Granzyme B-induced loss of mitochondrial inner membrane potential (ΔΨ(m)) and cytochrome c release are caspase independent

Journal of Immunology

Volumn 163, Issue 9, 1999, Pages 4683-4693

  Heibein, Jeffrey A ^a   Barry, Michele ^a   Motyka, Bruce ^a   Bleackley, R Chris ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; CYTOCHROME C; GRANZYME B;

APOPTOSIS; ARTICLE; CYTOTOXIC T LYMPHOCYTE; HUMAN; HUMAN CELL; MEMBRANE POTENTIAL; MITOCHONDRIAL MEMBRANE; PRIORITY JOURNAL; TARGET CELL;

ADENOVIRUSES, HUMAN; ANIMALS; APOPTOSIS; CASPASES; CYCLOSPORINE; CYTOCHROME C GROUP; DNA FRAGMENTATION; ENZYME ACTIVATION; GRANZYMES; HUMANS; INTRACELLULAR MEMBRANES; JURKAT CELLS; MEMBRANE GLYCOPROTEINS; MEMBRANE POTENTIALS; MITOCHONDRIA; PHOSPHATIDYLSERINES; PORE FORMING CYTOTOXIC PROTEINS; RATS; REACTIVE OXYGEN SPECIES; SERINE ENDOPEPTIDASES; T-LYMPHOCYTES, CYTOTOXIC;

EID: 0032752882     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (64)

1. Atkinson, E., and R. C. Bleackley. 1995. Mechanisms of lysis by cytotoxic T cells. Crit. Rev. Immunol. 15:359.
2. Darmon, A. J., M. J. Pinkoski, and R. C. Bleackley. 1999. Granule-mediated cytotoxicity. In Apoptosis: Biology and Mechanisms. S. Kumar, ed. Springer-Verlag, Berin Heidelberg, p. 103.
3. Kägi, D., B. Ledermann, K. Bürki, R. M. Zinkernagel, and H. Hengartner. 1996. Molecular mechanisms of lymphocyte-mediated cytotoxicity and their role in immunological protection and pathogenesis in vivo. Annu. Rev. Immunol. 14:207.
4. Shresta, S., C. T. Pham, D. A. Thomas, T. A. Graubert, and T. J. Ley. 1998. How do cytotoxic lymphocytes kill their targets? Curr. Opin. Immunol. 10:581.
5. Yannelli, J. R., J. A. Sullivan, G. L. Mandel, and V. H. Engelhard. 1986. Reorientation and fusion of cytotoxic T lymphocyte granules after interaction with target cells as determined by high resolution cinematography. J. Immunol. 136: 377.
6. Kupfer, A., S. J. Singer, and G. Dennart. 1986. On the mechanism of unidirectional killing in mixtures of two cytotoxic lymphocytes. J. Exp. Med. 163:489.
7. Berke, G. 1995. The CTL's kiss of death. Cell 81:9.
8. Thornberry, N. A., and Y. Lazebnik. 1998. Caspases, enemies within. Science 281:1312.
9. Nicholson, D. W., and N. A. Thornberry. 1997. Caspases: killer proteases. Trends Biochem. Sci. 22:299.
10. 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.
11. Darmon, A. J., T. J. Ley, D. W. Nicholson, and R. C. Bleackley. 1996. Cleavage of CPP32 by granzyme B represents a critical role for granzyme B in the induction of target cell DNA fragmentation. J. Biol. Chem. 271:21709.
12. Martin, S. J., G. P. Amarante-Mendes, L. 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 J. 15:2407.
13. Quan, L. T., M. Tewari, K. O'Rourke, V. Dixit, S. J. Snipas, G. G. Poirier, C. Ray, D. J. Pickup, and G. S. Salvesen. 1996. Proteolytic activation of the cell death prolease Yama/CPP32 by granzyme B. Proc. Natl. Acad. Sci. USA 93:1972.
14. Chinnaiyan, A. R., 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. Curr. Biol. 6:897.
15. Gu, Y., C. Sarnecki, M. A. Fleming, J. A. Lippke, R. C. Bleackley, and M. S. Su. 1996. Processing and activation of CMH-1 by granzyme B. J. Biol. Chem. 271: 10816.
16. Srinivasula, S., T. Fernandes-Alnemri, J. Zangirlli, N. Robertson, R. Armstrong, L. Wang, J. Trapani, K. Tomaselli, G. Litwack, and E. Alnemri. 1996. The Ced-3/interleukin 1β converting enzyme-like homolog Mch6 and the lamin-cleaving enzyme Mch2α are substrates for the apoplolic mediator CPP32. J. Biol. Chem. 271:27099.
17. Orth, K., A. Chinnaiyan, M. Garg, C. Froelich, and V. 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.
18. 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.
19. 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.
20. Fernandez-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.
21. Shi, L., G. Chen, G. MacDonald, L. Bergeron, H. Li, M. Miura, R. J. Rotello, D. K. Miller, P. Li, T. Sheshardri, J. 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.
22. Atkinson, E. A., M. Barry, A. J. Darmon, I. Shostak, P. C. Turner, R. W. Moyer, and R. C. Bleackley. 1998. Cytotoxic T lymphocyte-assisted suicide: caspase 3 activation is primarily the result of the direct action of granzyme B. J. Biol. Chem. 273:21261.
23. Enari, M., H. Skahira, H. Yokoyama, K. Okawa, A. Iwamatsu, and S. Nagata, 1998. A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 393:43.
24. Kothakota, S., T. Azuma, C. Reinhard, A. Klippel, J. Tang, K. Chu, T. McGarry, M. Kirschner, K. Koths, D. Kwiatkowski, and L. Williams. 1997. Caspase-3-generated fragment of gelsolin: effector of morphological change in apoptosis. Science 278:294.
25. Stroh, C., and K. Schulze-Osthoff. 1998. Death by a thousand cuts: an ever increasing list of caspase substrates. Cell Death Differ. 5:997.
26. Sarin, A., M. S. Williams, M. A. Alexander-Miller, J. A. Berzofsky, C. M. Zacharachuk, and P. A. Henkart. 1997. Target cell lysis by CTL granule exocylosis is independent of ICE/Ced-3 family proteases. Immunity 6:209.
27. Sarin, A., E. K. Haddad, and P. A. Henkart. 1998. Caspase dependence of target cell damage induced by cytotoxic lymphocytes. J. Immunol. 161:2810.
28. Kroemer, G., N. Zamzami, and S. A. Susin. 1997. Mitochondrial control of apoptosis. Immunol. Today 18:44.
29. Green, D., and G. Kroemer. 1998. The central executioners of apoptosis: caspases or mitochondria? Trends Cell Biol. 8:267.
30. Green, D. R., and J. C. Reed. 1998. Mitochondria and apoptosis. Science 281: 1309.
31. Green, D. R. 1998. Apoptotic pathways: roads to ruin. Cell 94:695.
32. Zoratti, M., and I. Szabò. 1995. The mitochondrial permeability transition. Biochim. Biophys. Acta 1241:139.
33. Liu, X., C. N. 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.
34. 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.
35. Yang, J., X. Liu, K. Bhalla, C. N. Kim, A. M. Ibrado, J. Cai, T.-I. Pen, D. P. Jones, and X. Wang. 1997. Prevention of apoptosis by Bcl-2: release of cytochrome c from mitochondria blocked. Science 275:1129.
36. 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.
37. Susin, S. A., H. K. Lorenzo, N. Zamzami, I. Marzo, C. Brenner, N. Larochette, M.-C. Prévost, P. M. Alzari, and G. Kroemer. 1999. Mitochondrial release of caspase-2 and -9 during the apoptotic process. J. Exp. Med. 189:381.
38. Li, P., D. Nijhawan, I. Budihardjo, S. M. Srinivasula, M. Ahmad, E. S. Alnemri, and X. Wang. 1997. Cytochrome c and dATP-dependent formation of Apaf-1/ caspase-9 complex initiates an apoptotic protease cascade. Cell 91:479.
39. 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.
40. Froelich, C. J., K. Orth, J. Turbov, P. Seth, R. Gottleib, 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.
41. Caputo, A., J. C. Parrish, M. N. James, J. C. Powers, and R. C. Bleackley. 1999. Electrostatic reversal of serine proteinase substrate specificity. Proteins 35:415.
42. Gavrieli, Y., Y. Sherman, and S. A. Ben-Sasson. 1992. Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119.
43. Fadok, V. A., D. R. Voelker, P. A. Campell, J. J. Cohen, D. L. Bratton, and P. M. Henson. 1992. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 148:2207.
44. Koopman, G., C. P. M. Reutelingsperger, G. A. M. Kuijten, R. M. J. Keehnen, S. T. Pals, and M. H. J. v. Oers. 1994. Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 84:1415.
45. Adam, S. A., R. S. Marr, and L. Gerace. 1990. Nuclear protein import in permeabilized mammalian cells requires soluble cytoplasmic factors. J. Cell Biol. 111:807.
46. Wyllie, A. H. 1980. Glucocorticoid induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature 284:555.
47. Martin, S. J., C. P. M. Reutelingsperger, A. J. McGahon, J. A. Rader, R. C. van Schie, D. M. LaFace, and D. R. Green. 1995. Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Ab1. J. Exp. Med. 182:1545.
48. Pinkoski, M. J., M. Hobman, J. A. Heibein, K. Tomaselli, F. Li, P. Seth, C. J. Froelich, and R. C. Bleackley. 1998. Entry and trafficking of granzyme B in target cells during granzyme B-perforin-mediated apoptosis. Blood 92:1044.
49. Heytler, P. G., and W. W. Pritchard. 1962. A new class of uncoupling agents-carbonyl cyanide phenylhydrazones. Biochem. Biophys. Res. Commun. 7:272.
50. Peter, M. E., and P. H. Krammer. 1998. Mechanisms of CD95 (APO-1/Fas)-mediated apoptosis. Curr. Opin. Immunol. 10:545.
51. Garcia-Calvo, M., E. P. Peterson, B. Leiting, R. Ruel, D. W. Nicholson, and N. A. Thornberry. 1998. Inhibition of human caspases by peptide-based and macromolecular inhibitors. J. Biol. Chem. 273:32608.
52. Marchetti, P., T. Hirsch, N. Zamzami, M. Castedo, D. Decaudin, S. A. Susin, B. Masse, and G. Kroemer. 1996. Mitochondrial permeability transition triggers lymphocyte apoptosis. J. Immunol. 157:4830.
53. +-ATPase in intact cells by use of a fluorescent derivative of ouabain: salinity and teleost chloride cells. Cell Tissue Res. 260:529.
54. Marshall, W., S. Bryson, and C. Wood. 1992. Calcium transport by isolated skin of rainbow trout. J. Exp. Biol. 166:297.
55. Reed, J. C. 1997. Cytochrome c: can't live with it - can't live without it. Cell 91:559.
56. 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 J. 17:1675.
57. Yang, X., H. R. Stennicke, B. Wang, D. R. Green, R. U. Jänicke, A. Srinivasan, P. Seth, G. S. Salvesen, and C. J. Froelich. 1998. Granzyme B mimics apical caspases: description of a unified pathway for trans-activation of executioner caspase-3 and -7. J. Biol. Chem. 273:34278.
58. Vanags, D. M., M. I. Pörn-Ares, S. Coppola, D. H. Burgess, and S. Orrenius. 1996. Protease involvement in fodrin cleavage and phosphatidylserine exposure in apoptosis. J. Biol. Chem. 271:31075.
59. Deveraux, Q. L., and J. C. Reed. 1999 IAP family proteins: suppressors of apoptosis. Genes Dev. 13:239.
60. Mac-Donald, G., L. Shi, C. Vande Velde, J. Lieberman, and A. H. Greenberg. 1999. Mitochondria-dependent and -independent regulation of granzyme B-in-duced apoptosis. J. Exp. Med. 189:131.
61. Vande Craen, M., I. Vandenbrande, W. Declercq, M. Irmler, R. Beyaert, J. Tschopp, W. Fiers, and P. Vandenabeele. 1997. Cleavage of caspase family members by granzyme B: a comparative study in vitro. Eur. J. Immunol. 27:1296.
62. Verma, A., J. S. Nye, and S. H. Snyder. 1988. Porphyrins are endogenous ligands for the mitochondrial (peripheral-type) benzodiazepine receptor. Proc. Natl. Acad. Sci. USA 84:2256.
63. Zamzami, N., P. Marchetti, M. Castedo, C. Zanin, J-L. Vassière, P. X. Petit, and G. Kroemer. 1995. Reduction in mitochondrial potential constitutes an early irreversible step of programmed lymphocyte death in vivo. J. Exp. Med. 182:1661.
64. Pahl, H. L., and P. A. Baeuerle. 1997. The ER-overload response: activation of NF-κB. Trends Biochem. Sci. 22:63.