Maintenance of fork integrity at damaged DNA and natural pause sites

DNA Repair

Volumn 6, Issue 7, 2007, Pages 900-913

  Tourrière, Hélène ^a   Pasero, Philippe ^a  

^a INSTITUTE OF HUMAN GENETICS   (France)

Author keywords

Genomic instability; Replication fork; S phase checkpoints

Indexed keywords

CHECKPOINT KINASE 2; DOUBLE STRANDED DNA; FORKHEAD TRANSCRIPTION FACTOR;

ARTICLE; CELL CYCLE S PHASE; CELL SURVIVAL; CELLULAR STRESS RESPONSE; DNA DAMAGE; DNA DENATURATION; DNA REPLICATION; DNA RESPONSIVE ELEMENT; DNA SEQUENCE; DNA STRAND BREAKAGE; EUKARYOTIC CELL; GENE AMPLIFICATION; GENE DUPLICATION; GENE TARGETING; GENOMIC INSTABILITY; GENOTOXICITY; HOMOLOGOUS RECOMBINATION; HUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

DNA DAMAGE; DNA REPAIR; DNA REPLICATION; GENOMIC INSTABILITY; HUMANS; RECOMBINATION, GENETIC; S PHASE;

EUKARYOTA;

EID: 34249935010     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2007.02.004     Document Type: Article

References (166)

1. Diffley J.F. Regulation of early events in chromosome replication. Curr. Biol. 14 (2004) R778-R786
2. Kolodner R.D., Putnam C.D., and Myung K. Maintenance of genome stability in Saccharomyces cerevisiae. Science 297 (2002) 552-557
3. Nyberg K.A., Michelson R.J., Putnam C.W., and Weinert T.A. Toward maintaining the genome: DNA damage and replication checkpoints. Annu. Rev. Genet. 36 (2002) 617-656
4. Branzei D., and Foiani M. The Rad53 signal transduction pathway: replication fork stabilization, DNA repair, and adaptation. Exp. Cell Res. 312 (2006) 2654-2659
5. Rouse J., and Jackson S.P. Lcd1p recruits Mec1p to DNA lesions in vitro and in vivo. Mol. Cell 9 (2002) 857-869
6. Zou L., and Elledge S.J. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300 (2003) 1542-1548
7. Namiki Y., and Zou L. ATRIP associates with replication protein A-coated ssDNA through multiple interactions. Proc. Natl. Acad. Sci. USA 103 (2006) 580-585
8. Brush G.S., Morrow D.M., Hieter P., and Kelly T.J. The ATM homologue MEC1 is required for phosphorylation of replication protein A in yeast. Proc. Natl. Acad. Sci. USA 93 (1996) 15075-15080
9. Paciotti V., Clerici M., Lucchini G., and Longhese M.P. The checkpoint protein Ddc2, functionally related to S. pombe Rad26, interacts with Mec1 and is regulated by Mec1-dependent phosphorylation in budding yeast. Genes Dev. 14 (2000) 2046-2059
10. Osborn A.J., and Elledge S.J. Mrc1 is a replication fork component whose phosphorylation in response to DNA replication stress activates Rad53. Genes Dev. 17 (2003) 1755-1767
11. Kumagai A., and Dunphy W.G. Claspin, a novel protein required for the activation of Chk1 during a DNA replication checkpoint response in Xenopus egg extracts. Mol. Cell 6 (2000) 839-849
12. Alcasabas A.A., Osborn A.J., Bachant J., Hu F., Werler P.J., Bousset K., Furuya K., Diffley J.F., Carr A.M., and Elledge S.J. Mrc1 transduces signals of DNA replication stress to activate Rad53. Nat. Cell Biol. 3 (2001) 958-965
13. Sogo J.M., Lopes M., and Foiani M. Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science 297 (2002) 599-602
14. Walter J., and Newport J. Initiation of eukaryotic DNA replication: origin unwinding and sequential chromatin association of Cdc45, RPA, and DNA polymerase [alpha]. Mol. Cell 5 (2000) 617-627
15. Byun T.S., Pacek M., Yee M.-C., Walter J.C., and Cimprich K.A. Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev. 19 (2005) 1040-1052
16. Cortez D. Unwind and slow down: checkpoint activation by helicase and polymerase uncoupling. Genes Dev. 19 (2005) 1007-1012
17. Neecke H., Lucchini G., and Longhese M.P. Cell cycle progression in the presence of irreparable DNA damage is controlled by a Mec1- and Rad53-dependent checkpoint in budding yeast. EMBO J. 18 (1999) 4485-4497
18. Shimada K., Pasero P., and Gasser S.M. ORC and the intra-S-phase checkpoint: a threshold regulates Rad53p activation in S phase. Genes Dev. 16 (2002) 3236-3252
19. Tercero J.A., Longhese M.P., and Diffley J.F. A central role for DNA replication forks in checkpoint activation and response. Mol. Cell 11 (2003) 1323-1336
20. Pacek M., Tutter A.V., Kubota Y., Takisawa H., and Walter J.C. Localization of MCM2-7, Cdc45, and GINS to the site of DNA unwinding during eukaryotic DNA replication. Mol. Cell 21 (2006) 581-587
21. Lambert S., Mason S.J., Barber L.J., Hartley J.A., Pearce J.A., Carr A.M., and McHugh P.J. Schizosaccharomyces pombe checkpoint response to DNA interstrand cross-links. Mol. Cell Biol. 23 (2003) 4728-4737
22. Pichierri P., and Rosselli F. The DNA crosslink-induced S-phase checkpoint depends on ATR-CHK1 and ATR-NBS1-FANCD2 pathways. EMBO J. 23 (2004) 1178-1187
23. Redon C., Pilch D.R., Rogakou E.P., Orr A.H., Lowndes N.F., and Bonner W.M. Yeast histone [2A] serine 129 is essential for the efficient repair of checkpoint-blind DNA damage. EMBO Rep. 4 (2003) 678-684
24. Gruber M., Wellinger R.E., and Sogo J.M. Architecture of the replication fork stalled at the 3′ end of yeast ribosomal genes. Mol. Cell Biol. 20 (2000) 5777-5787
25. Michael W.M., Ott R., Fanning E., and Newport J. Activation of the DNA replication checkpoint through RNA synthesis by primase. Science 289 (2000) 2133-2137
26. Stokes M.P., and Michael W.M. DNA damage-induced replication arrest in Xenopus egg extracts. J. Cell Biol. 163 (2003) 245-255
27. Ball H.L., Myers J.S., and Cortez D. ATRIP binding to replication protein A-single-stranded DNA promotes ATR-ATRIP localization but is dispensable for Chk1 phosphorylation. Mol. Biol. Cell 16 (2005) 2372-2381
28. Kim S.-M., Kumagai A., Lee J., and Dunphy W.G. Phosphorylation of Chk1 by ATR in Xenopus egg extracts requires binding of ATRIP to ATR but not the stable DNA-binding or coiled-coil domains of ATRIP. J. Biol. Chem. 280 (2005) 38355-38364
29. Kumagai A., Lee J., Yoo H.Y., and Dunphy W.G. TopBP1 activates the ATR-ATRIP complex. Cell 124 (2006) 943-955
30. Petermann E., and Caldecott K.W. Evidence that the ATR/Chk1 pathway maintains normal replication fork progression during unperturbed S phase. Cell Cycle 5 (2006) 2203-2209
31. Lucca C., Vanoli F., Cotta-Ramusino C., Pellicioli A., Liberi G., Haber J., and Foiani M. Checkpoint-mediated control of replisome-fork association and signalling in response to replication pausing. Oncogene 23 (2004) 1206-1213
32. Kanoh Y., Tamai K., and Shirahige K. Different requirements for the association of ATR-ATRIP and 9-1-1 to the stalled replication forks. Gene 377 (2006) 88-95
33. Liberi G., Maffioletti G., Lucca C., Chiolo I., Baryshnikova A., Cotta-Ramusino C., Lopes M., Pellicioli A., Haber J.E., and Foiani M. Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes Dev. 19 (2005) 339-350
34. Miyabe I., Morishita T., Hishida T., Yonei S., and Shinagawa H. Rhp51-dependent recombination intermediates that do not generate checkpoint signal are accumulated in Schizosaccharomyces pombe rad60 and smc5/6 mutants after release from replication arrest. Mol. Cell Biol. 26 (2006) 343-353
35. Cobb J.A., Schleker T., Rojas V., Bjergbaek L., Tercero J.A., and Gasser S.M. Replisome instability, fork collapse, and gross chromosomal rearrangements arise synergistically from Mec1 kinase and RecQ helicase mutations. Genes Dev. 19 (2005) 3055-3069
36. Frei C., and Gasser S.M. RecQ-like helicases: the DNA replication checkpoint connection. J. Cell Sci. 113 (2000) 2641-2646
37. Liberi G., Chiolo I., Pellicioli A., Lopes M., Plevani P., Muzi-Falconi M., and Foiani M. Srs2 DNA helicase is involved in checkpoint response and its regulation requires a functional Mec1-dependent pathway and Cdk1 activity. EMBO J. 19 (2000) 5027-5038
38. Versini G., Comet I., Wu M., Hoopes L., Schwob E., and Pasero P. The yeast Sgs1 helicase is differentially required for genomic and ribosomal DNA replication. EMBO J. 22 (2003) 1939-1949
39. Gilbert C.S., Green C.M., and Lowndes N.F. Budding yeast Rad9 is an ATP-dependent Rad53 activating machine. Mol. Cell 8 (2001) 129-136
40. Pellicioli A., and Foiani M. Signal transduction: how rad53 kinase is activated. Curr. Biol. 15 (2005) R769-R771
41. Sweeney F.D., Yang F., Chi A., Shabanowitz J., Hunt D.F., and Durocher D. Saccharomyces cerevisiae Rad9 acts as a Mec1 adaptor to allow Rad53 activation. Curr. Biol. 15 (2005) 1364-1375
42. Nedelcheva M.N., Roguev A., Dolapchiev L.B., Shevchenko A., Taskov H.B., Stewart A.F., and Stoynov S.S. Uncoupling of unwinding from DNA synthesis implies regulation of MCM helicase by Tof1/Mrc1/Csm3 checkpoint complex. J. Mol. Biol. 347 (2005) 509-521
43. Tanaka K., and Russell P. Mrc1 channels the DNA replication arrest signal to checkpoint kinase Cds1. Nat. Cell Biol. 3 (2001) 966-972
44. Zhao H., Tanaka K., Nogochi E., Nogochi C., and Russell P. Replication checkpoint protein Mrc1 is regulated by Rad3 and Tel1 in fission yeast. Mol. Cell Biol. 23 (2003) 8395-8403
45. Foss E.J. Tof1p regulates DNA damage responses during S phase in Saccharomyces cerevisiae. Genetics 157 (2001) 567-577
46. Tourrière H., Versini G., Cordon-Preciado V., Alabert C., and Pasero P. Mrc1 and tof1 promote replication fork progression and recovery independently of Rad53. Mol. Cell 19 (2005) 699-706
47. Kumagai A., and Dunphy W.G. Repeated phosphopeptide motifs in Claspin mediate the regulated binding of Chk1. Nat. Cell Biol. 5 (2003) 161-165
48. Lin S.Y., Li K., Stewart G.S., and Elledge S.J. Human Claspin works with BRCA1 to both positively and negatively regulate cell proliferation. Proc. Natl. Acad. Sci. USA 101 (2004) 6484-6489
49. Yoo H.Y., Jeong S.-Y., and Dunphy W.G. Site-specific phosphorylation of a checkpoint mediator protein controls its responses to different DNA structures. Genes Dev. 20 (2006) 772-783
50. Kumagai A., Kim S.M., and Dunphy W.G. Claspin and the activated form of ATR-ATRIP collaborate in the activation of Chk1. J. Biol. Chem. 279 (2004) 49599-49608
51. Chini C.C.S., and Chen J. Repeated phosphopeptide motifs in human claspin are phosphorylated by CHK1 and mediate claspin function. J. Biol. Chem. 281 (2006) 33276-33282
52. Yan S., Lindsay H.D., and Michael W.M. Direct requirement for Xmus101 in ATR-mediated phosphorylation of Claspin bound Chk1 during checkpoint signaling. J. Cell Biol. 173 (2006) 181-186
53. Wang X., Zou L., Lu T., Bao S., Hurov K.E., Hittelman W.N., Elledge S.J., and Li L. Rad17 phosphorylation is required for Claspin recruitment and Chk1 activation in response to replication stress. Mol. Cell 23 (2006) 331-341
54. Smolka M.B., Albuquerque C.P., Chen S.-H., Schmidt K.H., Wei X.X., Kolodner R.D., and Zhou H. Dynamic changes in protein-protein interaction and protein phosphorylation probed with amine-reactive isotope tag. Mol. Cell Proteomics 4 (2005) 1358-1369
55. Desany B.A., Alcasabas A.A., Bachant J.B., and Elledge S.J. Recovery from DNA replicational stress is the essential function of the S-phase checkpoint pathway. Genes Dev. 12 (1998) 2956-2970
56. Paulovich A.G., and Hartwell L.H. A checkpoint regulates the rate of progression through S phase in S. cerevisiae in response to DNA damage. Cell 82 (1995) 841-847
57. Tercero J.A., and Diffley J.F. Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 412 (2001) 553-557
58. Santocanale C., and Diffley J.F. A Mec1- and Rad53-dependent checkpoint controls late-firing origins of DNA replication. Nature 395 (1998) 615-618
59. Shirahige K., Hori Y., Shiraishi K., Yamashita M., Takahashi K., Obuse C., Tsurimoto T., and Yoshikawa H. Regulation of DNA-replication origins during cell-cycle progression. Nature 395 (1998) 618-621
60. Larner J.M., Lee H., Little R.D., Dijkwel P.A., Schildkraut C.L., and Hamlin J.L. Radiation down-regulates replication origin activity throughout the S phase in mammalian cells. Nucl. Acids Res. 27 (1999) 803-809
61. Merrick C.J., Jackson D., and Diffley J.F.X. Visualization of altered replication dynamics after DNA damage in human cells. J. Biol. Chem. 279 (2004) 20067-20075
62. Henry-Mowatt J., Jackson D., Masson J.Y., Johnson P.A., Clements P.M., Benson F.E., Thompson L.H., Takeda S., West S.C., and Caldecott K.W. XRCC3 and Rad51 modulate replication fork progression on damaged vertebrate chromosomes. Mol. Cell 11 (2003) 1109-1117
63. Pasero P., Duncker B.P., Schwob E., and Gasser S.M. A role for the cdc7 kinase regulatory subunit dbf4p in the formation of initiation-competent origins of replication. Genes Dev. 13 (1999) 2159-2176
64. Weinreich M., and Stillman B. Cdc7p-Dbf4p kinase binds to chromatin during S phase and is regulated by both the APC and the RAD53 checkpoint pathway. EMBO J. 18 (1999) 5334-5346
65. Shechter D., and Gautier J. ATM and ATR check in on origins: a dynamic model for origin selection and activation. Cell Cycle 4 (2005) 235-238
66. Lopes M., Cotta-Ramusino C., Pellicioli A., Liberi G., Plevani P., Muzi-Falconi M., Newlon C.S., and Foiani M. The DNA replication checkpoint response stabilizes stalled replication forks. Nature 412 (2001) 557-561
67. Cotta-Ramusino C., Fachinetti D., Lucca C., Doksani Y., Lopes M., Sogo J., and Foiani M. Exo1 processes stalled replication forks and counteracts fork reversal in checkpoint-defective cells. Mol. Cell 17 (2005) 153-159
68. Gabrielse C., Miller C.T., McConnell K.H., DeWard A., Fox C.A., and Weinreich M. A Dbf4p BRCT-like domain required for the response to replication fork arrest in budding yeast. Genetics 173 (2006) 541-555
69. Bjergbaek L., Cobb J.A., Tsai-Pflugfelder M., and Gasser S.M. Mechanistically distinct roles for Sgs1p in checkpoint activation and replication fork maintenance. EMBO J. 24 (2005) 405-417
70. Trenz K., Smith E., Smith S., and Costanzo V. ATM and ATR promote Mre11 dependent restart of collapsed replication forks and prevent accumulation of DNA breaks. EMBO J. 25 (2006) 1764-1774
71. Michel B., Grompone G., Flores M.-J., and Bidnenko V. Multiple pathways process stalled replication forks. Proc. Natl. Acad. Sci. USA 101 (2004) 12783-12788
72. Boddy M.N., Shanahan P., McDonald W.H., Lopez-Girona A., Noguchi E., Yates I.J., and Russell P. Replication checkpoint kinase Cds1 regulates recombinational repair protein Rad60. Mol. Cell Biol. 23 (2003) 5939-5946
73. Kai M., Boddy M.N., Russell P., and Wang T.S. Replication checkpoint kinase Cds1 regulates Mus81 to preserve genome integrity during replication stress. Genes Dev. 19 (2005) 919-932
74. Meister P., Taddei A., Vernis L., Poidevin M., Gasser S.M., and Baldacci G. Temporal separation of replication and recombination requires the intra-S checkpoint. J. Cell Biol. 168 (2005) 537-544
75. Pan X., Ye P., Yuan D.S., Wang X., Bader J.S., and Boeke J.D. A DNA integrity network in the yeast Saccharomyces cerevisiae. Cell 124 (2006) 1069-1081
76. Herzberg K., Bashkirov V.I., Rolfsmeier M., Haghnazari E., McDonald W.H., Anderson S., Bashkirova E.V., Yates III J.R., and Heyer W.-D. Phosphorylation of Rad55 on serines 2, 8, and 14 is required for efficient homologous recombination in the recovery of stalled replication forks. Mol. Cell Biol. 26 (2006) 8396-8409
77. Flott S., and Rouse J. Slx4 becomes phosphorylated after DNA damage in a Mec 1/Tel1-dependent manner and is required for repair of DNA alkylation damage. Biochem. J. 391 (2005) 325-333
78. Roberts T.M., Kobor M.S., Bastin-Shanower S.A., Ii M., Horte S.A., Gin J.W., Emili A., Rine J., Brill S.J., and Brown G.W. Slx4 regulates DNA damage checkpoint-dependent phosphorylation of the BRCT domain protein Rtt107/Esc4. Mol. Biol. Cell 17 (2006) 539-548
79. Katou Y., Kanoh Y., Bando M., Noguchi H., Tanaka H., Ashikari T., Sugimoto K., and Shirahige K. S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 424 (2003) 1078-1083
80. Moyer S.E., Lewis P.W., and Botchan M.R. Isolation of the Cdc45/Mcm2-7/GINS (CMG) complex, a candidate for the eukaryotic DNA replication fork helicase. Proc. Natl. Acad. Sci. USA 103 (2006) 10236-10241
81. Gambus A., Jones R.C., Sanchez-Diaz A., Kanemaki M., van Deursen F., Edmondson R.D., and Labib K. GINS maintains association of Cdc45 with MCM in replisome progression complexes at eukaryotic DNA replication forks. Nat. Cell Biol. 8 (2006) 358-366
82. Szyjka S.J., Viggiani C.J., and Aparicio O.M. Mrc1 is required for normal progression of replication forks throughout chromatin in S. cerevisiae. Mol. Cell 19 (2005) 691-697
83. Nedelcheva-Veleva M.N., Krastev D.B., and Stoynov S.S. Coordination of DNA synthesis and replicative unwinding by the S-phase checkpoint pathways. Nucl. Acids Res. 34 (2006) 4138-4146
84. Nitani N., Nakamura K.-i., Nakagawa C., Masukata H., and Nakagawa T. Regulation of DNA replication machinery by Mrc1 in fission yeast. Genetics 174 (2006) 155-165
85. Emili A., Schieltz D.M., Yates III J.R., and Hartwell L.H. Dynamic interaction of DNA damage checkpoint protein Rad53 with chromatin assembly factor Asf1. Mol. Cell 7 (2001) 13-20
86. Gunjan A., and Verreault A. A Rad53 kinase-dependent surveillance mechanism that regulates histone protein levels in S. cerevisiae. Cell 115 (2003) 537-549
87. Franco A.A., Lam W.M., Burgers P.M., and Kaufman P.D. Histone deposition protein Asf1 maintains DNA replisome integrity and interacts with replication factor C. Genes Dev. 19 (2005) 1365-1375
88. Barbour L., and Xiao W. Regulation of alternative replication bypass pathways at stalled replication forks and its effects on genome stability: a yeast model. Mutat. Res. 532 (2003) 137-155
89. Branzei D., and Foiani M. The DNA damage response during DNA replication. Curr. Opin. Cell Biol. 17 (2005) 568-575
90. Lengronne A., McIntyre J., Katou Y., Kanoh Y., Hopfner K.P., Shirahige K., and Uhlmann F. Establishment of sister chromatid cohesion at the S. cerevisiae replication fork. Mol. Cell 23 (2006) 787-799
91. Sjogren C., and Nasmyth K. Sister chromatid cohesion is required for postreplicative double-strand break repair in Saccharomyces cerevisiae. Curr. Biol. 11 (2001) 991-995
92. Lopes M., Cotta-Ramusino C., Liberi G., and Foiani M. Branch migrating sister chromatid junctions form at replication origins through Rad5l/Rad52-independent mechanisms. Mol. Cell 12 (2003) 1499-1510
93. Branzei D., Sollier J., Liberi G., Zhao X., Maeda D., Seki M., Enomoto T., Ohta K., and Foiani M. Ubc9- and Mms21-mediated sumoylation counteracts recombinogenic events at damaged replication forks. Cell 127 (2006) 509-522
94. Raghuraman M.K., Winzeler E.A., Collingwood D., Hunt S., Wodicka L., Conway A., Lockhart D.J., Davis R.W., Brewer B.J., and Fangman W.L. Replication dynamics of the yeast genome. Science 294 (2001) 115-121
95. Lambert S., and Carr A.M. Checkpoint responses to replication fork barriers. Biochimie 87 (2005) 591-602
96. Greenfeder S.A., and Newlon C.S. Replication forks pause at yeast centromeres. Mol. Cell Biol. 12 (1992) 4056-4066
97. Ivessa A.S., Zhou J.Q., Schulz V.P., Monson E.K., and Zakian V.A. Saccharomyces Rrm3p, a 5′ to 3′ DNA helicase that promotes replication fork progression through telomeric and subtelomeric DNA. Genes Dev. 16 (2002) 1383-1396
98. Makovets S., Herskowitz I., and Blackburn E.H. Anatomy and dynamics of DNA replication fork movement in yeast telomeric regions. Mol. Cell Biol. 24 (2004) 4019-4031
99. Deshpande A.M., and Newlon C.S. DNA replication fork pause sites dependent on transcription. Science 272 (1996) 1030-1033
100. Ivessa A.S., Lenzmeier B.A., Bessler J.B., Goudsouzian L.K., Schnakenberg S.L., and Zakian V.A. The Saccharomyces cerevisiae helicase Rrm3p facilitates replication past nonhistone protein-DNA complexes. Mol. Cell 12 (2003) 1525-1536
101. Wang Y., Vujcic M., and Kowalski D. DNA replication forks pause at silent origins near the HML locus in budding yeast. Mol. Cell Biol. 21 (2001) 4938-4948
102. Prado F., and Aguilera A. Impairment of replication fork progression mediates RNA polII transcription-associated recombination. EMBO J. 24 (2005) 1267-1276
103. Boule J.B., Vega L.R., and Zakian V.A. The yeast Pif1p helicase removes telomerase from telomeric DNA. Nature 438 (2005) 57-61
104. Azvolinsky A., Dunaway S., Torres J.Z., Bessler J.B., and Zakian V.A. The S. cerevisiae Rrm3p DNA helicase moves with the replication fork and affects replication of all yeast chromosomes. Genes Dev. 20 (2006) 3104-3116
105. Schmidt K.H., and Kolodner R.D. Requirement of Rrm3 helicase for repair of spontaneous DNA lesions in cells lacking Srs2 or Sgs1 helicase. Mol. Cell Biol. 24 (2004) 3213-3226
106. Torres J.Z., Schnakenberg S.L., and Zakian V.A. Saccharomyces cerevisiae Rrm3p DNA helicase promotes genome integrity by preventing replication fork stalling: viability of rrm3 cells requires the intra-S-phase checkpoint and fork restart activities. Mol. Cell Biol. 24 (2004) 3198-3212
107. Luke B., Versini G., Jaquenoud M., Zaidi I.W., Kurz T., Pintard L., Pasero P., and Peter M. The Cullin Rtt101p promotes replication fork progression through damaged DNA and natural pause sites. Curr. Biol. 16 (2006) 786-792
108. Brewer B.J., and Fangman W.L. A replication fork barrier at the 3′ end of yeast ribosomal RNA genes. Cell 55 (1988) 637-643
109. Linskens M.H., and Huberman J.A. Organization of replication of ribosomal DNA in Saccharomyces cerevisiae. Mol. Cell Biol. 8 (1988) 4927-4935
110. Calzada A., Hodgson B., Kanemaki M., Bueno A., and Labib K. Molecular anatomy and regulation of a stable replisome at a paused eukaryotic DNA replication fork. Genes Dev. 19 (2005) 1905-1919
111. Kobayashi T., and Horiuchi T. A yeast gene product, Fob1 protein, required for both replication fork blocking and recombinational hotspot activities. Genes Cells 1 (1996) 465-474
112. Takeuchi Y., Horiuchi T., and Kobayashi T. Transcription-dependent recombination and the role of fork collision in yeast rDNA. Genes Dev. 17 (2003) 1497-1506
113. Kaplan D.L. Replication termination: mechanism of polar arrest revealed. Curr. Biol. 16 (2006) R684-R686
114. Krings G., and Bastia D. swi1- and swi3-dependent and independent replication fork arrest at the ribosomal DNA of Schizosaccharomyces pombe. Proc. Natl. Acad. Sci. USA 101 (2004) 14085-14090
115. Mohanty B.K., Bairwa N.K., and Bastia D. The Tof1p-Csm3p protein complex counteracts the Rrm3p helicase to control replication termination of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 103 (2006) 897-902
116. Kobayashi T. Strategies to maintain the stability of the ribosomal RNA gene repeats. Genes Genet. Syst. 81 (2006) 155-161
117. Petes T.D. Unequal meiotic recombination within tandem arrays of yeast ribosomal DNA genes. Cell 19 (1980) 765-774
118. Sinclair D.A., and Guarente L. Extrachromosomal rDNA circles-a cause of aging in yeast. Cell 91 (1997) 1033-1042
119. Defossez P.A., Prusty R., Kaeberlein M., Lin S.J., Ferrigno P., Silver P.A., Keil R.L., and Guarente L. Elimination of replication block protein Fob1 extends the life span of yeast mother cells. Mol. Cell 3 (1999) 447-455
120. Kobayashi T., Heck D.J., Nomura M., and Horiuchi T. Expansion and contraction of ribosomal DNA repeats in Saccharomyces cerevisiae: requirement of replication fork blocking (Fob1) protein and the role of RNA polymerase I. Genes Dev. 12 (1998) 3821-3830
121. Rothstein R., Michel B., and Gangloff S. Replication fork pausing and recombination or "gimme a break". Genes Dev. 14 (2000) 1-10
122. Fritze C.E., Verschueren K., Strich R., and Easton Esposito R. Direct evidence for SIR2 modulation of chromatin structure in yeast rDNA. EMBO J. 16 (1997) 6495-6509
123. Pasero P., Bensimon A., and Schwob E. Single-molecule analysis reveals clustering and epigenetic regulation of replication origins at the yeast rDNA locus. Genes Dev. 16 (2002) 2479-2484
124. Kobayashi T., Horiuchi T., Tongaonkar P., Vu L., and Nomura M. SIR2 regulates recombination between different rDNA repeats, but not recombination within individual rRNA genes in yeast. Cell 117 (2004) 441-453
125. Kobayashi T., and Ganley A.R.D. Recombination regulation by transcription-induced cohesin dissociation in rDNA repeats. Science 309 (2005) 1581-1584
126. Huang J., Brito I.L., Villen J., Gygi S.P., Amon A., and Moazed D. Inhibition of homologous recombination by a cohesin-associated clamp complex recruited to the rDNA recombination enhancer. Genes Dev. 20 (2006) 2887-2901
127. Arcangioli B., and de Lahondes R. Fission yeast switches mating type by a replication-recombination coupled process. EMBO J. 19 (2000) 1389-1396
128. Dalgaard J.Z., and Klar A.J. A DNA replication-arrest site RTS1 regulates imprinting by determining the direction of replication at matl in S. pombe. Genes Dev. 15 (2001) 2060-2068
129. Ahn J.S., Osman F., and Whitby M.C. Replication fork blockage by RTS1 at an ectopic site promotes recombination in fission yeast. EMBO J. 24 (2005) 2011-2023
130. Lambert S., Watson A., Sheedy D.M., Martin B., and Carr A.M. Gross chromosomal rearrangements and elevated recombination at an inducible site-specific replication fork barrier. Cell 121 (2005) 689-702
131. Lobachev K.S., Stenger J.E., Kozyreva O.G., Jurka J., Gordenin D.A., and Resnick M.A. Inverted Alu repeats unstable in yeast are excluded from the human genome. EMBO J. 19 (2000) 3822-3830
132. Narayanan V., Mieczkowski P.A., Kim H.-M., Petes T.D., and Lobachev K.S. The pattern of gene amplification is determined by the chromosomal location of hairpin-capped breaks. Cell 125 (2006) 1283-1296
133. Lemoine F.J., Degtyareva N.P., Lobachev K., and Petes T.D. Chromosomal translocations in yeast induced by low levels of DNA polymerase a model for chromosome fragile sites. Cell 120 (2005) 587-598
134. Raveendranathan M., Chattopadhyay S., Bolon Y.T., Haworth J., Clarke D.J., and Bielinsky A.K. Genome-wide replication profiles of S-phase checkpoint mutants reveal fragile sites in yeast. EMBO J. 25 (2006) 3627-3639
135. Admire A., Shanks L., Danzl N., Wang M., Weier U., Stevens W., Hunt E., and Weinert T. Cycles of chromosome instability are associated with a fragile site and are increased by defects in DNA replication and checkpoint controls in yeast. Genes Dev. 20 (2006) 159-173
136. Mieczkowski P.A., Lemoine F.J., and Petes T.D. Recombination between retrotransposons as a source of chromosome rearrangements in the yeast Saccharomyces cerevisiae. DNA Repair 5 (2006) 1010-1020
137. Casper A.M., Nghiem P., Arlt M.F., and Glover T.W. ATR regulates fragile site stability. Cell 111 (2002) 779-789
138. Gorgoulis V.G., Vassiliou L.V., Karakaidos P., Zacharatos P., Kotsinas A., Liloglou T., Venere M., Ditullio Jr. R.A., Kastrinakis N.G., Levy B., Kletsas D., Yoneta A., Herlyn M., Kittas C., and Halazonetis T.D. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434 (2005) 907-913
139. Bartkova J., Horejsi Z., Koed K., Kramer A., Tort F., Zieger K., Guldberg P., Sehested M., Nesland J.M., Lukas C., Orntoft T., Lukas J., and Bartek J. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434 (2005) 864-870
140. Zhao X., Muller E.G., and Rothstein R. A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools. Mol. Cell 2 (1998) 329-340
141. Cha R.S., and Kleckner N. ATR homolog Mec1 promotes fork progression thus averting breaks in replication slow zones. Science 297 (2002) 602-606
142. Petermann E., Maya-Mendoza A., Zachos G., Gillespie D.A.F., Jackson D.A., and Caldecott K.W. Chk1 requirement for high global rates of replication fork progression during normal vertebrate S phase. Mol. Cell Biol. 26 (2006) 3319-3326
143. C.H. Freudenreich, M. Lahiri, Structure-forming CAG/CTG repeat sequences are sensitive to breakage in the absence of Mrc1 checkpoint function and S-phase checkpoint signaling: implications for trinucleotide repeat expansion diseases. Cell Cycle 3 (2004).
144. Lucas I., and Feng W. The essence of replication timing: determinants and significance. Cell Cycle 2 (2003) 560-563
145. Shechter D., Costanzo V., and Gautier J. ATR and ATM regulate the timing of DNA replication origin firing. Nat. Cell Biol. 6 (2004) 648-655
146. Marheineke K., and Hyrien O. Control of replication origin density and firing time in Xenopus egg extracts: role of a caffeine-sensitive, ATR-dependent checkpoint. J. Biol. Chem. 279 (2004) 28071-28081
147. Diaz-Martinez L., and Clarke D.J. Self-regulating model for control of replication origin firing in budding yeast. Cell Cycle 2 (2003) 576-578
148. Nougarede R., Della Seta F., Zarzov P., and Schwob E. Hierarchy of S-phase-promoting factors: yeast Dbf4-Cdc7 kinase requires prior S-phase cyclin-dependent kinase activation. Mol. Cell Biol. 20 (2000) 3795-3806
149. van Brabant A.J., Buchanan C.D., Charboneau E., Fangman W.L., and Brewer B.J. An origin-deficient yeast artificial chromosome triggers a cell cycle checkpoint. Mol. Cell 7 (2001) 705-713
150. Semple J.W., Da-Silva L.F., Jervis E.J., Ah-Kee J., Al-Attar H., Kummer L., Heikkila J.J., Pasero P., and Duncker B.P. An essential role for Orc6 in DNA replication through maintenance of pre-replicative complexes. EMBO J. 25 (2006) 5150-5158
151. Bell S.P., Kobayashi R., and Stillman B. Yeast origin recognition complex functions in transcription silencing and DNA replication. Science 262 (1993) 1844-1849
152. Dillin A., and Rine J. Roles for ORC in M phase and S phase. Science 279 (1998) 1733-1737
153. Watanabe K., Morishita J., Umezu K., Shirahige K., and Maki H. Involvement of RAD9-dependent damage checkpoint control in arrest of cell cycle, induction of cell death, and chromosome instability caused by defects in origin recognition complex in Saccharomyces cerevisiae. Eukaryot. Cell 1 (2002) 200-212
154. Gibson D.G., Bell S.P., and Aparicio O.M. Cell cycle execution point analysis of ORC function and characterization of the checkpoint response to ORC inactivation in Saccharomyces cerevisiae. Genes Cells 11 (2006) 557-573
155. Gibson D.G., Aparicio J.G., Hu F., and Aparicio O.M. Diminished S-phase cyclin-dependent kinase function elicits vital Rad53-dependent checkpoint responses in Saccharomyces cerevisiae. Mol. Cell Biol. 24 (2004) 10208-10222
156. Piatti S., Lengauer C., and Nasmyth K. Cdc6 is an unstable protein whose de novo synthesis in G1 is important for the onset of S phase and for preventing a 'reductional' anaphase in the budding yeast Saccharomyces cerevisiae. EMBO J. 14 (1995) 3788-3799
157. Lengronne A., and Schwob E. The yeast CDK inhibitor Sic1 prevents genomic instability by promoting replication origin licensing in late G(1). Mol. Cell 9 (2002) 1067-1078
158. Ide S., Watanabe K., Watanabe H., Shirahige K., Kobayashi T., and Maki H. Abnormality in initiation program of DNA replication is monitored by the highly repetitive rDNA array on chromosome XII in budding yeast. Mol. Cell Biol. 27 (2007) 568-578
159. Kaliraman V., and Brill S.J. Role of SGS1 and SLX4 in maintaining rDNA structure in Saccharomyces cerevisiae. Curr. Genet. 41 (2002) 389-400
160. Torres-Rosell J., Machin F., and Aragon L. Smc5-Smc6 complex preserves nucleolar integrity in S. cerevisiae. Cell Cycle 4 (2005) 868-872
161. Koszul R., Caburet S., Dujon B., and Fischer G. Eucaryotic genome evolution through the spontaneous duplication of large chromosomal segments. EMBO J. 23 (2004) 234-243
162. Nasmyth K., and Haering C.H. The structure and function of SMC and kleisin complexes. Annu. Rev. Biochem. 74 (2005) 595-648
163. Lobachev K.S., Gordenin D.A., and Resnick M.A. The Mrell complex is required for repair of hairpin-capped double-strand breaks and prevention of chromosome rearrangements. Cell 108 (2002) 183-193
164. Coquelle A., Pipiras E., Toledo F., Buttin G., and Debatisse M. Expression of fragile sites triggers intrachromosomal mammalian gene amplification and sets boundaries to early amplicons. Cell 89 (1997) 215-225
165. Breger K.S., Smith L., and Thayer M.J. Engineering translocations with delayed replication: evidence for cis control of chromosome replication timing. Hum. Mol. Genet. 14 (2005) 2813-2827
166. 1 defines a "point of no return" after which Cdc6 synthesis cannot promote DNA replication in yeast. Genes Dev. 10 (1996) 1516-1531