Dynamic localization of human RAD18 during the cell cycle and a functional connection with DNA double-strand break repair

DNA Repair

Volumn 8, Issue 2, 2009, Pages 190-201

  Inagaki, Akiko ^a   van Cappellen, Wiggert A ^a   van der Laan, Roald ^a   Houtsmuller, Adriaan B ^b   Hoeijmakers, Jan H J ^a   Grootegoed, J Anton ^a   Baarends, Willy M ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b JOSEPHINE NEFKENS INSTITUTE   (Netherlands)

Author keywords

Cell cycle; DNA double strand breaks; PCNA; RAD18

Indexed keywords

DOUBLE STRANDED DNA; RAD18 PROTEIN; RAD51 PROTEIN;

ARTICLE; CELL CULTURE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE PHASE; CELL CYCLE S PHASE; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; HUMAN; HUMAN CELL; HUMAN TISSUE; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; ULTRAVIOLET C RADIATION;

CELL CYCLE; CELL NUCLEUS; CELL SURVIVAL; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA-BINDING PROTEINS; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; G1 PHASE; HELA CELLS; HUMANS; KINETICS; LASERS; PROLIFERATING CELL NUCLEAR ANTIGEN; PROTEIN TRANSPORT; RADIATION, IONIZING; RECOMBINANT FUSION PROTEINS; S PHASE; ULTRAVIOLET RAYS;

EID: 58149151193     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2008.10.008     Document Type: Article

References (42)

1. Ulrich H.D. The RAD6 pathway: control of DNA damage bypass and mutagenesis by ubiquitin and SUMO. ChemBioChem 6 (2005) 1735-1743
2. Hoege C., Pfander B., Moldovan G.L., Pyrowolakis G., and Jentsch S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419 (2002) 135-141
3. Moldovan G.L., Pfander B., and Jentsch S. PCNA, the maestro of the replication fork. Cell 129 (2007) 665-679
4. Lehmann A.R., Niimi A., Ogi T., Brown S., Sabbioneda S., Wing J.F., Kannouche P.L., and Green C.M. Translesion synthesis: Y-family polymerases and the polymerase switch. DNA Repair (Amst.) 6 (2007) 891-899
5. Yang W., and Woodgate R. What a difference a decade makes: insights into translesion DNA synthesis. Proc. Natl. Acad. Sci. USA 104 (2007) 15591-15598
6. Xin H., Lin W., Sumanasekera W., Zhang Y., Wu X., and Wang Z. The human RAD18 gene product interacts with HHR6A and HHR6B. Nucleic Acids Res. 28 (2000) 2847-2854
7. Kannouche P.L., Wing J., and Lehmann A.R. Interaction of human DNA polymerase eta with monoubiquitinated PCNA: a possible mechanism for the polymerase switch in response to DNA damage. Mol. Cell 14 (2004) 491-500
8. Watanabe K., Tateishi S., Kawasuji M., Tsurimoto T., Inoue H., and Yamaizumi M. Rad18 guides poleta to replication stalling sites through physical interaction and PCNA monoubiquitination. EMBO J. 23 (2004) 3886-3896
9. Tateishi S., Niwa H., Miyazaki J., Fujimoto S., Inoue H., and Yamaizumi M. Enhanced genomic instability and defective postreplication repair in RAD18 knockout mouse embryonic stem cells. Mol. Cell. Biol. 23 (2003) 474-481
10. Miyase S., Tateishi S., Watanabe K., Tomita K., Suzuki K., Inoue H., and Yamaizumi M. Differential regulation of Rad18 through Rad6-dependent mono- and polyubiquitination. J. Biol. Chem. 280 (2005) 515-524
11. Shiomi N., Mori M., Tsuji H., Imai T., Inoue H., Tateishi S., Yamaizumi M., and Shiomi T. Human RAD18 is involved in S phase-specific single-strand break repair without PCNA monoubiquitination. Nucleic Acids Res. 35 (2007) e9
12. Nakajima S., Lan L., Kanno S., Usami N., Kobayashi K., Mori M., Shiomi T., and Yasui A. Replication-dependent and -independent responses of RAD18 to DNA damage in human cells. J. Biol. Chem. 281 (2006) 34687-34695
13. Sonoda E., Hochegger H., Saberi A., Taniguchi Y., and Takeda S. Differential usage of non-homologous end-joining and homologous recombination in double strand break repair. DNA Repair (Amst.) 5 (2006) 1021-1029
14. Saberi A., Hochegger H., Szuts D., Lan L., Yasui A., Sale J.E., Taniguchi Y., Murakawa Y., Zeng W., Yokomori K., Helleday T., Teraoka H., Arakawa H., Buerstedde J.M., and Takeda S. RAD18 and poly(ADP-ribose) polymerase independently suppress the access of nonhomologous end joining to double-strand breaks and facilitate homologous recombination-mediated repair. Mol. Cell. Biol. 27 (2007) 2562-2571
15. Essers J., Theil A.F., Baldeyron C., van Cappellen W.A., Houtsmuller A.B., Kanaar R., and Vermeulen W. Nuclear dynamics of PCNA in DNA replication and repair. Mol. Cell. Biol. 25 (2005) 9350-9359
16. van der Laan R., Uringa E.J., Wassenaar E., Hoogerbrugge J.W., Sleddens E., Odijk H., Roest H.P., de Boer P., Hoeijmakers J.H., Grootegoed J.A., and Baarends W.M. Ubiquitin ligase Rad18Sc localizes to the XY body and to other chromosomal regions that are unpaired and transcriptionally silenced during male meiotic prophase. J. Cell Sci. 117 (2004) 5023-5033
17. Essers J., Hendriks R.W., Wesoly J., Beerens C.E., Smit B., Hoeijmakers J.H., Wyman C., Dronkert M.L., and Kanaar R. Analysis of mouse Rad54 expression and its implications for homologous recombination. DNA Repair (Amst.) 1 (2002) 779-793
18. Miura N., Miyamoto I., Asahina H., Satokata I., Tanaka K., and Okada Y. Identification and characterization of xpac protein, the gene product of the human XPAC (xeroderma pigmentosum group A complementing) gene. J. Biol. Chem. 266 (1991) 19786-19789
19. van Royen M.E., Cunha S.M., Brink M.C., Mattern K.A., Nigg A.L., Dubbink H.J., Verschure P.J., Trapman J., and Houtsmuller A.B. Compartmentalization of androgen receptor protein-protein interactions in living cells. J. Cell Biol. 177 (2007) 63-72
20. Dinant C., de Jager M., Essers J., van Cappellen W.A., Kanaar R., Houtsmuller A.B., and Vermeulen W. Activation of multiple DNA repair pathways by sub-nuclear damage induction methods. J. Cell Sci. 120 (2007) 2731-2740
21. Essers J., van Cappellen W.A., Theil A.F., van Drunen E., Jaspers N.G., Hoeijmakers J.H., Wyman C., Vermeulen W., and Kanaar R. Dynamics of relative chromosome position during the cell cycle. Mol. Biol. Cell 16 (2005) 769-775
22. Mortusewicz O., and Leonhardt H. XRCC1 and PCNA are loading platforms with distinct kinetic properties and different capacities to respond to multiple DNA lesions. BMC Mol. Biol. 8 (2007) 81
23. Perdiz D., Grof P., Mezzina M., Nikaido O., Moustacchi E., and Sage E. Distribution and repair of bipyrimidine photoproducts in solar UV-irradiated mammalian cells. Possible role of Dewar photoproducts in solar mutagenesis. J. Biol. Chem. 275 (2000) 26732-26742
24. Rodrigo G., Roumagnac S., Wold M.S., Salles B., and Calsou P. DNA replication but not nucleotide excision repair is required for UVC-induced replication protein A phosphorylation in mammalian cells. Mol. Cell. Biol. 20 (2000) 2696-2705
25. Tashiro S., Walter J., Shinohara A., Kamada N., and Cremer T. Rad51 accumulation at sites of DNA damage and in postreplicative chromatin. J. Cell Biol. 150 (2000) 283-291
26. Mari P.O., Florea B.I., Persengiev S.P., Verkaik N.S., Bruggenwirth H.T., Modesti M., Giglia-Mari G., Bezstarosti K., Demmers J.A., Luider T.M., Houtsmuller A.B., and van Gent D.C. Dynamic assembly of end-joining complexes requires interaction between Ku70/80 and XRCC4. Proc. Natl. Acad. Sci. USA 103 (2006) 18597-18602
27. Fulford J., Nikjoo H., Goodhead D.T., and O'Neill P. Yields of SSB and DSB induced in DNA by Al(K) ultrasoft X-rays and alpha-particles: comparison of experimental and simulated yields. Int. J. Radiat. Biol. 77 (2001) 1053-1066
28. Charlton D.E., Nikjoo H., and Humm J.L. Calculation of initial yields of single- and double-strand breaks in cell nuclei from electrons, protons and alpha particles. Int. J. Radiat. Biol. 56 (1989) 1-19
29. Meldrum R.A., Botchway S.W., Wharton C.W., and Hirst G.J. Nanoscale spatial induction of ultraviolet photoproducts in cellular DNA by three-photon near-infrared absorption. EMBO Rep. 4 (2003) 1144-1149
30. Barlow J.H., Lisby M., and Rothstein R. Differential regulation of the cellular response to DNA double-strand breaks in G1. Mol. Cell 30 (2008) 73-85
31. Zierhut C., and Diffley J.F. Break dosage, cell cycle stage and DNA replication influence DNA double strand break response. EMBO J. 27 (2008) 1875-1885
32. Szuts D., Simpson L.J., Kabani S., Yamazoe M., and Sale J.E. Role for RAD18 in homologous recombination in DT40 cells. Mol. Cell. Biol. 26 (2006) 8032-8041
33. Fu Y., Zhu Y., Zhang K., Yeung M., Durocher D., and Xiao W. Rad6-Rad18 mediates a eukaryotic SOS response by ubiquitinating the 9-1-1 checkpoint clamp. Cell 133 (2008) 601-611
34. Tarsounas M., Davies D., and West S.C. BRCA2-dependent and independent formation of RAD51 nuclear foci. Oncogene 22 (2003) 1115-1123
35. Tarsounas M., Davies A.A., and West S.C. RAD51 localization and activation following DNA damage. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 359 (2004) 87-93
36. Taniguchi T., Garcia-Higuera I., Andreassen P.R., Gregory R.C., Grompe M., and D'Andrea A.D. S-phase-specific interaction of the Fanconi anemia protein, FANCD2, with BRCA1 and RAD51. Blood 100 (2002) 2414-2420
37. Scully R., Chen J., Ochs R.L., Keegan K., Hoekstra M., Feunteun J., and Livingston D.M. Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell 90 (1997) 425-435
38. Tembe V., and Henderson B.R. Protein trafficking in response to DNA damage. Cell. Signal. 19 (2007) 1113-1120
39. Deckbar D., Birraux J., Krempler A., Tchouandong L., Beucher A., Walker S., Stiff T., Jeggo P., and Lobrich M. Chromosome breakage after G2 checkpoint release. J. Cell Biol. 176 (2007) 749-755
40. Mahadevaiah S.K., Turner J.M., Baudat F., Rogakou E.P., de Boer P., Blanco-Rodriguez J., Jasin M., Keeney S., Bonner W.M., and Burgoyne P.S. Recombinational DNA double-strand breaks in mice precede synapsis. Nat. Genet. 27 (2001) 271-276
41. de Vries F.A., de Boer E., van den Bosch M., Baarends W.M., Ooms M., Yuan L., Liu J.G., van Zeeland A.A., Heyting C., and Pastink A. Mouse Sycp1 functions in synaptonemal complex assembly, meiotic recombination, and XY body formation. Genes Dev. 19 (2005) 1376-1389
42. Moens P.B., Chen D.J., Shen Z., Kolas N., Tarsounas M., Heng H.H., and Spyropoulos B. Rad51 immunocytology in rat and mouse spermatocytes and oocytes. Chromosoma 106 (1997) 207-215