The relative role of lymphocyte granule exocytosis versus death receptor-mediated cytotoxicity in viral pathophysiology

Journal of Virology

Volumn 72, Issue 1, 1998, Pages 1-9

  Smyth, Mark J ^a   Trapani, Joseph A ^a  

^a AUSTIN RESEARCH INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN RECOGNITION; AUTOIMMUNITY; CELL DEATH; CELL KILLING; CELL MEDIATED CYTOTOXICITY; CYTOTOXIC T LYMPHOCYTE; CYTOTOXICITY; EXOCYTOSIS; IMMUNE RESPONSE; LYMPHOCYTE FUNCTION; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RECEPTOR AFFINITY; REVIEW; TARGET CELL; VIRUS INFECTION;

EID: 0031975821     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/jvi.72.1.1-9.1998     Document Type: Review

References (124)

1. Ahn, K., A. Gruhler, B. Galocha, T. R. Jones, E. J. Wiertz, H. L. Ploegh, P. A. Peterson, Y. Yang, and K. Fruh. 1997. The ER-luminal domain of the HCMV glycoprotein US6 inhibits peptide translocation by TAP. Immunity 6:613-621.
2. Ando, K., K. Hiroishi, T. Kaneko, T. Moriyama, Y. Muto, N. Kayagaki, H. Yagita, K. Okumura, and M. Imawari. 1997. Perforin, Fas/Fas ligand, and TNF-α pathways as specific and bystander killing mechanisms of hepatitis C virus-specific human CTL. J. Immunol. 158:5283-5291.
3. Anel, A., M. Buferne, C. Boyer, A.-M. Schmitt-Verhulst, and P. Golstein. 1994. T cell receptor-induced Fas ligand expression in cytotoxic T lymphocyte clones is blocked by protein tyrosine kinase inhibitors and cyclosporin A. Eur. J. Immunol. 24:2469-2476.
4. Arase, H., N. Arase, and T. Saito. 1995. Fas-mediated cytotoxicity by freshly isolated natural killer cells. J. Exp. Med. 181:1235-1238.
5. Ashwell, J. D., and R. D. Klausner. 1990. Genetic and mutational analysis of the T cell antigen receptor. Annu. Rev. Immunol. 8:139-167.
6. Bancroft, G. J. 1993. The role of natural killer cells in innate resistance to infection. Curr. Opin. Immunol. 5:503-510.
7. Beidler, D. R., M. Tewari, P. D. Friesen, G. Poirier, and V. M. Dixit. 1995. The baculovirus p35 protein inhibits Fas- and tumor necrosis factor-induced apoptosis. J. Biol. Chem. 270:16526-16528.
8. + peripheral blood progenitor cells mobilized by chemotherapy and granulocyte-colony stimulating factor. Blood 86:3500-3506.
9. Bertin, J., R. C. Armstrong, S. Ottilie, D. A. Martin, Y. Wang, S. Banks, G. H. Yang, T. G. Senkevich, E. S. Alnemri, B. Moss, M. J. Lenardo, K. J. Tomaselli, and J. I. Cohen. 1997. Death effector domain-containing herpesvirus and poxvirus proteins inhibit both Fas- and TNFR1-induced apoptosis. Proc. Natl. Acad. Sci. USA 94:1172-1176.
10. Boismenu, R., and W. L. Havran. 1997. An innate view of gamma delta T cells. Curr. Opin. Immunol. 9:57-63.
11. Brossart, P., and M. J. Bevan. 1996. Selective activation of Fas/Fas ligand-mediated cytotoxicity by a self-peptide. J. Exp. Med. 183:2449-2458.
12. Buchmeier, M. J., R. M. Welsh, F. J. Dutko, and M. B. A. Oldstone. 1980. The virology and immunobiology of lymphocytic choriomeningitis virus infection. Adv. Immunol. 30:275-331.
13. Carter, C. R., T. J. Sayers, R. H. Wiltrout, S. M. Turcovski-Corrales, and D. D. Taub. 1996. Generation of antigenic peptides by lymphocyte granule serine proteases (granzymes). Cell. Immunol. 172:235-245.
14. + T cells by a self-derived peptide. Nature 378:295-298.
15. Cheng, E. H., J. Nicholas, D. S. Bellows, G. S. Hayward, H. G. Guo, M. S. Reitz, and J. M. Hardwick. 1997. A Bcl-2 homolog encoded by Kaposi sarcoma-associated virus, human herpesvirus 8, inhibits apoptosis but does not heterodimerize with Bax or Bak. Proc. Natl. Acad. Sci. USA 94:690-694.
16. Chisari, F. V. 1996. Hepatitis B virus transgenic mice: models of viral immunobiology and pathogenesis. Curr. Top. Microbiol. Immunol. 206:149-173.
17. Cohen, P., and R. A. Eisenberg. 1991. Lpr and gld: single gene models of systemic autoimmunity and lymphoproliferative disease. Annu. Rev. Immunol. 9:243-269.
18. Colonna, M. 1997. Specificity and function of immunoglobulin superfamily NK cell inhibitory and stimulatory receptors. Immunol. Rev. 155:127-134.
19. Cuturi, M. C., I. Anegon, F. Sherman, R. Loudon, S. C. Clark, B. Perussia, and G. Trinchieri. 1989. Production of hematopoietic colony-stimulating factors by human natural killer cells. J. Exp. Med. 169:569-583.
20. Darmon, A. J., D. W. Nicholson, and R. C. Bleackley. 1996. Activation of the apoptotic protease CPP32 by cytotoxic T-cell derived granzyme B. Nature 377:446-448.
21. Dhein, J., H. Walczak, C. Baumler, K.-M. Debatin, and P. H. Krammer. 1995. Autocrine T-cell suicide mediated by APO-1 (Fas/CD95). Nature 373:438-441.
22. + T cells. Immunol. Today 11:55-59.
23. Duke, R. C., R. Chervenak, and J. J. Cohen. 1983. Endogenous endonuclease-induced DNA fragmentation. Proc. Natl. Acad. Sci. USA 80:6361-6365.
24. Ebnet, K., M. Hausmann, F. Lehmann-Grube, A. Mullbacher, M. Kopf, M. Lamers, and M. M. Simon. 1995. Granzyme A-deficient mice retain potent cell-mediated cytotoxicity. EMBO J. 14:4230-4239.
25. Ehl, S., U. Hoffman-Rohrer, S. Nagata, H. Hengartner, and R. Zinkernagel. 1996. Different susceptibility of cytotoxic T cells to CD95 (Fas/Apo-1) ligand-mediated cell death after activation in vitro versus in vivo. J. Immunol. 156:2357-2360.
26. Farrell, H. E., H. Vally, D. M. Lynch, P. Fleming, G. R. Shellam, A. A. Scalzo, and N. J. Davis-Poynter. 1997. Inhibition of natural killer cells by a cytomegalovirus MHC class I homologue in vivo. Nature 386:510-514.
27. Farrow, S. N., J. H. White, I. Martinou, T. Raven, K. T. Pun, C. J. Grinham. J. C. Marinou, and R. Brown. 1995. Cloning of a bcl-2 homologue by interaction with adenovirus E1B 19K. Nature 374:731-733.
28. Fernandes-Alnemri, T., R. Armstrong, J. Krebs, S. M. Srinivasula, L. Wang, F. Bullrich, L. C. Fritz, J. A. Trapani, K. J. Tomaselli, G. Litwack, and E. S. Alnemri. 1996. Activation of CPP32 and Mch3 by Mch4, a novel human apoptotic cysteine protease containing two FADD-like domains. Proc. Natl. Acad. Sci. USA 93:7464-7469.
29. Froelich, C. J., K. Orth, J. Turbov, P. Seth, R. Gottlieb, B. Bahior, G. M. Shah, R. C. Bleackley, V. M. Dixit, and W. Hanna. 1996. New paradigm for lymphocyte granule-mediated cytotoxicity. Target cells bind and internalize granzyme B, but an endosomolytic agent is necessary for cytosolic delivery and subsequent apoptosis. J. Biol. Chem. 271:29073-29079.
30. Galocha, B., A. Hill, B. C. Barnett, A. Dolan, A. Raimondi, R. F. Cook, J. Brunner, D. J. McGeoch, and H. L. Ploegh. 1997. The active site of ICP47, a herpes simplex virus-encoded inhibitor of the major histocompatibility complex (MHC)-encoded peptide transporter associated with antigen processing (TAP), maps to the NH2-terminal 35 residues. J. Exp. Med. 185:1565-1572.
31. 30a. Greenberg, P. 1997. Abstract. EMBO Cell Mediated Cytotoxicity Workshop. Kerkrade, The Netherlands.
32. Griffiths, G. M., and C. Mueller. 1991. Expression of perforin and granzymes in vivo: potential diagnostic markers for activated cytotoxic cells. Immunol. Today 12:415-419.
33. Guidotti, L. G., K. Ando, M. V. Hobbs, T. Ishikawa, L. Runkel, R. D. Schreiber, and F. V. Chisari. 1994. Cytotoxic T lymphocytes inhibit hepatitis B virus gene expression by a noncytolytic mechanism in transgenic mice. Proc. Natl. Acad. Sci. USA 91:3764-3768.
34. Hacker, G., C. J. Hawkins, K. G. Smith, and D. L. Vaux. 1996. Effects of viral inhibitors of apoptosis in models of mammalian cell death. Behring Inst. Mitt. 97:118-126.
35. Henkart, P. A. 1985. Mechanism of lymphocyte-mediated cytotoxicity. Annu. Rev. Immunol. 3:31-58.
36. Henkart, P. A. 1994. Lymphocyte-mediated cytotoxicity: two pathways and multiple effector molecules. Immunity 1:343-346.
37. Heusel, J. W., R. L. Wesselschmidt, S. Shresta, J. H. Russell, and T. Ley. 1994. Cytotoxic lymphocytes require granzyme B for the rapid induction of DNA fragmentation and apoptosis in allogeneic target cells. Cell 76:977-987.
38. Hiromatsu, K., J. Usami, Y. Aoki, M. Makino, and Y. Yoshikai. 1997. Accelerated progression of a murine retrovirus-induced immunodeficiency syndrome in Fas mutant C57BL/61pr/1pr mice. Microbiol. Immunol. 41:221-227.
39. Hu, S., C. Vincenz, M. Buller, and V. M. Dixit. 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.
40. Itoh, N., S. Yonehara, A. Ishii, M. Yonehara, S. Mizushima, M. Sameshima, A. Has, Y. Seto, and S. Nagata. 1991. The polypeptide encoded by the cDNA for human cell surface antigen Fas can mediate apoptosis. Cell 66:233-243.
41. Jenne, D. E., and J. Tschopp. 1988. Granzymes, a family of serine proteases released from granules of cytolytic T-lymphocytes upon T-cell receptor stimulation. Immunol. Rev. 103:53-71.
42. + cytotoxic T cells. Proc. Natl. Acad. Sc. USA 91:4185-4189.
43. Ju, S.-T., D. J. Panka, H. Cui, R. Ettinger, M. El-Khatib, D. H. Sherr, B. Z. Stanger, and A. Marshak-Rothstein. 1995. Fas (CD95)/FasL interactions required for programmed cell death after T-cell activation. Nature 373:444-448.
44. Kagi, D., B. Ledermann, K. Burki, P. Seiler, B. Odermatt, K. J. Olsen, E. R. Podack, R. M. Zinkernagel, and H. Hengartner. 1994. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature 369:31-37.
45. Kagi, D., P. Seiler, J. Pavlovic, B. Ledermann, K. Burki, R. M. Zinkernagel, and H. Hengartner. 1995. The roles of perforin- and Fas-dependent cytotoxicity in protection against cytopathic and noncytopathic viruses. Eur. J. Immunol. 25:3256-3262.
46. Kagi, D., B. Ledermann, K. Burki, R. M. Zinkernagel, and H. Hengartner. 1995. Molecular mechanisms of lymphocyte-mediated cytotoxicity and their role in immunological protection and pathogenesis in vivo. Immunol. Rev. 146:95-115.
47. Kagi, D., and H. Hengartner. 1996. Different roles for cytotoxic T cells in the control of infections with cytopathic versus noncytopathic viruses. Curr. Opin. Immunol. 8:472-477.
48. Kawanishi, M. 1997. Epstein-Barr virus BHRF1 protein protects intestine 407 epithelial cells from apoptosis induced by tumor necrosis factor alpha and anti-Fas antibody. J. Virol. 71:3319-3322.
49. Kerkau, T., I. Bacik, J. R. Bennink, J. W. Yewdell, T. Hunig, A. Schimpl, and U. Schubert. 1997. The human immunodeficiency virus type 1 (HIV-1) Vpu protein interferes with an early step in the biosynthesis of major histocompatibility complex (MHC) class I molecules. J. Exp. Med. 185:1295-1305.
50. Kettle, S., A. Alcami, A. Khanna, R. Ehret, C. Jassoy, and G. L. Smith. 1997. Vaccinia virus serpin B13R (SPI-2) inhibits interleukin-1 beta-converting enzyme and protects virus-infected cells from TNF- and Fas-mediated apoptosis, but does not prevent IL-1 beta-induced fever. J. Gen. Virol. 78:677-685.
51. Kondo, T., T. Suda, H. Fukuyama, M. Adachi, and S. Nagata. 1997. Essential roles of the Fas ligand in the development of hepatitis. Nat. Med. 3:409-413.
52. Lanier, L. L., A. M. Le, J. H. Phillips, N. L. Warner, and G. F. Babcock. 1983. Subpopulations of human natural killer cells defined by expression of the Leu-7 (HNK-1) and Leu-11 (NK-15) antigens. J. Immunol. 131:1789-1796.
53. Lanier, L. L., J. J. Ruitenberg, and J. H. Phillips. 1988. Functional and biochemical analysis of CD16 antigen on natural killer cells and granulocytes. J. Immunol. 141:3478-3485.
54. Lanier, L. L. 1997. Natural killer cells: from no receptors to too many. Immunity 6:371-378.
55. Lefrancois, L., and D. S. Lyles. 1982. The interaction of antibody with the major surface glycoprotein of vesicular stomatitis virus. II. Monoclonal antibodies of nonneutralizing and cross-reactive epitopes of Indiana and New Jersey serotypes. Virology 121:168-174.
56. Levine, A. 1997. p53, the cellular gatekeeper for growth and division. Cell 88:323-331.
57. Li, H., U. Pohler, I. Strehlow, S. Hertig, M. Baccarini, A. Emmendorffer, J. Tschopp, and M. L. Lohmann-Matthes. 1994. Macrophage precursor cells produce perforin and perform Yac-1 lytic activity in response to stimulation with interleukin-2. J. Leukocyte Biol. 56:117-123.
58. Lichtenheld, M. G., K. J. Olsen, P. Lu, D. M. Lowrey, A. Hameed, H. Hengartner, and E. R. Podack. 1988. Structure and function of human perforin. Nature 335:448-451.
59. Lin, M. T., S. A. Stohlman, and D. R. Hinton. 1997. Mouse hepatitis virus is cleared from the central nervous systems of mice lacking perforin-mediated cytolysis. J. Virol. 71:383-391.
60. Lohman, B. L., E. S. Razvi, and R. M. Welsh. 1996. T-lymphocyte down-regulation after acute viral infection is not dependent on CD95 (Fas) receptor-ligand interactions. J. Virol. 70:8199-8203.
61. Los, M., M. Van de Craen, L. C. Penning, H. Schenk, M. Westendorp, P. A. Baeuerle, W. Droge, P. H. Krammer, W. Fiers, and K. Schulze-Osthoff. 1995. Requirement of an ICE/CED-3 protease for Fas/APO-1-mediated apoptosis. Nature 375:81-83.
62. Machold, R. P., E. J. Wiertz, T. R. Jones, and H. L. Ploegh. 1997. The HCMV gene products US11 and US2 differ in their ability to attack allelic forms of murine major histocompatibility complex (MHC) class I heavy chains. J. Exp. Med. 185:363-366.
63. Mori, T., K. Ando, K. Tanaka, Y. Ikeda, and Y. Koga. 1997. Fas-mediated apoptosis of the hematopoietic progenitor cells in mice infected with murine cytomegalovirus. Blood 89:3565-3573.
64. Mullbacher, A., K. Ebnet, R. V. Blanden, R. T. Hla, T. Stehle, C. Museteanu, and M. M. Simon. 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.
65. Muller, U., U. Steinhoff, L. F. Reis, S. Hemmi, J. Pavlovic, R. M. Zinkernagel, and M. Aguet. 1994. Functional role of type I and type II interferons in antiviral defense. Science 264:1918-1921.
66. Muzio, M., A. M. Chinnaiyan, F. C. Kischkel, K. O'Rourke, A. Shevchenko, J. Ni, C. Scaffidi, J. D. Bretz, M. Zang, R. Gentz, M. Mann, P. H. Krammer, M. E. Peter, and V. M. Dixit. 1996. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex. Cell 85:817-827.
67. Nakata, M., M. J. Smyth, Y. Norihisa, A. Kawasaki, Y. Shinkai, K. Okumura, and H. Yagita. 1990. Constitutive expression of pore-forming protein in peripheral blood gamma delta T cells: Implication for their cytotoxic role in vivo. J. Exp. Med. 172:1777-1784.
68. Nava, V. E., E. H. Cheng, M. Veliuona, S. Zou, R. J. Clem, M. L. Mayer, and J. M. Hardwick. 1997. Herpesvirus saimiri encodes a functional homolog of the human bcl-2 oncogene. J. Virol. 71:4118-4122.
69. Pantaleo, G., C. Graziosi, and A. S. Fauci. 1993. The immunopathogenesis of human immunodeficiency virus infection. N. Eng. J. Med. 328:327-335.
70. Podack, E. R., and G. Dennert. 1983. Assembly of two types of tubules with putative cytolytic function by cloned natural killer cells. Nature 302:442-445.
71. Querido, E., R. C. Marcellus, A. Lai, R. Charbonneau, J. G. Teodoro, G. Ketner, and P. E. Branton. 1997. Regulation of p53 levels by the E1B 55-kilodalton protein and E4orf6 in adenovirus-infected cells. J. Virol. 71:3788-3798.
72. Ramsay, A. J., J. Ruby, and I. A. Ramshaw. 1993. A case for cytokines as effector molecules in the resolution of virus infection. Immunol. Today 14:155-157.
73. Reddehase, M. J., W. Mutter, K. Munch, H.-J. Buhring, and U. H. Koszinowski. 1987. CD8-positive T lymphocytes specific for murine cytomegalovirus immediate-early antigens mediate protective immunity. J. Virol. 61:3102-3108.
74. Revilla, Y., A. Cebrian, E. Baixeras, C. Martinez, E. Vinuela, and M. L. Salas. 1997. Inhibition of apoptosis by the African swine fever virus Bcl-2 homologue: role of BH1 domain. Virology 228:400-404.
75. Reyburn, H. T., O. Mandelboim, M. Vales-Gomez, D. M. Davis, L. Pazmany, and J. L. Strominger. 1997. The class I MHC homologue of human cytomegalovirus inhibits attack by natural killer cells. Nature 386:514-517.
76. Riddell, S. R., K. S. Watanabe, J. M. Goodrich, C. R. Li, M. E. Agha, and P. D. Greenberg. 1992. Restoration of viral immunity in immunodeficient humans by the adoptive transfer of T cell clones. Science 257:238-241.
77. + cytotoxic T cell therapy of cytomegalovirus and HIV infection. Curr. Opin. Immunol. 5:484-491.
78. Rothe, M., M. G. Pan, W. J. Henzel, T. M. Ayres, and D. V. Goeddel. 1995. The TNFR2-TRAF signaling complex contains two novel proteins related to baculoviral inhibitor of apoptosis proteins. Cell 83:1243-1252.
79. 2+-independent T cell-mediated cytotoxicity. J. Exp. Med. 177:195-200.
80. Russell, J. H., and C. B. Dubos. 1980. Mechanisms of immune lysis. II. CTL-induced nuclear disintegration of the target begins within minutes of cell contact. J. Immunol. 125:1256-1261.
81. Sarin, A., M. S. Williams, M. A. Alexander-Miller, J. A. Berzofsky, C. M. Zacharchuk, and P. A. Henkart. 1997. Target cell lysis by CTL granule exocytosis is independent of ICE/Ced-3 family proteases. Immunity 6:209-215.
82. + T cell subsets and induces early resistance to Leishmania major in mice. J. Exp. Med. 178:567-577.
83. Scheffner, M., J. M. Huibregtse, R. D. Vierstra, and P. M. Howley. 1993. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the uhiquitination of p53. Cell 75:495-505.
84. Schreiber, M., L. Sedger, and G. McFadden. 1997. Distinct domains of M-T2, the myxoma virus tumor necrosis factor (TNF) receptor homolog, mediate extracellular TNF binding and intracellular apoptosis inhibition. J. Virol. 71:2171-2181.
85. Scott, P., and G. Trinchieri. 1995. The role of natural killer cells in host-parasite interactions. Curr. Opin. Immunol. 7:34-40.
86. Shi, L., C.-M. Kam, J. C. Powers, R. Aebersold, and A. H. Greenberg. 1992. Purification of three cytotoxic lymphocyte granule serine proteases that induce apoptosis through distinct substrate and target cell interactions. J. Exp. Med. 176:1521-1529.
87. Shinkai, Y., K. Takio, and K. Okumura. 1988. Homology of perforin to the ninth component of complement (C9). Nature 334:525-527.
88. Shiver, J. W., L. Su, and P. A. Henkart. 1992. Cytotoxicity with target DNA breakdown by rat basophilic leukemia cells expressing both cytolysin and granzyme A. Cell 71:315-322.
89. Sieg, S., L. Xia, Y. Huang, and D. Kaplan. 1995. Specific inhibition of granzyme B by parainfluenza virus type 3. J. Virol. 69:3538-3541.
90. Sieg, S., Z. Yildirim, D. Smith, N. Kayagaki, H. Yagita, Y. Huang, and D. Kaplan. 1996. Herpes simplex virus type 2 inhibition of Fas ligand expression. J. Virol. 70:8747-8751.
91. Sieg, S., D. Smith, Z. Yildirim, and D. Kaplan. 1997. Fas ligand deficiency in HIV disease. Proc. Natl. Acad. Sci. USA 94:5860-5865.
92. 90a. Simon, M. 1997. Abstract. EMBO Cell Mediated Cytotoxicity Workshop. Kerkrade, The Netherlands.
93. Sloand, E. M., N. S. Young, P. Kumar, F. F. Weichold, T. Sato, and J. P. Maciejewski. 1997. Role of Fas ligand and receptor in the mechanism of T-cell depletion in acquired immunodeficiency syndrome: effect on CD4+ lymphocyte depletion and human immunodeficiency virus replication. Blood 89:1357-1363.
94. + T cells. J. Exp. Med. 171:1269-1281.
95. Smyth, M. J., Y. Norihisa, and J. R. Ortaldo. 1992. Multiple cytolytic mechanisms displayed by activated human peripheral blood T cell subsets. J. Immunol. 148:55-62.
96. Smyth, M. J., and J. A. Trapani. 1995. Granzymes: exogenous proteinases that induce target cell apoptosis. Immunol. Today 19:202-206.
97. Smyth, M. J. 1997. FasL-mediated bystander lysis of syngeneic cells in response to an allogeneic stimulus. J. Immunol. 158:5765-5772.
98. Song, Q., S. R. Burrows, G. Smith, S. P. Lees-Miller, S. Kumar, D. W. Chan, J. A. Trapani, E. Alnemri, G. Litwack, H. Lu, D. J. Moss, S. Jackson, and M. F. Lavin. 1996. Interleukin-1 beta converting enzyme-like protease cleaves DNA-dependent protein kinase in cytotoxic T cell killing. J. Exp. Med. 184:619-626.
99. Sower, L. E., C. J. Froelich, N. Allegretto, P. M. Rose, W. D. Hanna, and G. R. Klimpel. 1996. Extracellular activities of human granzyme A. Monocyte activation by granzyme A versus alpha-thrombin. J. Immunol. 156:2585-2590.
100. + T-cell-deficient mice survive inoculation with high doses of vaccinia virus and exhibit altered IgG responses. Proc. Natl. Acad. Sci. USA 89:6070-6074.
101. Srinivasula, S. M., T. Fernandes-Alnemri, J. Zangrilli, N. Robertson, R. C. Armstrong, L. Wang, J. A. Trapani, K. J. Tomaselli, G. Litwack, and E. S. Alnemri. 1996. The Ced-3/interleukin 1beta converting enzyme-like homolog Mch6 and the lamin-cleaving enzyme Mch2alpha are substrates for the apoptotic mediator CPP32. J. Biol. Chem. 271:27099-27106.
102. Suda, T., and S. Nagata. 1994. Purification and characterization of the Fas-ligand that induces apoptosis. J. Exp. Med. 179:873-879.
103. Sytwu, H. K., R. S. Liblau, and H. O. McDevitt. 1996. The roles of Fas/ APO-1 (CD95) and TNF in antigen-induced programmed cell death in T cell receptor transgenic mice. Immunity 5:17-30.
104. + T cells or perforin. J. Virol. 71:1808-1813.
105. Tartaglia, L. A., T. M. Ayres, G. H. W. Wong, and D. V. Goeddel. 1993. A novel domain within the 55 kd TNF receptor signals cell death. Cell 74:845-853.
106. Tay, C. H., and R. M. Welsh. 1997. Distinct organ-dependent mechanisms for the control of murine cytomegalovirus infection by natural killer cells. J. Virol. 71:267-275.
107. Tewari, M., and V. M. Dixit. 1995. Fas- and tumor necrosis factor-induced apoptosis is inhibited by the poxvirus crmA gene product. J. Biol. Chem. 270:3255-3260.
108. Thome, M., P. Schneider, K. Hofmann, H. Fickenscher, E. Meinl, F. Neipel, C. Mattmann, K. Burns, J. L. Bodmer, M. Schroter, C. Scaffidi, P. H. Krammer, M. E. Peter, and J. Tschopp. 1997. Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 386:517-521.
109. Trapani, J. A., K. A. Browne, M. J. Smyth, and D. A. Jans. 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.
110. Trauth, B. C., C. Klas, A. M. J. Peters, S. Matzku, P. Moller, W. Falk, K. M. Debatin, and P. H. Krammer. 1989. Monoclonal antibody-mediated tumor regression by induction of apoptosis. Science 245:301-305.
111. Tschopp, J., and M. Nabholz. 1990. Perforin-meuiated target cell lysis by cytolytic T lymphocytes. Annu. Rev. Immunol. 8:279-302.
112. Walsh, C. M., M. Matloubian, C.-C. Liu, R. Ueda, C. G. Kurahara, J. L. Christensen, M. T. Huang, J. D. Young, R. Ahmed, and W. R. Clark. 1994. Immune function in mice lacking the perforin gene. Proc. Natl. Acad. Sci. USA 91:10854-10858.
113. Welsh, R. M. 1981. Natural cell-mediated immunity during viral infections. Curr. Top. Microbiol. Immunol. 92:83-106.
114. Westendorp, M. O., R. Frank, C. Ochsenbauer, K. Stricker, J. Dhein, H. Walczak, K. M. Debatin, and P. H. Krammer. 1995. Sensitization of T cells to CD95-mediated apoptosis by HIV-1 Tat and gp120. Nature 375:497-500.
115. Wiertz, E. J. H. J., T. R. Jones, L. Sun, M. Bogyo, H. J. Geuze, and H. L. Ploegh. 1996. The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell 84:769-779.
116. Xu, X.-N., G. R. Screaton, F. M. Gotch, T. Dong, R. Tan, N. Almond, B. Walker, R. Stebbings, K. Kent, S. Nagata, J. E. Stott, and A. J. McMichael. 1997. Evasion of cytotoxic T lymphocyte (CTL) responses by nef-dependent induction of Fas ligand (CD95L) expression on simian immunodeficiency virus-infected cells. J. Exp. Med. 186:7-16.
117. Yokoyama, W. M., and W. E. Seaman. 1993. The Ly-49 and NKR-P1 gene families encoding lectin like receptors on natural killer cells: the NK gene complex. Annu. Rev. Immunol. 11:613-635.
118. Yoshida, H., H. Sumichika, S. Hamano, X. He, Y. Minamishima, G. Kimura, and K. Nomoto. 1995. Induction of apoptosis of T cells by infecting mice with murine cytomegalovirus. J. Virol. 69:4769-4775.
119. Yuan, J. 1997. Transducing signals of life and death. Curr. Opin. Cell. Biol. 9:247-251.
120. + cytotoxic T-cell-mediated pathogenesis during virus infection. Proc. Natl. Acad. Sci. USA 93:14730-14735.
121. Zheng, L., G. Fisher, R. E. Miller, J. Peschon, D. H. Lynch, and M. L. Lenardo. 1995. Induction of apoptosis in mature T cells by tumour necrosis factor. Nature 377:348-351.
122. Ziegler, H., R. Thale, P. Lucin, W. Muranyi, T. Flohr, H. Hengel, H. Farrell, W. Rawlinson, and U. H. Koszinowski. 1997. A mouse cytomegalovirus glycoprotein retains MHC class I complexes in the ERGIC/cis-Golgi compartments. Immunity 6:57-66.
123. Zinkernagel, R. M., and K. L. Rosenthal. 1981. Experiments and speculation on antiviral specificity of T and B cells. Immunol. Rev. 58:131-155.
124. Zinkernagel, R. M., and H. Hengartner. 1994. T-cell-mediated immunopathology versus direct cytolysis by virus: implications for HIV and AIDS. Immunol. Today 15:262-268.