Telomere dysfunction and DNA-PKcs deficiency: Characterization and consequence

Cancer Research

Volumn 69, Issue 5, 2009, Pages 2100-2107

  Williams, Eli S ^a,b   Klingler, Rebekah ^a   Ponnaiya, Brian ^c   Hardt, Tanja ^d,e   Schrock, Evelin ^d   Lees Miller, Susan P ^f   Meek, Katheryn ^g   Ullrich, Robert L ^a   Bailey, Susan M ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

^c Och Spine at New York Presbyterian Hospitals   (United States)

^d DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^e RUHR UNIVERSITY BOCHUM   (Germany)

^f UNIVERSITY OF CALGARY   (Canada)

^g MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DEPENDENT PROTEIN KINASE; THREONINE; DNA BINDING PROTEIN; NUCLEAR PROTEIN; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE (ATP); PRKDC PROTEIN, MOUSE;

ANIMAL CELL; ARTICLE; BREAST; BREAST CANCER; CANCER SUSCEPTIBILITY; CARCINOGENESIS; CONTROLLED STUDY; DNA DEPENDENT PROTEIN KINASE DEFICIENCY; DOUBLE STRANDED DNA BREAK; EMBRYO; ENVIRONMENTAL FACTOR; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME PHOSPHORYLATION; FEMALE; GENETIC DISORDER; GENETIC SUSCEPTIBILITY; GENOMIC INSTABILITY; IONIZING RADIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; RADIOSENSITIVITY; SINGLE NUCLEOTIDE POLYMORPHISM; TELOMERE; TELOMERE DYSFUNCTION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; PHOSPHORYLATION; PHYSIOLOGY;

ANIMALS; DNA BREAKS, DOUBLE-STRANDED; DNA LIGASES; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; FEMALE; GENOMIC INSTABILITY; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NUCLEAR PROTEINS; PHOSPHORYLATION; TELOMERE;

EID: 62449198947     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-2854     Document Type: Article

References (52)

1. Bailey SM, Meyne J, Chen. DJ, et al. DNA double-strand break repair proteins are required to cap the ends of mammalian chromosomes. Proc Natl Acad Sei U S A 1999;96:14899-14904
2. Verdun RE, Karlseder J. Replication and protection, of telomeres. Nature 2007:447:924-931
3. CuI X, Yu Y, Gupta S, Cho YM, Lees-Miller SP, Meek K. Autophosphorylation of DNA-dependent protein kinase regulates DNA end processing and may also alter double-strand break repair pathway choice. MoI Cell Biol 2005;25:10842-10852
4. Block. WD, Yu Y1 Merkle D1 et al. Autophosphorylation-dependent remodeling of the DNA-dependent protein kinase catalytic subunit regulates ligation of DNA ends. Nucleic Acids Res 2004;32:4351-4357
5. Chan DW, Chen BP, Prithivirajsingh S, et al. Auto-phosphorylation of the DNA-dependent protein, kinase catalytic subunit is required for rejoining of DNA double-strand breaks. Genes Dev 2002;16:2333-2338
6. Ding Q, Reddy YV Wang W, et al. Autophosphorylation of the catalytic subunit of the DNA-dependent protein kinase is required for efficient end processing during DNA double-strand break repair. MoI Cell Biol 2003:23: 5836-5848
7. Soubeyrand S, Pope L1 Pakuts B1 Hache RJ. Threonines 2638/2647 in DNA-PK are essential for cellular resistance to ionizing radiation. Cancer Res 2003; 63:1.198-201.
8. Douglas P, Sapkota GP, Morrice N, et al. Identification of in vitro and in vivo phosphorylation sites in the catalytic subunit of the DNA-dependent protein kinase. Biochem. J 2002;368:243-251
9. Meek K, Douglas P1 Cui X, Ding Q, Lees-Miller SP. trans Autophosphorylation at DNA-dependent protein kinase's two major autophosphorylation site clusters facilitates end processing but not end joining. MoI Cell Biol 2007;27:3881-3890
10. Chen BP, Uematsu N, Kobayashi J, et al. Ataxia telangiectasia mutated (ATM) is essential for DNA-PKcs phosphorylations at the Thr-2609 cluster upon DNA double strand break. J Biol Chem 2007;282:6582-6587
11. Bredemeyer AL, Sharma GG1 Huang CY1 et al. ATM stabilizes DNA double-strand-break complexes during V(D)J recombination. Nature 2006;442:466-470
12. Bailey SM, Goodwin EH. DNA and telomeres: beginnings and endings. Cytogenet Genome Res 2004; 104:109-115
13. Goytlsolo FA, Samper E, Edmonson S1 Taccloli GE1 Blasco MA. The absence of the DNA-dependent protein kinase catalytic subunit in mice results in. anaphase bridges and in increased telomeric fusions with normal telomere length and. G-strand overhang. MoI Cell Biol 2001;21:3642-51.
14. Gilley D, Tanaka H, Hande MP, et al. DNA-PKcs is critical, for telomere capping. Proc Natl. Acad Sei U S A 2001;98:15084-15088
15. Bailey SM, Cornforth MN, Ullrich RL, Goodwin EH. Dysfunctional mammalian telomeres join with DNA double-strand breaks. DNA Repair (Amst) 2004;3:349-357
16. Bailey SM, Cornforth MN. Telomeres and DNA double-strand breaks: ever the twain shall meet? Cell Mol Life Sei 2007;64:2956-2964
17. Bailey SM, Goodwin EH, Cornforth MN. Strand-specific fluorescence in situ hybridization: the CO-FISH family. Cytogenet Genome Res 2004;107:14-17
18. Kllburn AE, Shea MJ1 Sargent RG1 Wilson JH. Insertion of a telomere repeat sequence into a mammalian gene causes chromosome instability. MoI Cell BIoI 2001;21:126-135
19. Ohki R, Ishikawa F. Telomere-bound TRFl. and TRF2 stall the replication fork at telomerlc repeats. Nucleic Acids Res 2004;32:1627-1637
20. Sabotier L1 Rlcoul M1 Pottier G1 Murnane JP. The loss of a single telomere can result in instability of multiple chromosomes in a human tumor ceU line. MoI Cancer Res 2005;3:139-150
21. Bhatti P, Struewing JP, Alexander BH, et al. Poly-morphisms in. DNA repair genes, ionizing radiation exposure and risk of breast cancer In U.S. Radiologic technologists. Int J Cancer 2008;122:177-182
22. Yu Y, Okayasu R, Well MM, et al. Elevated breast cancer risk in irradiated BALB/c mice associates with unique functional polymorphism of the Prkdc (DNA-dependent protein, kinase catalytic subunit) gene. Cancer Res 2001;61:1820-1824.
23. Okayasu R1 Suetoml K1 Yu Y1 et al. A deficiency in DNA repair and DNA-PKcs expression in the radiosen-sitive BALB/c mouse. Cancer Res 2000;60:4342-4345
24. Ullrich RL, Bowles ND, Satterfield LC, Davis CM. Strain-dependent susceptibility to radiation-induced mammary cancer is a result of differences in epithelial cell sensitivity to transformation. Radiât Res 1996:1.46: 353-355
25. Moll U, Lau R1 Sypes MA1 Gupta MM1 Anderson CW. DNA-PK, the DNA-activated protein kinase, is differen-tially expressed in normal and malignant human tissues. Oncogene 1999:18:3114-3126
26. Someya M, Sakata K, Matsumoto Y, et al. The association of DNA-dependent protein, kinase activity with chromosomal instability and risk of cancer. Carcinogenesis 2006;27:117-122
27. Riballo E, Kühne M1 Rief N1 et al. A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to 7-H2AX foci. MoI Cell 2004;16:715-724
28. Ethier SP, Mahacek ML, GulUck WJ, Frank TS, Weber BL. Differential isolation of normal, luminal mammary epithelial cells and breast cancer cells from primary and metastatic sites using selective media Cancer Res 1993; 53:627-635
29. Ethier SP, Ullrich RL. Detection of ductal dysplasia in mammary outgrowths derived from carcinogen-treated virgin female BALB/c mice. Cancer Res 1982; 42:1753-1760
30. Medina D, Kittrell FS. p53 function is required for hormone-mediated protection of mouse mammary tumorigenesis. Cancer Res 2003:63:61.40-3
31. Ponnaiya B, Cornforth MN, Ullrich RL. Radiation-induced chromosomal instability in BALB/c and CSTBLI 6 mice: the difference is as clear as black and white. Radiât Res 1997;147:121-125
32. Zhang Y, Lim. CU, Williams ES, et al. NBSI knockdown by small interfering RNA increases ionizing radiation mutagenesis and telomere association in. human cells. Cancer Res 2005;65:5544-5553
33. Schrock E, Zschieschang P, O'Brien P, et al. Spectral karyotyping of human, mouse, rat and ape chromo-somes-applications for genetic diagnostics and re-search. Cytogenet Genome Res 2006:114:199-221.
34. Schrock E, du Manoir S, Veldman T1 et al. Multicolor spectral karyotyping of human chromosomes. Science 1996;273:494-497
35. Smogorzewska A, De Lange T. Different telomere damage signaling pathways in human and mouse ceUs. EMBO J 2002;21:4338-4348
36. Veuger SJ, Curün NJ, Richardson CJ, Smith GC, Durkacz BW. Radiosensitization. and DNA repair inhibition by the combined use of novel inhibitors of DNA-dependent protein kinase and poly(ADP-ribose) polymerase-!. Cancer Res 2003;63:6008-6015
37. Frank KM, Sharpless NE, Gao Y, et al. DNA ligase IV deficiency in mice leads to defective neurogenesis and embryonic lethality via the p53 pathway. MoI. Cell 2000; 5:993-1002.
38. Ferguson DO, Sekiguchi JM, Chang S, et al. The nonhomologous end-joining pathway of DNA repair is required for genomic stability and the suppression of translocations. Proc Natl. Acad ScI USA. 2000;97:6630-6633
39. Bailey SM, Cornforth MN, Kurimasa A, Chen DJ, Goodwin EH. Strand-specific postreplicative processing of mammalian telomeres. Science 2001;293:2462-2465
40. Bailey SM, Brenneman. MA, Halbrook J, Nickoloff JA, Ullrich RL, Goodwin EH. The kinase activity of DNA-PK is required to protect mammalian telomeres. DNA Repair (Amst) 2004;3:225-233
41. Takal H, Smogorzewska A, de Lange T. DNA damage foci at dysfunctional telomeres. Curr Biol 2003; 13:1549-1556
42. Zhang Y, Zhou J, Cao X, et al. Partial deficiency of DNA-PKcs increases ionizing radiation-induced muta-genesis and telomere instability in human cells. Cancer Lett 2007;250:63-73.
43. van. Steensel B, Smogorzewska A, de Lange T. TRF2 protects human telomeres from end-to-end fusions. Cell 1998:92:401-413
44. Selvanayagam CS, Davis CM, Cornforth MN, Ullrich RL. Latent expression of p53 mutations and radiation-induced mammary cancer. Cancer Res 1995; 55:3310-3317
45. Maser RS, Wong KK, Sahin E, et al. DNA-dependent protein, kinase catalytic subunit is not required for dysfunctional telomere fusion and checkpoint response in the telomerase-deficient mouse. MoI. Cell Biol 2007;27: 2253-2265
46. Capper R, Britt-Compton B, Tankimanova M, et al. The nature of telomere fusion and a definition of the critical telomere length in human ceUs. Genes Dev 2007; 21:2495-2508
47. Smogorzewska A, Karlseder J, Holtgreve-Grez H, Jauch A, de Lange T. DNA. ligase IV-dependent NHEJ of deprotected mammalian telomeres In G1 and G2. Curr Biol 2002:12:1635.
48. Wang X, Baumann P. Chromosome fusions following telomere loss are mediated by single-strand annealing. MoI Cell 2008:31:463-473
49. Karlseder J, Hoke K1 Mirzoeva O.K., et al. The telomeric protein. TRF2 binds the ATM kinase and can inhibit the ATM-dependent DNA damage response. PLoS Biol 2004;2:E240.
50. Wang RC, Smogorzewska A de Lange T. Homologous recombination generates T-loop-sized deletions at human telomeres. CeU 2004;119:355-368
51. Crabbe L, Verdun RE, Haggblom CI, Karlseder J. Defective telomere lagging strand synthesis in cells lacking WRN heUcase activity. Science 2004;306:1951-1953.
52. Martin M, Genesca A, Latre L, et al. Postreplicative joining of DNA double-strand breaks causes genomic instability in DNA-PKcs-deficient mouse embryonic fibroblasts. Cancer Res 2005;65:10223-10232