Dual mechanisms of apoptosis induction by cytotoxic lymphocytes

International Review of Cytology

Volumn 182, Issue , 1998, Pages 111-192

  Trapani, Joseph A ^a  

^a AUSTIN RESEARCH INSTITUTE   (Australia)

Author keywords

Apoptosis; Caspase; Cytotoxic lymphocyte; Fas; Granzyme; Perforin

Indexed keywords

CALCIUM ION; CASPASE; CELL ENZYME; FAS ANTIGEN; GRANZYME A; GRANZYME B; PERFORIN; PROTEINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL MEMBRANE; CELL TRANSFORMATION; CHANNEL GATING; CONTROLLED STUDY; CYTOPLASM; CYTOTOXIC T LYMPHOCYTE; EXOCYTOSIS; HUMAN; HUMAN CELL; IMMUNE SYSTEM; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TARGET CELL;

ANIMALIA; VERMES;

EID: 0031899584     PISSN: 00747696     EISSN: None     Source Type: Book Series    
DOI: 10.1016/s0074-7696(08)62169-5     Document Type: Article

References (355)

1. Abdelhaleem, M. M., Hameed, S., Klassen, D., and Greenberg, A. H. (1996). Leukophysin: An RNA helicase a-related molecule identified incytotoxic T cell granules and vesicles. J. Immunol. 156, 2026-2035.
2. Ahmed, K. R., Guo, T. B., and Gaal, K. K. (1997). Islet rejection in perforin-deficient mice: The role of perforin and Fas. Transplantation 63, 951-957.
3. Allbritton, N. L., Verret, C. R., Wolley, R. C., and Eisen, H. N. (1988). Calcium ion concentrations and DNA fragmentation in target cell destruction by murine cloned cytotoxic T lymphocytes. J. Exp. Med. 167, 514-527.
4. Alnemri, E. S., Livingston, D. J., Nicholson, D. W., Salvesen, G., Thornberry, N. A., Wong, W. W., and Yuan, J. (1996). Human ICE/CED-3 protease nomenclature. CellSl, 171. [Letter]
5. Anderson, K. R., Kedersha, N., Tian, Q., and Strueli, M. (1997). The fast track: RNAbinding proteins involved in signaling stress-induced apoptosis. Proc. EMBO Workshop Cell-mediated Cytotoxidty, 6th, Kerkrade, The Netherlands, Abstr., p. 1.
6. Anderson, P., Nagler-Anderson, C., O'Brien, C., Levine, H., Watkins, S., Slayter, H. S., Blue, M. L., and Schlossman, S. F. (1990). A monoclonal antibody reactive with a 150-kDa cytoplasmic granule-associated protein defines a subpopulation of CD8+ T lymphocytes. J. Immunol. 144, 574-582.
7. Ando, K., Hiroishi, K., Kaneko, T., Moriyama, T., Muto, Y., Kayagaki, N., Yagita, H., Okumura, K., and Imawari, M. (1997). Perforin, Fas/Fas ligand, and TNF-alpha pathways as specific and bystander killing mechanisms of hepatitis C virus-specific human CTL. J. Immunol. 158, 5283-5291.
8. Anel, A., Garnen, S., Alava, M. A., Schmitt-Verhulst, A. M., Peneiro, A., and Naval, J. (1997). Inhibition of CPP32-like proteases prevents granzyme B- and Fas-, but not granzyme A-based cytotoxicity exerted by CTL clones. J. Immunol. 158, 1999-2006.
9. Baker, E., Sutherland, G. R., and Smyth, M. J. (1994a). The gene encoding a human natural killer cell granule serine protease, Met-ase 1, maps to chromosome 19pl3.3. Imimmogenetics 39, 294-295.
10. Baker, E., Sayers, T. J., Sutherland, G. R., and Smyth, M. J. (1994b). 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. Imimmogenetics 40, 235-237.
11. Baker, M. B., Riley, R. L., Podack, E. R., and Levy, R. B. (1997). Graft-versus-host-disease-associated lymphoid hypoplasia and B cell dysfunction is dependent upon donor T cell-mediated Fas-ligand function, but not perforin function. Proc. Natl. Acad. Sci. USA 94,1366-1371.
12. Banner, D. W., D'Arcy, A., Janes, W., Gentz, R., Schoenfeld, H. J., Broger, C., Loetscher, H., and Lesslauer, W. (1993). Crystal structure of the soluble human 55 kd TNF receptor-human TNF beta complex: Implications for TNF receptor activation. Cell 73, 431-445.
13. Beidler, D. R., Tewari, M., Friesen, P. D., Poirier, G., and Dixit, V. M. (1995). The baculovirus p35 protein inhibits Fas- and tumor necrosis factor- induced apoptosis. J. Biol. Chem. 270, 16526-16528.
14. Berke, G. (1989). The cytolytic Tlymphocyte and its mode of action. Immtmol Lett. 20,169-178.
15. Berke, G. (1991). Debate: The mechanism of lymphocyte-mediated killing. Lymphocyte-triggered internal target disintegration. Immunol. Today 12, 396-399; discussion, p. 402.
16. Berke, G., and Rosen, D. (1988). Highly lytic in vivo primed cytolytic T lymphocytes devoid of lytic granules and BLT-esterase activity acquire these constituents in the presence of T cell growth factors upon blast transformation in vitro. J. Immunol. 141, 1429-1436.
17. Berthou, C., Marolleau, J. P., Lafaurie, C., Soulie, A., Dal Cortivo, L., Bourge, J. F., Benbunan, M., and Sasportes, M. (1995). Granzyme B and perforin lytic proteins are expressed in CD34+ peripheral blood progenitor cells mobilized by chemotherapy and granulocyte colony-stimulating factor. Blood 86, 3500-3506.
18. Bertin, J., Armstrong, R. C., Ottilie, S., Martin, D. A., Wang, Y., Banks, S., Wang, G. H., Senkevich, T. G., Alnemri, E. S., Moss, B., Lenardo, M. J., Tomaselli, K. J., and Cohen, J. I. (1997). A novel family of viral death effector domain containing molecules that inhibit both CD95- and tumor necrosis factor receptor-1-induced apoptosis. J. Biol. Chem. 272, 9621-9624.
19. Bird, C., Sutton, V. R., Trapani, J. A., and Bird, P. I. (1998). In preparation.
20. Blakely, A., German, K., Ostergaard, H., Svoboda, K., Liu, C. C., Young, J. D., and Clark, W. R. (1987). Resistance of cloned cytotoxic T lymphocytes to cell-mediated cytotoxicity. J. Exp. Med. 166, 1070-1083.
21. Bleackley, R. C., Lobe, C. G., Duggan, B., Ehrman, N., Fregeau, C., Meier, M., Letellier, M., Havele, C., Shaw, J., and Paetkau, V. (1988). The isolation and characterization of a family of serine protease genes expressed in activated cytotoxic T lymphocytes. Imimmol. Rev. 103, 5-19.
22. Bleackley, R. C., Atkinson, E. A., Burns, K., and Michalak, M. (1995). Calreticulin: A granuleprotein by default or design? Ctirr. Top. Microbiol. Immunol. 198, 145-159.
23. Bode, W., Meyer, E., Jr., and Powers, J. C. (1989). Human leukocyte and porcine pancreatic elastase: X-ray crystal structures, mechanism, substrate specificity, and mechanism-based inhibitors. Biochemistry 28, 1951-1963.
24. Boldin, M. P., Varfolomeev, E. E., Pancer, Z., Melt, I. L., Camonis, J. H., and Wallach, D. (1995). A novel protein that interacts with the death domain of Fas/APOl contains a sequence motif related to the death domain. J. Biol. Chem. 270, 7795-7798.
25. Boldin, M. P., Goncharov, T. M., Goltsev, Y. V., and Wallach, D. (1996). Involvement of MACH, a novel MORTl/FADD-interacting protease, in Fas/APO-1- and TNF receptorinduced cell death. Cell 85, 803-815.
26. Borregaard, N., Heiple, J. M., Simons, E. R., and Clark, R. A. (1983). Subcellular localization of the b-cytochrome component of the human neutrophil microbicidal oxidase: Translocation during activation. J. Cell Biol. 97, 52-61.
27. Braun, M. Y., Lowin, B., French, L., Acha-Orbea, H., and Tschopp, J. (1996). Cytotoxic T cells deficient in both functional fas ligand and perforin show residual cytolytic activity yet lose their capacity to induce lethal acute graft-versus-host disease. J. Exp. Med. 183,657-661.
28. Brooks, M. A., Ali, A. N., Turner, P. C., and Moyer, R. W. (1995). A rabbitpox virus serpin gene controls host range by inhibiting apoptosis in restrictive cells. J. Virol. 69,7688-7698.
29. Brown, G. R., McGuire, M. J., and Thiele, D. L. (1993). Dipeptidyl peptidase I is enriched in granules of in vitro- and in vivo-activated cytotoxic T lymphocytes. J. Immunol. ISO, 47334742.
30. Brunei, J. F., Dosseto, M., Denizot, F., Mattei, M. G., Clark, W. R., Haqqi, T. M., Ferrier, P., Nabholz, M., Schmitt-Verhulst, A. M., Luciani, M. F., et al. (19S6). The inducible cytotoxic T-lymphocyte-associated gene transcript CTLA-1 sequence and gene localization to mouse chromosome 14. Nature 322, 268-271.
31. Brunner, G., Simon, M. M., and Kramer, M. D. (1990). Activation of pro-urokinase by the human T cell-associated serine proteinase HuTSP-1. FEES Lett. 260, 141-144.
32. Bump, N. J., Hackett, M., Hugunin, M., Seshagiri, S., Brady, K., Chen, P., Ferenz, C., Franklin, S., Ghayur, T., Li, P., et al. (1995). Inhibition of ICE family proteases by baculovirus antiapoptotic protein p35. Science 269, 1885-1888.
33. Burkhardt, J. K., Hester, S., Lapham, C. K., and Argon, Y. (1990). The lytic granules of natural killer cells are dual-function organelles combining secretory and pre-lysosomal compartments. J. Cell Biol. Ill, 2327-2340.
34. Burns, K., Helgason, C. D., Bleackley, R. C., and Michalak, M. (1992). Calreticulin in T lymphocytes: Identification of calreticulin in T lymphocytes and demonstration that activation of T cells correlates with increased levels of calreticulin mRNA and protein. J. Biol. Chem. 267,19039-19042.
35. Bykovskaja, S. N., Rytenko, A. N., Rauschenbach, M. O., and Bykovsky, A. F. (1978). Ultrastructural alteration of cytolytic T lymphocytes following their interaction with target cells. II. Morphogenesis of secretory granules and intracellular vacuoles. Cell. Immunol. 40, 175-185.
36. Caputo, A., Garner, R. S., Winkler, U., Hudig, D., and 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.
37. Caputo, A., James, M. N., Powers, J. C., Hudig, D., and Bleackley, R. C. (1994). Conversion of the substrate specificity of mouse proteinase granzyme B. Nat. Struct. Biol. 1, 364-367.
38. Casciola-Rosen, L. A., Anhalt, G. J., and Rosen, A. (1995). DNA-dependent protein kinase is one of a subset of autoantigens specifically cleaved early during apoptosis. J. Exp. Med. 182, 1625-1634.
39. Casciola-Rosen, L., Nicholson, D. W., Chong, T., Rowan, K. R., Thornberry, N. A., Miller, D. K., and Rosen, A. (1996). Apopain/CPP32 cleaves proteins that are essential for cellular repair: A fundamental principle of apoptotic death [see comments]. J. Exp. Med. 183,1957-1964.
40. Cerretti, D. P., Kozlosky, C. J., Mosley, B., Nelson, N., Van Ness, K., Greenstreet, T. A., March, C. J., Kronheim, S. R., Druck, T., Cannizzaro, L. A., et ai. (1992). Molecular cloning of the interleukin-l beta converting enzyme. Science 256, 97-100.
41. Chang, T. W., and Eisen, H. N. (1980). Effects of N alpha-tosyl-L-lysyl-chloromethylketone on the activity of cytotoxic T lymphocytes. J. Immunol. 124, 1028-1033.
42. Chen, G., Shi, L., Litchfield, D. W., and Greenberg, A. H. (1995). Rescue from granzyme B-induced apoptosis by Wee 1 kinase. J. Exp. Med. 181, 2295-2300.
43. Chen, R. H., Ivens, K. W., Alpert, S., Billingham, M. E., Fathman, C. G., Flavin, T. F., Shizuru, J. A., Starnes, V. A., Weissman, I. L., and Griffiths, G. M. (1993). The use of granzyme A as a marker of heart transplant rejection in cyclosporine or anti-CD4 monoclonal antibodytreated rats. Transplantation 55, 146-153.
44. Cheng, E. H., Nicholas, J., Bellows, D. S., Hayward, G. S., Guo, H. G., Reitz, M. S., and Hardwick, J. M. (1997). A Bcl-2 homolog encoded by Kaposi sarcoma-associated virus, human herpesvirus 8, inhibits apoptosis but does not hcterodimerize with Bax or Bak. Proc. Natl. Acad. Sci. USA 94, 690-694.
45. Chinnaiyan, A. M., O'Rourke, K., Tewari, M., and Dixit, V. M. (1995). FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell 81, 505-512.
46. Chinnaiyan, A. M., Tepper, C. G., Scidin, M. F., O'Rourke, K., Kischkel, F. C., Hellbardt, S., Krammer, P. H., Peter, M. E., and Dixit, V. M. (1996). FADD/MORT1 is a common mediator of CD95 (Fas/APO-1) and tumor necrosis factor receptor-induced apoptosis. J. Biol. Chem. 271, 4961-4965.
47. Chinnaiyan, A. M., O'Rourke, K., Lane, B. R., and Dixit, V. M. (1997). Interaction of CED-4 with CED-3 and CED-9: A molecular framework for cell death. Science 275,1122-1126.
48. Chiu, V. K., Walsh, C. M., Liu, C. C., Reed, J. C., and Clark, W. R. (1995). Bcl-2 blocks degranulation but not fas-based cell-mediated cytotoxicity. J. Immunol. 154, 2023-2032.
49. Clem, R. J., and Miller, L. K. (1993). Apoptosis reduces both the in vitro replication and the in vivo infectivity of a baculovirus. J. Virol. 67, 3730-3738.
50. Clem, R. J., and Miller, L. K. (1994). Control of programmed cell death by the baculovirus genes p35 and iap. Mol. Cell. Biol. 14, 5212-5222.
51. Clem, R. J., Fechheimer, M., and Miller, L. K. (1991). Prevention of apoptosis by a baculovirus gene during infection of insect cells. Science 254, 1388-1390.
52. Clement, M. V., Haddad, P., Ring, G. H., Pruna, A., and Sasportes, M. (1990). Granzyme B-gene expression: A marker of human lymphocytes "activated" in vitro or in renal allografts. Hum. Immunol. 28,159-166.
53. Clement, M. V., Haddad, P., Soulie, A., Benvenuti, C., Lichtenheld, M. G., Podack, E. R., Sigaux, N., and Sasportes, M. (1991). Perform and granzyme B as markers for acute rejection in heart transplantation. Int. Immunol. 3, 1175-1181.
54. Cleveland, J. L., and Ihle, J. N. (1995). Contenders in FasL/TNF death signaling. Cell 81, 479-482.
55. Cory, S. (1995). Regulation of lymphocyte survival by the bcl-2 gene family. Annu. Rev. Immunol. 13, 513-543.
56. Ishikawa, H., Shinkai, Y., Yagita, H., Vue, C. C., Henkart, P. A., Sawada, S., Young, H. A., Reynolds, C. W., and Okumura, K. (1989). Molecular cloning of rat cytolysin. J. Immwiol. 143, 3069-3073.
57. Itoh, N., and Nagata, S. (1993). A novel protein domain required for apoptosis. Mutational analysis of human Fas antigen. J. Biol. Chem. 268, 10932-10937.
58. Jacobson, M. D., Burne, J. F., and Raff, M. C. (1994). Programmed cell death and Bcl-2 protection in the absence of a nucleus. EMBO J. 13, 1899-1910.
59. Janicke, R. U., Walker, P. A., Lin, X. Y., and Porter, A. G. (1996). Specific cleavage of the retinoblastoma protein by an ICE-like protease in apoptosis. EMBO J. 15, 6969-6978.
60. Jans, D. A., Ackermann, M. J., Bischoff, J. R., Beach, D. H., and Peters, R. (1991). p34cdc2-mediated phosphorylation at T124 inhibits nuclear import of SV-40 T antigen proteins. J. Cell Biol. 115, 1203-1212.
61. Jans, D. A., Jans, P., Briggs, L. J., Sutton, V., and Trapani, J. A. (1996). Nuclear transport of granzyme B (fragmentin-2). Dependence of perform in vivo and cytosolic factors in vitro. J. Biol. Chem. 271, 30781-38789.
62. Jans, D. A., Briggs, L. J., Sutton, V., Froelich, C. J., and Trapani, J. (Submitted).
63. Jenne, D. E., and 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.
64. Jenne, D., Rey, C., Haefliger, J. A., Qiao, B. Y., Groscurth, P., and Tschopp, J. (1988a). 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.
65. Jenne, D., Rey, C., Masson, D., Stanley, K. K., Herz, J., Plaetinck, G., and Tschopp, J. (1988b). cDNA cloning of granzyme C., a granule-associated serine protease of cytolytic T lymphocytes. J. Immunol. 140, 318-323.
66. Jenne, D. E., Masson, D., Zimmer, M., Haefliger, J. A., Li, W. H., and 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.
67. Jenne, D. E., Zimmer, M., Garcia-Sanz, J. A., Tschopp, J., and Lichter, P. (1991). Genomic organization and subchromosomal in situ localization of the murine granzyme F, a serine protease expressed in CD8+ T cells. J. Immunol. 147,1045-1052.
68. Jiang, S. B., Persechini, P. M., Zychlinsky, A., Liu, C. C., Perussia, B., and Young, J. D. (1988). Resistance of cytolytic lymphocytes to perforin-mediated killing. Lack of correlation with complement-associated homologous species restriction. J. Exp. Med. 168,2207-2219.
69. Jongstra, J., Schall, T. J., Dyer, B. J., Clayberger, C., Jorgensen, J., Davis, M. M., and Krensky, A. M. (1987). The isolation and sequence of a novel gene from a human functional T cell line. J. Exp. Med. 165, 601-614.
70. Ju, S. T., Cui, H., Panka, D. J., Ettinger, R., and Marshak-Rothstein, A. (1994). Participation of target Fas protein in apoptosis pathway induced by CD4+ Thl and CD8+ cytotoxic T cells. Proc. Natl. Acad. Sci. USA 91, 4185-4189.
71. Kagi, D., Ledermann, B., Burki, K., Sciler, P., Odermatt, B., Olsen, K. J., Podack, E. R., Zinkernagel, R. M., and Hengartner, H. (1994a). Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 369, 31-37.
72. Kagi, D., Ledermann, B., Burki, K., Hengartner, H., and Zinkernagel, R. M. (1994b). CD8+ T cell-mediated protection against an intracellular bacterium by perforin-dependent cytotoxicity. EUT. J. Immunol. 24, 3068-3072.
73. Kagi, D., Sciler, P., Pavlovic, J., Ledermann, B., Burki, K., Zinkernagel, R. M., and Hengartner, H. (1995). The roles of perform- and Fas-dependent cytotoxicity in protection against cytopathic and noncytopathic viruses. Eur. J. Immunol. 25, 3256-3262.
74. Kagi, D., Odermatt, B., Ohashi, P. S., Zinkernagel, R. M., and Hengartner, H. (1996). Development of insulitis without diabetes in transgenic mice lacking perforin dependent cytotoxicity. J. Exp. Med. 183, 2143-2152.
75. Karre, K. (1997). How to recognize a foreign submarine. Immunol. Rev. 155, 5-9.
76. Karre, K., Ljunggren, H. G., Piontek, G., and Kiessling, R. (1986). Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 319, 675-678.
77. Kataoka, K., Naomoto, Y., Shiozaki, S., Matsuno, T., Sakagami, K., Okumura, K., and Orita, K. (1992). Infiltration of perforin-positive mononuclear cells into the rejected kidney allograft. Transplantation 53, 240-242.
78. Kaufmann, S. H. (1989). Induction of endonucleolytic DNA cleavage in human acute myelogenous leukemia cells by etoposide, camptothecin, and other cytotoxic anticancer drugs: A cautionary note. Cancer Res. 49, 5870-5878.
79. Kaufmann, S. H., Desnoyers, S., Ottaviano, Y., Davidson, N. E., and Poirier, G. G. (1993). Specific proteolytic cleavage of poly(ADP-ribose) polymerase: An early marker of chemotherapy-induced apoptosis. Cancer Res. 53, 3976-3985.
80. Kawakami, A., Tian, Q., Duan, X., Streuli, M., Schlossman, S. F., and Anderson, P. (1992). Identification and functional characterization of a TIA-1-related nucleolysin. Proc. Natl. Acad. Sci. USA 89, 8681-8685.
81. Kayalar, C., Ord, T., Testa, M. P., Zhong, L. T., and Bredesen, D. E. (1996). Cleavage of actin by interleukin 1 beta-converting enzyme to reverse DNase I inhibition. Proc. Natl. Acad. Sci. USA 93, 2234-2238.
82. Kelly, J. M., O'Connor, M. D., Hulett, M. D., Thia, K. Y. T., and Smyth, M. J. (1996). Cloning and expression of the recombinant mouse natural killer cell granzyme Met-ase-1. Immiinogenetics 44, 340-350.
83. Kischkel, F. C., Peter, M. E., Medema, J. P., Scaffidi, C., Scheuerpflug, C., Debatin, K., and Krammer, P. H. (1997). FLICE is involved in regulation of activation induced cell death (AICD) in peripheral T cells. Proc. EMBO Workshop Cell-mediated Cytotoxicity, 6th, Kerkrade, The Netherlands, Abstr., p. 36.
84. Klein, J. L., Shows, T. B., Dupont, B., and Trapani, J. A. (1989). Genomic organization and chromosomal assignment for a serine protease gene (CSPB) expressed by human cytotoxic lymphocytes. Genomics 5, 110-117.
85. Klein, J. L., Selvakumar, A., Trapani, J. A., and Dupont, B. (1990). Characterization of a novel, human cytotoxic lymphocyte-specific serine protease cDNA clone (CSP-C). Tissue Antigens 35, 220-228.
86. Kluck, R. M., Bossy-Wetzel, E., Green, D. R., and Newmeyer, D. D. (1997). The release of cytochrome c from mitochondria: A primary site for Bcl-2 regulation of apoptosis. Science 275, 1132-1136.
87. Koizumi, H., Liu, C. C., Zheng, L. M., Joag, S. V., Bayne, N. K., Holoshitz, J., and Young, J. D. (1991). Expression of perforin and serine esterases by human gamma/delta T cells. J. Exp. Med. 173, 499-502.
88. Koizumi, H., Horta, M. F., Youn, B. S., Fu, K. C., Kwon, B. S., Young, J. D., and Liu, C-C. (1993). Identification of a killer cell specific regulatory element of the mouse perforin gene: An Ets-binding site-homologous motif that interacts with Ets-related proteins. Mol. Cell. Biol. 13, 6690-6697.
89. Kojima, H., Shinohara, N., Hanaoka, S., Someya-Shirota, Y., Takagaki, Y., Ohno, H., Saito, T., Katayama, T., Yagita, H., Okumura, K., et al. (1994). Two distinct pathways of specific killing revealed by perforin mutant cytotoxic T lymphocytes. Immunity 1, 357-364.
90. Kostura, M. J., Tocci, M. J., Limjuco, G., Chin, J., Cameron, P., Hillman, A. G., Chartrain, N. A., and Schmidt, J. A. (1989). Identification of a monocyte specific pre-interleukin 1 beta convertase activity. Proc. Natl. Acad. Sci. USA 86, 5227-5231.
91. Krahenbuhl, O., and Tschopp, J. (1991). Debate: The mechanism of lymphocyte-mediated killing. Perforin-induced pore formation. Immunol Today 12, 399-402; discussion, p. 403.
92. Krahenbuhl, O. P., Peter, H. H., and Tschopp, J. (1989). Absence of homologous restriction factor does not affect CTL-mediated cytolysis. Eitr. J. Immunol. 19, 217-219.
93. Kramer, M. D., Fruth, U., Simon, H. G., and Simon, M. M. (1989). Expression of cytoplasmic granules with T cell-associated serine proteinase-1 activity in Ly-2+(CD8+) T lymphocytes responding to lymphocytic choriomeningitis virus in vivo. Eur. J. Immunol. 19, 151-156.
94. Krammer, P. H., Behrmann, I., Daniel, P., Dhein, J., and Debatin, K. M. (1994). Regulation of apoptosis in the immune system. Curr. Opin. Immunol. 6, 279-289.
95. Kraut, J. (1977). Serine proteases: Structure and mechanism of catalysis. Annu. Rev. Biochem. 46, 331-358.
96. Krek, W., and Nigg, E. A. (1991). Mutations of p34cdc2 phosphorylation sites induce premature mitotic events in HeLa cells: Evidence for a double block to p34cdc2 kinase activation in vertebrates. EMBO J. 10, 3331-3341.
97. Krensky, A. M., Hanson, D. A., and Pena, S. V. (1997). Granulysin: A new molecule involved in cell-mediated cytotoxicity? Proc. EMBO Workshop Cell-mediated Cytotoxicity, 6th, Kerkrade, The Netherlands, Abstr., p. 37.
98. Kroemer, G., Zamzami, N., and Susin, S. A. (1997). Mitochondrial control of apoptosis. Immunol. Today 18, 44-51.
99. Kuida, K., Zheng, T. A., Na, S., Kuan, C., Yang, D., Karasuyama, H., Rakic, P., and Flavell, R. (1996). Decreased apoptosis in the brain and premature lethality in CPP32-deficient mice. Nature 38-1, 368-372.
100. Kumar, S. (1995). Inhibition of apoptosis by the expression of antisense Nedd2. FEBS Lett. 368, 69-72.
101. Kumar, S., and Lavin, M. F. (1996). The ICE family of cysteine proteases as effectors of cell death. Cell Death Differ. 3, 155-267.
102. Kumar, S., Kinoshita, M., Noda, M., Copeland, N. G., and Jenkins, N. A. (1994). Induction of apoptosis by the mouse Nedd2 gene, which encodes a protein similar to the product of the Caenorhabditis elegans cell death gene ced-3 and the mammalian IL-1 beta-converting enzyme. Genes Dev. 8,1613-1626.
103. Kupfer, A. (1991). T cell effector functions: Mechanisms for delivery of cytotoxicity or help. Annu. Rev. Cell Blol. 7, 479-504.
104. Kwon, B. S., Kestler, D., Lee, E., Wakulchik, M., and Young, J. D. (1988). Isolation and sequence analysis of serine protease cDNAs from mouse cytolytic T lymphocytes. J. Exp. Med. 168, 1839-1854.
105. Kwon, B. S., Wakulchik, M., Liu, C. C., Persechini, P. M., Trapani, J. A., Haq, A. K., Kim, Y., and Young, J. D. (1989). The structure of the mouse lymphocyte pore-forming protein perform. Biochem. Biophys. Res. Commun. 158, 1-10.
106. Lancki, D. W., Hsieh, C. S., and Fitch, F. W. (1991). Mechanisms of lysis by cytotoxic T lymphocyte clones. Lytic activity and gene expression in cloned antigen-specific CD4+ and CD8+ T lymphocytes. J. Immunol. 146, 3242-3249.
107. Lanier, L. L., Corliss, B., and Phillips, J. H. (1997). Arousal and inhibition of human NK cells. Immunol. Rev. 155, 145-154.
108. Lazebnik, Y. A., Cole, S., Cooke, C. A., Nelson, W. G., and Earnshaw, W. C. (1993). Nuclear events of apoptosis in vitro in cell-free mitotic extracts: A model system for analysis of the active phase of apoptosis. J. Cell Biol. 123, 7-22.
109. Lazebnik, Y. A., Kaufmann, S. H., Desnoyers, S., Poirier, G. G., and Earnshaw, W. C. (1994). Cleavage of poly(ADP-ribose) polymerase by a proteinase with properties like ICE. Nature 371, 346-347.
110. Lazebnik, Y. A., Takahashi, A., Moir, R. D., Goldman, R. D., Poirier, G. G., Kaufmann, S. H., and Earnshaw, W. C. (1995). Studies of the lamin proteinase reveal multiple parallel biochemical pathways during apoptotic execution. Proc. Natl. Acad. Sci. USA 92,9042-9046.
111. Li, H., Pohler, U., Strehlow, I., Hertig, S., Baccarini, M., Emmendorffer, A., Tschopp, J., and Lohmann-Matthes, M. L. (1994). Macrophage precursor cells produce perform and perform Yac-1 lytic activity in response to stimulation with interleukin-2. J. Leukocyte Biol. 56, 117-123.
112. Li, P., Alien, H., Bannerjee, S., Franklin, S., Herzog, L., Johnston, G, McDowell, J., Paskind, M., Rodman, L., Salfeld, J., Towne, E., Tracey, D., Wardwell, S., Wei, F.-Y., Wong, W., Kamen, R., and Seshadri, T. (1995). Mice deficient in IL-lb converting enzyme are defective in production of mature IL-lb and resistant to endotoxin shock. Cell 80, 401-411.
113. Lichtenheld, M. G., and Podack, E. R. (1989). Structure of the human perforin gene. A simple gene organization with interesting potential regulatory sequences. J. Immunol. 143,4267-4274.
114. Lichtenheld, M. G., Podack, E. R. (1992). Structure and function of the murine perforin promoter and upstream region. Reciprocal gene activation or silencing in perforin positive and negative cells. J. Immunol. 149, 2619-2626.
115. Lichtenheld, M. G., Olsen, K. J., Lu, P., Lowrey, D. M., Hameed, A., Hengartner, H., and Podack, E. R. (1988). Structure and function of human perforin. Nature 335, 448-451.
116. Lichtenheld, M. G., Podack, E. R., and Levy, R. B. (1995). Transgenic control of perforin gene expression. Functional evidence for two separate control regions. J. Immunol. 154, 2153-2163.
117. Lipman, M. L., Stevens, A. C., Bleackley, R. C., Helderman, J. H., McCune, T. R., Harmon, W. E., Shapiro, M. E., Rosen, S., and Strom, T. B. (1992). The strong correlation of cytotoxic T lymphocyte-specific serine protease gene transcripts with renal allograft rejection. Transplantation 53, 73-79.
118. Liston, P., Roy, N., Tamai, K., Lefebvre, C., Baird, S., Cherton-Horvat, G., Farahani, R., McLean, M., Ikeda, J. E., MacKenzie, A., and Korneluk, R. G. (1996). Suppression of apoptosis in mammalian cells by NAIP and a related family of IAP genes. Nature 379, 349-353.
119. Liu, C. C., Perussia, B., Cohn, Z. A., and Young, J. D. (1986). Identification and characterization of a pore-forming protein of human peripheral blood natural killer cells. J. Exp. Med. 164, 2061-2076.
120. Liu, C. C., Steffen, M., King, F., and Young, J. D. (1987). Identification, isolation, and characterization of a novel cytotoxin in murine cytolytic lymphocytes. Cell 51, 393-403.
121. Liu, C. C., Rafii, S., Granelli-Piperno, A., Trapani, J. A., and Young, J. D. (1989). Perforin and serine esterase gene expression in stimulated human T cells. Kinetics, mitogen requirements, and effects of cyclosporin A. J. Exp. Med. 170, 2105-2118.
122. Liu, C. C., Walsh, C. M., and Young, J. D. (1995). Perforin: Structure and function. Immunol. Today 16, 194-201.
123. Liu, C. C., Persechini, P. M., and Young, J. D. (1996). Expression and characterization of functionally active recombinant perforin produced in insect cells. J. Immunol. 156, 3292-3300.
124. Liu, X., Zou, H., Slaughter, C., and Wang, X. (1997). DFF, a heterodimeric protein that functions downstream of caspase-3 to trigger DNA fragmentation during apoptosis. Cell 89, 175-184.
125. Lobe, C. G., Finlay, B. B., Paranchych, W., Paetkau, V. H., and Bleackley, R. C. (1986a). Novel serine proteases encoded by two cytotoxic T lymphocyte-specific genes. Science 232, 858-861.
126. Lobe, C. G., Havele, C., and Bleackley, R. C. (1986b). Cloning of two genes that are specifically expressed in activated cytotoxic T lymphocytes. Proc. Natl. Acad. Sci. USA 83,1448-1452.
127. Lobe, C. G., Upton, C., Duggan, B., Ehrman, N., Letellier, M., Bell, J., McFadden, G., and Bleackley, R. C. (1988). Organization of two genes encoding cytotoxic T lymphocyte-specific serine proteases CCPI and CCPII. Biochemistry 27, 6941-6946.
128. Lowin, B., Beermann, F., Schmidt, A., and Tschopp, J. (1994). A null mutation in the perforin gene impairs cytolytic T lymphocyte- and natural killer cell-mediated cytotoxicity. froc. Natl. Acad. Sci. USA 91, 11571-11575.
129. Lowrey, D. M., Aebischer, T., Olsen, K., Lichtenheld, M., Rupp, F., Hengartner, H., and Podack, E. R. (1989). Cloning, analysis, and expression of murine perforin 1 cDNA, a component of cytolytic T-cell granules with homology to complement component C9. Proc. Natl. Acad. Sci. USA 86, 247-251.
130. Lu, P., Garcia-Sanz, J. A., Lichtenheld, M. G., and Podack, E. R. (1992). Perforin expression in human peripheral blood mononuclear cells. Definition of an IL-2-independent pathway of perforin induction in CD8+ T cells. J. Immunol. 148, 3354-3360.
131. Lynch, D. H., Watson, M. L., Alderson, M. R., Baum, P. R., Miller, R. E., Tough, T., Gibson, M., Davis-Smith, T., Smith, C. A., Hunter, K., et al. (1994). The mouse Fas-ligand gene is mutated in gld mice and is part of a TNF family gene cluster. Immunity 1, 131-136.
132. MacDermott, R. P., Schmidt, R. E., Caulfield, J. P., Hein, A., Bartley, G. T., Ritz, J., Schlossman, S. F., Austen, K. F., and Stevens, R. L. (1985). Proteoglycans in cell-mediated cytotoxicity. Identification, localization, and exocytosis of a chondroitin sulfate proteoglycan from human cloned natural killer cells during target cell lysis. J. Exp. Med. 162, 1771-1787.
133. Macen, J. L., Garner, R. S., Musy, P. Y., Brooks, M. A., Turner, P. C., Moyer, R. W., McFadden, G., and Bleackley, R. C. (1996). Differential inhibition of the Fas- and granulemediated cytolysis pathways by the orthopoxvirus cytokine response modifier A/SPI-2 and SPI-1 protein. Proc. Natl. Acad. Sci. USA 93, 9108-9113.
134. Maekawa, K., Imagawa, N., Nagamatsu, M., and Harada, S. (1994). Molecular cloning of a novel protein-tyrosine phosphatase containing a membrane-binding domain and GLGF repeats. FEBS Lett. 10, 200-206.
135. Manyak, C. L., Norton, G. P., Lobe, C. G., Bleackley, R. C., Gershenfeld, H. K., Weissman, I. L., Kumar, V., Sigal, N. H., and Koo, G. C. (1989). IL-2 induces expression of serine protease enzymes and genes in natural killer and nonspecific T killer cells. J. Immunol. 142, 3707-3713.
136. Marazziti, D., Eggertsen, G., Fey, G. H., and Stanley, K. K. (1988). Relationships between the gene and protein structure in human complement component C9. Biochemistry 27,6529-6534.
137. Marchetti, P., Hirsch, T., Zamzami, N., Castedo, M., Decaudin, D., Susin, S. A., Masse, B., and Kroemer, G. (1997). Mitochondria! permeability transition triggers lymphocyte apoptosis. J. Immunol. 157, 4830-4836.
138. 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., and 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. EMBO J. 15, 2407-2416.
139. Masson, D., and Tschopp, J. (1985). Isolation of a lytic, pore-forming protein (perforin) from cytolytic T-lymphocytes. J. Biol. Chem. 260, 9069-9072.
140. Masson, D., and Tschopp, J. (1987). A family of serine esterases in lytic granules of cytolytic T lymphocytes. Cell 49, 679-685.
141. Masson, D., Corthesy, P., Nabholz, M., and Tschopp, J. (1985). Appearance of cytolytic granules upon induction of cytolytic activity in CTL-hybrids. EMBO J. 4, 2533-2538.
142. Masson, D., Peters, P. J., Geuze, H. J., Borst, J., and Tschopp, J. (1990). Interaction of chondroitin sulfate with perforin and granzymes of cytolytic T-cells is dependent on pH. Biochemistry 29, 11229-11235.
143. Masson, D., and Tschopp, J. (1988). Inhibition of lymphocyte protease granzyme A by antithrombin III. Mol. Immunol. 25, 1283-1289.
144. Mattel, M. G., Harper, K., Brunei, J. F., Denizot, F., Mattel, J. F., Golstein, P., and Giraud, F. (1987). In situ mapping of four cytotoxic T lymphocyte associated proteins (CTL) to the mouse genome. Cylogenet. Cell Genet. 46, 657-658.
145. McGuire, M. J., Lipsky, P. E., and 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.
146. Millard, P- J-, Henkart, M. P., Reynolds, C. W., and Henkart, P. A. (1984). Purification and properties of cytoplasmic granules from cytotoxic rat LGL tumors. J. Imimmol 132,3197-3204.
147. Minn, A. J., Velez, P., Schendel, S. L., Liang, H., Muchmore, S. W., Fesik, S. W., Fill, M., and Thompson, C. B. (1997). Bcl-x(L) forms an ion channel in synthetic lipid membranes. Nature 385, 353-357.
148. Miura, M., Zhu, H., Rotello, R., Hartwieg, E. A., and 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.
149. Miura, M., Friedlander, R. M., and Yuan, J. (1995). Tumor necrosis factor-induced apoptosis is mediated by a CrmA-sensitive cell death pathway. Proc. Natl. Acail. Sci. USA 92,8318-8322.
150. Moll, H., Muller, C., Gillitzer, R., Fuchs, H., Rollinghoff, M., Simon, M. M., and Kramer, M. D. (1991). Expression of T-cell-associated serine proteinase 1 during murine Leishmania major infection correlates with susceptibility to disease. Infect. Immun. 59, 4701-4705.
151. Mueller, C., Shao, Y., Altermatt, H. J., Hess, M. W., and Shelby, J. (1993). The effect of cyclosporine treatment on the expression of genes encoding granzyme A and perforin in the infiltrate of mouse heart transplants. Transplantation 55, 139-145.
152. Mullbacher, A., Ebnet, K., Blanden, R. V., Hla, R. T., Stehle, T., Museteanu, C., and 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.
153. Muller, C., and Tschopp, J. (1994). Resistance of CTL to perforin-mediated lysis. Evidence for a lymphocyte membrane protein interacting with perforin. J. Immunol. 153,2470-2478.
154. Muller, C., Kagi, D., Aebischer, T., Odermatt, B., Held, W., Podack, E. R., Zinkernagel, R. M., and Hengartner, H. (1989). Detection of perforin and granzyme A mRNA in infiltrating cells during infection of mice with lymphocytic choriomeningitis virus. Eur. J. Immunol. 19, 1253-1259.
155. Muller, U., Steinhoff, U., Reis, L. F., Hemmi, S., Pavlovic, J., Zinkernagel, R. M., and Aguet, M. (1994). Functional role of type I and type II interferons in antiviral defense. Science 264, 1918-1921.
156. Munday, N. A., Vaillancourt, J. P., AH, A., Casano, F. J., Miller, D. K., Molineaux, S. M., Yamin, T. T., Yu, V. L., and Nicholson, D. W. (1995). Molecular cloning and pro-apoptotic activity of ICErelll and ICErelHI, members of the ICE/CED-3 family of cysteine proteases. J. Biol. Chem. 270, 15870-15876.
157. Murphy, M. E., Moult, J., Bleackley, R. C., Gershenfeld, H., Weissman, I. L., and James, M. N. (1988). Comparative molecular model building of two serine proteinases from cytotoxic T lymphocytes. Proteins 4, 190-204.
158. Muzio, M., Chinnaiyan, A. M., Kischkel, F. C., O'Rourke, K., Shevchenko, A., Ni, J., Scaffidi, C., Bretz, J. D., Zhang, M., Gentz, R., Mann, M., Krammer, P. H., Peter, M. E., and Dixit, V. M. (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.
159. Na, S., Chuang, T. H., Cunningham, A., Turi, T. G., Hanke, J. H., Bokoch, G. M., and Danley, D. E. (1996). D4-GDI, a substrate of CPP32, is proteolyzed during Fas-induced apoptosis. J. Biol Chem. 271, 11209-11213.
160. Nagata, S. (1996). Fas ligand and immune evasion. Nat. Med. 2,1306-1307.
161. [News; comment] Nagata, S., and Golstein, P. (1995). The Fas death factor. Science 267, 1449-1456.
162. Nagler-Anderson, C., Verret, C. R., Firmenich, A. A., Berne, M., and Eisen, H. N. (1988). Resistance of primary CD8+ cytotoxic T lymphocytes to lysis by cytotoxic granules from cloned T cell lines. J. Immunol. 141, 3299-3305.
163. Nakajima, H., and Henkart, P. A. (1994). Cytotoxic lymphocyte granzymes trigger a target cell internal disintegration pathway leading to cytolysis and DNA breakdown. J. Immunol. 152, 1057-1063.
164. Nakajima, H., Golstein, P., and Henkart, P. A. (1995). The target cell nucleus is not required for cell-mediated granzyme- or Fas-based cytotoxicity. J. Exp. Med. 181,1905-1909.
165. Nakata, M, Smyth, M. J., Norihisa, Y., Kawasaki, A., Shinkai, Y., Okumura, K., and Yagita, H. (1990). Constitutive expression of pore-forming protein in peripheral blood gamma/delta T cells: Implication for their cytotoxic role in vivo. J. Exp. Med 172, 1877-1880.
166. Nakata, M., Kawasaki, A., Azuma, M., Tsuji, K., Matsuda, H., Shinkai, Y., Yagita, H., and Okumura, K. (1992). Expression of perforin and cytolytic potential of human peripheral blood lymphocyte subpopulations. Int. Immunol. 4, 1049-1054.
167. Nalefski, E. A., and Falke, J. J. (1996). The C2 domain calcium-binding motif. Structural and functional diversity. Protein Sci. S, 2375-2390.
168. Nicholson, D. W., Ali, A., Thornberry, N. A., Vaillancourt, J. P., Ding, C. K., Gallant, M., Gareau, Y., Griffin, P. R., Labelle, M., Lazebnik, Y. A., et al. (1995). Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 376. 37-43.
169. Nishioka, W. K., and Welsh, R. M. (1994). Susceptibility to cytotoxic T lymphocyte-induced apoptosis is a function of the proliferative status of the target. J. Exp. Med. 179, 769-774.
170. Oberhammer, F. A., Hochegger, K., Froschl, G., Tiefenbacher, R., and Pavelka, M. (1994). Chromatin condensation during apoptosis is accompanied by degradation of lamin A+B, without enhanced activation of cdc2 kinase. J. Cell Biol. 126, 827-837.
171. O'Connell, J., O'Sullivan, G. C., Collins, J. K., and Shanahan, F. (1996). The Fas counterattack: Fas-mediated T cell killing by colon cancer cells expressing Fas ligand. J. Exp. Med. 184, 1075-1082.
172. Odake, S., Kam, C. M., Narasimhan, L., Poe, M., Blake, J. T., Krahenbuhl, O., Tschopp, J., and 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.
173. Ojcius, D. M., Persechini, P. M., Zheng, L. M., Notaroberto, P. C., Adeodato, S. C., and Young, J. D. (1991a). Cytolytic and ion channel-forming properties of the N terminus of lymphocyte perforin. Proc. Natl. Acad. Sci. USA 88, 4621-4625.
174. Ojcius, D. M., Zheng, L. M., Sphicas, E. C., Zychlinsky, A., and Young, J. D. (1991b). Subcellular localization of perforin and serine esterase in lymphokine-activated killer cells and cytotoxic T cells by immunogold labeling. J. Immunol. 146, 4427-4432.
175. Okura, T., Gong, L., Kamitani, T., Wada, T., Okura, I., Wei, C. F., Chang, H. M., and Yeh, E. T. (1996). Protection against Fas/APO-1- and tumor necrosis factor-mediated cell death by a novel protein, sentrin. J. Immunol. 157, 4277-4281.
176. Ortaldo, J. R., Winkler-Pickett, R. T., Nagashima, K., Yagita, H., and Okumura, K. (1992). Direct evidence for release of pore-forming protein during NK cellular lysis. J. Leukocyte Biol. 52, 483-488.
177. Ostergaard, H. L., and Clark, W. R. (1989). Evidence for multiple lytic pathways used by cytotoxic T lymphocytes. J. Immunol. 143, 2120-2126.
178. Ostergaard, H. L., Kane, K. P., Mescher, M. F., and Clark, W. R. (1987). Cytotoxic T lymphocyte mediated lysis without release of serine esterase. Nature 330, 71-72.
179. Parker, L. L., Walter, S. A., Young, P. G., and Piwnica-Worms, H. (1993). Phosphorylation and inactivation of the mitotic inhibitor Weel by the niml/cdrl kinase. Nature 363,736-738.
180. Parmley, R. T., Rahemtulla, F., Cooper, M. D., and Roden, L. (1985). Ultrastructural and biochemical characterization of glycosaminoglycans in HNK-1-positive large granular lymphocytes. Blood 66, 20-25.
181. Pasternack, M. S., Verret, C. R., Liu, M. A., and Eisen, H. N. (1986). Serine esterase in cytolytic T lymphocytes. Nature 322, 740-743.
182. Pasternack, M. S., Bleier, K. J., and Mclnerney, T. N. (1991). Granzyme A binding to target cell proteins. Granzyme A binds to and cleaves nucleolin in vitro. J. Biol. Chem. 266,14703-14708.
183. Peitsch, M. G, and Tschopp, J. (1994). Granzyme B. In "Methods in Enzymology" (A. J. Barrett, ed.), Vol. 244, pp. 80-87. Academic Press, San Diego, CA.
184. Persechini, P. M, and Young, J. D. (1988). The primary structure of the lymphocyte poreforming protein perforin: Partial amino acid sequencing and determination of isoelectric point. Biochem. Biophys. Res, Commun. 156, 740-745.
185. Peters, P. J., Geuze, H. J., Van der Donk, H. A., Slot, J. W., Griffith, J. M., Stam, N. J., devers, H. C., and Borst, J. (1989). Molecules relevant for T cell-target cell interaction are present in cytolytic granules of human T lymphocytes. Eur. J. Imnwnol. 19, 1469-1475.
186. Peters, P. J., Geuze, H. J., van der Donk, H. A., and Borst, J. (1990). A new model for lethal hit delivery by cytotoxic T lymphocytes. ImmunoL Today 11, 28-32.
187. Peters, P. J., Borst, J., Oorschot, V., Fukuda, M., Krahenbuhl, O., Tschopp, J., Slot, J. W., and Geuze, H. J. (1991). Cytotoxic T lymphocyte granules are secretory lysosomes, containing both perforin and granzymes. J. Exp. Med. 173, 1099-1109.
188. Pfeffer, K., Matsuyama, T., Kundig, T. M., Wakeham, A., Kishihara, K., Shahinian, A., Wiegmann, K., Ohashi, P. S., Kronke, M., and Mak, T. W. (1993). Mice deficient for the 55 kd tumor necrosis factor receptor are resistant to endotoxic shock, yet succumb to L. monocytogenes infection. Cell 73, 457-467.
189. Pilat, D., Fink, T., Obermaier-Skrobanek, B., Zimmer, M., Wekerle, H., Lichter, P., and 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.
190. Pinkoski, M. J., Winkler, U., Hudig, D., and Bleackley, R. G (1996). Binding of granzyme B in the nucleus of target cells. Recognition of an 80-kilodalton protein. J. Biol. Chem. 271, 10225-10229.
191. Podack, E. R. (1989). Granule-mediated cytolysis of target cells. Curr. Top. Microbiol. Iminitnol 140, 1-9.
192. Podack, E. R. (1992). Perforin: Structure, function, and regulation. Curr. Top. Microbiol. ImmunoL 178, 175-184.
193. Podack, E. R. (1995). Functional significance of two cytolytic pathways of cytotoxic T lymphocytes. J. Leukocyte Biol. 57, 548-552.
194. Podack, E. R., and Dennert, G. (1983). Assembly of two types of tubules with putative cytolytic function by cloned natural killer cells. Nature 302, 442-445.
195. Podack, E. R., Young, J. D., and Cohn, Z. A. (1985). Isolation and biochemical and functional characterization of perforin 1 from cytolytic T-cell granules. Proc. Natl. Acad. Sci. USA 82, 8629-8633.
196. Podack, E. R., Hengartner, H., and Lichtenheld, M. G. (1991). A central role of perforin in cytolysis? Annu. Rev. ImmunoL 9, 129-157.
197. Poe, M., Blake, J. T., Boulton, D. A., Gammon, M., Sigal, N. H., Wu, J. K., and Zweerink, H. J. (1991). Human cytotoxic lymphocyte granzyme B. Its purification from granules and the characterization of substrate and inhibitor specificity. J. Biol. Chem. 266, 98-103.
198. Potempa, J., Korzus, E., and Travis, J. (1994). The serpin superfamily of proteinase inhibitors: Structure, function, and regulation. J. Biol. Chem. 269, 15957-15960.
199. Quan, L. T., Caputo, A., Bleackley, R. G, Pickup, D. J., and Salvesen, G. S. (1995). Granzyme B is inhibited by the cowpox virus serpin cytokine response modifier A. J. Biol. Chem. 270, 10377-10379.
200. Rabizadeh, S., LaCount, D. J., Friesen, P. D., and Bredesen, D. E. (1993). Expression of the baculovirus p35 gene inhibits mammalian neural cell death. J. Neurochem. 61, 2318-2321.
201. Ramsay, A. J., Ruby, J., and Ramshaw, I. A. (1993). A case for cytokines as effector molecules in the resolution of virus infection. ImmunoL Today 14, 155-157.
202. Ray, C. A., Black, R. A., Kronheim, S. R., Greenstreet, T. A., Sleath, P. R., Salvesen, G. S., and Pickup, D. J. (1992). Viral inhibition of inflammation: Cowpox virus encodes an inhibitor of the interleukin-1 beta converting enzyme. Cell 69, 597-604.
203. Remington, S. J., Woodbury, R. G., Reynolds, R. A., Matthews, B. W., and Neurath, H. (1988). The structure of rat mast cell protease II at 1.9-A resolution. Biochemistry 27, 8097-8105.
204. Rouvier, E., Luciani, M. F., and Golstein, P. (1993). Fas involvement in Ca(2+)-independent T cell-mediated cytotoxicity. J. Exp. Med. 177, 195-200.
205. Roy, N., Mahadevan, M. S., McLean, M., Shutler, G., Yaraghi, Z., Farahani, R., Baird, S., Besner-Johnston, A., Lcfebvre, C., Kang, X., el a!. (1995). The gene for neuronal apoptosis inhibitory protein is partially deleted in individuals with spinal muscular atrophy. Cell 80, 167-178.
206. Russell, J. H. (1983). Internal disintegration model of cytotoxic lymphocyte-induced target damage. Immunol Rev. 72, 97-118.
207. Salcedo, T. W., Azzoni, L., Wolf, S. F., and Perussia, B. (1993). Modulation of perforin and granzyme messenger RNA expression in human natural killer cells. J. Immunol. 151,2511-2520.
208. Salvesen, G., Parley, D., Shuman, J., Przybyla, A., Reilly, C., and Travis, J. (1987). Molecular cloning of human cathepsin G: Structural similarity to mast cell and cytotoxic T lymphocyte proteinascs. Biochemistry 26, 2289-2293.
209. Sarin, A., Williams, M. S., Alexander-Miller, M. A., Berzofsky, J. A., Zacharchuk, C. M., and Henkart, P. A. (1997a). CTL lysis via the two CTL pathways differs with respect to utilization of target caspases: Lysis via Fas requires caspases while granule exocytosis does not. Proc. EMBO Workshop Cell-mediated Cytotoxicity, 6th, Kerkrade, The Netherlands, Abstr., p. 28.
210. Sarin, A., Williams, M. S., Alexander-Miller, M. A., Berzofsky, J. A., Zacharchuk, C. M., and Henkart, P. A. (1997b). Target cell lysis by CTL granule exocytosis is independent of ICE/Ced-3 family proteases. Immunity 6, 209-215.
211. Sayers, T. J., Wiltrout, T. A., Sowder, R., Munger, W. L., Smyth, M. J., and 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 a granule serine protease (RNKP-1). J. Immunol. 148, 292-300.
212. Sayers, T. J., Wiltrout, T. A., Smyth, M. J., Ottaway, K. S., Pilaro, A. M., Sowder, R., Henderson, L. E., Sprenger, H., and 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.
213. Schmid, D. S., Tite, J. P., and Ruddle, N. H. (1986). DNA fragmentation: manifestation of target cell destruction mediated by cytotoxic T-cell lines, lymphotoxin-secreting helper T-cell clones, and cell-free lymphotoxin-containing supernatant. Proc. Natl. Acad. Sci. USA 83, 1881-1885.
214. Schmid, J., and Weissmann, C. (1987). Induction of mRNA for a serine protease and a beta-thromboglobulin-like protein in mitogen-stimulated human leukocytes. J. Immunol. 139, 250-256.
215. Schmidt, R. E., MacDermott, R. P., Bartley, G., Bertovich, M., Amato, D. A., Austen, K. F., Schlossman, S. F., Stevens, R. L., and Ritz, J. (1985). Specific release of proteoglycans from human natural killer cells during target lysis. Nature 318, 289-291.
216. Schroter, M., Lowin, B., Borner, C., and Tschopp, J. (1995). Regulation of Fas(Apo-l/CD95)-and perforin-mediated lytic pathways of primary cytotoxic T lymphocytes by the protoonco-gene bcl-2. Eur. J. Immunol. 25, 3509-3513.
217. Schulz, M., Schuurman, H. J., Joergensen, J., Steiner, C., Meerloo, T., Kagi, D., Hengartner, H., Zinkernagel, R. M., Schreier, M. H., Burki, K., et al. (1995). Acute rejection of vascular heart allografts by perforin-deficient mice. Eur. J. Immunol. 25, 474-480.
218. Schulze-Osthoff, K., Walczak, H., Droge, W., and Krammer, P. H. (1994). Cell nucleus and DNA fragmentation are not required for apoptosis. J. Cell Biol. 127, 15-20.
219. Selvaggi, G., Ricordi, G, Podack, E. R., and Inverardi, L. (1996). The role of the perform and Fas pathways of cytotoxicity in skin graft rejection. Transplantation 62, 1912-1915.
220. Selvakumar, A., Steffens, U., and Dupont, B. (1997). Polymorphism and domain variability of human killer cell inhibitory receptors. Immunol. Rev. 155, 183-196.
221. Seth, P. (1994). A simple and efficient method of protein delivery into cells using adenovirus. Biochem. Biophys. Res. Commun. 203, 582-587.
222. Shi, L., Kraut, R. P., Aebersold, R., and Greenberg, A. H. (1992a). A natural killer cell granule protein that induces DNA fragmentation and apoptosis. J. Exp. Med. 175,553-566.
223. Shi, L., Kam, C. M., Powers, J. C-, Aebersold, R., and Greenberg, A. H. (1992b). Purification of three cytotoxic lymphocyte granule serine proteases that induce apoptosis through distinct substrate and target cell interactions. J. Exp. Med. 176, 1521-1529.
224. Shi, L., Nishioka, W. K., Th'ng, J., Bradbury, E. M., Litchfield, D. W., and Greenberg, A. H. (1994). Premature p34cdc2 activation required for apoptosis [sec comments]. Science 263, 1143-1145.
225. Shi, L., Chen, G., He, D., Bosc, D. G., Litchfield, D. W., and Greenberg, A. H. (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.
226. Shi, L., Mai, S., Israels, S., Browne, K.,Trapani, J. A., and Greenberg, A. H. (1997). Granzyme B (GraB) autonomously crosses the cell membrane and perform initiates apoptosis and GraB nuclear localization. J. Exp. Med. 185, 855-866.
227. Shinkai, Y., Takio, K., and Okumura, K. (1988). Homology of perforin to the ninth component of complement (C9). Nature 334, 525-527.
228. Shinkai, Y., Yoshida, M. C., Maeda, K., Kobata, T., Maruyama, K., Yodoi, J., Yagita, H., and Okumura, K. (1989). Molecular cloning and chromosomal assignment of a human perforin (PFP) gene. Immunogenetics 30, 452-457.
229. Shiver, J. W., and Henkart, P. A. (1991). A noncytotoxic mast cell tumor line exhibits potent IgE-dependent cytotoxicity after transfection with the cytolysin/perforin gene. Cell 64,1175-1181.
230. Shiver, J. W., Su, L., and Henkart, P. A. (1992). Cytotoxicity with target DNA breakdown by rat basophilic leukemia cells expressing both cytolysin and granzyme A. Cell 71,315-322.
231. Sieg, S., Xia, and L., Huang, Y., and Kaplan, D. (1995). Specific inhibition of granzyme B by parainfluenza virus type 3. J. Virol. 69, 3538-3541.
232. Simon, H. G., Fruth, U., Kramer, M. D., and Simon, M. M. (1987a). A secretable serine proteinase with highly restricted specificity from cytolytic T lymphocytes inactivates retrovirus-associated reverse transcriptase. FEBS Lett. 223, 352-360.
233. Simon, M. M., and Kramer, M. D. (1994). Granzyme A. In "Methods in Enzymology" (A. J. Barrett, ed.), Vol. 244, pp. 68-79. Academic Press, San Diego, CA.
234. Simon, M. M., Hoschutzky, H., Fruth, U., Simon, H. G., and Kramer, M. D. (1986). Purification and characterization of a T cell specific serine proteinase (TSP-1) from cloned cytolytic T lymphocytes. EMBO J. 5, 3267-3274.
235. Simon, M. M., Simon, H. G., Fruth, U., Epplen, J., Muller-Hermelink, H. K., and Kramer, M. D. (1987b). Cloned cytolytic T-effector cells and their malignant variants produce an extracellular matrix degrading trypsin-like serine proteinase. Immunology 60, 219-230.
236. Simon, M. M., Kramer, M. D., Prester, M., and Gay, S. (1991). Mouse T-cell associated serine proteinase 1 degrades collagen type IV: A structural basis for the migration of lymphocytes through vascular basement membranes. Immunology 73, 117-119.
237. Simon, M. M., Hausmann, M., and Mullbacher, A. (1997). Granzyme A: Involvement in lymphocyte-mediated cytotoxicity and recovery of mice from infection with viral pathogens. Proc. EMBO Workshop Cell-mediated Cytotoxicity, 6th, Kerkrade, The Netherlands, Abstr., p. 65.
238. Smyth, M. J., and Ortaldo, J. R. (1991). Comparison of the effect of IL-2 and IL-6 on the lytic activity of purified human peripheral blood large granular lymphocytes. J. Immunol. 146, 1380-1384.
239. Smyth, M. J., and Trapani, J. A. (1995). Granzymes: Exogenous proteinases that induce target cell apoptosis. Immunol. Today 16, 202-206.
240. Smyth, M. J., Ortaldo, J. R., Bere, W., Yagita, H., Okumura, K., and Young, H. A. (1990a). IL-2 and IL-6 synergize to augment the pore-forming protein gene expression and cytotoxic potential of human peripheral blood T cells. J. Immunol. 145, 1159-1166.
241. Smyth, M. J., Ortaldo, J. R., Shinkai, Y., Yagita, H., Nakata, M., Okumura, K., and Young, H. A. (1990b). Interleukin 2 induction of pore-forming protein gene expression in human peripheral blood CD8+ T cells. J. Exp. Med. 171, 1269-1281.
242. Smyth, M. J., Norihisa, Y., Gerard, J. R., Young, H. A., and Ortaldo, J. R. (1991a). IL-7 regulation of cytotoxic lymphocytes: Pore-forming protein gene expression, interferon-gamma production, and cytotoxicity of human peripheral blood lymphocytes subsets. Cell. Immunol. 138, 390-403.
243. Smyth, M. J., StrobI, S. L., Young, H. A., Ortaldo, J. R., and Ochoa, A. C. (1991b). Regulation of lymphokine-activated killer activity and pore-forming protein gene expression in human peripheral blood CD8+ T lymphocytes. Inhibition by transforming growth factor-beta. J. Immunol. 146, 3289-3297.
244. Smyth, M. J., Wiltrout, T., Trapani, J. A., Ottaway, K. S., Sowder, R., Henderson, L. E., Kam, C. M., Powers, J. C., Young, H. A., and 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.
245. Smyth, M. J., Sayers, T. J., Wiltrout, T., Powers, J. C., and 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, 6195-6205.
246. Smyth, M. J., Kershaw, M. H., Hulett, M. D., McKenzie, I. F., and Trapani, J. A. (1994). Use of the 5'-flanking region of the mouse perforin gene to express human Fc gamma receptor I in cytotoxic T lymphocytes. J. Leukocyte Biol. 55, 514-522.
247. Smyth, M. J., Hulett, M. D., Thia, K. Y., Young, H. A., Sayers, T. J., Carter, C. R., and Trapani, J. A. (1995a). Cloning and characterization of a novel NK cell-specific serine protease gene and its functional 5'-flanking sequences. Immunogenetics 42, 101-111.
248. Smyth, M. J., McGuire, M. J., and Thia, K. Y. (1995b). Expression of recombinant human granzyme B. A processing and activation role for dipeptidyl peptidase I. J. Immunol. 154, 6299-6305.
249. Smyth, M. J., O'Connor, M. D., Trapani, J. A., Kershaw, M. H., and Brinkworth, R. I. (1996a). A novel substrate-binding pocket interaction restricts the specificity of the human NK cell-specific serine protease, Met-ase-1. J. Immunol. 156, 4174-4181.
250. Smyth, M. J., Sutton, V. R., Kershaw, M. H., and Trapani, J. A. (1996b). Xenospecific cytotoxic T lymphocytes use perforin- and Fas-mediated lytic pathways. Transplantation 62, 1529-1532.
251. Smyth, M. J., O'Connor, M. D., and Trapani, J. A. (1996c). Granzymes: A variety of serine protease specificities encoded by genetically distinct subfamilies. J. Leukocyte Biol. 60, 555-562.
252. Sneller, M. C., Straus, S. E., Jaffe, E. S., Jaffe, J. S., Fleisher, T. A., Stetler-Stevenson, M., and Strober, W. (1992). A novel lymphoproliferative/autoimmune syndrome resembling murine Ipr/gld disease. J. C//n. Invest. 90, 334-341.
253. Song, Q., Lees-Miller, S. P., Kumar, S., Zhang, Z., Chan, D. W., Smith, G. C., Jackson, S. P., Alnemri, E. S., Litwack, G., Khanna, K. K., and Lavin, M. F. (1996). DNA-dependent protein kinase catalytic subunit: a target for an ICE-like protease in apoptosis. EMBO J. 15, 3238-3246.
254. Sower, L. E., Froelich, C. J., Allegretto, N., Rose, P. M., Hanna, W. D., and Kumpel, G. R. (1996a). Extracellular activities of human granzyme A. Monocyte activation by granzyme A versus alpha-thrombin. J. Immunol. 156, 2585-2590.
255. Sower, L. E., Kumpel, G. R., Hanna, W., and Froelich, C. J. (1996b). Extracellular activities of human granzymes. I. Granzyme A induces IL6 and IL8 production in fibroblast and epithelial cell lines. Cell. Imiminol. 171, 159-163.
256. Spielman, J., Baker, M. B., Levy, R. B., Lee, R. K., and Podack, E. R. (1997). Perforin, antigen presentation and T cell homeostasis. Proc. EMBO Workshop Cell-mediated Cytotoxicity, 6th, Kerkrade, The Netherlands, Abstr., pp. 51-52.
257. Sprecher, C. A., Morgenstern, K. A., Mathewes, S., Dahlen, J. R., Schrader, S. K., Foster, D. C., and Kisiel, W. (1995). Molecular cloning, expression, and partial characterization of two novel members of the ovalbumin family of serine proteinase inhibitors. J. Biol. Chem. 270, 29854-29861.
258. Srinivasula, S. M., Fernandes-AInemri, T., Zangrilli, J., Robertson, N., Armstrong, R. C., Wang, L., Trapani, J. A., Tomaselli, K. J., Litwack, G., and Alnemri, E. S. (1996a). The Ced-3/interIeukin Ibeta converting enzyme-like homolog Mch6 and the lamin-cleaving enzyme Mch2alpha are substrates for the apoptotic mediator CPP32. J. Biol. Chem. 271, 27099-27106.
259. Srinivasula, S. M., Ahmad, M., Fernandes-AInemri, T., Litwack, G., and Alnemri, E. (1996b). Molecular ordering of the Fas-apoptotic pathway: the FAS/APO-1 protease Mch5 is crmA-inhibitable protease that activates multiple Ced-3/ICE-like cysteine proteases. Proc. Natl. Acad. Sci. USA 93, 14486-14491.
260. Stalder, T., Hahn, S., and Erb, P. (1994). Fas antigen is the major target molecule for CD4+ T cell-mediated cytotoxicity. J. Immunol. 152, 1127-1133.
261. Stanley, K. K., Page, M., Campbell, A. K., and Luzio, J. P. (1986). A mechanism for the insertion of complement component C9 into target membranes. Mol. Immunol. 23,451-458.
262. Stevens, R. L., Otsu, K., Weis, J. H., Tantravahi, R. V., Austen, K. F., Henkart, P. A., Galli, M. C., and Reynolds, C. W. (1987). Co-sedimentation of chondroitin sulfate A glycosaminoglycans and proteoglycans with the cytolytic secretory granules of rat large granular lymphocyte (LGL) tumor cells, and identification of a mRNA in normal and transformed LGL that encodes proteoglycans. J. Immunol. 139, 863-868.
263. Stevens, R. L., Kamada, M. M., and Serafm, W. E. (1989). Structure and function of the family of proteoglycans that reside in the secretory granules of natural killer cells and other effector cells of the immune response. Curr. Top. Microbiol. Immunol. 140, 93-108.
264. Strand, S., Hofmann, W. J., Hug, H., Muller, M., Otto, G., Strand, D., Mariani, S. M., Stremmel, W., Krammer, P. H., and Galle, P. R. (1996). Lymphocyte apoptosis induced by CD95 (APO-1/Fas) ligand-expressing tumor cells-A mechanism of immune evasion? [see comments]. Nat. Med. 2,1361-1366.
265. Strasser, A., Harris, A. W., Huang, D. C., Krammer, P. H., and Cory, S. (1995). Bcl-2 and Fas/APO-1 regulate distinct pathways to lymphocyte apoptosis. EMBO J. 14, 6136-6147.
266. Suda, T., and Nagata, S. (1994). Purification and characterization of the Fas-ligand that induces apoptosis. J. Exp. Med. 179, 873-879.
267. Suidan, H. S., Bouvier, J., Schraer, S., Stone, S. R., Monard, D., and Tschopp, J. (1994). Granzyme A release upon stimulation of cytotoxic T lymphocytes activates the thrombin receptor on neuronal cells and astrocytes. Proc. Natl. Acad. Sci. USA 91, 8112-8116.
268. Sun, J., Bird, C. H., Sutton, V., McDonald, L., Coughlin, P. B., De Jong, T. A., Trapani, J. A., and Bird, P. I. (1996). A cytosolic granzyme B inhibitor related to the viral apoptotic regulator cytokine response modifier A is present in cytotoxic lymphocytes. J. Biol. Chem. 271, 27802-27889.
269. Sun, J., Ooms, L., Bird, C. H., Sutton, V. R., Trapani, J. A., and Bird, P. I. (1997). A new family of 10 murine ovalbumin serpins includes two homologs of proteinase inhibitor 8 and two homologs of the granzyme B inhibitor (Proteinase inhibitor 9) [In Process Citation]. J. Biol. Chem. 272, 15434-15441.
270. Susin, S. A., Zamzami, N., Castedo, M., Hirsch, T., Marchetti, P., Macho, A., Daugas, E., Geuskens, M., and Kroemer, G. (1996). Bcl-2 inhibits the mitochondrial release of an apoptogenic protease. J. Exp. Med. 184, 1331-1341.
271. Sutton, V. R., Vaux, D. L., and Trapani, J. A. (1997). Bcl-2 prevents apoptosis induced by perforin and granzyme B, but not that mediated by whole cytotoxic lymphocytes. J. Iminunol. 158, 5783-5790.
272. Tak, P. P., Kummer, J. A., Hack, C. E., Daha, M. R., Smeets, T. J., Erkelens, G. W., Meinders, A. E., Kluin, P. M., and Breedveld, F. C. (1994). Granzyme-positive cytotoxic cells are specifically increased in early rheumatoid synovial tissue. Arthritis Rheum. 37, 1735-1743.
273. Takahashi, K., Nakamura, T., Adachi, H., Yagita, H., and Okumura, K. (1991). Antigen-independent T cell activation mediated by a very late activation antigen-like extracellular matrix receptor. Eur. J. Iminunol. 21, 1559-1562.
274. Takahashi, T., Tanaka, M., Brannan, C. I., Jenkins, N. A., Copeland, N. G., Suda, T., and Nagata, S. (1994). Generalized lymphoproliferative disease in mice, caused by a point mutation in the Fas ligand. Cell 76, 969-976.
275. Takayama, H., Trenn, G., Humphrey, W., Jr., Bluestone, J. A., Henkart, P. A., and Sitkovsky, M. V. (1987). Antigen receptor-triggered secretion of a trypsin-type esterase from cytotoxic T lymphocytes. J. Iminunol. 138, 566-569.
276. Talento, A., Nguyen, M., Law, S., Wu, J. K., Poe, M., Blake, J. T., Patel, M., Wu, T. J., Manyak, C. L., Silberklang, M., et al. (1992). Transfection of mouse cytotoxic T lymphocyte with an antisense granzyme A vector reduces lytic activity. J. Iminunol. 149, 4009-4015.
277. Tanaka, M., Suda, T., Haze, K., Nakamura, N., Sato, K., Kimura, F., Motoyoshi, K., Mizuki, M., Tagawa, S., Ohga, S., Hatake, K., Drummond, A. H., and Nagata, S. (1996). Fas ligand in human serum. Nat. Med. 2, 317-322.
278. Tartaglia, L. A., Ayres, T. M., Wong, G. H., and Goeddel, D. V. (1993). A novel domain within the 55 kd TNF receptor signals cell death. Cell 74, 845-853.
279. Tay, C. H., and Welsh, R. M. (1997). Distinct organ-dependent mechanisms for the control of murine cytomegalovirus infection by natural killer cells. J. Virol. 71, 267-275.
280. Tewari, M., and Dixit, V. M. (1995). Fas- and tumor necrosis factor-induced apoptosis is inhibited by the poxvirus crmA gene product. J. Biol. Chem. 270, 3255-3260.
281. Tewari, M., Quan, L. T., O'Rourke, K., Desnoyers, S., Zeng, Z., Beidler, D. R., Poirier, G. G., Salvesen, G. S., and Dixit, V. M. (1995a). Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 81, 801-809.
282. Tewari, M., Telford, W. G., Miller, R. A., and Dixit, V. M. (1995b). CrmA, a poxvirus-encoded serpin, inhibits cytotoxic T-lymphocyte-mediated apoptosis. J. Biol. Chem. 270, 22705-22708.
283. Thia, K. Y., Jenkins, N. A., Gilbert, D. J., Copeland, N. G., and Smyth, M. J. (1995). The natural killer cell serine protease gene Lmetl maps to mouse chromosome 10. Immiinogenetics 41, 47-49.
284. Thome, M., Schneider, P., Hofmann, K., Fickenscher, H., Meinl, E., Neipel, F., Mattmann, C., Burns, K., Bodmer, J. L., Schroter, M., Scaffidi, C., Krammer, P. H., Peter, M. E., and Tschopp, J. (1997). Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 386, 517-521.
285. Thornberry, N. A., Bull, H. G., Calaycay, J. R., Chapman, K. T., Howard, A. D., Kostura, M. J., Miller, D. K., Molineaux, S. M., Weidner, J. R., Aunins, J., et al. (1992). A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature 356, 768-774.
286. Tian, Q., Streuli, M., Saito, H., Schlossman, S. F., and Anderson, P. (1991). A polyadenylate binding protein localized to the granules of cytolytic lymphocytes induces DNA fragmentation in target cells. Cell 67, 629-639.
287. Trapani, J. A., and Dupont, B. (1990). Novel putative promoter/enhancer sequences are shared by the mouse and human perforin (Pfp) genes. Tissue Antigens 36, 228-234.
288. Trapani, J. A., and Smyth, M. J. (1993). Killing by cytotoxic T cells and natural killer cells: Multiple granule serine proteases as initiators of DNA fragmentation. Immimol. Cell Biol. 71, 201-208.
289. Trapani, J. A., Klein, J. L., White, P. C., and Dupont, B. (1988). Molecular cloning of an inducible serine esterase gene from human cytotoxic lymphocytes. Proc. Natl. Acad. Sci. USA 85, 6924-6928.
290. Trapani, J. A., Kwon, B. S., Kozak, C. A., Chintamaneni, C., Young, J. D., and Dupont, B. (1990). Genomic organization of the mouse pore-forming protein (perform) gene and localization to chromosome 10. Similarities to and differences from C9. J. Exp. Med. 171, 545-557.
291. Trapani, J. A., Browne, K. A., Dawson, M., and Smyth, M. J. (1993). Immunopurification of functional Asp-ase (natural killer cell granzyme B) using a monoclonal antibody. Biochem. Biopliys. Res. Commun. 195, 910-920.
292. Trapani, J. A., Smyth, M. J., Apostolidis, V. A., Dawson, M., and Browne, K. A. (1994). Granule serine proteases are normal nuclear constituents of natural killer cells. J. Biol. Chem. 269, 18359-18365.
293. Trapani, J. A., Browne, K. A., Smyth, M. J., and 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.
294. Trapani, J. A., Jans, P., Froelich, C. J., Smyth, M. J., Sutton, V. R., and Jans, D. (1997). Perforin-dependent nuclear entry of granzyme B precedes apoptosis, and is not a consequence of nuclear membrane dysfunction. In press.
295. Trauth, B. C., Klas, C., Peters, A. M., Matzku, S., Moller, P., Falk, W., Debatin, K. M., and Krammer, P. H. (1989). Monoclonal antibody-mediated tumor regression by induction of apoptosis. Science 245, 301-305.
296. Trenn, G., Takayama, H., and Sitkovsky, M. V. (1987). Exocytosis of cytolytic granules may not be required for target cell lysis by cytotoxic T-lymphocytes. Nature 330, 72-74.
297. Tschopp, J., and Jongeneel, C. V. (1988). Cytotoxic T lymphocyte mediated cytolysis. Biochemistry 27, 2641-2646.
298. Tschopp, J., and Nabholz, M. (1990). Perforin-mediated target cell lysis by cytotoxic T lymphocytes. Anmi. Rev. Immimol. 8, 279-302.
299. Tschopp, J., Masson, D., and Stanley, K. K. (1986). Structural/functional similarity between proteins involved in complement- and cytotoxic T-lymphocyte-mediated cytolysis. Nature 322, 831-834.
300. Tschopp, J., Schafer, S., Masson, D., Peitsch, M. C., and Heusser, C. (1989). Phosphorylcholine acts as a Ca2+-dependent receptor molecule for lymphocyte perform. Nature 337,272-274.
301. Ucker, D. S., Obermiller, P. S., Eckhart, W., Apgar, J. R., Berger, N. A., and Meyers, J. (1992). Genome digestion is a dispensable consequence of physiological cell death mediated by cytotoxic T lymphocytes. Mol. Cell. Biol. 12, 3060-3069.
302. Uellner, R., Jones, J., and Griffiths, G. M. (1997). Perforin is activated by proteolytic cleavage during biosynthesis which reveals a phospholipid binding domain. Proc. EMBO Workshop Cell-mediated Cytotoxicity, 6th, Kerkrade, The Netherlands, Abstr., p. 25.
303. Uren, A. G., Pakusch, M., Hawkins, C. J., Puls, K. L., and Vaux, D. L. (1996). Cloning and expression of apoptosis inhibitory protein homologs that function to inhibit apoptosis and/or bind tumor necrosis factor receptor-associated factors. Proc. Natl. Acad. Sci. USA 93, 4974-4978.
304. Uyttenhove, C., Maryanski, J., and Boon, T. (1983). Escape of mouse mastocytoma P815 after nearly complete rejection is due to antigen-loss variants rather than immunosuppression. J. Exp. Med. 157, 1040-1052.
305. van den Broek, M. R, Kagi, D., Zinkernagel, R. M., and Hengartner, H. (1995). Perforin dependence of natural killer cell-mediated tumor control in vivo. EUT. J. Immimol. 25,3514-3516.
306. van den Broek, M. E., Kagi, D., Ossendorp, F., Toes, R., Vamvakas, S., Lutz, W. K., Melief, C. J., Zinkernagel, R. M., and Hengartner, H. (1996). Decreased tumor surveillance in perforin-deficient mice. J. Exp. Med. 184, 1781-1790.
307. Varfolomeev, E. E., Boldin, M. P., Goncharov, T. M., and Wallach, D. (1996). A potential mechanism of "cross-talk" between the p55 tumor necrosis factor receptor and Fas/APOl: Proteins binding to the death domains of the two receptors also bind to each other. J. Exp. Med. 183, 1271-1275.
308. Vaux, D. L., Weissman, I. L., and Kim, S. K. (1992a). Prevention of programmed cell death in Caenorhabditis elegans by human bcl-2. Science 258, 1955-1957.
309. Vaux, D. L., Aguila, H. L., and Weissman, I. L. (1992b). Bcl-2 prevents death of factordeprived cells but fails to prevent apoptosis in targets of cell mediated killing. Int. Immitnol. 4, 821-824.
310. Vaux, D. L., Haecker, G., and Strasser, A. (1994). An evolutionary perspective on apoptosis. Cell 76, 777-779.
311. Verret, C. R., Firmenich, A. A., Kranz, D. M., and Eisen, H. N. (1987). Resistance of cytotoxic T lymphocytes to the lytic effects of their toxic granules. J. Exp. Med. 166, 1536-1547.
312. von Heijne, G. (1986). A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 14, 4683-4690.
313. Wagtmann, N., Biassoni, R., Cantoni, C., Verdiani, S., Malnati, M. S., Vitale, M., Bottino, C., Moretta, L., Moretta, A., and Long, E. O. (1995). Molecular clones of the p58 NK cell receptor reveal immunoglobulin-related molecules with diversity in both the extra- and intracellular domains. Immunity 2, 439-449.
314. Walsh, C. M., Matloubian, M., Liu, C. C., Ueda, R., Kurahara, C. G., Christensen, J. L., Huang, M. T., Young, J. D., Ahmed, R., and Clark, W. R. (1994). Immune function in mice lacking the perform gene. Proc. Natl. Acad. Sci. USA 91, 10854-10858.
315. Walsh, C. M., Hayashi, F., Saffran, D. C., Ju, S. T., Berke, G., and Clark, W. R. (1996). Cellmediated cytotoxicity results from, but may not be critical for, primary allograft rejection. J. Immunol. 156, 1436-1441.
316. Wang, L., Miura, M., Bergeron, L., Zhu, H., and Yuan, J. (1994). Ich-1, an Ice/ced-3-related gene, encodes both positive and negative regulators of programmed cell death. Cell 78, 739-750.
317. Wang, X., Zelenski, N. G., Yang, J., Sakai, J., Brown, M. S., and Goldstein, J. L. (1996). Cleavage of sterol regulatory element binding proteins (SREBPs) by CPP32 during apoptosis. EMBO J. 15,1012-1020.
318. Wang, Z. Q., Auer, B., Stingl, L., Berghammer, H., Haidacher, D., Schweiger, M., and Wagner, E. F. (1995). Mice lacking ADPRT and poly(ADP-ribosyl)ation develop normally but are susceptible to skin disease. Genes Dev. 9, 509-520.
319. Watanabe-Fukunaga, R., Brannan, C. I., Copeland, N. G., Jenkins, N. A., and Nagata, S. (1992). Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis. Nature 356, 314-317.
320. Welsh, R. M. (1981). Natural cell-mediated immunity during viral infections. Curr. Top. Microbiol. Immunol. 92, 83-106.
321. White, E., Cipriani, R., Sabbatini, P., and Denton, A. (1991). Adenovirus E1B 19-kilodalton protein overcomes the cytotoxicity of E1A proteins. J. Virol. 65, 2968-2978.
322. White, K., Grether, M. E., Abrams, J. M., Young, L., Farrell, K., and Steller, H. (1994). Genetic control of programmed cell death in Drosophila [see comments]. Science 264, 677-683.
323. Wilson, K. P., Black, J. A., Thomson, J. A., Kirn, E. E., Griffith, J. P., Navia, M. A., Murcko, M. A., Chambers, S. P., Aldape, R. A., Raybuck, S. A., era/. (1994). Structure and mechanism of interleukin-1 beta converting enzyme [see comments]. Nature 370, 270-275.
324. Wood, G. S., Mueller, C., Warnke, R. A., and Weissman, I. L. (1988). In situ localization of HuHF serine protease mRNA and cytotoxic cell-associated antigens in human dermatoses. A novel method for the detection of cytotoxic cells in human tissues. Am. J. Palhol. 133, 218-225.
325. Woodard, S. L., Jackson, D. S., Abuelyaman, A. S., Powers, J. C., VVinkler, U, and Hudig, D. (1994). Chymase-directed serine protease inhibitor that reacts with a single 30-kDa granzyme and blocks NK-mediated cytotoxicity. J. Imimmol. 153, 5016-5025.
326. Wu, D., Wallen, H. D., and Nunez, G. (1997). Interaction and regulation of subcellular localization of CED-4 by CED-9 [see comments]. Science 275, 1126-1129.
327. Xiang, J., Chao, D. T., and Korsmeyer, S. J. (1996). BAX-induced cell death may not require interleukin 1 beta-converting enzyme-like proteases. Proc. Natl. Acad. Sci. USA 93,14559-14563.
328. Xue, D., and 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.
329. Yagita, H., Nakata, M., Kawasaki, A., Shinkai, Y., and Okumura, K. (1992). Role of perforin in lymphocyte-mediated cytolysis. Adv. Immunol. 51, 215-242.
330. Yang, J., Liu, X., Bhalla, K., Kirn, C. N., Ibrado, A. M., Cai, J., Peng, T. I., Jones, D. P., and Wang, X. (1997). Prevention of apoptosis by Bcl-2: Release of cytochrome c from mitochondria blocked [see comments]. Science 275, 1129-1132.
331. Yannelli, J. R., Sullivan, J. A., Mandell, G. L., and Engelhard, V. H. (19S6). Reorientation and fusion of cytotoxic T lymphocyte granules after interaction with target cells as determined by high resolution cinemicrography. J. Immunol. 136, 377-382.
332. Ymer, S., and Jans, D. A. (1996). In vivo chromatin structure of the murine interIeukin-5 gene region: A new intact cell system. BioTechniqiies 20, 834-838, 840.
333. Yonehara, S., Ishii, A., and Yonehara, M. (1989). A cell-killing monoclonal antibody (antiFas) to a cell surface antigen co-downregulated with the receptor of tumor necrosis factor. J. Exp. Med. 169, 1747-1756.
334. Young, J. D., and Cohn, Z. A. (1986). Cell-mediated killing: A common mechanism? Cell 46. 641-642.
335. Young, J. D., Cohn, Z. A., and Podack, E. R. (1986a). The ninth component of complement and the pore-forming protein (perforin 1) from cytotoxic T cells: Structural, immunological, and functional similarities. Science 233, 184-190.
336. Young, J. D., Hengartner, H., Podack, E. R., and Cohn, Z. A. (1986b). Purification and characterization of a cytolytic pore-forming protein from granules of cloned lymphocytes with natural killer activity. Cell 44, 849-859.
337. Young, J. D., Leong, L. G., Liu, C. C., Damiano, A., Wall, D. A., and Cohn, Z. A. (1986c). Isolation and characterization of a serine esterase from cytolytic T cell granules. Cell 47. 183-194.
338. Young, J. D., Liu, C. C., Leong, L. G., and Cohn, Z. A. (1986d). The pore-forming protein (perforin) of cytolytic T lymphocytes is immunologically related to the components of membrane attack complex of complement through cysteine-rich domains. J. Exp. Med. 164, 2077-2082.
339. Young, J. D., Damiano, A., DiNome, M. A., Leong, L. G., and Cohn, Z. A. (1987). Dissociation of membrane binding and lytic activities of the lymphocyte pore-forming protein (perforin). J. Exp. Med. 165, 1371-1382.
340. Young, L. H., Joag, S. V., Zheng, L. M., Lee, C. P., Lee, Y. S., and Young, J. D. (1990). Perforin-mediated myocardial damage in acute myocarditis. Lancet 336, 1019-1021.
341. Young, L. H., Joag, S. V., Lin, P. Y., Luo, S. F., Zheng, L. M., Liu, C. C., and Young, J. D. (1992). Expression of cytolytic mediators by synovial fluid lymphocytes in rheumatoid arthritis. Am. J. Pathol. 140, 1261-1268.
342. Yuan, J., and Horvitz, H. R. (1992). The Caenorhabditis elegans cell death gene ced-4 encodes a novel protein and is expressed during the period of extensive programmed cell death. Development 116, 309-320.
343. Yuan, J., Shaham, S., Ledoux, S., Ellis, H. M., and 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.
344. Yue, C. C., Reynolds, C. W., and Henkart, P. A. (1987). Inhibition of cytolysin activity in large granular lymphocyte granules by lipids: Evidence for a membrane insertion mechanism of lysis. A/o/. ImmunoL 24, 647-653.
345. Zagury, D., Bernard, J., Thierness, N., Feldman, M., and Berke, G. (1975). Isolation and characterization of individual functionally reactive cytotoxic T lymphocytes: Conjugation, killing and recycling at the single cell level. EUT. J. Imtmmol. 5, 818-822.
346. Zalman, L. S., Brothers, M. A., Chiu, F. J., and Muller-Eberhard, H. J. (1986a). Mechanism of cytotoxicity of human large granular lymphocytes: Relationship of the cytotoxic lymphocyte protein to the ninth component (C9) of human complement. Proc. Natl. Acad. Sci. USA 83, 5262-5266.
347. Zalman, L. S., Wood, L. M., and Muller-Eberhard, H. J. (1986b). Isolation of a human erythrocyte membrane protein capable of inhibiting expression of homologous complement transmembrane channels. Proc. Natl. Acad. Sci. USA 83, 6975-6979.
348. Zalman, L. S., Wood, L. M., and Muller-Eberhard, H. J. (1987). Inhibition of antibodydependent lymphocyte cytotoxicity by homologous restriction factor incorporated into target cell membranes. J. Exp. Med. 166, 947-955.
349. Zhang, Y., and Lichtenheld, M. G. (1997). Non-killer cell-specific transcription factors silence the perforin promoter. J. linnnmol. 158, 1734-1741.
350. Zheng, L. M., Ojcius, D. M., Liu, C. C., Kramer, M. D., Simon, M. M., Parr, E. L., and Young, J. D. (1991). Immunogold labeling of perforin and serine esterases in granulated metrial gland cells. FASEB J. 5, 79-85.
351. Zhivotovsky, B., Gahm, A., Ankarcrona, M., Nicotera, P., and Orrenius, S. (1995). Multiple protease are involved in thymocyte apoptosis. Exp. Cell Res. 221, 404-412.
352. Zimmer, M., Medcalf, R. L., Fink, T. M., Mattmann, C., Lichter, P., and Jenne, D. E. (1992). Three human elastase-Iike genes coordinately expressed in the myelomonocyte lineage are organized as a single genetic locus on 19pter. Proc. Natl. Acad. Sci. USA 89, 8215-8219.
353. Zinkernagel, R. M., and Rosenthal, K. L. (1981). Experiments and speculation on antiviral specificity of T and B cells. Immunol. Rev. 58, 131-155.
354. Zunino, S. J., Allison, N. J., Kam, C. M., Powers, J. C., and Hudig, D. (1988). Localization, implications for function, and gene expression of chymotrypsin-like proteinases of cytotoxic RNK-16 lymphocytes. Biochim. Biophys. Acta 967, 331-340.
355. Zunino, S. J., Bleackley, R. C., Martinez, J., and Hudig, D. (1990). RNKP-1, a novel natural killer-associated serine protease gene cloned from RNK-16 cytotoxic lymphocytes./. Immunol. 144, 2001-2009.