Inhibition of NF-κ B activity and cFLIP expression contribute to viral-induced apoptosis

Apoptosis

Volumn 10, Issue 3, 2005, Pages 513-524

  Clarke, P ^a,c   DeBiasi, R L ^a,b,c   Meintzer, S M ^a,c   Robinson, B A ^a,c   Tyler, K L ^a,c  

^a UNIVERSITY OF COLORADO   (United States)

^b Children's Hospital Colorado   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

cFLIP; Myocytes; NF B; Reovirus

Indexed keywords

FLICE INHIBITORY PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN;

APOPTOSIS; ARTICLE; CONTROLLED STUDY; HEART MUSCLE CELL; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REOVIRUS; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; VIRUS STRAIN;

APOPTOSIS; CASP8 AND FADD-LIKE APOPTOSIS REGULATING PROTEIN; CELL LINE; GENE EXPRESSION REGULATION; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MAMMALIAN ORTHOREOVIRUS 3; MYOCYTES, CARDIAC; NF-KAPPA B; ORTHOREOVIRUS, MAMMALIAN; REASSORTANT VIRUSES; REOVIRIDAE INFECTIONS;

ORTHOREOVIRUS; REOVIRUS SP.;

EID: 21244479741     PISSN: 13608185     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10495-005-1881-4     Document Type: Article

References (75)

1. Clarke P, Tyler KL. Reovirus-induced apoptosis: A minireview. Apoptosis 2003; 8: 141-150.
2. Oberhaus SM, Smith RL, Clayton GH, Dermody TS, Tyler KL. Reovirus infection and tissue injury in the mouse central nervous system are associated with apoptosis. J Virol 1997; 71: 2100-2106.
3. Richardson-Burns SM, Kominsky DJ, Tyler KL. Reovirus-induced neuronal apoptosis is mediated by caspase 3 and is associated with the activation of death receptors. J Neuroviro 2002; 8: 365-380.
4. DeBiasi RL, Edelstein CL, Sherry B, Tyler KL. Calpain inhibition protects against virus-induced apoptotic myocardial injury. J Virol 2001; 75: 351-361.
5. Richardson-Burns SM, Tyler KL. Regional differences in viral growth and central nervous system injury correlate with apoptosis. J Virol 2004; 78: 5466-5475.
6. Clarke P, Meintzer SM, Gibson S, et al. Reovirus-induced apoptosis is mediated by TRAIL. J Virol 2000; 74: 8135-8139.
7. Kominsky DJ, Bickel RJ, Tyler KL. Reovirus-induced apoptosis requires both death receptor- and mitochondrial-mediated caspase-dependent pathways of cell death. Cell Death Differ 2002; 9: 926-933.
8. Kominsky DJ, Bickel RJ, Tyler KL. Reovirus-induced apoptosis requires mitochondrial release of Smac/DIABLO and involves reduction of cellular inhibitor of apoptosis protein levels. J Virol 2002; 76: 11414-11424.
9. Clarke P, Meintzer SM, Spalding AC, Johnson GL, Tyler KL. Caspase 8-dependent sensitization of cancer cells to TRAIL-induced apoptosis following reovirus-infection. Oncogene 2001; 20: 6910-6919.
10. Baeuerle PA, Baltimore D. A 65-kappaD subunit of active NF-kappaB is required for inhibition of NF-kappaB by I kappaB. Genes Dev 1989; 3: 1689-1698.
11. Ghosh S, Gifford AM, Riviere LR, Tempst P, Nolan GP, Baltimore D. Cloning of the p50 DNA binding subunit of NF-kappa B: homology to rel and dorsal. Cell 1990; 62: 1019-1029.
12. Baeuerle PA, Baltimore D. I kappa B: A specific inhibitor of the NF-kappa B transcription factor. Science 1988; 242: 540-546.
13. Verma IM, Stevenson JK, Schwarz EM, Van Antwerp D, Miyamoto S. Rel/NF-kappa B/I kappa B family: Intimate tales of association and dissociation. Genes Dev 1995; 9: 2723-2735.
14. Brockman JA, Scherer DC, McKinsey TA, et al. Coupling of a signal response domain in I kappa B alpha to multiple pathways for NF-kappa B activation. Mol Cell Biol 1995; 15: 2809-2818.
15. Brown K, Gerstberger S, Carlson L, Franzoso G, Siebenlist U. Control of I kappa B-alpha proteolysis by site-specific, signal-induced phosphorylation. Science 1995; 267: 1485-1488.
16. Chen Z, Hagler J, Palombella VJ, et al. Signal-induced site-specific phosphorylation targets I kappa B alpha to the ubiquitin-proteasome pathway. Genes Dev 1995; 9: 1586-1597.
17. Traenckner EB, Pahl HL, Henkel T, Schmidt KN, Wilk S, Baeuerle PA. Phosphorylation of human I kappa B-alpha on serines 32 and 36 controls I kappa B-alpha proteolysis and NF-kappa B activation in response to diverse stimuli. EMBO J 1995; 14: 2876-2883.
18. Connolly JL, Rodgers SE, Clarke P, et al. Reovirus-induced apoptosis requires activation of transcription factor NF-kappaB. J Virol 2000; 74: 2981-2989.
19. Clarke P, Meintzer SM, Moffitt LA, Tyler KL. Two distinct phases of virus-induced nuclear factor kappa B regulation enhance tumor necrosis factor-related apoptosis-inducing ligand-mediated apoptosis in virus-infected cells. J Biol Chem 2003; 278: 18092-18100.
20. Tyler KL, Squier MK, Rodgers SE, et al. 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.
21. Tyler KL, Squier MK, Brown AL, et al. Linkage between reovirus-induced apoptosis and inhibition of cellular DNA synthesis: role of the S1 and M2 genes. J Virol 1996; 70: 7984-7991.
22. Rodgers SE, Barton ES, Oberhaus SM, et al. Reovirus-induced apoptosis of MDCK cells is not linked to viral yield and is blocked by Bcl-2. J Virol 1997; 71: 2540-2546.
23. Connolly JL, Barton ES, Dermody TS. Reovirus binding to cell surface sialic acid potentiates virus-induced apoptosis. J Virol 2001; 75: 4029-4039.
24. Wilson GA, Morrison LA, Fields BN. Association of the reovirus S1 gene with serotype 3-induced biliary atresia in mice. J Virol 1994; 68: 6458-6465.
25. Sherry B, Fields BN. The reovirus M1 gene, encoding a viral core protein, is associated with the myocarditic phenotype of a reovirus variant. J Virol 1989; 63: 4850-4856.
26. Sherry B, Blum MA. Multiple viral core proteins are determinants of reovirus-induced acute myocarditis. J Virol 1994; 68: 8461-8465.
27. Perlman H, Pagliari LJ, Georganas C, Mano T, Walsh K, Pope RM. FLICE-inhibitory protein expression during macrophage differentiation confers resistance to Fas-mediated apoptosis. J Exp Med 1999; 190: 1679-1688.
28. Okano H, Shiraki K, Inoue H, et al. Cellular FLICE/caspase-8-inhibitory protein as a principal regulator of cell death and survival in human hepatocellular carcinoma. Lab Invest 2003; 83: 1033-1043.
29. Sherry B. Pathogenesis of reovirus myocarditis. In: KL Tyler Oldstone MBA eds. Reoviruses II: Cytopathogenicity and Pathogenesis. Berlin, Germany: Springer-Verlag 1998: 51-66.
30. Sherry B, Schoen FJ, Wenske E, Fields BN. Derivation and characterization of an efficiently myocarditic reovirus variant. J Virol 1989; 63: 4840-4849.
31. DeBiasi RL, Robinson BA, Sherry B, et al. Caspase inhibition protects against reovirus-induced myocardial injury in vitro and in vivo. J Virol 2004; 78: 11040-11050.
32. Stewart MJ, Blum MA, Sherry B. PKR's protective role in viral myocarditis. Virology 2003; 314: 92-100.
33. Azzam-Smoak K, Noah DL, Stewart MJ, Blum MA, Sherry B. Interferon regulatory factor-1, interferon-beta, and reovirus-induced myocarditis. Virology 2002; 298: 20-29.
34. Sherry B, Torres J, Blum MA. Reovirus induction of and sensitivity to beta interferon in cardiac myocyte cultures correlate with induction of myocarditis and are determined by viral core proteins. J Virol 1998; 72: 1314-1323.
35. Noah DL, Blum MA, Sherry B. Interferon regulatory factor 3 is required for viral induction of beta interferon in primary cardiac myocyte cultures. J Virol 1999; 73: 10208-10213.
36. Kreuz S, Siegmund D, Scheurich P, Wajant H. NF-kappaB inducers upregulate cFLIP, a cycloheximide-sensitive inhibitor of death receptor signaling. Mol Cell Biol 2001; 21: 3964-3973.
37. Roulston A, Lin R, Beauparlant P, Wainberg MA, Hiscott J. Regulation of human immunodeficiency virus type 1 and cytokine gene expression in myeloid cells by NF-kappa B/Rel transcription factors. Microbiol Rev 1995; 59: 481-505.
38. Sun SC, Ballard DW. Persistent activation of NF-kappaB by the tax transforming protein of HTLV-1: Hijacking cellular IkappaB kinases. Oncogene 1999; 18: 6948-6958.
39. Weil R, Sirma H, Giannini C, et al. Direct association and nuclear import of the hepatitis B virus X protein with the NF-kappaB inhibitor IkappaBalpha. Mol Cell Biol 1999; 19: 6345-6354.
40. You LR, Chen CM, Lee YH. Hepatitis C virus core protein enhances NF-kappaB signal pathway triggering by lymphotoxin-beta receptor ligand and tumor necrosis factor alpha. J Virol 1999; 73: 1672-1681.
41. Tai DI, Tsai SL, Chen YM, et al. Activation of nuclear factor kappaB in hepatitis C virus infection: Implications for pathogenesis and hepatocarcinogenesis. Hepatology 2000; 31: 656-664.
42. Sylla BS, Hung SC, Davidson DM, et al. Epstein-Barr virus-transforming protein latent infection membrane protein 1 activates transcription factor NF-kappaB through a pathway that includes the NF-kappaB-inducing kinase and the IkappaB kinases IKKalpha and IKKbeta. Proc Natl Acad Sci USA 1998; 95: 10106-10111.
43. Casola A, Garofalo RP, Crawford SE, et al. Interleukin-8 gene regulation in intestinal epithelial cells infected with rotavirus: Role of viral-induced IkappaB kinase activation. Virology 2002; 298: 8-19.
44. Pahl HL, Baeuerle PA. The ER-overload response: Activation of NF-kappa B. Trends Biochem Sci 1997; 22: 63-67.
45. Hiscott J, Kwon H, Genin P. Hostile takeovers: Viral appropriation of the NF-kappaB pathway. J Clin Invest 2001; 107: 143-151.
46. Lin KI, Lee SH, Narayanan R, Baraban JM, Hardwick JM, Ratan RR. Thiol agents and Bcl-2 identify an alphavirus-induced apoptotic pathway that requires activation of the transcription factor NF-kappaB. J Cell Biol 1995; 131: 1149-1161.
47. Lin KI, DiDonato JA, Hoffmann A, Hardwick JM, Ratan RR. Suppression of steady-state, but not stimulus-induced NF-kappaB activity inhibits alphavirus-induced apoptosis. J Cell Biol 1998; 141: 1479-1487.
48. Jan JT, Chen BH, Ma SH, et al. Potential dengue virus-triggered apoptotic pathway in human neuroblastoma cells: Arachidonic acid, superoxide anion, and NF-kappaB are sequentially involved. J Virol 2000; 74: 8680-8691.
49. Shao R, Hu MC, Zhou BP, et al. E1A sensitizes cells to tumor necrosis factor-induced apoptosis through inhibition of IkappaB kinases and nuclear factor kappaB activities. J Biol Chem 1999; 274: 21495-21498.
50. Shrivastava A, Manna SK, Ray R, Aggarwal BB. Ectopic expression of hepatitis C virus core protein differentially regulates nuclear transcription factors. J Virol 1998; 72: 9722-9728.
51. Powell PP, Dixon LK, Parkhouse RM. An IkappaB homolog encoded by African swine fever virus provides a novel mechanism for downregulation of proinflammatory cytokine responses in host macrophages. J Virol 1996; 70: 8527-8533.
52. 2/M cell cycle arrest requires σ1s and occurs in the absence of apoptosis. J Virol 2000; 74: 9562-9570.
53. Poggioli GJ, Dermody TS, Tyler KL. Reovirus-induced σ1s-dependent G2/M phase cell cycle arrest is associated with inhibition of p34cdc2. J Virol 2001; 75: 7429-7434.
54. Hoyt CC, Bouchard RJ, Tyler KL. Novel nuclear herniations induced by nuclear localization of a viral protein. J Virol 2004; 78: 6360-6369.
55. Hoyt CC, Richardson-Burns SM, Goody RJ, Robinson BA, DeBiasi RL, Tyler KL. Nonstructural protein σ1s is a determinant of reovirus virulence and influences the kinetics and severity of apoptosis induction in the heart and central nervous system. J Virol 2005; 79: 2743-2753.
56. Chappell JD, Prota AE, Dermody TS, Stehle T. Crystal structure of reovirus attachment protein sigma 1 reveals evolutionary relationship to adenovirus fiber. EMBO J 2002; 15: 1-11.
57. Barton ES, Forrest JC, Connolly JL, et al. Junction adhesion molecule is a receptor for reovirus. Cell 2001; 104: 441-451.
58. Chappell JD, Duong JL, Wright BW, Dermody TS. Identification of carbohydrate-binding domains in the attachment proteins of Type 1 and Type 3 reoviruses. J Virol 2000; 74: 8472-8479.
59. Clarke P, Meintzer SM, Widmann C, Johnson GL, Tyler KL. Reovirus infection activates JNK and the JNK-dependent transcription factor c-Jun. J Virol 2001; 75: 11275-11283.
60. Clarke P, Meintzer SM, Wang Y, et al. JNK regulates the release of proapoptotic mitochondrial factors in reovirus-infected cells. J Virol 2004; 78: 13132-13138.
61. Gibson SB, Oyer R, Spalding AC, Anderson SM, Johnson GL. Increased expression of death receptors 4 and 5 synergizes the apoptosis response to combined treatment with etoposide and TRAIL. Mol Cell Biol 2000; 20: 205-212.
62. Ravi R, Bedi GC, Engstrom LW, et al. Regulation of death receptor expression and TRAIL/Apo2L-mduced apoptosis by NF-kappaB. Nat Cell Biol 2001; 3: 409-416.
63. Spalding AC, Jotte RM, Scheinman RI, et al. TRAIL and inhibitors of apoptosis are opposing determinants for NF-kappaB-dependent, genotoxin-induced apoptosis of cancer cells. Oncogene 2002; 21: 260-271.
64. Rivera-Walsh I, Waterfield M, Xiao G, Fong A, Sun SC. NF-kappaB signaling pathway governs TRAIL gene expression and human T-cell leukemia virus-I Tax-induced T-cell death. J Biol Chem 2001; 276: 40385-40388.
65. Jeremias I, Herr I, Boehler T, Debatin KM. TRAIL/Apo-2-ligand-induced apoptosis in human T cells. Eur J Immunol 1998; 28: 143-152.
66. Takizawa T, Matsukawa S, Higuchi Y, Nakamura S, Nakanishi Y, Fukuda R. Induction of programmed cell death (apoptosis) by influenza virus infection in tissue culture cells. J Gen Virol 1993; 74: 2347-2355.
67. Takizawa T, Fukuda R, Miyawaki T, Ohashi K, Nakanishi Y. Activation of the apoptotic Fas antigen-encoding gene upon influenza virus infection involving spontaneously produced beta-interferon. Virology 1995; 209: 288-296.
68. Sieg S, Yildirim Z, Smith D, et al. Herpes simplex virus type 2 inhibition of Fas ligand expression. J Virol 1996; 70: 8747-8751.
69. Wang GH, Bertin J, Wang Y, et al. Bovine herpesvirus 4 BORFE2 protein inhibits Fas- and tumor necrosis factor receptor 1-induced apoptosis and contains death effector domains shared with other gamma-2 herpesviruses. J Virol 1997; 71: 8928-8932.
70. Tollefson AE, Hermiston TW, Lichtenstein DL, et al. Forced degradation of Fas inhibits apoptosis in adenovirus-infected cells. Nature 1998; 392: 726-730.
71. Conaldi PG, Biancone L, Bottelli A, et al. HIV-1 kills renal tubular epithelial cells in vitro by triggering an apoptotic pathway involving caspase activation and Fas upregulation. J Clin Invest 1998; 102: 2041-2049.
72. Kaplan D, Sieg S. Role of the Fas/Fas ligand apoptotic pathway in human immunodeficiency virus type 1 disease. J Virol 1998; 72: 6279-6282.
73. Su F, Schneider RJ. Hepatitis B virus HBx protein sensitizes cells to apoptotic killing by tumor necrosis factor alpha. Proc Natl Acad Sci USA 1997; 94: 8744-8749.
74. Herbein G, Mahlknecht U, Batliwalla F, et al. Apoptosis of CD8+ T cells is mediated by macrophages through interaction of HIV gp120 with chemokine receptor CXCR4. Nature 1998; 395: 189-194.
75. Johnson DE, Gastman BR, Wieckowski E, et al. Inhibitor of apoptosis protein hILP undergoes caspase-mediated cleavage during T lymphocyte apoptosis. Cancer Res 2000; 60: 1818-1823.