Granule-mediated killing: Pathways for granzyme B-initiated apoptosis

Journal of Experimental Medicine

Volumn 186, Issue 8, 1997, Pages 1323-1331

  Talanian, Robert V ^a   Yang, Xiao He ^b   Turbov, Jane ^b   Seth, Prem ^e   Ghayur, Tariq ^a   Casiano, Carlos A ^c   Orth, Kim ^d   Froelich, Christopher J ^b,f  

^a BASF Bioresearch Corporation   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e NATIONAL CANCER INSTITUTE   (United States)

^f EVANSTON HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; GRANZYME B; LAMIN B; SERINE PROTEINASE INHIBITOR; SMALL NUCLEAR RIBONUCLEOPROTEIN;

APOPTOSIS; ARTICLE; AUTORADIOGRAPHY; CELL DEATH; CONTROLLED STUDY; DIAGNOSIS; DNA STRAND BREAKAGE; ETIOLOGY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL;

APOPTOSIS; BREAST NEOPLASMS; CASPASE 3; CASPASE 7; CASPASES; CELL DEATH; CYSTEINE ENDOPEPTIDASES; CYTOPLASMIC GRANULES; CYTOTOXICITY, IMMUNOLOGIC; ENZYME ACTIVATION; GRANZYMES; HUMANS; JURKAT CELLS; SERINE ENDOPEPTIDASES; SERINE PROTEINASE INHIBITORS; SUBSTRATE SPECIFICITY; TUMOR CELLS, CULTURED;

EID: 0030727712     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.186.8.1323     Document Type: Article

References (40)

1. Atkinson, E.A., and R.C. Bleackley. 1995. Mechanisms of lysis by cytotoxic T cells. Crit. Rev. Immunol. 15:359-384.
2. Darmon, A.J., N. Ehrman, A. Caputo, J. Fujinaga, and R.C. Bleackley. 1994. The cytotoxic T cell proteinase granzyme B does not activate interleukin-1β-converting enzyme. J. Biol. Chem. 269:32043-32046.
3. Darmon, A.J., D.W. Nicholson, and R.C. Bleackley. 1995. Activation of the apoptotic protease CPP32 by cytotoxic T-cell-derived granzyme B. Nature (Lond.). 377:446-448.
4. Quan, L.T., M. Tewari, K. O'Rourke, V.M. Dixit, S.J. Snipas, G.G. Poirier, C. Ray, D.J. Pickup, and G.S. Salvesen. 1996. Proteolytic activation of the cell death protease Yama/ CPP32 by granzyme B. Proc. Natl. Acad. Sci. USA. 93:1972-1976.
5. Martin, S.J., G.P. Amarante-Mendes, L.F. Shi, T.H. Chuang, C.A. Casiano, G.A. O'Brien, P. Fitzgerald, E.M. Tan, G.M. Bokoch, A.H. Greenberg, and D.R. Green. 1996. The cytotoxic cell protease granzyme B initiates apoptosis in a cell-free system by proteolytic processing and activation of the ICE/ CED-3 ramdy protease, CPP32, via a novel two-step mechanism. EMBO (Eur. Mol. Biol. Organ.) J. 15:2407-2416.
6. Orth, K., A.M. Chinnaiyan, M. Garg, C.J. Froelich, and V.M. Dixit. 1996. The CED-3/ICE-like protease Mch2 is activated during apoptosis and cleaves the death substrate lamin A. J. Biol. Chem. 271:16443-16446.
7. Fernandes-Alnemri, T., G. Litwack, and E.S. Alnemri. 1995. Mch2, a new member of the apoptotic Ced-3/Ice cysteine protease gene family. Cancer Res. 55:2737-2742.
8. Chinnaiyan, A.M., K. Orth, W.L. Hanna, H.J. Duan, G.G. Poirier, C.J. Froelich, and V.M. Dixit. 1996. Cytotoxic T cell-derived granzyme B activates the apoptotic protease ICE-LAP3. Cnrr. Biol. 6:897-899.
9. Gu, Y., C. Sarnecki, M.A. Fleming, J.A. Lippke, R.C. Bleackley, and M.S.S. Su. 1996. Processing and activation of CMH-1 by granzyme B. J. Biol. Chem. 271:10816-10820.
10. Fernandes-Alnemri, T., A. Takahashi, R. Armstrong, J. Krebs, L. Fritz, K.J. Tomaselli, L. Wang, Z. Yu, C.M. Croce, G. Salveson, et al. 1995. Mch3, a novel human apoptotic cysteine protease highly related to CPP32. Cancer Res. 55:6045-6052.
11. Boldin, M.P., T.M. Goncharov, Y.V. Goltsev, and D. Wallach. 1996. Involvement of MACH, a novel MORT1/ FADD-interacting protease, in Fas/APO-1-and TNF receptor-induced cell death. Cell. 85:803-815.
12. Muzio, M., A.M. Chinnaiyan, F.C. Kischkel, K. O'Rourke, A. Shevchenko, C. Scaffid, J.D. Bretz, M. Zhang, J. Ni, R. Gentz, et al. 1996. FLICE, a novel FADD-homologous ICE/ CED-3-like protease, is recruited to the CD-95 (FAS/Apo-1) death-inducing signaling complex (DISC). Cell. 86:817-821.
13. Srinivasula, S.M., M. Ahmad, T. Fernandes-Alnemri, G. Litwack, and E.S. Alnemri. 1996. Molecular ordering of the Fas-apoptotic pathway: the Fas/APO-1 protease Mch5 is a CrmA-inhibitable protease that activates multiple Ced-3/ ICE-like cysteine proteases. Proc. Natl. Acad. Sci. USA. 93: 14486-14491.
14. Duan, H.J., 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. 171: 16720-16724.
15. Fernandes-Alnemri, T., R.C. Armstrong, J. Krebs, S.M. Srinivasula, L. Wang, F. Bullrich, L.C. Fritz, J.A. Trapani, K.J. Tomaselli, G. Litwack, and E.S. Alnemri. 1996. In vitro activation of CPP32 and Mch3 by Mch4, a novel human apoptotic cysteine protease containing two FADD-like domains. Proc. Natl. Acad. Sci. USA. 93:7464-7469.
16. Vincenz, C., and V.M. Dixit. 1997. Fas-associated-death domain protein interleukin-1β-converting enzyme 2 (FLICE2), an ICE/Ced-3 homologue, is proximally involved in CD95-and p55-mediated death signaling. J. Biol. Chem. 272:6578-6583.
17. Froelich, C.J., K. Orth, J. Turbov, P. Seth, B.M. Babior, R.A. Gottlieb, G.M. Shah, R.C. Bleackley, V.M. Dixit, and W.L. Hanna. 1996. New paradigm for lymphocyte granule mediated cytotoxicity: targets bind and internalize granzyme B but a endosomolytic agent is necessary for cytosolic delivery and apoptosis. J. Biol. Chem. 271:29073-29081.
18. Shi, L.F., G. Chen, G. MacDonald, L. Bergeron, H.L. Li, M. Miura, R.J. Rotello, D.K. Miller, P. Li, T. Seshadri, J.Y. Yuan, and A.H. Greenberg. 1996. Activation of an interleukin 1 converting enzyme-dependent apoptosis pathway by granzyme B. Proc. Natl. Acad. Sci. USA. 93:11002-11007.
19. Krajewska, M., H.G. Wang, S. Krajewski, J.M. Zapata, A. Shabaik, R. Gascoyne, and J.C. Reed. 1997. Immunohistochemical analysis of in vivo patterns of expression of CPP32 (Caspase-3), a cell death protease. Cancer Res. 57:1605-1613.
20. Komiyama, T., C.A. Ray, D.J. Pickup, A.D. Howard, N.A. Thornberry, E.P. Peterson, and G. Salvesen. 1994. Inhibition of interleukin-1β converting enzyme by the cowpox virus serpin CrmA. An example of cross-class inhibition. J. Biol. Chem. 269:19331-19337.
21. Thome, M., P. Schneider, K. Hofmann, H. Fickenscher, E. Meinl, F. Neipel, C. Mattmann, K. Burns, J.L. Bodmer, M. Schröter. et al. 1997. Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature (Lond.). 386:517-521.
22. Shi, L., S. Mai, S. Israels, K.A. Browne, J.A. Trapani, and A.H. Greenberg. 1997. Granzyme B (GraB) autonomously crosses the cell membrane and perforin initiates apoptosis and GraB nuclear localization. J. Exp. Med. 185:855-866.
23. Hanna, W.L., X. Zhang, J. Turbov, U. Winkler, D. Hudig, and C.J. Froelich. 1993. Rapid purification of cationic granule proteases: application to human granzymes. Protein Purif. Exp. 4:398-402.
24. Seth, P. 1994. A simple and efficient method of protein delivery into cells using adenovirus. Biochem. Biophys. Res. Commun. 203:582-587.
25. Casiano, C.A., S.J. Martin, D.R. Green, and E.M. Tan. 1996. Selective cleavage of nuclear autoantigens during CD95 (Fas/APO-1)-mediated T cell apoptosis. J. Exp. Med. 184:765-770.
26. Hugunin, M., L.J. Quintal, J.A. Mankovich, and T. Ghayur. 1996. Protease activity of in vitro transcribed and translated Caenorhabditis elegans cell death gene (ced-3) product. J. Biol. Chem. 271:3517-3522.
27. Ghayur, T., M. Hugunin, R.V. Talanian, S. Ratnofsky, C. Quinlan, Y. Emoto, P. Pandey, R. Datta, Y.Y. Huang, S. Kharbanda, et al. 1996. Proteolytic activation of protein kinase C d by an ICE/CED 3-like protease induces characteristics of apoptosis. J. Exp. Med. 184:2399-2404.
28. Orth, K., K. O'Rourke, G.S. Salvesen, and V.M. Dixit. 1996. Molecular ordering of apoptotic mammalian Ced-3/ ICE proteases. J. Biol. Chem. 171:16443-16446.
29. Talanian, R.V., C. Quinlan, S. Trautz, M.C. Hackett, J.A. Mankovich, D. Banach, T. Ghayur, K.D. Brady, and W.W. Wong. 1997. Substrate specificities of caspase family proteases. J. Biol. Chem. 272:9677-9682.
30. Gorczyca, W., J. Gong, and Z. Darzynkiewicz. 1993. Detection of DNA strand breaks in individual apoptotic cells by the in situ terminal deoxynucleotidyl transferase and nick translation assays. Cancer Res. 53:1945-1951.
31. Duan, H.J., A.M. Chinnaiyan, P.L. Hudson, J.P. Wing, W.W. He, and V.M. Dixit. 1996. ICE-LAP3, a novel mammalian homologue of the Caenorhabditis elegans cell death protein ced-3 is activated during fas-and tumor necrosis factor-induced apoptosis. J. Biol. Chem. 271:1621-1625.
32. Enari, M., R.V. Talanian, W.W. Wong, and S. Nagata. 1996. Sequential activation of ICE-like and CPP32-like proteases during Fas-mediated apoptosis. Nature (Lond.). 380: 723-726.
33. Fernandes-Alnemri, T., G. Litwack, and E.S. Alnemri. 1994. CPP32, a novel human apoptotic protein with homology to Caenorhabditis elegans cell death protein Ced-3 and mammalian interleukin-1b-converting enzyme. J. Biol. Chem. 269: 30761-30764.
34. Müller, C., and J. Tschopp. 1994. Resistance of CTL to perforin-mediated lysis: evidence for a lymphocyte membrane protein interacting with pertorin. J. Immunol. 153:2470-2478.
35. Sarin, A., M.S. Williams, M.A. Alexander-Miller, J.A. Berzofsky, C. M. Zacharchuk, and P.A. Henkart. 1997. Target cell lysis by CTL granule exocytosis is independent of ICE/ Ced-3 family proteases. Immunity. 6:209-215.
36. Shi, L.F., G. Chen, D.L. He, D.G. Bosc, D.W. Litchfield, and A.H. Greenberg. 1996. Granzyme B induces apoptosis and cyclin A-associated cyclin-dependent kinase activity in all stages of the cell cycle. J. Immunol. 157:2381-2385.
37. Ongkeko, W., D.J.P. Ferguson, A.L. Harris, and C. Norbury. 1995. Inactivation of Cdc2 increases the level of apoptosis induced by DNA damage. J. Cell Sci. 108:2897-2904.
38. cdc2-dependent kinase activity during apoptosis: a possible activation mechanism of DNase I leading to DNA breakdown. Eur. J. Cell Biol. 69:143-150.
39. Chen, G., L. Shi, D.W. Litchfield, and A.H. Greenberg. 1995. Rescue from granzyme B-induced apoptosis by Wee1 kinase. J. Exp. Med. 181:2295-2300.
40. Zhou, Q., S. Snipas, K. Orth, M. Muzio, V.M. Dixit, and G.S. Salvesen. 1997. Target protease specificity of the viral serpin CrmA: analysis of five caspases. J. Biol. Chem. 272: 7797-7800.