Caffeine suppresses homologous recombination through interference with RAD51-mediated joint molecule formation

Nucleic Acids Research

Volumn 41, Issue 13, 2013, Pages 6475-6489

  Zelensky, Alex N ^a   Sanchez, Humberto ^a   Ristic, Dejan ^a   Vidic, Iztok ^a   Van Rossum Fikkert, Sari E ^a   Essers, Jeroen ^a   Wyman, Claire ^a   Kanaar, Roland ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 6 (1 THIANTHRENYL) 4 PYRANONE; CAFFEINE; DNA HOMOLOG; METHYLXANTHINE DERIVATIVE; RAD51 PROTEIN; ROSCOVITINE; THEOBROMINE; WORTMANNIN;

ANIMAL CELL; ARTICLE; CHEMICAL ANALYSIS; CHEMICAL STRUCTURE; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVITY; ENZYME INHIBITION; GENE TARGETING; HOMOLOGOUS RECOMBINATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION;

ANIMALS; CAFFEINE; CELL LINE; GENE TARGETING; MICE; NUCLEOPROTEINS; PROTEIN KINASE INHIBITORS; RAD51 RECOMBINASE; RECOMBINATIONAL DNA REPAIR;

EID: 84880554113     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt375     Document Type: Article

References (92)

1. Vasquez, K.M., Marburger, K., Intody, Z. and Wilson, J.H. (2001) Manipulating the mammalian genome by homologous recombination. Proc. Natl Acad. Sci. USA, 98, 8403-8410. (Pubitemid 32678042)
2. Glaser, S., Anastassiadis, K. and Stewart, A.F. (2005) Current issues in mouse genome engineering. Nat. Genet., 37, 1187-1193. (Pubitemid 41568698)
3. Szostak, J.W., Orr-Weaver, T.L., Rothstein, R.J. and Stahl, F.W. (1983) The double-strand-break repair model for recombination. Cell, 33, 25-35. (Pubitemid 13096431)
4. Orr-Weaver, T.L. and Szostak, J.W. (1983) Yeast recombination: the association between double-strand gap repair and crossing-over. Proc. Natl Acad. Sci. USA, 80, 4417-4421. (Pubitemid 13077849)
5. Rothstein, R.J. (1983) One-step gene disruption in yeast. Methods Enzymol., 101, 202-211. (Pubitemid 13071047)
6. Cruz, A. and Beverley, S.M. (1990) Gene replacement in parasitic protozoa. Nature, 348, 171-173.
7. Schaefer, D.G. and Zryd, J.P. (1997) Efficient gene targeting in the moss Physcomitrella patens. Plant J., 11, 1195-1206. (Pubitemid 27307237)
8. Adachi, N., So, S., Iiizumi, S., Nomura, Y., Murai, K., Yamakawa, C., Miyagawa, K. and Koyama, H. (2006) The human pre-B cell line Nalm-6 is highly proficient in gene targeting by homologous recombination. DNA Cell Biol., 25, 19-24. (Pubitemid 43089749)
9. Buerstedde, J.M. and Takeda, S. (1991) Increased ratio of targeted to random integration after transfection of chicken B cell lines. Cell, 67, 179-188. (Pubitemid 121001434)
10. Feederle, R., Delecluse, H.J., Rouault, J.P., Schepers, A. and Hammerschmidt, W. (2004) Efficient somatic gene targeting in the lymphoid human cell line DG75. Gene, 343, 91-97. (Pubitemid 39551032)
11. Thomas, K.R. and Capecchi, M.R. (1987) Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell, 51, 503-512.
12. Chapman, J.R., Taylor, M.R.G. and Boulton, S.J. (2012) Playing the end game: DNA double-strand break repair pathway choice. Mol. Cell, 47, 497-510.
13. Warmerdam, D.O., Freire, R., Kanaar, R. and Smits, V. (2009) Cell cycle-dependent processing of DNA lesions controls localization of Rad9 to sites of genotoxic stress. Cell Cycle, 8, 1765-1774.
14. Durocher, D. and Jackson, S.P. (2001) DNA-PK, ATM and ATR as sensors of DNA damage: variations on a theme? Curr. Opin. Cell Biol., 13, 225-231. (Pubitemid 32209224)
15. Huang, L.C., Clarkin, K.C. and Wahl, G.M. (1996) Sensitivity and selectivity of the DNA damage sensor responsible for activating p53-dependent G1 arrest. Proc. Natl Acad. Sci. USA, 93, 4827-4832. (Pubitemid 26162836)
16. Sandell, L.L. and Zakian, V.A. (1993) Loss of a yeast telomere: arrest, recovery, and chromosome loss. Cell, 75, 729-739. (Pubitemid 23346371)
17. Igoucheva, O., Alexeev, V. and Yoon, K. (2006) Differential cellular responses to exogenous DNA in mammalian cells and its effect on oligonucleotide-directed gene modification. Gene Ther., 13, 266-275. (Pubitemid 43148649)
18. Yanez, R.J. and Porter, A.C. (1999) Influence of DNA delivery method on gene targeting frequencies in human cells. Somat. Cell Mol. Genet., 25, 27-31.
19. Celeste, A., Petersen, S., Romanienko, P.J., Fernandez-Capetillo, O., Chen, H.T., Sedelnikova, O.A., Reina-San-Martin, B., Coppola, V., Meffre, E., Difilippantonio, M.J. et al. (2002) Genomic instability in mice lacking histone H2AX. Science, 296, 922-927. (Pubitemid 34464900)
20. 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. (Pubitemid 27199892)
21. Gao, Y., Chaudhuri, J., Zhu, C., Davidson, L., Weaver, D.T. and Alt, F.W. (1998) A targeted DNA-PKcs-null mutation reveals DNA-PK-independent functions for KU in V(D)J recombination. Immunity, 9, 367-376. (Pubitemid 28462757)
22. Jacks, T., Remington, L., Williams, B.O., Schmitt, E.M., Halachmi, S., Bronson, R.T. and Weinberg, R.A. (1994) Tumor spectrum analysis in p53-mutant mice. Curr. Biol., 4, 1-7.
23. Abraham, J., Lemmers, B., Hande, M.P., Moynahan, M.E., Chahwan, C., Ciccia, A., Essers, J., Hanada, K., Chahwan, R., Khaw, A.K. et al. (2003) Eme1 is involved in DNA damage processing and maintenance of genomic stability in mammalian cells. EMBO J., 22, 6137-6147. (Pubitemid 37463256)
24. Dannenberg, J.-H., Schuijff, L., Dekker, M., van der Valk, M. and Riele, Te, H. (2004) Tissue-specific tumor suppressor activity of retinoblastoma gene homologs p107 and p130. Genes Dev., 18, 2952-2962. (Pubitemid 39602313)
25. Yanez-Munoz, R.J. and Porter, A.C. (1999) Gene targeting is enhanced in human cells overexpressing hRAD51. Gene Ther., 6, 1282-1290. (Pubitemid 29359022)
26. Hanada, K., Budzowska, M., Modesti, M., Maas, A., Wyman, C., Essers, J. and Kanaar, R. (2006) The structure-specific endonuclease Mus81-Eme1 promotes conversion of interstrand DNA crosslinks into double-strands breaks. EMBO J., 25, 4921-4932. (Pubitemid 44607036)
27. Modesti, M., Ristic, D., van der Heijden, T., Dekker, C., van Mameren, J., Peterman, E.J.G., Wuite, G.J.L., Kanaar, R. and Wyman, C. (2007) Fluorescent human RAD51 reveals multiple nucleation sites and filament segments tightly associated along a single DNA molecule. Structure, 15, 599-609. (Pubitemid 46702688)
28. Henricksen, L.A., Umbricht, C.B. and Wold, M.S. (1994) Recombinant replication protein A: expression, complex formation, and functional characterization. J. Biol. Chem., 269, 11121-11132. (Pubitemid 24200317)
29. van der Linden, E., Sanchez, H., Kinoshita, E., Kanaar, R. and Wyman, C. (2009) RAD50 and NBS1 form a stable complex functional in DNA binding and tethering. Nucleic Acids Res., 37, 1580-1588.
30. Mazin, A.V., Zaitseva, E., Sung, P. and Kowalczykowski, S.C. (2000) Tailed duplex DNA is the preferred substrate for Rad51 protein-mediated homologous pairing. EMBO J., 19, 1148-1156. (Pubitemid 30119839)
31. Bugreev, D.V. and Mazin, A.V. (2004) Ca2+ activates human homologous recombination protein Rad51 by modulating its ATPase activity. Proc. Natl Acad. Sci. USA, 101, 9988-9993. (Pubitemid 38891183)
32. Kanaar, R., van de Putte, P. and Cozzarelli, N.R. (1989) Ginmediated recombination of catenated and knotted DNA substrates: implications for the mechanism of interaction between cis-acting sites. Cell, 58, 147-159. (Pubitemid 19180087)
33. Ristic, D., Wyman, C., Paulusma, C. and Kanaar, R. (2001) The architecture of the human Rad54-DNA complex provides evidence for protein translocation along DNA. Proc. Natl Acad. Sci. USA, 98, 8454-8460. (Pubitemid 32678049)
34. Ristic, D., Kanaar, R. and Wyman, C. (2011) Visualizing RAD51-mediated joint molecules: implications for recombination mechanism and the effect of sequence heterology. Nucleic Acids Res., 39, 155-167.
35. Kimler, B.F., Leeper, D.B., Snyder, M.H., Rowley, R. and Schneiderman, M.H. (1982) Modification of radiation-induced division delay by caffeine analogues and dibutyryl cyclic AMP. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med., 41, 47-58. (Pubitemid 12212687)
36. Tomasovic, S.P. and Dewey, W.C. (1978) Comparative studies of the effects of drugs on X-ray-induced G2 delay. Radiat Res., 74, 112-128. (Pubitemid 8330521)
37. Jirmanova, L., Bulavin, D.V. and Fornace, A.J. (2005) Inhibition of the ATR/Chk1 pathway induces a p38-dependent S-phase delay in mouse embryonic stem cells. Cell Cycle, 4, 1428-1434. (Pubitemid 41437134)
38. Asaad, N.A., Zeng, Z.C., Guan, J., Thacker, J. and Iliakis, G. (2000) Homologous recombination as a potential target for caffeine radiosensitization in mammalian cells: reduced caffeine radiosensitization in XRCC2 and XRCC3 mutants. Oncogene, 19, 5788-5800.
39. Cortez, D. (2003) Caffeine inhibits checkpoint responses without inhibiting the ataxia-telangiectasia-mutated (ATM) and ATM-and Rad3-related (ATR) protein kinases. J. Biol. Chem., 278, 37139-37145. (Pubitemid 37175228)
40. Wang, H., Boecker, W., Wang, H., Wang, X., Guan, J., Thompson, L.H., Nickoloff, J.A. and Iliakis, G. (2004) Caffeine inhibits homology-directed repair of I-SceI-induced DNA doublestrand breaks. Oncogene, 23, 824-834. (Pubitemid 38241283)
41. Banath, J.P., Banuelos, C.A., Klokov, D., Macphail, S.M., Lansdorp, P.M. and Olive, P.L. (2009) Explanation for excessive DNA single-strand breaks and endogenous repair foci in pluripotent mouse embryonic stem cells. Exp. Cell Res., 315, 1505-1520.
42. Sarkaria, J.N., Busby, E.C., Tibbetts, R.S., Roos, P., Taya, Y., Karnitz, L.M. and Abraham, R.T. (1999) Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res., 59, 4375-4382. (Pubitemid 29418757)
43. Bulavin, D.V., Higashimoto, Y., Popoff, I.J., Gaarde, W.A., Basrur, V., Potapova, O., Appella, E. and Fornace, A.J. (2001) Initiation of a G2/M checkpoint after ultraviolet radiation requires p38 kinase. Nature, 411, 102-107. (Pubitemid 32428198)
44. Charrier, J.D., Durrant, S.J., Golec, J.M.C., Kay, D.P., Knegtel, R.M.A., MacCormick, S., Mortimore, M., O'Donnell, M.E., Pinder, J.L., Reaper, P.M. et al. (2011) Discovery of potent and selective inhibitors of ataxia telangiectasia mutated and Rad3 related (ATR) protein kinase as potential anticancer agents. J. Med. Chem., 54, 2320-2330.
45. Graves, P.R., Yu, L., Schwarz, J.K., Gales, J., Sausville, E.A., O'Connor, P.M. and Piwnica-Worms, H. (2000) The Chk1 protein kinase and the Cdc25C regulatory pathways are targets of the anticancer agent UCN-01. J. Biol. Chem., 275, 5600-5605. (Pubitemid 30115197)
46. Kastan, M.B., Onyekwere, O., Sidransky, D., Vogelstein, B. and Craig, R.W. (1991) Participation of p53 protein in the cellular response to DNA damage. Cancer Res., 51, 6304-6311.
47. Huertas, P., Cortes-Ledesma, F., Sartori, A., Aguilera, A. and Jackson, S. (2008) CDK targets Sae2 to control DNA-end resection and homologous recombination. Nature, 455, 689-692. 10.1038/nature07215.
48. Esashi, F., Christ, N., Gannon, J., Liu, Y., Hunt, T., Jasin, M. and West, S.C. (2005) CDK-dependent phosphorylation of BRCA2 as a regulatory mechanism for recombinational repair. Nature, 434, 598-604. (Pubitemid 40488546)
49. Meijer, L., Borgne, A., Mulner, O., Chong, J.P., Blow, J.J., Inagaki, N., Inagaki, M., Delcros, J.G. and Moulinoux, J.P. (1997) Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5. Eur. J. Biochem., 243, 527-536. (Pubitemid 27060443)
50. Lehmann, A.R. and Kirk-Bell, S. (1974) Effects of caffeine and theophylline on DNA synthesis in unirradiated and UV-irradiated mammalian cells. Mutat. Res., 26, 73-82.
51. Liu, J., Sneeden, J. and Heyer, W.D. (2011) In vitro assays for DNA pairing and recombination-associated DNA synthesis. Methods Mol. Biol., 745, 363-383.
52. Tornaletti, S., Russo, P., Parodi, S. and Pedrini, A.M. (1989) Studies on DNA binding of caffeine and derivatives: evidence of intercalation by DNA-unwinding experiments. Biochim. Biophys. Acta, 1007, 112-115. (Pubitemid 19052404)
53. Fritzsche, H., Lang, H., Sprinz, H. and Pohle, W. (1980) On the interaction of caffeine with nucleic acids. IV. Studies of the caffeine-DNA interaction by infrared and ultraviolet linear dichroism, proton and deuteron nuclear magnetic resonance. Biophys. Chem., 11, 121-131. (Pubitemid 10136079)
54. Selby, C.P. and Sancar, A. (1990) Molecular mechanisms of DNA repair inhibition by caffeine. Proc. Natl Acad. Sci. USA, 87, 3522-3525.
55. Choulika, A., Perrin, A., Dujon, B. and Nicolas, J.F. (1995) Induction of homologous recombination in mammalian chromosomes by using the I-SceI system of Saccharomyces cerevisiae. Mol. Cell. Biol., 15, 1968-1973.
56. Smih, F., Rouet, P., Romanienko, P.J. and Jasin, M. (1995) Doublestrand breaks at the target locus stimulate gene targeting in embryonic stem cells. Nucleic Acids Res., 23, 5012-5019. (Pubitemid 26012483)
57. Yanez-Munoz, R.J. and Porter, A.C. (2002) A chromosomal position effect on gene targeting in human cells. Nucleic Acids Res., 30, 4892-4901. (Pubitemid 35414649)
58. Papadopoulou, B. and Dumas, C. (1997) Parameters controlling the rate of gene targeting frequency in the protozoan parasite Leishmania. Nucleic Acids Res., 25, 4278-4286. (Pubitemid 27485206)
59. Bertling, W., Hunger-Bertling, K. and Cline, M.J. (1987) Intranuclear uptake and persistence of biologically active DNA after electroporation of mammalian cells. J. Biochem. Biophys. Methods, 14, 223-232.
60. Rowley, R., Martin, J.H. and Leeper, D.B. (1988) Effect of poly(adenosinediphosphoribose) synthesis inhibitors and structurally related compounds on radiation-induced G2 arrest. Radiat. Res., 113, 58-70. (Pubitemid 18050030)
61. Grigg, G.W. (1972) Effects of coumarin, pyronin Y, 6,9-dimethyl 2-methylthiopurine and caffeine on excision repair and recombination repair in Escherichia coli. J. Gen. Microbiol., 70, 221-230.
62. Mazza, G., Eisenstark, H.M., Serra, M.C. and Polsinelli, M. (1972) Effect of caffeine on the recombination process of Bacillus subtilis. Mol. Gen. Genet., 115, 73-79.
63. Witkin, E.M. and Farquharson, E.L. (1969) Enhancement and Diminution of Ultraviolet-Light-Initiated Mutagenesis by Post-Treatment with Caffeine in Escherichia coli. In: Wolstenholme, G.E.W. and O'Connor, M. (eds), Ciba Foundation Symposium-Mutation as a Cellular Process. Churchill Livingstone, London, pp. 36-49.
64. Loprieno, N., Barale, R. and Baroncelli, S. (1974) Genetic effects of caffeine. Mutat. Res., 26, 83-87.
65. Fabre, F. (1972) Relation between repair mechanisms and induced mitotic recombination after UV irradiation, in the yeast Schizosaccharomyces pombe. Effects of caffeine. Mol. Gen. Genet., 117, 153-166.
66. Yefremova, G.I. and Filippova, L.M. (1974) Effect of caffeine on crossing-over in Drosophila melanogaster. Mutat. Res., 23, 347-352.
67. Wang, H., Wang, X., Iliakis, G. and Wang, Y. (2003) Caffeine could not efficiently sensitize homologous recombination repair-deficient cells to ionizing radiation-induced killing. Radiat. Res., 159, 420-425. (Pubitemid 36314957)
68. Al-Minawi, A.Z., Saleh-Gohari, N. and Helleday, T. (2008) The ERCC1/XPF endonuclease is required for efficient single-strand annealing and gene conversion in mammalian cells. Nucleic Acids Res., 36, 1-9.
69. Lim, D.S. and Hasty, P. (1996) A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol. Cell. Biol., 16, 7133-7143. (Pubitemid 26389773)
70. Tsuzuki, T., Fujii, Y., Sakumi, K., Tominaga, Y., Nakao, K., Sekiguchi, M., Matsushiro, A., Yoshimura, Y. and Morita, T. (1996) Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. Proc. Natl Acad. Sci. USA, 93, 6236-6240. (Pubitemid 26230288)
71. De Vlaminck, I., van Loenhout, M.T.J., Zweifel, L., Blanken, den, J., Hooning, K., Hage, S., Kerssemakers, J. and Dekker, C. (2012) Mechanism of homology recognition in DNA recombination from dual-molecule experiments. Mol. Cell, 46, 616-624.
72. Forget, A.L. and Kowalczykowski, S.C. (2012) Single-molecule imaging of DNA pairing by RecA reveals a three-dimensional homology search. Nature, 482, 423-427.
73. Bianco, P.R., Tracy, R.B. and Kowalczykowski, S.C. (1998) DNA strand exchange proteins: a biochemical and physical comparison. Front. Biosci., 3, D570-D603.
74. Aihara, H., Ito, Y., Kurumizaka, H., Yokoyama, S. and Shibata, T. (1999) The N-terminal domain of the human Rad51 protein binds DNA: structure and a DNA binding surface as revealed by NMR. J. Mol. Biol., 290, 495-504. (Pubitemid 29324833)
75. Zhang, X.P., Lee, K.I., Solinger, J.A., Kiianitsa, K. and Heyer, W.D. (2005) Gly-103 in the N-terminal domain of Saccharomyces cerevisiae Rad51 protein is critical for DNA binding. J. Biol. Chem., 280, 26303-26311. (Pubitemid 41022228)
76. Ts'o, P.O. and Lu, P. (1964) Interaction of nucleic acids, I. Physical binding of thymine, adenine, steroids, and aromatic hydrocarbons to nucleic acids. Proc. Natl Acad. Sci. USA, 51, 17-24.
77. Domon, M., Barton, B., Porte, A. and Rauth, A.M. (1970) The interaction of caffeine with ultra-violet-light-irradiated DNA. Int. J. Radiat. Biol. Relat. Stud. Phys. Chem. Med., 17, 395-399.
78. Ts'o, P.O., Helmkamp, G.K. and Sander, C. (1962) Interaction of nucleosides and related compounds with nucleic acids as indicated by the change of helix-coil transition temperature. Proc. Natl Acad. Sci. USA, 48, 686-698.
79. Chetsanga, C.J., Rushlow, K. and Boyd, V. (1976) Caffeine enhancement of digestion of DNA by nuclease S1. Mutat. Res., 34, 11-20.
80. Kihlman, B.A. (1977) Caffeine and Chromosomes. Elsevier, Amsterdam.
81. Kaufmann, W.K., Heffernan, T.P., Beaulieu, L.M., Doherty, S., Frank, A.R., Zhou, Y., Bryant, M.F., Zhou, T., Luche, D.D., Nikolaishvili-Feinberg, N. et al. (2003) Caffeine and human DNA metabolism: the magic and the mystery. Mutat. Res., 532, 85-102. (Pubitemid 37487848)
82. Landsverk, K.S., Patzke, S., Rein, I.D., Stokke, C., Lyng, H., De Angelis, P.M. and Stokke, T. (2011) Three independent mechanisms for arrest in G2 after ionizing radiation. Cell Cycle, 10, 819-829.
83. Piwko, W., Olma, M.H., Held, M., Bianco, J.N., Pedrioli, P.G., Hofmann, K., Pasero, P., Gerlich, D.W. and Peter, M. (2010) RNAi-based screening identifies the Mms22L-Nfkbil2 complex as a novel regulator of DNA replication in human cells. EMBO J., 29, 4210-4222.
84. Vassin, V.M., Wold, M.S. and Borowiec, J.A. (2004) Replication protein A (RPA) phosphorylation prevents RPA association with replication centers. Mol. Cell. Biol., 24, 1930-1943. (Pubitemid 38248934)
85. Han, W., Ming, M. and He, Y.Y. (2011) Caffeine promotes ultraviolet B-induced apoptosis in human keratinocytes without complete DNA repair. J. Biol. Chem., 286, 22825-22832.
86. Yan, C., Lu, J., Zhang, G., Gan, T., Zeng, Q., Shao, Z., Duerksen-Hughes, P.J. and Yang, J. (2011) Benzo[a]pyrene induces complex H2AX phosphorylation patterns by multiple kinases including ATM, ATR, and DNA-PK. Toxicol. In Vitro, 25, 91-99.
87. Block, W.D., Merkle, D., Meek, K. and Lees-Miller, S.P. (2004) Selective inhibition of the DNA-dependent protein kinase (DNA-PK) by the radiosensitizing agent caffeine. Nucleic Acids Res., 32, 1967-1972. (Pubitemid 38849355)
88. Lee, J.H. and Paull, T.T. (2005) ATM activation by DNA doublestrand breaks through the Mre11-Rad50-Nbs1 complex. Science, 308, 551-554. (Pubitemid 40570585)
89. Hall-Jackson, C.A., Cross, D.A., Morrice, N. and Smythe, C. (1999) ATR is a caffeine-sensitive, DNA-activated protein kinase with a substrate specificity distinct from DNA-PK. Oncogene, 18, 6707-6713.
90. Gottlieb, T.M. and Jackson, S.P. (1993) The DNA-dependent protein kinase: requirement for DNA ends and association with Ku antigen. Cell, 72, 131-142. (Pubitemid 23029700)
91. Agarwal, S., van Cappellen, W.A., Guenole, A., Eppink, B., Linsen, S.E.V., Meijering, E., Houtsmuller, A., Kanaar, R. and Essers, J. (2011) ATP-dependent and independent functions of Rad54 in genome maintenance. J. Cell Biol., 192, 735-750.
92. Eppink, B., Tafel, A.A., Hanada, K., van Drunen, E., Hickson, I.D., Essers, J. and Kanaar, R. (2011) The response of mammalian cells to UV-light reveals Rad54-dependent and independent pathways of homologous recombination. DNA Repair (Amst), 10, 1095-1105. Chemical Sciences (FP7/2007-2013)