The p53 response to DNA damage in vivo is independent of DNA-dependent protein kinase

Molecular and Cellular Biology

Volumn 20, Issue 11, 2000, Pages 4075-4083

  Jhappan, Chamelli ^a   Yusufzai, Timur M ^a   Anderson, Stacie ^b   Anver, Miriam R ^c   Merlino, Glenn ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DNA DEPENDENT PROTEIN KINASE; PROTEIN BAX; PROTEIN P21; PROTEIN P53;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVITY; IMMUNOHISTOCHEMISTRY; IONIZING RADIATION; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; RADIOSENSITIVITY; SIGNAL TRANSDUCTION; TELANGIECTASIA; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELL CYCLE; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P21; CYCLINS; DNA DAMAGE; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; FEMALE; G1 PHASE; GAMMA RAYS; MALE; MICE; MICE, MUTANT STRAINS; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2; S PHASE; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

ANIMALIA; ATAXIA; ATAXIA TELANGIECTASIA; MAMMALIA;

EID: 0034025078     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.11.4075-4083.2000     Document Type: Article

References (48)

1. Anderson, C. W., and S. P. Lees-Miller. 1992. The nuclear serine/threonine protein kinase DNA-PK. Crit. Rev. Eukaryot. Gene Expr. 2:283-314.
2. Araki, R., A. Fujimori, K. Hamatani, K. Mita, T. Saito, M. Mori, R. Fukumura, M. Morimyo, M. Muto, M. Itoh, K. Tatsumi, and M. Abe. 1997. Nonsense mutation at Tyr-4046 in the DNA-dependent protein kinase catalytic subunit of severe combined immune deficiency mice. Proc. Natl. Acad. Sci. USA 94:2438-2443.
3. Araki, R., R. Fukumura, A. Fujimori, Y. Taya, Y. Shiloh, A. Kurimasa, S. Burma, G. C. Li, D. J. Chen, K. Sato, Y. Hoki, K. Tatsumi, and M. Abe. 1999. Enhanced phosphorylation of p53 serine 18 following DNA damage in DNA-dependent protein kinase catalytic subunit-deficient cells. Cancer Res. 59:3543-3546.
4. Banin, S., L. Moyal, S. Shieh, Y. Taya, C. W. Anderson, L. Chessa, N. I. Smorodinsky, C. Prives, Y. Reiss, Y. Shiloh, and Y. Ziv. 1998. Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 281: 1674-1677.
5. Barlow, C., K. D. Brown, C.-X. Deng, D. A. Tagle, and A. Wynshaw-Boris. 1997. Atm selectively regulates distinct p53-dependent cell-cycle checkpoint and apoptotic pathways. Nat. Genet. 17:453-456.
6. Barlow, C., S. Hirotsune, R. Paylor, M. Liyanage, M. Eckhaus, F. Collins, Y. Shiloh, J. N. Crawley, T. Ried, D. Tagle, and A. Wynshaw-Boris. 1996. Atm-deficient mice: a paradigm of ataxia telangiectasia. Cell 86:159-171.
7. Blunt, T., D. Gell, M. Fox, G. E. Taccioli, A. R. Lehmann, S. P. Jackson, and P. A. Jeggo. 1996. Identification of a nonsense mutation in the carboxyl-terminal region of DNA-dependent protein kinase catalytic subunit in the scid mouse. Proc. Natl. Acad. Sci. USA 93:10285-10290.
8. Bogue, M. A., C. Jhappan, and D. B. Roth. 1998. Analysis of variable (diversity) joining recombination in DNA dependent protein kinase (DNA-PK)-deficient mice reveals DNA-PK-independent pathways for both signal and coding joint formation. Proc. Natl. Acad. Sci. USA 22:15559-15564.
9. Bosma, G. C., R. P. Custer, and M. J. Bosma. 1983. A severe combined immunodeficiency mutation in the mouse. Nature 301:527-530.
10. Burma, S., A. Kurimasa, G. Xie, Y. Taya, R. Araki, M. Abe, H. A. Crissman, H. Ouyang, G. C. Li, and D. J. Chen. 1999. DNA-dependent protein kinase-independent activation of p53 in response to DNA damage. J. Biol. Chem. 274:17139-17143.
11. Canman, C. E., D. S. Lim, K. A. Cimprich, Y. Taya, K. Tamai, K. Sakaguchi, E. Appella, M. B. Kastan, and J. D. Siliciano. 1998. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 281:1677-1679.
12. Clarke, A. R., C. A. Purdie, D. J. Harrison, R. G. Morris, C. C. Bird, M. L. Hooper, and A. H. Wyllie. 1993. Thymocyte apoptosis induced by p53-dependent and independent pathways. Nature 362:849-852.
13. Critchlow, S. E., and S. P. Jackson. 1998. DNA end-joining: from yeast to man. Trends Biochem. Sci. 23:394-398.
14. Danska, J. S., and C. J. Guidos. 1997. Essential and perilous: V(D)J recombination and DNA damage checkpoints in lymphocyte precursors. Semin. Immunol. 9:199-206.
15. Danska, J. S., D. P. Holland, S. Mariathasan, K. M. Williams, and C. J. Guidos. 1996. Biochemical and genetic defects in the DNA-dependent protein kinase in murine scid lymphocytes. Mol. Cell. Biol. 16:5507-5517.
16. Deng, C., P. Zhang, J. W. Harper, S. J. Elledge, and P. Leder. 1995. Mice lacking p21CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell 82:675-684.
17. el-Deiry, W. S., T. Tokino, V. E. Velculescu, D. B. Levy, R. Parsons, J. M. Trent, D. Lin, W. E. Mercer, K. W. Kinzler, and B. Vogelstein. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825.
18. Elson, A., Y. Wang, C. J. Daugherty, C. C. Morton, F. Zhou, J. Campos-Torres, and P. Leder. 1996. Pleiotropic defects in ataxia-telangiectasia protein-deficient mice. Proc. Natl. Acad. Sci. USA 93:13084-13089.
19. Finnie, N. J., T. M. Gottlieb, T. Blunt, P. A. Jeggo, and S. P. Jackson. 1995. DNA-dependent protein kinase activity is absent in xrs-6 cells: implications for site-specific recombination and DNA double-strand break repair. Proc. Natl. Acad. Sci. USA 92:320-324.
20. Fiscella, M., S. J. Ullrich, N. Zambrano, M. T. Shields, D. Lin, S. P. Lees-Miller, C. W. Anderson, W. E. Mercer, and E. Appella. 1993. Mutation of the serine 15 phosphorylation site of human p53 reduces the ability of p53 to inhibit cell cycle progression. Oncogene 8:1519-1528.
21. Fried, L. M., C. Koumenis, S. R. Peterson, S. L. Green, P. van Zijl, J. Allalunis-Turner, D. J. Chen, R. Fishel, A. J. Giaccia, J. M. Brown, and C. U. Kirchgessner. 1996. The DNA damage response in DNA-dependent protein kinase-deficient scid mouse cells: replication protein A hyperphosphorylation and p53 induction. Proc. Natl. Acad. Sci. USA 93:13825-13830.
22. Gao, Y., J. Chaudhuri, C. Zhu, L. Davidson, D. T. Wearer, and F. W. Alt. 1998. A targeted DNA-PKcs-null mutation reveals DNA-PK-independent functions for KU in V(D)J recombination. Immunity 9:367-376.
23. Gottlieb, T. M., and S. P. Jackson. 1993. The DNA-dependent protein kinase: requirement for DNA ends and association with Ku antigen. Cell 72: 131-142.
24. Gurley, K. E., and C. J. Kemp, 1996. p53 induction, cell cycle checkpoints, and apoptosis in DNAPK-deficient scid mice. Carcinogenesis 17:2537-2542.
25. Hartley, K. O., D. Gell, G. C. Smith, H. Zhang, N. Divecha, M. A. Connelly, A. Admon, S. P. Lees-Miller, C. W. Anderson, and S. P. Jackson. 1995. DNA-dependent protein kinase catalytic subunit: a relative of phosphatidylinositol 3-kinase and the ataxia telangiectasia gene product. Cell 82:849-856.
26. Huang, L. C., K. C. Clarkin, and G. M. Wahl. 1996. p53-dependent cell cycle arrests are preserved in DNA-activated protein kinase-deficient mouse fibroblasts. Cancer Res. 56:2940-2944.
27. Jeggo, P. A. 1997. DNA-PK: at the cross-roads of biochemistry and genetics. Mutat. Res. 384:1-14.
28. Jhappan, C., H. C. Morse III, R. D. Fleischmann, M. M. Gottesman, and G. Merlino. 1997. DNA-PKcs: a T-cell tumour suppressor encoded at the mouse scid locus. Nat. Genet. 17:483-486.
29. Jimenez, G. S., F. Bryntesson, M. I. Torres-Arzayus, A. Priestley, M. Beeche, S. Saito, K. Sakaguchi, E. Apella, P. A. Jeggo, G. E. Taccioli, G. M. Wahl, and M. Hubank. 1999. DNA-dependent protein kinase is not required for the p53-dependent response to DNA damage. Nature 400:81-83.
30. Kemp, C. J., K. Vo, and K. E. Gurley. 1999. Resistance to skin tumorigenesis in DNAPK-deficient SCID mice is not due to immunodeficiency but results from hypersensitivity to TPA-induced apoptosis. Carcinogenesis 11:2051-2056.
31. Kuhn, A., T. M. Gottlieb, S. P. Jackson, and I. Grummt. 1995. DNA-dependent protein kinase: a potent inhibitor of transcription by RNA polymerase I. Genes Dev. 9:193-203.
32. Lane, D. 1998. Awakening angels. Nature 394:616-617.
33. Lees-Miller, S. P., K. Sakaguchi, S. J. Ullrich, E. Appella, and C. W. Anderson. 1992. Human DNA-activated protein kinase phosphorylates serines 15 and 37 in the ammo-terminal transactivation domain of human p53. Mol. Cell. Biol. 12:5041-5049.
34. Levin, S., T. J. Bucci, S. M. Cohen, A. S. Fix, J. F. Hardisty, E. K. LeGrand, R. P. Maronpot, and B. F. Trump. 1999. The nomenclature of cell death: recommendations of an ad hoc committee of the Society of Toxicologic Pathologists. Toxicol. Pathol. 27:484-490.
35. Levine, A. J. 1997. p53, the cellular gatekeeper for growth and division. Cell 88:323-331.
36. Lieber, M. R. 1988. The defect in murine severe combined immune deficiency: joining of signal sequences but not coding segments in V(D)J recombination. Cell 55:7-16.
37. Lowe, S. W., E. M. Schmitt, S. W. Smith, B. A. Osborne, and T. Jacks. 1993. p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature 362:847-849.
38. Malynn, B. A., T. K. Blackwell, G. M. Fulop, G. A. Rathbun, A. J. Furley, P. Ferrier, L. B. Heinke, R. A. Phillips, G. D. Yancopoulos, and F. W. Alt. 1988. The scid defect affects the final step of the immunoglobulin VDJ recombinase mechanism. Cell 54:453-460.
39. Miyashita, T., and J. C. Reed. 1995. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 80:293-299.
40. Prives, C. 1998. Signaling to p53: breaking the MDM2-p53 circuit. Cell 95:5-8.
41. Rathmell, W. K., W. K. Kaufmann, J. C. Hurt, L. L. Byrd, and G. Chu. 1997. DNA-dependent protein kinase is not required for accumulation of p53 or cell cycle arrest after DNA damage. Cancer Res. 57:68-74.
42. Roth, D. B., J. P. Menetski, P. B. Nakajima, M. J. Bosma, and M. Gellert. 1992. V(D)J recombination: broken DNA molecules with covalently sealed (hairpin) coding ends in scid mouse thymocytes. Cell 70:983-991.
43. Savitsky, K., A. Bar-Shira, S. Gilad, G. Rotman, Y. Ziv, L. Vanagaite, D. A. Tagle, S. Smith, T. Uziel, S. Sfez, et al. 1995. A single ataxia telangiectasia gene with a product similar to PI-3 kinase. Science 268:1749-1753.
44. Suwa, A., M. Hirakata, Y. Takeda, S. A. Jesch, T. Mimori, and J. A. Hardin. 1994. DNA-dependent protein kinase (Ku protein-p350 complex) assembles on double-stranded DNA. Proc. Natl. Acad. Sci. USA 91:6904-6908.
45. Szumiel, I. 1998. Monitoring and signaling of radiation-induced damage in mammalian cells. Radiat. Res. 150:92-101.
46. Taccioli, G. E., A. G. Amatucci, H. J. Beamish, D. Gell, X. H. Xiang, M. I. Torres Arzayus, A. Priestley, S. P. Jackson, A. Marshak Rothstein, P. A. Jeggo, and V. L. Herrera. 1998. Targeted disruption of the catalytic subunit of the DNA-PK gene in mice confers severe combined immunodeficiency and radiosensitivity. Immunity 9:355-366.
47. Weaver, D. T. 1996. Regulation and repair of double-strand DNA breaks. Crit. Rev. Eukaryot. Gene Expr. 6:345-375.
48. Woo, R. A., K. G. McLure, S. P. Lees-Miller, D. E. Rancourt, and P. W. Lee. 1998. DNA-dependent protein kinase acts upstream of p53 in response to DNA damage. Nature 394:700-704.