Mechanisms of replication fork protection: a safeguard for genome stability
Abstract
During S-phase, the genome is extremely vulnerable and the progression of replication forks is often threatened by exogenous and endogenous challenges. When replication fork progression is halted, the intra S-phase checkpoint is activated to promote structural stability of stalled forks, preventing the dissociation of replisome components. This ensures the rapid resumption of replication following DNA repair. Failure in protecting and/or restarting the stalled forks contributes to alterations of the genome. Several human genetic diseases coupled to an increased cancer predisposition are caused by mutations in genes involved in safeguarding genome integrity during DNA replication. Both the ATR (ataxia telangiectasia and Rad3-related protein) kinase and the Replication pausing complex (RPC) components Tipin, Tim1 and Claspin play key roles in activating the intra S-phase checkpoint and in stabilizing the stalled replication forks. Here, we discuss the specific contribution of these factors in preserving fork structure and ensuring accurate completion of DNA replication.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The Tim-Tipin complex associates with ATR-Chk1 checkpoint proteins and plays an essential role in the DNA damage response.
“The circadian protein Tim (Timeless) -Tipin (Timeless-interacting protein) complex associates with ATR-Chk1 checkpoint proteins and plays an essential role in DDR as well [130–133].”
From Functional interplay between ATM/ATR-mediated DNA damage response and DNA repair pathways in oxidative stress (2014) · cites this paper as [133]
Cites
A comprehensive two-hybrid analysis to explore the yeast protein interactome
Ito, T., Chiba, T., Ozawa, R., Yoshida, M., Hattori, M., & Sakaki, Y. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.061034498 · Cited by 3,566 · see citing works
Checkpoints: Controls That Ensure the Order of Cell Cycle Events
Hartwell, L. H., & Weinert, T. A. (1989) · Science · doi:10.1126/science.2683079 · Cited by 3,053 · see citing works
Global landscape of protein complexes in the yeast Saccharomyces cerevisiae
Krogan, N. J., Cagney, G., Yu, H., Zhong, G., Guo, X., Ignatchenko, A., Li, J., Pu, S., Datta, N., Tikuisis, A., et al. (2006) · Nature · doi:10.1038/nature04670 · Cited by 2,915 · see citing works
Cell-cycle checkpoints and cancer
Kastan, M. B., & Bartek, J. (2004) · Nature · doi:10.1038/nature03097 · Cited by 2,836 · see citing works
Sensing DNA Damage Through ATRIP Recognition of RPA-ssDNA Complexes
Zou, L., & Elledge, S. J. (2003) · Science · doi:10.1126/science.1083430 · Cited by 2,693 · see citing works
ATR: an essential regulator of genome integrity
Cimprich, K. A., & Cortez, D. (2008) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2450 · Cited by 1,798 · see citing works
Regulation of DNA double-strand break repair pathway choice
Shrivastav, M., De Haro, L. P., & Nickoloff, J. A. (2008) · Cell Research · doi:10.1038/cr.2007.111 · Cited by 1,329 · see citing works
Schlacher, K., Christ, N., Siaud, N., Egashira, A., Wu, H., & Jasin, M. (2011) · Cell · doi:10.1016/j.cell.2011.03.041 · Cited by 1,258 · see citing works
ATR and ATRIP: Partners in Checkpoint Signaling
Cortez, D., Guntuku, S., Qin, J., & Elledge, S. J. (2001) · Science · doi:10.1126/science.1065521 · Cited by 985 · see citing works
Choreography of the DNA Damage Response
Lisby, M., Barlow, J. H., Burgess, R. C., & Rothstein, R. (2004) · Cell · doi:10.1016/j.cell.2004.08.015 · Cited by 891 · see citing works
Fork Reversal and ssDNA Accumulation at Stalled Replication Forks Owing to Checkpoint Defects
Sogo, J. M., Lopes, M., & Foiani, M. (2002) · Science · doi:10.1126/science.1074023 · Cited by 824 · see citing works
Petermann, E., Orta, M. L., Issaeva, N., Schultz, N., & Helleday, T. (2010) · Molecular Cell · doi:10.1016/j.molcel.2010.01.021 · Cited by 815 · see citing works
Toward Maintaining the Genome: DNA Damage and Replication Checkpoints
Nyberg, K. A., Michelson, R. J., Putnam, C. W., & Weinert, T. A. (2002) · Annual Review of Genetics · doi:10.1146/annurev.genet.36.060402.113540 · Cited by 770 · see citing works
Gambus, A., Jones, R. C., Sánchez‐Díaz, A., Kanemaki, M. T., van Deursen, F. J., Edmondson, R. D., & Labib, K. P. M. (2006) · Nature Cell Biology · doi:10.1038/ncb1382 · Cited by 769 · see citing works
Byun, T. S., Pacek, M., Yee, M.-C., Walter, J. C., & Cimprich, K. A. (2005) · Genes & Development · doi:10.1101/gad.1301205 · Cited by 767 · see citing works
The DNA replication checkpoint response stabilizes stalled replication forks
Lopes, M., Cotta‐Ramusino, C., Pellicioli, A., Liberi, G., Plevani, P., Muzi-Falconi, M., Newlon, C. S., & Foiani, M. (2001) · Nature · doi:10.1038/35087613 · Cited by 749 · see citing works
Moyer, S. E., Lewis, P. W., & Botchan, M. R. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602400103 · Cited by 704 · see citing works
Interfaces Between the Detection, Signaling, and Repair of DNA Damage
Rouse, J. W., & Jackson, S. P. (2002) · Science · doi:10.1126/science.1074740 · Cited by 688 · see citing works
Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint
Tercero, J. A., & Diffley, J. F. X. (2001) · Nature · doi:10.1038/35087607 · Cited by 667 · see citing works
The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair
Sørensen, C. S., Hansen, L. T., Dziegielewski, J., Syljuåsen, R. G., Lundin, C., Bartek, J., & Helleday, T. (2005) · Nature Cell Biology · doi:10.1038/ncb1212 · Cited by 666 · see citing works
A Mec1- and Rad53-dependent checkpoint controls late-firing origins of DNA replication
Santocanale, C., & Diffley, J. F. X. (1998) · Nature · doi:10.1038/27001 · Cited by 663 · see citing works
S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex
Katou, Y., Kanoh, Y., Bando, M., Noguchi, H., Tanaka, H., Ashikari, T., Sugimoto, K., & Shirahige, K. (2003) · Nature · doi:10.1038/nature01900 · Cited by 649 · see citing works
Gery, S., Komatsu, N., Baldjyan, L., Yu, A., Koo, D., & Koeffler, H. P. (2006) · Molecular Cell · doi:10.1016/j.molcel.2006.03.038 · Cited by 630 · see citing works
Dormant origins licensed by excess Mcm2–7 are required for human cells to survive replicative stressPreprint
Ge, X. Q., Jackson, D. A., & Blow, J. J. (2007) · Genes & Development · doi:10.1101/gad.457807 · Cited by 605 · see citing works
PARP is activated at stalled forks to mediate Mre11‐dependent replication restart and recombination
Bryant, H. E., Petermann, E., Schultz, N., Jemth, A., Loseva, O., Issaeva, N., Johansson, F., Fernandez, S., McGlynn, P., & Helleday, T. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.206 · Cited by 593 · see citing works
The Rad50 zinc-hook is a structure joining Mre11 complexes in DNA recombination and repair
Hopfner, K., Craig, L., Moncalián, G., Zinkel, R. A., Usui, T., Owen, B. A. L., Kärcher, A., Henderson, B., Bodmer, J.-L., McMurray, C. T., et al. (2002) · Nature · doi:10.1038/nature00922 · Cited by 571 · see citing works
Yeast DNA Polymerase ε Participates in Leading-Strand DNA Replication
Pursell, Z. F., Isoz, I., Lundström, E.-B., Johansson, E., & Kunkel, T. A. (2007) · Science · doi:10.1126/science.1144067 · Cited by 565 · see citing works
Lopes, M., Foiani, M., & Sogo, J. M. (2006) · Molecular Cell · doi:10.1016/j.molcel.2005.11.015 · Cited by 563 · see citing works
Syljuåsen, R. G., Sørensen, C. S., Hansen, L. T., Fugger, K., Lundin, C., Johansson, F., Helleday, T., Sehested, M., Lukas, J., & Bártek, J. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.9.3553-3562.2005 · Cited by 550 · see citing works
Surviving the Breakup: The DNA Damage Checkpoint
Harrison, J. C., & Haber, J. E. (2006) · Annual Review of Genetics · doi:10.1146/annurev.genet.40.051206.105231 · Cited by 550 · see citing works
Rad51 protects nascent DNA from Mre11-dependent degradation and promotes continuous DNA synthesis
Hashimoto, Y., Chaudhuri, A. R., Lopes, M., & Costanzo, V. (2010) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1927 · Cited by 537 · see citing works
Self-citationHuman Rad50/Mre11 Is a Flexible Complex that Can Tether DNA Ends
de Jager, M., van Noort, J., van Gent, D. C., Dekker, C., Kanaar, R., & Wyman, C. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00381-1 · Cited by 512 · see citing works
Division of labor at the eukaryotic replication fork.
McElhinny, S. A. N., Gordenin, D., Stith, C. M. W., Burgers, P., & Kunkel, T. (2008) · Molecules and Cells · doi:10.1016/j.molcel.2008.02.022 · Cited by 510 · see citing works
Ibarra, A., Schwob, É., & Méndez, J. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0803978105 · Cited by 505 · see citing works
Cdc6p-dependent loading of Mcm proteins onto pre-replicative chromatin in budding yeast
Donovan, S., Harwood, J. C., Drury, L. S., & Diffley, J. F. X. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.11.5611 · Cited by 495 · see citing works
A unified view of the DNA-damage checkpoint
Melo, J. A., & Toczyski, D. P. (2002) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(02)00312-5 · Cited by 457 · see citing works
The Rad9–Hus1–Rad1 (9–1–1) clamp activates checkpoint signaling via TopBP1Preprint
Delacroix, S., Wagner, J. M., Kobayashi, M., Yamamoto, K.-I., & Karnitz, L. M. (2007) · Genes & Development · doi:10.1101/gad.1547007 · Cited by 454 · see citing works
DNA end resection by Dna2–Sgs1–RPA and its stimulation by Top3–Rmi1 and Mre11–Rad50–Xrs2
Ćejka, P., Cannavò, E., Polaczek, P., Masuda-Sasa, T., Pokharel, S., Campbell, J. L., & Kowalczykowski, S. C. (2010) · Nature · doi:10.1038/nature09355 · Cited by 442 · see citing works
Skibbens, R. V., Corson, L., Koshland, D. E., & Hieter, P. (1999) · Genes & Development · doi:10.1101/gad.13.3.307 · Cited by 437 · see citing works
Regulation of DNA-replication origins during cell-cycle progression
Shirahige, K., Hori, Y., Shiraishi, K., Yamashita, M., Takahashi, K., Obuse, C., Tsurimoto, T., & Yoshikawa, H. (1998) · Nature · doi:10.1038/27007 · Cited by 415 · see citing works
Williams, R. S., Williams, J. S., & Tainer, J. A. (2007) · Biochemistry and Cell Biology · doi:10.1139/o07-069 · Cited by 399 · see citing works
Osborn, A. J., & Elledge, S. J. (2003) · Genes & Development · doi:10.1101/gad.1098303 · Cited by 371 · see citing works
Woodward, A. M., Göhler, T., Luciani, M. G., Oehlmann, M., Ge, X., Gartner, A., Jackson, D. A., & Blow, J. J. (2006) · The Journal of Cell Biology · doi:10.1083/jcb.200602108 · Cited by 369 · see citing works
TopBP1 activates ATR through ATRIP and a PIKK regulatory domainPreprint
Mordes, D. A., Glick, G. G., Zhao, R., & Cortez, D. (2008) · Genes & Development · doi:10.1101/gad.1666208 · Cited by 368 · see citing works
Dimitrova, D. S., & Gilbert, D. M. (1999) · Molecular Cell · doi:10.1016/s1097-2765(00)80227-0 · Cited by 356 · see citing works
Buis, J. M., Wu, Y., Deng, Y., Leddon, J. L., Westfield, G., Eckersdorff, M., Sekiguchi, J., Chang, S. S., & Ferguson, D. O. (2008) · Cell · doi:10.1016/j.cell.2008.08.015 · Cited by 345 · see citing works
Dial 9–1–1 for DNA damage: the Rad9–Hus1–Rad1 (9–1–1) clamp complex
Parrilla-Castellar, E. R., Arlander, S. J. H., & Karnitz, L. (2004) · DNA Repair · doi:10.1016/j.dnarep.2004.03.032 · Cited by 342 · see citing works
DNA polymerase stabilization at stalled replication forks requires Mec1 and the RecQ helicase Sgs1
Cobb, J. A., Bjergbæk, L., Shimada, K., Frei, C., & Gasser, S. M. (2003) · The EMBO Journal · doi:10.1093/emboj/cdg391 · Cited by 333 · see citing works
Minichromosome maintenance proteins are direct targets of the ATM and ATR checkpoint kinases
Cortez, D., Glick, G. G., & Elledge, S. J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0403410101 · Cited by 324 · see citing works
Identification of RFC(Ctf18p, Ctf8p, Dcc1p)
Mayer, M. L., Gygi, S. P., Aebersold, R. H., & Hieter, P. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00254-4 · Cited by 319 · see citing works
Activation of mammalian Chk1 during DNA replication arrest
Feijóo, C. G., Hall-Jackson, C. A., Wu, R., Jenkins, D., Leitch, J., Gilbert, D. M., & Smythe, C. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.200104099 · Cited by 318 · see citing works
Coupling of Human Circadian and Cell Cycles by the Timeless Protein
Ünsal-Kaçmaz, K., Mullen, T. E., Kaufmann, W. K., & Sancar, A. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.8.3109-3116.2005 · Cited by 310 · see citing works
Saccharomyces cerevisiae CTF18 and CTF4 Are Required for Sister Chromatid Cohesion
Hanna, J. S., Kroll, E., Lundblad, V., & Spencer, F. A. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.9.3144-3158.2001 · Cited by 302 · see citing works
Establishment of Sister Chromatid Cohesion at the S. cerevisiae Replication Fork
Lengronne, A., McIntyre, J., Katou, Y., Kanoh, Y., Hopfner, K., Shirahige, K., & Uhlmann, F. (2006) · Molecular Cell · doi:10.1016/j.molcel.2006.08.018 · Cited by 285 · see citing works
ATR autophosphorylation as a molecular switch for checkpoint activation
Liu, S., Shiotani, B., Lahiri, M., Maréchal, A., Tse, A., Leung, C. C. Y., Glover, J. N. M., Yang, X. H., & Zou, L. (2011) · Molecular Cell · doi:10.1016/j.molcel.2011.06.019 · Cited by 281 · see citing works
Exo1 Processes Stalled Replication Forks and Counteracts Fork Reversal in Checkpoint-Defective Cells
Cotta‐Ramusino, C., Fachinetti, D., Lucca, C., Doksani, Y., Lopes, M., Sogo, J. M., & Foiani, M. (2005) · Molecular Cell · doi:10.1016/j.molcel.2004.11.032 · Cited by 281 · see citing works
The Rad9-Hus1-Rad1 Checkpoint Clamp Regulates Interaction of TopBP1 with ATR
Lee, J., Kumagai, A., & Dunphy, W. G. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m704635200 · Cited by 281 · see citing works
Molecular anatomy and regulation of a stable replisome at a paused eukaryotic DNA replication forkPreprint
Calzada, A., Hodgson, B., Kanemaki, M. T., Bueno, A., & Labib, K. P. M. (2005) · Genes & Development · doi:10.1101/gad.337205 · Cited by 280 · see citing works
Mesoscale conformational changes in the DNA-repair complex Rad50/Mre11/Nbs1 upon binding DNA
Moreno‐Herrero, F., de Jager, M., Dekker, N. H., Kanaar, R., Wyman, C., & Dekker, C. (2005) · Nature · doi:10.1038/nature03927 · Cited by 278 · see citing works
Bressan, D. A., Baxter, B. K., & Petrini, J. H. J. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.11.7681 · Cited by 271 · see citing works
Mrc1 and Tof1 Promote Replication Fork Progression and Recovery Independently of Rad53
Tourrière, H., Versini, G., Cordón-Preciado, V., Alabert, C., & Pasero, P. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.07.028 · Cited by 265 · see citing works
Recruitment of Mec1 and Ddc1 Checkpoint Proteins to Double-Strand Breaks Through Distinct Mechanisms
Kondo, T., Wakayama, T., Naiki, T., Matsumoto, K., & Sugimoto, K. (2001) · Science · doi:10.1126/science.1063827 · Cited by 258 · see citing works
The ATR pathway: Fine-tuning the fork
PAULSEN, R., & Cimprich, K. A. (2007) · DNA repair · doi:10.1016/j.dnarep.2007.02.015 · Cited by 256 · see citing works
Gambus, A., van Deursen, F. J., Polychronopoulos, D., Foltman, M., Jones, R. C., Edmondson, R. D., Calzada, A., & Labib, K. P. M. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.226 · Cited by 256 · see citing works
Chromosome Cohesion, Condensation, and Separation
Hirano, T. (2000) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.69.1.115 · Cited by 253 · see citing works
Human Claspin Is Required for Replication Checkpoint Control
Chini, C. C. S., & Chen, J. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m301136200 · Cited by 244 · see citing works
The NuRD chromatin–remodeling complex regulates signaling and repair of DNA damage
Smeenk, G., Wiegant, W. W., Vrolijk, H., Solari, A. P., Pastink, A., & van Attikum, H. (2010) · Journal of Cell Biology · doi:10.1083/jcb.201001048 · Cited by 243 · see citing works
The DNA damage response during DNA replication
Branzei, D., & Foiani, M. (2005) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2005.09.003 · Cited by 240 · see citing works
Ünsal-Kaçmaz, K., Chastain, P. D., Qu, P.-P., Minoo, P., Cordeiro-Stone, M., Sancar, A., & Kaufmann, W. K. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.02190-06 · Cited by 240 · see citing works
Mre11 Protein Complex Prevents Double-Strand Break Accumulation during Chromosomal DNA Replication
Costanzo, V., Robertson, K., Bibikova, M., Kim, E., Grieco, D., Gottesman, M., Carroll, D., & Gautier, J. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00294-5 · Cited by 239 · see citing works
Self-citationIdentification of Protein Complexes Required for Efficient Sister Chromatid Cohesion
Mayer, M. L., Pot, I., Chang, M., Xu, H., Aneliunas, V., Kwok, T., Newitt, R., Aebersold, R. H., Boone, C. M., Brown, G. W., et al. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e03-08-0619 · Cited by 235 · see citing works
Feng, W., Collingwood, D., Boeck, M. E., Fox, L. A., Alvino, G. M., Fangman, W. L., Raghuraman, M. K., & Brewer, B. J. (2006) · Nature Cell Biology · doi:10.1038/ncb1358 · Cited by 234 · see citing works
Visualization of Altered Replication Dynamics after DNA Damage in Human Cells
Merrick, C. J., Jackson, D. A., & Diffley, J. F. X. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m400022200 · Cited by 228 · see citing works
Yoo, H. Y., Kumagai, A., Shevchenko, A., Shevchenko, A., & Dunphy, W. G. (2004) · Cell · doi:10.1016/s0092-8674(04)00417-9 · Cited by 228 · see citing works
Seiler, J. A., Conti, C., Syed, A., Aladjem, M. I., & Pommier, Y. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.02278-06 · Cited by 226 · see citing works
Trenz, K., Smith, E., Smith, S. J., & Costanzo, V. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601045 · Cited by 219 · see citing works
Self-citationMaser, R. S., Zinkel, R. A., & Petrini, J. H. J. (2001) · Nature Genetics · doi:10.1038/86920 · Cited by 217 · see citing works
Mcm10 and And-1/CTF4 recruit DNA polymerase α to chromatin for initiation of DNA replicationPreprint
Zhu, W., Ukomadu, C., Jha, S., Senga, T., Dhar, S. K., Wohlschlegel, J. A., Nutt, L. K., Kornbluth, S. A., & Dutta, A. (2007) · Genes & Development · doi:10.1101/gad.1585607 · Cited by 214 · see citing works
Phosphorylation of the Bloom's Syndrome Helicase and Its Role in Recovery from S-Phase Arrest
Davies, S. L., North, P. S., Dart, D. A., Lakin, N. D., & Hickson, I. D. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.3.1279-1291.2004 · Cited by 208 · see citing works
Activation of the DNA Replication Checkpoint Through RNA Synthesis by Primase
Michael, W. M., Ott, R., Fanning, E., & Newport, J. W. (2000) · Science · doi:10.1126/science.289.5487.2133 · Cited by 206 · see citing works
BRCA2-dependent and independent formation of RAD51 nuclear foci
Tarsounas, M., Davies, D. C., & West, S. C. (2003) · Oncogene · doi:10.1038/sj.onc.1206263 · Cited by 205 · see citing works
Swi1 and Swi3 Are Components of a Replication Fork Protection Complex in Fission Yeast
Noguchi, E., Noguchi, C., McDonald, W. H., Yates, J. R., & Russell, P. R. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.19.8342-8355.2004 · Cited by 205 · see citing works
Mrc1 and DNA Polymerase ɛ Function Together in Linking DNA Replication and the S Phase Checkpoint
Lou, H., Komata, M., Katou, Y., Guan, Z., Reis, C. C., Budd, M. E., Shirahige, K., & Campbell, J. L. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.08.020 · Cited by 204 · see citing works
Lee, J., Kumagai, A., & Dunphy, W. G. (2003) · Molecular Cell · doi:10.1016/s1097-2765(03)00045-5 · Cited by 199 · see citing works
Cobb, J. A., Schleker, T., Rojas, V., Bjergbæk, L., Tercero, J. A., & Gasser, S. M. (2005) · Genes & Development · doi:10.1101/gad.361805 · Cited by 197 · see citing works
Matsuno, K., Kumano, M., Kubota, Y., Hashimoto, Y., & Takisawa, H. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.02267-05 · Cited by 194 · see citing works
DNA replication-dependent nuclear dynamics of the Mre11 complex.
Mirzoeva, O. K., & Petrini, J. H. J. (2003) · PubMed · Cited by 188 · see citing works
Mrc1 Is Required for Normal Progression of Replication Forks throughout Chromatin in S. cerevisiae
Szyjka, S. J., Viggiani, C. J., & Aparicio, O. M. (2005) · Molecular Cell · doi:10.1016/j.molcel.2005.06.037 · Cited by 187 · see citing works
The ATM homologue MEC1 is required for phosphorylation of replication protein A in yeast
Brush, G. S., Morrow, D. M., Hieter, P., & Kelly, T. J. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.26.15075 · Cited by 185 · see citing works
Im, J., Ki, S.-H., Farina, A., Jung, D.-S., Hurwitz, J., & Lee, J.-K. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0908039106 · Cited by 185 · see citing works
Claspin Operates Downstream of TopBP1 To Direct ATR Signaling towards Chk1 Activation
Liu, S., Bekker‐Jensen, S., Mailand, N., Lukas, C., Bártek, J., & Lukas, J. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.00492-06 · Cited by 184 · see citing works
Rowles, A., Tada, S., & Blow, J. J. (1999) · Journal of Cell Science · doi:10.1242/jcs.112.12.2011 · Cited by 178 · see citing works
Regulation of Replicon Size in Xenopus Egg Extracts
Walter, J. C., & Newport, J. W. (1997) · Science · doi:10.1126/science.275.5302.993 · Cited by 176 · see citing works
Lei, M., Kawasaki, Y., & Tye, B. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.9.5081 · Cited by 175 · see citing works
Separate roles for the DNA damage checkpoint protein kinases in stabilizing DNA replication forksPreprint
Segurado, M., & Diffley, J. F. X. (2008) · Genes & Development · doi:10.1101/gad.477208 · Cited by 171 · see citing works
Lucca, C., Vanoli, F., Cotta‐Ramusino, C., Pellicioli, A., Liberi, G., Haber, J. E., & Foiani, M. (2003) · Oncogene · doi:10.1038/sj.onc.1207199 · Cited by 169 · see citing works
Chou, D. M., & Elledge, S. J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0609251103 · Cited by 166 · see citing works
Reconstitution of licensed replication origins on Xenopus sperm nuclei using purified proteins
Gillespie, P. J., Li, A., & Blow, J. J. (2001) · BMC Biochemistry · doi:10.1186/1471-2091-2-15 · Cited by 165 · see citing works
Cell Cycle Regulation of the Replication Licensing System: Involvement of a Cdk-dependent Inhibitor
Mahbubani, H. M., Chong, J. P. J., Chevalier, S., Thommes, P. A., & Blow, J. J. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.136.1.125 · Cited by 163 · see citing works
Swi1 Prevents Replication Fork Collapse and Controls Checkpoint Kinase Cds1
Noguchi, E., Noguchi, C., Du, L., & Russell, P. R. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.21.7861-7874.2003 · Cited by 163 · see citing works
Dimitrova, D. S., & Gilbert, D. M. (2000) · Nature Cell Biology · doi:10.1038/35036309 · Cited by 160 · see citing works
Human Claspin works with BRCA1 to both positively and negatively regulate cell proliferation
Lin, S.-Y., Li, K., Stewart, G. S., & Elledge, S. J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401847101 · Cited by 156 · see citing works
Furuya, K., Poitelea, M., Guo, L., Caspari, T., & Carr, A. M. (2004) · Genes & Development · doi:10.1101/gad.291104 · Cited by 155 · see citing works
Chl1p, a DNA Helicase-Like Protein in Budding Yeast, Functions in Sister-Chromatid Cohesion
Skibbens, R. V. (2004) · Genetics · doi:10.1534/genetics.166.1.33 · Cited by 154 · see citing works
Bando, M., Katou, Y., Komata, M., et al. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.065730 · Cited by 151 · see citing works
BRCA2: a universal recombinase regulator
Thorslund, T., & West, S. C. (2007) · Oncogene · doi:10.1038/sj.onc.1210870 · Cited by 150 · see citing works
Mrc1 and Tof1 Regulate DNA Replication Forks in Different Ways during Normal S Phase
Hodgson, B., Calzada, A., & Labib, K. P. M. (2007) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-05-0500 · Cited by 146 · see citing works
Robison, J. G., Elliott, J., Dixon, K., & Oakley, G. G. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m404750200 · Cited by 138 · see citing works
Mammalian TIMELESS and Tipin are Evolutionarily Conserved Replication Fork-associated Factors
Gotter, A. L., Suppa, C., & Emanuel, B. S. (2006) · Journal of Molecular Biology · doi:10.1016/j.jmb.2006.10.097 · Cited by 135 · see citing works
Nedelcheva, M. N., Roguev, A., Dolapchiev, L. B., Shevchenko, A., Taskov, H. B., Shevchenko, A., Stewart, A. F., & Stoynov, S. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.01.041 · Cited by 135 · see citing works
The Rad53 signal transduction pathway: Replication fork stabilization, DNA repair, and adaptation
Branzei, D., & Foiani, M. (2006) · Experimental Cell Research · doi:10.1016/j.yexcr.2006.06.012 · Cited by 134 · see citing works
Mohanty, B. K., Bairwa, N. K., & Bastia, D. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506540103 · Cited by 134 · see citing works
Interactions of human nuclear proteins P1Mcm3 and P1Cdc46.
Burkhart, R., Schulte, D., Hu, D., Musahl, C., Göhring, F., & Knippers, R. (1995) · PubMed · Cited by 132 · see citing works
Human Timeless and Tipin stabilize replication forks and facilitate sister-chromatid cohesion
Leman, A. R., Noguchi, C., Lee, C. Y., & Noguchi, E. (2010) · Journal of Cell Science · doi:10.1242/jcs.057984 · Cited by 131 · see citing works
Sengupta, S., Robles, A. I., Linke, S. P., Sinogeeva, N. I., Zhang, R., Pedeux, R., Ward, I. M., Celeste, A., Nussenzweig, A., Chen, J., et al. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200405128 · Cited by 130 · see citing works
Wang, H., Wang, H., Powell, S. N., Iliakis, G., & Wang, Y. (2004) · Cancer Research · doi:10.1158/0008-5472.can-04-1289 · Cited by 130 · see citing works
Yoshizawa-Sugata, N., & Masai, H. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m605596200 · Cited by 127 · see citing works
S-Phase Checkpoint Genes Safeguard High-Fidelity Sister Chromatid Cohesion
Warren, C. D., Eckley, D. M., Lee, M. S., Hanna, J. S., Hughes, A. L., Peyser, B. D., Jie, C., Irizarry, R. A., & Spencer, F. A. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e03-09-0637 · Cited by 127 · see citing works
Nam, E. A., Zhao, R., Glick, G. G., Bansbach, C. E., Friedman, D. B., & Cortez, D. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.248914 · Cited by 126 · see citing works
Formosa, T., & Nittis, T. (1999) · Genetics · doi:10.1093/genetics/151.4.1459 · Cited by 126 · see citing works
Genetic Dissection of Parallel Sister-Chromatid Cohesion Pathways
Xu, H., Boone, C. M., & Brown, G. W. (2007) · Genetics · doi:10.1534/genetics.107.072876 · Cited by 122 · see citing works
Arrested replication fork processing: Interplay between checkpoints and recombination
Lambert, S., Froget, B., & Carr, A. M. (2007) · DNA repair · doi:10.1016/j.dnarep.2007.02.024 · Cited by 120 · see citing works
UV stalled replication forks restart by re-priming in human fibroblasts
Elvers, I., Johansson, F., Groth, P., Erixon, K., & Helleday, T. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr420 · Cited by 120 · see citing works
Kemp, M. G., Akan, Z., Yilmaz, S., Grillo, M., Smith‐Roe, S. L., Kang, T., Cordeiro‐Stone, M., Kaufmann, W. K., Abraham, R. T., Sancar, A., et al. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.110304 · Cited by 120 · see citing works
Claspin Promotes Normal Replication Fork Rates in Human Cells
Petermann, E., Helleday, T., & Caldecott, K. W. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-10-1035 · Cited by 116 · see citing works
Naiki, T., Kondo, T., Nakada, D., Matsumoto, K., & Sugimoto, K. (2001) · Molecular and Cellular Biology · doi:10.1128/mcb.21.17.5838-5845.2001 · Cited by 115 · see citing works
Mrc1 Is Required for Sister Chromatid Cohesion To Aid in Recombination Repair of Spontaneous Damage
Xu, H., Boone, C. M., & Klein, H. L. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.16.7082-7090.2004 · Cited by 108 · see citing works
ATRIP associates with replication protein A-coated ssDNA through multiple interactions
Namiki, Y., & Zou, L. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510223103 · Cited by 107 · see citing works
TopBP1 and DNA polymerase-α directly recruit the 9-1-1 complex to stalled DNA replication forks
Yan, S., & Michael, W. M. (2009) · Journal of Cell Biology · doi:10.1083/jcb.200810185 · Cited by 107 · see citing works
Krings, G., & Bastia, D. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0406037101 · Cited by 106 · see citing works
Interactions of Human Nuclear Proteins P1Mcm3 and P1Cdc46
Burkhart, R., Schulte, D., Hu, B., Musahl, C., Göhring, F., & Knippers, R. (1995) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1995.tb20281.x · Cited by 104 · see citing works
Interaction between human MCM7 and Rad17 proteins is required for replication checkpoint signaling
Tsao, C., Geisen, C., & Abraham, R. T. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600463 · Cited by 101 · see citing works
Tittel-Elmer, M., Alabert, C., Pasero, P., & Cobb, J. A. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.60 · Cited by 95 · see citing works
Miles, J., & Formosa, T. (1992) · Molecular and Cellular Biology · doi:10.1128/mcb.12.12.5724-5735.1992 · Cited by 94 · see citing works
Regulation of DNA replication by the S-phase DNA damage checkpoint
Willis, N. A., & Rhind, N. (2009) · Cell Division · doi:10.1186/1747-1028-4-13 · Cited by 93 · see citing works
Smith, K. D., Fu, M. A., & Brown, E. J. (2009) · The Journal of Cell Biology · doi:10.1083/jcb.200905006 · Cited by 92 · see citing works
Errico, A., Costanzo, V., & Hunt, T. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0706347104 · Cited by 92 · see citing works
Self-citationRao, V. A., Fan, A. M., Meng, L., Doe, C. F., North, P. S., Hickson, I. D., & Pommier, Y. G. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.20.8925-8937.2005 · Cited by 87 · see citing works
Ctf4 coordinates the progression of helicase and DNA polymerase α
Tanaka, H., Katou, Y., Yagura, M., Saitoh, K., Itoh, T., Araki, H., Bando, M., & Shirahige, K. (2009) · Genes to Cells · doi:10.1111/j.1365-2443.2009.01310.x · Cited by 85 · see citing works
Temporal separation of replication and recombination requires the intra-S checkpoint
Meister, P., Taddei, A., Vernis, L., Poidevin, M., Gasser, S. M., & Baldacci, G. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200410006 · Cited by 84 · see citing works
The Mre11 Complex Mediates the S-Phase Checkpoint through an Interaction with Replication Protein A
Olson, E. E., Nievera, C. J., Liu, E., Lee, A. Y., Chen, L., & Wu, X. (2007) · Molecular and Cellular Biology · doi:10.1128/mcb.00532-07 · Cited by 81 · see citing works
Luciani, M. G., Oehlmann, M., & Blow, J. J. (2004) · Journal of Cell Science · doi:10.1242/jcs.01400 · Cited by 81 · see citing works
Distinct roles of DNA polymerases delta and epsilon at the replication fork inXenopusegg extracts
Fukui, T., Yamauchi, K., Muroya, T., Akiyama, M., Maki, H., Sugino, A., & Waga, S. (2004) · Genes to Cells · doi:10.1111/j.1356-9597.2004.00716.x · Cited by 80 · see citing works
Tipin/Tim1/And1 protein complex promotes Polα chromatin binding and sister chromatid cohesion
Errico, A., Cosentino, C., Rivera, T., Losada, A., Schwob, É., Hunt, T., & Costanzo, V. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.304 · Cited by 78 · see citing works
Self-citationYan, S., & Michael, W. M. (2009) · Cell Cycle · doi:10.4161/cc.8.18.9485 · Cited by 72 · see citing works
Lee, J., & Dunphy, W. G. (2010) · Molecular Biology of the Cell · doi:10.1091/mbc.e09-11-0958 · Cited by 70 · see citing works
Komata, M., Bando, M., Araki, H., & Shirahige, K. (2009) · Molecular and Cellular Biology · doi:10.1128/mcb.01934-08 · Cited by 66 · see citing works
Gotter, A. L. (2003) · Journal of Molecular Biology · doi:10.1016/s0022-2836(03)00633-8 · Cited by 64 · see citing works
Architecture of the Replication Fork Stalled at the 3′ End of Yeast Ribosomal Genes
Gruber, M., Wellinger, R. E., & Sogo, J. M. (2000) · Molecular and Cellular Biology · doi:10.1128/mcb.20.15.5777-5787.2000 · Cited by 64 · see citing works
Shou, W.-G., Masuda, T., Takisawa, H., & Sugino, A. (2001) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.081088798 · Cited by 60 · see citing works
Davalos, A. R., Kaminker, P. G., Hansen, R. K., & Campisi, J. (2004) · Cell Cycle · doi:10.4161/cc.3.12.1286 · Cited by 58 · see citing works
Miles, J., & Formosa, T. (1992) · Molecular and Cellular Biology · doi:10.1128/mcb.12.12.5724 · Cited by 56 · see citing works
Shimmoto, M., Matsumoto, S., Odagiri, Y., Noguchi, E., Russell, P. R., & Masai, H. (2009) · Genes to Cells · doi:10.1111/j.1365-2443.2009.01300.x · Cited by 55 · see citing works
Williams, D., & McIntosh, J. R. (2002) · Eukaryotic Cell · doi:10.1128/ec.1.5.758-773.2002 · Cited by 55 · see citing works
Sasaki, T., Ramanathan, S., Okuno, Y., et al. (2006) · Molecular and Cellular Biology · doi:10.1128/mcb.26.3.1051-1062.2006 · Cited by 55 · see citing works
Zhou, Y., & Wang, T. S. ‐. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.21.9568-9579.2004 · Cited by 54 · see citing works
Tanaka, H., Kubota, Y., Tsujimura, T., et al. (2009) · Genes to Cells · doi:10.1111/j.1365-2443.2009.01322.x · Cited by 52 · see citing works
Roles of Human AND-1 in Chromosome Transactions in S Phase
Yoshizawa-Sugata, N., & Masai, H. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m806711200 · Cited by 49 · see citing works
Naylor, M. L., Li, J.-M., Osborn, A. J., & Elledge, S. J. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0904623106 · Cited by 47 · see citing works
Skibbens, R. V. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200503129 · Cited by 46 · see citing works
Rad50 Is Dispensable for the Maintenance and Viability of Postmitotic Tissues
Adelman, C. A., De, S., & Petrini, J. H. J. (2008) · Molecular and Cellular Biology · doi:10.1128/mcb.01525-08 · Cited by 45 · see citing works
Urtishak, K. A., Smith, K. D., Chanoux, R. A., Greenberg, R. A., Johnson, F. B., & Brown, E. J. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m806103200 · Cited by 40 · see citing works
High‐Molecular‐Mass Complexes of Human Minichromosome‐Maintenance Proteins in Mitotic Cells
Richter, A., & Knippers, R. (1997) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1997.00136.x · Cited by 34 · see citing works
Tsutsui, Y., Morishita, T., Natsume, T., Yamashita, K., Iwasaki, H., Yamao, F., & Shinagawa, H. (2005) · Current Genetics · doi:10.1007/s00294-005-0584-2 · Cited by 32 · see citing works
XRad17 Is Required for the Activation of XChk1 But Not XCds1 during Checkpoint Signaling inXenopus
Jones, R. E., Chapman, J. R., Puligilla, C., Murray, J. M., Car, A. M., Ford, C. C., & Lindsay, H. D. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.e03-03-0138 · Cited by 25 · see citing works
The DNA damage response during an unperturbed S-phase
Ben‐Yehoyada, M., Gautier, J., & Dupré, A. (2007) · DNA repair · doi:10.1016/j.dnarep.2007.02.005 · Cited by 23 · see citing works
Replication forks, chromatin loops and dormant replication origins
Blow, J. J., & Ge, X. (2008) · Genome biology · doi:10.1186/gb-2008-9-12-244 · Cited by 22 · see citing works
The initiation of DNA replication in the budding yeast cell division cycle
Diffley, J. F. X. (1995) · Yeast · doi:10.1002/yea.320111608 · Cited by 20 · see citing works
Multiple ATR-Chk1 Pathway Proteins Preferentially Associate with Checkpoint-Inducing DNA Substrates
Yilmaz, S., Sancar, A., & Kemp, M. G. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022986 · Cited by 12 · see citing works
Making Connections at DNA Replication Forks: Mrc1 Takes the Lead
Labib, K. P. M. (2008) · Molecular Cell · doi:10.1016/j.molcel.2008.10.005 · Cited by 6 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The ATM protein kinase: regulating the cellular response to genotoxic stress, and more
Shiloh, Y., & Ziv, Y. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3546 · Cited by 1,649 · see citing works
Yan, S., Sorrell, M., & Berman, Z. (2014) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1666-4 · Cited by 247 · see citing works
Systemic DNA damage responses in aging and diseases
Ribezzo, F., Shiloh, Y., & Schumacher, B. (2016) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2015.12.005 · Cited by 116 · see citing works
Liang, J., Zhao, H., Diplas, B. H., Liu, S., Liu, J., Wang, D., Lu, Y., Zhu, Q., Wu, J., Wang, W., et al. (2020) · Cancer Research · doi:10.1158/0008-5472.can-18-3374 · Cited by 75 · see citing works
Deng, S., Vlatkovic, T., Li, M., Zhan, T., Veldwijk, M. R., & Herskind, C. (2022) · Cancers · doi:10.3390/cancers14194874 · Cited by 62 · see citing works
Hilton, B. A., Liu, J., Cartwright, B. M., Liu, Y., Breitman, M., Wang, Y., Jones, R., Tang, H., Rusinol, A., Musich, P. R., et al. (2017) · The FASEB Journal · doi:10.1096/fj.201700014r · Cited by 52 · see citing works
- Authors
- Errico, A., & Costanzo, V.
- Affiliations
- DNA damage and Genome Stability Unit, Clare Hall Laboratories, London Research Institute
- Corresponding author
- Costanzo, Vincenzo
- ORCID
- Costanzo, Vincenzo
- Venue
- Critical Reviews in Biochemistry and Molecular Biology
- Publisher
- Informa UK Limited
- Published
- 2012-02-11
- Volume
- 47
- Issue
- 3
- Pages
- 222-235
- ISSN
- 0045-6411 (ISSN-L)
- 1040-9238
- 1549-7798
- OpenAlex
- W2054468210
- Cited by
- 159
- References
- 170
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 1 · 2023: 6 · 2022: 12 · 2021: 15 · 2020: 9 · 2019: 10 · 2018: 12 · 2017: 19 · 2016: 15 · 2015: 14 · 2014: 20 · 2013: 16
- FWCI
- 1.46
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Critical Reviews in Biochemistry and Molecular Biology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Cancer Research UK
- Lister Institute of Preventive Medicine
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA Repair Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
- Health Sciences › Medicine › Oncology › Cancer-related Molecular Pathways
- Keywords
- replication fork protection, genome stability, S-phase checkpoint, replication fork restart, ATR kinase, TIPIN, TIM-1, Claspin, replisome, DNA repair, cancer predisposition syndromes, DNA replication
- MeSH terms
- Hepatitis A Virus Cellular Receptor 1, MRE11 Homologue Protein, Chromatids, DNA Damage, DNA Repair, DNA Replication, DNA-Binding Proteins, Humans, Membrane Glycoproteins, Phosphorylation, Receptors, Virus, Signal Transduction, Genome, Human, Protein Serine-Threonine Kinases, Replication Origin, Cell Cycle Proteins, Genetic Diseases, Inborn, Genomic Instability, Adaptor Proteins, Signal Transducing, S Phase Cell Cycle Checkpoints, Ataxia Telangiectasia Mutated Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review