Enter the kill zone: Initiation of death signaling during virus entry

Virology

Volumn 411, Issue 2, 2011, Pages 316-324

  Danthi, Pranav ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

Apoptosis; Pathogenesis; Virus entry

Indexed keywords

AMMONIUM CHLORIDE; CHLOROQUINE; DEATH RECEPTOR; DYNEIN ADENOSINE TRIPHOSPHATASE; GLYCOPROTEIN E1; GLYCOPROTEIN E2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN P54; RIBAVIRIN; TUMOR NECROSIS FACTOR RECEPTOR; VIRUS ENVELOPE PROTEIN;

AFRICAN SWINE FEVER VIRUS; APOPTOSIS; AVIAN ORTHOREOVIRUS; BLUETONGUE ORBIVIRUS; BOVINE HERPESVIRUS 1; CELL SURFACE; ENDOSOME; HERPES VIRUS; HUMAN; INTRACELLULAR TRANSPORT; MEMBRANE FUSION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; SINDBIS VIRUS; VIRUS ATTACHMENT; VIRUS CAPSID; VIRUS CELL INTERACTION; VIRUS ENTRY; VIRUS ENVELOPE; VIRUS GENOME; VIRUS PATHOGENESIS; VIRUS REPLICATION; VIRUS UNCOATING;

APOPTOSIS; HUMANS; SIGNAL TRANSDUCTION; VIRUS INTERNALIZATION; VIRUSES;

EID: 79952067487     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.12.043     Document Type: Review

References (113)

1. Agol V.I., Belov G.A., Bienz K., Egger D., Kolesnikova M.S., Romanova L.I., Sladkova L.V., Tolskaya E.A. Competing death programs in poliovirus-infected cells: commitment switch in the middle of the infectious cycle. J. Virol. 2000, 74:5534-5541.
2. Alonso C., Miskin J., Hernaez B., Fernandez-Zapatero P., Soto L., Canto C., Rodriguez-Crespo I., Dixon L., Escribano J.M. African swine fever virus protein p54 interacts with the microtubular motor complex through direct binding to light-chain dynein. J. Virol. 2001, 75:9819-9827.
3. Ammendolia M.G., Tinari A., Calcabrini A., Superti F. Poliovirus infection induces apoptosis in CaCo-2 cells. J. Med. Virol. 1999, 59:122-129.
4. Autret A., Martin-Latil S., Mousson L., Wirotius A., Petit F., Arnoult D., Colbere-Garapin F., Estaquier J., Blondel B. Poliovirus induces Bax-dependent cell death mediated by c-Jun NH2-terminal kinase. J. Virol. 2007, 81:7504-7516.
5. Autret A., Martin-Latil S., Brisac C., Mousson L., Colbere-Garapin F., Blondel B. Early phosphatidylinositol 3-kinase/Akt pathway activation limits poliovirus-induced JNK-mediated cell death. J. Virol. 2008, 82:3796-3802.
6. Banerjee M., Johnson J.E. Activation, exposure and penetration of virally encoded, membrane-active polypeptides during non-enveloped virus entry. Curr. Protein Pept. Sci. 2008, 9:16-27.
7. Barco A., Feduchi E., Carrasco L. Poliovirus protease 3C(pro) kills cells by apoptosis. Virology 2000, 266:352-360.
8. Barton E.S., Forrest J.C., Connolly J.L., Chappell J.D., Liu Y., Schnell F., Nusrat A., Parkos C.A., Dermody T.S. Junction adhesion molecule is a receptor for reovirus. Cell 2001, 104:441-451.
9. Beckham J.D., Goody R.J., Clarke P., Bonny C., Tyler K.L. A novel strategy for the treatment of viral CNS infection utilizing a cell-permeable inhibitor of c-Jun N-terminal kinase. J. Virol. 2007, 81:6984-6992.
10. Belnap D.M., McDermott B.M., Filman D.J., Cheng N., Trus B.L., Zuccola H.J., Racaniello V.R., Hogle J.M., Steven A.C. Three-dimensional structure of poliovirus receptor bound to poliovirus. Proc. Natl Acad. Sci. USA 2000, 97:73-78.
11. Benedict C.A., Norris P.S., Ware C.F. To kill or be killed: viral evasion of apoptosis. Nat. Immunol. 2002, 3:1013-1018.
12. Breckenridge D.G., Xue D. Regulation of mitochondrial membrane permeabilization by BCL-2 family proteins and caspases. Curr. Opin. Cell Biol. 2004, 16:647-652.
13. Brojatsch J., Naughton J., Rolls M.M., Zingler K., Young J.A. CAR1, a TNFR-related protein, is a cellular receptor for cytopathic avian leukosis-sarcoma viruses and mediates apoptosis. Cell 1996, 87:845-855.
14. Bron R., Wahlberg J.M., Garoff H., Wilschut J. Membrane fusion of Semliki Forest virus in a model system: correlation between fusion kinetics and structural changes in the envelope glycoprotein. EMBO J. 1993, 12:693-701.
15. Calandria C., Irurzun A., Barco A., Carrasco L. Individual expression of poliovirus 2Apro and 3Cpro induces activation of caspase-3 and PARP cleavage in HeLa cells. Virus Res. 2004, 104:39-49.
16. Carrascosa A.L., Bustos M.J., Nogal M.L., Gonzalez de Buitrago G., Revilla Y. Apoptosis induced in an early step of African swine fever virus entry into vero cells does not require virus replication. Virology 2002, 294:372-382.
17. Chattopadhyay S., Marques J.T., Yamashita M., Peters K.L., Smith K., Desai A., Williams B.R., Sen G.C. Viral apoptosis is induced by IRF-3-mediated activation of Bax. EMBO J. 2010, 29:1762-1773.
18. Chinchar V.G., Bryan L., Wang J., Long S., Chinchar G.D. Induction of apoptosis in frog virus 3-infected cells. Virology 2003, 306:303-312.
19. Chitnis N.S., D'Costa S.M., Paul E.R., Bilimoria S.L. Modulation of iridovirus-induced apoptosis by endocytosis, early expression, JNK, and apical caspase. Virology 2008, 370:333-342.
20. Clarke P., Meintzer S.M., Widmann C., Johnson G.L., Tyler K.L. Reovirus infection activates JNK and the JNK-dependent transcription factor c-Jun. J. Virol. 2001, 75:11275-11283.
21. Clarke P., Meintzer S.M., Wang Y., Moffitt L.A., Richardson-Burns S.M., Johnson G.L., Tyler K.L. JNK regulates the release of proapoptotic mitochondrial factors in reovirus-infected cells. J. Virol. 2004, 78:13132-13138.
22. Coffey C.M., Sheh A., Kim I.S., Chandran K., Nibert M.L., Parker J.S. Reovirus outer capsid protein μ1 induces apoptosis and associates with lipid droplets, endoplasmic reticulum, and mitochondria. J. Virol. 2006, 80:8422-8438.
23. Connolly J.L., Dermody T.S. Virion disassembly is required for apoptosis induced by reovirus. J. Virol. 2002, 76:1632-1641.
24. Connolly J.L., Rodgers S.E., Clarke P., Ballard D.W., Kerr L.D., Tyler K.L., Dermody T.S. Reovirus-induced apoptosis requires activation of transcription factor NF-kappaB. J. Virol. 2000, 74:2981-2989.
25. Connolly J.L., Barton E.S., Dermody T.S. Reovirus binding to cell surface sialic acid potentiates virus-induced apoptosis. J. Virol. 2001, 75:4029-4039.
26. Danthi P., Hansberger M.W., Campbell J.A., Forrest J.C., Dermody T.S. JAM-A-independent, antibody-mediated uptake of reovirus into cells leads to apoptosis. J. Virol. 2006, 80:1261-1270.
27. Danthi P., Coffey C.M., Parker J.S., Abel T.W., Dermody T.S. Independent regulation of reovirus membrane penetration and apoptosis by the mu1 phi domain. PLoS Pathog. 2008, 4:e1000248.
28. Danthi P., Kobayashi T., Holm G.H., Hansberger M.W., Abel T.W., Dermody T.S. Reovirus apoptosis and virulence are regulated by host cell membrane penetration efficiency. J. Virol. 2008, 82:161-172.
29. Danthi P., Guglielmi K.M., Kirchner E., Mainou B., Stehle T., Dermody T.S. From touchdown to transcription: the reovirus cell entry pathway. Curr. Top. Microbiol. Immunol. 2010, 343:91-113.
30. Danthi P., Pruijssers A.J., Berger A.K., Holm G.H., Zinkel S.S., Dermody T.S. Bid regulates the pathogenesis of neurotropic reovirus. PLoS Pathog. 2010, 6:e1000980.
31. DeBiasi R., Edelstein C., Sherry B., Tyler K. Calpain inhibition protects against virus-induced apoptotic myocardial injury. J. Virol. 2001, 75:351-361.
32. DeBiasi R.L., Robinson B.A., Sherry B., Bouchard R., Brown R.D., Rizeq M., Long C., Tyler K.L. Caspase inhibition protects against reovirus-induced myocardial injury in vitro and in vivo. J. Virol. 2004, 78:11040-11050.
33. Dorner A.J., Coffin J.M. Determinants for receptor interaction and cell killing on the avian retrovirus glycoprotein gp85. Cell 1986, 45:365-374.
34. Du C., Fang M., Li Y., Li L., Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell 2000, 102:33-42.
35. Finucane D.M., Bossy-Wetzel E., Waterhouse N.J., Cotter T.G., Green D.R. Bax-induced caspase activation and apoptosis via cytochrome c release from mitochondria is inhibitable by Bcl-xL. J. Biol. Chem. 1999, 274:2225-2233.
36. Forzan M., Marsh M., Roy P. Bluetongue virus entry into cells. J. Virol. 2007, 81:4819-4827.
37. Freistadt M.S., Eberle K.E. Physical association between CD155 and CD44 in human monocytes. Mol. Immunol. 1997, 34:1247-1257.
38. Freistadt M.S., Racaniello V.R. Mutational analysis of the cellular receptor for poliovirus. J. Virol. 1991, 65:3873-3876.
39. Frolov I., Schlesinger S. Comparison of the effects of Sindbis virus and Sindbis virus replicons on host cell protein synthesis and cytopathogenicity in BHK cells. J. Virol. 1994, 68:1721-1727.
40. Galindo I., Hernaez B., Diaz-Gil G., Escribano J.M., Alonso C. A179L, a viral Bcl-2 homologue, targets the core Bcl-2 apoptotic machinery and its upstream BH3 activators with selective binding restrictions for Bid and Noxa. Virology 2008, 375:561-572.
41. Girard S., Couderc T., Destombes J., Thiesson D., Delpeyroux F., Blondel B. Poliovirus induces apoptosis in the mouse central nervous system. J. Virol. 1999, 73:6066-6072.
42. Goldstaub D., Gradi A., Bercovitch Z., Grosmann Z., Nophar Y., Luria S., Sonenberg N., Kahana C. Poliovirus 2A protease induces apoptotic cell death. Mol. Cell. Biol. 2000, 20:1271-1277.
43. Gosselin A.S., Simonin Y., Guivel-Benhassine F., Rincheval V., Vayssiere J.L., Mignotte B., Colbere-Garapin F., Couderc T., Blondel B. Poliovirus-induced apoptosis is reduced in cells expressing a mutant CD155 selected during persistent poliovirus infection in neuroblastoma cells. J. Virol. 2003, 77:790-798.
44. Green D.R. Apoptotic pathways: paper wraps stone blunts scissors. Cell 2000, 102:1-4.
45. Hanon E., Vanderplasschen A., Lyaku S., Keil G., Denis M., Pastoret P.P. Inactivated bovine herpesvirus 1 induces apoptotic cell death of mitogen-stimulated bovine peripheral blood mononuclear cells. J. Virol. 1996, 70:4116-4120.
46. Hanon E., Meyer G., Vanderplasschen A., Dessy-Doize C., Thiry E., Pastoret P.P. Attachment but not penetration of bovine herpesvirus 1 is necessary to induce apoptosis in target cells. J. Virol. 1998, 72:7638-7641.
47. Hanon E., Keil G., van Drunen Littel-van den Hurk, S., Griebel P., Vanderplasschen A., Rijsewijk F.A., Babiuk L., Pastoret P.P. Bovine herpesvirus 1-induced apoptotic cell death: role of glycoprotein D. Virology 1999, 257:191-197.
48. Hansberger M.W., Campbell J.A., Danthi P., Arrate P., Pennington K.N., Marcu K.B., Ballard D.W., Dermody T.S. IκB kinase subunits α and γ are required for activation of NF-κB and induction of apoptosis by mammalian reovirus. J. Virol. 2007, 81:1360-1371.
49. Harrison S.C. Viral membrane fusion. Nat. Struct. Mol. Biol. 2008, 15:690-698.
50. Hay S., Kannourakis G. A time to kill: viral manipulation of the cell death program. J. Gen. Virol. 2002, 83:1547-1564.
51. Helenius A. Virus entry and uncoating. Fields Virology 2007, 99-118. Lippincott Williams & Wilkins, Philadelphia. Fifth ed. D.M. Knipe, P.M. Howley (Eds.).
52. Hernaez B., Diaz-Gil G., Garcia-Gallo M., Ignacio Quetglas J., Rodriguez-Crespo I., Dixon L., Escribano J.M., Alonso C. The African swine fever virus dynein-binding protein p54 induces infected cell apoptosis. FEBS Lett. 2004, 569:224-228.
53. Holm G.H., Zurney J., Tumilasci V., Leveille S., Danthi P., Hiscott J., Sherry B., Dermody T.S. Retinoic acid-inducible gene-I and interferon-beta promoter stimulator-1 augment proapoptotic responses following mammalian reovirus infection via interferon regulatory factor-3. J. Biol. Chem. 2007, 282:21953-21961.
54. Jan J.T., Griffin D.E. Induction of apoptosis by Sindbis virus occurs at cell entry and does not require viral replication. J. Virol. 1999, 73:10296-10302.
55. Jan J.T., Chatterjee S., Griffin D.E. Sindbis virus entry into cells triggers apoptosis by activating sphingomyelinase, leading to the release of ceramide. J. Virol. 2000, 74:6425-6432.
56. Joe A.K., Foo H.H., Kleeman L., Levine B. The transmembrane domains of Sindbis virus envelope glycoproteins induce cell death. J. Virol. 1998, 72:3935-3943.
57. Jones C., Chowdhury S. A review of the biology of bovine herpesvirus type 1 (BHV-1), its role as a cofactor in the bovine respiratory disease complex and development of improved vaccines. Anim. Health Res. Rev. 2007, 8:187-205.
58. Juo P., Kuo C.J., Yuan J., Blenis J. Essential requirement for caspase-8/FLICE in the initiation of the Fas-induced apoptotic cascade. Curr. Biol. 1998, 8:1001-1008.
59. Kurokawa M., Kornbluth S. Caspases and kinases in a death grip. Cell 2009, 138:838-854.
60. Labrada L., Bodelon G., Vinuela J., Benavente J. Avian reoviruses cause apoptosis in cultured cells: viral uncoating, but not viral gene expression, is required for apoptosis induction. J. Virol. 2002, 76:7932-7941.
61. Lavrik I., Golks A., Krammer P.H. Death receptor signaling. J. Cell Sci. 2005, 118:265-267.
62. Levine B., Goldman J.E., Jiang H.H., Griffin D.E., Hardwick J.M. Bcl-2 protects mice against fatal alphavirus encephalitis. Proc. Natl Acad. Sci. USA 1996, 93:4810-4815.
63. Lewis J., Wesselingh S.L., Griffin D.E., Hardwick J.M. Alphavirus-induced apoptosis in mouse brains correlates with neurovirulence. J. Virol. 1996, 70:1828-1835.
64. Li P., Nijhawan D., Budhardjo I., Srinivasula S.M., Ahmad M., Alnemri E.S., Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 1997, 91:479-489.
65. Lin K.I., Lee S.H., Narayanan R., Baraban J.M., Hardwick J.M., Ratan R.R. Thiol agents and Bcl-2 identify an alphavirus-induced apoptotic pathway that requires activation of the transcription factor NF-kappa B. J. Cell Biol. 1995, 131:1149-1161.
66. Liu X., Kim C.N., Yang J., Jemmerson R., Wang X. Induction of apoptotic program in cell-free extracts: requirement for dATP and cytochrome c. Cell 1996, 86:147-157.
67. Liu Y., Cai Y., Zhang X. Induction of caspase-dependent apoptosis in cultured rat oligodendrocytes by murine coronavirus is mediated during cell entry and does not require virus replication. J. Virol. 2003, 77:11952-11963.
68. Loo Y.M., Fornek J., Crochet N., Bajwa G., Perwitasari O., Martinez-Sobrido L., Akira S., Gill M.A., Garcia-Sastre A., Katze M.G., Gale M. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J. Virol. 2008, 82:335-345.
69. Lopez-Guerrero J.A., Alonso M., Martin-Belmonte F., Carrasco L. Poliovirus induces apoptosis in the human U937 promonocytic cell line. Virology 2000, 272:250-256.
70. McCrae M.A., Joklik W.K. The nature of the polypeptide encoded by each of the ten double-stranded RNA segments of reovirus type 3. Virology 1978, 89:578-593.
71. Montgomery R.I., Warner M.S., Lum B.J., Spear P.G. Herpes simplex virus-1 entry into cells mediated by a novel member of the TNF/NGF receptor family. Cell 1996, 87:427-436.
72. Morrison M.E., He Y.J., Wien M.W., Hogle J.M., Racaniello V.R. Homolog-scanning mutagenesis reveals poliovirus receptor residues important for virus binding and replication. J. Virol. 1994, 68:2578-2588.
73. Mortola E., Larsen A. Bluetongue virus infection: activation of the MAP kinase-dependent pathway is required for apoptosis. Res. Vet. Sci. 2010, 89:460-464.
74. Mortola E., Noad R., Roy P. Bluetongue virus outer capsid proteins are sufficient to trigger apoptosis in mammalian cells. J. Virol. 2004, 78:2875-2883.
75. Mustoe T.A., Ramig R.F., Sharpe A.H., Fields B.N. Genetics of reovirus: identification of the dsRNA segments encoding the polypeptides of the μ and σ size classes. Virology 1978, 89:594-604.
76. Narita M., Shimizu S., Ito T., Chittenden T., Lutz R.J., Matsuda H., Tsujimoto Y. Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria. Proc. Natl Acad. Sci. USA 1998, 95:14681-14686.
77. Nieva J.L., Bron R., Corver J., Wilschut J. Membrane fusion of Semliki Forest virus requires sphingolipids in the target membrane. EMBO J. 1994, 13:2797-2804.
78. Nogal M.L., Gonzalez de Buitrago G., Rodriguez C., Cubelos B., Carrascosa A.L., Salas M.L., Revilla Y. African swine fever virus IAP homologue inhibits caspase activation and promotes cell survival in mammalian cells. J. Virol. 2001, 75:2535-2543.
79. Oberhaus S.M., Smith R.L., Clayton G.H., Dermody T.S., Tyler K.L. Reovirus infection and tissue injury in the mouse central nervous system are associated with apoptosis. J. Virol. 1997, 71:2100-2106.
80. O'Connor L., Strasser A., O'Reilly L.A., Hausmann G., Adams J.M., Cory S., Huang D.C. Bim: a novel member of the Bcl-2 family that promotes apoptosis. EMBO J. 1998, 17:384-395.
81. O'Donnell S.M., Hansberger M.W., Connolly J.L., Chappell J.D., Watson M.J., Pierce J.M., Wetzel J.D., Han W., Barton E.S., Forrest J.C., Valyi-Nagy T., Yull F.E., Blackwell T.S., Rottman J.N., Sherry B., Dermody T.S. Organ-specific roles for transcription factor NF-κB in reovirus-induced apoptosis and disease. J. Clin. Investig. 2005, 115:2341-2350.
82. Opferman J.T., Korsmeyer S.J. Apoptosis in the development and maintenance of the immune system. Nat. Immunol. 2003, 4:410-415.
83. Oura C.A., Powell P.P., Parkhouse R.M. African swine fever: a disease characterized by apoptosis. J. Gen. Virol. 1998, 79(Pt 6):1427-1438.
84. Pettus B.J., Chalfant C.E., Hannun Y.A. Ceramide in apoptosis: an overview and current perspectives. Biochim. Biophys. Acta 2002, 1585:114-125.
85. Ping-Yuan L., Hung-Jen L., Meng-Jiun L., Feng-Ling Y., Hsue-Yin H., Jeng-Woei L., Wen-Ling S. Avian reovirus activates a novel proapoptotic signal by linking Src to p53. Apoptosis 2006, 11:2179-2193.
86. Puthalakath H., Huang D.C., O'Reilly L.A., King S.M., Strasser A. The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol. Cell 1999, 3:287-296.
87. Ramsey-Ewing A., Moss B. Apoptosis induced by a postbinding step of vaccinia virus entry into Chinese hamster ovary cells. Virology 1998, 242:138-149.
88. Riedel N., Hoover E.A., Dornsife R.E., Mullins J.I. Pathogenic and host range determinants of the feline aplastic anemia retrovirus. Proc. Natl Acad. Sci. USA 1988, 85:2758-2762.
89. Roulston A., Marcellus R.C., Branton P.E. Viruses and apoptosis. Annu. Rev. Microbiol. 1999, 53:577-628.
90. Roy P. Bluetongue virus proteins and particles and their role in virus entry, assembly, and release. Adv. Virus Res. 2005, 64:69-123.
91. Roy P. Orboviruses. Fields Virology 2007, 1975-1997. Lippincott Williams & Wilkins, Philadelphia. D.M. Knipe, P.M. Howley (Eds.).
92. Scaffidi C., Fulda S., Srinivasan A., Friesen C., Li F., Tomaselli K.J., Debatin K.M., Krammer P.H., Peter M.E. Two CD95 (APO-1/Fas) signaling pathways. EMBO J. 1998, 17:1675-1687.
93. Schiff L.A., Nibert M.L., Tyler K.L. Orthoreoviruses and their replication. Fields Virology 2007, 1853-1915. Lippincott Williams & Wilkins, Philadelphia. Fifth ed. D.M. Knipe, P.M. Howley (Eds.).
94. Shepley M.P., Racaniello V.R. A monoclonal antibody that blocks poliovirus attachment recognizes the lymphocyte homing receptor CD44. J. Virol. 1994, 68:1301-1308.
95. Shi Y. Caspase activation: revisiting the induced proximity model. Cell 2004, 117:855-858.
96. Shih W.L., Hsu H.W., Liao M.H., Lee L.H., Liu H.J. Avian reovirus sigmaC protein induces apoptosis in cultured cells. Virology 2004, 321:65-74.
97. Siliciano R.F. The role of CD4 in HIV envelope-mediated pathogenesis. Curr. Top. Microbiol. Immunol. 1996, 205:159-179.
98. Sprick M.R., Walczak H. The interplay between the Bcl-2 family and death receptor-mediated apoptosis. Biochem. Biophys. Acta 2004, 1644:125-132.
99. Srinivasula S.M., Ahmad M., Fernandes-Alnemri T., Alnemri E.S. Autoactivation of procaspase-9 by Apaf-1-mediated oligomerization. Mol. Cell 1998, 1:949-957.
100. Srinivasula S.M., Datta P., Fan X.J., Fernandes-Alnemri T., Huang Z., Alnemri E.S. Molecular determinants of the caspase-promoting activity of Smac/DIABLO and its role in the death receptor pathway. J. Biol. Chem. 2000, 275:36152-36157.
101. Tolskaya E.A., Romanova L.I., Kolesnikova M.S., Ivannikova T.A., Smirnova E.A., Raikhlin N.T., Agol V.I. Apoptosis-inducing and apoptosis-preventing functions of poliovirus. J. Virol. 1995, 69:1181-1189.
102. Tsai B. Penetration of nonenveloped viruses into the cytoplasm. Annu. Rev. Cell Dev. Biol. 2007, 23:23-43.
103. Tyler K.L., Squier M.K., Rodgers S.E., Schneider B.E., Oberhaus S.M., Grdina T.A., Cohen J.J., Dermody T.S. Differences in the capacity of reovirus strains to induce apoptosis are determined by the viral attachment protein sigma 1. J. Virol. 1995, 69:6972-6979.
104. Tyler K.L., Squier M.K., Brown A.L., Pike B., Willis D., Oberhaus S.M., Dermody T.S., Cohen J.J. Linkage between reovirus-induced apoptosis and inhibition of cellular DNA synthesis: role of the S1 and M2 genes. J. Virol. 1996, 70:7984-7991.
105. Urban C., Rheme C., Maerz S., Berg B., Pick R., Nitschke R., Borner C. Apoptosis induced by Semliki Forest virus is RNA replication dependent and mediated via Bak. Cell Death Differ. 2008, 15:1396-1407.
106. Wahid R., Cannon M.J., Chow M. Dendritic cells and macrophages are productively infected by poliovirus. J. Virol. 2005, 79:401-409.
107. Wei M.C., Lindsten T., Mootha V.K., Weiler S., Gross A., Ashiya M., Thompson C.B., Korsmeyer S.J. tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev. 2000, 14:2060-2071.
108. White J.M., Delos S.E., Brecher M., Schornberg K. Structures and mechanisms of viral membrane fusion proteins: multiple variations on a common theme. Crit. Rev. Biochem. Mol. Biol. 2008, 43:189-219.
109. Wisniewski M.L., Werner B.G., Hom L.G., Anguish L.J., Coffey C.M., Parker J.S. Reovirus infection or ectopic expression of outer-capsid protein {mu}1 induces apoptosis independently of the cellular proapoptotic proteins Bax and Bak. J. Virol. 2010, 85:296-304.
110. Yujiri T., Ware M., Widmann C., Oyer R., Russell D., Chan E., Zaitsu Y., Clarke P., Tyler K., Oka Y., Fanger G.R., Henson P., Johnson G.L. MEK kinase 1 gene disruption alters cell migration and c-Jun NH2-terminal kinase regulation but does not cause a measurable defect in NF-kappa B activation. Proc. Natl Acad. Sci. USA 2000, 97:7272-7277.
111. Zha J., Weiler S., Oh K.J., Wei M.C., Korsmeyer S.J. Posttranslational N-myristoylation of BID as a molecular switch for targeting mitochondria and apoptosis. Science 2000, 290:1761-1765.
112. Zhivotovsky B. Caspases: the enzymes of death. Essays Biochem. 2003, 39:25-40.
113. Zou H., Henzel W.J., Liu X., Lutschg A., Wang X. Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 1997, 90:405-413.