Antiapoptotic activity of the cardiovirus leader protein, a viral "security" protein

Journal of Virology

Volumn 83, Issue 14, 2009, Pages 7273-7284

  Romanova, Lyudmila I ^a   Lidsky, Peter V ^a   Kolesnikova, Marina S ^a   Fominykh, Ksenia V ^a,b   Gmyl, Anatoly P ^a   Sheval, Eugene V ^b   Hato, Stanleyson V ^c   Van Kuppeveld, Frank J M ^c   Agol, Vadim I ^a,b  

^a CHUMAKOV INSTITUTE OF POLIOMYELITIS AND VIRAL ENCEPHALITIDES   (Russian Federation)

^b MOSCOW STATE UNIVERSITY   (Russian Federation)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; CYTOCHROME C; MUTANT PROTEIN; VIRUS PROTEIN;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENCEPHALOMYOCARDITIS VIRUS; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; VIRUS CELL INTERACTION; VIRUS MUTANT; WILD TYPE;

ANIMALS; APOPTOSIS; CARDIOVIRUS; CARDIOVIRUS INFECTIONS; CELL LINE; CRICETINAE; CYTOCHROMES C; ENCEPHALOMYOCARDITIS VIRUS; HELA CELLS; HUMANS; MITOCHONDRIA; VIRAL PROTEINS;

CARDIOVIRUS; ENCEPHALOMYOCARDITIS VIRUS;

EID: 67650424325     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00467-09     Document Type: Article

References (108)

1. Agol, V. I. 2002. Picornavirus genome: an overview, p. 127-148. In B. L. Semler and E. Wimmer (ed.), Molecular biology of picornaviruses. ASM Press, Washington, DC.
2. Agol, V. I., G. A. Belov, K. Bienz, D. Egger, M. S. Kolesnikova, N. T. Raikhlin, L. I. Romanova, E. A. Smirnova, and E. A. Tolskaya. 1998. Two types of death of poliovirus-infected cells: caspase involvement in the apoptosis but not cytopathic effect. Virology 252:343-353.
3. Agol, V. I., G. A. Belov, K. Bienz, D. Egger, M. S. Kolesnikova, L. I. Romanova, L. V. Sladkova, and E. A. Tolskaya. 2000. Competing death programs in poliovirus-infected cells: commitment switch in the middle of infectious cycle. J. Virol. 74:5534-5541.
4. Ammendolia, M. G., A. Tinari, A. Calcabrini, and F. Superti. 1999. Poliovirus infection induces apoptosis in CaCo-2 cells. J. Med. Virol. 59:122-129.
5. Anderson, R., E. Harting, M. S. Frey, J. L. Leibowitz, and R. C. Miranda. 2000. Theiler's murine encephalomyelitis virus induces rapid necrosis and delayed apoptosis in myelinated mouse cerebellar explant cultures. Brain Res. 868:259-267.
6. Andoniou, C. E., and M. A. Degli-Esposti. 2006. Insights into the mechanisms of CMV-mediated interference with cellular apoptosis. Immunol. Cell Biol. 84:99-106.
7. Arnoult, D., L. M. Bartle, A. Skaletskaya, D. Poncet, N. Zamzami, P. U. Park, J. Sharpe, Ri. J. Youle, and V. S. Goldmacher. 2004. Cytomegalovirus cell death suppressor vMIA blocks Bax- but not Bak-mediated apoptosis by binding and sequestering Bax at mitochondria. Proc. Natl. Acad. Sci. USA 101:7988-7993.
8. Autret, A., S. Martin-Latil, C. Brisac, L. Mousson, F. Colbère-Garapin, and B. Blondel. 2008. Early phosphatidylinositol 3-kinase/Akt pathway activation limits poliovirus-induced JNK-mediated cell death. J. Virol. 82:3796-3802.
9. Autret, A., S. Martin-Latil, L. Mousson, A. Wirotius, F. Petit, D. Arnoult, F. Colbère-Garapin, J. Estaquier, and B. Blondel. 2007. Poliovirus induces Bax-dependent cell death mediated by c-Jun NH2-terminal kinase. J. Virol. 81:7504-7516.
10. Barber, G. N. 2001. Host defense, viruses and apoptosis. Cell Death Differ. 8:113-126.
11. Bardina, M. V., P. V. Lidsky, E. V. Sheval, K. V. Fominykh, F. J. M. van Kuppeveld, V. Y. Polyakov, and V. I. Agol. 2009. Mengovirus-induced rearrangement of the nuclear pore complex: hijacking cellular phosphorylation machinery. J. Virol. 83:3150-3161.
12. Belov, G. A., P. V. Lidsky, O. V. Mikitas, D. Egger, K. A. Lukyanov, K. Bienz, and V. I. Agol. 2004. Bidirectional increase in permeability of nuclear envelope upon poliovirus infection and accompanying alterations of nuclear pores. J. Virol. 78:10166-10177.
13. Belov, G. A., L. I. Romanova, E. A. Tolskaya, M. S. Kolesnikova, Y. A. Lazebnik, and V. I. Agol. 2003. The major apoptotic pathway activated and suppressed by poliovirus. J. Virol. 77:45-56.
14. Best, S. M. 2008. Viral subversion of apoptotic enzymes: escape from death row. Annu. Rev. Microbiol. 62:171-192.
15. Blondel, B., A. Autret, C. Brisac, S. Martin-Latil, L. Mousson, I. Pelletier, J. Estaquier, and F. Colbere-Garapin. 2009. Apoptotic signaling cascades operating in poliovirus-infected cells. Front. Biosci. 14:2181-2192.
16. Brack, K., W. Frings, A. Dotzauer, and A. Vallbracht. 1998. A cytopathogenic, apoptosis-inducing variant of hepatitis A virus. J. Virol. 72:3370-3376.
17. Brewer, L. A., H. C. Lwamba, M. P. Murtaugh, A. C. Palmenberg, C. Brown, and M. K. Njenga. 2001. Porcine encephalomyocarditis virus persists in pig myocardium and infects human myocardial cells. J. Virol. 75:11621-11629.
18. Calandria, C., A. Irurzun, A. Barco, and L. Carrasco. 2004. Individual expression of poliovirus 2Apro and 3Cpro induces activation of caspase-3 and PARP cleavage in HeLa cells. Virus Res. 104:39-49.
19. Calenoff, M. A., C. S. Badshah, M. C. Dal Canto, H. L. Lipton, and M. K. Rundell. 1995. The leader polypeptide of Theiler's virus is essential for neurovirulence but not for virus growth in BHK cells. J. Virol. 69:5544-5549.
20. Callus, B. A., and D. L. Vaux. 2007. Caspase inhibitors: viral, cellular and chemical. Cell Death Differ. 14:73-78.
21. 2+ homeostasis. J. Biol. Chem. 279:18440-18450.
22. Carthy, C. M., D. J. Granville, K. A. Watson, D. R. Anderson, J. E. Wilson, D. Yang, D. W. Hunt, and B. M. McManus. 1998. Caspase activation and specific cleavage of substrates after coxsackievirus B3-induced cytopathic effect in HeLa cells. J. Virol. 72:7669-7675.
23. Caserta, T. M., A. N. Smith, A. D. Gultice, M. A. Reedy, and T. L. Brown. 2003. Q.-VD-OPh, a broad spectrum caspase inhibitor with potent anti-apoptotic properties. Apoptosis 8:345-352.
24. Chan, D. C. 2006. Mitochondrial fusion and fission in mammals. Annu. Rev. Cell Dev. Biol. 22:79-99.
25. Chang, S.-C., J.-Y. Lin, L. Y.-C. Lo, M.-L. Li, and S.-R. Shih. 2004. Diverse apoptotic pathways in enterovirus 71-infected cells. J. Neurovirol. 10:338-349.
26. Chau, D. H., J. Yuan, H. Zhang, P. Cheung, T. Lim, Z. Liu, A. Sall, and D. Yang. 2007. Coxsackievirus B3 proteases 2A and 3C induce apoptotic cell death through mitochondrial injury and cleavage of eIF4GI but not DAP5/p97/NAT1. Apoptosis 12:513-524.
27. Chen, D., D. E. Texada, C. Duggan, Y. Deng, T. B. Redens, and M. P. Langford. 2006. Caspase-3 and -7 mediate apoptosis of human Chang's conjunctival cells induced by enterovirus 70. Virology 347:307-322.
28. Clemens, M. J. 2006. Epstein-Barr virus: inhibition of apoptosis as a mechanism of cell transformation. Int. J. Biochem. Cell Biol. 38:164-169.
29. de Jong, A. S., F. de Mattia, M. M. Van Dommelen, K. Lanke, W. J. G. Melchers, P. H. G. M. Willems, and F. J. M. van Kuppeveld. 2008. Functional analysis of picornavirus 2B proteins: effects on calcium homeostasis and intracellular protein trafficking. J. Virol. 82:3782-3790.
30. Delhaye, S., V. van Pesch, and T. Michiels. 2004. The leader protein of Theiler's virus interferes with nucleocytoplasmic trafficking of cellular proteins. J. Virol. 78:4357-4362.
31. de los Santos, T., S. de Avila Botton, R. Weiblen, and M. J. Grubman. 2006. The leader proteinase of foot-and-mouth disease virus inhibits the induction of beta interferon mRNA and blocks the host innate immune response. J. Virol. 80:1906-1914.
32. Deszcz, L., E. Gaudernak, E. Kuechler, and J. Seipelt. 2005. Apoptotic events induced by human rhinovirus infection. J. Gen. Virol. 86:1379-1389.
33. Devaney, M. A., V. N. Vakharia, R. E. Lloyd, E. Ehrenfeld, and M. J. Grubman. 1988. Leader protein of foot-and-mouth disease required for cleavage of the p220 component of the cap binding protein complex. J. Virol. 62:4407-4409.
34. Duke, G. M., and A. C. Palmenberg. 1989. Cloning and synthesis of infectious cardiovirus RNAs containing short, discrete poly(C) tracts. J. Virol. 63:1822-1826.
35. Dvorak, C. M., D. J. Hall, M. Hill, M. Riddle, A. Pranter, J. Dillman, M. Deibel, and A. C. Palmenberg. 2001. Leader protein of encephalomyocarditis virus binds zinc, is phosphorylated during viral infection, and affects the efficiency of genome translation. Virology 290:261-271.
36. Esfandiarei, M., S. Boroomand, A. Suarez, X. Si, M. Rahmani, and B. McManus. 2007. Coxsackievirus B3 activates nuclear factor kappa B transcription factor via a phosphatidylinositol-3 kinase/protein kinase B-dependent pathway to improve host cell viability. Cell Microbiol. 9:2358-2371.
37. Galluzzi, L., C. Brenner, E. Morselli, Z. Touat, and G. Kroemer. 2008. Viral control of mitochondrial apoptosis. PLoS Pathog. 4:e1000018.
38. Ghadge, G. D., L. Ma. S. Sato, J. Kim, and R. P. Roos. 1998. A protein critical for a Theiler's virus-induced immune system-mediated demyelinating disease has a cell type-specific antiapoptotic effect and a key role in virus persistence. J. Virol. 72:8605-8612.
39. Girard, S., T. Couderc, J. Destombes, D. Thiesson, F. Delpeyroux, and B. Blondel. 1999. Poliovirus induces apoptosis in the mouse central nervous system. J. Virol. 73:6066-6072.
40. Gmyl, A. P., E. V. Belousov, S. V. Maslova, E. V. Khitrina, A. B. Chetverin, and V. I. Agol. 1999. Nonreplicative RNA recombination in poliovirus. J. Virol. 73:8958-8965.
41. Goldmacher, V. S., L. M. Bartle, A. Skaletskaya, C. A. Dionne, N. L. Kedersha, C. A. Vater, J. W. Han, R. J. Lutz, S. Watanabe, E. D. Cahir McFarland, E. D. Kieff, E. S. Mocarski, and T. Chittenden. 1999. A cytomegalovirus-encoded mitochondria-localized inhibitor of apoptosis structurally unrelated to Bcl-2. Proc. Natl. Acad. Sci. USA 96:12536- 12541.
42. Goldstaub, D., A. Gradi, Z. Bercovitch, Z. Grosmann, Y. Nophar, S. Luria, N. Sonenberg, and C. Kahana. 2000. Poliovirus 2A protease induces apoptotic cell death. Mol. Cell. Biol. 20:1271-1277.
43. Gosert, R., D. Egger, and K. Bienz. 2000. A cytopathic and a cell culture adapted hepatitis A virus strain differ in cell killing but not in intracellular membrane rearrangements. Virology 266:157-169.
44. Groppo, R., and A. C. Palmenberg. 2007. Cardiovirus 2A protein associates with 40S but not 80S ribosome subunits during infection. J. Virol. 81:13067-13074.
45. Grubman, M. J., M. P. Moraes, F. Diaz-San Segundo, L. Pena, and T. de Los Santos. 2008. Evading the host immune response: how foot-and-mouth disease virus has become an effective pathogen. FEMS Immunol. Med. Microbiol. 53:8-17.
46. Hato, S. V., C. Ricour, B. M. Schulte, K. H. Lanke, M. de Bruijni, J. Zoll, W. J. Melchers, T. Michiels, and F. J. M. van Kuppeveld. 2007. The mengovirus leader protein blocks interferon-alpha/beta gene transcription and inhibits activation of interferon regulatory factor 3. Cell. Microbiol. 9:2921-2930.
47. Henke, A., H. Launhardt, K. Klement, A. Stelzner, R. Zell, and T. Munder. 2000. Apoptosis in coxsackievirus B3-caused diseases: interaction between the capsid protein VP2 and the proapoptotic protein siva. J. Virol. 74:4284-4290.
48. Himeda, T., Y. Ohara, K. Asakura, Y. Kontani, and M. Sawada. 2005. A lentiviral expression system demonstrates that L* protein of Theiler's murine encephalomyelitis virus (TMEV) has an anti-apoptotic effect in a macrophage cell line. Microb. Pathog. 38:201-207.
49. Iordanov, M. S., O. P. Ryabinina, P. Schneider, and B. E. Magun. 2005. Two mechanisms of caspase 9 processing in double-stranded RNA- and virus-triggered apoptosis. Apoptosis 10:153-166.
50. Jelachich, M. L., and H. L. Lipton. 1996. Theiler's murine encephalomyelitis virus kills restrictive but not permissive cells by apoptosis. J. Virol. 70:6856-6861.
51. Jelachich, M. L., and H. L. Lipton. 1999. Restricted Theiler's murine encephalomyelitis virus infection in murine macrophages induces apoptosis. J. Gen. Virol. 80:1701-1705.
52. Jelachich, M. L., and H. L. Lipton. 2001. Theiler's murine encephalomyelitis virus induces apoptosis in gamma interferon activated M1 differentiated myelomonocytic cells through a mechanism involving tumor necrosis factor alpha (TNF-α) and TNF-α-related apoptosis-inducing ligand. J. Virol. 75:5930-5938.
53. Jin, H., C. Xiao, G. Zhao, X. Du, Y. Yu, Y. Kang, and B. Wang. 2007. Induction of immature dendritic cell apoptosis by foot and mouth disease virus is an integrin receptor mediated event before viral infection. J. Cell. Biochem. 102:980-991.
54. Joo, C. H., Y. K. Kim, H. Lee, H. Hong, S. Y. Yoon, and D. Kim. 2002. Coxsackievirus B4-induced neuronal apoptosis in rat cortical cultures. Neurosci. Lett. 326:175-178.
55. Kazachkov, Y. A., T. V. Chernovskaya, E. Y. Siyanova, Y. V. Svitkin, T. Y. Ugarova, and V. I. Agol. 1982. Leader polypeptides encoded in the 5′-region of the encephalomyocarditis virus genome. FEBS Lett. 141:153-156.
56. Pro increases viral mRNA and polysome stability coordinately in time with cleavage of eIF4G. J. Virol. 82:5847-5859.
57. Kong, W. P., G. D. Ghadge, and R. P. Roos. 1994. Involvement of cardiovirus leader in host cell-restricted virus expression. Proc. Natl. Acad. Sci. USA 91:1796-1800.
58. Kong, W. P., and R. P. Roos. 1991. Alternative translation initiation site in the DA strain of Theiler's murine encephalomyelitis virus. J. Virol. 65:3395-3399.
59. Kuechler, E., J. Seipelt, H.-D. Liebig, and W. Sommergruber. 2002. Picornavirus proteinase-mediated shutoff of host cell translation: Direct cleavage of a cellular initiation factor, p. 301-311. In B. L. Semler and E. Wimmer (ed.), Molecular biology of picornaviruses. ASM Press, Washington, DC.
60. Kuo, R. L., S. H. Kung, Y. Y. Hsu, and W. T. Liu. 2002. Infection with enterovirus 71 or expression of its 2A protease induces apoptotic cell death. J. Gen. Virol. 83:1367-1376.
61. Lidsky, P. V., S. Hato, M. V. Bardina, A. G. Aminev, A. C. Palmenberg, F. J. M. van Kuppeveld, and V. I. Agol. 2006. Nucleocytoplasmic traffic disorder induced by cardioviruses. J. Virol. 80:2705-2717.
62. Liu, J., T. Wei, and J. Kwang. 2002. Avian encephalomyelitis virus induces apoptosis via major structural protein VP3. Virology 300:39-49.
63. Liu, J., T. Wei, and J. Kwang. 2004. Avian encephalomyelitis virus non-structural protein 2C induces apoptosis by activating cytochrome c/caspase-9 pathway. Virology 318:169-182.
64. Madan, V., A. Castello, and L. Carrasco. 2008. Viroporins from RNA viruses induce caspase-dependent apoptosis. Cell. Microbiol. 10:437-451.
65. Martin, U., N. Jarasch, M. Nestler, A. Rassmann, T. Munder, S. Seitz, R. Zell, P. Wutzler, and A. Henke. 2007. Antiviral effects of pan-caspase inhibitors on the replication of coxsackievirus B3. Apoptosis 12:525-533.
66. McCormick, A. L., C. D. Meiering, G. B. Smith, and E. S. Mocarski. 2005. Mitochondrial cell death suppressors carried by human and murine cytomegalovirus confer resistance to proteasome inhibitor-induced apoptosis. J. Virol. 79:12205-12217.
67. McCormick, A. L., V. L. Smith, D. Chow, and E. S. Mocarski. 2003. Disruption of mitochondrial networks by the human cytomegalovirus UL37 gene product viral mitochondrion-localized inhibitor of apoptosis. J. Virol. 77:631-641.
68. McLean, J. E., A. Ruck, A. Shirazian, F. Pooyaei-Mehr, and Z. F. Zakeri. 2008. Viral manipulation of cell death. Curr. Pharm. Des. 14:198-220.
69. Michiels, T., V. Dejong, R. Rodrigus, and C. Shaw-Jacson. 1997. Protein 2A is not required for Theiler's virus replication. J. Virol. 71:9549-9556.
70. Molla, A., A. V. Paul, M. Schmid, S. K. Jang, and E. Wimmer. 1993. Studies on dicistronic polioviruses implicate viral proteinase 2Apro in RNA replication. Virology 196:739-747.
71. pro is essential for enterovirus replication in type I interferon-treated cells. J. Virol. 83:4412-4422.
72. Neznanov, N., A. Kondratova, K. M. Chumakov, B. Angres, B. Zhumabayeva, V. I. Agol, and A. V. Gudkov. 2001. Poliovirus protein 3A inhibits tumor necrosis factor (TNF)-induced apoptosis by eliminating the TNF receptor from the cell surface. J. Virol. 75:10409-10420.
73. Nguyen, M. L., and J. A. Blaho. 2007. Apoptosis during herpes simplex virus infection. Adv. Virus Res. 69:67-97.
74. Norris, K. L., and R. J. Youle. 2008. Cytomegalovirus proteins vMIA and m38.5 link mitochondrial morphogenesis to Bcl-2 family proteins. J. Virol. 82:6232-6243.
75. Park, N., P. Katikaneni, T. Skern, and K. E. Gustin. 2008. Differential targeting of nuclear pore complex proteins in poliovirus-infected cells. J. Virol. 82:1647-1655.
76. Peng, J. M., S. M. Liang, and C. M. Liang. 2004. VP1 of foot-and-mouth disease virus induces apoptosis via the Akt signaling pathway. J. Biol. Chem. 279:52168-52174.
77. Perfettini, J. L., T. Roumier, and G. Kroemer. 2005. Mitochondrial fusion and fission in the control of apoptosis. Trends Cell Biol. 15:179-183.
78. Piccone, M. E., E. Rieder, P. W. Mason, and M. J. Grubman. 1995. The foot-and-mouth disease virus leader proteinase gene is not required for viral replication. J. Virol. 69:5376-5382.
79. Poncet, D., 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. 2004. An anti-apoptotic viral protein that recruits Bax to mitochondria. J. Biol. Chem. 279:22605-22614.
80. Porter, F. W., Y. A. Bochkov, A. J. Albee, C. Wiese, and A. C. Palmenberg. 2006. A picornavirus protein interacts with Ran-GTPase and disrupts nucleocytoplasmic transport. Proc. Natl. Acad. Sci. USA 103:12417-12422.
81. Porter, F. W., and A. C. Palmenberg. 2009. Leader-induced phosphorylation of nucleoporins correlates with nuclear trafficking inhibition by cardioviruses. J. Virol. 83:1941-1951.
82. Rasilainen, S., P. Ylipaasto, M. Roivainen, L. Bouwens, R. Lapatto, T. Hovi, and T. Otonkoski. 2004. Mechanisms of beta cell death during restricted and unrestricted enterovirus infection. J. Med. Virol. 72:451-461.
83. Ricour, C., S. Delhaye, S. V. Hato, T. D. Olenyik, B. Michel, F. J. M. van Kuppeveld, K. E. Gustin, and T. Michiels. 2009. Inhibition of mRNA export and dimerization of interferon regulatory factor 3 by Theiler's virus leader protein. J. Gen. Virol. 90:177-186.
84. Romanova, L. I., G. A. Belov, P. V. Lidsky, E. A. Tolskaya, M. S. Kolesnikova, A. G. Evstafieva, A. B. Vartapetian, D. Egger, K. Bienz, and V. I. Agol. 2005. Variability in apoptotic response to poliovirus infection. Virology 331:292-306.
85. Salako, M. A., M. J. Carter, and G. E. N. Kass. 2006. Coxsackievirus protein 2BC blocks host cell apoptosis by inhibiting caspase-3. J. Biol. Chem. 281:16296-16304.
86. Schlitt, B. P., M. Felrice, M. L. Jelachich, and H. L. Lipton. 2003. Apoptotic cells, including macrophages, are prominent in Theiler's virus-induced inflammatory, demyelinating lesions. J. Virol. 77:4383-4388.
87. Schwarz, E. M., C. Badorff, T. S. Hiura, R. Wessely, A. Badorff, I. M. Verma, and K. U. Knowlton. 1998. NF-κB-mediated inhibition of apoptosis is required for encephalomyocarditis virus virulence: a mechanism of resistance in p50 knockout mice. J. Virol. 72:5654-5660.
88. Shih, S. R., K. F. Weng, V. Stollar, and M. L. Li. 2008. Viral protein synthesis is required for enterovirus 71 to induce apoptosis in human glioblastoma cells. J. Neurovirol. 14:53-61.
89. Stanway, G., T. Hovi, N. J. Knowles, and T. Hyypiä. 2002. Molecular and biological basis of picornavirus taxonomy. In B. L. Semler and E. Wimmer (ed.), Molecular biology of picornaviruses. ASM Press, Washington, DC.
90. Svitkin, Y. V., H. Hahn, A. C. Gingras, A. C. Palmenberg, and N. Sonenberg. 1998. Rapamycin and wortmannin enhance replication of a defective encephalomyocarditis virus. J. Virol. 72:5811-5819.
91. 2+-mediated apoptosis. Mol. Cell 16:59-68.
92. Taimen, P., H. Berghäll, R. Vainionpää, and M. Kallajoki. 2004. NuMA and nuclear lamins are cleaved during viral infection - inhibition of caspase activity prevents cleavage and rescues HeLa cells from measles virus-induced but not from rhinovirus 1B-induced cell death. Virology 320:85-98.
93. Tan, Y. J., S. G. Lim, and W. Hong. 2007. Regulation of cell death during infection by the severe acute respiratory syndrome coronavirus and other coronaviruses. Cell. Microbiol. 9:2552-2561.
94. Taylor, J. M., and M. Barry. 2006. Near death experiences: poxvirus regulation of apoptotic death. Virology 344:139-150.
95. Tolskaya, E. A., L. I. Romanova, M. S. Kolesnikova, T. A. Ivannikova, E. A. Smirnova, N. T. Raikhlin, and V. I. Agol. 1995. Apoptosis-inducing and apoptosis-preventing functions of poliovirus. J. Virol. 69:1181-1189.
96. Tsunoda, I., C. I. Kurtz, and R. S. Fujinami. 1997. Apoptosis in acute and chronic central nervous system disease induced by Theiler's murine encephalomyelitis virus. Virology 228:388-393.
97. Tsunoda, I., J. E. Libbey, and R. S. Fujinami. 2007. TGF-β1 suppresses T cell infiltration and VP2 puff B mutation enhances apoptosis in acute polioencephalitis induced by Theiler's virus. J. Neuroimmunol. 190:80-89.
98. van Pesch, V., O. van Eyll, and T. Michiels. 2001. The leader protein of Theiler's virus inhibits immediate-early alpha/beta interferon production. J. Virol. 75:7811-7817.
99. Vercammen, E., J. Staal, and R. Beyaert. 2008. Sensing of viral infection and activation of innate immunity by toll-like receptor 3. Clin. Microbiol. Rev. 21:13-25.
100. Wark, P. A., S. L. Johnston, F. Bucchieri, R. Powell, S. Puddicombe, V. Laza-Stanca, S. T. Holgate, and D. E. Davies. 2005. Asthmatic bronchial epithelial cells have a deficient innate immune response to infection with rhinovirus. J. Exp. Med. 201:937-947.
101. White, E. 2006. Mechanisms of apoptosis regulation by viral oncogenes in infection and tumorigenesis. Cell Death Differ. 13:1371-1377.
102. Whitton, J. L., C. T. Cornell, and R. Feuer. 2005. Host and virus determinants of picornavirus pathogenesis and tropism. Nat. Rev. Microbiol. 3:765-776.
103. Yeung, M. C., D. L. Chang, R. E. Camantigue, and A. S. Lau. 1999. Inhibitory role of the host apoptogenic gene PKR in the establishment of persistent infection by encephalomyocarditis virus in U937 cells. Proc. Natl. Acad. Sci. USA 96:11860-11865.
104. Youle, R. J., and M. Karbowski. 2005. Mitochondrial fission in apoptosis. Nat. Rev. Mol. Cell Biol. 6:657-663.
105. Zaragoza, C., M. Saura, E. Y. Padalko, E. Lopez-Rivera, T. R. Lizarbe, S. Lamas, and C. J. Lowenstein. 2006. Viral protease cleavage of inhibitor of kappa-B alpha triggers host cell apoptosis. Proc. Natl. Acad. Sci. USA 103:19051-19056.
106. Zoll, J., J. M. Galama, F. J. M. van Kuppeveld, and W. J. Melchers. 1996. Mengovirus leader is involved in the inhibition of host cell protein synthesis. J. Virol. 70:4948-4952.
107. Zoll, J., W. J. Melchers, J. M. Galama, and F. J. M. van Kuppeveld. 2002. The mengovirus leader protein suppresses alpha/beta interferon production by inhibition of the iron/ferritin-mediated activation of NF-κB. J. Virol. 76:9664-9672.
108. Zoll, J., F. J. M. van Kuppeveld, J. M. Galama, and W. J. Melchers. 1998. Genetic analysis of mengovirus protein 2A: its function in polyprotein processing and virus reproduction. J. Gen. Virol. 79:17-25.