Cleavage and inactivation of DNA-dependent protein kinase catalytic subunit during apoptosis in Xenopus egg extracts

Journal of Cell Science

Volumn 109, Issue 13, 1996, Pages 3121-3127

  Le Romancer, Muriel ^a,b   Cosulich, Sabina C ^a   Jackson, Stephen P ^c   Clarke, Paul R ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b BICHAT HOSPITAL   (France)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Apoptosis; DNA dependent protein kinase; Programmed cell death; Protease; Xenopus

Indexed keywords

PROTEIN KINASE;

ANIMAL CELL; APOPTOSIS; ARTICLE; DNA REPAIR; ENZYME ACTIVE SITE; ENZYME DEGRADATION; ENZYME INACTIVATION; FEMALE; NONHUMAN; PRIORITY JOURNAL; XENOPUS;

1-PHOSPHATIDYLINOSITOL 3-KINASE; AMINO ACID SEQUENCE; ANDROSTADIENES; ANIMALS; APOPTOSIS; CATALYSIS; CELL EXTRACTS; CYSTEINE PROTEINASE INHIBITORS; DNA-ACTIVATED PROTEIN KINASE; DNA-BINDING PROTEINS; ENZYME INHIBITORS; HELA CELLS; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; OLIGOPEPTIDES; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-BCL-2; XENOPUS LAEVIS;

EID: 0030447538     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (50)

1. Ajmani, A. K., Satoh, M., Reap, E., Cohen, P. L. and Reeves, W. H. (1995). Absence of autoantigen Ku in mature human neutrophils and human promyelocytic leukemia line (HL-60) cells and lymphocytes undergoing apoptosis. J. Exp. Med. 181, 2049-2058.
2. Blier, P. R., Griffith, A. J., Craft, J. and Hardin, J. A. (1993). Binding of Ku protein to DNA. Measurement of affinity for ends and demonstration of binding to nicks. J. Biol. Chem. 268, 7594-7601.
3. Blunt, T., Finnie, N, J., Taccioli, G. E., Smith, G. C., Demengeot, J., Gottlieb, T. M., Mizuta, R., Varghese, A. J., Alt, F. W., Jeggo, P. A., et al. (1995). Defective DNA-dependent protein kinase activity is linked to V(D)J recombination and DNA repair defects associated with the murine scid mutation. Cell 80, 813-823.
4. Boubnov, N. V., Hall, K. T., Wills, Z., Lee, S. E., He, D. M., Benjamin, D. M., Pulaski, C. R., Band, H., Reeves, W., Hendrickson, E. A. and Weaver, D. T. (1995). Complementation of the ionizing radiation sensitivity, DNA end binding, and V(D)J recombination defects of double-stranded break repair mutants by p86 Ku autoantigen. Proc. Nat. Acad. Sci. USA 92, 890-894.
5. Casciola-Rosen, L. A., Anhalt, G. J. and Rosen, A. (1995). DNA-dependent protein kinase is one of a subset of autoantigens specifically cleaved early during apoptosis. J. Exp. Med. 182, 1625-1634.
6. Clarke, P. R. (1995). Preparation of Xenopus egg extracts and their utilization in cell cycle studies. In Cell Cycle: Materials and Methods (ed. M. Pagano), pp. 103-116. Springer-Verlag, Heidelberg.
7. Cosulich, S. C., Green, S. and Clarke, P. R. (1996). Bcl-2 regulates activation of apoptotic proteases in a cell-free system. Curr. Biol. 6, 997-1005.
8. de Murcia, G. and Menissier de Murcia, J. (1994). Poly(ADP-ribose) polymerase: a molecular nick-sensor. Trends Biochem. Sci. 19, 172-176.
9. Dvir, A., Peterson, S. R., Knuth, M. W., Lu, H. and Dynan, W. S. (1992). Ku autoantigen is the regulatory component of a template-associated protein kinase that phosphorylates RNA polymerase II. Proc. Nat. Acad. Sci. USA 89, 11920-11924.
10. Félix, M.-A., Clarke, P. R., Coleman, J., Verde, F. and Karsenti, E. (1993). Xenopus egg extracts as a system to study mitosis. In The Cell Cycle: A Practical Approach (ed. P. Fantes and R. Brooks), pp. 253-283. IRL Press, Oxford.
11. Fernandes-Alnemri, T., Litwack, G. and Alnemri, E. S. (1994) CPP32, a novel human apoptotic protein with homology to Caenorhabditis elegans cell death protein Ced-3 and mammalian interleukin-1β-converting enzyme. J. Biol. Chem. 269, 30761-30764.
12. Finnie, N. J., Gottlieb, T. M., Blunt, T., Jeggo, P. A. and Jackson, S. P. (1995). DNA-dependent protein kinase activity is absent in xrs-6 cells: implications for site-specific recombination and DNA double-strand break repair. Proc. Nat. Acad. Sci. USA 92, 320-324.
13. Genersch, E., Eckerskorn, C., Lottspeich, F., Herzog, C., Kuhn, K. and Poschl, E. (1995). Purification of the sequence-specific transcription factor CTCBF, involved in the control of human collagen IV genes: subunits with homology to Ku antigen. EMBO J. 14, 791-800.
14. Giffin, W., Torrance, H., Rodda, D. J., Préfontaine, G. G., Pope, L. and Haché, R. J. G. (1996). Sequence-specific DNA binding by Ku autoantigen and its effects on transcription. Nature 380, 265-268.
15. Gottlieb, T. M. and Jackson, S. P. (1993). The DNA-dependent protein kinase: requirement for DNA ends and association with Ku antigen. Cell 72, 131-42.
16. Greenwell, P. W., Kronmal, S. L., Porter, S. E., Gassenhuber, J., Obermaier, B. and Petes, T. D. (1995). TEL1, a gene involved in controlling telomere length in S. cerevisiae, is homologous to the human ataxia telangiectasia gene. Cell 82, 823-829.
17. Griffith, A. J., Blier, P. R., Mimori, T. and Hardin, J. A. (1992) Ku polypeptides synthesised in vitro assemble into complexes which recognise ends of double-stranded DNA. J. Biol. Chem. 267, 331-338.
18. Hari, K. L., Santerre, A., Sekelsky, J. J., McKim, K. S., Boyd, J. B. and Hawley, R. S. (1995). The mei-41 gene of D. melanogaster is a structural and functional homolog of the human ataxia telangiectasia gene. Cell 82, 815-821.
19. Hartley, K. O., Cell, D., Smith, G. C. M., Zhang, H., Divecha, N., Connely, M. A., Admon, A., Lees-Miller, S. P., Anderson, C. W. and Jackson, S. P. (1995). DNA-dependent protein kinase catalytic subunit: a relative of phosphatidylinositol 3-kinase and the ataxia telangiectasia gene product. Cell 82, 849-856.
20. Higashiura, M., Takasuga, Y., Vamashita, J. and Yagura, T. (1993). A protein homologous to human p70-protein is required for reconstitution of Xenopus sperm pronuclei. Chromosome Res. 1, 27-36.
21. Jackson, S. P. (1995). Ataxia-telangiectasia at the crossroads. Curr. Biol. 5, 1210-1212.
22. Jackson, S. P. (1996). The recognition of DNA damage. Curr. Opin. Genet. Dev. 6, 19-25.
23. Kato, R. and Ogawa, H. (1994). An essential gene, ESR1, is required for mitotic cell growth, DNA repair and meiotic recombination in Saccharomyces cerevisiae. Nucl. Acids Res. 22, 3104-3112.
24. Kaufmann, S. H., Desnoyers, S., Ottaviano, Y., Davidson, N. E. and Poirier, G. G. (1993). Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res. 53, 3976-3985.
25. Keith, C. T. and Schreiber, S. L. (1995). PIK-related kinases: DNA repair, recombination and cell cycle checkpoints. Science 270, 50-51.
26. Kuhn, A., Gottlieb, T. M., Jackson, S. P. and Grummt, I. (1995) DNA-dependent protein kinase: a potent inhibitor of transcription by RNA polymerase I. Genes Dev. 9, 193-203.
27. Kumar, S. (1995). ICE-like proteases in apoptosis. Trends Biochem. Sci. 20, 198-202.
28. Lazebnik, Y. A., Kaufmann, S. H., Desnoyers, S., Poirier, G. G. and Earnshaw, W. C. (1994). Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 371, 346-347.
29. Le Romancer, M., Reyl, D. F., Cherifi, Y., Pigeon, C., Bottari, S., Meyer, O. and Lewin, M. J. (1994). The 86-kDa subunit of autoantigen Ku is a somatostatin receptor regulating protein phosphatase-2A activity. J. Biol. Chem. 269, 17464-17468.
30. Lees-Miller, S. P., Sakaguchi, K., Ullrich, S. J., Appella, E. and Anderson, C. W. (1992). Human DNA-activated protein kinase phosphorylates serines 15 and 37 in the amino-terminal transactivation domain of human p53. Mol. Cell. Biol. 12, 5041-5049.
31. Lees-Miller, S. P., Godbout, R., Chan, D. W., Weinfeld, M., Day, R. R., Barron, G. M. and Allalunis-Turner, J. (1995). Absence of p350 subunit of DNA-activated protein kinase from a radiosensitive human cell line. Science 267, 1183-1185.
32. Martin, S. J. and Green, D. R. (1995). Protease activation during apoptosis: death by a thousand cuts? Cell 82, 349-352.
33. Mimori, T. and Hardin, J. A. (1986). Mechanism of interaction between Ku protein and DNA. J. Biol. Chem. 261, 10375-10379.
34. Molinete, M., Vermeulen, W., Burkle, A., Menissier-de Murcia, J., Kupper, J. H., Hoeijmakers, J. H. and de Murcia, G. (1993) Overproduction of the poly(ADP-ribose) polymerase DNA-binding domain blocks alkylation-induced DNA repair synthesis in mammalian cells. EMBO J. 12, 2109-2117.
35. Morrow, D. M., Tagle, D. A., Shiloh, Y., Collins, F. S. and Heiter, P. (1995) HATI/TELI, an S. cerevisiae homologue of the human gene mutated in ataxia-telangiectasia, is functionally related to the yeast checkpoint gene MECI. Cell 82, 831-840.
36. Newmeyer, D. D., Farschon, D. M. and Reed, J. C. (1994). Cell-free apoptosis in Xenopus egg extracts: inhibition by Bcl-2 and requirement for an organelle fraction enriched in mitochondria. Cell 79, 353-364.
37. Nicholson, D. W., Ali, A., Thornberry, N. A., Vaillancourt, J. P., Ding, C. K., Gallant, M., Gareau, Y., Griffin, P. R., Labelle, M., Lazebnik, Y. A. et al. (1995). Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376, 37-43.
38. Paillard, S. and Strauss, F. (1991). Analysis of the mechanism of interaction of simian Ku protein with DNA. Nucl. Acids. Res. 19, 5619-5624.
39. Paulovich, A. G. and Hartwell, L. H. (1995). A checkpoint regulates the rate of progression through S phase in S. cerevisiae in response to DNA damage. Cell 82, 841-847.
40. Peterson, S. R., Kurimasa, A., Oshimura, M., Dynan, W. S., Bradbury, E. M. and Chen, D. J. (1995). Loss of the catalytic subunit of the DNA-dependent protein kinase in DNA double-strand-break-repair mutant mammalian cells. Proc. Nat. Acati. Sci. USA 92, 3171-3174.
41. Rathmell, W. K. and Chu, G. (1994). Involvement of the Ku autoantigen in the cellular response to DNA double-strand breaks. Proc. Nat. Acad. Sci. USA 91, 7623-7627.
42. Reeves, W. H. (1992). Antibodies to the p70/p80 (Ku) antigens in systemiclupus erythematosus. Rheumatic. Dis. Clin. North. Am. 18, 391-414.
43. Savitsky, K., Bar-Shira, A., Gilad, S., Rotman, G., Ziv, Y., Vanagaite, L., Tagle, D. A., Smith, S., Uziel, T., Sfez, S. et al. (1995). A single ataxia telangiectasia gene with a product similar to PI 3-kinase. Science 268, 1749-1753.
44. Seaton, B. L., Yucel, J., Sunnerhagen, P. and Subramani, S. (1992). Isolation and charaterization of the Schizosaccharomyces pombe rad3 gene involved in the DNA damage and DNA synthesis checkpoints. Gene 119, 83-89.
45. Smider, V., Rathmell, W. K., Lieber, M. R. and Chu, G. (1994). Restoration of X-ray resistance and V(D)J recombination in mutant cells by Ku cDNA. Science 266, 288-291.
46. Song, Q., Lees-Miller, S. P., Kumar, S., Zhang, N., Chan, D. W., Smith, G. C. M., Jackson, S. P., Alnemri, E. S., Litwack, G. and Lavin, M. F. (1996). DNA-dependent protein kinase catalytic subunit: a target for an ICE-like protease in apoptosis. EMBO J. 15, 3238-3246.
47. Taccioli, G. E., Gottlieb, T. M., Blunt, T., Priestley, A., Demengeot, J., Mizuta, R., Lehmann, A. R., Alt, F. W., Jackson, S. P. and Jeggo, P. A. (1994). Ku80: product of the XRCC5 gene and its role in DNA repair and V(D)J recombination. Science 265, 1442-1445.
48. Walker, A. I., Hunt, T., Jackson, R. J. and Anderson, C. W. (1985). Double-stranded DNA induces the phosphorylation of several proteins including the 90 000 mol. wt. heat-shock protein in animal cell extracts. EMBO J. 4, 139-145.
49. Yuan, J., Shaham, S., Ledoux, S., Ellis, H. M. and Horvitz, H. R. (1993). The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell 75, 641-652.
50. Zhang, W,-W. and Yaneva, M. (1992). On the mechanisms of Ku protein protein binding to DNA. Biochem. Biophys. Res. Commun. 186, 574-579.