Evasion of apoptosis by DNA viruses

Immunology and Cell Biology

Volumn 74, Issue 6, 1996, Pages 527-537

  Cuff, Simone ^a   Ruby, Janet ^b  

^a Australian National University   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

adenovirus; apoptosis; crmA; E1A; E1B 19K; E1B 55K; poxvirus

Indexed keywords

PROTEIN P53;

ADENOVIRUS; APOPTOSIS; CELL CYCLE; CYTOTOXIC T LYMPHOCYTE; HOST RESISTANCE; HUMAN; MOUSE; NONHUMAN; POXVIRUS; RAT; REVIEW;

ADENOVIRIDAE; DNA VIRUSES; POXVIRIDAE;

EID: 0029772185     PISSN: 08189641     EISSN: None     Source Type: Journal    
DOI: 10.1038/icb.1996.86     Document Type: Review

References (137)

1. Darmon A, Nicholson D, Bleackley R. Activation of the apoptotic protease CPP32 by cytotoxic T cell-derived granzyme B. Nature 1995; 377: 446-8.
2. Puisieux A, Ji J, Guillot C et al. p53-mediated cellular response to DNA damage in cells with replicative hepatitis B virus. Proc. Natl Acad. Sci. USA 1995; 92: 1342-6.
3. Hale A, Smith C, Sutherland L et al. Apoptosis: molecular regulation of cell death. Eur. J. Biochem. 1996; 236: 1-26.
4. Savill J, Dransfield I, Hogg N, Haslett C. Vitronectin receptor-mediated phagocytosis of cells undergoing apoptosis. Nature 1990; 343: 170-3.
5. Savill J, Fadok V, Henson P, Haslett C. Phagocyte recognition of cells undergoing apoptosis. Immunol. Today 1993; 14: 131-6.
6. Ren Y, Silverstein R, Allen J, Savill J. CD36 gene transfer confers capacity for phagocytosis of cells undergoing apoptosis. J. Exp. Med. 1995; 181: 1857-62.
7. Zamzami N, Marchetti P, Castedo M et al. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J. Exp. Med. 1995; 182: 367-77.
8. Pilder S, Logan J, Shenk T. Deletion of the gene encoding the adenovirus 5 early region 1B-21 000-molecular weight polypeptide leads to a degradation of viral and cellular DNA. J. Virol. 1984; 52: 664-71.
9. Liebermann D, Hoffman B, Steinman R. Molecular controls of growth arrest and apoptosis: p53-dependent and independent pathways. Oncogene 1995; 11: 199-210.
10. Meikrantz W, Schlegel R. Apoptosis and the cell cycle. J. Cell. Biochem. 1995; 58: 160-74.
11. Olson D, Marechal V, Momand J, Chen J, Romocki C, Levine A. Identification and characterization of multiple mdm-2 proteins and mdm-2-p53 protein complexes. Oncogene 1993; 8: 2353-60.
12. Shaulian E, Zauberman A, Ginsberg D, Wagner E, Oren M. Identification of a minimal transforming domain of p53: negative dominance through abrogation of sequence-specific DNA binding. Mol. Cell Biol. 1992; 12: 5581-92.
13. Hupp T, Lane D. Allosteric activation of latent p53 tetramers. Curr. Biol. 1994; 4: 865-75.
14. Miyashita T, Reed JC. Tumor suppressor p53 is a direct transcriptional activator of the human bax gene. Cell 1995; 80: 293-9.
15. Barak Y, Juven T, Haffner R, Oren M. Mdm-2 expression is induced by wild-type p53 activity. EMBO J. 1993; 12: 461-8.
16. Wu X, Bayle J, Olson D, Levine A. The p53-mdm-2 autoregulatory feedback loop. Genes Dev. 1993; 7: 1126-32.
17. Okamoto K, Beach D. Cyclin G is a transcriptional target of the p53 tumor suppressor protein. EMBO J. 1994; 13: 4816-22.
18. Zauberman A, Lupo A, Oren M. Identification of p53 target genes through immune selection of genomic DNA: the cyclin G gene contains two distinct p53 binding sites. Oncogene 1995; 10: 2361-6.
19. El-Deiry W, Tokino T, Velculescu V et al. WAF1, a potential mediator of p53 tumor suppression. Cell 1993; 75: 817-25.
20. Harper J, Adami G, Wei N, Keyomarsi K, Elledge S. The p21 Cdk-interacting protein Cip-1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 1993; 75: 805-16.
21. Shio Y, Yamamoto T, Yamaguchi N. Negative regulation of Rb expression by the p53 gene product. Proc. Natl Acad. Sci. USA 1992; 89: 5206-10.
22. Seto E, Usheva A, Zambetti G et al. Wild-type p53 binds to the TATA-binding protein and represses transcription. Proc. Natl Acad. Sci. USA 1992; 89: 12 028-32.
23. Momand J, Zambetti G, Olson D, George D, Levine A. The mdm-2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 1992; 69: 1237-45.
24. Chen C, Oliner J, Zhan Q, Fornace AJ Jr, Vogelstein B, Kastan M. Interactions between p53 and MDM2 in a mammalian cell cycle checkpoint pathway. Proc. Natl Acad. Sci. USA 1994; 91: 2684-8.
25. Cobrinik D. Regulatory interactions among E2Fs and cell cycle control proteins. Curr. Top. Microbiol. Immunol. 1996; 208: 31-62.
26. Slansky J, Farnham P. Introduction to the E2F family: protein structure and gene regulation. Curr. Top. Microbiol. Immunol. 1996; 208: 1-30.
27. Blake M, Azizkhan J. Transcription factor E2F is required for efficient expression of the hamster dihydrofolate reductase gene in vitro and in vivo. Mol. Cell. Biol. 1989; 9: 4994-5002.
28. Mudryj M, Hiebert S, Nevins J. A role for the adenovirus inducible E2F transcription factor in a proliferation dependent signal transduction pathway. EMBO J. 1990; 9: 2179-84.
29. Pearson B, Nasheuer H, Wang T. Human DNA polymerase alpha gene: sequences controlling expression in cycling and serum-stimulated cells. Mol. Cell. Biol. 1991; 11: 2081-95.
30. Sala A, Nicolaides N, Engelhard A et al. Correlation between E2F-1 requirement in the S phase and E2F-1 transactivation of cell cycle-related genes in human cells. Cancer Res. 1994; 54: 1402-6.
31. DeGregori J, Kowalik T, Nevins J. Cellular targets for activation by the E2F1 transcription factor include DNA synthesis- and G1/S-regulatory genes. Mol. Cell. Biol. 1995; 15: 4215-24.
32. Dou Q, Markell P, Pardee A. Thymidine kinase transcription is regulated at G1/S phase by a complex that contains retinoblastoma-like protein and a cdc-2 kinase. Proc. Natl Acad. Sci. USA 1992; 89: 3256-60.
33. Tommasi S, Pfeifer G. In vivo structure of the human cdc2 promoter: release of a p130-E2F-4 complex from sequences immediately upstream of the transcription initiation site coincides with induction of cdc2 expression. Mol. Cell. Biol. 1995; 15: 6901-13.
34. Schulze A, Zerfass K, Spitkovsky D et al. Cell cycle regulation of the cyclin A gene promoter is mediated by a variant E2F site. Proc. Natl Acad. Sci. USA 1995; 92: 11 264-8.
35. Motokura T, Arnold A. PRAD1/cyclin D1 proto-oncogene: genomic organisation, 5′ DNA sequence, and sequence of a tumor-specific rearrangement break-point. Genes Chromosom. Cancer 1993; 7: 89-95.
36. Duronio R, O'Farrell P. Developmental control of the G1 to S transition in Drosophila: Cyclin E is a limiting downstream target of E2F. Genes Dev. 1995; 9: 1445-55.
37. Bagchi S, Weinmann R, Raychaudhuri P. The retinoblastoma protein copurifies with E2F-1, an E1A-regulated inhibitor of the transcription factor E2F. Cell 1991; 65: 1063-72.
38. Zhu L, Zhu L, Xie E, Chang L. Differential roles of two tandem E2F sites in repression of the human p 107 promoter by retinoblastoma and p 107 proteins. Mol. Cell. Biol. 1995; 15: 3552-62.
39. Hsaio K, McMahon S, Farnham P. Multiple DNA elements are required for the growth regulation of the mouse E2F1 promoter. Genes Dev. 1994; 8: 1526-37.
40. Johnson D, Ohtani K, Nevins J. Autoregulatory control of E2F-1 expression in response to positive and negative regulators of cell cycle expression. Genes Dev. 1994; 8: 1514-25.
41. Neuman E, Flemington E, Sellers W, Kaelin W. Transcription of the E2F1 gene is rendered cell cycle-dependent by E2F DNA binding sites within its promoter. Mol. Cell. Biol. 1994; 14: 6607-15.
42. Adnane J, Shao Z, Robbins P. The retinoblastoma susceptibility gene product represses transcription when directly bound to the promoter. J Biol. Chem. 1995; 270: 8837-43.
43. Zhu L, Harlow E, Dynlacht B. p 107 uses a p21CIP1-related domain to bind cyclin/cdk2 and regulate interactions with E2F. Genes Dev. 1995; 9: 1740-52.
44. Miyashita T, Krajewski S, Krajewska M et al. Tumor-suppressor p53 is a regulator of bcl-2 and bax gene-expression in vitro and in vivo. Oncogens 1994; 9: 1799-1805.
45. Oltvai Z, Milliman C, Korsmeyer S. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell 1993; 74: 609-19.
46. Chiou S, Rao L, White E. Bcl-2 blocks p53-dependent apoptosis. Mol. Cell. Biol. 1994; 14: 2556-63.
47. Sabbatini P, Chiou S, Rao L, White E. Modulation of p53-mediated transcriptional repression and apoptosis by the adenovirus E1B 19K protein. Mol. Cell. Biol. 1995; 15: 1060-70.
48. Shan B, Lee W. Deregulated expression of E2F-1 induces S-phase entry and leads to apoptosis. Mol. Cell. Biol. 1994; 14: 8166-73.
49. Kowalik T, DeGregori J, Schwarz J, Nevins J. E2F1 overexpression in quiescent fibroblasts leads to induction of cellular DNA synthesis and apoptosis. J. Virol. 1995; 69: 2491-500.
50. Wu X, Levine A. p53 and E2F1 cooperate to mediate apoptosis. Proc. Natl Acad. Sci. USA 1994; 91: 3602-6.
51. Qin X, Livingston D, Kaelin WG Jr, Adams P. Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53-mediated apoptosis. Proc. Natl Acad. Sci. USA 1994; 91: 10 918-22.
52. White E. Regulation of p53-dependent apoptosis by E1A and E1B. Curr. Top. Microbiol. Immunol. 1996; 199: 33-58.
53. Boyd J, Malstrom S, Subramanian T et al. Adenovirus E1B-19K and Bcl-2 proteins interact with a common set of cellular proteins. Cell 1994; 79: 341-51.
54. Yew P, Berk A. Inhibition of p53 transactivation required for transformation by adenovirus early 1B protein. Nature 1992; 357: 82-5.
55. Zheng D, Vayssiere J, Petit P et al. Apoptosis is antagonized by large T antigens in the pathway to immortalization by polyomaviruses. Oncogene 1994; 9: 3345-51.
56. Scheffner M, Huibregtse J, Vierstra R, Howley P. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 1993; 75: 495-505.
57. Dyson N, Howley P, Munger K, Harlow E. The human papillomavirus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product. J. Virol. 1989; 66: 4606-11.
58. Boulanger P, Blair G. Expression and interactions of human adenovirus oncoproteins. Biochem. J. 1991; 275: 281-99.
59. Raychaudhuri P, Bagchi S, Devoto S, Kraus V, Moran E, Nevins J. Domains of the adenovirus E1A protein required for oncogenic activity are also required for dissociation of E2F transcription factor complexes. Curr. Top. Microbiol. Immunol. 1991; 208: 63-78.
60. Reed S. The role of p34 kinases in the G1 to S phase transition. Annu. Rev. Cell Biol. 1992; 8: 529-61.
61. Ikeda M-A, Nevins J. Identification of distinct roles for separate ElA domains in the disruption of E2F complexes. Mol. Cell. Biol. 1993; 13: 7029-35.
62. Fattaey A, Harlow E, Helin K. Independent regions of adenovirus ElA are required for binding to and dissociation of E2F-protein complexes. Mol. Cell. Biol. 1993; 13: 7267-77.
63. Jones N. Transcriptional modulation by the adenovirus E1A gene. Curr. Top. Microbiol. Immunol. 1995; 208: 59-80.
64. White E, Sabbatini P, Debbas M, Wold W, Kusher D, Gooding L. The 19-kilodalton adenovirus E1B transforming protein inhibits programmed cell death and prevents cytolysis by tumor necrosis factor alpha. Mol. Cell. Biol. 1992; 12: 2570-80.
65. Rao L, Debbas M, Sabbatini P, Hockenberry D, Korsmeyer S, White E. The adenovirus E1A proteins induce apoptosis which is inhibited by the E1B 19K and Bcl-2 proteins (published erratum appears in Proc. Natl Acad. Sci. USA 1992; 89: 9974). Proc. Natl Acad. Sci. USA 1992; 89: 7742-6.
66. Subramanian T, Kupposwamy M, Gysbers J, Mak S, Chinnadurai G. 19-kDa tumor antigen coded by early region E1b of adenovirus 2 is required for efficient synthesis and for protection of viral DNA. J. Biol. Chem. 1984; 259: 11 777-83.
67. Morganbesser S, Williams B, Jacks T, Depino R. p53-dependent apoptosis produced by Rb-deficiency in the eye. Nature 1994; 371: 72-4.
68. Kao C, Yew P, Berk A. Domains required for in vitro association between the cellular p53 and the adenovirus 2 ElB 55K proteins. Virology 1990; 179: 806-14.
69. Zantema A, Frasen J, Davis-Olivier A et al. Localisation of the E1B proteins of adenovirus 5 in transformed cells, as revealed by interaction with monoclonal antibodies. Virology 1985; 142: 44-58.
70. Zantema A, Schrier P, Davis-Olivier A, Laar TV, Vaessen R, Van-der-Eb A. Adenovirus serotype determines association and localisation of the large E1B tumor antigen with cellular tumor antigen p53 in transformed cells. Mol. Cell. Biol. 1985; 5: 3084-91.
71. Steegenga W, Van-Laar T, Shvarts A, Terleth C, Van-der-Eb A, Jochemsen-AG A. Distinct modulation of p53 activity in transcription and cell-cycle regulation by the large (54 kDa) and small (21 kDa) adenovirus E1B proteins. Virology 1995; 212: 543-54.
72. Gooding L, Aquino L, Duerksen-Hughes P et al. The E1B-19K protein of group C adenoviruses prevents cytolysis by tumor necrosis factor of human cells but not mouse cells. J. Virol. 1991; 65: 3083-94.
73. Hashimoto S, Ishii A, Yonehara S. The E1B oncogene of adenovirus confers cellular resistance to cytotoxicity of tumor necrosis factor and monoclonal anti-Fas antibody. Int. Immunol. 1991; 3: 343-51.
74. Debbas M, White E. Wild-type p53 mediates apoptosis by E1A which is inhibited by E1B. Genes Dev. 1993; 7: 546-54.
75. Chiou S, Tseng C, Rao L, White E. Functional complementation of the adenovirus E1B 19K protein with Bcl-2 in the inhibition of apoptosis in infected cells. J. Virol. 1994; 68: 6553-66.
76. Han J, Sabbatini P, Perez D, Rao L, Modha D, White E. The E1B 19K protein blocks apoptosis by interacting with and inhibiting the p53-inducible and death-promoting Bax protein. Genes Dev. 1996; 10: 461-77.
77. Pickup D, Ink B, Hu W, Ray C, Joklik W. Hemorrhage in lesions caused by cowpox virus is induced by a viral protein that is related to plasma protein inhibitors of serine proteases. Proc. Natl Acad. Sci. USA 1986; 83: 7698-702.
78. Hu F, Smith C, Pickup D. Cowpox virus contains two copies of an early gene encoding a soluble secreted form of the type II TNF receptor. Virology 1994; 204: 343-56.
79. Spriggs M, Hruby D, Maliszewski C et al. Vaccinia and cowpox viruses encode a novel secreted interleukin-1-binding protein. Cell 1992; 71: 145-52.
80. All A, Turner P, Brooks M, Moyer R. The SPI-1 gene of rabbitpox virus determines host range and is required for hemorrhagic pock formation. Virology 1994; 202: 305-14.
81. Schreiber M, McFadden G. The myxoma virus TNF-receptor homologue (T2) inhibits tumor necrosis factor-alpha in a species-specific fashion. Virology 1994; 204: 692-705.
82. Upton C, Mossman K, McFadden G. Encoding of a homolog of the IFN-gamma receptor by myxoma virus. Science 1992; 258: 1369-72.
83. Zhou J, Sun X, Fernando G, Frazer I. The vaccinia virus K2L gene encodes a serine protease inhibitor which inhibits cell fusion. Virology 1992; 189: 678-86.
84. Turner P, Moyer R. Orthopoxvirus fusion inhibitor glycoprotein SPI-3 (open reading frame K2L) contains motifs characteristic of serine protease inhibitors that are not required for control of cell fusion. J. Virol. 1995; 69: 5978-87.
85. Kotwal G, Moss B. Vaccinia virus encodes two proteins that are structurally related to members of the plasma serine protease inhibitor superfamily (published erratum appears in J. Virol. 1990; 64: 966). J. Virol. 1989; 63: 600-6.
86. Howard A, Kostura M, Thornberry N et al. IL-1-converting enzyme requires aspartic acid residues for processing of the IL-1 beta precursor at two distinct sites and does not cleave 31-kDa IL-1 alpha. J. Immunol. 1991; 147: 2964-9.
87. Alcami A, Smith G. Vaccinia, cowpox, and camelpox viruses encode soluble gamma interferon receptors with novel broad species specificity. J. Virol. 1995; 69: 4633-9.
88. Alcami A, Smith G. A soluble receptor for interleukin-1 beta encoded by vaccinia virus: a novel mechanism of virus modulation of the host response to infection. Cell 1992; 71: 153-67.
89. Howard S, Chan Y, Smith G. Vaccinia virus homologues of the Shope fibroma virus inverted terminal repeat proteins and a discontinuous ORF related to the tumor necrosis factor receptor family. Virology 1991; 180: 633-47.
90. McFadden G. DNA viruses that affect cytokine networks. In: Aggarwal B, Puri R, eds. Human Cytokines: Their Role in Health and Disease. Cambridge, MA: Blackwell Science, 1994; 403-22.
91. Chacon M, Almazan F, Nogal M, Vinuela E, Rodriguez J. The African swine fever virus IAP homolog is a late structural polypeptide. Virology 1995; 214: 670-4.
92. Dixon L, Baylis S, Vydelingum S et al. African Swine Fever Virus genome content and variability. Arch. Virol. 1993; 7 (Suppl.): S185-99.
93. Neilan J, Lu Z, Alfonso C, Kutish G, Sussman M, Rock D. An african swine fever virus gene with similarity to the proto-oncogene bcl-2 and the Epstein-Barr virus gene BHRF1. J. Virol. 1993;67:4391-4.
94. Yanez R, Rodriguez J, Nogal M et al. Analysis of the complete nucleotide sequence of african swine fever virus. Virology 1995; 208: 249-78.
95. Henderson S, Rowe M, Gregory C et al. Induction of bcl-2 expression by Epstein-Barr virus latent membrane protein 1 protects infected B cells from programmed cell death. Cell 1991; 65: 1107-15.
96. Tewari M, Wolf F, Seldin M, O'Shea K, Dixit V, Turka L. Lymphoid expression and regulation of A20, an inhibitor of programmed cell death. J. Immunol. 1995; 154: 1699-1706.
97. Henderson S, Huen D, Rowe M, Dawson C, Johnson G, Rickinson A. Epstein-Barr virus-coded BHRF1 protein, a viral homolog of Bcl-2 protects human B cells from programmed cell death. Proc. Natl Acad. Sci. USA 1993; 90: 8479-83.
98. Smith C. A novel viral homologue of bcl-2 and ced-9. Trends Cell. Biol. 1995; 5: 344-7.
99. Truant R, Antunovic J, Greenblatt J, Prives C, Cromlish J. Direct interaction of the hepatitis B virus HBx protein with p53 leads to inhibition by HBx of p53 response element-directed transactivation. J. Virol. 1995; 69: 1851-9.
100. Henkart P. ICE family proteases: mediators of all cell death? Immunity 1996; 4: 195-201.
101. Kayalar C, Ord T, Testa MP, Zhong L-T, Bredesen D. Cleavage of actin by interleukin 1 beta-converting enzyme to reverse DNase I inhibition. Proc. Natl Acad. Sci. USA 1996; 93: 2234-8.
102. Gu Y, Sarnecki C, Aldape R, Livingston D, Su M. Cleavage of poly(ADP-ribose) polymerase by interleukin-1 beta converting enzyme and its homologs TX and Nedd-2. J. Biol. Chem. 1995; 270: 18715-8.
103. Tewari M, Quan L, O'Rourke K et al. Yama/CPP32 beta, a mammalian homolog of CED-3, is a CrmA-inhibitable protease that cleaves the death substrate poly(ADP-ribose) polymerase. Cell 1995; 81: 801-9.
104. Casciola-Rosen L, Miller D, Anhalt G, Rosen A. Specific cleavage of the 70-kDa protein component of the U1 small nuclear ribonucleoprotein is a characteristic biochemical feature of apoptotic cell death. J. Biol Chem. 1994; 269: 30757-60.
105. Lazebnik Y, Takahashi A, Moir R et al. Studies of the lamin proteinase reveal multiple parallel biochemical pathways during apoptotic execution. Proc. Natl Acad. Sci. USA 1995; 92: 9042-6.
106. Mashima T, Naito M, Fujita N, Noguchi K, Tsuruo T. Identification of actin as a substrate of ICE and an ICE-like protease and involvement of an ICE-like protease but not ICE in VP-16-induced U937 apoptosis. Biochem. Biophys. Res. Commun. 1995; 217: 1185-92.
107. Enari M, Talanian R, Wong W, Nagata S. Sequential activation of ICE-like and CPP32-like proteases during Fas-mediated apoptosis. Nature 1996; 380: 723-6.
108. Komiyama T, Ray C, Pickup D et al. Inhibition of interleukin-1 beta converting enzyme by the cowpox virus serpin CrmA. An example of cross-class inhibition. J. Biol. Chem. 1994; 269: 19 331-7.
109. Quan L, Caputo A, Bleackley R, Pickup D, Salvesen G. Granzyme B is inhibited by the cowpox virus serpin cytokine response modifier A. J. Biol. Chem. 1995; 270: 10 377-9.
110. Tewari M, Telford W, Miller R, Dixit V. CrmA, a poxvirus-encoded serpin, inhibits cytotoxic T-lymphocyte-mediated apoptosis. J. Biol. Chem. 1995; 270: 22 705-8.
111. Los M, Van-de-Craen M, Penning L et al. Requirement of an ICE/CED-3 protease for Fas/APO-1-mediated apoptosis. Nature 1995; 375: 81-3.
112. Miura M, Friedlander R, Yuan J. Tumor necrosis factor-induced apoptosis is mediated by a CrmA-sensitive cell death pathway. Proc. Natl Acad. Sci. USA 1995; 92: 8318-22.
113. Ray C, Black R, Kronheim S et al. Viral inhibition of inflammation: cowpox virus encodes an inhibitor of the interleukin-1 beta converting enzyme. Cell 1992; 69: 597-604.
114. Henkart P. Lymphocyte-mediated cytotoxicity: two pathways and multiple effector molecules. Immunity 1994; 1: 343-6.
115. Podack E, Young J, Cohn Z. Isolation and biochemical and functional characterization of perforin 1 from cytolytic T-cell granules. Proc. Natl Acad. Sci. USA 1985; 82: 8629-33.
116. Liu C, Persechini P, Young J. Perforin and lymphocyte-mediated cytolysis. Immunol. Rev. 1995; 146: 145-75.
117. Lowin B, Peitsch M, Tschopp J. Perforin and granzymes: crucial effector molecules in cytolytic T lymphocyte and natural killer cell-mediated cytotoxicity. Curr. Top. Microbiol. Immunol. 1995; 198: 1-24.
118. Irmler M, Hertig S, MacDonald H et al. Granzyme A is an interleukin 1 beta-converting enzyme. J. Exp. Med. 1995; 181: 1917-22.
119. Mizutani H, Black R, Kupper T. Human keratinocytes produce but do not process pro-interleukin-1 (IL-1) beta. Different strategies of IL-1 production and processing in monocytes and keratinocytes. Proc. Natl Acad. Sci. USA 1991; 90: 1809-13.
120. Ebnet K, Hausmann M, Lehmann-Grube F et al. Granzyme A-deficient mice retain potent cell-mediated cytotoxicity. EMBO J. 1995; 14: 4230-9.
121. Hsu H, Xiong J, Goeddel D. The TNF receptor 1-associated protein TRADD signals cell death and NF-kappa B activation. Cell 1995; 81: 495-504.
122. Aggarwal B, Singh S, LaPushin R, Totpal K. Fas antigen signals proliferation of normal human diploid fibroblast and its mechanism is different from tumor necrosis factor receptor. FEBS Lett. 1995; 364: 5-8.
123. Nagata S, Golstein P. The Fas death factor. Science 1995; 267: 1449-56.
124. Enari M, Hug H, Nagata S. Involvement of an ICE-like protease in Fas-mediated apoptosis. Nature 1995; 375: 78-81.
125. Tewari M, Beidler D, Dixit V. CrmA-inhibitable cleavage of the 70-kDa protein component of the U1 small nuclear ribonucleoprotein during Fas- and tumor necrosis factor-induced apoptosis. J. Biol. Chem. 1995; 270: 18 738-41.
126. Tewari M, Dixit V. Fas- and tumor necrosis factor-induced apoptosis is inhibited by the poxvirus crmA gene product. J. Biol. Chem. 1995; 270: 3255-60.
127. Chinnaiyan A, O'Rourke K, Tewari M, Dixit V. FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell 1995; 81: 505-12.
128. Boldin M, Goncharov T, Goltsev Y, Wallach D. Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1- and TNF receptor-induced cell death. Cell 1996; 85: 803-15.
129. Muzio M, Chinnaiyan A, Kischkel F et al. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signal complex. Cell 1996; 85: 817-27.
130. Fernandes-Alnemri T, Armstrong R, Krebs J et al. In vitro activation of CPP32 and Mch3 by Mch4, a novel human apoptotic cysteine protease containing two FADD-like domains. Proc. Natl Acad. Sci. USA 1996; 93: 7464-9.
131. Hsu H, Shu H, Pan M, Goeddel D. TRADD-TRAF2 and TRADD-FADD interactions define two distinct TNF receptor 1 signal transduction pathways. Cell 1996; 84: 299-308.
132. Wong G, Goeddel D. Tumour necrosis factors alpha and beta inhibit virus replication and synergise with interferons. Nature 1986; 322: 819-22.
133. Gold R, Toyka K, Hartung H. Synergistic effect of IFN-gamma and TNFalpha on expression of immune molecules and antigen presentation by Schwann cells. Cell. Immunol. 1995; 165: 65-70.
134. Mossman K, Nation P, Macen J, Garbutt M, Lucas A, McFadden G. Myxoma virus M-T7, a secreted homolog of the interferon-gamma receptor, is a critical virulence factor for the development of myxomatosis in European rabbits. Virology 1996; 215: 17-30.
135. Upton C, Macen J, Schreiber M, McFadden G. Myxoma virus expresses a secreted protein with homology to the tumor necrosis factor receptor gene family that contributes to viral virulence. Virology 1991; 184: 370-82.
136. Macen J, Graham K, Lee S, Schreiber M, Boshkov L, McFadden G. Expression of the myxoma virus tumor necrosis factor receptor homologue and M11L genes is required to prevent virus-induced apoptosis in infected rabbit T lymphocytes. Virology 1996; 218: 232-7.
137. Ray C, Pickup D. The mode of death of pig kidney cells infected with cowpox virus is governed by the expression of the crmA gene. Virology 1996; 217: 384-91.