Granzyme B directly and efficiently cleaves several downstream caspases substrates: Implications for CTL-induced apoptosis

Immunity

Volumn 8, Issue 4, 1998, Pages 451-460

  Andrade, Felipe ^a   Roy, Sophie ^b   Nicholson, Donald ^b   Thornberry, Nancy ^c   Rosen, Antony ^a   Casciola Rosen, Livia ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MERCK FROSST CENTRE FOR THERAPEUTIC RESEARCH   (Canada)

^c MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; CYSTEINE PROTEINASE; GRANZYME B; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL DEATH; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; HUMAN; HUMAN CELL; LYMPHOKINE ACTIVATED KILLER CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION;

EID: 0032055097     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-7613(00)80550-6     Document Type: Article

References (42)

1. Beidler, D.R., Tewari, M., Friesen, P.D., Poirier, G., and Dixit, V.M. (1995). The baculovirus p35 protein inhibits Fas-and tumor necrosis factor-induced apoptosis. J. Biol. Chem. 270, 16526-16528.
2. Bump, N.J., Hackett, M., Hugunin, M., Seshagiri, S., Brady, K., Chen, P., Ferenz, C., Franklin, S., Ghayur, T., Li, P., et al. (1995). Inhibition of ICE family proteases by baculovirus antiapoptotic protein p35. Science 269, 1885-1888.
3. Casciola-Rosen, L.A., Anhalt, G.J., and Rosen, A. (1994a). Autoantigens targeted in systemic lupus erythematosus are clustered in two populations of surf ace structures on apoptotic keratinocytes. J. Exp. Med. 179, 1317-1330.
4. Casciola-Rosen, L.A., Miller, D.K., Anhalt, G.J., and Rosen, A. (1994b). Specific cleavage of the 70-kDa protein component of the U1 small nuclear ribonucleoprotein is a characteristic biochemical feature of apoptotic cell death. J. Biol. Chem. 269, 30757-30760.
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. Casciola-Rosen, L.A., Nicholson, D.W., Chong, T., Rowan, K.R., Thornberry, N.A., Miller, D.K., and Rosen, A. (1996). Apopain/CPP32 cleaves proteins that are essential for cellular repair: a fundamental principle of apoptotic death. J. Exp. Med. 183, 1957-1964.
7. Casiano, C.A., Martin, S.J., Green, D.R., and Tan, E.M. (1996). Selective cleavage of nuclear autoantigens during CD95 (Fas/APO-1)-mediated T cell apoptosis. J. Exp. Med. 184, 765-770.
8. Darmon, A.J., Nicholson, D.W., and Bleackley, R.C. (1995). Activation of the apoptotic protease CPP32 by cytotoxic T-cell-derived granzyme B. Nature 377, 446-448.
9. Deveraux, Q.L., Takahashi, R., Salvesen, G.S., and Reed, J.C. (1997). X-linked IAP is a direct inhibitor of cell-death proteases. Nature 38, 300-304.
10. Froelich, C.J., Hanna, W.L., Poirier, G.G., Duriez, P.J., D'Amours, D., Salvesen, G.S., Alnemri, E.S., Earnshaw, W.C., and Shah, G.M. (1996a). Granzyme B perforin-mediated apoptosis of jurkat cells results in cleavage of poly(ADP-ribose) polymerase to the 89-kDa apoptotic fragment and less abundant 64-kDa fragment. Biochem. Biophys. Res. Commun. 227, 658-665.
11. Froelich, C.J., Orth, K., Turbov, J., Seth, P., Gottlieb, R., Babior, B., Shah, G.M., Bleackley, R.C., Dixit, V.M., and Hanna, W. (1996b). New paradigm for lymphocyte granule-mediated cytotoxicity: target cells bind and internalize granzyme B, but an endosomolytic agent is necessary for cytosolic delivery and subsequent apoptosis. J. Biol. Chem. 271, 29073-29079.
12. Greidinger, E.L., Miller, D.K., Yamin, T.-T., Casciola-Rosen, L., and Rosen, A. (1996). Sequential activation of three distinct ICE-like activities in Fas-ligated Jurkat cells. FEBS Lett. 390, 299-303.
13. Heusel, J.W., Wesselschmidt, R.L., Shresta, S., Russell, J.H., and Ley, T.J. (1994). Cytotoxic lymphocytes require granzyme B for the rapid induction of DNA fragmentation and apoptosis in allogeneic target cells. Cell 76, 977-987.
14. Irmler, M., Thome, M., Hahne, M., Schneider, P., Hofmann, B., Steiner, V., Bodmer, J.L., Schröter, M., Burns, K., Mattmann, C., et al. (1997). Inhibition of death receptor signals by cellular FLIP. Nature 388, 190-195.
15. Jacobson, M.D., Weil, M., and Raff, M.C. (1997). Programmed cell death in animal development. Cell 88, 347-354.
16. Jans, D.A., Jans, P., Briggs, L.J., Sutton, V., and Trapani, J.A. (1996). Nuclear transport of granzyme B (fragmentin 2). Dependence on perform in vivo and cytosolic factors in vitro. J. Biol. Chem. 271, 30781-30789.
17. Krajewska, M., Wang, H.G., Krajewski, S., Zapata, J.M., Shabaik, A., Gascoyne, R., and Reed, J.C. (1997). Immunohistochemical analysis of in vivo patterns of expression of CPP32 (Caspase-3), a cell death protease. Cancer Res. 57, 1605-1613.
18. Krajewski, S., Gascoyne, R.D., Zapata, J.M., Krajewska, M., Kitada, S., Chhanabhai, M., Horsman, D., Berean, K., Piro, L.D., Fugier-Vivier, I., et al. (1997). Immunolocalization of the ICE/Ced-3-family protease, CPP32 (Caspase-3), in non-Hodgkin's lymphomas, chronic lymphocytic leukemias, and reactive lymph nodes. Blood 89, 3817-3825.
19. Liu, X., Zou, H., Slaughter, C., and Wang, X. (1997). DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell 89, 175-184.
20. McGahon, A.J., Nishioka, W.K., Martin, S.J., Mahboubi, A., Cotter, T.G., and Green, D.R. (1995). Regulation of the Fas apoptotic cell death pathway by Abl. J. Biol. Chem. 270, 22625-22631.
21. Nicholson, D.W., and Thornberry, N.A. (1997). Caspases: killer proteases. Trends Biol. Sci. 22, 299-306.
22. 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.
23. Odake, S., Kam, C.M., Narasimhan, L., Poe, M., Blake, J.T., Krahenbuhl, O., Tschopp, J., and Powers, J.C. (1991). Human and murine cytotoxic T lymphocyte serine proteases: subsite mapping with peptide thioester substrates and inhibition of enzyme activity and cytolysis by isocoumarins. Biochemistry 30, 2217-2227.
24. Pinkoski, M.J., Winkler, U., Hudig, D., and Bleackley, R.C. (1996). Binding of granzyme B in the nucleus of target cells. Recognition of an 80 kDa protein. J. Biol. Chem. 271, 10225-10229.
25. Podack, E., and Konigsberg, P.J. (1984). Cytolytic T cell granules. Isolation, structural, biochemical and functional characterization. J. Exp. Med. 160, 695-710.
26. Poe, M., Blake, J.T., Boulton, D.A., Gammon, M., Sigal, N.H., Wu, J.K., and Zweerink, H.J. (1991). Human cytotoxic lymphocyte granzyme B: its purification from granules and the characterization of substrate and inhibitor specificity. J. Biol. Chem. 266, 98-103.
27. Salvesen, G.S., and Dixit, V.M. (1997). Caspases: intracellular signaling by proteases. Cell 91, 443-446.
28. Sarin, A., Williams, M.S., Alexander-Miller, M.A., Berzofsky, J.A., Zacharchuk, C.M., and Henkart, P.A. (1997). Target cell lysis by CTL granule exocytosis is independent of ICE/Ced-3 family proteases. Immunity 6, 209-215.
29. Shi, L., Kam, C.-M., Powers, J.C., Aebersold, R., and Greenberg, A.H. (1992). Purification of three cytotoxic lymphocyte granule serine proteases that induce apoptosis through distinct substrate and target cell interactions. J. Exp. Med. 176, 1521-1529.
30. Shi, L.F., Mai, S., Israel, S., Browne, K., Trapani, J.A., and Greenberg, A.H. (1997). Granzyme B (GraB) autonomously crosses the cell membrane and perform initiates apoptosis and GraB nuclear localization. J. Exp. Med. 185, 855-866.
31. Song, Q.Z., Burrows, S.R., Smith, G., Lees-Miller, S.P., Kumar, S., Chan, D.W., Trapani, J.A., Alnemri, E., Litwack, G., Lu, H., et al. (1996a). Interleukin-1b-converting enzyme-like protease cleaves DNA-dependent protein kinase in cytotoxic T cell killing. J. Exp. Med. 184, 619-626.
32. Song, Q.Z., Lees-Miller, S.P., Kumar, S., Zhang, N., Chan, D.W., Smith, G.C.M., Jackson, S.P., Alnemri, E.S., Litwack, G., Khanna, K.K., et al. (1996b). DNA-dependent protein kinase catalytic subunit: a target for an ICE-like protease in apoptosis. EMBO J. 15, 3238-3246.
33. Srinivasula, S.M., Ahmad, M., Ottilie, S., Bullrich, F., Banks, S., Wang, Y., Fernandes-Alnemri, T., Croce, C.M., Litwack, G., Tomaselli, K.J., et al. (1997). FLAME-1, a novel FADD-like anti-apoptotic molecule that regulates Fas/TNFR1-induced apoptosis. J. Biol. Chem. 272, 18542-18545.
34. Talanian, R.V., Yang, X., Turbov, J., Seth, P., Ghayur, T., Casiano, C.A., Orth, K., and Froelich, C.J. (1997). Granule-mediated killing: pathways for granzyme B-initiated apoptosis. J. Exp. Med. 186, 1323-1331.
35. Thome, M., Schneider, P., Hofmann, K., Fickenscher, H., Meinl, E., Neipel, F., Mattmann, C., Burns, K., Bodmer, J.L., Schröter, M., et al. (1997). Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 386, 517-521.
36. Thompson, C.B. (1995). Apoptosis in the pathogenesis and treatment of disease. Science 267, 1456-1462.
37. Thornberry, N.A., Ranon, T.A., Pieterson, E.P., Rasper, D.M., Timkey, T., Garcia-Calvo, M., Houtzager, V.M., Nordstrom, P.A., Roy, S., Vaillancourt, J.P., et al. (1997). A combinatorial approach defines specificities of members of the caspase family and granzyme B: functional, relationships established for key mediators of apoptosis. J. Biol. Chem. 272, 17907-17911.
38. Topalian, S.L., Solomon, D., and Rosenberg, S.A. (1989). Tumor-specific cytolysis by lymphocytes infiltrating human melanomas. J. Immunol. 142, 3714-3725.
39. Trapani, J.A., Browne, K.A., Smyth, M.J., and Jans, D.A. (1996). Localization of granzyme B in the nucleus: a putative role in the mechanism of cytotoxic lymphocyte-mediated apoptosis. J. Biol. Chem. 271, 4127-4133.
40. Tschopp, J. (1994). Granzyme B. Methods Enzymol. 244, 80-87.
41. White, E. (1996). Life, death, and the pursuit of apoptosis. Genes Dev. 10, 1-15.
42. Xue, D., and Horvitz, H.R. (1995). Inhibition of the Caenorhabditis elegans cell-death protease CED-3 by a CED-3 cleavage site in baculovirus p35 protein. Nature 377, 248-251.