More forks on the road to replication stress recovery

Journal of Molecular Cell Biology

Volumn 3, Issue 1, 2011, Pages 4-12

  Allen, Chris ^a   Ashley, Amanda K ^a   Hromas, Robert ^b   Nickoloff, Jac A ^a  

^a Veterinary Dentistry and Oral Surgery   (United States)

^b UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

Author keywords

Cancer therapy; DNA repair; Genome instability

Indexed keywords

EID: 79951470434     PISSN: 16742788     EISSN: 17594685     Source Type: Journal    
DOI: 10.1093/jmcb/mjq049     Document Type: Article

References (123)

1. Adachi, N., So, S., and Koyama, H. (2004). Loss of nonhomologous end joining confers camptothecin resistance in DT40 cells. Implications for the repair of to (Pubitemid 39195442)
2. Ahnesorg, P., Smith, P., and Jackson, S. P. (2006). XLF interacts with the XRCC4-DNA ligase IV complex to promote DNA nonhomologous end-joining. Cell 124, 301-313. (Pubitemid 43121979)
3. Allen, C., Kurimasa, A., Brennemann, M. A., et al. (2002). DNA-dependent protein kinase suppresses double-strand break-induced and spontaneous homologous recombination. Proc. Natl. Acad. Sci. USA 99, 3758-3763. (Pubitemid 34252179)
4. Anantha, R. W., Vassin, V. M., and Borowiec, J. A. (2007). Sequential and synergistic modification of human RPA stimulates chromosomal DNA repair. J. Biol. Chem. 282, 35910-35923. (Pubitemid 350277090)
5. Arnaudeau, C., Lundin, C., and Helleday, T. (2001). DNA double-strand breaks associated with replication forks are predominantly repaired by homologous recombination involving an exchange mechanism in mammalian cells. J. Mol. Biol. 307, 1235-1245. (Pubitemid 33027636)
6. Baskaran, R., Wood, L. D., Whitaker, L. L., et al. (1997). Ataxia telangiectasia mutant protein activates c-Abl tyrosine kinase in response to ionizing radiation. Nature 387, 516-519. (Pubitemid 27235471)
7. Benson, F. E., Baumann, P., and West, S. C. (1998). Synergistic actions of Rad51 and Rad52 in recombination and DNA repair. Nature 391, 401-404. (Pubitemid 28093516)
8. Beucher, A., Birraux, J., Tchouandong, L., et al. (2009). ATM and Artemis promote homologous recombination of radiation-induced DNA doublestrand breaks in G2. EMBO J. 28, 3413-3427.
9. Block, W. D., Yu, Y., and Lees-Miller, S. P. (2004). Phosphatidyl inositol 3-kinase-like serine/threonine protein kinases (PIKKs) are required for DNA damage-induced phosphorylation of the 32 kDa subunit of replication protein A at threonine 21. Nucleic Acids Res. 32, 997-1005. (Pubitemid 38854700)
10. Boubnov, N. V., Hall, K. T., Wills, Z., et al. (1995). Complementation of the ionizing radiation sensitivity, DNA end binding, and V (D) J recombination defects of double-strand break repair mutants by the p86 Ku autoantigen. Proc. Natl. Acad. Sci. USA 92, 890-894.
11. Branzei, D., and Foiani, M. (2009). The checkpoint response to replication stress. DNA Repair 8, 1038-1046.
12. Branzei, D., and Foiani, M. (2010). Maintaining genome stability at the replication fork. Nat. Rev. Mol. Cell Biol. 11, 208-219.
13. Bryant, H. E., Petermann, E., Schultz, N., et al. (2009). PARP is activated at stalled forks to mediate Mre11-dependent replication restart and recombination. EMBO J. 28, 2601-2615.
14. Budzowska, M., and Kanaar, R. (2009). Mechanisms of dealing with DNA damage-induced replication problems. Cell Biochem. Biophys. 53, 17-31.
15. Burma, S., Chen, B. P., Murphy, M., et al. (2001). ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J. Biol. Chem. 276, 42462-42467.
16. Chan, D. W., Chen, B. P.-C., Prithivirasingh, S., et al. (2002). Autophosphorylation of the DNA-dependent protein kinase catalytic subunit is required for rejoining of DNA double-strand breaks. Genes Dev. 16, 2333-2338. (Pubitemid 35034402)
17. Chanoux, R. A., Yin, B., Urtishak, K. A., et al. (2008). ATR and H2AX cooperate in maintaining genome stability under replication stress. J. Biol. Chem. 284, 5994-6003.
18. Chen, B. P., Chan, D. W., Kobayashi, J., et al. (2005). Cell cycle dependence of DNA-dependent protein kinase phosphorylation in response to DNA double strand breaks. J. Biol. Chem. 280, 14709-14715. (Pubitemid 40562818)
19. Chen, B. P., Uematsu, N., Kobayashi, J., et al. (2007). Ataxia telangiectasia mutated (ATM) is essential for DNA-PKcs phosphorylations at the Thr-2609 cluster upon DNA double strand break. J. Biol. Chem. 282, 6582-6587. (Pubitemid 47100815)
20. Ciccia, A., and Elledge, S. J. (2010). The DNA damage response: making it safe to play with knives. Mol. Cell 40, 179-204.
21. Cimprich, K. A., and Cortez, D. (2008). ATR: an essential regulator of genome integrity. Nat. Rev. Mol. Cell Biol. 9, 616-627. (Pubitemid 352032926)
22. Cordaux, R., Udit, S., Batzer, M. A., et al. (2006). Birth of a chimeric primate gene by capture of the transposase gene from a mobile element. Proc. Natl. Acad. Sci. USA 103, 8101-8106. (Pubitemid 43801059)
23. Cruet-Hennequart, S., Coyne, S., Glynn, M. T., et al. (2006). UV-induced RPA phosphorylation is increased in the absence of DNA polymerase eta and requires DNA-PK. DNA Repair 5, 491-504.
24. Cruet-Hennequart, S., Glynn, M. T., Murillo, L. S., et al. (2008). Enhanced DNA-PK-mediated RPA2 hyperphosphorylation in DNA polymerase etadeficient human cells treated with cisplatin and oxaliplatin. DNA Repair 7, 582-596.
25. Davies, S. L., North, P. S., and Hickson, I. D. (2007). Role for BLM in replicationfork restart and suppression of origin firing after replicative stress. Nat. Struct. Mol. Biol. 14, 677-679. (Pubitemid 47037072)
26. Davis, A. P., and Symington, L. S. (2004). RAD51-dependent break-induced replication in yeast. Mol. Cell. Biol. 24, 2344-2351. (Pubitemid 38325991)
27. De Haro, L. P., Wray, J., Williamson, E. A., et al. (2010). Metnase promotes restart and repair of stalled and collapsed replication forks. Nucleic Acids Res. 38, 5681-5691.
28. Deininger, P. L., and Batzer, M. A. (1999). Alu repeats and human disease. Mol. Genet. Metab. 67, 183-193. (Pubitemid 29390169)
29. Doe, C. L., Ahn, J. S., Dixon, J., et al. (2002). Mus81-Eme1 and Rqh1 involvement in processing stalled and collapsed replication forks. J. Biol. Chem. 277, 32753-32759. (Pubitemid 34984783)
30. Doksani, Y., Bermejo, R., Fiorani, S., et al. (2009). Replicon dynamics, dormant origin firing, and terminal fork integrity after double-strand break formation. Cell 137, 247-258.
31. Downey, M., and Durocher, D. (2006). γH2AX as a checkpoint maintenance signal. Cell Cycle 5, 1376-1381.
32. Elliott, B., Richardson, C., and Jasin, M. (2005). Chromosomal translocation mechanisms at intronic alu elements in mammalian cells. Mol. Cell 17, 885-894. (Pubitemid 40386948)
33. Fanning, E., Klimovich, V., and Nager, A. R. (2006). A dynamic model for replication protein A (RPA) function in DNA processing pathways. Nucleic Acids Res. 34, 4126-4137. (Pubitemid 44542191)
34. Feng, J., Wakeman, T., Yong, S., et al. (2009). Protein phosphatase 2A-dependent dephosphorylation of replication protein A is required for the repair of DNA breaks induced by replication stress. Mol. Cell. Biol. 29, 5696-5709.
35. Fried, L. M., Koumenis, C., Peterson, S. R., et al. (1996). The DNA damage response in DNA-dependent kinase-deficient SCID mouse cells: replication protein A hyperphosphorylation and p53 induction. Proc. Natl. Acad. Sci. USA 93, 13825-13830.
36. Gangloff, S., Soustelle, C., and Fabre, F. (2000). Homologous recombination is responsible for cell death in the absence of the Sgs1 and Srs2 helicases. Nat. Genet. 25, 192-194. (Pubitemid 30394991)
37. Gu, J., Li, S., Zhang, X., et al. (2010). DNA-PKcs regulates a single-stranded DNA endonuclease activity of Artemis. DNA Repair 9, 429-437.
38. Hanks, S., Coleman, K., Reid, S., et al. (2004). Constitutional aneuploidy and cancer predisposition caused by biallelic mutations in BUB1B. Nat. Genet. 36, 1159-1161. (Pubitemid 41288963)
39. Hastings, P. J., Lupski, J. R., Rosenberg, S. M., et al. (2009). Mechanisms of change in gene copy number. Nat. Rev. Genet. 10, 551-564.
40. Hayden, E. C. (2008). Cancer complexity slows quest for cure. Nature 455, 148.
41. Helleday, T., Petermann, E., Lundin, C., et al. (2008). DNA repair pathways as targets for cancer therapy. Nat. Rev. Cancer 8, 193-204. (Pubitemid 351301852)
42. Hromas, R., Wray, J., Lee, S. H., et al. (2008). The human set and transposase domain protein Metnase interacts with DNA Ligase IV and enhances the efficiency and accuracy of non-homologous end-joining. DNA Repair 7, 1927-1937.
43. Hutchinson, L. (2010). Targeted therapies: PARP inhibitor olaparib is safe and effective in patients with BRCA1 and BRCA2 mutations. Nat. Rev. Clin. Oncol. 7, 549-549.
44. Kastan, M. B., Lim, D. S., Kim, S. T., et al. (2001). ATM-a key determinant of multiple cellular responses to irradiation. Acta Oncol. 40, 686-688. (Pubitemid 33081975)
45. Kaygun, H., and Marzluff, W. F. (2005). Regulated degradation of replicationdependent histone mRNAs requires both ATR and Upf1. Nat. Struct. Mol. Biol. 12, 794-800. (Pubitemid 43086254)
46. Kemp, M. G., Akan, Z., Yilmaz, S., et al. (2010). Tipin-replication protein A interaction mediates Chk1 phosphorylation by ATR in response to genotoxic stress. J. Biol. Chem. 285, 16562-16571.
47. Kitagawa, R., Bakkenist, C. J., McKinnon, P. J., et al. (2004). Phosphorylation of SMC1 is a critical downstream event in the ATM-NBS1-BRCA1 pathway. Genes Dev. 18, 1423-1438. (Pubitemid 38780629)
48. Kolomietz, E., Meyn, M. S., Pandita, A., et al. (2002). The role of Alu repeat clusters as mediators of recurrent chromosomal aberrations in tumors. Genes Chromosomes Cancer 35, 97-112. (Pubitemid 34919966)
49. Krishna, S., Wagener, B. M., Liu, H. P., et al. (2007). Mre11 and Ku regulation of double-strand break repair by gene conversion and break-induced replication. DNA Repair 6, 797-808. (Pubitemid 46670092)
50. Lee, S. H., Oshige, M., Durant, S. T., et al. (2005). The SET domain protein Metnase mediates foreign DNA integration and links integration to nonhomologous end-joining repair. Proc. Natl. Acad. Sci. USA 102, 18075-18080. (Pubitemid 41798504)
51. Lettier, G., Feng, Q., de Mayolo, A. A., et al. (2006). The role of DNA doublestrand breaks in spontaneous homologous recombination in S. cerevisiae. PLoS Genet. 2, 1773-1786. (Pubitemid 44813575)
52. Liberi, G., Maffioletti, G., Lucca, C., et al. (2005). Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes Dev. 19, 339-350. (Pubitemid 40189297)
53. Lisby, M., Rothstein, R., and Mortensen, U. H. (2001). Rad52 forms DNA repair and recombination centers during S phase. Proc. Natl. Acad. Sci. USA 98, 8276-8282. (Pubitemid 32678024)
54. Lisby, M., Mortensen, U. H., and Rothstein, R. (2003). Colocalization of multiple DNA double-strand breaks at a single Rad52 repair centre. Nat. Cell Biol. 5, 572-577. (Pubitemid 36781093)
55. Llorente, B., Smith, C. E., and Symington, L. S. (2008). Break-induced replication: what is it and what is it for? Cell Cycle 7, 859-864. (Pubitemid 351573777)
56. Lobrich, M., and Jeggo, P. A. (2005). Harmonising the response to DSBs: a new string in the ATM bow. DNA Repair 4, 749-759. (Pubitemid 40835847)
57. Lundin, C., Erixon, K., Arnaudeau, C., et al. (2002). Different roles for nonhomologous end joining and homologous recombination following replication arrest in mammalian cells. Mol. Cell. Biol. 22, 5869-5878. (Pubitemid 34815835)
58. Lydeard, J. R., Jain, S., Yamaguchi, M., et al. (2007). Break-induced replication and telomerase-independent telomere maintenance require Pol32. Nature 448, 820-823. (Pubitemid 47266343)
59. Machida, Y. J., Hamlin, J. L., and Dutta, A. (2005). Right place, right time, and only once: replication initiation in metazoans. Cell 123, 13-24. (Pubitemid 41414525)
60. Malkova, A., Signon, L., Schaefer, C. B., et al. (2001). RAD51-independent break-induced replication to repair a broken chromosome depends on a distant enhancer site. Genes Dev. 15, 1055-1060. (Pubitemid 32417298)
61. Manthey, K. C., Opiyo, S., Glanzer, J. G., et al. (2007). NBS1 mediates ATR-dependent RPA hyperphosphorylation following replication-fork stall and collapse. J. Cell Sci. 120, 4221-4229.
62. Manthey, K. C., Glanzer, J. G., Dimitrova, D. D., et al. (2010). Hyperphosphorylation of replication protein A in cisplatin-resistant and-sensitive head and neck squamous cell carcinoma cell lines. Head Neck 32, 636-645.
63. Matheos, D., Ruiz, M. T., Price, G. B., et al. (2002). Ku antigen, an origin-specific binding protein that associates with replication proteins, is required for mammalian DNA replication. Biochim. Biophys. Acta 1578, 59-72. (Pubitemid 35223457)
64. McNeely, S., Conti, C., Sheikh, T., et al. (2010). Chk1 inhibition after replicative stress activates a double strand break response mediated by ATM and DNA-dependent protein kinase. Cell Cycle 9, 995-1004.
65. Miyoshi, T., Kanoh, J., and Ishikawa, F. (2009). Fission yeast Ku protein is required for recovery from DNA replication stress. Genes Cells 14, 1091-1103.
66. Moldovan, G. L., Pfander, B., and Jentsch, S. (2007). PCNA, the maestro of the replication fork. Cell 129, 665-679. (Pubitemid 46802385)
67. Montecucco, A., Rossi, R., Ferrari, G., et al. (2001). Etoposide induces the dispersal of DNA ligase I from replication factories. Mol. Biol. Cell 12, 2109-2118. (Pubitemid 33049703)
68. Muller, B., Blackburn, J., Feijoo, C., et al. (2007). DNA-activated protein kinase functions in a newly observed S phase checkpoint that links histone mRNA abundance with DNA replication. J. Cell Biol. 179, 1385-1398.
69. Nick McElhinny, S. A., Snowden, C. M., McCarville, J., et al. (2000). Ku recruits the XRCC4-ligase IV complex to DNA ends. Mol. Cell. Biol. 20, 2996-3003. (Pubitemid 30215012)
70. Niimi, A., Brown, S., Sabbioneda, S., et al. (2008). Regulation of proliferating cell nuclear antigen ubiquitination in mammalian cells. Proc. Natl. Acad. Sci. USA 105, 16125-16130.
71. Nuss, J. E., Patrick, S. M., Oakley, G. G., et al. (2005). DNA damage induced hyperphosphorylation of replication protein A. 1. Identification of novel sites of phosphorylation in response to DNA damage. Biochemistry 44, 8428-8437. (Pubitemid 40799923)
72. Oakley, G. G., Patrick, S. M., Yao, J., et al. (2003). RPA phosphorylation in mitosis alters DNA binding and protein-protein interactions. Biochemistry 42, 3255-3264. (Pubitemid 36348634)
73. Oakley, G. G., Tillison, K., Opiyo, S. A., et al. (2009). Physical interaction between replication protein A (RPA) and MRN: involvement of RPA2 phosphorylation and the N-terminus of RPA1. Biochemistry 48, 7473-7481.
74. Park, S. J., Ciccone, S. L., Freie, B., et al. (2004). A positive role for the Ku complex in DNA replication following strand break damage in mammals. J. Biol. Chem. 279, 6046-6055. (Pubitemid 38220637)
75. Peng, Y., Woods, R. G., Beamish, H., et al. (2005). Deficiency in the catalytic subunit of DNA-dependent protein kinase causes down-regulation of ATM. Cancer Res. 65, 1670-1677. (Pubitemid 40478591)
76. Petermann, E., and Helleday, T. (2010). Pathways of mammalian replication fork restart. Nat. Rev. Mol. Cell Biol. 11, 683-687.
77. Pierce, A. J., Hu, P., Han, M. G., et al. (2001). Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev. 15, 3237-3242. (Pubitemid 34008189)
78. Rampakakis, E., Di Paola, D., and Zannis-Hadjopoulos, M. (2008). Ku is involved in cell growth, DNA replication and G1-S transition. J. Cell Sci. 121, 590-600. (Pubitemid 351524157)
79. Ramsden, D. A., and Gellert, M. (1998). Ku protein stimulates DNA end joining by mammalian DNA ligases: a direct role for Ku in repair of DNA doublestrand breaks. EMBO J. 17, 609-614. (Pubitemid 28045500)
80. Rijkers, T., Vandenouweland, J., Morolli, B., et al. (1998). Targeted inactivation of mouse RAD52 reduces homologous recombination but not resistance to ionizing radiation. Mol. Cell. Biol. 18, 6423-6429. (Pubitemid 28500532)
81. Robison, J. G., Elliott, J., Dixon, K., et al. (2004). Replication protein A and the Mre11. Rad50. Nbs1 complex co-localize and interact at sites of stalled replication forks. J. Biol. Chem. 279, 34802-34810. (Pubitemid 39318113)
82. Robison, J. G., Lu, L., Dixon, K., et al. (2005). DNA lesion-specific co-localization of the Mre11/Rad50/Nbs1 (MRN) complex and replication protein A (RPA) to repair foci. J. Biol. Chem. 280, 12927-12934.
83. Roman, Y., Oshige, M., Lee, Y.-J., et al. (2007). Biochemical characterization of a SET and transposase fusion protein, Metnase (SETMAR) for its DNA binding and DNA cleavage activity. Biochemistry 46, 11369-11376. (Pubitemid 47556764)
84. Rossi, R., Lidonnici, M. R., Soza, S., et al. (2006). The dispersal of replication proteins after etoposide treatment requires the cooperation of Nbs1 with the Ataxia telangiectasia Rad3-related/Chk1 pathway. Cancer Res. 66, 1675-1683. (Pubitemid 43259952)
85. Saintigny, Y., Delacote, F., Vares, G., et al. (2001). Characterization of homologous recombination induced by replication inhibition in mammalian cells. EMBO J. 20, 3861-3870. (Pubitemid 32694383)
86. Saleh-Gohari, N., Bryant, H. E., Schultz, N., et al. (2005). Spontaneous homologous recombination is induced by collapsed replication forks that are caused by endogenous DNA single-strand breaks. Mol. Cell. Biol. 25, 7158-7169. (Pubitemid 41105912)
87. Schwartz, M., Oren, Y. S., Bester, A. C., et al. (2009). Impaired replication stress response in cells from immunodeficiency patients carrying Cernunnos/XLF mutations. PLoS One 4, e4516.
88. Shao, R. G., Cao, C. X., Zhang, H., et al. (1999). Replication-mediated DNA damage by camptothecin induces phosphorylation of RPA by DNA-dependent protein kinase and dissociates RPA:DNA-PK complexes. EMBO J. 18, 1397-1406. (Pubitemid 29110323)
89. Sharma, S., Otterlei, M., Sommers, J. A., et al. (2004). WRN helicase and FEN-1 form a complex upon replication arrest and together process branch migrating DNA structures associated with the replication fork. Mol. Biol. Cell 15, 734-750. (Pubitemid 38146489)
90. Shen, Z., and Nickoloff, J. A. (2007). Mammalian homologous recombination repair and cancer intervention. In DNA Repair, Genetic Instability, and Cancer, Q. Wei, L. Li, and D. J. Chen, eds. (Singapore: World Scientific Publishing Co.), pp. 119-156.
91. Shen, Z., Denison, K., Lobb, R., et al. (1995). The human and mouse homologs of the yeast RAD52 gene: cDNA cloning, sequence analysis, assignment to human chromosome 12p12.2-p13, and mRNA expression in mouse tissues. Genomics 25, 199-206.
92. Shimada, K., Oma, Y., Schleker, T., et al. (2008). Ino80 chromatin remodeling complex promotes recovery of stalled replication forks. Curr. Biol. 18, 566-575.
93. Shimura, T., Martin, M. M., Torres, M. J., et al. (2007). DNA-PK is involved in repairing a transient surge of DNA breaks induced by deceleration of DNA replication. J. Mol. Biol. 367, 665-680. (Pubitemid 46330376)
94. Shimura, T., Torres, M. J., Martin, M. M., et al. (2008). Bloom's syndrome helicase and Mus81 are required to induce transient double-strand DNA breaks in response to DNA replication stress. J. Mol. Biol. 375, 1152-1164. (Pubitemid 350309393)
95. Shrivastav, M., De Haro, L. P., and Nickoloff, J. A. (2008). Regulation of DNA double-strand break repair pathway choice. Cell Res. 18, 134-147.
96. Shrivastav, M., Miller, C. A., De Haro, L. P., et al. (2009). DNA-PKcs and ATM co-regulate DNA double-strand break repair. DNA Repair 8, 920-929.
97. Smits, V. A., Warmerdam, D. O., Martin, Y., et al. (2010). Mechanisms of ATR-mediated checkpoint signalling. Front. Biosci. 15, 840-853.
98. Sonoda, E., Sasaki, M. S., Buerstedde, J. M., et al. (1998). Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J. 17, 598-608. (Pubitemid 28045499)
99. Stephan, H., Concannon, C., Kremmer, E., et al. (2009). Ionizing radiationdependent and independent phosphorylation of the 32-kDa subunit of replication protein A during mitosis. Nucleic Acids Res. 37, 6028-6041.
100. Strout, M. P., Marcucci, G., Bloomfield, C. D., et al. (1998). The partial tandem duplication of ALL1 (MLL) is consistently generated by ALU-mediated homologous recombination in acute myeloid leukemia. Proc. Natl. Acad. Sci. USA 95, 2390-2395. (Pubitemid 28145951)
101. Taylor, J. H., and Hozier, J. C. (1976). Evidence for a four micron replication unit in CHO cells. Chromosoma 57, 341-350.
102. Teo, S. H., and Jackson, S. P. (1997). Identification of Saccharomyces cerevisiae DNA ligase IV: involvement in DNA double-strand break repair. EMBO J. 16, 4788-4795. (Pubitemid 27326616)
103. Tutt, A., Bertwistle, D., Valentine, J., et al. (2001). Mutation in Brca2 stimulates error-prone homology-directed repair of DNA double-strand breaks occurring between repeated sequences. EMBO J. 20, 4704-4716. (Pubitemid 32848624)
104. Ui, A., Seki, M., Ogiwara, H., et al. (2005). The ability of Sgs1 to interact with DNA topoisomerase III is essential for damage-induced recombination. DNA Repair 4, 191-201. (Pubitemid 39601407)
105. van Veelen, L. R., Essers, J., van de Rakt, M. W., et al. (2005). Ionizing radiation-induced foci formation of mammalian Rad51 and Rad54 depends on the Rad51 paralogs, but not on Rad52. Mutat. Res. 574, 34-49. (Pubitemid 40725966)
106. Wang, H., Guan, J., Perrault, A. R., et al. (2001). Replication protein A2 phosphorylation after DNA damage by the coordinated action of Ataxia telangiectasia-mutated and DNA-dependent protein kinase. Cancer Res. 61, 8554-8563. (Pubitemid 33131139)
107. Wang, H., Zhang, X., Geng, L., et al. (2009). Artemis regulates cell cycle recovery from the S phase checkpoint by promoting degradation of cyclin E. J. Biol. Chem. 284, 18236-18243.
108. Ward, I. M., and Chen, J. (2001). Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J. Biol. Chem. 276, 47759-47762.
109. Warmerdam, D. O., Kanaar, R., and Smits, V. A. (2010). Differential dynamics of ATR-mediated checkpoint regulators. J. Nucleic Acids. doi: 10.4061/2010/319142.
110. Weinstock, D. M., Richardson, C. A., Elliott, B., et al. (2006). Modeling oncogenic translocations: distinct roles for double-strand break repair pathways in translocation formation in mammalian cells. DNA Repair 5, 1065-1074. (Pubitemid 44291619)
111. West, S. C. (2003). Molecular views of recombination proteins and their control. Nat. Rev. Mol. Cell Biol. 4, 435-445. (Pubitemid 36648589)
112. Williamson, E. A., Farrington, J., Martinez, L., et al. (2008a). Expression levels of the human DNA repair protein Metnase influence lentiviral genomic integration. Biochimie 90, 1422-1426.
113. Williamson, E. A., Rasila, K. K., Corwin, L. K., et al. (2008b). The SET and transposase domain protein Metnase enhances chromosome decatenation: regulation by automethylation. Nucleic Acids Res. 36, 5822-5831.
114. 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. (Pubitemid 27274652)
115. Wray, J., Liu, J., Nickoloff, J. A., et al. (2008). Distinct RAD51 associations with RAD52 and BCCIP in response to DNA damage and replication stress. Cancer Res. 68, 2699-2707. (Pubitemid 351556267)
116. Wray, J., Williamson, E. A., Fnu, S., et al. (2009a). Metnase mediates chromosome decatenation in acute leukemia cells. Blood 114, 1852-1858.
117. Wray, J., Williamson, E. A., Royce, M., et al. (2009b). Metnase mediates resistance to topoisomerase II inhibitors in breast cancer cells. PLoS One 4, e5323.
118. Wu, L., and Hickson, I. D. (2003). The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426, 870-874. (Pubitemid 38056876)
119. Yajima, H., Lee, K.-J., and Chen, B. P. C. (2006). ATR-dependent phosphorylation of DNA-dependent protein kinase catalytic subunit in Response to UV-induced replication stress. Mol. Cell. Biol. 26, 7520-7528. (Pubitemid 44547702)
120. Yamaguchi-Iwai, Y., Sonoda, E., Buerstedde, J. M., et al. (1998). Homologous recombination, but not DNA repair, is reduced in vertebrate cells deficient in RAD52. Mol. Cell. Biol. 18, 6430-6435. (Pubitemid 28500533)
121. Yamana, Y., Maeda, T., Ohba, H., et al. (2005). Regulation of homologous integration in yeast by the DNA repair proteins Ku70 and RecQ. Mol. Genet. Genomics 273, 167-176. (Pubitemid 40674716)
122. Zhou, X. Y., Wang, X., Wang, H., et al. (2002). Ku affects the ATM-dependent S phase checkpoint following ionizing radiation. Oncogene 21, 6377-6381.
123. Zou, Y., Liu, Y., Wu, X., et al. (2006). Functions of human replication protein A (RPA): from DNA replication to DNA damage and stress responses. J. Cell. Physiol. 208, 267-273. (Pubitemid 43993416)