Werner syndrome protein participates in a complex with RAD51, RAD54, RAD54B and ATR in response to ICL-induced replication arrest

Journal of Cell Science

Volumn 119, Issue 24, 2006, Pages 5137-5146

  Otterlei, Marit ^a,b   Bruheim, Per ^a,b   Ahn, Byungchan ^a,c   Bussen, Wendy ^d   Karmakar, Parimal ^a,e   Baynton, Kathy ^f   Bohr, Vilhelm A ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^c University of Ulsan   (South Korea)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e JADAVPUR UNIVERSITY   (India)

^f UNIVERSITY OF MONTREAL   (Canada)

Author keywords

ATR; DNA repair; ICL; RAD51; RAD54B; WRN

Indexed keywords

ATR PROTEIN; MULTIPROTEIN COMPLEX; RAD51 PROTEIN; RAD54 PROTEIN; WERNER SYNDROME PROTEIN;

ARTICLE; CONTROLLED STUDY; DNA CROSS LINKING; DNA REPAIR; DNA REPLICATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETIC CODE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; VALIDATION STUDY;

BLOTTING, WESTERN; CELL CYCLE PROTEINS; CELL NUCLEUS; CELL SURVIVAL; CROSS-LINKING REAGENTS; DNA HELICASES; DNA REPLICATION; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; NUCLEAR PROTEINS; PROTEIN BINDING; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; RAD51 RECOMBINASE; RECOMBINANT FUSION PROTEINS; RECQ HELICASES;

EID: 33846141125     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.03291     Document Type: Article

References (76)

1. Aas, P. A., Otterlei, M., Falnes, P. O., Vagbo, C. B., Skorpen, F., Akbari, M., Sundheim, O., Bjoras, M., Slupphaug, G., Seeberg, E. et al. (2003). Human and bacteria] oxidative demethylases repair alkylation damage in both RNA and DNA. Nature 421, 859-863.
2. Akkari, Y. M., Bateman, R. L., Reifsteck, C. A., Olson, S. B. and Grompe, M. (2000). DNA replication is required to elicit cellular responses to psoralen-induced DNA interstrand cross-links. Mol. Cell. Biol. 20, 8283-8289.
3. Alexeev, A., Mazin, A. and Kowalczykowski, S. C. (2003). Rad54 protein possesses chromatin-remodeling activity stimulated by the Rad51-ssDNA nucleoprotein filament. Nat. Struct. Biol. 10. 182-186.
4. Barr, S. M., Leung, C. G., Chang, E. E. and Cimprich, K. A. (2003). ATR kinase activity regulates the intranuclear translocation of ATR and RPA following ionizing radiation. Curr. Biol. 13, 1047-1051.
5. Baynton, K., Otterlei, M., Bjoras, M., von Kobbe, C., Bohr, V. A. and Seeberg, E. (2003). WRN interacts physically and functionally with the recombination mediator protein RAD52. J. Biol. Chem. 278, 36476-36486.
6. Benson, F. E., Stasiak, A. and West, S. C. (1994). Purification and characterization of the human Rad51 protein, an analogue of E. coli RecA. EMBO J. 13, 5764-5771.
7. Brosh, R. M., Jr, Li, J. L., Kenny, M. K., Karow, J. K., Cooper, M. P., Kureekattil, R. P., Hickson, I. D. and Bohr, V. A. (2000). Replication protein A physically interacts with the Bloom's syndrome protein and stimulates its helicase activity. J. Biol. Chem. 275. 11500-23508.
8. Brosh, R. M., Jr, Orren, D. K., Nehlin, J.O., Ravn, P. H., Kenny, M. K., Machwe, A. and Bohr, V. A. (1999). Functional and physical interaction between WRN helicase and human replication protein A. J. Biol. Chem. 274, 18341-18350.
9. Brosh, R. M., Jr, von Kobbe, C., Sommers, J. A., Karmakar, P., Opresko, P. L., Piotrowski, J., Dianov, I., Dianov, G. L. and Bohr, V. A. (2001). Werner syndrome protein interacts with human flap endonuclease I and stimulates its cleavage activity. EMBO J. 20, 5791-5801.
10. Bryan, T. M., Englezou, A., Dalla-Pozza, L., Dunham, M. A. and Reddel, R. R. (1997). Evidence for an alternative mechanism for maintaining Lelomere length in human tumors and tumor-derived cell lines. Nat. Med. 3, 1271-1274.
11. Chang, S., Multani, A. S., Cabrera, N. G., Naylor, M. L., Laud, P., Lombard, D., Pathak, S., Guarente, L. and DePinho, R. A. (2004). Essential role of limiting telomeres in the pathogenesis of Werner syndrome. Nat. Genet. 36, 877-882.
12. Cheng, W. H., Von Kobbe, C., Opresko, P. L., Arthur, L. M., Komatsu, K., Seidman, M. M., Carney, J. P. and Bohr, V. A. (2004). Linkage between werner syndrome protein and the Mre11 complex via Nbs1. J. Biol. Chem. 279, 21169-21176.
13. Colgin, L. M. and Reddel, R. R. (1999). Telomere maintenance mechanisms and cellular immortalization. Curr. Opin. Genet. Dev. 9, 97-103.
14. Constantinou, A., Tarsounas, M., Karow, J. K., Brosh, R. M., Bohr, V. A., Hickson, I. D. and West, S. C. (2000). Werner's syndrome protein (WRN) migrates Holliday junctions and co-localizes with RPA upon replication arrest. EMBO Rep. 1, 80-84.
15. Cooper, M. P., Machwe, A., Orren, D. K., Brush, R. M., Ramsden, D. and Bohr, V. A. (2000). Ku complex interacts with and stimulates the Werner protein. Genes Dev. 14, 907-912.
16. Courcelle, J., Donaldson, J. R., Chow, K. H. and Courcelle, C. T. (2003). DNA damage-induced replication fork regression and processing in Escherichia coli. Science 299, 1064-1067.
17. Cui, S., Arosio, D., Doherty, K. M., Brosh, R. M., Jr, Falaschi, A. and Vindigni, A. (2004). Analysis of the unwinding activity of the dimeric RECQ1 helicase in the presence ot'human replication protein A. Nucleic Acids Res. 32, 2158-2170.
18. Cui, S., Klima, R., Ochem, A., Arosio, D., Falaschi, A. and Vindigni, A. (2003). Characterization of the DNA-unwinding activity of human RECQ1, a helicase specifically stimulated by human replication protein A. J. Biol. Chem. 278, 1424-1432.
19. Davies, S. L., North, P. S., Dart, A., Lakin, N. D. and Hickson, I. D. (2004). Phosphorylation of the Bloom's syndrome helicase and its role in recovery from Sphase arrest. Mol. Cell. Biol. 24, 1279-1291.
20. De Silva, I. U., McHugh, P. J., Clingen, P. H. and Hartley, J. A. (2000). Defining the roles of nucleotide excision repair and recombination in the repair of DNA interstrand cross-links in mammalian cells. Mol. Cell. Biol. 20, 7980-7990.
21. Essers, J., Hendriks, R. W., Swagemakers, S. M., Troelstra, C., de Wit, J., Bootsma, D., Hoeijmakers, J. H. and Kanaar, R. (1997). Disruption of mouse RAD54 reduces ionizing radiation resistance and homologous recombination. Cell 89, 195-204.
22. Franchitto, A. and Pichierri, P. (2004). Werner syndrome protein and the MRE11 complex are involved in a common pathway of replication fork recovery. Cell Cycle 3, 1331-1339.
23. Fukuchi, K., Martin, G. M. and Monnat, R. J., Jr (1989). Mutator phenotype of Werner syndrome is characterized by extensive deletions. Proc. Natl. Acad. Sci. USA 86, 5893-5897.
24. Golub, E. I., Kovalenko, O. V., Gupta, R. C., Ward, D. C. and Radding, C. M. (1997). Interaction of human recombination proteins Rad51 and Rad54. Nucleic Acids Res. 25, 4106-4110.
25. Grigorova, M., Balajee, A. S. and Natarajan, A. T. (2000). Spontaneous and X-ray-induced chromosomal aberrations in Werner syndrome cells detected by FISH using chromosome-specific painting probes. Mutagenesis 15. 303-310.
26. Helleday, T. (2003). Pathways for mitotic homologous recombination in mammalian cells. Mutat. Res. 532, 103-115.
27. Henson, J. D., Neumann, A. A., Yeager, T. R. and Reddel, R. R. (2002) Alternative lengthening of telomeres in mammalian cells. Oncogene 21, 598-610.
28. Hickson, I. D. (2003). RecQ helicases: caretakers of the genome. Nat. Rev. Cancer 3. 169-178.
29. Hook, G. J., Kwok, E. and Heddle, J. A. (1984). Sensitivity of Bloom syndrome fibroblasts to mitomycin C. Mutat. Res. 131, 223-230.
30. Hsu, H. L., Gilley, D., Galande, S. A., Hande, M. P., Allen, B., Kim, S. H., Li, G. C., Campisi, J., Kohwi-Shigematsu, T. and Chen, D. J. (2000). Ku acts in a unique way at the mammalian telomere to prevent end joining. Genes Dev. 14, 2807-2812.
31. Huang, S., Li, B., Gray, M. D., Oshima, J., Mian, I. S. and Campisi, J. (1998). The premature ageing syndrome protein, WRN. is a 3′→5′ exonuclease. Nat. Genet. 20, 114-116.
32. Kamath-Loeb, A. S., Johansson, E., Burgers, P. M. and Loeb, L. A. (2000). Functional interaction between the Werner Syndrome protein and DNA polymerase delta. Proc. Natl. Acad. Sci. USA 97. 4603-4608.
33. Le, S., Moore, J. K., Haber, J. E. and Greider, C. W. (1999). RAD50 and RAD51 define two pathways that collaborate to maintain telomeres in the absence of telomerae. Genetics 152, 143-152.
34. Lebel, M., Spillare, E. A., Harris, C. C. and Leder, P. (1999). The Werner syndrome gene product co-purifies with the DNA replication complex and interacts with PCNA and topoisomerase 1. J. Biol. Chem. 274, 37795-37799.
35. Leonhardt, H., Rahn, H. P., Weinzierl, P., Sporbert, A., Cremer, T., Zink, D. and Cardoso, M. C. (2000). Dynamics of DNA replication factories in living cells. J. Cell Biol. 149, 271-280.
36. Lieber, M. R., Ma, Y., Pannicke, U. and Schwarz, K. (2003). Mechanism and regulation of human non-homologous DNA end-joining. Nat. Rev. Mol. Cell. Biol. 4, 712-720.
37. Lundin, C., Schultz, N., Arnaudeau, C., Mohindra, A., Hansen, L. T. and Helleday, T. (2003). RAD51 is involved in repair of damage associated with DNA replication in mammalian cells. J. Mol. Biol. 328, 521-535.
38. Martin, G. M. (1978). Genetic syndromes in man with potential relevance to the pathobiology of aging. Birth. Defects Orig. Artic. Set. 14, 5-39.
39. Martin, G. M., Sprague, C. A. and Epstein, C. J. (1970). Replicative life-span of cultivated human cells. Effects of donor's age, tissue, and genotype. Lab. Invest. 23. 86-92.
40. Mazin, A. V., Alexeev, A. A. and Kowalezykowski, S. C. (2003). A novel function of Rad54 protein. Stabilization of the Rad51 nucleoprotein filament. J. Biol. Chem. 278, 14029-14036.
41. Mosmann, T. (1983). Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63.
42. Motycka, T. A., Bessho, T., Post, S. M., Sung, P. and Tomkinson, A. E. (2004). Physical and functional interaction between the XPF/ERCCI endonuclease and hRad52. J. Biol. Chem. 279. 13634-13639.
43. Opresko, P. L., Cheng, W. H., von Kobbe, C., Harrigan, J. A. and Bohr, V. A. (2003). Werner syndrome and the function of the Werner protein: what they can teach us about the molecular aging process. Carcinogenesis 24. 791-802.
44. Opresko, P. L., Laine, J. P., Brosh, R. M., Jr, Seidman, M. M. and Bohr, V. A. (2001). Coordinate action of the helicase and 3′ to 5′ exonuclease of Werner syndrome protein. J. Biol. Chem. 276, 44677-44687.
45. Opresko, P. L., Otterlei, M., Graakjaer, J., Bruheim, P., Dawut, L., Kolvraa, S., May, A., Seidman, M. M. and Bohr, V. A. (2004). The Werner syndrome helicase and exonuclease cooperate to resolve telomeric D loops in a manner regulated by TRF1 and TRF2. Mot. Cell 14, 763-774.
46. Opresko, P. L., von Kobbe, C., Laine, J. P., Harrigan, J., Hickson, I. D. and Bohr, V. A. (2002). Telomere-binding protein TRF2 binds to and stimulates the Werner and Bloom syndrome helicases. J. Biol. Chem. 277, 41110-41119.
47. Otterlei, M., Warbrick, E., Nagelhus, T. A., Haug, T., Slupphaug, G., Akbari, M., Aas, P. A., Steinsbekk, K., Bakke, O. and Krokan, H. E. (1999). Post-replicative base excision repair in replication foci. EMBO J. 18, 3834-3844.
48. Pichierri, P. and Franchitto, A. (2004). Werner syndrome protein, the MRE11 complex and ATR: menage-a-trois in guarding genome stabilitv during DNA replication? BioEssays 26, 306-313.
49. Pichierri, P. and Rosselli, F. (2004). The DNA crosslink-induced S-phase checkpoint depends on ATR-CHK1 and ATR-NBS1-FANCD2 pathways. EMBO J. 23, 1178-1187.
50. Pichierri, P., Rosselli, F. and Franchitto, A. (2003). Werner's syndrome protein is phosphorylated in an ATR/ATM-dependent manner following replication arrest and DNA damage induced during the S phase ofthe cell cycle. Oncogene 22, 1491-1500.
51. Rijkers, T., Van Den Ouweland, J., Morolli, B., Rolink, A. G., Baarends, W. M., Van Sloun, P. P., Lohman, P. H. and Pastink, A. (1998). Targeted inactivation of mouse RAD52 reduces homologous recombination but not resistance to ionizing radiation. Mol. Cell. Biol. 18, 6423-6429.
52. Rosselli, E, Briot, D. and Pichierri, P. (2003). The Fanconi anemia pathway and the DNA interstrand cross-links repair. Biochimie 85, 1175-1184.
53. Sakamoto, S., Nishikawa, K., Heo, S. J., Goto, M., Furuichi, Y. and Shimamoto, A. (2001). Werner helicase relocates into nuclear foci in response to DNA damaging agents and co-localizes with RPA and Rad51. Genes Cells 6, 421-430.
54. Salk, D. (1982). Werner's syndrome: a review of recent research with an analysis of connective tissue metabolism, growth control of cultured cells, and chromosomal aberrations. Hum. Genet. 62, 1-5.
55. Sehorn, M. G., Sigurdsson, S., Bussen, W., Unger, V. M. and Sung, P. (2004). Human meiotic recombinase Dmc1 promotes ATP-dependent homologous DNA strand exchange. Nature 429, 433-437.
56. Sharma, S., Otterlei, M., Sommers, J. A., Driscoll, H. C., Dianov, G. L., Kao, H. I., Bambara, R. A. and Brosh, R. M., Jr (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.
57. Shen, Z., Cloud, K. G., Chen, D. J. and Park, M. S. (1996). Specific interactions between the human RAD51 and RAD52 proteins. J. Biol. Chem. 271, 148-152.
58. Sigurdsson, S., Van Komen, S., Petukhova, G. and Sung, P. (2002). Homologous DNA pairing by human recombination factors Rad51 and Rad54. J. Biol. Chem. 277, 42790-42794.
59. Swagemakers, S. M., Essers, J., de Wit, J., Hoeijmakers, J. H. and Kanaar, R. (1998). The human RAD54 recombinational DNA repair protein is a double-stranded DNA-dependent ATPase. J. Biol. Chem. 273, 28292-28297.
60. Tan, T. L., Kanaar, R. and Wyman, C. (2003). Rad54, a Jack of all trades in homologous recombination. DNA Repair 2, 787-794,
61. Tanaka, K., Hiramoto, T., Fukuda, T. and Miyagawa, K. (2000). A novel human rad54 homologue, Rad54B, associates with Rad51. J. Biol. Chem. 275, 26316-26321.
62. Tanaka, K., Kagawa, W., Kinebuchi, T., Kurumizaka, H. and Miyagawa, K. (2002). Human Rad54B is a double-stranded DNA-dependent ATPase and has biochemical properties different from its structural homolog in yeast, Tid1/Rdh54. Nucleic Acids Res. 30, 1346-1353.
63. Tarsounas, M., Davies, D. and West, S. C. (2003). BRCA2-dependent and independent formation of RAD51 nuclear foci. Oncogene 22, 1115-1123.
64. Tashiro, S., Kotomura, N., Shinohara, A., Tanaka, K., Ueda, K. and Kamada, N. (1996). S phase specific formation of the human Rad51 protein nuclear foci in lymphocytes. Oncogene 12. 2165-2170.
65. Teng, S. C. and Zakian, V. A. (1999). Telomere-telomere recombination is an efficient bypass pathway for telomere maintenance in Saccharomyces cerevisiae. Mol. Cell. Biol. 19, 8083-8093.
66. von Kobbe, C. and Bohr, V. A. (2002). A nucleolar targeting sequence in the Werner syndrome protein resides within residues 949-1092. J. Cell Sci. 115, 3901-3907.
67. von Kobbe, C., Karmakar, P., Dawut, L., Opresko, P., Zeng, X., Brash, R. M., Jr, Hickson, I. D. and Bohr, V. A. (2002). Colocalization. physical, and functional interaction between Werner and Bloom syndrome proteins. J. Biol. Chem. 277, 22035-22044.
68. Wesoly, J., Agarwal, S., Sigurdsson, S., Bussen, W., Van Komen, S., Qin, J., van Steeg, H., van Benthem, J, Wassenaar, E., Baarends, W. M. et al. (2006). Differential contributions of mammalian Rad54 paralogs to recombination, DNA damage repair, and meiosis. Mol. Cell. Biol. 26, 976-989.
69. West, S. C. (2003). Molecular views of recombination proteins and their control. Nat. Rev Mol. Cell. Biol. 4, 435-445.
70. Wu, L., Davies, S. L., Levitt, N. C. and Hickson, I. D. (2001). Potential role for the BLM helicase in recombinational repair via a conserved interaction with RAD51. J. Biol. Chem. 276, 19375-19381.
71. Xia, Z. and Liu, Y. (2001). Reliable and global measurement of fluorescence resonance energy transfer using fluorescence microscopes. Biophys. J. 81, 2395-2402.
72. Yu, C. E., Oshima, J., Fu, Y. H., Wijsman, E. M., Hisama, F., Alisch, R., Matthews, S., Nakura, J., Miki, T., Ouais, S. et al. (1996). Positional cloning of the Werner's syndrome gene. Science 272, 258-262.
73. Zhang, N., Kaur, R., Lu, X., Shen, X., Li, L. and Legerski, R. J. (2005). The Pso4 mRNA splicing and DNA repair complex interacts with WRN for processing of DNA interstrand cross-links. J. Biol. Chem. 280, 40559-40567.
74. Zhang, N., Lu, X. and Legerski, R. J. (2003). Partial reconstitution of human interstrand cross-link repair in vitro: characterization of the roles of RPA and PCNA. Biochem. Biophys. Res. Commun. 309, 71-78.
75. Zhang, N., Lu, X., Zhang, X., Peterson, C. A. and Legerski, R. J. (2002). hMutSbeta is required for the recognition and uncoupling of psoralen interstrand cross-links in vitro. Mol. Cell. Biol. 22, 2388-2397.
76. Zheng, H., Wang, X., Warren, A. J., Legerski, R. J., Nairn, R. S., Hamilton, J. W. and Li, L. (2003). Nucleotide excision repair and polymerase eta-mediated error-prone removal of mitomycin C interstrand cross-tinks. Mol. Cell. Biol. 23. 754-761.