Mitochondria-dependent and -independent regulation of granzyme B- induced apoptosis

Journal of Experimental Medicine

Volumn 189, Issue 1, 1999, Pages 131-143

  MacDonald, Glen ^a   Shi, Lianfa ^a   Vande Velde, Christine ^a   Lieberman, Judy ^b   Greenberg, Arnold H ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Apoptosis; Caspase; Cytochrome c; Granzyme B; Mitochondria

Indexed keywords

CASPASE 3; CASPASE INHIBITOR; CYTOCHROME C; GRANZYME B; PERFORIN; PROTEIN BCL 2; PROTEIN BCL X; REACTIVE OXYGEN METABOLITE;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOFLUORESCENCE MICROSCOPY; MEMBRANE POTENTIAL; MITOCHONDRION; PRIORITY JOURNAL;

ANIMALS; APOPTOSIS; CASPASES; CELL LINE; CHYMASES; CYTOCHROME C GROUP; FLUORESCENT ANTIBODY TECHNIQUE; GENES, BCL-2; GRANZYMES; HUMANS; MEMBRANE GLYCOPROTEINS; MEMBRANE POTENTIALS; MITOCHONDRIA; PORE FORMING CYTOTOXIC PROTEINS; RATS; REACTIVE OXYGEN SPECIES; SERINE ENDOPEPTIDASES; SERINE PROTEINASE INHIBITORS; TRYPTASES;

EID: 0033521626     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.189.1.131     Document Type: Article

References (65)

1. Nagata, S. 1997. Apoptosis by death factor. Cell. 88:355-365.
2. Shi, L., R.P. Kraut, R. Aebersold, and A.H. Greenberg. 1992. A natural killer cell granule protein that induces DNA fragmentation and apoptosis. J. Exp. Med. 175:553-566.
3. Heusel, J.W., R.L. Wesselschmidt, S. Shresta, J.H. Russell, and T.J. Ley. 1994. Cytotoxic lymphocytes require granzyme B for the rapid induction of DNA fragmentation and apoptosis in allogeneic target cells. Cell. 76:977-987.
4. Nicholson, D.W., and N.A. Thornberry. 1997. Caspases: killer proteases. Trends Biochem. Sci. 22:299-306.
5. Martin, S.J., and D.R. Green. 1995. Protease activation during apoptosis: death by a thousand cuts? Cell. 82:349-352.
6. 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.
7. Muzio, M., A.M. Chinnaiyan, F.C. Kischkel, K. O'Rourke, A. Shevchenko, J. Ni, C. Scaffidi, J.D. Bretz, M. Zhang, R. Gentz, et al. 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.
8. Jans, D.A., P. Jans, L.J. Briggs, V. Sutton, and J.A. Trapani. 1996. Nuclear transport of granzyme B (fragmentin-2). Dependence on perforin in vivo and cytosolic factors in vitro. J. Biol. Chem. 271:30781-30789.
9. Shi, L.F., S. Mai, S. Israels, K. 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.
10. Froelich, C.J., K. Orth, J. Turbov, P. Seth, R. Gottlieb, B. Babior, G.M. Shah, R.C. Bleackley, V.M. Dixit, and W. Hanna. 1996. 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.
11. Shi, L., C.M. Kam, J.C. Powers, R. Aebersold, and A.H. Greenberg. 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.
12. Poe, M., J.T. Blake, D.A. Boulton, M. Gammon, N.H. Sigal, J.K. Wu, and H.J. Zweerink. 1991. Human cytotoxic lymphocyte granzyme B. Its purification from granules and the characterization of substrate and inhibitor specificity. J. Biol. Chem. 266:98-103.
13. Thornberry, N.A., T.A. Ranon, E.P. Pieterson, D.M. Rasper, T. Timkey, M. Garcia-Calvo, V.M. Houtzager, P.A. Nordstrom, S. Roy, 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.
14. 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 family protease, CPP32, via a novel two-step mechanism. EMBO (Eur. Mol. Biol. Organ.) J. 15:2407-2416.
15. Han, Z.Y., E.A. Hendrickson, T.A. Bremner, and J.H. Wyche. 1997. A sequential two-step mechanism for the production of the mature p17:p12 form of caspase-3 in vitro. J. Biol. Chem. 272:13432-13436.
16. Muzio, M., G.S. Salvesen, and V.M. Dixit. 1997. FLICE induced apoptosis in a cell-free system. Cleavage of caspase zymogens. J. Biol. Chem. 272:2952-2956.
17. 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. 377:446-448.
18. 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.
19. 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.
20. Talanian, R.V., X.H. Yang, J. Turbov, P. Seth, T. Ghayur, C.A. Casiano, K. Orth, and C.J. Froelich. 1997. Granule-mediated killing: pathways for granzyme B-initiated apoptosis. J. Exp. Med. 186:1323-1331.
21. Zamzami, N., S.A. Susin, P. Marchetti, T. Hirsch, I. Gomez-Monterrey, M. Castedo, and G. Kroemer. 1996. Mitochondrial control of nuclear apoptosis. J. Exp. Med. 183:1533-1544.
22. Marchetti, P., M. Castedo, S.A. Susin, N. Zamzami, T. Hirsch, A. Macho, A. Haeffner, F. Hirsch, M. Geuskens, and G. Kroemer. 1996. Mitochondrial permeability transition is a central coordinating event of apoptosis. J. Exp. Med. 184: 1155-1160.
23. Susin, S.A., N. Zamzami, M. Castedo, E. Daugas, H.G. Wang, S. Geley, F. Fassy, J.C. Reed, and G. Kroemer. 1997. The central executioner of apoptosis: multiple connections between protease activation and mitochondria in Fas/APO-1/CD95-and ceramide-induced apoptosis. J. Exp. Med. 186: 25-37.
24. Liu, X., C. Kim, J. Yang, R. Jemmerson, and X. Wang. 1996. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell. 86:147-157.
25. 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.
26. Yang, J., X. Liu, K. Bhalla, C.N. 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.
27. Zou, H., W.J. Henzel, X. Liu, A. Lutschg, and X. Wang. 1997. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell. 90:405-413.
28. Li, P., D. Nijhawan, I. Budihardjo, S.M. Srinivasula, M. Ahmad, E.S. Alnemri, and X.D. Wang. 1997. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell. 91:479-489.
29. Krajewski, S., S. Tanaka, S. Takayama, M.J. Schibler, W. Fenton, and J.C. Reed. 1993. Investigation of the subcellular distribution of the bcl-2 oncoprotein: residence in the nuclear envelope, endoplasmic reticulum, and outer mitochondrial membranes. Cancer Res. 53:4701-4714.
30. Tanaka, S., K. Saito, and J.C. Reed. 1993. Structure-function analysis of the Bcl-2 oncoprotein. Addition of a heterologous transmembrane domain to portions of the Bcl-2 beta protein restores function as a regulator of cell survival. J. Biol. Chem. 268:10920-10926.
31. Zhu, W., A. Cowie, G.W. Wasfy, L.Z. Penn, B. Leber, and D.A. Andrews. 1996. Bcl-2 mutants with restricted subcellular location reveal spatially distance pathways for apoptosis in different cell types. EMBO (Eur. Mol. Biol. Organ.) J. 15: 4130-4141.
32. Chinnaiyan, A.M., K. O'Rourke, B.R. Lane, and V.M. Dixit. 1997. Interaction of CED-4 with CED-3 and CED-9: a molecular framework for cell death. Science. 275:1122-1126.
33. Wu, D., H.D. Wallen, N. Inohara, and G. Nunez. 1997. Interaction and regulation of the Caenorhabditis elegans death protease CED-3 by CED-4 and CED-9. J. Biol. Chem. 272: 21449-21454.
34. Susin, S.A., N. Zamzami, M. Castedo, T. Hirsch, P. Marchetti, A. Macho, E. Daugas, M. Geuskens, and G. Kroemer. 1996. Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J. Exp. Med. 184:1331-1341.
35. Sutton, V.R., D.L. Vaux, and J.A. Trapani. 1997. Bcl-2 prevents apoptosis induced by perform and granzyme B, but not that mediated by whole cytotoxic lymphocytes. J. Immunol. 158:5783-5790.
36. Chiu, V.K., C.M. Walsh, C.C. Liu, J.C. Reed, and W.R. Clark. 1995. Bcl-2 blocks degranulation but not fas-based cell-mediated cytotoxicity. J. Immunol. 154:2023-2032.
37. Schroeter, M., B. Lowin, C. Borner, and J. Tschopp. 1995. Regulation of Fas (Apo-1/CD95)- and perforin-mediated lytic pathways of primary cytotoxic T lymphocytes by the protooncogene bcl-2. Eur. J. Immunol. 25:3509-3513.
38. Xia, Z., C.M. Kam, C. Huang, J.C. Powers, R.J. Mandle, R.L. Stevens, and J. Lieberman. 1998. Expression and purification of enzymatically active recombinant granzyme B in a baculovirus system. Biochem. Biophys. Res. Commun. 243: 384-389.
39. Pedersen, P.L., J.W. Greenwalt, B. Reynafarje, J. Hullihen, G.L. Decker, J.W. Soper, and E. Bustamente. 1978. Preparation and characterization of mitochondria and submitochondrial particles of rat liver and liver-derived tissues. Methods Cell. Biol. 20:411-481.
40. Kluck, R.M., S.J. Martin, B.M. Hoffman, J.S. Zhou, D.R. Green, and D.D. Newmeyer. 1997. Cytochrome c activation of CPP32-like proteolysis plays a critical role in a Xenopus cell-free apoptosis system. EMBO (Eur. Mol. Biol. Organ.) J. 16:4639-4649.
41. Kroemer, G., N. Zamzami, and S.A. Susin. 1997. Mitochondrial control of apoptosis. Immunol. Today. 18:44-51.
42. 2+ and susceptibility to cytolysis. J. Immunol. 148:2489-2496.
43. Szabo, I., P. Bernardi, and M. Zoratti. 1992. Modulation of the mitochondrial megachannel by divalent cations and protons. J. Biol. Chem. 267:2940-2946.
44. 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.
45. Medema, J.P., R.E. Toes, C. Scaffidi, T.S. Zheng, R.A. Flavell, C.J. Melief, M.E. Peter, R. Offringa, and P.H. Krammer. 1997. Cleavage of FLICE (caspase-8) by granzyme B during cytotoxic T lymphocyte-induced apoptosis. Eur. J. Immunol. 27:3492-3498.
46. Shi, L., G. Chen, G. MacDonald, L. Bergeron, H. Li, M. Miura, R. Rotello, D.K. Miller, P. Li, T. Seshadri, J. Yuan, and A.H. Greenberg. 1996. Activation of an ICE dependent apoptosis pathway by granzyme B. Proc. Natl. Acad. Sci. USA. 93:11002-11007.
47. 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.
48. Bossy-Wetzel, E., D.D. Newmeyer, and D.R. Green. 1998. Mitochondrial cytochrome c release in apoptosis occurs upstream of DEVD-specific caspase activation and independently of mitochondrial transmembrane depolarization. EMBO (Eur. Mol. Biol. Organ.) J. 17:37-49.
49. L interacts with Apaf-1 and inhibits Apaf-1-dependent caspase-9 activation. Proc. Natl. Acad. Sci. USA. 95:4386-4391.
50. L, and Apaf-1 form a ternary complex. J. Biol. Chem. 273:5841-5845.
51. Rosse, T., R. Olivier, L. Monney, M. Rager, S. Conus, I. Fellay, B. Jansen, and C. Borner. 1998. Bcl-2 prolongs cell survival after Bax-induced release of cytochrome c. Nature. 391:496-499.
52. Ng, F.W.H., M. Nguyen, T. Kwan, P.E. Branton, D.W. Nicholson, J.A. Cromlish, and G.C. Shore. 1997. p28 Bap31, a Bcl-2/Bcl-XL- and procaspase-8-associated protein in the endoplasmic reticulum. J. Cell Biol. 139:327-338.
53. L has activity independent of cytochrome c release. J. Biol. Chem. 272: 30299-30305.
54. Chiu, V.K., C.M. Walsh, C.C. Liu, J.C. Reed, and W.R. Clark. 1995. Bcl-2 blocks degranulation but not fas-based cell-mediated cytotoxicity. J. Immunol. 154:2023-2032.
55. Schroter, M., M.C. Peitsch, and J. Tschopp. 1996. Increased p34cdc2-dependent kinase activity during apoptosis: a possible activation mechanism of DNase I leading to DNA breakdown. Eur. J. Cell Biol. 69:143-150.
56. Renvoize, C., R. Roger, N. Moulian, J. Bertoglio, and J. Breard. 1997. Bcl-2 expression in target cells leads to functional inhibition of caspase-3 protease family in human NK and lymphokine-activated killer cell granule-mediated apoptosis. J. Immunol. 159:126-134.
57. Vaux, D.L., H.L. Aguila, and I.L. Weissman. 1992. Bcl-2 prevents death of factor-deprived cells but fails to prevent apoptosis in targets of cell mediated killing. Int. Immunol. 4:821-824.
58. Scaffidi, C., S. Fulda, A. Srinivasan, C. Friesen, F. Li, K.J. Tomaselli, K.-M. Debatin, P.H. Krammer, and M.E. Peter. 1998. Two CD95 (APO-1/Fas) signaling pathways. EMBO (Eur. Mol. Biol. Organ.) J. 17:1675-1687.
59. Shi, L., R.P. Kraut, R. Aebersold, and A.H. Greenberg. 1992. A natural killer cell granule protein that induces DNA fragmentation and apoptosis. J. Exp. Med. 175:553-566.
60. Nakajima, H., H.L. Park, and P.A. Henkart. 1995. Synergistic roles of granzymes A and B in mediating target cell death by rat basophilic leukemia mast cell tumors also expressing cytolysin/perforin. J. Exp. Med. 181:1037-1046.
61. Simon, M.M., M. Hausmann, T. Tran, K. Ebnet, J. Tschopp, R. ThaHla, and A. Mullbacher. 1997. In vitro-and ex vivo-derived cytolytic leukocytes from granzyme A X B double knockout mice are defective in granule-mediated apoptosis but not lysis of target cells. J. Exp. Med. 186:1781-1786.
62. Masson, D., and J. Tschopp. 1987. A family of serine esterases in lytic granules of cytolytic T lymphocytes. Cell. 49: 679-685.
63. Jaenicke, R.U., M.L. Sprengart, M.R. Wati, and A.G. Porter. 1998. Caspase-3 is required for DNA fragmentation and morphological changes associated with apoptosis. J. Biol. Chem. 273:9357-9360.
64. Cheng, E.H.Y., D.G. Kirsch, R.J. Clem, R. Ravi, M.B. Kastan, A. Bedi, K. Ueno, and J.M. Hardwick. 1997. Conversion of Bcl-2 to a Bax-like death effector by caspases. Science. 278:1966-1968.
65. L through caspase interaction. Proc. Natl. Acad. Sci. USA. 95:554-559.