Inhibition of CPP32-Like Proteases Prevents Granzyme B- and Fas-, but Not Granzyme A-Based Cytotoxicity Exerted by CTL Clones

Journal of Immunology

Volumn 158, Issue 5, 1997, Pages 1999-2006

  Anel, Alberto ^a   Gamen, Susana ^a   Alava, Maria A ^a   Schmitt Verhulst, Anne Marie ^b   Piñeiro, Andrés ^a   Naval, Javier ^a  

^a UNIVERSITY OF ZARAGOZA   (Spain)

^b CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL ASPARTYL GLUTAMYL VALYL ASPARTAL; ACETYL-ASPARTYL-GLUTAMYL-VALYL-ASPARTAL; ALLOANTIGEN; CASP3 PROTEIN, HUMAN; CASP3 PROTEIN, MOUSE; CASPASE; CASPASE 3; CERAMIDE; CYSTEINE PROTEINASE; CYSTEINE PROTEINASE INHIBITOR; FAS ANTIGEN; GRANZYME; GZMA PROTEIN, HUMAN; GZMB PROTEIN, HUMAN; GZMB PROTEIN, MOUSE; IMMUNOGLOBULIN A; MEMBRANE PROTEIN; OLIGOPEPTIDE; PERFORIN; PORE FORMING CYTOTOXIC PROTEIN; SERINE PROTEINASE;

ANIMAL; ARTICLE; C57BL MOUSE; CBA MOUSE; CELL CLONE; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; CYTOTOXICITY TEST; DRUG COMBINATION; DRUG EFFECT; HUMAN; IMMUNOLOGY; METABOLISM; MOUSE;

ANIMALS; ANTIGENS, CD95; CASPASE 3; CASPASES; CERAMIDES; CLONE CELLS; CYSTEINE ENDOPEPTIDASES; CYSTEINE PROTEINASE INHIBITORS; CYTOTOXICITY TESTS, IMMUNOLOGIC; CYTOTOXICITY, IMMUNOLOGIC; DRUG COMBINATIONS; GRANZYMES; HUMANS; IMMUNOGLOBULIN A; ISOANTIGENS; MEMBRANE GLYCOPROTEINS; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; OLIGOPEPTIDES; PORE FORMING CYTOTOXIC PROTEINS; SERINE ENDOPEPTIDASES; T-LYMPHOCYTES, CYTOTOXIC;

EID: 0031091770     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (53)

1. Kägi, D., B. Ledermann, K. Bürki, P. Seiler, B. Odermatt, K. J. Olsen, E. R. Podack, R. M. Zinkernagel, and H. Hengartner. 1994. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-knockout mice. Nature 369:31.
2. Henkart, P. A. 1994. Lymphocyte-mediated cytotoxicity: two pathways and multiple effector molecules. Immunity 1:343.
3. 2+-independent T cell-mediated cytotoxicity. J. Exp. Med. 177:195.
4. Suda, T., T. Takahashi, P. Golstein, and S. Nagata. 1993. Molecular cloning and expression of the Fas ligand, a novel member of the tumor necrosis factor family. Cell 75:1169.
5. Kägi, D., F. Vignaux, B. Ledermann, K. Bürki, V. Depraetere, S. Nagata, H. Hengartner, and P. Golstein. 1994. Fas and perform pathways as major mechanisms of T-cell mediated cytotoxicity. Science 265:528.
6. Henkart, P. A., P. Millard, C. W. Reynolds, and M. P. Henkart. 1984. Cytolytic activity of purified cytoplasmic granules from cytotoxic rat large granular lymphocyte tumors. J. Exp. Med. 160:75.
7. 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.
8. Van den Broek, M. F., D. Kägi, R. M. Zinkernagel, and H. Hengartner. 1995. Peforin dependence of natural killer cell-mediated tumor control in vivo. Eur. J. Immunol. 25:3514.
9. Russell, J. H., B. Rush, C. Weaver, and R. Wang. 1993. Mature T cells of autoimmune lpr/lpr mice have a defect in antigen-stimulated suicide. Proc. Natl. Acad. Sci. USA 90:4409.
10. Vignaux, F., and P. Golstein. 1994. Fas-based lymphocyte-mediated cytotoxicity against syngeneic activated lymphocytes: a regulatory pathway? Eur. J. Immunol. 24:923.
11. Singer, G. G., and A. K. Abbas. 1994. The Fas antigen is involved in peripheral but not thymic deletion of T lymphocytes in T cell receptor transgenic mice. Immunity 1:365.
12. Dhein, J., H. Walczak, C. Bäumler, K. M. Debatin, and P. H. Krammer. 1995. Autocrine T-cell suicide mediated by APO-1 (Fas/CD95). Nature 373:438.
13. Alderson, M. R., T. W. Tough, T. Davis-Smith, S. Braddy, B. Falk, K. A. Schooley, R. G. Goodwin, C. A. Smith, F. Ramsdell, and D. H. Lynch. 1995. Fas ligand mediates activation-induced cell death in human T lymphocytes. J. Exp. Med. 181:71.
14. Zheng, L., G. Fisher, R. E. Miller, J. Peschon, D. H. Lynch, and M. J. Lenardo. 1995. Induction of apoptosis in mature T cells by tumor necrosis factor. Nature 377:348.
15. Martin, S. J., and D. R. Green. 1995. Protease activation during apoptosis: death by a thousand cuts? Cell 82:349.
16. 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. 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.
17. 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-1β-converting enzyme. J. Biol. Chem. 269:30761.
18. Tewari, M., L. T. Quan, K. O'Rourke, S. Desnoyers, Z. Zeng, D. R. Beidler, G. G. Poirier, G. S. Salvesen, and V. M. Dixit. 1995. Yama/CPP32β, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 81:801.
19. Schlegel, J., I. Peters, S. Orrenius, D. K. Miller, N. A. Thornberry, T. T. Yamin, and D. W. Nicholson. 1996. CPP32/apopain is a key ICE-like protease involved in Fas-mediated apoptosis. J. Biol. Chem. 271:1841.
20. Gamen, S., I. Marzo, A. Anel, A. Piñeiro, and J. Naval. 1996. CPP32 inhibition prevents Fas-induced ceramide generation and apoptosis in human cells. FEBS Lett. 390:233.
21. Anel, A., S. Gamen, M. A. Alava, A. M. Schmitt-Verhulst, A. Piñeiro, and J. Naval. 1996. Role of oxidative damage and ICE-like proteases in Fas-based cytotoxicity exerted by effector T cells. Int. Immunol. 8:1173.
22. Liu, C. C., C. M. Walsh, and J. D. E. Young. 1995. Perforin: structure and function. Immunol. Today 16:194.
23. Smyth, M. J., and J. A. Trapani. 1995. Granzymes: exogenous proteinases that induce target cell apoptosis. Immunol. Today 16:202.
24. Kumar, S., and N. L. Harvey. 1995. Role of multiple cellular proteases in the execution of programmed cell death. FEBS Lett. 375:169.
25. Ebnet, K., M. Hausmann, F. Lehmann-Grube, A. Müllbacher, M. Kopf, M. Lamers, and M. M. Simon. 1995. Granzyme A-deficient mice retain potent cell-mediated cytotoxicity. EMBO J. 14:4230.
26. 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.
27. 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.
28. 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. Proleolytic activation of the cell death protease Yama/CPP32 by granzyme B. Proc. Natl. Acad. Sci. USA 93: 1972.
29. 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.
30. 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.
31. Hua, C., C. Boyer, A. Guimezanes, F. Albert, and A.-M. Schmitt-Verhulst. 1986. Analysis of T cell activation requirements with the use of alloantigens or an anti-clonotypic monoclonal antibody. J. Immunol. 136:1927.
32. Anel, A., M. Buferne, C. Boyer, A. M. Schmitt-Verhulst, and P. Golstein. 1994. T cell receptor-induced Fas ligand expression in cytotoxic T lymphocyte clones is blocked by protein tyrosine kinase inhibitors and cyclosporin A. Eur. J. Immunol. 24:2469.
33. Odake, S., C. M. Kam, L. Narasimhan, M. Poe, J. T. Blake, O. Krahenbuhl, J. Tschopp, and J. C. Powers. 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.
34. Song, Q., S. R. Burrows, G. Smith, S. P. Lees-Miller, S. Kumar, D. W. Chan, J. A. Trapani, E. Alnemri, G. Litwack, H. Lu, D. J. Moss, S. Jackson, and M. F. Lavin. 1996. Interleukin-1β-converting enzyme-like protease cleaves DNA-dependent protein kinase in cytotoxic T cell killing. J. Exp. Med. 184:619.
35. Kam, C. M., J. E. Kerrigan, R. R. Plaskon, E. J. Duffy, P. Lollar, F. L. Suddath, and J. C. Powers. 1994. Mechanism-based isocoumarin inhibitors for blood coagulation serine proteases: effect of the 7-substituent in 7-amino-4-chloro-3-(iosthioueridoalkoxy) isocoumarins on inhibitory and anticoagulant potency. J. Med. Chem. 37:1298.
36. Kam, C. M., M. A. Hernandez, G. S. Patil, T. Ueda, W. H. Simmons, V. J. Braganza, and J. C. Powers. 1995. Mammalian tissue trypsin-like enzymes: substrate specificity and inhibitory potency of substituted isocoumarin mechanism-based inhibitors, benzamidine derivatives, and arginine fluoroalkyl ketone transition-state inhibitors. Arch. Biochem. Biophys. 316:808.
37. Irmler, M., S. Hertig, H. R. MacDonald, R. Sadoul, J. D. Becherer, A. Proudfoot, R. Solari, and J. Tschopp. 1995. Granzyme A is an interleukin 1β-converting enzyme. J. Exp. Med. 181:1917.
38. Bernard, K. N., N. Auphan, S. Gajeaud, G. Victorero, A. M. Schmitt-Verhulst, B. R. Jordan, and C. Nguyen. 1996. Multiplex messenger assay: simultaneous quantitative measurement of expression for many genes in the context of T cell activation. Nucleic Acids Res. 24:1435.
39. + cytotoxic T lymphocyte clones. Eur. J. Immunol. 25:3381.
40. Nagata, S., and P. Golstein. 1995. The Fas death factor. Science 267:1449.
41. Isaaz, S., K. Baetz, K. Olsen, E. Podack, and G. M. Griffiths. 1995. Serial killing by cytotoxic T lymphocytes: T cell receptor triggers degranulation, re-filling of the lytic granules and secretion of lytic proteins via a non-granule pathway. Eur. J. Immunol. 25:1071.
42. Kolesnick, R., and D. W. Golde. 1994. The sphingomyelin pathway in tumor necrosis factor and interleukin-1 signaling. Cell 77:325.
43. Tepper, C. G., S. Jayadev, B. Liu, A. Bielawska, R. Wolff, S. Yonehara, Y. A. Hannun, and M. F. Seldin. 1995. Role of ceramide as an endogenous nediator of Fas-induced cytotoxicity. Proc. Natl. Acad. Sci. USA 92:8443.
44. Darmon, A. J., T. J. Ley, D. W. Nicholson, and C. R. 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.
45. Muzio, M., A. M. Chinnayian, 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.
46. 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.
47. 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.
48. 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.
49. 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.
50. Cifone, M. G., R. De Maria, P. Roncaioli, M. R. Rippo, M. Azuma, L. L. Lanier, A. Santoni, and R. Testi. 1994. Apoptotic signaling through CD95 (Fas/Apo-1) activates an acidic sphingomyelinase. J. Exp. Med. 177:1547.
51. Chinnayian, A. M., C. G. Tepper, M. F. Seldin, K. O'Rourke, F. C. Kischkel, S. Hellbard, P. H. Krammer, M. E. Peter, and V. M. Dixit. 1996. FADD/MORT1 is a common mediator of CD95 (Fas/APO1) and tumor necrosis factor receptor-induced apoptosis. J. Biol. Chem. 271:4961.
52. Williams, M. S., and P. A. Henkart. 1994. Apoptotic cell death induced by intracellular proteolysis. J. Immunol. 153:4247.
53. 2+ is mediated by the activation of a non-lysosomal proteolytic system. FEBS Lett. 209:139.