DNA replication stress: Causes, resolution and disease

Experimental Cell Research

Volumn 329, Issue 1, 2014, Pages 85-93

  Mazouzi, Abdelghani ^a   Velimezi, Georgia ^a   Loizou, Joanna I ^a  

^a ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

Author keywords

Chromosome fragile sites; DNA damage signaling; DNA replication; Genome stability; Replication stress

Indexed keywords

ATM PROTEIN; ATR PROTEIN; DNA;

CARCINOGENESIS; CELL CYCLE PROGRESSION; CHROMATIN STRUCTURE; DNA DAMAGE; DNA REPLICATION; DNA REPLICATION STRESS; DNA STRUCTURE; DNA TRANSCRIPTION; GENE LOCUS; GENETIC DISORDER; GENOMIC INSTABILITY; HUMAN; HUMAN GENOME; NONHUMAN; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; ANIMAL; DISEASES; GENETICS;

ANIMALS; DISEASE; DNA DAMAGE; DNA REPLICATION; GENOMIC INSTABILITY; HUMANS;

EID: 84919413650     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2014.09.030     Document Type: Review

References (86)

1. Sacco E., Hasan M.M., Alberghina L., Vanoni M. Comparative analysis of the molecular mechanisms controlling the initiation of chromosomal DNA replication in yeast and in mammalian cells. Biotechnol. Adv. 2012, 30:73-98.
2. Gambus A., Khoudoli G.A., Jones R.C., Blow J.J. MCM2-7 form double hexamers at licensed origins in Xenopus egg extract. J. Biol. Chem. 2011, 286:11855-11864.
3. Yamazaki S., Hayano M., Masai H. Replication timing regulation of eukaryotic replicons: Rif1 as a global regulator of replication timing. Trends Genet. TIG 2013, 29:449-460.
4. Boos D., Frigola J., Diffley J.F. Activation of the replicative DNA helicase: breaking up is hard to do. Curr. Opin. Cell Biol. 2012, 24:423-430.
5. Errico A., Costanzo V. Mechanisms of replication fork protection: a safeguard for genome stability. Crit. Rev. Biochem. Mol. Biol. 2012, 47:222-235.
6. Moyer S.E., Lewis P.W., 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 2006, 103:10236-10241.
7. Ilves I., Petojevic T., Pesavento J.J., Botchan M.R. Activation of the MCM2-7 helicase by association with Cdc45 and GINS proteins. Mol. Cell 2010, 37:247-258.
8. Fu Y.V., et al. Selective bypass of a lagging strand roadblock by the eukaryotic replicative DNA helicase. Cell 2011, 146:931-941.
9. Labib K. How do Cdc7 and cyclin-dependent kinases trigger the initiation of chromosome replication in eukaryotic cells?. Genes Dev. 2010, 24:1208-1219.
10. Tanaka S., Araki H. Regulation of the initiation step of DNA replication by cyclin-dependent kinases. Chromosoma 2010, 119:565-574.
11. Zeman M.K., Cimprich K.A. Causes and consequences of replication stress. Nat. Cell Biol. 2014, 16:2-9.
12. Durkin S.G., Glover T.W. Chromosome fragile sites. Annu. Rev. Genet. 2007, 41:169-192.
13. Ying S., et al. MUS81 promotes common fragile site expression. Nat. Cell Biol. 2013, 15:1001-1007.
14. Naim V., Wilhelm T., Debatisse M., Rosselli F. ERCC1 and MUS81-EME1 promote sister chromatid separation by processing late replication intermediates at common fragile sites during mitosis. Nat. Cell Biol. 2013, 15:1008-1015.
15. Glover T.W., Berger C., Coyle J., Echo B. DNA polymerase alpha inhibition by aphidicolin induces gaps and breaks at common fragile sites in human chromosomes. Hum. Genet. 1984, 67:136-142.
16. Becker N.A., Thorland E.C., Denison S.R., Phillips L.A., Smith D.I. Evidence that instability within the FRA3B region extends four megabases. Oncogene 2002, 21:8713-8722.
17. Bednarek A.K., et al. WWOX, the FRA16D gene, behaves as a suppressor of tumor growth. Cancer Res. 2001, 61:8068-8073.
18. Denison S.R., Callahan G., Becker N.A., Phillips L.A., Smith D.I. Characterization of FRA6E and its potential role in autosomal recessive juvenile parkinsonism and ovarian cancer. Genes Chromosomes Cancer 2003, 38:40-52.
19. Wang L., et al. Aphidicolin-induced FRA3B breakpoints cluster in two distinct regions. Genomics 1997, 41:485-488.
20. Poulogiannis G., et al. PARK2 deletions occur frequently in sporadic colorectal cancer and accelerate adenoma development in Apc mutant mice. Proc. Natl. Acad. Sci. USA 2010, 107:15145-15150.
21. Gao G., et al. A selected group of large common fragile site genes have decreased expression in oropharyngeal squamous cell carcinomas. Genes Chromosomes Cancer 2014, 53:392-401.
22. Ohta M., et al. The FHIT gene, spanning the chromosome 3p14.2 fragile site and renal carcinoma-associated t(3;8) breakpoint, is abnormal in digestive tract cancers. Cell 1996, 84:587-597.
23. Letessier A., et al. Cell-type-specific replication initiation programs set fragility of the FRA3B fragile site. Nature 2011, 470:120-123.
24. Barlow J.H., et al. Identification of early replicating fragile sites that contribute to genome instability. Cell 2013, 152:620-632.
25. Vieira K.F., et al. Recruitment of transcription complexes to the beta-globin gene locus in vivo and in vitro. J. Biol. Chem. 2004, 279:50350-50357.
26. Helmrich A., Ballarino M., Tora L. Collisions between replication and transcription complexes cause common fragile site instability at the longest human genes. Mol. Cell 2011, 44:966-977.
27. Wahba L., Amon J.D., Koshland D., Vuica-Ross M. RNase H and multiple RNA biogenesis factors cooperate to prevent RNA:DNA hybrids from generating genome instability. Mol. Cell 2011, 44:978-988.
28. Bhatia V., et al. BRCA2 prevents R-loop accumulation and associates with TREX-2 mRNA export factor PCID2. Nature 2014, 511:362-365.
29. Bermejo R., et al. The replication checkpoint protects fork stability by releasing transcribed genes from nuclear pores. Cell 2011, 146:233-246.
30. Halazonetis T.D., Gorgoulis V.G., Bartek J. An oncogene-induced DNA damage model for cancer development. Science 2008, 319:1352-1355.
31. Bartkova J., et al. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 2005, 434:864-870.
32. Gorgoulis V.G., et al. Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 2005, 434:907-913.
33. Bartkova J., et al. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 2006, 444:633-637.
34. Di Micco R., et al. Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 2006, 444:638-642.
35. Srinivasan S.V., Dominguez-Sola D., Wang L.C., Hyrien O., Gautier J. Cdc45 is a critical effector of myc-dependent DNA replication stress. Cell Rep. 2013, 3:1629-1639.
36. Reimann M., et al. The Myc-evoked DNA damage response accounts for treatment resistance in primary lymphomas in vivo. Blood 2007, 110:2996-3004.
37. Neiman P.E., et al. Genomic instability during Myc-induced lymphomagenesis in the bursa of Fabricius. Oncogene 2006, 25:6325-6335.
38. Rohban S., Campaner S. Myc induced replicative stress response: How to cope with it and exploit it. Biochim. Biophys. Acta 2014.
39. Aparicio J.G., Viggiani C.J., Gibson D.G., Aparicio O.M. The Rpd3-Sin3 histone deacetylase regulates replication timing and enables intra-S origin control in Saccharomyces cerevisiae. Mol. Cell Biol. 2004, 24:4769-4780.
40. Boyer A.S., Grgurevic S., Cazaux C., Hoffmann J.S. The human specialized DNA polymerases and non-B DNA: vital relationships to preserve genome integrity. J. Mol. Biol. 2013, 425:4767-4781.
41. Ciccia A., Elledge S.J. The DNA damage response: making it safe to play with knives. Mol. Cell 2010, 40:179-204.
42. Lavin M.F., Kozlov S. ATM activation and DNA damage response. Cell Cycle 2007, 6:931-942.
43. Derheimer F.A., Kastan M.B. Multiple roles of ATM in monitoring and maintaining DNA integrity. FEBS Lett. 2010, 584:3675-3681.
44. Lopez-Contreras A.J., Fernandez-Capetillo O. The ATR barrier to replication-born DNA damage. DNA Repair (Amst) 2010, 9:1249-1255.
45. Fernandez-Capetillo O., Nussenzweig A. Naked replication forks break apRPArt. Cell 2013, 155:979-980.
46. Toledo L.I., et al. ATR prohibits replication catastrophe by preventing global exhaustion of RPA. Cell 2013, 155:1088-1103.
47. Yamada M., et al. ATR-Chk1-APC/CCdh1-dependent stabilization of Cdc7-ASK (Dbf4) kinase is required for DNA lesion bypass under replication stress. Genes Dev. 2013, 27:2459-2472.
48. Petermann E., Helleday T. Pathways of mammalian replication fork restart. Nature reviews. Mol. Cell Biol. 2010, 11:683-687.
49. Falck J., et al. CDK targeting of NBS1 promotes DNA-end resection, replication restart and homologous recombination. EMBO Rep. 2012, 13:561-568.
50. Robison J.G., Elliott J., Dixon K., Oakley G.G. Replication protein A and the Mre11.Rad50.Nbs1 complex co-localize and interact at sites of stalled replication forks. J. Biol. Chem. 2004, 279:34802-34810.
51. Duursma A.M., Driscoll R., Elias J.E., Cimprich K.A. A role for the MRN complex in ATR activation via TOPBP1 recruitment. Mol. Cell 2013, 50:116-122.
52. Lee J., Dunphy W.G. The Mre11-Rad50-Nbs1 (MRN) complex has a specific role in the activation of Chk1 in response to stalled replication forks. Mol. Biol. Cell 2013, 24:1343-1353.
53. Shiotani B., et al. Two distinct modes of ATR activation orchestrated by Rad17 and Nbs1. Cell Rep. 2013, 3:1651-1662.
54. Trenz K., Smith E., Smith S., Costanzo V. ATM and ATR promote Mre11 dependent restart of collapsed replication forks and prevent accumulation of DNA breaks. EMBO J. 2006, 25:1764-1774.
55. Ammazzalorso F., Pirzio L.M., Bignami M., Franchitto A., Pichierri P. ATR and ATM differently regulate WRN to prevent DSBs at stalled replication forks and promote replication fork recovery. EMBO J. 2010, 29:3156-3169.
56. Davalos A.R., Kaminker P., Hansen R.K., Campisi J. ATR and ATM-dependent movement of BLM helicase during replication stress ensures optimal ATM activation and 53BP1 focus formation. Cell Cycle 2004, 3:1579-1586.
57. Harrigan J.A., et al. Replication stress induces 53BP1-containing OPT domains in G1 cells. J. Cell Biol. 2011, 193:97-108.
58. Lukas C., et al. 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat. Cell Biol. 2011, 13:243-253.
59. Ozeri-Galai E., Schwartz M., Rahat A., Kerem B. Interplay between ATM and ATR in the regulation of common fragile site stability. Oncogene 2008, 27:2109-2117.
60. Ray Chaudhuri A., et al. Topoisomerase I poisoning results in PARP-mediated replication fork reversal. Nat. Struct. Mol. Biol. 2012, 19:417-423.
61. Alabert C., et al. Nascent chromatin capture proteomics determines chromatin dynamics during DNA replication and identifies unknown fork components. Nat. Cell Biol. 2014, 16:281-293.
62. Kanu N., Behrens A. ATMIN defines an NBS1-independent pathway of ATM signalling. EMBO J. 2007, 26:2933-2941.
63. McNees C.J., Conlan L.A., Tenis N., Heierhorst J. ASCIZ regulates lesion-specific Rad51 focus formation and apoptosis after methylating DNA damage. EMBO J. 2005, 24:2447-2457.
64. Zhang T., et al. Competition between NBS1 and ATMIN controls ATM signaling pathway choice. Cell Rep. 2012, 2:1498-1504.
65. Iwabuchi K., et al. Stimulation of p53-mediated transcriptional activation by the p53-binding proteins, 53BP1 and 53BP2. J. Biol. Chem. 1998, 273:26061-26068.
66. Bicknell L.S., et al. Mutations in the pre-replication complex cause Meier-Gorlin syndrome. Nat. Genet. 2011, 43:356-359.
67. O'Driscoll M., Ruiz-Perez V.L., Woods C.G., Jeggo P.A., Goodship J.A. A splicing mutation affecting expression of ataxia-telangiectasia and Rad3-related protein (ATR) results in Seckel syndrome. Nat. Genet. 2003, 33:497-501.
68. Qvist P., et al. CtIP Mutations Cause Seckel and Jawad Syndromes. PLoS Genet. 2011, 7:e1002310.
69. Stracker T.H., Petrini J.H. The MRE11 complex: starting from the ends. Nature reviews. Mol. Cell Biol. 2011, 12:90-103.
70. Griffith E., et al. Mutations in pericentrin cause Seckel syndrome with defective ATR-dependent DNA damage signaling. Nat. Genet. 2008, 40:232-236.
71. Singh M., et al. Lamin A/C depletion enhances DNA damage-induced stalled replication fork arrest. Mol. Cell Biol. 2013, 33:1210-1222.
72. Larrieu D., Britton S., Demir M., Rodriguez R., Jackson S.P. Chemical inhibition of NAT10 corrects defects of laminopathic cells. Science 2014, 344:527-532.
73. Boerkoel C.F., et al. Mutant chromatin remodeling protein SMARCAL1 causes Schimke immuno-osseous dysplasia. Nat. Genet. 2002, 30:215-220.
74. Clynes D., et al. ATRX dysfunction induces replication defects in primary mouse cells. PloS One 2014, 9:e92915.
75. Crow Y.J., et al. Mutations in genes encoding ribonuclease H2 subunits cause Aicardi-Goutieres syndrome and mimic congenital viral brain infection. Nat. Genet. 2006, 38:910-916.
76. Tumbale P., Williams J.S., Schellenberg M.J., Kunkel T.A., Williams R.S. Aprataxin resolves adenylated RNA-DNA junctions to maintain genome integrity. Nature 2014, 506:111-115.
77. Tischkowitz M., Dokal I. Fanconi anaemia and leukaemia - clinical and molecular aspects. Br. J. Haematol. 2004, 126:176-191.
78. Howlett N.G., Taniguchi T., Durkin S.G., D'Andrea A.D., Glover T.W. The Fanconi anemia pathway is required for the DNA replication stress response and for the regulation of common fragile site stability. Hum. Mol. Genet. 2005, 14:693-701.
79. Bachrati C.Z., Hickson I.D. RecQ helicases: guardian angels of the DNA replication fork. Chromosoma 2008, 117:219-233.
80. Burrell R.A., et al. Replication stress links structural and numerical cancer chromosomal instability. Nature 2013, 494:492-496.
81. Lossaint G., et al. FANCD2 binds MCM proteins and controls replisome function upon activation of s phase checkpoint signaling. Mol. Cell 2013, 51:678-690.
82. Yeo J.E., Lee E.H., Hendrickson E., Sobeck A. CtIP mediates replication fork recovery in a FANCD2-regulated manner. Hum. Mol. Genet. 2014.
83. Chaudhury I., Sareen A., Raghunandan M., Sobeck A. FANCD2 regulates BLM complex functions independently of FANCI to promote replication fork recovery. Nucleic Acids Res. 2013, 41:6444-6459.
84. Sirbu B.M., Couch F.B., Cortez D. Monitoring the spatiotemporal dynamics of proteins at replication forks and in assembled chromatin using isolation of proteins on nascent DNA. Nat. Protoc. 2012, 7:594-605.
85. Crosetto N., et al. Nucleotide-resolution DNA double-strand break mapping by next-generation sequencing. Nat. Methods 2013, 10:361-365.
86. Chen B., et al. Dynamic imaging of genomic loci in living human cells by an optimized CRISPR/Cas system. Cell 2013, 155:1479-1491.