Ku regulates signaling to DNA damage response pathways through the Ku70 von Willebrand A domain

Molecular and Cellular Biology

Volumn 32, Issue 1, 2012, Pages 76-87

  Fell, Victoria L ^a   Schild Poulter, Caroline ^a  

^a ROBARTS RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; KU ANTIGEN; UNCLASSIFIED DRUG; VON WILLEBRAND A; VON WILLEBRAND FACTOR;

ALPHA HELIX; APOPTOSIS; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; ENZYME ACTIVATION; HUMAN; IONIZING RADIATION; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ACTIVATING TRANSCRIPTION FACTOR 2; ANIMALS; ANTIGENS, NUCLEAR; APOPTOSIS; CELL LINE; CELL SURVIVAL; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; HUMANS; MUTATION; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; VON WILLEBRAND FACTOR;

EID: 84856770897     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.05661-11     Document Type: Article

References (77)

1. Abraham RT. 2004. PI 3-kinase related kinases: 'big' players in stressinduced signaling pathways. DNA Repair (Amsterdam) 3:883-887.
2. Andrews NC, Faller DV. 1991. A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res. 19:2499.
3. Aravind L, Koonin EV. 2000. SAP-a putative DNA-binding motif involved in chromosomal organization. Trends Biochem. Sci. 25:112-114.
4. Aravind L, Koonin EV. 2001. Prokaryotic homologs of the eukaryotic DNA-end-binding protein Ku, novel domains in the Ku protein and prediction of a prokaryotic double-strand break repair system. Genome Res. 11:1365-1374.
5. Bennetzen MV, et al. 2010. Site-specific phosphorylation dynamics of the nuclear proteome during the DNA damage response. Mol. Cell Proteomics 9:1314-1323.
6. Bertinato J, Schild-Poulter C, Hache RJ. 2001. Nuclear localization of Ku antigen is promoted independently by basic motifs in the Ku70 and Ku80 subunits. J. Cell Sci. 114:89-99.
7. Bhoumik A, Lopez-Bergami P, Ronai Z. 2007. ATF2 on the double-activating transcription factor and DNA damage response protein. Pigment Cell Res. 20:498-506.
8. Bhoumik A, et al. 2005. ATM-dependent phosphorylation of ATF2 is required for the DNA damage response. Mol. Cell 18:577-587.
9. Cann KL, Hicks GG. 2007. Regulation of the cellular DNA double-strand break response. Biochem. Cell Biol. 85:663-674.
10. Chan DW, Ye R, Veillette CJ, Lees-Miller SP. 1999. DNA-dependent protein kinase phosphorylation sites in Ku 70/80 heterodimer. Biochemistry 38:1819-1828.
11. Cohen HY, et al. 2004. Acetylation of the C terminus of Ku70 by CBP and PCAF controls Bax-mediated apoptosis. Mol. Cell 13:627-638.
12. Collis SJ, Deweese TL, Jeggo PA, Parker AR. 2005. The life and death of DNA-PK. Oncogene 24:949-961.
13. Costantini S, Woodbine L, Andreoli L, Jeggo PA, Vindigni A. 2007. Interaction of the Ku heterodimer with the DNA ligase IV/Xrcc4 complex and its regulation by DNA-PK. DNA Repair (Amsterdam) 6:712-722.
14. Dobbs TA, Tainer JA, Lees-Miller SP. 2010. A structural model for regulation of NHEJ by DNA-PKcs autophosphorylation. DNA Repair 9:1307-1314.
15. Downs JA, Jackson SP. 2004. A means to a DNA end: the many roles of Ku. Nat. Rev. Mol. Cell Biol. 5:367-378.
16. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
17. Fernandez-Capetillo O, Lee A, Nussenzweig M, Nussenzweig A. 2004. H2AX: the histone guardian of the genome. DNA Repair (Amsterdam) 3:959-967.
18. Fulop GM, Phillips RA. 1990. The scid mutation in mice causes a general defect in DNA repair. Nature 347:479-482.
19. Gama V, et al. 2009. Hdm2 is a ubiquitin ligase of Ku70-Akt promotes cell survival by inhibiting Hdm2-dependent Ku70 destabilization. Cell Death Differ. 16:758-769.
20. Gu Y, Jin S, Gao Y, Weaver DT, Alt FW. 1997. Ku70-deficient embryonic stem cells have increased ionizing radiosensitivity, defective DNA end-binding activity, and inability to support V(D)J recombination. Proc. Natl. Acad. Sci. U. S. A. 94:8076-8081.
21. Gu Y, et al. 1997. Growth retardation and leaky SCID phenotype of Ku70-deficient mice. Immunity 7:653-665.
22. Hahn WC, Weinberg RA. 2002. Modelling the molecular circuitry of cancer. Nat. Rev. Cancer 2:331-341.
23. Hai T, Hartman MG. 2001. The molecular biology and nomenclature of the activating transcription factor/cAMP responsive element binding family of transcription factors: activating transcription factor proteins and homeostasis. Gene 273:1-11.
24. Harris R, et al. 2004. The 3D solution structure of the C-terminal region of Ku86 (Ku86CTR). J. Mol. Biol. 335:573-582.
25. Hartlerode AJ, Scully R. 2009. Mechanisms of double-strand break repair in somatic mammalian cells. Biochem. J. 423:157-168.
26. Helleday T, Lo J, van Gent DC, Engelward BP. 2007. DNA doublestrand break repair: from mechanistic understanding to cancer treatment. DNA Repair (Amsterdam) 6:923-935.
27. Hill R, Lee PW. 2010. The DNA-dependent protein kinase (DNA-PK): more than just a case of making ends meet? Cell Cycle 9:3460-3469.
28. Jiang H-Y, Wek SA, McGrath BC, Lu D, Hai T, Harding HP, Wang X, Ron D, Cavener DR, Wek RC. 2004. Activating transcription factor 3 is integral to the eukaryotic initiation factor 2 kinase stress response. Mol. Cell. Biol. 24:1365-1377.
29. Kang Y, Chen C-R, Massagué J. 2003. A self-enabling TGF[beta] response coupled to stress signaling: Smad engages stress response factor ATF3 for Id1 repression in epithelial cells. Mol. Cell 11:915-926.
30. Karagiannis TC, El-Osta A. 2004. Double-strand breaks: signaling pathways and repair mechanisms. Cell. Mol. Life Sci. 61:2137-2147.
31. Kashiwakura Y, et al. 2008. Down-regulation of inhibition of differentiation-1 via activation of activating transcription factor 3 and Smad regulates REIC/Dickkopf-3-induced apoptosis. Cancer Res. 68:8333-8341.
32. Kim J-S, Krasieva TB, Kurumizaka H, Chen DJ, Taylor AMR, Yokomori K. 2005. Independent and sequential recruitment of NHEJ and HR factors to DNA damage sites in mammalian cells. J. Cell Biol. 170:341-347.
33. Kinner A, Wu W, Staudt C, Iliakis G. 2008. γ-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res. 36:5678-5694.
34. Kool J, et al. 2003. Induction of ATF3 by ionizing radiation is mediated via a signaling pathway that includes ATM, Nibrin1, stress-induced MAP kinases and ATF-2. Oncogene 22:4235-4242.
35. Kurz EU, Lees-Miller SP. 2004. DNA damage-induced activation of ATM and ATM-dependent signaling pathways. DNA Repair 3:889-900.
36. Lavin MF, Kozlov S. 2007. ATM activation and DNA damage response. Cell Cycle 6:931-942.
37. Lee JH, Paull TT. 2007. Activation and regulation of ATM kinase activity in response to DNA double-strand breaks. Oncogene 26:7741-7748.
38. Lee SH, Bahn JH, Whitlock NC, Baek SJ. 2010. Activating transcription factor 2 (ATF2) controls tolfenamic acid-induced ATF3 expression via MAP kinase pathways. Oncogene 29:5182-5192.
39. Li GC, et al. 1998. Ku70: a candidate tumor suppressor gene for murine T cell lymphoma. Mol. Cell 2:1-8.
40. Li S, et al. 2010. Radiation sensitivity and tumor susceptibility in ATM phospho-mutant ATF2 mice. Genes Cancer 1:316-330.
41. Lieber MR. 2010. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu. Rev. Biochem. 79:181-211.
42. Lieber MR, Ma Y, Pannicke U, Schwarz K. 2003. Mechanism and regulation of human non-homologous DNA end-joining. Nat. Rev. Mol. Cell Biol. 4:712-720.
43. Lieber MR, Yu K, Raghavan SC. 2006. Roles of nonhomologous DNA end joining, V(D)J. recombination, and class switch recombination in chromosomal translocations. DNA Repair (Amsterdam) 5:1234-1245.
44. Linding R, et al. 2008. NetworKIN: a resource for exploring cellular phosphorylation networks. Nucleic Acids Res. 36:D695-D699.
45. Lopez-Bergami P, Lau E, Ronai Z. 2010. Emerging roles of ATF2 and the dynamic AP1 network in cancer. Nat. Rev. Cancer 10:65-76.
46. Lu D, Wolfgang CD, Hai T. 2006. Activating transcription factor 3, a stress-inducible gene, suppresses Ras-stimulated tumorigenesis. J. Biol. Chem. 281:10473-10481.
47. Mahaney BL, Meek K, Lees-Miller SP. 2009. Repair of ionizing radiationinduced DNA double-strand breaks by non-homologous end-joining. Biochem. J. 417:639-650.
48. Maytin EV, Ubeda M, Lin JC, Habener JF. 2001. Stress-inducible transcription factor CHOP/gadd153 induces apoptosis in mammalian cells via p38 kinase-dependent and -independent mechanisms. Exp. Cell Res. 267:193-204.
49. Meek K, Dang V, Lees-Miller SP. 2008. DNA-PK: the means to justify the ends, p. 33-58. InFrederick WA (ed.), Advances in immunology. Academic Press, New York, NY.
50. Mern DS, Hasskarl J, Burwinkel B. 2010. Inhibition of Id proteins by a peptide aptamer induces cell-cycle arrest and apoptosis in ovarian cancer cells. Br. J. Cancer 103:1237-1244.
51. Norbury CJ, Zhivotovsky B. 2004. DNA damage-induced apoptosis. Oncogene 23:2797-2808.
52. Nussenzweig A, Nussenzweig MC. 2007. A backup DNA repair pathway moves to the forefront. Cell 131:223-225.
53. Nussenzweig A, Sokol K, Burgman P, Li L, Li GC. 1997. Hypersensitivity of Ku80-deficient cell lines and mice to DNA damage: the effects of ionizing radiation on growth, survival, and development. Proc. Natl. Acad. Sci. U. S. A. 94:13588-13593.
54. Perk J, Iavarone A, Benezra R. 2005. Id family of helix-loop-helix proteins in cancer. Nat. Rev. Cancer 5:603-614.
55. Rathaus M, Lerrer B, Cohen HY. 2009. DeubiKuitylation: a novel DUB enzymatic activity for the DNA repair protein, Ku70. Cell Cycle 8:1843-1852.
56. Ribes-Zamora A, Mihalek I, Lichtarge O, Bertuch AA. 2007. Distinct faces of the Ku heterodimer mediate DNA repair and telomeric functions. Nat. Struct. Mol. Biol. 14:301-307.
57. Riches LC, Lynch AM, Gooderham NJ. 2008. Early events in the mammalian response to DNA double-strand breaks. Mutagenesis 23:331-339.
58. Riha K, Heacock ML, Shippen DE. 2006. The role of the nonhomologous end-joining DNA double-strand break repair pathway in telomere biology. Annu. Rev. Genet. 40:237-277.
59. Roberts SA, et al. 2010. Ku is a 5'-dRP/AP lyase that excises nucleotide damage near broken ends. Nature 464:1214-1217.
60. Roos WP, Kaina B. 2006. DNA damage-induced cell death by apoptosis. Trends Mol. Med. 12:440-450.
61. Rothkamm K, Kruger I, Thompson LH, Lobrich M. 2003. Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol. Cell. Biol. 23:5706-5715.
62. Ruzinova MB, Benezra R. 2003. Id proteins in development, cell cycle and cancer. Trends Cell Biol. 13:410-418.
63. Schild-Poulter C, Haché RJG, Soubeyrand S. 2004. Ku antigen: a versatile DNA binding protein with multiple cellular functions, p. 257-284. In Parisi V, De Fonzo V, Aluffi-Pentini F (ed.), Recent research developments in dynamical genetics, Research Signpost, Transworld Research Network.
64. Schild-Poulter C, et al. 2007. DNA-PK phosphorylation sites on Oct-1 promote cell survival following DNA damage. Oncogene 26:3980-3988.
65. Sekiguchi JM, Ferguson DO. 2006. DNA double-strand break repair: a relentless hunt uncovers new prey. Cell 124:260-262.
66. Shim EY, Ma JL, Oum JH, Yanez Y, Lee SE. 2005. The yeast chromatin remodeler RSC complex facilitates end joining repair of DNA doublestrand breaks. Mol. Cell. Biol. 25:3934-3944.
67. Smith GC, Jackson SP. 1999. The DNA-dependent protein kinase. Genes Dev. 13:916-934.
68. Su TT. 2006. Cellular responses to DNA damage: one signal, multiple choices. Annu. Rev. Genet. 40:187-208.
69. Thompson M, Xu D, Williams B. 2009. ATF3 transcription factor and its emerging roles in immunity and cancer. J. Mol. Med. 87:1053-1060.
70. Turchi L, et al. 2008. Hif-2alpha mediates UV-induced apoptosis through a novel ATF3-dependent death pathway. Cell Death Differ. 15:1472-1480.
71. Valerie K, Povirk LF. 2003. Regulation and mechanisms of mammalian double-strand break repair. Oncogene 22:5792-5812.
72. Walker JR, Corpina RA, Goldberg J. 2001. Structure of the Ku heterodimer bound to DNA and its implications for double-strand break repair. Nature 412:607-614.
73. Wek RC, Jiang HY, Anthony TG. 2006. Coping with stress: eIF2 kinases and translational control. Biochem. Soc. Trans. 34:7-11.
74. Whittaker CA, Hynes RO. 2002. Distribution and evolution of von Willebrand/integrin a domains: widely dispersed domains with roles in cell adhesion and elsewhere. Mol. Biol. Cell 13:3369-3387.
75. Xia Y, Ongusaha P, Lee SW, Liou Y-C. 2009. Loss of Wip1 sensitizes cells to stress- and DNA damage-induced apoptosis. J. Biol. Chem. 284:17428-17437.
76. Zhang X, Ling MT, Wong YC, Wang X. 2007. Evidence of a novel antiapoptotic factor: role of inhibitor of differentiation or DNA binding (Id-1) in anticancer drug-induced apoptosis. Cancer Sci. 98:308-314.
77. Zhang Z, et al. 2004. Solution structure of the C-terminal domain of Ku80 suggests important sites for protein-protein interactions. Structure (Cambridge) 12:495-502.