The multiple facets of the intra-S checkpoint

Cell Cycle

Volumn 7, Issue 15, 2008, Pages 2315-2320

  Grallert, Beáta ^a,b   Boye, Erik ^a  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b INSTITUTE OF CANCER RESEARCH   (Norway)

Author keywords

Checkpoint in normal S phase; Elongation checkpoint; Intra S checkpoint; Origin firing; Replication stress

Indexed keywords

CHECKPOINT KINASE 1; HYDROXYUREA;

CARCINOGENESIS; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL DIVISION; DNA DAMAGE; DNA REPLICATION; DNA REPLICATION ORIGIN; DNA STRUCTURE; HUMAN; MOLECULAR MODEL; NONHUMAN; PROTEIN FUNCTION; REGULATORY MECHANISM; REVIEW;

EID: 48849097263     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.6389     Document Type: Review

References (65)

1. Bartek J, Lukas C, Lukas J. Checking on DNA damage in S phase. Nat Rev Mol Cell Biol 2004; 5:792-804.
2. Lambert S, Carr AM. Checkpoint responses to replication fork barriers. Biochimie 2005; 87:591-602.
3. Conti C, Seiler JA, Pommier Y. The mammalian DNA replication elongation checkpoint: implication of Chk1 and relationship with origin firing as determined by single DNA molecule and single cell analyses. Cell Cycle 2007; 6:2760-7.
4. Shimada K, Pasero P, Gasser SM. ORC and the intra-S-phase checkpoint: a threshold regulates Rad53p activation in S phase. Genes and Development 2002; 16:3236-52.
5. Petermann E, Caldecott KW. Evidence that the ATR/Chk1 pathway maintains normal replication fork progression during unperturbed S phase. Cell Cycle 2006; 5:2203-9.
6. Cimprich KA. Probing ATR activation with model DNA templates. Cell Cycle 2007; 6:2348-54.
7. Gilbert D. Replication origin plasticity, Taylor-made: inhibition vs recruitment of origins under conditions of replication stress. Chromosoma 2007; 116:341-7.
8. Herrick J, Bensimon A. Global regulation of genome duplication in eukaryotes: an overview from the epifluorescence microscope. Chromosoma 2008; 117:243-60.
9. Shechter D, Gautier J. ATM and ATR check in on origins: a dynamic model for origin selection and activation. Cell Cycle 2005; 4:235-8.
10. Santocanale C, Diffley JF. A Mec1- and Rad53-dependent checkpoint controls late-firing origins of DNA replication. Nature 1998; 395:615-8.
11. Tercero JA, Diffley JF. Regulation of DNA replication fork progression through damaged DNA by the Mec1/Rad53 checkpoint. Nature 2001; 412:553-7.
12. Kim SM, Huberman JA. Regulation of replication timing in fission yeast. EMBO J 2001; 20:6115-26.
13. Merrick CJ, Jackson D, Diffley JFX. Visualization of Altered Replication Dynamics after DNA Damage in Human Cells. Journal of Biological Chemistry 2004; 279:20067-75.
14. Chastain PD, Heffernan TP, Nevis KR, Lin L, Kaufmann WK, Kaufman DG, Cordeiro-Stone M. Checkpoint regulation of replication dynamics in UV-irradiated human cells. Cell Cycle 2006; 5:2160-7.
15. Alvino GM, Collingwood D, Murphy JM, Delrow J, Brewer BJ, Raghuraman MK. Replication in Hydroxyurea: It's a Matter of Time. Molecular and Cellular Biology 2007; 27:6396-406.
16. Raveendranathan M, Chattopadhyay S, Bolon YT, Haworth J, Clarke DJ, Bielinsky AK. Genome-wide replication profiles of S-phase checkpoint mutants reveal fragile sites in yeast. Embo J 2006; 25:3627-39.
17. Meister P, Taddei A, Ponti A, Baldacci G, Gasser SM. Replication foci dynamics: replication patterns are modulated by S-phase checkpoint kinases in fission yeast. Embo J 2007; 26:1315-26.
18. Seiler JA, Conti C, Syed A, Aladjem MI, Pommier Y. The Intra-S-Phase Checkpoint Affects both DNA Replication Initiation and Elongation: Single-Cell and -DNA Fiber Analyses. Molecular and Cellular Biology 2007; 27:5806-18.
19. Unsal-Kacmaz K, Chastain PD, Qu PP, Minoo P, Cordeiro-Stone M, Sancar A, Kaufmann WK. The human Tim/Tipin complex coordinates an Intra-S checkpoint response to UV that slows replication fork displacement. Mol Cell Biol 2007; 27:3131-42.
20. Heichinger C, Penkett CJ, Bahler J, Nurse P. Genome-wide characterization of fission yeast DNA replication origins. Embo J 2006; 25:5171-9.
21. Mickle KL, Ramanathan S, Rosebrock A, Oliva A, Chaudari A, Yompakdee C, Scott D, Leatherwood J, Huberman JA. Checkpoint independence of most DNA replication origins in fission yeast. BMC Mol Biol 2007; 8:112.
22. Breier A, Chatterji S, Cozzarelli N. Prediction of Saccharomyces cerevisiae replication origins 2004; 5:22.
23. Allen JB, Zhou Z, Siede W, Friedberg EC, Elledge SJ. The SAD1/RAD53 protein kinase controls multiple checkpoints and DNA damage-induced transcription in yeast. Genes and Development 1994; 8:2401-15.
24. Kato R, Ogawa H. An essential gene, ESR1, is required for mitotic cell growth, DNA repair and meiotic recombination in Saccharomyces cerevisiae. Nucleic Acids Res 1994; 22:3104-12.
25. Liu Q, Guntuku S, Cui XS, Matsuoka S, Cortez D, Tamai K, Luo G, Carattini-Rivera S, DeMayo F, Bradley A, Donehower LA, Elledge SJ. Chk1 is an essential kinase that is regulated by atr and required for the G(2)/M DNA damage checkpoint. Genes and Development 2000; 14:1448-59.
26. Brown EJ, Baltimore D. ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes and Development 2000; 14:397-402.
27. Marheineke K, Hyrien O. Control of Replication Origin Density and Firing Time in Xenopus Egg Extracts: ROLE OF A CAFFEINE-SENSITIVE, ATR-DEPENDENT CHECKPOINT. Journal of Biological Chemistry 2004; 279:28071-81.
28. Sorensen CS, Syljuasen RG, Lukas J, Bartek J. ATR, Claspin and the Rad9-Rad1-Hus1 complex regulate Chk1 and Cdc25A in the absence of DNA damage. Cell Cycle 2004; 3:941-5.
29. Maya-Mendoza A, Petermann E, Gillespie DA, Caldecott KW, Jackson DA. Chk1 regulates the density of active replication origins during the vertebrate S phase. Embo J 2007; 26:2719-31.
30. Miao H, Seiler JA, Burhans WC. Regulation of cellular and SV40 virus origins of replication by Chk1-dependent intrinsic and UVC radiation-induced checkpoints. J Biol Chem 2003; 278:4295-304.
31. Shechter D, Costanzo V, Gautier J. Regulation of DNA replication by ATR: signaling in response to DNA intermediates. DNA Repair (Amst) 2004; 3:901-8.
32. Ben-Yehoyada M, Gautier J, Dupre A. The DNA damage response during an unperturbed S-phase. DNA Repair 2007; 6:914-22.
33. Bielinsky AK. Replication origins: why do we need so many? Cell Cycle 2003; 2:307-9.
34. Conti C, Sacca B, Herrick J, Lalou C, Pommier Y, Bensimon A. Replication Fork Velocities at Adjacent Replication Origins Are Coordinately Modified during DNA Replication in Human Cells. Molecular Biology of the Cell 2007; 18:3059-67.
35. Frum RA, Chastain PD, 2nd, Qu P, Cohen SM, Kaufman DG. DNA replication in early S phase pauses near newly activated origins. Cell Cycle 2008; 7.
36. Calzada A, Hodgson B, Kanemaki M, Bueno A, Labib K. Molecular anatomy and regulation of a stable replisome at a paused eukaryotic DNA replication fork. Genes and Development 2005; 19:1905-19.
37. Noguchi E, Noguchi C, McDonald WH, Yates JR, III, Russell P. Swi1 and Swi3 are components of a replication fork protection complex in fission yeast. Molecular and Cellular Biology 2004; 24:8342-55.
38. Osborn AJ, Elledge SJ. Mrc1 is a replication fork component whose phosphorylation in response to DNA replication stress activates Rad53. Genes and Development 2003; 17:1755.
39. Szyjka SJ, Viggiani CJ, Aparicio OM. Mrc1 is required for normal progression of replication forks throughout chromatin in S. cerevisiae. MolCell 2005; 19:691-7.
40. Lee J, Kumagai A, Dunphy WG. Claspin, a Chk1-Regulatory Protein, Monitors DNA Replication on Chromatin Independently of RPA, ATR and Rad17. MolCell 2003; 11:329-40.
41. Dart DA, Adams KE, Akerman I, Lakin ND. Recruitment of the Cell Cycle Checkpoint Kinase ATR to Chromatin during S-phase. Journal of Biological Chemistry 2004; 279:16433-40.
42. Hekmat-Nejad M, You Z, Yee M, Newport JW, Cimprich KA. Xenopus ATR is a replication-dependent chromatin-binding protein required for the DNA replication checkpoint. Current Biology 2000; 10:1565-73.
43. Hartwell LH, Weinert TA. Checkpoints: controls that ensure the order of cell cycle events. Science 1989; 246:629-34.
44. Anglana M, Apiou F, Bensimon A, Debatisse M. Dynamics of DNA replication in mammalian somatic cells: nucleotide pool modulates origin choice and interorigin spacing. Cell 2003; 114:385-94.
45. Ge XQ, Jackson DA, Blow JJ. Dormant origins licensed by excess Mcm2 7 are required for human cells to survive replicative stress. Genes and Development 2007; 21:3331-41.
46. Lebofsky R, Heilig R, Sonnleitner M, Weissenbach J, Bensimon A. DNA Replication Origin Interference Increases the Spacing between Initiation Events in Human Cells. Molecular Biology of the Cell 2006; 17:5337-45.
47. Petermann E, Maya-Mendoza A, Zachos G, Gillespie DAF, Jackson DA, Caldecott KW. Chk1 Requirement for High Global Rates of Replication Fork Progression during Normal Vertebrate S Phase. Molecular and Cellular Biology 2006; 26:3319-26.
48. Syljuasen RG, Sorensen CS, Hansen LT, Fugger K, Lundin C, Johansson F, Helleday T, Sehested M, Lukas J, Bartek J. Inhibition of human Chk1 causes increased initiation of DNA replication, phosphorylation of ATR targets, and DNA breakage. Mol Cell Biol 2005; 25:3553-62.
49. Kitamura E, Blow JJ, Tanaka TU. Live-cell imaging reveals replication of individual replicons in eukaryotic replication factories. Cell 2006; 125:1297-308.
50. Jackson DA, Pombo A. Replicon Clusters Are Stable Units of Chromosome Structure: Evidence That Nuclear Organization Contributes to the Efficient Activation and Propagation of S Phase in Human Cells. The Journal of Cell Biology 1998; 140:1285-95.
51. Yoo HY, Jeong SY, Dunphy WG. Site-specific phosphorylation of a checkpoint mediator protein controls its responses to different DNA structures. Genes and Development 2006; 20:772-83.
52. Furuya K, Poitelea M, Guo L, Caspari T, Carr AM. Chk1 activation requires Rad9 S/ TQ-site phosphorylation to promote association with C-terminal BRCT domains of Rad4TOPBP1. Genes and Development 2004; 18:1154-64.
53. Kai M, Furuya K, Paderi F, Carr AM, Wang TS. Rad3-dependent phosphorylation of the checkpoint clamp regulates repair-pathway choice. Nat Cell Biol 2007; 9:691-7.
54. Niida H, Katsuno Y, Banerjee B, Hande MP, Nakanishi M. Specific Role of Chk1 Phosphorylations in Cell Survival and Checkpoint Activation. Molecular and Cellular Biology 2007; 27:2572-81.
55. Wang X, Zou L, Lu T, Bao S, Hurov KE, Hittelman WN, Elledge SJ, Li L. Rad17 phosphorylation is required for claspin recruitment and Chk1 activation in response to replication stress. Mol Cell 2006; 23:331-41.
56. Aparicio OM, Stout AM, Bell SP. Differential assembly of Cdc45p and DNA polymerases at early and late origins of DNA replication. Proc Natl Acad Sci USA 1999; 96:9130-5.
57. Zegerman P, Diffley JF. Phosphorylation of Sld2 and Sld3 by cyclin-dependent kinases promotes DNA replication in budding yeast. Nature 2007; 445:281-5.
58. Tanaka S, Umemori T, Hirai K, Muramatsu S, Kamimura Y, Araki H. CDK-dependent phosphorylation of Sld2 and Sld3 initiates DNA replication in budding yeast. Nature 2007; 445:328-32.
59. Cha RS, Kleckner N. ATR homolog Mec1 promotes fork progression, thus averting breaks in replication slow zones. Science 2002; 297:602-6.
60. Bartek J, Bartkova J, Lukas J. DNA damage signalling guards against activated oncogenes and tumour progression. Oncogene 2007; 26:7773-9.
61. Groth A, Corpet A, Cook AJ, Roche D, Bartek J, Lukas J, Almouzni G. Regulation of replication fork progression through histone supply and demand. Science 2007; 318:1928-31.
62. Bartkova J, Rezaei N, Liontos M, Karakaidos P, Kletsas D, Issaeva N, Vassiliou LVF, Kolettas E, Niforou K, Zoumpourlis VC, Takaoka M, Nakagawa H, Tort F, Fugger K, Johansson F, Sehested M, Andersen CL, Dyrskjot L, Orntoft T, Lukas J, Kittas C, Helleday T, Halazonetis TD, Bartek J, Gorgoulis VG. Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 2006; 444:633-7.
63. Di Micco R, Fumagalli M, Cicalese A, Piccinin S, Gasparini P, Luise C, Schurra C, Garre M, Nuciforo PG, Bensimon A, Maestro R, Pelicci PG, d'Adda di Fagagna F. Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 2006; 444:638-42.
64. Sherr CJ, McCormick F. The RB and p53 pathways in cancer. Cancer Cell 2002; 2:103-12.
65. 1 and S-phase checkpoints, chromosome instability, and cancer. Methods Mol Biol 2004; 280:3-49.