Accumulation of Ku80 proteins at DNA double-strand breaks in living cells

Experimental Cell Research

Volumn 314, Issue 5, 2008, Pages 1061-1070

  Koike, Manabu ^a   Koike, Aki ^a  

^a NATIONAL INSTITUTE OF RADIOLOGICAL SCIENCES   (Japan)

Author keywords

DNA double strand breaks; Irradiation; Ku70; Ku80; H2AX

Indexed keywords

DNA BINDING PROTEIN; DOUBLE STRANDED DNA; ENHANCED GREEN FLUORESCENT PROTEIN; KU ANTIGEN; PROTEIN KU80; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DNA BINDING; DOUBLE STRANDED DNA BREAK; HUMAN; HUMAN CELL; IRRADIATION; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SUMOYLATION;

EID: 39549104283     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yexcr.2007.11.014     Document Type: Article

References (45)

1. Khanna K.K., and Jackson S.P. DNA double-strand breaks: signaling, repair and the cancer connection. Nat. Genet. 27 (2001) 247-254
2. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev., Cancer 3 (2003) 155-168
3. Rogakou E.P., Pilch D.R., Orr A.H., Ivanova V.S., and Bonner W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273 (1998) 5858-5868
4. Rogakou E.P., Boon C., Redon C., and Bonner W.M. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146 (1999) 905-916
5. Hopfner K.P., Putnam C.D., and Tainer J.A. DNA double-strand break repair from head to tail. Curr. Opin. Struct. Biol. 12 (2002) 115-122
6. Lees-Miller S.P. The DNA-dependent protein kinase, DNA-PK: 10 years and no ends in sight. Biochem. Cell. Biol. 74 (1996) 503-512
7. Critchlow S.E., Bowater R.P., and Jackson S.P. Mammalian DNA double-strand break repair protein XRCC4 interacts with DNA ligase IV. Curr. Biol. 7 (1997) 588-598
8. Leber R., Wise T.W., Mizuta R., and Meek K. The XRCC4 gene product is a target for and interacts with the DNA-dependent protein kinase. J. Biol. Chem. 273 (1998) 1794-1801
9. Ma Y., Pannicke U., Schwarz K., and Lieber M.R. Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination. Cell 108 (2002) 781-794
10. Gottlieb T.M., and Jackson S.P. The DNA-dependent protein kinase: requirement for DNA ends and association with Ku antigen. Cell 72 (1993) 131-142
11. Gell D., and Jackson S.P. Mapping of protein-protein interactions within the DNA-dependent protein kinase complex. Nucleic Acids Res. 27 (1999) 3494-3502
12. Walker J.R., Corpina R.A., and Goldberg J. Structure of the Ku heterodimer bound to DNA and its implications for double-strand break repair. Nature 412 (2001) 607-614
13. Wang J., Dong X., Myung K., Hendrickson E.A., and Reeves W.H. Identification of two domains of the p70 Ku protein mediating dimerization with p80 and DNA binding. J. Biol. Chem. 273 (1998) 842-848
14. Rivera-Calzada A., Spagnolo L., Pearl L.H., and Llorca O. Structural model of full-length human Ku70-Ku80 heterodimer and its recognition of DNA and DNA-PKcs. EMBO Rep. 8 (2007) 56-62
15. Koike M. Dimerization, translocation and localization of Ku70 and Ku80 proteins. J. Radiat. Res. 43 (2002) 223-236
16. Song Y., Lim J.W., Kim H., Morio T., and Kim K.H. Oxidative stress induces nuclear loss of DNA repair proteins Ku70 and Ku80 and apoptosis in pancreatic acinar AR42J cells. J. Biol. Chem. 278 (2003) 36676-36687
17. Yurchenko V., Xue Z., and Sadofsky M.J. SUMO modification of human XRCC4 regulates its localization and function in DNA double-strand break repair. Mol. Cell. Biol. 26 (2006) 1786-1794
18. Gocke C.B., Yu H., and Kang J. Systematic identification and analysis of mammalian small ubiquitin-like modifier substrates. J. Biol. Chem. 280 (2005) 5004-5012
19. Zhao X., and Blobel G. A SUMO ligase is part of a nuclear multiprotein complex that affects DNA repair and chromosomal organization. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 4777-4782
20. Jakob B., Scholz M., and Taucher-Scholz G. Characterization of CDKN1A (p21) binding to sites of heavy-ion-induced damage: colocalization with proteins involved in DNA repair. Int. J. Radiat. Biol. 78 (2002) 75-88
21. Lisby M., Barlow J.H., Burgess R.C., and Rothstein R. Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 118 (2004) 699-713
22. Kim J.S., Krasieva T.B., Kurumizaka H., Chen D.J., Taylor A.M., and Yokomori K.J. Independent and sequential recruitment of NHEJ and HR factors to DNA damage sites in mammalian cells. J. Cell Biol. 170 (2005) 341-347
23. 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. U. S. A. 103 (2006) 18597-18602
24. Singleton B.K., Priestley A., Steingrimsdottir H., Gell D., Blunt T., Jackson S.P., Lehmann A.R., and Jeggo P.A. Molecular and biochemical characterization of xrs mutants defective in Ku80. Mol. Cell. Biol. 17 (1997) 1264-1273
25. Koike M., and Koike A. Establishment and characterization of stable cell Lines expressing human Ku80 tagged with enhanced green fluorescent protein. J. Radiat. Res. 45 (2004) 119-125
26. Koike M., Ikuta T., Miyasaka T., and Shiomi T. The nuclear localization signal of the human Ku70 is a variant bipartite type recognized by the two components of nuclear pore-targeting complex. Exp. Cell Res. 250 (1999) 401-413
27. Koike M., Miyasaka T., Mimori T., and Shiomi T. Subcellular localization and protein-protein interaction regions of Ku proteins. Biochem. Biophys. Res. Commun. 252 (1998) 679-685
28. Koike M., Shiomi T., and Koike A. Dimerization and nuclear localization of Ku proteins. J. Biol. Chem. 276 (2001) 11167-11173
29. Koike M., Ikuta T., Miyasaka T., and Shiomi T. Ku80 can translocate to the nucleus independent of the translocation of Ku70 using its own nuclear localization signal. Oncogene 18 (1999) 7495-7505
30. Koike M., and Koike A. The Ku70-binding site of Ku80 is required for the stabilization of Ku70 in the cytoplasm, for the nuclear translocation of Ku80, and for Ku80-dependent DNA repair. Exp. Cell Res. 305 (2005) 266-276
31. Koike M., Awaji T., Kataoka M., Tsujimoto G., Kartasova T., Koike A., and Shiomi T. Differential subcellular localization of DNA-dependent protein kinase components Ku and DNA-PKcs during mitosis. J. Cell Sci. 112 (1999) 4031-4039
32. Jin S., and Weaver D.T. Double-strand break repair by Ku70 requires heterodimerization with Ku80 and DNA binding functions. EMBO J. 16 (1997) 6874-6885
33. Tuteja R., and Tuteja N. Ku autoantigen: a multifunctional DNA-binding protein. Crit. Rev. Biochem. Mol. Biol. 35 (2000) 1-33
34. Williams E.S., Stap J., Essers J., Ponnaiya B., Luijsterburg M.S., Krawczyk P.M., Ullrich R.L., Aten J.A., and Bailey S.M. DNA double-strand breaks are not sufficient to initiate recruitment of TRF2. Nat. Genet. 39 (2007) 696-698
35. Uematsu N., Weterings E., Yano K., Morotomi-Yano K., Jakob B., Taucher-Scholz G., Mari P.O., van Gent D.C., Chen B.P., and Chen D.J. Autophosphorylation of DNA-PKCS regulates its dynamics at DNA double-strand breaks. J. Cell Biol. 177 (2007) 219-229
36. Wang J., Dong X., and Reeves W.H. A Model for Ku heterodimer assembly and interaction with DNA. Implications for the function of Ku antigen. J. Biol. Chem. 273 (1998) 31068-31074
37. Rodriguez M.S., Dargemont C., and Hay R.T. SUMO-1 conjugation in vivo requires both a consensus modification motif and nuclear targeting. J. Biol. Chem. 276 (2001) 12654-12659
38. Sampson D.A., Wang M., and Matunis M.J. The small ubiquitin-like modifier-1 (SUMO-1) consensus sequence mediates Ubc9 binding and is essential for SUMO-1 modification. J. Biol. Chem. 276 (2001) 21664-21669
39. Jakob B., Scholz M., and Taucher-Scholz G. Immediate localized CDKN1A (p21) radiation response after damage produced by heavy-ion tracks. Radiat. Res. 154 (2000) 398-405
40. Rapp A., and Greulich K.O. After double-strand break induction by UV-A, homologous recombination and nonhomologous end joining cooperate at the same DSB if both systems are available. J. Cell Sci. 117 (2004) 4935-4945
41. Bekker-Jensen S., Lukas C., Kitagawa R., Melander F., Kastan M.B., Bartek J., and Lukas J. Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J. Cell Biol. 173 (2006) 195-206
42. Chou C.H., Wang J., Knuth M.W., and Reeves W.H. Role of a major autoepitope in forming the DNA binding site of the p70 (Ku) antigen. J. Exp. Med. 175 (1992) 1677-1684
43. Yoo S., and Dynan W.S. Geometry of a complex formed by double strand break repair proteins at a single DNA end: recruitment of DNA-PKcs induces inward translocation of Ku protein. Nucleic Acids Res. 27 (1999) 4679-4686
44. Wang H., Perrault A.R., Takeda Y., Qin W., Wang H., and Iliakis G. Biochemical evidence for Ku-independent backup pathways of NHEJ. Nucleic Acids Res. 31 (2003) 5377-5388
45. Guirouilh-Barbat J., Huck S., Bertrand P., Pirzio L., Desmaze C., Sabatier L., and Lopez B.S. Impact of the KU80 pathway on NHEJ-induced genome rearrangements in mammalian cells. Mol. Cell. 14 (2004) 611-623