
  ident: 10.1016/j.celrep.2018.08.019_bib60
  article-title: Rad51-mediated replication fork reversal is a global response to genotoxic treatments in human cells
  publication-title: J. Cell Biol.
  doi: 10.1083/jcb.201406099
– volume: 51
  start-page: 678
  year: 2013
  ident: 10.1016/j.celrep.2018.08.019_bib34
  article-title: FANCD2 binds MCM proteins and controls replisome function upon activation of S phase checkpoint signaling
  publication-title: Mol. Cell
  doi: 10.1016/j.molcel.2013.07.023
– volume: 26
  start-page: 3319
  year: 2006
  ident: 10.1016/j.celrep.2018.08.019_bib37
  article-title: Chk1 requirement for high global rates of replication fork progression during normal vertebrate S phase
  publication-title: Mol. Cell. Biol.
  doi: 10.1128/MCB.26.8.3319-3326.2006
– volume: 32
  start-page: 313
  year: 2008
  ident: 10.1016/j.celrep.2018.08.019_bib9
  article-title: FANCM and FAAP24 function in ATR-mediated checkpoint signaling independently of the Fanconi anemia core complex
  publication-title: Mol. Cell
  doi: 10.1016/j.molcel.2008.10.014
– volume: 21
  start-page: 15
  year: 2006
  ident: 10.1016/j.celrep.2018.08.019_bib32
  article-title: Multiple mechanisms control chromosome integrity after replication fork uncoupling and restart at irreparable UV lesions
  publication-title: Mol. Cell
  doi: 10.1016/j.molcel.2005.11.015
– volume: 57
  start-page: 123
  year: 2015
  ident: 10.1016/j.celrep.2018.08.019_bib16
  article-title: The SLX4 complex is a SUMO E3 ligase that impacts on replication stress outcome and genome stability
  publication-title: Mol. Cell
  doi: 10.1016/j.molcel.2014.11.014
– volume: 58
  start-page: 1090
  year: 2015
  ident: 10.1016/j.celrep.2018.08.019_bib23
  article-title: HLTF’s ancient HIRAN domain binds 3′ DNA ends to drive replication fork reversal
  publication-title: Mol. Cell
  doi: 10.1016/j.molcel.2015.05.013
– volume: 16
  start-page: 207
  year: 2015
  ident: 10.1016/j.celrep.2018.08.019_bib36
  article-title: Replication fork reversal in eukaryotes: from dead end to dynamic response
  publication-title: Nat. Rev. Mol. Cell Biol.
  doi: 10.1038/nrm3935
– volume: 22
  start-page: 242
  year: 2015
  ident: 10.1016/j.celrep.2018.08.019_bib62
  article-title: DNA interstrand cross-link repair requires replication-fork convergence
  publication-title: Nat. Struct. Mol. Biol.
  doi: 10.1038/nsmb.2956
– volume: 475
  start-page: 53
  year: 2011
  ident: 10.1016/j.celrep.2018.08.019_bib28
  article-title: Fancd2 counteracts the toxic effects of naturally produced aldehydes in mice
  publication-title: Nature
  doi: 10.1038/nature10192
– volume: 52
  start-page: 434
  year: 2013
  ident: 10.1016/j.celrep.2018.08.019_bib19
  article-title: The DNA translocase FANCM/MHF promotes replication traverse of DNA interstrand crosslinks
  publication-title: Mol. Cell
  doi: 10.1016/j.molcel.2013.09.021
– volume: 122
  start-page: 4070
  year: 2009
  ident: 10.1016/j.celrep.2018.08.019_bib54
  article-title: Human RPA phosphorylation by ATR stimulates DNA synthesis and prevents ssDNA accumulation during DNA-replication stress
  publication-title: J. Cell Sci.
  doi: 10.1242/jcs.053702
– volume: 23
  start-page: 103
  year: 2016
  ident: 10.1016/j.celrep.2018.08.019_bib4
  article-title: Replication stress: getting back on track
  publication-title: Nat. Struct. Mol. Biol.
  doi: 10.1038/nsmb.3163
– volume: 467
  start-page: 479
  year: 2010
  ident: 10.1016/j.celrep.2018.08.019_bib33
  article-title: Damage-induced phosphorylation of Sld3 is important to block late origin firing
  publication-title: Nature
  doi: 10.1038/nature09377
– volume: 18
  start-page: 431
  year: 2007
  ident: 10.1016/j.celrep.2018.08.019_bib51
  article-title: Psoralen conjugates for visualization of genomic interstrand cross-links localized by laser photoactivation
  publication-title: Bioconjug. Chem.
  doi: 10.1021/bc060309t
– volume: 19
  start-page: 135
  year: 2014
  ident: 10.1016/j.celrep.2018.08.019_bib61
  article-title: Mechanism and regulation of incisions during DNA interstrand cross-link repair
  publication-title: DNA Repair (Amst.)
  doi: 10.1016/j.dnarep.2014.03.018
– volume: 33
  start-page: 1830
  year: 2013
  ident: 10.1016/j.celrep.2018.08.019_bib48
  article-title: ATM- and ATR-mediated phosphorylation of XRCC3 regulates DNA double-strand break-induced checkpoint activation and repair
  publication-title: Mol. Cell. Biol.
  doi: 10.1128/MCB.01521-12
– volume: 351
  start-page: 846
  year: 2016
  ident: 10.1016/j.celrep.2018.08.019_bib26
  article-title: Ubiquitinated Fancd2 recruits Fan1 to stalled replication forks to prevent genome instability
  publication-title: Science
  doi: 10.1126/science.aad5634
– volume: 68
  start-page: 830
  year: 2017
  ident: 10.1016/j.celrep.2018.08.019_bib39
  article-title: Replication fork reversal: players and guardians
  publication-title: Mol. Cell
  doi: 10.1016/j.molcel.2017.11.022
– volume: 25
  start-page: 621
  year: 2011
  ident: 10.1016/j.celrep.2018.08.019_bib21
  article-title: The effect of the intra-S-phase checkpoint on origins of replication in human cells
  publication-title: Genes Dev.
  doi: 10.1101/gad.2029711
– volume: 167
  start-page: 498
  year: 2016
  ident: 10.1016/j.celrep.2018.08.019_bib46
  article-title: Replication-dependent unhooking of DNA interstrand cross-links by the NEIL3 glycosylase
  publication-title: Cell
  doi: 10.1016/j.cell.2016.09.008
– volume: 20
  start-page: 347
  year: 2013
  ident: 10.1016/j.celrep.2018.08.019_bib5
  article-title: Human RECQ1 promotes restart of replication forks reversed by DNA topoisomerase I inhibition
  publication-title: Nat. Struct. Mol. Biol.
  doi: 10.1038/nsmb.2501
– volume: 27
  start-page: 1610
  year: 2013
  ident: 10.1016/j.celrep.2018.08.019_bib11
  article-title: ATR phosphorylates SMARCAL1 to prevent replication fork collapse
  publication-title: Genes Dev.
  doi: 10.1101/gad.214080.113
– volume: 27
  start-page: 5806
  year: 2007
  ident: 10.1016/j.celrep.2018.08.019_bib45
  article-title: The intra-S-phase checkpoint affects both DNA replication initiation and elongation: single-cell and -DNA fiber analyses
  publication-title: Mol. Cell. Biol.
  doi: 10.1128/MCB.02278-06
– volume: 23
  start-page: 3419
  year: 2018
  ident: 10.1016/j.celrep.2018.08.019_bib3
  article-title: Replication fork reversal during DNA interstrand crosslink repair requires CMG unloading
  publication-title: Cell Rep.
  doi: 10.1016/j.celrep.2018.05.061
– volume: 297
  start-page: 599
  year: 2002
  ident: 10.1016/j.celrep.2018.08.019_bib47
  article-title: Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects
  publication-title: Science
  doi: 10.1126/science.1074023
– volume: 155
  start-page: 1088
  year: 2013
  ident: 10.1016/j.celrep.2018.08.019_bib53
  article-title: ATR prohibits replication catastrophe by preventing global exhaustion of RPA
  publication-title: Cell
  doi: 10.1016/j.cell.2013.10.043
– volume: 80
  start-page: 8790
  year: 2008
  ident: 10.1016/j.celrep.2018.08.019_bib27
  article-title: Quantitative analysis of DNA interstrand cross-links and monoadducts formed in human cells induced by psoralens and UVA irradiation
  publication-title: Anal. Chem.
  doi: 10.1021/ac801520m
– volume: 36
  start-page: 2047
  year: 2017
  ident: 10.1016/j.celrep.2018.08.019_bib1
  article-title: RPA activates the XPF-ERCC1 endonuclease to initiate processing of DNA interstrand crosslinks
  publication-title: EMBO J.
  doi: 10.15252/embj.201796664
– volume: 47
  start-page: 222
  year: 2012
  ident: 10.1016/j.celrep.2018.08.019_bib13
  article-title: Mechanisms of replication fork protection: a safeguard for genome stability
  publication-title: Crit. Rev. Biochem. Mol. Biol.
  doi: 10.3109/10409238.2012.655374
– volume: 17
  start-page: 337
  year: 2016
  ident: 10.1016/j.celrep.2018.08.019_bib7
  article-title: The Fanconi anaemia pathway: new players and new functions
  publication-title: Nat. Rev. Mol. Cell Biol.
  doi: 10.1038/nrm.2016.48
– volume: 134
  start-page: 969
  year: 2008
  ident: 10.1016/j.celrep.2018.08.019_bib40
  article-title: Mechanism of replication-coupled DNA interstrand crosslink repair
  publication-title: Cell
  doi: 10.1016/j.cell.2008.08.030
– volume: 47
  start-page: 396
  year: 2012
  ident: 10.1016/j.celrep.2018.08.019_bib8
  article-title: Polyubiquitinated PCNA recruits the ZRANB3 translocase to maintain genomic integrity after replication stress
  publication-title: Mol. Cell
  doi: 10.1016/j.molcel.2012.05.024
– volume: 54
  start-page: 460
  year: 2014
  ident: 10.1016/j.celrep.2018.08.019_bib24
  article-title: XPF-ERCC1 acts in unhooking DNA interstrand crosslinks in cooperation with FANCD2 and FANCP/SLX4
  publication-title: Mol. Cell
  doi: 10.1016/j.molcel.2014.03.015
– volume: 11
  start-page: 203
  year: 2003
  ident: 10.1016/j.celrep.2018.08.019_bib10
  article-title: An ATR- and Cdc7-dependent DNA damage checkpoint that inhibits initiation of DNA replication
  publication-title: Mol. Cell
  doi: 10.1016/S1097-2765(02)00799-2
– volume: 493
  start-page: 356
  year: 2013
  ident: 10.1016/j.celrep.2018.08.019_bib25
  article-title: Fanconi anaemia and the repair of Watson and Crick DNA crosslinks
  publication-title: Nature
  doi: 10.1038/nature11863
– volume: 107
  start-page: 16090
  year: 2010
  ident: 10.1016/j.celrep.2018.08.019_bib38
  article-title: Chk1 promotes replication fork progression by controlling replication initiation
  publication-title: Proc. Natl. Acad. Sci. USA
  doi: 10.1073/pnas.1005031107
– volume: 67
  start-page: 882
  year: 2017
  ident: 10.1016/j.celrep.2018.08.019_bib55
  article-title: Replication fork slowing and reversal upon DNA damage require PCNA polyubiquitination and ZRANB3 DNA translocase activity
  publication-title: Mol. Cell
  doi: 10.1016/j.molcel.2017.08.010
– volume: 16
  start-page: 1058
  year: 1977
  ident: 10.1016/j.celrep.2018.08.019_bib20
  article-title: Synthesis and characterization of new psoralen derivatives with superior photoreactivity with DNA and RNA
  publication-title: Biochemistry
  doi: 10.1021/bi00625a005
– volume: 208
  start-page: 545
  year: 2015
  ident: 10.1016/j.celrep.2018.08.019_bib50
  article-title: DNA2 drives processing and restart of reversed replication forks in human cells
  publication-title: J. Cell Biol.
  doi: 10.1083/jcb.201406100
– volume: 56
  start-page: 2125
  year: 2013
  ident: 10.1016/j.celrep.2018.08.019_bib14
  article-title: Discovery of 4-4-[(3R)-3-methylmorpholin-4-yl]-6-[1-(methylsulfonyl)cyclopropyl]pyrimidin-2-yl-1H-indole (AZ20): a potent and selective inhibitor of ATR protein kinase with monotherapy in vivo antitumor activity
  publication-title: J. Med. Chem.
  doi: 10.1021/jm301859s
– volume: 106
  start-page: 3184
  year: 2009
  ident: 10.1016/j.celrep.2018.08.019_bib22
  article-title: Cyclin A-Cdk1 regulates the origin firing program in mammalian cells
  publication-title: Proc. Natl. Acad. Sci. USA
  doi: 10.1073/pnas.0809350106
– volume: 206
  start-page: 493
  year: 2014
  ident: 10.1016/j.celrep.2018.08.019_bib35
  article-title: Phosphorylated RPA recruits PALB2 to stalled DNA replication forks to facilitate fork recovery
  publication-title: J. Cell Biol.
  doi: 10.1083/jcb.201404111
– volume: 29
  start-page: 806
  year: 2010
  ident: 10.1016/j.celrep.2018.08.019_bib44
  article-title: ATR activation and replication fork restart are defective in FANCM-deficient cells
  publication-title: EMBO J.
  doi: 10.1038/emboj.2009.385
– volume: 56
  start-page: 174
  year: 2014
  ident: 10.1016/j.celrep.2018.08.019_bib31
  article-title: BRCA1 promotes unloading of the CMG helicase from a stalled DNA replication fork
  publication-title: Mol. Cell
  doi: 10.1016/j.molcel.2014.08.012
– volume: 358
  start-page: 797
  year: 2017
  ident: 10.1016/j.celrep.2018.08.019_bib49
  article-title: Redox-sensitive alteration of replisome architecture safeguards genome integrity
  publication-title: Science
  doi: 10.1126/science.aao3172
– volume: 47
  start-page: 410
  year: 2012
  ident: 10.1016/j.celrep.2018.08.019_bib57
  article-title: The HARP-like domain-containing protein AH2/ZRANB3 binds to PCNA and participates in cellular response to replication stress
  publication-title: Mol. Cell
  doi: 10.1016/j.molcel.2012.05.025
– volume: 57
  start-page: 492
  year: 2015
  ident: 10.1016/j.celrep.2018.08.019_bib17
  article-title: Interaction of Chk1 with Treslin negatively regulates the initiation of chromosomal DNA replication
  publication-title: Mol. Cell
  doi: 10.1016/j.molcel.2014.12.003
– volume: 10
  start-page: 1957
  year: 2015
  ident: 10.1016/j.celrep.2018.08.019_bib52
  article-title: UHRF1 contributes to DNA damage repair as a lesion recognition factor and nuclease scaffold
  publication-title: Cell Rep.
  doi: 10.1016/j.celrep.2015.03.038
– volume: 11
  start-page: 467
  year: 2011
  ident: 10.1016/j.celrep.2018.08.019_bib12
  article-title: DNA interstrand crosslink repair and cancer
  publication-title: Nat. Rev. Cancer
  doi: 10.1038/nrc3088
– volume: 467
  start-page: 343
  year: 2010
  ident: 10.1016/j.celrep.2018.08.019_bib29
  article-title: Phosphorylation of MLL by ATR is required for execution of mammalian S-phase checkpoint
  publication-title: Nature
  doi: 10.1038/nature09350
– volume: 1672
  start-page: 261
  year: 2018
  ident: 10.1016/j.celrep.2018.08.019_bib59
  article-title: Dynamic architecture of eukaryotic DNA replication forks in vivo, visualized by electron microscopy
  publication-title: Methods Mol. Biol.
  doi: 10.1007/978-1-4939-7306-4_19
– volume: 2004
  start-page: 1983
  year: 2004
  ident: 10.1016/j.celrep.2018.08.019_bib6
  article-title: Amphiphilic [5:1]- and [3:3]-hexakisadducts of C60
  publication-title: Eur. J. Org. Chem.
  doi: 10.1002/ejoc.200300663
– volume: 29
  start-page: 141
  year: 2008
  ident: 10.1016/j.celrep.2018.08.019_bib15
  article-title: The Fanconi anemia protein FANCM can promote branch migration of Holliday junctions and replication forks
  publication-title: Mol. Cell
  doi: 10.1016/j.molcel.2007.11.032
– volume: 18
  start-page: 622
  year: 2017
  ident: 10.1016/j.celrep.2018.08.019_bib42
  article-title: The essential kinase ATR: ensuring faithful duplication of a challenging genome
  publication-title: Nat. Rev. Mol. Cell Biol.
  doi: 10.1038/nrm.2017.67
– volume: 19
  start-page: 417
  year: 2012
  ident: 10.1016/j.celrep.2018.08.019_bib41
  article-title: Topoisomerase I poisoning results in PARP-mediated replication fork reversal
  publication-title: Nat. Struct. Mol. Biol.
  doi: 10.1038/nsmb.2258
– reference: 16387650 - Mol Cell. 2006 Jan 6;21(1):15-27
– reference: 27113759 - EMBO Rep. 2016 May;17(5):671-81
– reference: 21719678 - Science. 2011 Jul 1;333(6038):84-7
– reference: 17373769 - Bioconjug Chem. 2007 Mar-Apr;18(2):431-7
– reference: 29123070 - Science. 2017 Nov 10;358(6364):797-802
– reference: 26797144 - Science. 2016 Feb 19;351(6275):846-9
– reference: 20805465 - Proc Natl Acad Sci U S A. 2010 Sep 14;107(37):16090-5
– reference: 28607004 - EMBO J. 2017 Jul 14;36(14):2047-2060
– reference: 28811666 - Nat Rev Mol Cell Biol. 2017 Oct;18(10):622-636
– reference: 25733714 - J Cell Biol. 2015 Mar 2;208(5):563-79
– reference: 24726325 - Mol Cell. 2014 May 8;54(3):460-71
– reference: 23394205 - J Med Chem. 2013 Mar 14;56(5):2125-38
– reference: 25733713 - J Cell Biol. 2015 Mar 2;208(5):545-62
– reference: 20818375 - Nature. 2010 Sep 16;467(7313):343-6
– reference: 21734703 - Nature. 2011 Jul 06;475(7354):53-8
– reference: 25818288 - Cell Rep. 2015 Mar 31;10(12):1957-66
– reference: 26051180 - Mol Cell. 2015 Jun 18;58(6):1090-100
– reference: 19843584 - J Cell Sci. 2009 Nov 15;122(Pt 22):4070-80
– reference: 20670894 - Mol Cell. 2010 Jul 30;39(2):259-68
– reference: 21701511 - Nat Rev Cancer. 2011 Jun 24;11(7):467-80
– reference: 22324461 - Crit Rev Biochem Mol Biol. 2012 May-Jun;47(3):222-35
– reference: 12535533 - Mol Cell. 2003 Jan;11(1):203-13
– reference: 19221029 - Proc Natl Acad Sci U S A. 2009 Mar 3;106(9):3184-9
– reference: 20057355 - EMBO J. 2010 Feb 17;29(4):806-18
– reference: 26840898 - Nat Struct Mol Biol. 2016 Feb;23(2):103-9
– reference: 25219499 - Mol Cell. 2014 Oct 2;56(1):174-85
– reference: 29043630 - Methods Mol Biol. 2018;1672:261-294
– reference: 16581803 - Mol Cell Biol. 2006 Apr;26(8):3319-26
– reference: 12142537 - Science. 2002 Jul 26;297(5581):599-602
– reference: 25557548 - Mol Cell. 2015 Feb 5;57(3):492-505
– reference: 25714681 - Nat Rev Mol Cell Biol. 2015 Apr;16(4):207-20
– reference: 17515603 - Mol Cell Biol. 2007 Aug;27(16):5806-18
– reference: 22705370 - Mol Cell. 2012 Aug 10;47(3):410-21
– reference: 30122534 - Mol Cell. 2018 Jul 24;:null
– reference: 21406556 - Genes Dev. 2011 Mar 15;25(6):621-33
– reference: 27145721 - Nat Rev Mol Cell Biol. 2016 Jun;17(6):337-49
– reference: 29220651 - Mol Cell. 2017 Dec 7;68(5):830-833
– reference: 23325218 - Nature. 2013 Jan 17;493(7432):356-63
– reference: 24768452 - DNA Repair (Amst). 2014 Jul;19:135-42
– reference: 24207054 - Mol Cell. 2013 Nov 7;52(3):434-46
– reference: 849407 - Biochemistry. 1977 Mar 22;16(6):1058-64
– reference: 20865002 - Nature. 2010 Sep 23;467(7314):479-83
– reference: 29924986 - Cell Rep. 2018 Jun 19;23(12):3419-3428
– reference: 18805090 - Cell. 2008 Sep 19;134(6):969-80
– reference: 25643322 - Nat Struct Mol Biol. 2015 Mar;22(3):242-7
– reference: 24267891 - Cell. 2013 Nov 21;155(5):1088-103
– reference: 23873943 - Genes Dev. 2013 Jul 15;27(14):1610-23
– reference: 18206976 - Mol Cell. 2008 Jan 18;29(1):141-8
– reference: 23396353 - Nat Struct Mol Biol. 2013 Mar;20(3):347-54
– reference: 23438602 - Mol Cell Biol. 2013 May;33(9):1830-44
– reference: 22704558 - Mol Cell. 2012 Aug 10;47(3):396-409
– reference: 23993743 - Mol Cell. 2013 Sep 12;51(5):678-90
– reference: 28886337 - Mol Cell. 2017 Sep 7;67(5):882-890.e5
– reference: 25533188 - Mol Cell. 2015 Jan 8;57(1):123-37
– reference: 25113031 - J Cell Biol. 2014 Aug 18;206(4):493-507
– reference: 18995830 - Mol Cell. 2008 Nov 7;32(3):313-24
– reference: 23830640 - Trends Biochem Sci. 2013 Aug;38(8):386-93
– reference: 27693351 - Cell. 2016 Oct 6;167(2):498-511.e14
– reference: 20835227 - Nature. 2010 Sep 23;467(7314):474-8
– reference: 22388737 - Nat Struct Mol Biol. 2012 Mar 04;19(4):417-23
– reference: 18947205 - Anal Chem. 2008 Nov 15;80(22):8790-8
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Snippet Interstrand cross-links (ICLs) are toxic DNA lesions interfering with DNA metabolism that are induced by widely used anticancer drugs. They have long been...
Graphical Abstract Highlights d Fork slowing and reversal are also observed at forks not directly challenged by ICLs d Fork reversal assists ICL traverse and...
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SubjectTerms ATR checkpoint
Chemical Sciences
DNA interstrand crosslinks
DNA replication
DNA replication stress response
electron microscopy
fork traverse
global fork slowing
ICL immunolabeling
Medicinal Chemistry
replication fork reversal
Title ATR-Mediated Global Fork Slowing and Reversal Assist Fork Traverse and Prevent Chromosomal Breakage at DNA Interstrand Cross-Links
URI https://dx.doi.org/10.1016/j.celrep.2018.08.019
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