Near death experiences: Poxvirus regulation of apoptotic death

Virology

Volumn 344, Issue 1, 2006, Pages 139-150

  Taylor, John M ^a   Barry, Michele ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS; CELL DEATH; CELL SURVIVAL; CHORDOPOXVIRINAE; EFFECTOR CELL; ENTOMOPOXVIRUS; ENZYME ACTIVATION; LEPORIPOXVIRUS; MITOCHONDRION; NONHUMAN; ORTHOPOXVIRUS; POXVIRUS; POXVIRUS INFECTION; PRIORITY JOURNAL; PROTEIN BINDING; REVIEW; VACCINIA VIRUS; VIRUS INFECTION;

ANIMALS; ANTIGENS, HELMINTH; APOPTOSIS; CELL DEATH; HELMINTH PROTEINS; HUMANS; INHIBITOR OF APOPTOSIS PROTEINS; MITOCHONDRIA; POXVIRIDAE; POXVIRIDAE INFECTIONS; RECEPTORS, TUMOR NECROSIS FACTOR; SERPINS; UBIQUITIN-PROTEIN LIGASES; VIRAL PROTEINS; VIRUS REPLICATION;

CHORDOPOXVIRINAE; LEPORIPOXVIRUS; ORTHOPOXVIRUS; POXVIRIDAE; VACCINIA VIRUS;

EID: 29144495592     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2005.09.032     Document Type: Review

References (145)

1. C.L. Afonso, E.R. Tulman, Z. Lu, E. Oma, G.F. Kutish, and D.L. Rock The genome of Melanoplus sanguinipes entomopoxvirus J. Virol. 73 1 1999 533 552
2. C.L. Afonso, E.R. Tulman, Z. Lu, L. Zsak, G.F. Kutish, and D.L. Rock The genome of fowlpox virus J. Virol. 74 2000 3815 3831
3. D. Arnoult, L.M. Bartle, A. Skaletskaya, D. Poncet, N. Zamzami, P.U. Park, J. Sharpe, R.J. Youle, and V.S. Goldmacher Cytomegalovirus cell death suppressor vMIA blocks Bax- but not Bak-mediated apoptosis by binding and sequestering Bax at mitochondria Proc. Natl. Acad. Sci. U.S.A. 101 21 2004 7988 7993
4. A. Ashkenazi Targeting death and decoy receptors of the tumour-necrosis factor superfamily Nat. Rev., Cancer 2 6 2002 420 430
5. E. Baixeras, A. Cebrian, J.P. Albar, J. Salas, A.C. Martinez, E. Vinuela, and Y. Revilla Vaccinia virus-induced apoptosis in immature B lymphocytes: role of cellular Bcl-2 Virus Res. 58 1998 107 113
6. M. Barry, and R.C. Bleackley Cytotoxic T lymphocytes: all roads lead to death Nat. Rev., Immunol. 2 6 2002 401 409
7. M. Barry, S. Hnatiuk, K. Mossman, S.F. Lee, L. Boshkov, and G. McFadden The myxoma virus M-T4 gene encodes a novel RDEL-containing protein that is retained within the endoplasmic reticulum and is important for the productive infection of lymphocytes Virology 239 2 1997 360 377
8. M. Barry, J.A. Heibein, M.J. Pinkoski, S.F. Lee, R.W. Moyer, D.R. Green, and R.C. Bleackley Granzyme B short-circuits the need for caspase 8 activity during granule-mediated cytotoxic T-lymphocyte killing by directly cleaving Bid Mol. Cell. Biol. 20 11 2000 3781 3794
9. M. Barry, S.T. Wasilenko, T.L. Stewart, and J.M. Taylor Apoptosis regulator genes encoded by poxviruses Prog. Mol. Subcell. Biol. 36 2004 19 37
10. A.L. Bawden, K.J. Glassberg, J. Diggans, R. Shaw, W. Farmerie, and R.W. Moyer Complete genomic sequence of the Amsacta moorei entomopoxvirus: analysis and comparison with other poxviruses Virology 274 1 2000 120 139
11. C.A. Benedict, P.S. Norris, and C.F. Ware To kill or be killed: viral evasion of apoptosis Nat. Immunol. 3 11 2002 1013 1018
12. A. Bergmann, A.Y. Yang, and M. Srivastava Regulators of IAP function: coming to grips with the grim reaper Curr. Opin. Cell Biol. 15 6 2003 717 724
13. J. Bertin, R.C. Armstrong, S. Ottilie, D.A. Martin, Y. Wang, S. Banks, G.H. Wang, T.G. Senkevich, E.S. Alnemri, B. Moss, M.J. Lenardo, K.J. Tomaselli, and J.I. Cohen Death effector domain-containing herpesvirus and poxvirus proteins inhibit both Fas- and TNFR1-induced apoptosis Proc. Natl. Acad. Sci. U.S.A. 94 4 1997 1172 1176
14. M.J. Birnbaum, R.J. Clem, and L.K. Miller An apoptosis-inhibiting gene from a nuclear polyhedrosis virus encoding a polypeptide with Cys/His sequence motifs J. Virol. 68 1994 2521 2528
15. P. Boya, B. Roques, and G. Kroemer New EMBO members' review: viral and bacterial proteins regulating apoptosis at the mitochondrial level EMBO J. 20 16 2001 4325 4331
16. T.A. Brandt, and B.L. Jacobs Both carboxy- and amino-terminal domains of the vaccinia virus interferon resistance gene, E3L, are required for pathogenesis in a mouse model J. Virol. 75 2 2001 850 856
17. D.J. Brick, R.D. Burke, A.A. Minkley, and C. Upton Ectromelia virus virulence factor p28 acts upstream of caspase-3 in response to UV light-induced apoptosis J. Gen. Virol. 81 Pt. 4 2000 1087 1097
18. M.A. Brooks, A.N. Ali, P.C. Turner, and R.W. Moyer A rabbitpox virus serpin gene controls host range by inhibiting apoptosis in restrictive cells J. Virol. 69 12 1995 7688 7698
19. C.R. Brunetti, M. Paulose-Murphy, R. Singh, J. Qin, J.W. Barrett, A. Tardivel, P. Schneider, K. Essani, and G. McFadden A secreted high-affinity inhibitor of human TNF from Tanapox virus Proc. Natl. Acad. Sci. U.S.A. 100 8 2003 4831 4836
20. C. Cameron, S. Hota-Mitchell, L. Chen, J. Barrett, J.X. Cao, C. Macaulay, D. Willer, D. Evans, and G. McFadden The complete DNA sequence of myxoma virus Virology 264 2 1999 298 318
21. P.F. Cartron, H. Arokium, L. Oliver, K. Meflah, S. Manon, and F.M. Vallette Distinct domains control the addressing and the insertion of Bax into mitochondria J. Biol. Chem. 280 11 2005 10587 10598
22. H.W. Chang, and B.L. Jacobs Identification of a conserved motif that is necessary for binding of the vaccinia virus E3L gene products to double-stranded RNA Virology 194 1993 537 547
23. P.M. Chaudhary, A. Jasmin, M.T. Eby, and L. Hood Modulation of the NF-kappa B pathway by virally encoded death effector domains-containing proteins Oncogene 18 42 1999 5738 5746
24. E.H. Cheng, T.V. Sheiko, J.K. Fisher, W.J. Craigen, and S.J. Korsmeyer VDAC2 inhibits BAK activation and mitochondrial apoptosis Science 301 5632 2003 513 517
25. R.J. Clem, and L.K. Miller Control of programmed cell death by the baculovirus genes p35 and iap Mol. Cell. Biol. 14 8 1994 5212 5222
26. S. Cory, D.C. Huang, and J.M. Adams The Bcl-2 family: roles in cell survival and oncogenesis Oncogene 22 53 2003 8590 8607
27. N.E. Crook, R.J. Clem, and L.K. Miller An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif J. Virol. 67 1993 2168 2174
28. A. Cuconati, and E. White Viral homologs of BCL-2: role of apoptosis in the regulation of virus infection Genes Dev. 16 19 2002 2465 2478
29. A. Cuconati, K. Degenhardt, R. Sundararajan, A. Anschel, and E. White Bak and Bax function to limit adenovirus replication through apoptosis induction J. Virol. 76 9 2002 4547 4558
30. A. Cuconati, C. Mukherjee, D. Perez, and E. White DNA damage response and MCL-1 destruction initiate apoptosis in adenovirus-infected cells Genes Dev. 17 23 2003 2922 2932
31. R. Datta, H. Kojima, D. Banach, N.J. Bump, R.V. Talanian, E.S. Alnemri, R.R. Weichselbaum, W.W. Wong, and D.W. Kufe Activation of a CrmA-insensitive, p35-sensitive pathway in ionizing radiation-induced apoptosis J. Biol. Chem. 272 3 1997 1965 1969
32. M.V. Davies, H.W. Chang, B.L. Jacobs, and R.J. Kaufman The E3L and K3L vaccinia virus gene products stimulate translation through inhibition of the double-stranded RNA-dependent protein kinase by different mechanisms J. Virol. 67 3 1993 1688 1692
33. M. Degli Esposti, and C. Dive Mitochondrial membrane permeabilisation by Bax/Bak Biochem. Biophys. Res. Commun. 304 2003 455 461
34. M. Ditzel, R. Wilson, T. Tenev, A. Zachariou, A. Paul, E. Deas, and P. Meier Degradation of DIAP1 by the N-end rule pathway is essential for regulating apoptosis Nat. Cell Biol. 5 2003 467 473
35. C. Du, M. Fang, Y. Li, L. Li, and X. Wang Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition Cell 102 2000 33 42
36. C.S. Duckett, V.E. Nava, R.W. Gedrich, R.J. Clem, J.L. Van Dongen, M.C. Gilfillan, H. Shiels, J.M. Hardwick, and C.B. Thompson A conserved family of cellular genes related to the baculovirus iap gene and encoding apoptosis inhibitors EMBO J. 15 1996 2685 2694
37. J. Engelmayer, M. Larsson, M. Subklewe, A. Chahroudi, W.I. Cox, R.M. Steinman, and N. Bhardwaj Vaccinia virus inhibits the maturation of human dendritic cells: a novel mechanism of immune evasion J. Immunol. 163 1999 6762 6768
38. R. Eskes, S. Desagher, B. Antonsson, and J.C. Martinou Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane Mol. Cell. Biol. 20 3 2000 929 935
39. H. Everett, and G. McFadden Apoptosis: an innate immune response to virus infection Trends Microbiol. 7 4 1999 160 165
40. H. Everett, and G. McFadden Poxviruses and apoptosis: a time to die Curr. Opin. Microbiol. 5 4 2002 395
41. H. Everett, M. Barry, S.F. Lee, X. Sun, K. Graham, J. Stone, R.C. Bleackley, and G. McFadden M11L: a novel mitochondria-localized protein of myxoma virus that blocks apoptosis of infected leukocytes J. Exp. Med. 191 9 2000 1487 1498
42. H. Everett, M. Barry, X. Sun, S.F. Lee, C. Frantz, L.G. Berthiaume, G. McFadden, and R.C. Bleackley The myxoma poxvirus protein, M11L, prevents apoptosis by direct interaction with the mitochondrial permeability transition pore J. Exp. Med. 196 9 2002 1127 1140
43. U. Fischer, R.U. Janicke, and K. Schulze-Osthoff Many cuts to ruin: a comprehensive update of caspase substrates Cell Death Differ. 10 1 2003 76 100
44. S.F. Fischer, H. Ludwig, J. Holzapfel, M. Kvansakul, L. Chen, D.C. Huang, G. Sutter, M. Knese, and G. Hacker Modified vaccinia virus Ankara protein F1L is a novel BH3-domain-binding protein and acts together with the early viral protein E3L to block virus-associated apoptosis Cell Death Differ. 2005
45. M.A. Garcia, S. Guerra, J. Gil, V. Jimenez, and M. Esteban Anti-apoptotic and oncogenic properties of the dsRNA-binding protein of vaccinia virus, E3L Oncogene 21 55 2002 8379 8387
46. T.L. Garvey, J. Bertin, R.M. Siegel, G.H. Wang, M.J. Lenardo, and J.I. Cohen Binding of FADD and caspase-8 to molluscum contagiosum virus MC159 v-FLIP is not sufficient for its antiapoptotic function J. Virol. 76 2 2002 697 706
47. J. Gil, J. Rullas, J. Alcami, and M. Esteban MC159L protein from the poxvirus molluscum contagiosum virus inhibits NF-kappaB activation and apoptosis induced by PKR J. Gen. Virol. 82 Pt. 12 2001 3027 3034
48. K.A. Graham, A. Opgenorth, C. Upton, and G. McFadden Myxoma virus M11L ORF encodes a protein for which cell surface localization is critical in manifestation of viral virulence Virology 191 1 1992 112 124
49. D.R. Green G. Kroemer The Pathophysiology of Mitochondrial Cell Death vol. 305 2004 Science
50. G.J. Griffiths, L. Dubrez, C.P. Morgan, N.A. Jones, J. Whitehouse, B.M. Corfe, C. Dive, and J.A. Hickman Cell damage-induced conformational changes of the pro-apoptotic protein Bak in vivo precede the onset of apoptosis J. Cell Biol. 144 5 1999 903 914
51. A. Gross, J.M. McDonnell, and S.J. Korsmeyer BCL-2 family members and the mitochondria in apoptosis Genes Dev. 13 15 1999 1899 1911
52. J.M. Hardwick, and D.S. Bellows Viral versus cellular BCL-2 proteins Cell Death Differ. 10 Suppl. 1 2003 S68 S76
53. M.H. Harris, and C.B. Thompson The role of the Bcl-2 family in the regulation of outer mitochondrial membrane permeability Cell Death Differ. 7 12 2000 1182 1191
54. M.O. Hengartner The biochemistry of apoptosis Nature 407 6805 2000 770 776
55. L. Hicke Protein regulation by monoubiquitin Nat. Rev., Mol. Cell Biol. 2 3 2001 195 201
56. R.M. Hofmann, and C.M. Pickart In vitro assembly and recognition of Lys-63 polyubiquitin chains J. Biol. Chem. 276 30 2001 27936 27943
57. S. Hu, C. Vincenz, M. Buller, and V.M. Dixit A novel family of viral death effector domain-containing molecules that inhibit both CD-95- and tumor necrosis factor receptor-1-induced apoptosis J. Biol. Chem. 272 15 1997 9621 9624
58. D.C. Huang, and A. Strasser BH3-Only proteins-essential initiators of apoptotic cell death Cell 103 6 2000 839 842
59. J. Huang, Q. Huang, X. Zhou, M.M. Shen, A. Yen, S.X. Yu, G. Dong, K. Qu, P. Huang, E.M. Anderson, S. Daniel-Issakani, R.M. Buller, D.G. Payan, and H.H. Lu The poxvirus p28 virulence factor is an E3 ubiquitin ligase J. Biol. Chem. 279 52 2004 54110 54116
60. Z. Humlova, M. Vokurka, M. Esteban, and Z. Melkova Vaccinia virus induces apoptosis of infected macrophages J. Gen. Virol. 83 2002 2821 2832
61. V. Jesenberger, and S. Jentsch Deadly encounter: ubiquitin meets apoptosis Nat. Rev., Mol. Cell Biol. 3 2 2002 112 121
62. C.A. Joazeiro, and A.M. Weissman RING finger proteins: mediators of ubiquitin ligase activity Cell 102 5 2000 549 552
63. J.F. Kerr, A.H. Wyllie, and A.R. Currie Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics Br. J. Cancer 26 4 1972 239 257
64. K.V. Kibler, T. Shors, K.B. Perkins, C.C. Zeman, M.P. Banaszak, J. Biesterfeldt, J.O. Langland, and B.L. Jacobs Double-stranded RNA is a trigger for apoptosis in vaccinia virus-infected cells J. Virol. 71 3 1997 1992 2003
65. T. Komiyama, C.A. Ray, D.J. Pickup, A.D. Howard, N.A. Thornberry, E.P. Peterson, and G. Salvesen Inhibition of interleukin-1 beta converting enzyme by the cowpox virus serpin CrmA. An example of cross-class inhibition J. Biol. Chem. 269 30 1994 19331 19337
66. S.B. Lee, and M. Esteban The interferon-induced double-stranded RNA-activated protein kinase induces apoptosis Virology 199 2 1994 491 496
67. P. Li, D. Nijhawan, I. Budihardjo, S.M. Srinivasula, M. Ahmad, E.S. Alnemri, and X. Wang Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade Cell 91 4 1997 479 489
68. Q. Li, P. Liston, and R.W. Moyer Functional analysis of the inhibitor of apoptosis (iap) gene carried by the entomopoxvirus of Amsacta moorei J. Virol. 79 4 2005 2335 2345
69. Q. Li, P. Liston, N. Schokman, J.M. Ho, and R.W. Moyer Amsacta moorei entomopoxvirus inhibitor of apoptosis suppresses cell death by binding Grim and Hid J. Virol. 79 6 2005 3684 3691
70. P. Liston, N. Roy, K. Tamai, C. Lefebvre, S. Baird, G. Cherton-Horvat, R. Farahani, M. McLean, J.E. Ikeda, A. MacKenzie, and R.G. Korneluk Suppression of apoptosis in mammalian cells by NAIP and a related family of IAP genes Nature 379 1996 349 353
71. X. Liu, C.N. Kim, J. Yang, R. Jemmerson, and X. Wang Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c Cell 86 1 1996 147 157
72. S.J. Lord, R.V. Rajotte, G.S. Korbutt, and R.C. Bleackley Granzyme B: a natural born killer Immunol. Rev. 193 2003 31 38
73. X. Luo, I. Budihardjo, H. Zou, C. Slaughter, and X. Wang Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors Cell 94 4 1998 481 490
74. J.L. Macen, K.A. Graham, S.F. Lee, M. Schreiber, L.K. Boshkov, and G. McFadden 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 218 1 1996 232 237
75. J. Macen, A. Takahashi, K.B. Moon, R. Nathaniel, P.C. Turner, and R.W. Moyer Activation of caspases in pig kidney cells infected with wild-type and CrmA/SPI-2 mutants of cowpox and rabbitpox viruses J. Virol. 72 5 1998 3524 3533
76. L.M. Martins, I. Iaccarino, T. Tenev, S. Gschmeissner, N.F. Totty, N.R. Lemoine, J. Savopoulos, C.W. Gray, C.L. Creasy, C. Dingwall, and J. Downward The serine protease Omi/HtrA2 regulates apoptosis by binding XIAP through a reaper-like motif J. Biol. Chem. 277 2002 439 444
77. F. Messud-Petit, J. Gelfi, M. Delverdier, M.F. Amardeilh, R. Py, G. Sutter, and S. Bertagnoli Serp2, an inhibitor of the interleukin-1beta- converting enzyme, is critical in the pathobiology of myxoma virus J. Virol. 72 10 1998 7830 7839
78. B. Moss Poxviridae: the viruses and their replication M. Knipe M. Howley 4th eds. Fields Virology 2nd ed. 2001 Lippincott Williams and Wilkins Philadelphia
79. K. Mossman, S.F. Lee, M. Barry, L. Boshkov, and G. McFadden Disruption of M-T5, a novel myxoma virus gene member of poxvirus host range superfamily, results in dramatic attenuation of myxomatosis in infected European rabbits J. Virol. 70 7 1996 4394 4410
80. L.E. Murao, and J.L. Shisler The MCV MC159 protein inhibits late, but not early, events of TNF-alpha-induced NF-kappaB activation Virology 2005
81. M. Muzio, A.M. Chinnaiyan, F.C. Kischkel, K. O'Rourke, A. Shevchenko, J. Ni, C. Scaffidi, J.D. Bretz, M. Zhang, R. Gentz, M. Mann, P.H. Krammer, M.E. Peter, and V.M. Dixit FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death-inducing signaling complex Cell 85 6 1996 817 827
82. R. Nathaniel, A.L. MacNeill, Y.X. Wang, P.C. Turner, and R.W. Moyer Cowpox virus CrmA, Myxoma virus SERP2 and baculovirus P35 are not functionally interchangeable caspase inhibitors in poxvirus infections J. Gen. Virol. 85 Pt. 5 2004 1267 1278
83. B.T. Nerenberg, J. Taylor, E. Bartee, K. Gouveia, M. Barry, and K. Fruh The poxviral RING protein p28 is a ubiquitin ligase that targets ubiquitin to viral replication factories J. Virol. 79 1 2005 597 601
84. A. Opgenorth, K. Graham, N. Nation, D. Strayer, and G. McFadden Deletion analysis of two tandemly arranged virulence genes in myxoma virus, M11L and myxoma growth factor J. Virol. 66 8 1992 4720 4731
85. J.F. Panus, C.A. Smith, C.A. Ray, T.D. Smith, D.D. Patel, and D.J. Pickup Cowpox virus encodes a fifth member of the tumor necrosis factor receptor family: a soluble, secreted CD30 homologue Proc. Natl. Acad. Sci. U.S.A. 99 12 2002 8348 8353
86. M.E. Perkus, S.J. Goebel, S.W. Davis, G.P. Johnson, E.K. Norton, and E. Paoletti Deletion of 55 open reading frames from the termini of vaccinia virus Virology 180 1 1991 406 410
87. D.J. Pickup, B.S. Ink, W. Hu, C.A. Ray, and W.K. Joklik 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. U.S.A. 83 20 1986 7698 7702
88. D. Poncet, N. Larochette, A.L. Pauleau, P. Boya, A.A. Jalil, P.F. Cartron, F. Vallette, C. Schnebelen, L.M. Bartle, A. Skaletskaya, D. Boutolleau, J.C. Martinou, V.S. Goldmacher, G. Kroemer, and N. Zamzami An anti-apoptotic viral protein that recruits Bax to mitochondria J. Biol. Chem. 279 21 2004 22605 22614
89. L.T. Quan, A. Caputo, R.C. Bleackley, D.J. Pickup, and G.S. Salvesen Granzyme B is inhibited by the cowpox virus serpin cytokine response modifier A J. Biol. Chem. 270 18 1995 10377 10379
90. A. Ramsey-Ewing, and B. Moss Apoptosis induced by a postbinding step of vaccinia virus entry into Chinese hamster ovary cells Virology 242 1 1998 138 149
91. J.C. Rathmell, and C.B. Thompson The central effectors of cell death in the immune system Annu. Rev. Immunol. 17 1999 781 828
92. C.A. Ray, and D.J. Pickup The mode of death of pig kidney cells infected with cowpox virus is governed by the expression of the crmA gene Virology 217 1 1996 384 391
93. C.A. Ray, R.A. Black, S.R. Kronheim, T.A. Greenstreet, P.R. Sleath, G.S. Salvesen, and D.J. Pickup Viral inhibition of inflammation: cowpox virus encodes an inhibitor of the interleukin-1 beta converting enzyme Cell 69 4 1992 597 604
94. C. Rivas, J. Gil, Z. Melkova, M. Esteban, and M. Diaz-Guerra Vaccinia virus E3L protein is an inhibitor of the interferon (i.f.n.)-induced 2-5A synthetase enzyme Virology 243 1998 406 414
95. P.R. Romano, F. Zhang, S.L. Tan, M.T. Garcia-Barrio, M.G. Katze, T.E. Dever, and A.G. Hinnebusch Inhibition of double-stranded RNA-dependent protein kinase PKR by vaccinia virus E3: role of complex formation and the E3 N-terminal domain Mol. Cell. Biol. 18 1998 7304 7316
96. M. Rothe, M.G. Pan, W.J. Henzel, T.M. Ayres, and D.V. Goeddel The TNFR2-TRAF signaling complex contains two novel proteins related to baculoviral inhibitor of apoptosis proteins Cell 83 1995 1243 1252
97. A. Roulston, R.C. Marcellus, and P.E. Branton Viruses and apoptosis Annu. Rev. Microbiol. 53 1999 577 628
98. N. Roy, M.S. Mahadevan, M. McLean, G. Shutler, Z. Yaraghi, R. Farahani, S. Baird, A. Besner-Johnston, C. Lefebvre, and X. Kang The gene for neuronal apoptosis inhibitory protein is partially deleted in individuals with spinal muscular atrophy Cell 80 1995 167 178
99. J.H. Russell, and T.J. Ley Lymphocyte-mediated cytotoxicity Annu. Rev. Immunol. 20 2002 323 370
100. G.S. Salvesen, and J.M. Abrams Caspase activation-stepping on the gas or releasing the brakes? Lessons from humans and flies Oncogene 23 16 2004 2774 2784
101. G.S. Salvesen, and C.S. Duckett IAP proteins: blocking the road to death's door Nat. Rev., Mol. Cell Biol. 3 6 2002 401 410
102. C. Scaffidi, S. Fulda, A. Srinivasan, C. Friesen, F. Li, K.J. Tomaselli, K.M. Debatin, P.H. Krammer, and M.E. Peter Two CD95 (APO-1/Fas) signaling pathways EMBO J. 17 6 1998 1675 1687
103. M. Schreiber, and G. McFadden The myxoma virus TNF-receptor homologue (T2) inhibits tumor necrosis factor-alpha in a species-specific fashion Virology 204 2 1994 692 705
104. M. Schreiber, K. Rajarathnam, and G. McFadden Myxoma virus T2 protein, a tumor necrosis factor (TNF) receptor homolog, is secreted as a monomer and dimer that each bind rabbit TNFalpha, but the dimer is a more potent TNF inhibitor J. Biol. Chem. 271 23 1996 13333 13341
105. L. Scorrano, and S.J. Korsmeyer Mechanisms of cytochrome c release by proapoptotic BCL-2 family members Biochem. Biophys. Res. Commun. 304 2003 437 444
106. B.T. Seet, and G. McFadden Viral chemokine-binding proteins J. Leukocyte Biol. 72 1 2002 24 34
107. B.T. Seet, J.B. Johnston, C.R. Brunetti, J.W. Barrett, H. Everett, C. Cameron, J. Sypula, S.H. Nazarian, A. Lucas, and G. McFadden Poxviruses and immune evasion Annu. Rev. Immunol. 21 2003 377 423
108. T.G. Senkevich, E.V. Koonin, and R.M. Buller A poxvirus protein with a RING zinc finger motif is of crucial importance for virulence Virology 198 1 1994 118 128
109. T.G. Senkevich, E.J. Wolffe, and R.M. Buller Ectromelia virus RING finger protein is localized in virus factories and is required for virus replication in macrophages J. Virol. 69 7 1995 4103 4111
110. T.V. Sharp, F. Moonan, A. Romashko, B. Joshi, G.N. Barber, and R. Jagus The vaccinia virus E3L gene product interacts with both the regulatory and the substrate binding regions of PKR: implications for PKR autoregulation Virology 250 1998 302 315
111. Y. Shi Mechanisms of caspase activation and inhibition during apoptosis Mol. Cell 9 3 2002 459 470
112. J.L. Shisler, and B. Moss Molluscum contagiosum virus inhibitors of apoptosis: the MC159 v-FLIP protein blocks Fas-induced activation of procaspases and degradation of the related MC160 protein Virology 282 1 2001 14 25
113. G.A. Silverman, P.I. Bird, R.W. Carrell, F.C. Church, P.B. Coughlin, P.G. Gettins, J.A. Irving, D.A. Lomas, C.J. Luke, R.W. Moyer, P.A. Pemberton, E. Remold-O'Donnell, G.S. Salvesen, J. Travis, and J.C. Whisstock The serpins are an expanding superfamily of structurally similar but functionally diverse proteins. Evolution, mechanism of inhibition, novel functions, and a revised nomenclature J. Biol. Chem. 276 36 2001 33293 33296
114. C.A. Smith, T. Davis, D. Anderson, L. Solam, M.P. Beckmann, R. Jerzy, S.K. Dower, D. Cosman, and R.G. Goodwin A receptor for tumor necrosis factor defines an unusual family of cellular and viral proteins Science 248 4958 1990 1019 1023
115. C.A. Smith, T. Davis, J.M. Wignall, W.S. Din, T. Farrah, C. Upton, G. McFadden, and R.G. Goodwin T2 open reading frame from the Shope fibroma virus encodes a soluble form of the TNF receptor Biochem. Biophys. Res. Commun. 176 1 1991 335 342
116. G.L. Smith, J.A. Symons, and A. Alcami Immune modulation by proteins secreted from cells infected by vaccinia virus Arch. Virol., Suppl. 15 1999 111 129
117. S.M. Srinivasula, P. Datta, X.J. Fan, T. Fernandes-Alnemri, Z. Huang, and E.S. Alnemri Molecular determinants of the caspase-promoting activity of Smac/DIABLO and its role in the death receptor pathway J. Biol. Chem. 275 2000 36152 36157
118. H.R. Stennicke, C.A. Ryan, and G.S. Salvesen Reprieval from execution: the molecular basis of caspase inhibition Trends Biochem. Sci. 27 2 2002 94 101
119. T.L. Stewart, S.T. Wasilenko, and M. Barry Vaccinia virus F1L protein is a tail-anchored protein that functions at the mitochondria to inhibit apoptosis J. Virol. 79 2 2005 1084 1098
120. A. Strasser The role of BH3-only proteins in the immune system Nat. Rev., Immunol. 5 3 2005 189 200
121. Y. Sun, and D.W. Leaman Involvement of Noxa in cellular apoptotic responses to interferon, double-stranded RNA, and virus infection J. Biol. Chem. 280 16 2005 15561 15568
122. R. Sundararajan, A. Cuconati, D. Nelson, and E. White Tumor necrosis factor-alpha induces Bax-Bak interaction and apoptosis, which is inhibited by adenovirus E1B 19K J. Biol. Chem. 276 48 2001 45120 45127
123. Y. Suzuki, Y. Imai, H. Nakayama, K. Takahashi, K. Takio, and R. Takahashi A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death Mol. Cell 8 2001 613 621
124. M. Tewari, and V.M. Dixit Fas- and tumor necrosis factor-induced apoptosis is inhibited by the poxvirus crmA gene product J. Biol. Chem. 270 7 1995 3255 3260
125. M. Tewari, W.G. Telford, R.A. Miller, and V.M. Dixit CrmA, a poxvirus-encoded serpin, inhibits cytotoxic T-lymphocyte- mediated apoptosis J. Biol. Chem. 270 39 1995 22705 22708
126. M. Thome, 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 Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors Nature 386 6624 1997 517 521
127. N.A. Thornberry, and Y. Lazebnik Caspases: enemies within Science 281 5381 1998 1312 1316
128. J.A. Trapani, and V.R. Sutton Granzyme B: pro-apoptotic, antiviral and antitumor functions Curr. Opin. Immunol. 15 5 2003 533 543
129. S.I. Tsukumo, and S. Yonehara Requirement of cooperative functions of two repeated death effector domains in caspase-8 and in MC159 for induction and inhibition of apoptosis, respectively Genes Cells 4 9 1999 541 549
130. E.R. Tulman, C.L. Afonso, Z. Lu, L. Zsak, G.F. Kutish, and D.L. Rock The genome of canarypox virus J. Virol. 78 2004 353 366
131. P.C. Turner, M.C. Sancho, S.R. Thoennes, A. Caputo, R.C. Bleackley, and R.W. Moyer Myxoma virus Serp2 is a weak inhibitor of granzyme B and interleukin-1beta-converting enzyme in vitro and unlike CrmA cannot block apoptosis in cowpox virus-infected cells J. Virol. 73 8 1999 6394 6404
132. C. Upton, J.L. Macen, M. Schreiber, and G. McFadden Myxoma virus expresses a secreted protein with homology to the tumor necrosis factor receptor gene family that contributes to viral virulence Virology 184 1 1991 370 382
133. C. Upton, L. Schiff, S.A. Rice, T. Dowdeswell, X. Yang, and G. McFadden A poxvirus protein with a RING finger motif binds zinc and localizes in virus factories J. Virol. 68 7 1994 4186 4195
134. A.G. Uren, M. Pakusch, C.J. Hawkins, K.L. Puls, and D.L. Vaux 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. U.S.A. 93 1996 4974 4978
135. D.L. Vaux, and J. Silke Mammalian mitochondrial IAP binding proteins Biochem. Biophys. Res. Commun. 304 3 2003 499 504
136. G. Wang, J.W. Barrett, S.H. Nazarian, H. Everett, X. Gao, C. Bleackley, K. Colwill, M.F. Moran, and G. McFadden Myxoma virus M11L prevents apoptosis through constitutive interaction with Bak J. Virol. 78 13 2004 7097 7111
137. S.T. Wasilenko, A.F. Meyers, K. Vander Helm, and M. Barry Vaccinia virus infection disarms the mitochondrion-mediated pathway of the apoptotic cascade by modulating the permeability transition pore J. Virol. 75 23 2001 11437 11448
138. S.T. Wasilenko, T.L. Stewart, A.F. Meyers, and M. Barry Vaccinia virus encodes a previously uncharacterized mitochondrial-associated inhibitor of apoptosis Proc. Natl. Acad. Sci. U.S.A. 100 24 2003 14345 14350
139. Wasilenko, S.T., Banadyga, L., Bond, D., and Barry, M., in press. The vaccinia virus F1L protein interacts with the pro-apoptotic protein Bak and inhibits Bak activation. J. Virol.
140. P.F. Wehrle A reality in our time-certification of the global eradication of smallpox J. Infect. Dis. 142 4 1980 636 638
141. M.C. Wei, W.X. Zong, E.H. Cheng, T. Lindsten, V. Panoutsakopoulou, A.J. Ross, K.A. Roth, G.R. MacGregor, C.B. Thompson, and S.J. Korsmeyer Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death Science 292 5517 2001 727 730
142. A.M. Weissman Themes and variations on ubiquitylation Nat. Rev., Mol. Cell Biol. 2 3 2001 169 178
143. R. Wilson, L. Goyal, M. Ditzel, A. Zachariou, D.A. Baker, J. Agapite, H. Steller, and P. Meier The DIAP1 RING finger mediates ubiquitination of Dronc and is indispensable for regulating apoptosis Nat. Cell Biol. 4 2002 445 450
144. G. Wu, J. Chai, T.L. Suber, J.W. Wu, C. Du, X. Wang, and Y. Shi Structural basis of IAP recognition by Smac/DIABLO Nature 408 2000 1008 1012
145. Q. Zhou, S. Snipas, K. Orth, M. Muzio, V.M. Dixit, and G.S. Salvesen Target protease specificity of the viral serpin CrmA, analysis of five caspases J. Biol. Chem. 272 12 1997 7797 7800