Separation of intra-S checkpoint protein contributions to DNA replication fork protection and genomic stability in normal human fibroblasts

Cell Cycle

Volumn 12, Issue 2, 2013, Pages 332-345

  Smith Roe, Stephanie L ^d   Patel, Shivani S ^e   Zhou, Yingchun ^a   Simpson, Dennis A ^a   Rao, Shangbang ^b   Ibrahim, Joseph G ^a,b,c   Cordeiro Stone, Marila ^a,c   Kaufmann, William K ^a,c  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b IL   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

^d NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^e MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

ATR; CHK1; Chromosomal aberration; CLASPIN; Genome maintenance; Human fibroblast; Intra s checkpoint; Replication fork protection; TIMELESS; TIPIN

Indexed keywords

ATR PROTEIN; CHECKPOINT KINASE 1; CLASPIN PROTEIN; DNA; PROTEIN; PROTEIN TIMELESS; TIPIN PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CHROMOSOMAL INSTABILITY; CHROMOSOME ABERRATION; CLONOGENESIS; CONTROLLED STUDY; DNA DAMAGE; DNA METABOLISM; DNA REPLICATION; DNA SYNTHESIS; FIBROBLAST; HUMAN; HUMAN CELL; PHENOTYPE; PROTEIN DEPLETION; S PHASE CELL CYCLE CHECKPOINT;

EID: 84873682704     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.23177     Document Type: Article

References (70)

1. Paulsen RD, Cimprich KA. The ATR pathway: finetuning the fork. DNA Repair (Amst) 2007; 6:953- 66; PMID:17531546; http://dx.doi.org/10.1016/j.dnarep.2007. 02.015.
2. Kaufmann WK. The human intra-S checkpoint response to UVC-induced DNA damage. Carcinogenesis 2010; 31:751-65; PMID:19793801; http://dx.doi.org/10. 1093/carcin/bgp230.
3. Nam EA, Cortez D. ATR signalling: more than meeting at the fork. Biochem J 2011; 436:527- 36; PMID:21615334; http://dx.doi.org/10.1042/BJ20102162.
4. MacDougall CA, Byun TS, Van C, Yee MC, Cimprich KA. The structural determinants of checkpoint activation. Genes Dev 2007; 21:898-903; PMID:17437996; http://dx.doi.org/10.1101/gad.1522607.
5. Zou L, Elledge SJ. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 2003; 300:1542-8; PMID:12791985; http://dx.doi.org/10.1126/science.1083430.
6. Zou L, Cortez D, Elledge SJ. Regulation of ATR substrate selection by Rad17-dependent loading of Rad9 complexes onto chromatin. Genes Dev 2002; 16:198- 208; PMID:11799063; http://dx.doi.org/10.1101/gad.950302.
7. Bermudez VP, Lindsey-Boltz LA, Cesare AJ, Maniwa Y, Griffith JD, Hurwitz J, et al. Loading of the human 9-1-1 checkpoint complex onto DNA by the checkpoint clamp loader hRad17-replication factor C complex in vitro. Proc Natl Acad Sci USA 2003; 100:1633-8; PMID:12578958; http://dx.doi.org/10.1073/pnas. 0437927100.
8. Ellison V, Stillman B. Biochemical characterization of DNA damage checkpoint complexes: clamp loader and clamp complexes with specificity for 5' recessed DNA. PLoS Biol 2003; 1:E33; PMID:14624239; http://dx.doi.org/10.1371/ journal.pbio.0000033.
9. Delacroix S, Wagner JM, Kobayashi M, Yamamoto K, Karnitz LM. The Rad9-Hus1-Rad1 (9-1-1) clamp activates checkpoint signaling via TopBP1. Genes Dev 2007; 21:1472-7; PMID:17575048; http://dx.doi.org/10.1101/gad.1547007.
10. Chini CC, Chen J. Human claspin is required for replication checkpoint control. J Biol Chem 2003; 278:30057-62; PMID:12766152; http://dx.doi.org/10. 1074/jbc.M301136200.
11. Unsal-Kaçmaz K, Mullen TE, Kaufmann WK, Sancar A. Coupling of human circadian and cell cycles by the timeless protein. Mol Cell Biol 2005; 25:3109- 16; PMID:15798197; http://dx.doi.org/10.1128/MCB.25.8.3109-3116.2005.
12. Unsal-Kaçmaz K, Chastain PD, Qu PP, Minoo P, Cordeiro-Stone M, Sancar A, et al. 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; PMID:17296725; http://dx.doi.org/10.1128/MCB.02190-06.
13. Yoshizawa-Sugata N, Masai H. Human Tim/Timelessinteracting protein, Tipin, is required for efficient progression of S phase and DNA replication checkpoint. J Biol Chem 2007; 282:2729-40; PMID:17102137; http://dx.doi.org/10. 1074/jbc.M605596200.
14. Smith-Roe SL, Patel SS, Simpson DA, Zhou YC, Rao S, Ibrahim JG, et al. Timeless functions independently of the Tim-Tipin complex to promote sister chromatid cohesion in normal human fibroblasts. Cell Cycle 2011; 10:1618-24; PMID:21508667; http://dx.doi.org/10.4161/cc.10.10.15613.
15. Gotter AL, Suppa C, Emanuel BS. Mammalian TIMELESS and Tipin are evolutionarily conserved replication fork-associated factors. J Mol Biol 2007; 366:36-52; PMID:17141802; http://dx.doi.org/10.1016/j.jmb.2006.10.097.
16. Kemp MG, Akan Z, Yilmaz S, Grillo M, Smith-Roe SL, Kang TH, et al. Tipin-replication protein A interaction mediates Chk1 phosphorylation by ATR in response to genotoxic stress. J Biol Chem 2010; 285:16562- 71; PMID:20233725; http://dx.doi.org/10.1074/jbc.M110.110304.
17. Serçin O, Kemp MG. Characterization of functional domains in human Claspin. Cell Cycle 2011; 10:1599- 606; PMID:21478680; http://dx.doi.org/10. 4161/cc.10.10.15562.
18. De Piccoli G, Katou Y, Itoh T, Nakato R, Shirahige K, Labib K. Replisome stability at defective DNA replication forks is independent of S phase checkpoint kinases. Mol Cell 2012; 45:696-704; PMID:22325992; http://dx.doi.org/10.1016/j.molcel.2012.01.007.
19. Brown EJ, Baltimore D. ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev 2000; 14:397-402; PMID:10691732.
20. Liu Q, Guntuku S, Cui XS, Matsuoka S, Cortez D, Tamai K, et al. Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/M DNA damage checkpoint. Genes Dev 2000; 14:1448-59; PMID:10859164.
21. Gotter AL, Manganaro T, Weaver DR, Kolakowski LF Jr., Possidente B, Sriram S, et al. A time-less function for mouse timeless. Nat Neurosci 2000; 3:755-6; PMID:10903565; http://dx.doi.org/10.1038/77653.
22. Casper AM, Nghiem P, Arlt MF, Glover TW. ATR regulates fragile site stability. Cell 2002; 111:779-89; PMID:12526805; http://dx.doi.org/10.1016/ S0092-8674(02)01113-3.
23. Durkin SG, Arlt MF, Howlett NG, Glover TW. Depletion of CHK1, but not CHK2, induces chromosomal instability and breaks at common fragile sites. Oncogene 2006; 25:4381-8; PMID:16732333; http://dx.doi.org/10.1038/sj.onc. 1209466.
24. Lam MH, Liu Q, Elledge SJ, Rosen JM. Chk1 is haploinsufficient for multiple functions critical to tumor suppression. Cancer Cell 2004; 6:45- 59; PMID:15261141; http://dx.doi.org/10.1016/j.ccr.2004.06.015.
25. Focarelli ML, Soza S, Mannini L, Paulis M, Montecucco A, Musio A. Claspin inhibition leads to fragile site expression. Genes Chromosomes Cancer 2009; 48:1083-90; PMID:19760606; http://dx.doi.org/10.1002/gcc.20710.
26. Leman AR, Noguchi C, Lee CY, Noguchi E. Human Timeless and Tipin stabilize replication forks and facilitate sister-chromatid cohesion. J Cell Sci 2010; 123:660-70; PMID:20124417; http://dx.doi.org/10.1242/jcs.057984.
27. Zhao X, Muller EG, Rothstein R. A suppressor of two essential checkpoint genes identifies a novel protein that negatively affects dNTP pools. Mol Cell 1998; 2:329-40; PMID:9774971; http://dx.doi.org/10.1016/S1097-2765(00)80277-4.
28. Myung K, Datta A, Kolodner RD. Suppression of spontaneous chromosomal rearrangements by S phase checkpoint functions in Saccharomyces cerevisiae. Cell 2001; 104:397-408; PMID:11239397; http://dx.doi.org/10.1016/S0092-8674(01) 00227-6.
29. Sørensen CS, Syljuåsen RG. Safeguarding genome integrity: the checkpoint kinases ATR, CHK1 and WEE1 restrain CDK activity during normal DNA replication. Nucleic Acids Res 2012; 40:477-86; PMID:21937510; http://dx.doi.org/10.1093/nar/gkr697.
30. Jones RM, Petermann E. Replication fork dynamics and the DNA damage response. Biochem J 2012; 443:13-26; PMID:22417748; http://dx.doi.org/10.1042/ BJ20112100.
31. Voineagu I, Freudenreich CH, Mirkin SM. Checkpoint responses to unusual structures formed by DNA repeats. Mol Carcinog 2009; 48:309-18; PMID:19306277; http://dx.doi.org/10.1002/mc.20512.
32. McFarlane RJ, Mian S, Dalgaard JZ. The many facets of the Tim-Tipin protein families' roles in chromosome biology. Cell Cycle 2010; 9:700-5; PMID:20139726; http://dx.doi.org/10.4161/cc.9.4.10676.
33. Dheekollu J, Wiedmer A, Hayden J, Speicher D, Gotter AL, Yen T, et al. Timeless links replication termination to mitotic kinase activation. PLoS One 2011; 6:e19596; PMID:21573113; http://dx.doi.org/10.1371/journal.pone.0019596.
34. Dheekollu J, Lieberman PM. The replisome pausing factor Timeless is required for episomal maintenance of latent Epstein-Barr virus. J Virol 2011; 85:5853- 63; PMID:21490103; http://dx.doi.org/10.1128/JVI.02425-10.
35. Liu G, Chen X, Gao Y, Lewis T, Barthelemy J, Leffak M. Altered replication in human cells promotes DMPK (CTG)(n) · (CAG)(n) repeat instability. Mol Cell Biol 2012; 32:1618-32; PMID:22354993; http://dx.doi.org/ 10.1128/MCB.06727-11.
36. Leman AR, Dheekollu J, Deng Z, Lee SW, Das MM, Lieberman PM, et al. Timeless preserves telomere length by promoting efficient DNA replication through human telomeres. Cell Cycle 2012; 11:2337- 47; PMID:22672906; http://dx.doi.org/10.4161/cc.20810.
37. Katou Y, Kanoh Y, Bando M, Noguchi H, Tanaka H, Ashikari T, et al. S-phase checkpoint proteins Tof1 and Mrc1 form a stable replication-pausing complex. Nature 2003; 424:1078-83; PMID:12944972; http://dx.doi.org/10.1038/ nature01900.
38. Bando M, Katou YM, Komata M, Tanaka H, Itoh T, Sutani T, et al. Csm3, Tof1, and Mrc1 form a heterotrimeric mediator complex that associates with DNA replication forks. J Biol Chem 2009; 284:34355- 65; PMID:19819872; http://dx.doi.org/10.1074/jbc.M109.065730.
39. Chou DM, Elledge SJ. Tipin and Timeless form a mutually protective complex required for genotoxic stress resistance and checkpoint function. Proc Natl Acad Sci USA 2006; 103:18143-7; PMID:17116885; http://dx.doi.org/10.1073/ pnas.0609251103.
40. Yang XH, Shiotani B, Classon M, Zou L. Chk1 and Claspin potentiate PCNA ubiquitination. Genes Dev 2008; 22:1147-52; PMID:18451105; http://dx.doi.org/10. 1101/gad.1632808.
41. Smith KD, Fu MA, Brown EJ. Tim-Tipin dysfunction creates an indispensible reliance on the ATR-Chk1 pathway for continued DNA synthesis. J Cell Biol 2009; 187:15-23; PMID:19805627; http://dx.doi.org/10.1083/jcb.200905006.
42. Tanaka K. Multiple functions of the S-phase checkpoint mediator. Biosci Biotechnol Biochem 2010; 74:2367- 73; PMID:21150122; http://dx.doi.org/10.1271/ bbb.100583.
43. Noguchi E, Noguchi C, McDonald WH, Yates JR 3rd, Russell P. Swi1 and Swi3 are components of a replication fork protection complex in fission yeast. Mol Cell Biol 2004; 24:8342-55; PMID:15367656; http://dx.doi.org/10.1128/MCB.24.19. 8342-8355.2004.
44. Nedelcheva MN, Roguev A, Dolapchiev LB, Shevchenko A, Taskov HB, Shevchenko A, et al. Uncoupling of unwinding from DNA synthesis implies regulation of MCM helicase by Tof1/Mrc1/Csm3 checkpoint complex. J Mol Biol 2005; 347:509- 21; PMID:15755447; http://dx.doi.org/10.1016/j.jmb.2005.01.041.
45. Errico A, Costanzo V. Mechanisms of replication fork protection: a safeguard for genome stability. Crit Rev Biochem Mol Biol 2012; 47:222-35; PMID:22324461; http://dx.doi.org/10.3109/10409238.2012.655374.
46. Chini CC, Wood J, Chen J. Chk1 is required to maintain claspin stability. Oncogene 2006; 25:4165- 71; PMID:16501606; http://dx.doi.org/10.1038/sj.onc. 1209447.
47. Petermann E, Maya-Mendoza A, Zachos G, Gillespie DA, Jackson DA, Caldecott KW. Chk1 requirement for high global rates of replication fork progression during normal vertebrate S phase. Mol Cell Biol 2006; 26:3319-26; PMID:16581803; http://dx.doi.org/10.1128/MCB.26.8.3319-3326.2006.
48. Chastain PD 2nd, Heffernan TP, Nevis KR, Lin L, Kaufmann WK, Kaufman DG, et al. Checkpoint regulation of replication dynamics in UV-irradiated human cells. Cell Cycle 2006; 5:2160-7; PMID:16969085; http://dx.doi.org/10.4161/cc.5. 18.3236.
49. Petermann E, Helleday T, Caldecott KW. Claspin promotes normal replication fork rates in human cells. Mol Biol Cell 2008; 19:2373-8; PMID:18353973; http://dx.doi.org/10.1091/mbc.E07-10-1035.
50. Scorah J, McGowan CH. Claspin and Chk1 regulate replication fork stability by different mechanisms. Cell Cycle 2009; 8:1036-43; PMID:19270516; http://dx.doi.org/10.4161/cc.8.7.8040.
51. Durkin SG, Glover TW. Chromosome fragile sites. Annu Rev Genet 2007; 41:169-92; PMID:17608616; http://dx.doi.org/10.1146/annurev.genet.41.042007. 165900.
52. Petermann E, Helleday T. Pathways of mammalian replication fork restart. Nat Rev Mol Cell Biol 2010; 11:683-7; PMID:20842177; http://dx.doi.org/10.1038/ nrm2974.
53. Brown EJ, Baltimore D. Essential and dispensable roles of ATR in cell cycle arrest and genome maintenance. Genes Dev 2003; 17:615-28; PMID:12629044; http://dx.doi.org/10.1101/gad.1067403.
54. Jiang K, Pereira E, Maxfield M, Russell B, Goudelock DM, Sanchez Y. Regulation of Chk1 includes chromatin association and 14-3-3 binding following phosphorylation on Ser-345. J Biol Chem 2003; 278:25207- 17; PMID:12676962; http://dx.doi.org/10.1074/jbc.M300070200.
55. Zhang YW, Otterness DM, Chiang GG, Xie W, Liu YC, Mercurio F, et al. Genotoxic stress targets human Chk1 for degradation by the ubiquitin-proteasome pathway. Mol Cell 2005; 19:607-18; PMID:16137618; http://dx.doi.org/10.1016/j. molcel.2005.07.019.
56. Smits VA, Reaper PM, Jackson SP. Rapid PIKKdependent release of Chk1 from chromatin promotes the DNA-damage checkpoint response. Curr Biol 2006; 16:150-9; PMID:16360315; http://dx.doi.org/10.1016/j.cub.2005.11.066.
57. Speroni J, Federico MB, Mansilla SF, Soria G, Gottifredi V. Kinase-independent function of checkpoint kinase 1 (Chk1) in the replication of damaged DNA. Proc Natl Acad Sci USA 2012; 109:7344-9; PMID:22529391; http://dx.doi.org/10.1073/pnas.1116345109.
58. Arlt MF, Glover TW. Inhibition of topoisomerase I prevents chromosome breakage at common fragile sites. DNA Repair (Amst) 2010; 9:678-89; PMID:20413351; http://dx.doi.org/10.1016/j.dnarep.2010.03.005.
59. Tanaka H, Kubota Y, Tsujimura T, Kumano M, Masai H, Takisawa H. Replisome progression complex links DNA replication to sister chromatid cohesion in Xenopus egg extracts. Genes Cells 2009; 14:949-63; PMID:19622120; http://dx.doi.org/10.1111/j.1365-2443.2009.01322.x.
60. Sjögren C, Nasmyth K. Sister chromatid cohesion is required for postreplicative double-strand break repair in Saccharomyces cerevisiae. Curr Biol 2001; 11:991-5; PMID:11448778; http://dx.doi.org/10.1016/S0960-9822(01) 00271-8.
61. Urtishak KA, Smith KD, Chanoux RA, Greenberg RA, Johnson FB, Brown EJ. Timeless Maintains Genomic Stability and Suppresses Sister Chromatid Exchange during Unperturbed DNA Replication. J Biol Chem 2009; 284:8777-85; PMID:19112184; http://dx.doi.org/10.1074/jbc.M806103200.
62. Unal E, Arbel-Eden A, Sattler U, Shroff R, Lichten M, Haber JE, et al. DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol Cell 2004; 16:991- 1002; PMID:15610741; http://dx.doi.org/10.1016/j.molcel.2004.11.027.
63. Sabouri N, McDonald KR, Webb CJ, Cristea IM, Zakian VA. DNA replication through hard-to-replicate sites, including both highly transcribed RNA Pol II and Pol III genes, requires the S. pombe Pfh1 helicase. Genes Dev 2012; 26:581-93; PMID:22426534; http://dx.doi.org/10.1101/gad.184697.111.
64. Petermann E, Woodcock M, Helleday T. Chk1 promotes replication fork progression by controlling replication initiation. Proc Natl Acad Sci USA 2010; 107:16090-5; PMID:20805465; http://dx.doi.org/10.1073/pnas.1005031107.
65. Shechter D, Costanzo V, Gautier J. ATR and ATM regulate the timing of DNA replication origin firing. Nat Cell Biol 2004; 6:648-55; PMID:15220931; http://dx.doi.org/10.1038/ncb1145.
66. Boyer JC, Kaufmann WK, Brylawski BP, Cordeiro- Stone M. Defective postreplication repair in xeroderma pigmentosum variant fibroblasts. Cancer Res 1990; 50:2593-8; PMID:2109654.
67. Heffernan TP, Simpson DA, Frank AR, Heinloth AN, Paules RS, Cordeiro-Stone M, et al. An ATR- and Chk1-dependent S checkpoint inhibits replicon initiation following UVC-induced DNA damage. Mol Cell Biol 2002; 22:8552-61; PMID:12446774; http://dx.doi.org/10.1128/MCB.22.24.8552-8561.2002.
68. Simpson DA, Livanos E, Heffernan TP, Kaufmann WK. Telomerase expression is sufficient for chromosomal integrity in cells lacking p53 dependent G1 checkpoint function. J Carcinog 2005; 4:18; PMID:16209708; http://dx.doi.org/10. 1186/1477- 3163-4-18.
69. Zhou T, Chou JW, Simpson DA, Zhou Y, Mullen TE, Medeiros M, et al. Profiles of global gene expression in ionizing-radiation-damaged human diploid fibroblasts reveal synchronization behind the G1 checkpoint in a G0-like state of quiescence. Environ Health Perspect 2006; 114:553-9; PMID:16581545; http://dx.doi.org/10.1289/ehp.8026.
70. Anderson EM, Birmingham A, Baskerville S, Reynolds A, Maksimova E, Leake D, et al. Experimental validation of the importance of seed complement frequency to siRNA specificity. RNA 2008; 14:853- 61; PMID:18367722; http://dx.doi.org/ 10.1261/rna.704708.