Role of replication protein A as sensor in activation of the S-phase checkpoint in Xenopus egg extracts

Nucleic Acids Research

Volumn 40, Issue 8, 2012, Pages 3431-3442

  Recolin, Bénédicte ^a   Van Der Laan, Siem ^a   Maiorano, Domenico ^a  

^a INSTITUTE OF HUMAN GENETICS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ATR PROTEIN; CAFFEINE; CHECKPOINT KINASE 1; DNA; REPLICATION FACTOR A; SINGLE STRANDED DNA;

ANIMAL CELL; ARTICLE; CELL CYCLE PARAMETERS; CELL CYCLE REGULATION; CONTROLLED STUDY; DNA DAMAGE CHECKPOINT; DNA SYNTHESIS; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REPLICATION FORK UNCOUPLING; S PHASE CELL CYCLE CHECKPOINT; ULTRAVIOLET IRRADIATION; XENOPUS;

ANIMALS; CAFFEINE; CELL EXTRACTS; DNA REPLICATION; OVUM; PHOSPHORYLATION; PROTEIN KINASES; REPLICATION PROTEIN A; S PHASE CELL CYCLE CHECKPOINTS; STRESS, PHYSIOLOGICAL; XENOPUS;

EID: 84860356328     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr1241     Document Type: Article

References (71)

1. Byun, T.S., Pacek, M., Yee, M.C., Walter, J.C. and Cimprich, K.A. (2005) Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev., 19, 1040-1052.
2. Zou, L. and Elledge, S.J. (2003) Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science, 300, 1542-1548.
3. Walter, J. and Newport, J. (2000) Initiation of eukaryotic DNA replication: origin unwinding and sequential chromatin association of Cdc45, RPA, and DNA polymerase alpha. Mol. Cell., 5, 617-627.
4. Lonn, U. and Lonn, S. (1988) Extensive regions of single-stranded DNA in aphidicolin-treated melanoma cells. Biochemistry, 27, 566-570.
5. Sogo, J.M., Lopes, M. and Foiani, M. (2002) Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science, 297, 599-602.
6. Feng, W., Collingwood, D., Boeck, M.E., Fox, L.A., Alvino, G.M., Fangman, W.L., Raghuraman, M.K. and Brewer, B.J. (2006) Genomic mapping of single-stranded DNA in hydroxyurea-challenged yeasts identifies origins of replication. Nat. Cell. Biol., 8, 148-155.
7. Shechter, D., Costanzo, V. and Gautier, J. (2004) ATR and ATM regulate the timing of DNA replication origin firing. Nat. Cell. Biol., 6, 648-655.
8. MacDougall, C.A., Byun, T.S., Van, C., Yee, M.C. and Cimprich, K.A. (2007) The structural determinants of checkpoint activation. Genes Dev., 21, 898-903.
9. Van, C., Yan, S., Michael, W.M., Waga, S. and Cimprich, K.A. (2010) Continued primer synthesis at stalled replication forks contributes to checkpoint activation. J. Cell. Biol., 189, 233-246.
10. Parrilla-Castellar, E.R., Arlander, S.J. and Karnitz, L. (2004) Dial 9-1-1 for DNA damage: the Rad9-Hus1-Rad1 (9-1-1) clamp complex. DNA Repair, 3, 1009-1014.
11. Bermudez, V.P., Lindsey-Boltz, L.A., Cesare, A.J., Maniwa, Y., Griffith, J.D., Hurwitz, J. and Sancar, A. (2003) 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, 100, 1633-1638.
12. Ellison, V. and Stillman, B. (2003) Biochemical characterization of DNA damage checkpoint complexes: clamp loader and clamp complexes with specificity for 5' recessed DNA. PLoS Biol., 1, E33.
13. Mimura, S., Masuda, T., Matsui, T. and Takisawa, H. (2000) Central role for cdc45 in establishing an initiation complex of DNA replication in Xenopus egg extracts. Genes Cells, 5, 439-452.
14. Michael, W.M., Ott, R., Fanning, E. and Newport, J. (2000) Activation of the DNA replication checkpoint through RNA synthesis by primase. Science, 289, 2133-2137.
15. Lupardus, P.J., Byun, T., Yee, M.C., Hekmat-Nejad, M. and Cimprich, K.A. (2002) A requirement for replication in activation of the ATR-dependent DNA damage checkpoint. Genes Dev., 16, 2327-2332.
16. Majka, J., Binz, S.K., Wold, M.S. and Burgers, P.M. (2006) Replication protein A directs loading of the DNA damage checkpoint clamp to 5'-DNA junctions. J. Biol. Chem., 281, 27855-27861.
17. Zou, L., Liu, D. and Elledge, S.J. (2003) Replication protein A-mediated recruitment and activation of Rad17 complexes. Proc. Natl Acad. Sci. USA, 100, 13827-13832.
18. Lee, J., Kumagai, A. and Dunphy, W.G. (2003) Claspin, a Chk1-regulatory protein, monitors DNA replication on chromatin independently of RPA, ATR, and Rad17. Mol. Cell., 11, 329-340.
19. Choi, J.H., Lindsey-Boltz, L.A., Kemp, M., Mason, A.C., Wold, M.S. and Sancar, A. (2010) Reconstitution of RPA-covered single-stranded DNA-activated ATR-Chk1 signaling. Proc. Natl Acad. Sci. USA, 107, 13660-13665.
20. Lucca, C., Vanoli, F., Cotta-Ramusino, C., Pellicioli, A., Liberi, G., Haber, J. and Foiani, M. (2004) Checkpoint-mediated control of replisome-fork association and signalling in response to replication pausing. Oncogene, 23, 1206-1213.
21. Kondo, T., Wakayama, T., Naiki, T., Matsumoto, K. and Sugimoto, K. (2001) Recruitment of Mec1 and Ddc1 checkpoint proteins to double-strand breaks through distinct mechanisms. Science, 294, 867-870.
22. Melo, J.A., Cohen, J. and Toczyski, D.P. (2001) Two checkpoint complexes are independently recruited to sites of DNA damage in vivo. Genes Dev., 15, 2809-2821.
23. Bonilla, C.Y., Melo, J.A. and Toczyski, D.P. (2008) Colocalization of sensors is sufficient to activate the DNA damage checkpoint in the absence of damage. Mol. Cell., 30, 267-276.
24. Ball, H.L., Myers, J.S. and Cortez, D. (2005) ATRIP binding to replication protein A-single-stranded DNA promotes ATR-ATRIP localization but is dispensable for Chk1 phosphorylation. Mol. Biol. Cell., 16, 2372-2381.
25. Dodson, G.E., Shi, Y. and Tibbetts, R.S. (2004) DNA replication defects, spontaneous DNA damage, and ATM-dependent checkpoint activation in replication protein A-deficient cells. J. Biol. Chem., 279, 34010-34014.
26. Wold, M.S. (1997) Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu. Rev. Biochem., 66, 61-92.
27. Sikorski, T.W., Ficarro, S.B., Holik, J., Kim, T., Rando, O.J., Marto, J.A. and Buratowski, S. (2011) Sub1 and RPA Associate with RNA Polymerase II at Different Stages of Transcription. Mol. Cell., 44, 397-409.
28. Adachi, Y. and Laemmli, U.K. (1994) Study of the cell cycle-dependent assembly of the DNA pre-replication centres in Xenopus egg extracts. EMBO J., 13, 4153-4164.
29. Waga, S. and Stillman, B. (1994) Anatomy of a DNA replication fork revealed by reconstitution of SV40 DNA replication in vitro. Nature, 369, 207-212.
30. Van Hatten, R.A., Tutter, A.V., Holway, A.H., Khederian, A.M., Walter, J.C. and Michael, W.M. (2002) The Xenopus Xmus101 protein is required for the recruitment of Cdc45 to origins of DNA replication. J. Cell. Biol., 159, 541-547.
31. Hashimoto, Y., Tsujimura, T., Sugino, A. and Takisawa, H. (2006) The phosphorylated C-terminal domain of Xenopus Cut5 directly mediates ATR-dependent activation of Chk1. Genes Cells, 11, 993-1007.
32. Parrilla-Castellar, E.R. and Karnitz, L.M. (2003) Cut5 is required for the binding of Atr and DNA polymerase alpha to genotoxin-damaged chromatin. J. Biol. Chem., 278, 45507-45511.
33. Murray, A.W. (1991) Cell cycle extracts. Methods Cell Biol., 36, 581-605.
34. Mechali, M. and Harland, R.M. (1982) DNA synthesis in a cell-free system from Xenopus eggs: priming and elongation on single-stranded DNA in vitro. Cell, 30, 93-101.
35. Jackson, P.K., Chevalier, S., Philippe, M. and Kirschner, M.W. (1995) Early events in DNA replication require cyclin E and are blocked by p21CIP1. J. Cell. Biol., 130, 755-769.
36. Coue, M., Amariglio, F., Maiorano, D., Bocquet, S. and Mechali, M. (1998) Evidence for different MCM subcomplexes with differential binding to chromatin in Xenopus. Exp. Cell Res., 245, 282-289.
37. Jones, R.E., Chapman, J.R., Puligilla, C., Murray, J.M., Car, A.M., Ford, C.C. and Lindsay, H.D. (2003) XRad17 is required for the activation of XChk1 but not XCds1 during checkpoint signaling in Xenopus. Mol. Biol. Cell., 14, 3898-3910.
38. Costanzo, V., Robertson, K., Bibikova, M., Kim, E., Grieco, D., Gottesman, M., Carroll, D. and Gautier, J. (2001) Mre11 protein complex prevents double-strand break accumulation during chromosomal DNA replication. Mol. Cell., 8, 137-147.
39. Liao, S., Toczylowski, T. and Yan, H. (2008) Identification of the Xenopus DNA2 protein as a major nuclease for the 5'-3' strand-specific processing of DNA ends. Nucleic Acids Res., 36, 6091-6100.
40. Liao, S., Toczylowski, T. and Yan, H. (2011) Mechanistic analysis of Xenopus EXO1's function in 5'-strand resection at DNA double-strand breaks. Nucleic Acids Res., 39, 5967-5977.
41. Maiorano, D., Cuvier, O., Danis, E. and Mechali, M. (2005) MCM8 is an MCM2-7-related protein that functions as a DNA helicase during replication elongation and not initiation. Cell, 120, 315-328.
42. Hekmat-Nejad, M., You, Z., Yee, M.C., Newport, J.W. and Cimprich, K.A. (2000) Xenopus ATR is a replication-dependent chromatin-binding protein required for the DNA replication checkpoint. Curr. Biol., 10, 1565-1573.
43. Maiorano, D., Rul, W. and Mechali, M. (2004) Cell cycle regulation of the licensing activity of Cdt1 in Xenopus laevis. Exp. Cell Res., 295, 138-149.
44. Francon, P., Lemaitre, J.M., Dreyer, C., Maiorano, D., Cuvier, O. and Mechali, M. (2004) A hypophosphorylated form of RPA34 is a specific component of pre-replication centers. J. Cell Sci., 117, 4909-4920.
45. Groth, A., Ray-Gallet, D., Quivy, J.P., Lukas, J., Bartek, J. and Almouzni, G. (2005) Human Asf1 regulates the flow of S phase histones during replicational stress. Mol. Cell., 17, 301-311.
46. Stokes, M.P., Van Hatten, R., Lindsay, H.D. and Michael, W.M. (2002) DNA replication is required for the checkpoint response to damaged DNA in Xenopus egg extracts. J. Cell. Biol., 158, 863-872.
47. Hubscher, U., Maga, G. and Spadari, S. (2002) Eukaryotic DNA polymerases. Annu. Rev. Biochem., 71, 133-163.
48. Raschle, M., Knipscheer, P., Enoiu, M., Angelov, T., Sun, J., Griffith, J.D., Ellenberger, T.E., Scharer, O.D. and Walter, J.C. (2008) Mechanism of replication-coupled DNA interstrand crosslink repair. Cell, 134, 969-980.
49. Kannouche, P.L. and Lehmann, A.R. (2004) Ubiquitination of PCNA and the polymerase switch in human cells. Cell Cycle, 3, 1011-1013.
50. Paulsen, R.D., Soni, D.V., Wollman, R., Hahn, A.T., Yee, M.C., Guan, A., Hesley, J.A., Miller, S.C., Cromwell, E.F., Solow-Cordero, D.E. et al. (2009) A genome-wide siRNA screen reveals diverse cellular processes and pathways that mediate genome stability. Mol. Cell., 35, 228-239.
51. Lovejoy, C.A., Xu, X., Bansbach, C.E., Glick, G.G., Zhao, R., Ye, F., Sirbu, B.M., Titus, L.C., Shyr, Y. and Cortez, D. (2009) Functional genomic screens identify CINP as a genome maintenance protein. Proc. Natl Acad. Sci. USA, 106, 19304-19309.
52. McGarry, T.J. and Kirschner, M.W. (1998) Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell, 93, 1043-1053.
53. Crevel, G., Hashimoto, R., Vass, S., Sherkow, J., Yamaguchi, M., Heck, M.M. and Cotterill, S. (2007) Differential requirements for MCM proteins in DNA replication in Drosophila S2 cells. PLoS One, 2, e833.
54. You, Z., Kong, L. and Newport, J. (2002) The role of single-stranded DNA and polymerase alpha in establishing the ATR, Hus1 DNA replication checkpoint. J. Biol. Chem., 277, 27088-27093.
55. Liu, S., Chu, J., Yucer, N., Leng, M., Wang, S.Y., Chen, B.P., Hittelman, W.N. and Wang, Y. (2011) RFWD3 associates with replication protein A and facilitates RPA-mediated DNA damage response. J. Biol. Chem., 286, 22314-22322.
56. Liu, Y., Vaithiyalingam, S., Shi, Q., Chazin, W.J. and Zinkel, S.S. (2011) BID binds to replication protein A and stimulates ATR function following replicative stress. Mol. Cell. Biol, 31, 4298-4309.
57. Schlacher, K., Christ, N., Siaud, N., Egashira, A., Wu, H. and Jasin, M. (2011) Double-strand break repair-independent role for BRCA2 in blocking stalled replication fork degradation by MRE11. Cell, 145, 529-542.
58. Shiotani, B. and Zou, L. (2009) Single-stranded DNA orchestrates an ATM-to-ATR switch at DNA breaks. Mol. Cell., 33, 547-558.
59. Kumagai, A., Lee, J., Yoo, H.Y. and Dunphy, W.G. (2006) TopBP1 activates the ATR-ATRIP complex. Cell, 124, 943-955.
60. Mordes, D.A., Glick, G.G., Zhao, R. and Cortez, D. (2008) TopBP1 activates ATR through ATRIP and a PIKK regulatory domain. Genes Dev., 22, 1478-1489.
61. Lindsey-Boltz, L.A. and Sancar, A. (2011) Tethering DNA damage checkpoint mediator proteins topoisomerase II{beta}-binding protein 1 (TopBP1) and claspin to DNA activates ataxia-telangiectasia mutated and RAD3-related (ATR) phosphorylation of checkpoint kinase 1 (Chk1). J. Biol. Chem., 286, 19229-19236.
62. Dorneiter, I., Erdile, L.F., Gilbert, I.U., von Winkler, D., kelly, T.J. and Fanning, E. (1992) Interaction of DNA polymerase a-primase with cellular replication protein A and SV40 T antigen. EMBO J., 11, 769-776.
63. Melendy, T. and Stillman, B. (1993) An interaction between replication protein A and SV40 T antigen appears essential for primosome assembly during SV40 DNA replication. J. Biol. Chem., 268, 3389-3395.
64. Gambus, A., van Deursen, F., Polychronopoulos, D., Foltman, M., Jones, R.C., Edmondson, R.D., Calzada, A. and Labib, K. (2009) A key role for Ctf4 in coupling the MCM2-7 helicase to DNA polymerase alpha within the eukaryotic replisome. EMBO J., 28, 2992-3004.
65. Maiorano, D., Blom van Assendelft, G. and Kearsey, S.E. (1996) Fission yeast cdc21, a member of the MCM protein family, is required for onset of S phase and is located in the nucleus throughout the cell cycle. EMBO J., 15, 861-872.
66. Nasmyth, K. and Nurse, P. (1981) Cell division cycle mutants altered in DNA replication and mitosis in the fission yeast Schizosaccharomyces pombe. Mol. Gen. Genet., 182, 119-124.
67. Haring, S.J., Mason, A.C., Binz, S.K. and Wold, M.S. (2008) Cellular functions of human RPA1. Multiple roles of domains in replication, repair, and checkpoints. J. Biol. Chem., 283, 19095-19111.
68. Wang, Y., Putnam, C.D., Kane, M.F., Zhang, W., Edelmann, L., Russell, R., Carrion, D.V., Chin, L., Kucherlapati, R., Kolodner, R.D. et al. (2005) Mutation in Rpa1 results in defective DNA double-strand break repair, chromosomal instability and cancer in mice. Nat. Genet., 37, 750-755.
69. Shima, N., Alcaraz, A., Liachko, I., Buske, T.R., Andrews, C.A., Munroe, R.J., Hartford, S.A., Tye, B.K. and Schimenti, J.C. (2007) A viable allele of Mcm4 causes chromosome instability and mammary adenocarcinomas in mice. Nat. Genet., 39, 93-98.
70. Gorgoulis, V.G., Vassiliou, L.V., Karakaidos, P., Zacharatos, P., Kotsinas, A., Liloglou, T., Venere, M., Ditullio, R.A. Jr, Kastrinakis, N.G., Levy, B. et al. (2005) Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature, 434, 907-913.
71. Bartkova, J., Horejsi, Z., Koed, K., Kramer, A., Tort, F., Zieger, K., Guldberg, P., Sehested, M., Nesland, J.M., Lukas, C. et al. (2005) DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature, 434, 864-870.