DNA-dependent protein kinase catalytic subunit: A target for an ICE-like protease in apoptosis

EMBO Journal

Volumn 15, Issue 13, 1996, Pages 3238-3246

  Song, Qizhong ^a   Lees Miller, Susan P ^b   Kumar, Sharad ^c   Zhang, Ning ^a   Chan, Doug W ^b   Smith, Graeme C M ^d   Jackson, Stephen P ^d   Alnemri, Emad S ^e   Litwack, Gerald ^e   Khanna, Kum Kum ^a   Lavin, Martin F ^a,f  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b UNIVERSITY OF CALGARY   (Canada)

^c HANSON INSTITUTE   (Australia)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e THOMAS JEFFERSON UNIVERSITY   (United States)

^f UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Apoptosis; DNA dependent protein kinase; Etoposide; ICE like protease; Substrate

Indexed keywords

CYSTEINE PROTEINASE; DNA; DNA BINDING PROTEIN; INTERLEUKIN 1BETA CONVERTING ENZYME; PROTEIN KINASE; PROTEINASE; PROTEINASE INHIBITOR;

AMINO ACID SEQUENCE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME DEGRADATION; ENZYME INACTIVATION; ENZYME STRUCTURE; HUMAN; HUMAN CELL; PRIORITY JOURNAL;

EID: 8944241298     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00688.x     Document Type: Article

References (65)

1. Allalunis-Turner, J.M., Lintott, L.G., Barron, G.M., Day, R.S. and Lees-Miller, S.P. (1995) Lack of correlation between DNA-dependent protein kinase activity and tumor cell radiosensitivity. Cancer Res., 55, 5200-5202.
2. Blunt, T. 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.
3. Boubnov, N.V. et al. (1995) Complementation of the ionizing radiation sensitivity, DNA end binding, and V(D)J recombination defects of double strand break repair mutants by p86 Ku autoantigen. Proc. Natl Acad. Sci. USA, 92, 890-894.
4. Brancolini, C., Benedetti, M. and Schneider, C. (1995) Microfilament reorganization during apoptosis: the role of Gas2, a possible substrate for ICE-like proteases. EMBO J., 14, 5179-5190.
5. Carter, T., Vancurova, I., Sun, I., Lou, W. and DeLeon, S. (1990) A DNA-activated protein kinase from HeLa cell nuclei. Mol. Cell Biol., 10, 6460-6471.
6. Casciola-Rosen, L.A., Miller, D.K., Anhalt, G.J. and Rosen, A. (1994) Specific cleavage of the 70 kDa protein component on the U1 small nuclear ribonucleoprotein is a characteristic biochemical feature of apoptotic cell death. J. Biol. Chem., 269, 30757-30760.
7. Chan, D.W., Mody, C.H., Ting, N.S.Y. and Lees-Miller, S.P. (1996) Purification and characterization of the DNA-activated protein kinase DNA-PK from human placenta. Biochem. Cell. Biol., 74, 67-73.
8. de Murcia, G. and de Murcia, J.M. (1994) Poly(ADP-ribose) polymerase: a molecular nick-sensor. Trends Biochem. Sci., 19, 172-176.
9. Dvir, A., Peterson, S.R., Knuth, M., Lu, H. and Williams, S.D. (1992) Ku autoantigen is the regulatory component of a template-associated protein kinase that phosphorylates RNA polymerase II. Proc. Natl. Acad. Sci. USA. 89, 11920-11924.
10. Ellis, H. and Horvitz, H.R. (1986) Genetic control of programmed cell death in the nematode C. elegans. Cell, 44, 817-829.
11. Ellis, R.E., Yuan, J. and Horwitz, H.R. (1991) Mechanisms and functions of cell death. Annu. Rev. Cell Biol., 7, 663-698.
12. Emoto, Y. et al. (1995) Proteolytic activation of protein kinase C5 by an ICE-like protease in apoptotic cells. EMBO J., 14, 6148-6156.
13. Faucheu, C. et al. (1995) A novel human protease similar to the interleukin-1β converting enzyme induces apoptosis in transfected cells. EMBO J., 14, 1914-1922.
14. 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-1-β-converting enzyme. J. Biol. Chem., 269, 30761-30764.
15. Fernandes-Alnemri, T., Litwack, G. and Alnemri, E.S. (1995a) Mch2, a new member of apoptotic Ced-3/Ice cysteine protease gene family. Cancer Res., 55, 2737-2742.
16. Fernandes-Alnemri, T. et al. (1995b) Mch3, a novel human apoptotic cysteine protease highly related to CPP32. Cancer Res., 55, 6045-6052.
17. Filippovich, I., Sorokina, N., Khanna, K.K. and Lavin, M.F. (1994) Butyrate induced apoptosis in lymphoid cells preceded by transient over-expression of hsp70 mRNA. Biochem. Biophys. Res. Commun., 198, 257-265.
18. Gottlieb, T.M. and Jackson, S.P. (1993) The DNA-dependent protein kinase: requirement for DNA ends and association with Ku antigen. Cell, 72, 131-142.
19. Gu, Y., Sarnecki, C., Aldape, R.A., Livingston, D.J. and Su, M.S.-S. (1995) Cleavage of poly (ADP-ribose) polymerase by interleukin-1β converting enzyme and its homologs TX and NEDD2. J. Biol Chem., 270, 18715-18718.
20. Hari, K.L. Santerre, A., Sekelsky, J.J., McKim, K.S., Boyd, J.B. and Hawley, R.S. (1995) The mei-41 gene of Drosophila melanogaster is a strucural and functional homolog of the human ataxia-telangiectasia gene. Cell, 82, 815-821.
21. Hartley, K.O. et al. (1995) DNA-dependent protein kinase catalytic subunit: a relative of phosphatidylinositol 3-kinase and the ataxia-telangiectasia gene product. Cell, 82, 849-856.
22. Hengartner, M.O., Ellis, R.E. and Horvitz, H.R. (1992) Caenorhabditis elegans gene ced-9 protects cells from programmed cell death. Nature, 356, 494-499.
23. Jackson, S.P. (1995) Ataxia-telangiectasia at the crossroads. Curr. Biol., 5, 1210-1212.
24. Kaufmann, S.H. (1989) Induction of endonucleolytic DNA cleavage in human acute myelogenous leukemia cells by etoposide, camptothesin, and other cytotoxic anticancer drugs: a cautionary note. Cancer Res., 49, 5870-5878.
25. Kaufmann, S.H., Desnoyers, S., Ohaviano, 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.
26. Kerr, J.F.R., Wyllie, A.H. and Currie, A.R. (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer, 26, 239-257.
27. Kirchgessner, C., Patil, C.K., Evans, J.W., Cuomo, C.A., Fried, L.M., Carter, T., Oettinger, M.A. and Brown, J.M. (1995) DNA-dependent kinase (p350) as a candidate gene for murine scid defect. Science, 267, 1178-1183.
28. Kumar, S. (1995a) ICE-like proteases in apoptosis. Trends Biochem. Sci., 20, 198-202.
29. Kumar, S. (1995b) Inhibition of apoptosis by the expression of antisense Nedd2. FEBS Lett., 368, 69-72.
30. Kumar, S. and Harvey, N.L. (1995) Role of multiple cellular proteases in the execution of programmed cell death. FEBS Lett., 375, 169-173.
31. Kumar, S. and Lavin, M.F. (1996) The ICE family of cysteine proteases as effectors of cell death. Cell Death Different., in press.
32. Kumar, S., Kinoshita, M., Noda, M., Copeland, N.G. and Jenkins, N.A. (1994) Induction of apoptosis by the mouse Nedd2 gene, which encodes a protein similar to the product of the Caenorhabditis elegans cell death gene ced-3 and the mammalian IL-1β-converting enzyme. Genes Dev., 8, 1613-1626.
33. Kumar, S., White, D.L., Takai, S., Turczynowicz, S., Juttner, C.A. and Hughes, T.P. (1995) Apoptosis regulatory gene NEDD2 maps to human chromosome segment 7q34-35, a region frequently affected in haematological neoplasms. Hum. Genet., 95, 641-644.
34. Lavin, M.F., Khanna, K.K., Beamish, H., Spring, K., Watters, D. and Shiloh, Y. (1995) Relationship of the ataxia-telangiectasia protein ATM to phosphoinositide 3-kinase. Trends Biochem. Sci., 20, 382-383.
35. Lazebnik, Y.A., Kaufmann, S.H., Desmoyners, 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.
36. Lazebnik, Y.A., Takahashi, A., Moir, R.D., Goldman, R.D., Poirier, G.G., Kaufmann, S.H. and Earnshaw, W.C. (1995) Studies of the lamin proteinase reveal multiple parallel biochemical pathways during apoptotic execution. Proc. Natl Acad. Sci. USA, 92, 9042-9046.
37. Lees-Miller, S.P., Godbout, R., Chan, D.W., Weinfeld, M., Day, R.S. III, Barron, G.M. and Turner, J.A. (1995) Absence of p350 subunit of DNA-activated protein kinase from a radiosensitive human cell line. Science, 267, 1183-1185.
38. Martin, S.J. and Green, D.R. (1995) Protease activation during apoptosis: death by a thousand cuts. Cell, 82, 349-352.
39. Martin, S.J., O'Brien, G.A., Nishioka, W.K., McGahon, A.J., Mahboubi, A., Saido, T.C. and Green, D.R. (1995) Proteolysis of fodrin (non-erythroid spectrin) during apoptosis. J. Biol. Chem., 270, 6425-6428.
40. Mashima, T., Naito, M., Fujita, N., Noguchi, K. and Tsuruo, T. (1995) Identification of actin as a substrate of ICE and an ICE-like protease and involvement fo ICE-like protease but not ICE in VP-16-induced U937 apoptosis. Biochem. Biophys. Res. Commun., 217, 1185-1192.
41. Miller, S.A., Dykes, D.D. and Polesky, H.F. (1988) A simple salting out procedure for extracting DNA from human nucleated cell. Nucleic Adds Res., 16, 1215.
42. relIII, members of the ICE/CED-3 family of cysteine proteases. J. Biol. Chem., 270, 15870-15876.
43. Neamati, N., Fernandez, A., Wright, S., Kiefer, J. and McConkey, D.J. (1995) Degradation of lamin B1 precedes oligonucleosomal DNA fragmentation in apoptotic thymocytes and isolated thymocyte nuclei. J. Immunol., 154, 3788-3795.
44. Nicholson, D.W. et al. (1995) Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature, 376, 37-43.
45. Peitsch, M.C., Potzar, B., Stephan, H., Crompton, T., MacDonald, H.R., Mannherz, H.G. and Tschopp, J. (1993) Characterization of the endogenous deoxyribonuclease involved in nuclear DNA degradation during apoptosis (programmed cell death). EMBO J., 12, 371-377.
46. Peterson, S.R., Kurimasa, A., Oshimura, M., Dynan, W.S., Bradbury, E.M. and Chen, D. (1995) Loss of the catalytic subunit of the DNA-dependent protein kinase in DNA double-strand break repair mutant mammalian cells. Proc. Natl Acad. Sci. USA, 92, 3171-3174.
47. Savitsky, K. et al. (1995) A single ataxia-telangiectasia gene with a product similar to PI-3 kinase. Science, 268, 1749-1793.
48. Schwartzmann, R.A. and Cidlowski, J.A. (1993) Apoptosis: the biochemistry and molecular biology of programmed cell death. Endocrinol. Rev., 14, 133-151.
49. Sedgwick, R.P. and Boder, E. (1991) Ataxia-telangiectasia (208900; 208910; 208920). In de Jong, J.M.B.V. (ed.), Hereditary Neuropathies and Spinocerebellar Atrophies. Elsevier Science Publishers, Amsterdam, pp. 347-423.
50. Steller, H. (1995) Mechanism and genes of cellular suicide. Science, 267, 1445-1449.
51. Strasser, A. (1995) Life and death during lymphocyte development and function: evidence for two distinct killing mechanisms. Curr. Opin. Immunol., 7, 228-234.
52. Taccioli, G.E. et al. (1994) Ku 80: product of the XRCC5 gene and its role in DNA repair and V(D)J recombination. Science, 265, 1442-1445.
53. Teh, B.S., Chen, P., Lavin, M.F., Seow, W.K. and Thong, Y.H. (1991) Demonstration of the induction of apoptosis (programmed cell death) by tetrandrine, a novel anti-inflammatory agent. Int. J. Immunopharmacol., 13, 1117-1126.
54. Tewari, M., Quan, L.T., O'Rourke, K., Desnoyers, S., Zeng, Z., Beidler, D.R., Poirier, G.G., Salvesen, G.S. and Dixit, V.M. (1995a) Yama/CPP32β, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-Ribose) polymerase. Cell, 81, 801-809.
55. Tewari, M., Beidler, D.R. and Dixit, V.M. (1995b) CrmA-inhibitable cleavage of the 70 kDa protein component of the U1 small nuclear ribonucleoprotein during fas- and tumor necrosis factor-induced apoptosis. J. Biol. Chem., 270, 18738-18741.
56. Thornberry, N.A., Peterson, E.P., Zhao, J.J., Howard, A.D., Griffin, P.R. and Chapman, K.T. (1994) Inactivation of interleukin-1β converting enzyme by peptide (acyloxy)methyl ketones. Biochemistry, 33, 3934-3940.
57. Vaux, D.L. (1993) Towards an understanding of the molecular mechanisms of physiological cell death. Proc. Natl Acad. Sci. USA, 90, 786-789.
58. Vaux, D.L., Haecker, G. and Strasser, A. (1994) An evolutionary perspective on apoptosis. Cell, 76, 777-779.
59. Voelkel-Johnson, C., Entingh, A.J., Wold, W.S.M., Golding, L.-R. and Laster, S.M. (1995) Activation of intracellular protease is an early event in TNF-induced apoptosis. J. Immunol., 154, 1707-1716.
60. Wang, L., Miura, M., Bergeron, L., Zhu, H. and Yuan, J. (1994) IcH-1, an Ice/ced-3-related gene, encodes both positive and negative regulators of programmed cell death. Cell, 78, 739-750.
61. Wang, Z.-Q., Auer, B., Sting, L., Berghammer, H., Haidacher, D., Schweigher, H. and Wagner, E.F. (1995) Mice lacking ADPRT and poly(ADP-ribosyl)ation develop normally but are susceptible to skin disease. Genes Dev., 9, 509-520.
62. White, E. (1996) Life, death and the pursuit of apoptosis. Genes Dev., 10, 1-15.
63. Wyllie, A.H., Kerr, J.F.R. and Currie, A.R. (1980) Cell death: the significance of apoptosis. Int. Rev. Cytol., 68, 251-306.
64. Yaneva, M. and Busch, H. (1986) A 10S particle released from deoxyribonuclease sensitive region of HeLa cell nuclei contains the 86-kilodalton-70-kilodalton protein complex. Biochemistry, 25, 5057-5063.
65. Yuan, J., Shaham, S., Ledoux, S., Ellis, H. and Horvitz, H.R. (1993) The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1β-converting enzyme. Cell, 75, 641-652.