Role for Rif1 in the checkpoint response to damaged DNA in Xenopus egg extracts

Cell Cycle

Volumn 11, Issue 6, 2012, Pages 1183-1194

  Kumar, Sanjay ^a   Yoo, Hae Yong ^b   Kumagai, Akiko ^a   Shevchenko, Anna ^c   Shevchenko, Andrej ^c   Dunphy, William G ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b Samsung Medical Center   (South Korea)

^c MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

ATR; Cell cycle control; Checkpoint mechanisms; Chk1; Rif1; TopBP1; Xenopus egg extract

Indexed keywords

ATM PROTEIN; ATR PROTEIN; CHECKPOINT KINASE 1; MRE11 PROTEIN; NIBRIN; PROTEIN; PROTEIN RIF1; RAD50 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHROMATIN; CONTROLLED STUDY; DNA DAMAGE CHECKPOINT; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; EGG; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; XENOPUS;

VERTEBRATA;

EID: 84863368632     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.11.6.19636     Document Type: Article

References (66)

1. Sancar A, Lindsey-Boltz LA, Unsal-Kaçmaz K, Linn S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 2004; 73:39-85; PMID:15189136; http://dx.doi.org/10.1146/annurev. biochem.73.011303.073723.
2. Cimprich KA, Cortez D. ATR: an essential regulator of genome integrity. Nat Rev Mol Cell Biol 2008; 9:616-27; PMID:18594563; http://dx.doi.org/10.1038/ nrm2450.
3. Ciccia A, Elledge SJ. The DNA damage response: making it safe to play with knives. Mol Cell 2010; 40:179-204; PMID:20965415; http://dx.doi.org/10. 1016/j.molcel.2010.09.019.
4. Polo SE, Jackson SP. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev 2011; 25:409-33; PMID:21363960; http://dx.doi.org/10.1101/gad.2021311.
5. Houldsworth J, Lavin MF. Effect of ionizing radiation on DNA synthesis in ataxia telangiectasia cells. Nucleic Acids Res 1980; 8:3709-20; PMID:7433105; http://dx.doi.org/10.1093/nar/8.16.3709.
6. Painter RB, Young BR. Radiosensitivity in ataxia-telangiectasia: a new explanation. Proc Natl Acad Sci USA 1980; 77:7315-7; PMID:6938978; http://dx.doi.org/10.1073/pnas.77.12.7315.
7. Savitsky K, Bar-Shira A, Gilad S, Rotman G, Ziv Y, Vanagaite L, et al. A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science 1995; 268:1749-53; PMID:7792600; http://dx.doi.org/10.1126/science.7792600.
8. Abraham RT. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev 2001; 15:2177-96; PMID:11544175; http://dx.doi.org/10.1101/ gad.914401.
9. Lavin MF. Ataxia-telangiectasia: from a rare disorder to a paradigm for cell signalling and cancer. Nat Rev Mol Cell Biol 2008; 9:759-69; PMID:18813293; http:// dx.doi.org/10.1038/nrm2514.
10. Shiloh Y. The ATM-mediated DNA-damage response: taking shape. Trends Biochem Sci 2006; 31:402-10; PMID:16774833; http://dx.doi.org/10.1016/j.tibs. 2006.05.004.
11. Lee JH, Paull TT. Activation and regulation of ATM kinase activity in response to DNA double-strand breaks. Oncogene 2007; 26:7741-8; PMID:18066086; http://dx.doi.org/10.1038/sj.onc.1210872.
12. Cortez D, Guntuku S, Qin J, Elledge SJ. ATR and ATRIP: partners in checkpoint signaling. Science 2001; 294:1713-6; PMID:11721054; http://dx.doi.org/10.1126/science.1065521.
13. Kumagai A, Lee J, Yoo HY, Dunphy WG. TopBP1 activates the ATR-ATRIP complex. Cell 2006; 124:943-55; PMID:16530042; http://dx.doi.org/10.1016/j.cell. 2005.12.041.
14. Mordes DA, Glick GG, Zhao R, Cortez D. TopBP1 activates ATR through ATRIP and a PIKK regulatory domain. Genes Dev 2008; 22:1478-89; PMID:18519640; http://dx.doi.org/10.1101/gad.1666208.
15. Yoo HY, Kumagai A, Shevchenko A, Shevchenko A, Dunphy WG. Ataxia-telangiectasia mutated (ATM)-dependent activation of ATR occurs through phosphorylation of TopBP1 by ATM. J Biol Chem 2007; 282:17501-6; PMID:17446169; http://dx.doi.org/10.1074/jbc.M701770200.
16. Perry JA, Kornbluth S. Cdc25 and Wee1: analogous opposites? Cell Div 2007; 2:12; PMID:17480229; http://dx.doi.org/10.1186/1747-1028-2-12.
17. Enders GH. Expanded roles for Chk1 in genome maintenance. J Biol Chem 2008; 283:17749-52; PMID:18424430; http://dx.doi.org/10.1074/jbc.R800021200.
18. Silverman J, Takai H, Buonomo SB, Eisenhaber F, de Lange T. Human Rif1, ortholog of a yeast telomeric protein, is regulated by ATM and 53BP1 and functions in the S-phase checkpoint. Genes Dev 2004; 18:2108-19; PMID:15342490; http://dx.doi.org/10.1101/gad.1216004.
19. Xu L, Blackburn EH. Human Rif1 protein binds aberrant telomeres and aligns along anaphase midzone microtubules. J Cell Biol 2004; 167:819-30; PMID:15583028; http://dx.doi.org/10.1083/jcb.200408181.
20. Buonomo SB, Wu Y, Ferguson D, de Lange T. Mammalian Rif1 contributes to replication stress survival and homology-directed repair. J Cell Biol 2009; 187:385-98; PMID:19948482; http://dx.doi.org/10.1083/jcb.200902039.
21. Xu D, Muniandy P, Leo E, Yin J, Thangavel S, Shen X, et al. Rif1 provides a new DNA-binding interface for the Bloom syndrome complex to maintain normal replication. EMBO J 2010; 29:3140-55; PMID:20711169; http://dx.doi.org/10.1038/ emboj.2010.186.
22. Yoo HY, Kumagai A, Shevchenko A, Shevchenko A, Dunphy WG. The Mre11-Rad50-Nbs1 complex mediates activation of TopBP1 by ATM. Mol Biol Cell 2009; 20:2351-60; PMID:19279141; http://dx.doi.org/10.1091/mbc.E08-12-1190.
23. Kumagai A, Shevchenko A, Shevchenko A, Dunphy WG. Treslin collaborates with TopBP1 in triggering the initiation of DNA replication. Cell 2010; 140:349- 59; PMID:20116089; http://dx.doi.org/10.1016/j.cell.2009.12.049.
24. Sansam CL, Cruz NM, Danielian PS, Amsterdam A, Lau ML, Hopkins N, et al. A vertebrate gene, ticrr, is an essential checkpoint and replication regulator. Genes Dev 2010; 24:183-94; PMID:20080954; http:// dx.doi.org/10.1101/gad. 1860310.
25. Kobayashi T, Tada S, Tsuyama T, Murofushi H, Seki M, Enomoto T. Focus-formation of replication protein A, activation of checkpoint system and DNA repair synthesis induced by DNA double-strand breaks in Xenopus egg extract. J Cell Sci 2002; 115:3159-69; PMID:12118071.
26. Yoo HY, Shevchenko A, Shevchenko A, Dunphy WG. Mcm2 is a direct substrate of ATM and ATR during DNA damage and DNA replication checkpoint responses. J Biol Chem 2004; 279:53353-64; PMID:15448142; http://dx.doi.org/10.1074/jbc. M408026200.
27. Costanzo V, Shechter D, Lupardus PJ, Cimprich KA, Gottesman M, Gautier J. An ATR- and Cdc7- dependent DNA damage checkpoint that inhibits initiation of DNA replication. Mol Cell 2003; 11:203-13; PMID:12535533; http://dx.doi.org/10. 1016/S1097-2765(02)00799-2.
28. Luciani MG, Oehlmann M, Blow JJ. Characterization of a novel ATR-dependent, Chk1-independent, intra- S-phase checkpoint that suppresses initiation of replication in Xenopus. J Cell Sci 2004; 117:6019-30; PMID:15536124; http://dx.doi.org/10.1242/jcs.01400.
29. Petersen P, Chou DM, You Z, Hunter T, Walter JC, Walter G. Protein phosphatase 2A antagonizes ATM and ATR in a Cdk2- and Cdc7-independent DNA damage checkpoint. Mol Cell Biol 2006; 26:1997-2011; PMID:16479016; http://dx.doi.org/10.1128/MCB.26.5.1997-2011.2006.
30. Mimura S, Masuda T, Matsui T, Takisawa H. Central role for cdc45 in establishing an initiation complex of DNA replication in Xenopus egg extracts. Genes Cells 2000; 5:439-52; PMID:10886370; http://dx.doi.org/10.1046/j.1365- 2443.2000.00340.x.
31. Walter J, Newport J. Initiation of eukaryotic DNA replication: origin unwinding and sequential chromatin association of Cdc45, RPA and DNA polymerase alpha. Mol Cell 2000; 5:617-27; PMID:10882098; http://dx.doi.org/10.1016/S1097- 2765(00)80241-5.
32. Karnani N, Dutta A. The effect of the intra-S-phase checkpoint on origins of replication in human cells. Genes Dev 2011; 25:621-33; PMID:21406556; http:// dx.doi.org/10.1101/gad.2029711.
33. Postow L, Ghenoiu C, Woo EM, Krutchinsky AN, Chait BT, Funabiki H. Ku80 removal from DNA through double strand break-induced ubiquitylation. J Cell Biol 2008; 182:467-79; PMID:18678709; http:// dx.doi.org/10.1083/jcb.200802146.
34. Wawrousek KE, Fortini BK, Polaczek P, Chen L, Liu Q, Dunphy WG, et al. Xenopus DNA2 is a helicase/ nuclease that is found in complexes with replication proteins And-1/Ctf4 and Mcm10 and DSB response proteins Nbs1 and ATM. Cell Cycle 2010; 9:1156-66; PMID:20237432; http://dx.doi.org/10.4161/cc.9.6.11049.
35. Paull TT. Making the best of the loose ends: Mre11/ Rad50 complexes and Sae2 promote DNA double-strand break resection. DNA Repair (Amst) 2010; 9:1283-91; PMID:21050828; http://dx.doi.org/10.1016/j.dnarep.2010.09.015.
36. Mimitou EP, Symington LS. DNA end resection - unraveling the tail. DNA Repair (Amst) 2011; 10:344-8; PMID:21227759; http://dx.doi.org/10.1016/j.dnarep. 2010.12.004.
37. You Z, Bailis JM. DNA damage and decisions: CtIP coordinates DNA repair and cell cycle checkpoints. Trends Cell Biol 2010; 20:402-9; PMID:20444606; http://dx.doi.org/10.1016/j.tcb.2010.04.002.
38. You Z, Shi LZ, Zhu Q, Wu P, Zhang YW, Basilio A, et al. CtIP links DNA double-strand break sensing to resection. Mol Cell 2009; 36:954-69; PMID:20064462; http://dx.doi.org/10.1016/j.molcel.2009.12.002.
39. Ramírez-Lugo JS, Yoo HY, Yoon SJ, Dunphy WG. CtIP interacts with TopBP1 and Nbs1 in the response to double-stranded DNA breaks (DSBs) in Xenopus egg extracts. Cell Cycle 2011; 10:469-80; PMID:21263215; http://dx.doi.org/10. 4161/cc.10.3.14711.
40. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 2003; 421:499-506; PMID:12556884; http://dx.doi.org/10.1038/nature01368.
41. You Z, Chahwan C, Bailis J, Hunter T, Russell P. ATM activation and its recruitment to damaged DNA require binding to the C terminus of Nbs1. Mol Cell Biol 2005; 25:5363-79; PMID:15964794; http://dx.doi.org/10.1128/MCB.25.13.5363- 79.2005.
42. Hashimoto Y, Tsujimura T, Sugino A, Takisawa H. The phosphorylated C-terminal domain of Xenopus Cut5 directly mediates ATR-dependent activation of Chk1. Genes Cells 2006; 11:993-1007; PMID:16923121; http://dx.doi.org/10.1111/j. 1365-2443.2006.00998.x.
43. Cuadrado M, Martinez-Pastor B, Murga M, Toledo LI, Gutierrez-Martinez P, Lopez E, et al. ATM regulates ATR chromatin loading in response to DNA double-strand breaks. J Exp Med 2006; 203:297- 303; PMID:16461339; http://dx.doi.org/10.1084/jem.20051923.
44. Jazayeri A, Falck J, Lukas C, Bartek J, Smith GC, Lukas J, et al. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat Cell Biol 2006; 8:37-45; PMID:16327781; http:// dx.doi.org/10.1038/ ncb1337.
45. Myers JS, Cortez D. Rapid activation of ATR by ionizing radiation requires ATM and Mre11. J Biol Chem 2006; 281:9346-50; PMID:16431910; http://dx.doi.org/10.1074/jbc.M513265200.
46. McGarry TJ, Kirschner MW. Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell 1998; 93:1043-53; PMID:9635433; http://dx.doi.org/10.1016/S0092-8674(00)81209-X.
47. Hashimoto Y, Takisawa H. Xenopus Cut5 is essential for a CDK-dependent process in the initiation of DNA replication. EMBO J 2003; 22:2526-35; PMID:12743046; http://dx.doi.org/10.1093/emboj/cdg238.
48. Van Hatten RA, Tutter AV, Holway AH, Khederian AM, Walter JC, Michael WM. The Xenopus Xmus101 protein is required for the recruitment of Cdc45 to origins of DNA replication. J Cell Biol 2002; 159:541-7; PMID:12438414; http://dx.doi.org/10.1083/jcb.200207090.
49. You Z, Bailis JM, Johnson SA, Dilworth SM, Hunter T. Rapid activation of ATM on DNA flanking double-strand breaks. Nat Cell Biol 2007; 9:1311-8; PMID:17952060; http://dx.doi.org/10.1038/ncb1651.
50. Hardy CF, Sussel L, Shore DA. A RAP1-interacting protein involved in transcriptional silencing and telomere length regulation. Genes Dev 1992; 6:801-14; PMID:1577274; http://dx.doi.org/10.1101/gad.6.5.801.
51. Shore D, Bianchi A. Telomere length regulation: coupling DNA end processing to feedback regulation of telomerase. EMBO J 2009; 28:2309-22; PMID:19629031; http://dx.doi.org/10.1038/emboj.2009.195.
52. Xue Y, Rushton MD, Maringele L. A novel checkpoint and RPA inhibitory pathway regulated by Rif1. PLoS Genet 2011; 7:1002417; PMID:22194703; http:// dx.doi.org/10.1371/journal.pgen.1002417.
53. Morishima K, Sakamoto S, Kobayashi J, Izumi H, Suda T, Matsumoto Y, et al. TopBP1 associates with NBS1 and is involved in homologous recombination repair. Biochem Biophys Res Commun 2007; 362:872-9; PMID:17765870; http://dx.doi.org/10.1016/j.bbrc.2007.08.086.
54. Falck J, Coates J, Jackson SP. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage. Nature 2005; 434:605-11; PMID:15758953; http://dx.doi.org/10.1038/nature03442.
55. Bartek J, Lukas C, Lukas J. Checking on DNA damage in S phase. Nat Rev Mol Cell Biol 2004; 5:792-804; PMID:15459660; http://dx.doi.org/10.1038/nrm1493.
56. 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.
57. Zhu Z, Chung WH, Shim EY, Lee SE, Ira G. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 2008; 134:981-94; PMID:18805091; http://dx.doi.org/10.1016/j.cell.2008.08.037.
58. Cejka P, Cannavo E, Polaczek P, Masuda-Sasa T, Pokharel S, Campbell JL, et al. DNA end resection by Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2. Nature 2010; 467:112-6; PMID:20811461; http://dx.doi.org/10. 1038/nature09355.
59. Niu H, Chung WH, Zhu Z, Kwon Y, Zhao W, Chi P, et al. Mechanism of the ATP-dependent DNA end-resection machinery from Saccharomyces cerevisiae. Nature 2010; 467:108-11; PMID:20811460; http:// dx.doi.org/10.1038/nature09318.
60. Adams IR, McLaren A. Identification and characterisation of mRif1: a mouse telomere-associated protein highly expressed in germ cells and embryo-derived pluripotent stem cells. Dev Dyn 2004; 229:733-44; PMID:15042697; http://dx.doi.org/10.1002/dvdy.10471.
61. Murray AW. Cell cycle extracts. Methods Cell Biol 1991; 36:581-605; PMID:1839804; http://dx.doi.org/10.1016/S0091-679X(08)60298-8.
62. Lee J, Kumagai A, Dunphy WG. Claspin, a Chk1- regulatory protein, monitors DNA replication on chromatin independently of RPA ATR and Rad17. Mol Cell 2003; 11:329-40; PMID:12620222; http:// dx.doi.org/10.1016/S1097-2765(03) 00045-5.
63. Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 2006; 1:2856-60; PMID:17406544; http://dx.doi.org/10.1038/nprot.2006.468.
64. Junqueira M, Spirin V, Santana Balbuena T, Waridel P, Surendranath V, Kryukov G, et al. Separating the wheat from the chaff: unbiased filtering of background tandem mass spectra improves protein identification. J Proteome Res 2008; 7:3382-95; PMID:18558732; http://dx.doi.org/10.1021/pr800140v.
65. Carpenter PB, Mueller PR, Dunphy WG. Role for a Xenopus Orc2-related protein in controlling DNA replication. Nature 1996; 379:357-60; PMID:8552193; http://dx.doi.org/10.1038/379357a0.
66. Kumagai A, Kim SM, Dunphy WG. Claspin and the activated form of ATR-ATRIP collaborate in the activation of Chk1. J Biol Chem 2004; 279:49599- 608; PMID:15371427; http://dx.doi.org/10.1074/jbc.M408353200.