Granzymes: A variety of serine protease specificities encoded by genetically distinct subfamilies

Journal of Leukocyte Biology

Volumn 60, Issue 5, 1996, Pages 555-562

  Smyth, Mark J ^a   O'Connor, Michael D ^a   Trapani, Joseph A ^a  

^a AUSTIN RESEARCH INSTITUTE   (Australia)

Author keywords

Apoptosis; Cytotoxic lymphocytes; Gene structure; Perforin; Serpin

Indexed keywords

GRANZYME; PERFORIN; SERINE PROTEINASE INHIBITOR; UNCLASSIFIED DRUG;

APOPTOSIS; CYTOTOXIC T LYMPHOCYTE; GENE STRUCTURE; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW;

POX VIRUS;

EID: 0029838802     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1002/jlb.60.5.555     Document Type: Review

References (107)

1. Trinichieri, G., Perussia, B. (1984) Human natural killer cells. Biologic and pathologic aspects. Lab. Invest. 50, 489-513.
2. Doherty, P. C. (1993) Cell-mediated cytotoxicity. Cell 75, 607-612.
3. Kupfer, A. (1991) T-cell effector functions: mechanisms for delivery of cytotoxicity and help. Arum. Rev. Cell Biol. 7, 479-504.
4. Peters, P. J., Geuze, H. J., Ban der Donk, H. A., Borst, J. (1990) A new model for lethal hit delivery by cytotoxic T lymphocytes. Immunol. Today 11, 28-32.
5. Young, J. D-E., Cohn, Z. A. (1986) Cell-mediated killing: a common mechanism? Cell 46, 641-642.
6. Kagi, D., Ledermann, B., Burki, K., Seiler, P., Odermatt, B., Olsen, K. J., Podack, E. R., Zinkernagel, R. M., Hengartner, H. (1994) Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforindeficient mice. Nature 369, 31-37.
7. Lowin, B., Beermann, F., Schmidt, A., Tschopp, J. (1994) A null mutation in the perform gene impairs cytolytic T lymphocyte- and natural killer cell-mediated cytoxicity. Proc. Natl. Acad. Sci. USA 91, 11571-11575.
8. Talento, A., Nguyen, M., Law, S., Wu, J. K., Poe, M., Blake, J. T., Patel, M., Wu, T-J., Manyak, C. L., Silberklang, M., Mark, G., Springer, M., Sigal, N. H., Weissman, I. L., Bleackley, R. C., Podack, E. R., Tykocinski, M. L., Koo, G.C. (1992) Transfection of mouse cytotoxic T lymphocytes with an antisense granzyme A vector reduces lytic activity. J. Immunol. 149, 4009-4015.
9. Burkhardt, J. K., Hester, S., Lapham, C. K., Argon, Y. (1990) The lytic granules of natural killer cells are dual-function organelles combining secretory and pre-lysosomal compartments. J. Cell Biol. 11, 2327-2340.
10. Peters, P. J., Geuze, H. J., Van der Donk, H. A., Slot, J. W., Griffith, J. M., Stam, N. J., Clevers, H. C., Borst, J. (1989) Molecules relevant for T cell-target cell interaction are present in cytolytic granules of human T lymphocytes. Eur. J. Immunol. 19, 1469-1475.
11. Jenne, D. E., Tschopp, J. (1988) Granzymes, a family of serine proteases released from granules of cytolytic T lymphocytes upon T cell receptor stimulation. Immunol. Rev. 103, 53-71.
12. Bleackley, R. C., Lobe, C. C., Duggan, B., Ehrman, N., Fregeau, C., Meier, M., Letellier, M., Havele, C., Shaw, J., Paetkau, V. (1988) The isolation and characterization of a family of serine protease genes expressed in activated cytotonic T lymphocytes. Immunol. Rev. 103, 5-19.
13. Masson, D., Tschopp, J. (1985) Isolation of a lytic pore-forming protein (perforin) from cytolytic T lymphocytes. J. Biol. Chem. 260, 9069-9072.
14. Young, J. D-E., Hengartner, H., Podack, E. R., Cohn, Z. A. (1986) Purification and characterization of a cytolytic pore-forming protein from granules of cloned lymphocytes with natural killer activity. Cell 44, 849-859.
15. Muller-Eberhard, H. J. (1986) The membrane attack complex of complement. Annu. Rev. Immunol. 4, 503-528.
16. Tschopp, J., Schafer, S., Masson, D., Peitsch, M. C., Heusser, C. (1989) Phosphorylcholine acts as a calcium dependent receptor molecule for lymphocyte perforin. Nature 337, 272-274.
17. Liu, C-C., Walsh, C. M., Young, J. D-E. (1995) Perforin: structure and function. Immunol. Today 16, 194-201.
18. Henkart, P. A., Berrebi, G. A., Takayama, H., Munger, W. E., Sitkovsky, M. B. (1987) Biochemical and functional properties of serine esterases in acidic cytoplasmic granules of cytotoxic T lymphocytes. J. Immunol. 139, 2398-2405.
19. Jenne, D. E., Masson, D., Zimmer, M., Haefliger, J-A., Li, W-H., Tschopp, J. (1989) Isolation and complete structure of the lymphocyte serine protease granzyme G, a novel member of the granzyme multigene family in murine cytolytic T lymphocytes. Evolutionary origin of lymphocyte proteases. Biochemistry 28, 7953-7961.
20. Odake, S., Kam, C-M., Narasimhan, L., Poe, M., Blake, J. T., Krahenbuhl, O., Tschopp, J., 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 isocumarins. Biochemistry 30, 2217-2227.
21. Chang, T. W., Eisen, H. N. (1980) Effects of N-tosyl-L-lysyl-chloromethylketone on the activity of cytotoxic T lymphocytes. J. Immunol. 124, 1028-1033.
22. Woodard, S. L., Jackson, D. S., Abuelyaman, A. S., Powers, J. C., Winkler, U., Hudig, D. (1994) Chymase-directed serine protease inhibitor that reacts with a single 30 kDa granzyme and blocks NK-mediated cytotoxicity. J. Immunol. 153, 5016-5025.
23. Smyth, M. J., Trapani, J. A. (1995) Granzymes: exogenous proteinases that induce target cell apoptosis. Immunol. Today 19, 202-206.
24. Haddad, P., Jenne, D., Tschopp, J., Clement, M-V., Mathieu-Mahul, D., Sasportes, M. (1990) Structure and evolutionary origin of the human granzyme H gene. Int. Immunol. 3, 57-66.
25. Caputo, A., Garner, R. S., Winkler, U., Hudig, D., Bleackley, R. C. (1993) Activation of recombinant murine cytotoxic cell proteinase-1 requires deletion of an amino-terminal dipeptide. J. Biol. Chem. 268, 17672-17675.
26. McGuire, M. J., Lipsky, P. E., Thiele, D. L. (1993) Generation of active myeloid and lymphoid granule serine proteases requires processing by the granule thiol protease dipeptidyl peptidase I. J. Biol. Chem. 268, 2458-2467.
27. von Heijne, G. (1986) A new method for prediction signal sequence cleavage sites. Nucleic Acids Res. 14, 4683-4690.
28. Smyth, M. J., McGuire, M.J., Thia, K. Y. T. (1995) Expression of recombinant human granzyme B: a processing and activation role for dipeptidyl peptidase I. J. Immunol. 154, 6299-6305.
29. Smyth, M. J., Sayers, T. J., Wiltrout, T., Powers, J. C., Trapani, J. A. (1993) Met-ase: Cloning and distinct chromosomal location of a serine protease preferentially expressed in human natural killer cells. J Immunol. 151, 1-11.
30. Griffiths, G. M., Isaaz, S. (1993) Granzymes A and B are targeted to the lytic granules of lymphocytes by the mannose-6-phosphate receptor. J. Cell Biol. 120, 885-896.
31. Alberts, B., Bray, D., Lewis, J., Raff, M., Roberts, K., Watson, J. D. (1989) Molecular Biology of the Cell (R. Adams, A. Walker, eds.), New York, Garland 446-455.
32. Masson, D., Peters, P. J., Geuze, H. J., Borst, J., Tschopp, J. (1990) Interaction of chondroitin sulfate with perforin and granzymes of cytolytic T-cells is dependent on pH. Biochemistry 29, 11229-11235.
33. Pfeffer, S., R. (1988) Mannose-6-phosphate receptors and their role in targeting proteins to lysosomes. J. Memb. Biol. 103, 7-16.
34. Orci, L., Ravazolla, M., Amherdt, M., Madsen, O., Perrelet, A., Vassalli, J.-D., Anderson, R. G. W. (1986) Conversion of proinsulin to insulin occurs coordinately with acidification of maturing secretory vesicles. J. Cell Biol. 103, 2273-2281.
35. Branden, C., Tooze, J. (1991) Introduction to Protein Structure New York, Garland, 231-246.
36. McMurry, J. (1988) Organic Chemistry (S. Ewing, L. McCloud, H. Wieland, eds.), Belmont, Brooks/Cole, 970-1008.
37. Kraut, J. (1977) Serine proteases: Structure and mechanism of catalysis. Annu. Rev. Biochem. 46, 331-358.
38. Murphy, M. E. P., Moult, J., Bleackley, R. C., Gershenfeld, H., Weissman, I. L., James, M. N. G. (1988) Comparative molecular model building of two serine proteinases from cytotoxic T lymphocytes. Proteins Struct. Funct. Genet. 4, 190-204.
39. Salvesen, G., Farley, D., Shuman, J., Przybyla, A., Reilly, C., Travis, J. (1987) Molecular cloning of human cathepsin G: structural similarity to mast cell and cytotoxic T lymphocyte proteinases. Biochemistry 26, 2289-2293.
40. Trong, H. L., Parmelee, D. C., Walsh, K. A., Neurath, H., Woodbury, R. G. (1987) Amino acid sequence of rat mast cell protease I (chymase). Biochemistry 26, 6988-6994.
41. Woodbury, R. G., Katunuma, N., Kobayashi, K., Titani, K., Neurath, H. (1978) Covalent structure of a group-specific protease from rat small intestine. Biochemistry 17, 811-820.
42. Harper, J. W., Cook, R. R., Roberts, J., McLaughlin, B. J., Powers, J. C. (1984) Active site mapping of the serine proteases human leukocyte elastase, cathepsin G, porcine pancreatic elastase, rat mast cell proteases I and II, bovine chymotrypsin A, and Staphylococcus aureus protease V-8 using tripeptide thiobenzyl ester substrates. Biochemistry 23, 2995-3002.
43. Odake, S., Kam, C-M., Narasimhan, L., Poe, M., Blake, J. T., Krahenbuhl, O., Tschopp, J., 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.
44. Fink, T. M., Lichter, P., Wekerle, H., Zimmer, M., Jenne, D. E. (1993) The human granzyme A (HFSP, CTLA3) gene maps to 5q11-q12 and defines a new locus of the serine protease superfamily. Genomics 18, 401-403.
45. Baker, E., Sayers, T. J., Sutherland, G. R., Smyth, M. J. (1994) The genes encoding NK cell granule serine proteases, human Tryptase-2 (TRYP2) and human granzyme A (HFSP), both map to chromosome 5q11-q12 and define a new locus for cytotoxic lymphocyte granule tryptases. Immunogenetics 40, 235-237.
46. Harper, K., Mattei, M-G., Simon, D., Suzan, M., Guenet, J-L., Haddad, P., Sasportes, M., Golstein, P. (1988) Proximity of the CTLA-1 serine esterase and Tcr alpha loci in mouse and man. Immunogenetics 28, 439-444.
47. Hanson, R. D., Hohn, P. A., Popescu, N. C., Ley, T. J. (1990) A cluster of hematopoietic serine protease genes is found on the same chromosomal band as the human α/δ T-cell receptor locus. Proc. Natl. Acad. Sci. USA 87, 960-963.
48. Baker, E., Sutherland, G. R., Smyth, M. J. (1994) The gene encoding a human natural killer cell granule serine protease, Met-ase 1, maps to chromosome 19p13.3. Immunogenetics 39, 294-295.
49. Pilat, D., Fink, T., Obermaier-Skrobanek, B., Zimmer, M., Wekerle, H., Lichter, P., Jenne, D. E. (1994) The human Met-ase gene (GZMM): structure, sequence, and close physical linkage to the serine protease gene cluster on 19p13.3. Genomics 24, 445-450.
50. Mattei, M. G., Harper, K., Brunet, J. F., Denizot, F., Mattei, J. F., Golstein, P., Giraud, F. (1987) In situ mapping of four cytotoxic T-lymphocyte associated proteins (CTLA) to the mouse genome. Cytogenet. Cell Genet. 46, 657-658.
51. Crosby, J. L., Bleackley, R. C., Nadeau, J. H. (1990) A complex of serine protease genes expressed preferentially in cytotoxic T-lymphocytes is closely linked to the T-cell receptor α- and δ-chain genes on mouse chromosome 14. Genomics 6, 252-259.
52. + T cells. J. Immunol. 147, 1045-1052.
53. Thia, K. Y. T., Jenkins, N. A., Gilbert, D. J., Copeland, N. G., Smyth, M. J. (1995) The gene encoding a mouse natural killer cell granule serine protease, Met-ase 1, maps to mouse chromosome 10q21.2. Immunogenetics 41, 47-49.
54. Irwin, D. M., Robertson, K. A., MacGillivray, R. T. (1988) Structure and evolution of the bovine prothrombin gene. J. Mol. Biol. 200, 31-45.
55. Hershberger, R. J., Gershenfeld, H. K., Weissman, I. L., Su, L. (1992) Genomic organization of the mouse granzyme A gene. Two mRNAs encode the same mature granzyme A with different leader peptides. J. Biol. Chem. 267, 25488-25493.
56. Lobe, C. G., Upton, C., Duggan, B., Ehrman, N., Letellier, M., Bell, J., Bleackley, R. C. (1988) Organization of two genes encoding murine cytotoxic T-lymphocyte-specific serine proteases CCPI and CCPII. Biochemistry 27, 6941-6946.
57. Klein, J. L., Shows, T. B., Dupont, B., Trapani, J. A. (1989) Genomic organization and chromosomal assignment for a serine protease gene (CSPB) expressed by human cytotoxic lymphocytes. Genomics 5, 110-117.
58. Smyth, M. J., Hulett, M. D., Thia, K. Y. T., Sayers, T. J., Carter, C. R. D., Young, H. A., Trapani, J. A. (1995) Cloning and characterization of a novel NK-cell specific serine protease gene and its functional 5′-flanking sequences. Immunogenetics 42, 101-111.
59. Kelly, J. M., Hulett, M. D., Thia, K. Y. T., O'Connor, M. D., Smyth, M. J. (1996) Cloning, characterization, and expression of mouse natural killer cell Met-ase. Immunogenetics, in press.
60. Zimmer, M., Medcalf, R. L., Fink, T. M., Mattmann, C., Lichter, P., Jenne, D. E. (1992) Three human elastase-like genes coordinately expressed in the myelomonocytic lineage are organized as a single genetic locus on 19pter. Proc. Natl. Acad. Sci. USA 89, 8215-8219.
61. Sayers, T. J., Wiltrout, T. A., Smyth, M. J., Ottaway, K. S., Pilaro, A. M., Sowder, R., Henderson, L. E., Sprenger, H., Lloyd, A. R. (1994) Purification and cloning of a novel serine protease, RNK-Tryp-2, from the granules of a rat NK cell leukemia. J. Immunol. 152, 2289-2297.
62. Smyth, M. J., Wiltrout, T., Trapani, J. A., Ottaway, K. S., Sowder, R., Henderson, L., Powers, J., Sayers, T. J. (1992) Purification and cloning of a novel serine protease, RNK-Met-1, from the granules of a rat natural killer cell leukemia. J. Biol. Chem. 267, 24418-24425.
63. Smyth, M. J., O'Connor, M. D., Trapani, J. A., Kershaw, M. H., Brinkworth, R. (1996) A novel substrate binding pocket interaction restricts the specificity of the human natural killer cell-specific serine protease, Met-ase-1. J. Immunol. 156: 4174-4181.
64. Caputo, A., James, M. N. G., Powers, J. C., Hudig, D., Bleackley, R. C. (1995) Conversion of the substrate specificity of mouse proteinase granzyme B. Nature Struct. Biol. 1, 364-367.
65. Hudig, D., Allison, N. J., Pickett, T. M., Winkler, U., Kam, C-M., Powers, J. C. (1991) The function of lymphocyte proteases. Inhibition and restoration of granule-mediated lysis with isocoumarin serine protease inhibitors. J. Immunol. 147, 1360-1368.
66. Shi, L., Kam, C-M., Powers, J. C., Aebersold, R., 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.
67. Russell, J. H. (1983) Internal disintegration model of cytotoxic lymphocyte-induced target damage. Immunol. Rev. 72, 97-118.
68. Trapani, J. A., Smyth, M. J. (1993) Killing by cytotoxic T cells and NK cells: multiple granule serine proteases as initiators of DNA fragmentation. Immunol. Cell Biol. 71, 201-208.
69. Shi, L., Kraut, R. P., Aebersold, R., Greenberg, A. H. (1992) A natural killer cell granule protein that induces DNA fragmentation and apoptosis. J. Exp. Med. 175, 553-566.
70. Hayes, M. P., Berrebi, G. A., Henkart, P. A. (1989) Induction of target cell DNA release by the cytotoxic T lymphocyte granule protease granzyme A. J. Exp. Med. 170, 933-946.
71. Shiver, J. W., Su, L., Henkart, P. A. (1992) Cytotoxicity with target DNA breakdown by rat basophilic leukemia cells expressing both cytolysin and granzyme A. Cell 71, 315-322.
72. Heusel, J. W., Wesselschmidt, R. L., Shresta, S., Russell, J. H., 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.
73. Shi, L., Nishioka, W. K., Th'ng, J., Bradbury, E. M., Litchfield, D. W., Greenberg, A. H. (1994) Premature p34 cdc2 activation required for apoptosis. Science 263, 1143-1145.
74. Vaux, D. L., Haecker, G., Strasser, A. (1994) An evolutionary perspective on apoptosis. Cell 76, 777-779.
75. Yuan, J., Shaham, S., Ledoux, S., Ellis, H. M., Horvitz, H. R. (1993) The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell 75, 641-652.
76. Miura, M., Zhu, H., Rotello, R., Hartweig, E. A., Yuan, J. (1993) Induction of apoptosis in fibroblasts by IL-1 beta-converting enzyme, a mammalian homolog of the C. elegans cell death gene ced-3. Cell 75, 653-660.
77. Sleath, P. R., Hendrickson, R. C., Kronheim, S. R., March, C. J., Black, R. A. (1990) Substrate specificity of the protease that processes human interleukin-1 beta. J. Biol. Chem. 265, 14526-14528.
78. Thornberry, N. A., Bull, H. G., Calaycay, J. R., Chapman, K. T., Howard, A. D., Kostura, M. J., et al. (1992) A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Science 356, 768-774.
79. Darmon, A. J., Ehrman, N., Caputo, A., Fujinaga, J., Bleackley, R. C. (1994) The cytotoxic T cell proteinase granzyme B does not activate interleukin-1β converting enzyme. J. Biol. Chem. 269, 32043-32046.
80. Darmon, A. J., Nicholson, D. W., Bleackley, R.C. (1995) Activation of the apoptotic protease CPP32 by cytotoxic T-cell-derived granzyme B. Nature 377, 446-448.
81. Fernandes-Alnemri, T., Armstrong, R., Krebs, J., Srivasula, S. M., Wang, L., Bullrich, F., Fritz, L., Tomaselli, K. J., Trapani, J. A., Croce, M., Litwack, G., Alnemri, E. S. (1996) Activation of CPP32 and Mch3 by Mch4, a novel human apoptotic cysteine protease and a substrate for granzyme B. Proc. Natl. Acad. Sci. USA, in press.
82. Martin, S. J., Amarante-Mendes, G. P., Shi, L., Chuang, T. H., Casiano, C. A., O'Brien, G. A., Fitzgerald, P., Tan, E. M., Bokoch, G. M., Greenberg, A. H., Green, D. R. (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. Eur. Mol. Biol. Org. J. 15, 2407-2416.
83. Lazebnik, Y. A., Kaufmann, S. H., Desnoyers, S., Poirier, G. G., Earnshaw, W. C. (1994) Cleavage of poly (ADP) ribose polymerase by a proteinase with properties like ICE. Nature 371, 346-347.
84. Kaufmann, S. H. (1989) Induction of endonucleolytic DNA cleavage in human acute myelogenous leukemia cells by etoposide, campothecin, and other cytotoxic anticancer drugs: a cautionary note. Cancer Res. 49, 5870-5878.
85. Kaufmann, S. H., Desnoyers, S., Ottaviano, Y., Davidson, N. E., Poirier, G. G. (1993) Specific proteolytic cleavage of poly (ADP) ribose polymerase: an early marker of chemotherapy induced apoptosis. Cancer Res. 53, 3976-3985.
86. Trapani, J. A., Browne, K. A., Smyth, M. J., 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.
87. Pinkoski, M. J., Winkler, U., Hudig, D., Bleackley, R. C. (1996) Binding of granzyme B in the target cell nucleus: recognition of an 80-kilodalton protein. J. Biol. Chem. 271, 10225-10229.
88. Ebnet, K., Hausmann, M., Lehman-Grube, F., Mullbacher, A., Kopf, M., Lamers, M., Simon, M. M. (1995) Granzyme A-deficient mice retain potent cell-mediated cytotoxicity. Eur. Mol. Biol. Org. J. 14, 4230-4239.
89. Mullbacher, A., Ebnet, K., Blanden, R. V., Hla, R. T., Stehle, T., Museteanu, C., Simon, M. M. (1996) Granzyme A is critical for recovery of mice from infection with the natural cytopathic viral pathogen, ectromelia. Proc. Natl. Acad. Sci. USA 93, 5783-5787.
90. Irmler, M., Hertig, S., MacDonald, H. R., Sadoul, R., Becherer, D., Proudfoot, A., Solari, R., Tschopp, J. (1995) Granzyme A is an interleukin 1 beta converting enzyme. J. Exp. Med. 181, 1917-1922.
91. Simon, M. M., Kramer, M. D., Prester, M., Gay, S. (1991) Mouse T cell associated serine protease I degrades collagen type IV: a structural basis for the migration of lymphocytes through vascular basement membranes. Immunology 73, 117-119.
92. Sayers, T. J., Wiltrout, T. A., Sowder, R., Munger, W. L., Smyth, M. J., Henderson, L. E. (1992) Purification of a factor from the granules of a rat natural killer cell line (RNK) that reduces tumor cell growth and changes tumor morphology. Molecular identity with granule serine protease (RNKP-1). J. Immunol. 148, 292-300.
93. Sower, L., Froelich, C. J., Allegretto, N., Rose, P. M., Hanna, W. D., Klimpel, G. R. (1996) Extracellular activities of human granzyme A. Monocyte activation by granzyme A versus α-thrombin. J. Immunol. 156, 2585-2590.
94. Jenne, D. E., Tschopp, J., Ludemann, J., Utecht, B., Gross, W. L. (1990) Wegner's autoantigen decoded. Nature 346, 520.
95. Porteu, F., Brockhaus, M., Wallach, D., Engelmann, H., Nathan, C. F. (1991) Human neutrophil elastase releases a ligand-binding fragment from the 75-kDa tumor necrosis factor (TNF) receptor. Comparison with the proteolytic activity responsible for shedding of TNF receptors from stimulated neutrophils. J. Biol. Chem. 266, 18846-18853.
96. Pereira, H. A., Shafer, W. M., Pohl, J., Martin, L. E., Spitznagel, J. K. (1990) CAP37, a human neutrophil-derived chemotactic factor with monocyte specific activity J. Clin. Invest. 85, 1468-1476.
97. Neilan, J. G., Lu, Z., Afonso, C. L., Kutish, G. F., Sussman, M. D., Rock, D. L. (1993) An African swine fever virus gene with similarity to the proto-oncogene bcl-2 and the Epstein-Barr virus gene BHRF1. J. Virol. 67, 4391-4394.
98. Debbas, M., White, E. (1993) Wild-type p53 mediates apoptosis by E1A, which is inhibited by E1B. Genes Dev. 7, 546-554.
99. Hashimoto, S., Ishii, A., Yonehara, S. (1991) The E1b oncogene of adenovirus confers cellular resistance to cytotoxicity of tumor necrosis factor and monoclonal anti-Fas antibody. Int. Immunol. 3, 343-351.
100. Tewari, M., Quan, L. T., O'Rourke, K., Desnoyers, S., Zeng, Z., Beidler, D. R., Poirier, C. G., Salvesen, G. S., Dixit, V. M. (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, 801-809.
101. Enari, M., Hug, H., Nagata, S. (1995) Involvement of a ICE-like protease in Fas-mediated apoptosis. Nature 375, 78-81.
102. Xue, D., 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.
103. Quan, L. T., Caputo, A., Bleackley, R. C., Pickup, D. J., Salvesen, G. S. (1995) Granzyme B is inhibited by the cow pox virus cytokine response modifier A. J. Biol. Chem. 270, 10377-10379.
104. Sprecher, C. A., Morgenslern, K. A., Mathewes, S., Dahlen, J. R., Schrader, S. K., Foster, D. C., Kisiel, W. (1995) Molecular cloning, expression and partial characterization of two novel members of the ovalbumin family of serine protease inhibitors. J. Biol. Chem. 270, 29854-29861.
105. Lobe, C. G., Finlay, B. B., Paranchych, W., Paetkau, V. H., Bleackley, R. C. (1986) Novel serine proteinases encoded by two cytotoxic T lymphocyte-specific genes. Science 232, 858-861.
106. Jenne, D., Rey, C., Masson, D., Stanley, K. K., Herz, J., Plaetinck, G. (1988) cDNA cloning of granzyme C, a granule-associated serine protease of cytolytic T lymphocytes. J. Immunol. 140, 318-323.
107. Jenne, D., Rey, C., Haefliger, J. A., Qiao, B. Y., Groscurth, P., Tschopp, J. (1988) Identification and sequencing of cDNA clones encoding the granule-associated serine proteases granzymes D, E, and F of cytolytic T lymphocytes. Proc. Natl. Acad. Sci. USA 85, 4814-4818.