Inactivation of DNA-Dependent Protein Kinase by Protein Kinase Cδ: Implications for Apoptosis

REFERENCES

• Alnemri, E. S., D. J. Livingston, D. W. Nicholson, G. Salvesen, N. A. Thornberry, W. W. Wong, and J. Yuan 1996. Human ICE/CED-3 protease nomenclature. Cell 87: 171.
   PubMed Web of Science ®Google Scholar
• Anderson, C. W., and S. P. Lees-Miller 1992. The nuclear serine/threonine protein kinase DNA-PK. Crit. Rev. Eukaryotic Gene Expression 2: 283–314.
   PubMedGoogle Scholar
• Armstrong, R. C., T. Aja, J. Xiang, S. Gaur, J. F. Krebs, K. Hoang, X. Bai, S. J. Korsmeyer, D. S. Karanewsky, L. C. Fritz, and K. J. Tomaselli 1996. Fas-induced activation of the cell death-related protease CPP32 is inhibited by Bcl-2 and by ICE family protease inhibitors. J. Biol. Chem. 271: 16850–16855.
   PubMed Web of Science ®Google Scholar
• Beyaert, R., V. J. Kidd, S. Cornelis, M. Van de Craen, G. Denecker, J. M. Lahti, R. Gururajan, P. Vandenabeele, and W. Fiers 1997. Cleavage of PITSLRE kinases by ICE/CASP-1 and CPP32/CASP-3 during apoptosis induced by tumor necrosis factor. J. Biol. Chem. 272: 11694–11697.
   PubMedGoogle Scholar
• Boubnov, N. V., and D. T. Weaver 1995. Scid cells are deficient in Ku and replication protein A phosphorylation by the DNA-dependent protein kinase. Mol. Cell. Biol. 15: 5700–5706.
   PubMedGoogle Scholar
• Bump, N. J., M. Hackett, M. Hugunin, S. Seshagiri, K. Brady, P. Chen, C. Ferenz, S. Franklin, T. Ghayur, P. Li, P. Licari, J. Mankovich, L. Shi, A. H. Greenberg, L. K. Miller, and W. W. Wong 1995. Inhibition of ICE family proteases by baculovirus antiapoptotic protein p35. Science 269: 1885–1888.
   PubMed Web of Science ®Google Scholar
• Casciola-Rosen, L., D. W. Nicholson, T. Chong, K. R. Rowan, N. A. Thornberry, D. K. Miller, and A. Rosen 1996. Apopain/CPP32 cleaves proteins that are essential for cellular repair: a fundamental principle of apoptotic death. J. Exp. Med. 183: 1957–1964.
   PubMed Web of Science ®Google Scholar
• Chan, D. W., and S. P. Lees-Miller 1996. The DNA-dependent protein kinase is inactivated by autophosphorylation of the catalytic subunit. J. Biol. Chem. 271: 8936–8941.
   PubMed Web of Science ®Google Scholar
• Chu, G. 1997. Double strand break repair. J. Biol. Chem. 272: 24097–24100.
   PubMed Web of Science ®Google Scholar
• Datta, R., H. Kojima, D. Banach, N. J. Bump, R. V. Talanian, E. S. Alnemri, R. R. Weichselbaum, W. W. Wong, and D. W. Kufe 1997. Activation of a CrmA-insensitive, p35-sensitive, pathway in ionizing radiation-induced apoptosis. J. Biol. Chem. 272: 1965–1969.
   PubMed Web of Science ®Google Scholar
• Denning, M. F., A. A. Dlugosz, D. W. Threadgill, T. Magnuson, and S. H. Yuspa 1996. Activation of the epidermal growth factor receptor signal transduction pathway stimulates tyrosine phosphorylation of protein kinase C δ. J. Biol. Chem. 271: 5325–5331.
   PubMedGoogle Scholar
• Duan, H., K. Orth, A. M. Chinnaiyan, G. G. Poirier, C. J. Froelich, W.-W. He, and V. M. Dixit 1996. ICE-LAP6, a novel member of the ICE/Ced-3 gene family, is activated by the cytotoxic T cell protease granzyme B. J. Biol. Chem. 271: 16720–16724.
   PubMed Web of Science ®Google Scholar
• Emoto, Y., H. Kisaki, Y. Manome, S. Kharbanda, and D. Kufe 1996. Activation of protein kinase C δ in human myeloid leukemia cells treated with 1-β-d-arabinofuranosylcytosine. Blood 87: 1990–1996.
   PubMed Web of Science ®Google Scholar
• Emoto, Y., G. Manome, G. Meinhardt, H. Kisaki, S. Kharbanda, M. Robertson, T. Ghayur, W. W. Wong, R. Kamen, R. Weichselbaum, and D. Kufe 1995. Proteolytic activation of protein kinase Cδ by an ICE-like protease in apoptotic cells. EMBO J. 14: 6148–6156.
   PubMed Web of Science ®Google Scholar
• Enari, M., H. Hug, and S. Nagata 1995. Involvement of an ICE-like protease in Fas-mediated apoptosis. Nature 375: 78–81.
   PubMed Web of Science ®Google Scholar
• Fukumoto, S., Y. Nishizawa, M. Hosoi, H. Koyama, K. Yamakawa, S. Ohno, and H. Morii 1997. Protein kinase C delta inhibits the proliferation of vascular smooth muscle cells by suppressing G1 cyclin expression. J. Biol. Chem. 272: 13816–13822.
   PubMed Web of Science ®Google Scholar
• Ghayur, T., M. Hugunin, R. V. Talanian, S. Ratnofsky, C. Quinlan, Y. Emoto, P. Pandey, R. Datta, S. Kharbanda, H. Allen, R. Kamen, W. Wong, and D. Kufe 1996. Proteolytic activation of protein kinase C δ by an ICE/CED 3-like protease induces characteristics of apoptosis. J. Exp. Med. 184: 2399–2404.
   PubMed Web of Science ®Google Scholar
• Hammarsten, O., and G. Chu 1998. DNA-dependent protein kinase: DNA binding and activation in the absence of Ku. Proc. Natl. Acad. Sci. USA 95: 525–530.
   PubMed Web of Science ®Google Scholar
• Han, Z., N. Malik, T. Carter, W. H. Reeves, J. H. Wyche, and E. A. Hendrickson 1996. DNA-dependent protein kinase is a target for a CPP32-like apoptotic protease. J. Biol. Chem. 271: 25035–25040.
   PubMed Web of Science ®Google Scholar
• Hartley, K. O., D. Gell, G. C. M. 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.
   PubMed Web of Science ®Google Scholar
• Horvitz, H. R., S. Shaham, and M. O. Hengartner 1994. The genetics of programmed cell death in the nematode Caenorhabditis elegans. Cold Spring Harbor Symp. Quant. Biol. 59: 377–385.
   PubMedGoogle Scholar
• Jackson, S. P., and P. A. Jeggo 1995. DNA double-strand break repair, V(D)J recombination: involvement of DNA-PK. Trends Biochem. Sci. 20: 412–415.
   PubMed Web of Science ®Google Scholar
• Jacobson, M. D., M. Weil, and M. C. Raff 1997. Programmed cell death in animal development. Cell 88: 347–354.
   PubMed Web of Science ®Google Scholar
• Jin, S., S. Kharbanda, B. Mayer, D. Kufe, and D. T. Weaver 1997. Binding of Ku and c-Abl at the kinase homology region of DNA-dependent protein kinase catalytic subunit. J. Biol. Chem. 272: 24763–24766.
   PubMed Web of Science ®Google Scholar
• Kaufmann, S. H., S. Desnoyers, Y. Ottaviano, N. E. Davidson, and G. G. Poirier 1993. Specific proteolytic cleavage of poly(ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res. 53: 3976–3985.
   PubMed Web of Science ®Google Scholar
• Kerr, J. F. R., A. H. Wyllie, and A. R. Currie 1972. Apoptosis: a basic biological phenomenon with wide-ranging implication in tissue kinetics. Br. J. Cancer 26: 239–257.
   PubMed Web of Science ®Google Scholar
• Kharbanda, S., P. Pandey, S. Jin, S. Inoue, A. Bharti, Z.-M. Yuan, R. Weichselbaum, D. Weaver, and D. Kufe 1997. Functional interaction of DNA-PK and c-Abl in response to DNA damage. Nature 386: 732–735.
   PubMed Web of Science ®Google Scholar
• Kharbanda, S., P. Pandey, L. Schofield, R. Roncinske, S. Israel, A. Bharti, Z.-M. Yuan, R. Weichselbaum, S. Saxena, C. Nalin, and D. Kufe 1997. Role for Bcl-xL as an inhibitor of cytosolic cytochrome C accumulation in apoptosis. Proc. Natl. Acad. Sci. USA 94: 6939–6942.
   PubMed Web of Science ®Google Scholar
• Kikkawa, U., A. Kishimoto, and Y. Nishizuka 1989. The protein kinase C family: heterogeneity and its implications. Annu. Rev. Biochem. 58: 31–44.
   PubMed Web of Science ®Google Scholar
• Kirchgessner, C. U., C. K. Patil, J. W. Evans, C. A. Cuomo, L. M. Fried, T. Carter, M. A. Oettinger, and J. M. Brown 1995. DNA-dependent kinase (p350) as a candidate gene for the murine SCID defect. Science 267: 1178–1183.
   PubMed Web of Science ®Google Scholar
• Kluck, R. M., E. Bossy-Wetzel, D. R. Green, and D. D. Newmeyer 1997. The release of cytochrome c from mitochondria: a primary site for Bcl-2 regulation of apoptosis. Science 275: 1132–1136.
   PubMed Web of Science ®Google Scholar
• Lazebnik, Y. A., S. Cole, C. A. Cooke, W. G. Nelson, and W. C. Earnshaw 1993. Nuclear events of apoptosis in vitro in cell-free mitotic extracts: a model system for analysis of the active phase of apoptosis. J. Cell Biol. 123: 7–22.
   PubMed Web of Science ®Google Scholar
• Lees-Miller, S. P., Y. Chen, and C. W. Anderson 1990. Human cells contain a DNA-activated protein kinase that phosphorylates simian virus 40 T antigen, mouse p53 and the human Ku autoantigen. Mol. Cell. Biol. 10: 6472–6481.
   PubMed Web of Science ®Google Scholar
• Lees-Miller, S. P., R. Godbout, D. W. Chan, M. Weinfeld, R. S. I. Day, G. M. Barron, and J. Allalunis-Turner 1995. Absence of p350 subunit of DNA-activated protein kinase from a radiosensitive human cell line. Science 267: 1183–1185.
   PubMed Web of Science ®Google Scholar
• 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 amino-terminal transactivation domain of human p53. Mol. Cell. Biol. 12: 5041–5049.
   PubMed Web of Science ®Google Scholar
• Li, P., D. Nijhawan, I. Budihardjo, S. M. Srinivasula, M. Ahmad, E. S. Alnemn, and X. Wang 1997. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91: 479–489.
   PubMed Web of Science ®Google Scholar
• Li, W., P. Michieli, M. Alimandi, M. V. Lorenzi, Y. Wu, L. H. Wang, M. A. Heidaran, and J. H. Pierce 1996. Expression of an ATP binding mutant of PKC-delta inhibits Sis-induced transformation of NIH3T3 cells. Oncogene 13: 731–737.
   PubMedGoogle Scholar
• Liu, X., H. Zou, C. Slaughter, and X. Wang 1997. DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell 89: 175–184.
   PubMed Web of Science ®Google Scholar
• Los, M., M. van de Craen, L. C. Penning, H. Schenk, M. Westendorp, P. A. Baeuerle, W. Droge, P. H. Krammer, W. Fiers, and K. Schulze-Osthoff 1995. Requirement of an ICE-CED-3 protease for Fas/APO-1-mediated apoptosis. Nature 375: 81–83.
   PubMed Web of Science ®Google Scholar
• Lu, Z., A. Hornia, Y.-W. Jiang, Q. Zang, S. Ohno, and D. A. Foster 1997. Tumor promotion by depleting cells of protein kinase Cδ. Mol. Cell. Biol. 17: 3418–3428.
   PubMed Web of Science ®Google Scholar
• Muzio, M., A. M. Chinnaiyan, F. C. Kischkel, K. O’Rourke, A. Shevchenko, J. Ni, C. Scaffidi, J. D. Bretz, M. Zhang, R. Gentz, M. Mann, P. H. Krammer, M. E. Peter, and V. M. Dixit 1996. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell 85: 817–827.
   PubMed Web of Science ®Google Scholar
• Nicholson, D. W. 1996. ICE/CED3-like proteases as therapeutic targets for the control of inappropriate apoptosis. Nat. Biotechnol. 14: 297–301.
   PubMedGoogle Scholar
• Nicholson, D. W., A. Ali, N. A. Thornberry, J. P. Vaillancourt, C. K. Ding, M. Gallant, Y. Gareau, P. R. Griffin, M. Labelle, Y. A. Lazebnik, N. A. Munday, S. M. Raju, M. E. Smulson, T.-T. Yamin, V. L. Yu, and D. K. Miller 1995. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376: 37–43.
   PubMed Web of Science ®Google Scholar
• Pai, J. T., M. S. Brown, and J. L. Goldstein 1996. Purification and cDNA cloning of a second apoptosis-related cysteine protease that cleaves and activates sterol regulatory element binding proteins. Proc. Natl. Acad. Sci. USA 93: 5437–5442.
   PubMedGoogle Scholar
• Pandey, P., J. Raingeaud, M. Kaneki, R. Weichselbaum, R. Davis, D. Kufe, and S. Kharbanda 1996. Activation of p38 MAP kinase by c-Abl-dependent and -independent mechanisms. J. Biol. Chem. 271: 23775–23779.
   PubMedGoogle Scholar
• Park, D. S., L. Stefanis, C. Y. I. Yan, S. E. Farinelli, and L. A. Greene 1996. Ordering the cell death pathway. J. Biol. Chem. 271: 21898–21905.
   PubMed Web of Science ®Google Scholar
• Pronk, G. J., K. Ramer, P. Amiri, and L. T. Williams 1996. Requirement of an ICE-like protease for induction of apoptosis and ceramide generation by REAPER. Science 271: 808–810.
   PubMed Web of Science ®Google Scholar
• Ray, C. A., R. A. Black, S. R. Kronheim, T. A. Greenstreet, P. R. Sleath, G. S. Salvesen, and D. J. Pickup 1992. Viral inhibition of inflammation: cowpox virus encodes an inhibitor of the interleukin-1β-converting enzyme. Cell 69: 597–604.
   PubMed Web of Science ®Google Scholar
• Rudel, T., and G. M. Bokoch 1997. Membrane and morphological changes in apoptotic cells regulated by caspase-mediated activation of PAK2. Science 276: 1571–1574.
   PubMed Web of Science ®Google Scholar
• Singleton, B. K., A. Priestley, H. Steingrimsdottir, D. Gell, T. Blunt, S. P. Jackson, A. R. Lehmann, and P. A. Jeggo 1997. Molecular and biochemical characterization of xrs mutants defective in Ku80. Mol. Cell. Biol. 17: 1264–1273.
   PubMed Web of Science ®Google Scholar
• Song, Q., S. P. Lees-Miller, S. Kumar, N. Zhang, D. W. Chan, G. C. M. Smith, S. P. Jackson, E. S. Alnemri, G. Litwack, K. K. Khanna, and M. F. Lavin 1996. DNA-dependent protein kinase catalytic subunit: a target for an ICE-like protease in apoptosis. EMBO J. 15: 3238–3246.
   PubMedGoogle Scholar
• Taccioli, G. E., H.-L. Cheng, A. J. Varghese, G. Whitmore, and F. W. Alt 1994. A DNA repair defect in Chinese hamster ovary cells affects V(D)J recombinant similarly to the murine Scid mutation. J. Biol. Chem. 269: 7439–7442.
   PubMedGoogle Scholar
• Tewari, M., and V. M. Dixit 1995. Fas- and tumor necrosis factor-induced apoptosis is inhibited by the poxvirus crmA gene product. J. Biol. Chem. 270: 3255–3260.
   PubMed Web of Science ®Google Scholar
• Watanabe, T., Y. Ono, Y. Taniyama, K. Hazama, K. Igarashi, K. Ogita, U. Kikkawa, and Y. Nishizuka 1992. Cell division arrest induced by phorbol ester in CHO cells overexpressing protein kinase C-δ subspecies. Proc. Natl. Acad. Sci. USA 89: 10159–10163.
   PubMed Web of Science ®Google Scholar
• Weaver, D. T. 1995. What to do at an end: DNA double-strand break repair. Trends Genet. 11: 388–392.
   PubMedGoogle Scholar
• Wissing, D., H. Mouritzen, M. Egeblad, G. G. Poirier, and M. Jaattela 1997. Involvement of caspase-dependent activation of cystolic phospholipase A2 in tumor necrosis factor-induced apoptosis. Proc. Natl. Acad. Sci. USA 94: 5073–5077.
   PubMed Web of Science ®Google Scholar
• Wyllie, A. H. 1984. Chromatin cleavage in apoptosis: association with condensed chromatin morphology and dependence on macromolecular synthesis. J. Pathol. 142: 66–77.
   Google Scholar
• Yang, J., X. Liu, K. Bhalla, C. Kaekyung Kim, A. M. Ibrado, J. Cai, T.-I. Peng, D. P. Jones, and X. Wang 1997. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275: 1129–1132.
   PubMed Web of Science ®Google Scholar
• Yuan, Z.-M., T. Utsugisawa, T. Ishiko, S. Nakada, Y. Huang, S. Kharbanda, R. Weichselbaum, and D. Kufe 1998. Activation of protein kinase C δ by the c-Abl tyrosine kinase in response to ionizing radiation. Oncogene 16: 1643–1648.
   PubMed Web of Science ®Google Scholar
• Zang, Q., Z. Lu, M. Curto, N. Barile, D. Shalloway, and D. A. Foster 1997. Association between v-Src and protein kinase C δ in v-Src-transformed fibroblasts. J. Biol. Chem. 272: 13275–13280.
   PubMedGoogle Scholar