NF-κB and virus infection: Who controls whom

EMBO Journal

Volumn 22, Issue 11, 2003, Pages 2552-2560

  Santoro, M Gabriella ^a   Rossi, Antonio ^a   Amici, Carla ^a  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

Antiviral; Cyclopentenone prostanoids; I B qkinase; NF B; Viral infection

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NUCLEIC ACID; REGULATOR PROTEIN; STRUCTURAL PROTEIN; TRANSCRIPTION FACTOR;

CELL MEMBRANE PERMEABILITY; GENOME; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROGENY; PROTEIN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION; VIRUS CELL INTERACTION; VIRUS GENOME; VIRUS INFECTION; VIRUS REPLICATION; VIRUS SURVIVAL; ANIMAL; BIOLOGICAL MODEL; HUMAN; PATHOGENICITY; PATHOPHYSIOLOGY; PHYSIOLOGY; VIRAL PHENOMENA AND FUNCTIONS; VIROLOGY; VIRUS;

ANIMALS; HUMANS; MODELS, BIOLOGICAL; NF-KAPPA B; SIGNAL TRANSDUCTION; VIRAL PHYSIOLOGY; VIRUS DISEASES; VIRUSES;

EID: 0038605236     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/cdg267     Document Type: Review

References (99)

1. Akari, H., Bour, S., Kao, S., Adachi, A. and Strebel, K. (2001) The human immunodeficiency virus type 1 accessory protein Vpu induces apoptosis by suppressing the nuclear factor κB-dependent expression of antiapoptotic factors. J. Exp. Med., 194, 1299-1311.
2. Amici, C., Belardo, G., Rossi, A. and Santoro, M.G. (2001) Activation of IκB kinase by herpes simplex virus type 1. A novel target for antiherpetic therapy. J. Biol. Chem., 276, 28759-28766.
3. Bargou, R.C. et al. (1997) Constitutive nuclear factor-κB-RelA activation is required for proliferation and survival of Hodgkin's disease tumor cells. J. Clin. Invest., 100, 2961-2969.
4. Baud, V. and Karin, M. (2001) Signal transduction by tumor necrosis factor and its relatives. Trends Cell Biol., 11, 372-377.
5. Biswas, D.K. et al. (1998) Inhibition of HIV-1 replication by combination of a novel inhibitor of TNF-α with AZT. J. Acquir. Immune Defic. Syndr. Hum. Retrovirol., 15, 426-434.
6. Boivin, G., Coulombe, Z. and Rivest, S. (2002) Intranasal herpes simplex virus type 2 inoculation causes a profound thymidine kinase dependent cerebral inflammatory response in the mouse hindbrain. Eur. J. Neurosci., 16, 29-43.
7. Bour, S., Perrin, C., Akari, H. and Strebel, K. (2001) The human immunodeficiency virus type 1 Vpu protein inhibits NF-κB activation by interfering with βTrCP-mediated degradation of IκB. J. Biol. Chem., 276, 15920-15928.
8. Bowie, A., Kiss-Toth, E., Symons, J.A., Smith, G.L., Dower, S.K. and O'Neill, L.A.J. (2000) A46R and A52R from vaccinia virus are antagonists of host IL-1 and toll-like receptor signaling. Proc. Natl Acad. Sci. USA, 97, 10162-10167.
9. Briand, G., Barbeau, B. and Tremblay, M. (1997) Binding of HIV-1 to its receptor induces tyrosine phosphorylation of several CD4-associated proteins, including the phosphatidylinositol 3-kinase. Virology, 228, 171-179.
10. Busch, L.K. and Bishop, G.A. (2001) Multiple carboxyl-terminal regions of the EBV oncoprotein, latent membrane protein 1, cooperatively regulate signaling to B lymphocytes via TNF receptor-associated factor (TRAF)-dependent and TRAF-independent mechanisms. J. Immunol., 167, 5805-5813.
11. Cahir-McFarland, E.D., Davidson, D.M., Schauer, S.L., Duong, J. and Kieff, E. (2000) NF-κB inhibition causes spontaneous apoptosis in Epstein-Barr virus-transformed lymphoblastoid cells. Proc. Natl Acad. Sci. USA, 97, 6055-6060.
12. Chen, G. and Goeddel, D.V. (2002) TNF-R1 signaling: a beautiful pathway. Science, 296, 1634-1635.
13. Chen, L.F., Fischle, W., Verdin, E. and Greene, W.C. (2001) Duration of nuclear NF-κB action regulated by reversible acetylation. Science, 293, 1653-1657.
14. Cherrington, J.M. and Mocarski, E.S. (1989) Human cytomegalovirus IE1 transactivates the α promoter-enhancer via an 18-base-pair repeat element. J. Virol., 63, 1435-1440.
15. Chiao, P.J., Na, R., Niu, J., Sclabas, G.M., Dong, Q. and Curley, S.A. (2002) Role of Rel/NF-κB transcription factors in apoptosis of human hepatocellular carcinoma cells. Cancer, 95, 1696-1705.
16. Chu, Z.L., Shin, Y.A., Yang, J.M., DiDonato, J.A. and Ballard, D.W. (1999) IKKγ mediates the interaction of cellular IκB kinases with the tax transforming protein of human T cell leukemia virus type 1. J. Biol. Chem., 274, 15297-15300.
17. Conant, K., Ma, M., Nath, A. and Major, E.O. (1996) Extracellular human immunodeficiency virus type 1 Tat protein is associated with an increase in both NF-κB binding and protein kinase C activity in primary human astrocytes. J. Virol., 70, 1384-1389.
18. Connolly, S.A., Landsburg, D.J., Carfi, A., Wiley, D.C., Eisenberg, R.J. and Cohen, G.H. (2002) Structure-based analysis of the herpes simplex virus glycoprotein D binding site present on herpesvirus entry mediator HveA (HVEM). J. Virol., 76, 10894-10904.
19. D'Addario, M., Ahmad, A., Morgan, A. and Menezes, J. (2000) Binding of the Epstein-Barr virus major envelope glycoprotein gp350 results in the up-regulation of the TNF-α gene expression in monocytic cells via NF-κB involving PKC, PI3-K and tyrosine kinases. J. Mol. Biol., 298, 765-778.
20. Delhase, M., Hayakawa, M., Chen, Y. and Karin, M. (1999) Positive and negative regulation of IκB kinase activity through IKKβ subunit phosphorylation. Science, 284, 309-313.
21. Demarchi, F., Gutierrez, M.I. and Giacca, M. (1999) Human immunodeficiency virus type 1 tat protein activates transcription factor NF-κB through the cellular interferon-inducible, double-stranded RNA-dependent protein kinase, PKR. J. Virol., 73, 7080-7086.
22. Diao, J., Garces, R. and Richardson, C.D. (2001) X protein of hepatitis B virus modulates cytokine and growth factor related signal transduction pathways during the course of viral infections and hepatocarcinogenesis. Cytokine Growth Factor Rev., 12, 189-205.
23. Doria, M., Klein, N., Lucito, R. and Schneider, R.J. (1995) The hepatitis B virus HBx protein is a dual specificity cytoplasmic activator of Ras and nuclear activator of transcription factors. EMBO J., 14, 4747-4757.
24. Dreyfus, D.H., Nagasawa, M., Pratt, J.C., Kelleher, C.A. and Gelfand, E.W. (1999) Inactivation of NF-κB by EBV BZLF-1-encoded ZEBRA protein in human T cells. J. Immunol., 163, 6261-6268.
25. Eliopoulos, A.G. et al. (2002) The oncogenic protein kinase Tpl-2/Cot contributes to Epstein-Barr virus-encoded latent infection membrane protein 1-induced NF-κB signaling downstream of TRAF2. J. Virol., 76, 4567-4579.
26. Flory, E., Weber, C.K., Chen, P., Hoffmeyer, A., Jassoy, C. and Rapp, U.R. (1998) Plasma membrane-targeted Raf kinase activates NF-κB and human immunodeficiency virus type 1 replication in T lymphocytes. J. Virol., 72, 2788-2794.
27. Flory, E. et al. (2000) Influenza virus-induced NF-κB-dependent gene expression is mediated by overexpression of viral proteins and involves oxidative radicals and activation of IκB kinase. J. Biol. Chem., 275, 8307-8314.
28. Fu, D.X., Kuo, Y.L., Liu, B.Y., Jeang, K.T. and Giam, C.Z. (2003) Human T-lymphotropic virus type I tax activates IκB kinase by inhibiting IKKγ-associated serine/threonine protein phosphatase 2A. J. Biol. Chem., 278, 1487-1493.
29. Furia, B. et al. (2002) Enhancement of nuclear factor-κB acetylation by coactivator p300 and HIV-1 Tat proteins. J. Biol. Chem., 277, 4973-4980.
30. Ghosh, S., May, M.J. and Kopp, E.B. (1998) NF-κB and Rel proteins: evolutionarily conserved mediators of immune responses. Annu. Rev. Immunol., 16, 225-260.
31. Gil, J., Rullas, J., Garcia, M.A., Alcami, J. and Esteban, M. (2001) The catalytic activity of dsRNA-dependent protein kinase, PKR, is required for NF-κB activation. Oncogene, 20, 385-394.
32. Gong, G., Waris, G., Tanveer, R. and Siddiqui, A. (2001) Human hepatitis C virus NS5A protein alters intracellular calcium levels, induces oxidative stress and activates STAT-3 and NF-κB. Proc. Natl Acad. Sci. USA, 98, 9599-9604.
33. Harhaj, E.W. and Sun, S.C. (1999) IKKγ serves as a docking subunit of the IκB kinase (IKK) and mediates interaction of IKK with the human T-cell leukemia virus Tax protein. J. Biol. Chem., 274, 22911-22914.
34. Harling-McNabb, L., Deliyannis, G., Jackson, D.C., Gerondakis, S., Grigoriadis, G. and Brown, L.E. (1999) Mice laking the transcription factor subunit Rel can clear an influenza infection and have functional anti-viral cytotoxic T cells but do not develop an optimal antibody response. Int. Immunol., 11, 1431-1439.
35. Hildt, E., Munz, B., Saher, G., Reifenberg, K. and Hofschneider, P.H. (2002) The PreS2 activator MHBs(t) of hepatitis B virus activates c-raf-1/Erk2 signaling in transgenic mice. EMBO J., 21, 525-535.
36. Hiscott, J., Kwon, H. and Genin, P. (2001) Hostile takeovers: viral appropriation of the NF-κB pathway. J. Clin. Invest., 107, 143-151.
37. Hoeflich, K.P., Luo, J., Rubie, E.A., Tsao, M.S., Jin, O. and Woodgett, J.R. (2000) Requirement for glycogen synthase kinase-3β in cell survival and NF-κB activation. Nature, 406, 86-90.
38. Hoffmann, A., Levchenko, A., Scott, M.L. and Baltimore, D. (2002) The IκB-NF-κB signaling module: temporal control and selective gene activation. Science, 298, 1241-1245.
39. Huen, D.S., Henderson, S.A., Croom-Carter, D. and Rowe, M. (1995) The Epstein-Barr virus latent membrane protein 1 (LMP1) mediates activation of NF-κB and cell surface phenotype via two effector regions in its carboxyl-terminal cytoplasmic domain. Oncogene, 10, 549-560.
40. Ishii, T., Kwon, H., Hiscott, J., Mosialos, G. and Koromilas, A.E. (2001) Activation of the IκBα kinase (IKK) complex by double-stranded RNA-binding defective and catalytic inactive mutants of the interferon-inducible protein kinase PKR. Oncogene, 20, 1900-1912.
41. Israel, A. (2000) The IKK complex: an integrator of all signals that activate NF-κB? Trends Cell Biol., 10, 129-133.
42. Jin, D.Y., Giordano, V., Kibler, K.V., Nakano, H. and Jeang, K.T. (1999) Role of adapter function in oncoprotein-mediated activation of NF-κB. Human T-cell leukemia virus type I Tax interacts directly with IκB kinase γ. J. Biol. Chem., 274, 17402-17405.
43. Johnson, R.A., Wang, X., Ma, X.L., Huong, S.M. and Huang, E.S. (2001) Human cytomegalovirus up-regulates the phosphatidylinositol 3-kinase (PI3-K) pathway: inhibition of PI3-K activity inhibits viral replication and virus-induced signaling. J. Virol., 75, 6022-6032.
44. Karin, M. and Ben-Neriah, Y. (2000) Phosphorylation meets ubiquitination: the control of NF-κB activity. Annu. Rev. Immunol., 18, 621-663.
45. Karin, M. and Lin, A. (2002) NF-κB at the crossroads of life and death. Nat. Immunol., 3, 221-227.
46. Karin, M., Cao, Y., Greten, F.R. and Li, Z (2002) NF-κB in cancer: from innocent bystander to major culprit. Nat. Rev. Cancer, 2, 301-310.
47. Kawanishi, M. (1997) Expression of Epstein-Barr virus latent membrane protein 1 protects Jurkat T cells from apoptosis induced by serum deprivation. Virology, 228, 244-250.
48. Kim, H., Lee, Y.H., Won, J. and Yun, Y. (2001) Through induction of juxtaposition and tyrosine kinase activity of Jak1, X-gene product of hepatitis B virus stimulates Ras and the transcriptional activation through AP-1, NF-κB and SRE enhancers. Biochem. Biophys. Res. Commun., 286, 886-894.
49. Krappmann, D., Emmerich, F., Kordes, U., Scharschmidt, E., Dorken, B. and Scheidereit, C. (1999) Molecular mechanisms of constitutive NF-κB/Rel activation in Hodgkin/Reed-Sternberg cells. Oncogene, 18, 943-953.
50. LaMonica, R. et al. (2001) VP4 differentially regulates TRAF2 signaling, disengaging JNK activation while directing NF-κB to effect rotavirus-specific cellular responses. J. Biol. Chem., 276, 19889-19896.
51. Li, Q. and Verma, I.M. (2002) NF-κB regulation in the immune system. Nat. Rev. Immunol., 2, 725-734.
52. Lokensgard, J.R., Gekker, G., Hu, S., Arthur, A.F., Chao, C.C. and Peterson, P.K. (1997) Diazepam-mediated inhibition of human immunodeficiency virus type 1 expression in human brain cells. Antimicrob. Agents Chemother., 41, 2566-2569.
53. Makris, C., Roberts, J.L. and Karin, M. (2002) The carboxyl-terminal region of IκB kinase y (IKKγ) is required for full IKK activation. Mol. Cell. Biol., 22, 6573-6581.
54. lck in HIV-tat versus TNF-induced cellular responses: effects on NF-κB, activator protein-1, c-Jun N-terminal kinase and apoptosis. J. Immunol., 164, 5156-5166.
55. Margolis, D.M., Rabson, A.B., Straus, S. and Ostrove, J.M. (1992) Transactivation of the HIV-1 LTR by HSV-1 immediate-early genes. Virology, 186, 788-791.
56. Marsters, S.A., Ayres, T.M., Skubatch, M., Gray, C.L., Rothe, M. and Ashkenazi, A. (1997) Herpesvirus entry mediator, a member of the tumor necrosis factor receptor (TNFR) family, interacts with members of the TNFR-associated factor family and activates the transcription factors NF-κB and AP-1. J. Biol. Chem., 272, 14029-14032.
57. Mogensen, T.H. and Paludan, S.R. (2001) Molecular pathways in virus-induced cytokine production. Microbiol. Mol. Biol. Rev., 65, 131-150.
58. Morimoto, R.I. and Santoro, M.G. (1998) Stress-inducible responses and heat shock proteins: new pharmacologic targets for cytoprotection. Nat. Biotechnol., 16, 833-838.
59. Nabel, G. and Baltimore, D. (1987) An inducible transcription factor activates expression of human immunodeficiency virus in T cells. Nature, 326, 711-713.
60. Oie, K.L. and Pickup, D.J. (2001) Cowpox virus and other members of the Orthopoxvirus genus interfere with the regulation of NF-κB. Virology, 288, 175-187.
61. Pahl, H.L. (1999) Activators and target genes of Rel/NF-κB transcription factors. Oncogene, 18. 6853-6866.
62. Pahl, H.L. and Baeuerle, P.A. (1997) The ER-overload response: activation of NF-κB. Trends Biochem. Sci., 22, 63-67.
63. Patel, A. et al. (1998) Herpes simplex virus type I induction of persistent NF-κB nuclear translocation increases the efficiency of virus replication. Virology, 247, 212-222.
64. Popik, W. and Pitha, P.M. (1996) Binding of human immunodeficiency virus type 1 to CD4 induces association of Lck and Raf-1 and activates Raf-1 by a Ras-independent pathway. Mol. Cell. Biol., 16, 6532-6541.
65. Portis, T., Hardling, J.C. and Ratner, L. (2001) The contribution of NF-κB activity to spontaneous proliferation and resistance to apoptosis in human T-cell leukemia virus type 1 Tax-induced tumors. Blood, 98, 1200-1208.
66. Revilla, Y. et al. (1998) Inhibition of nuclear factor κB activation by a virus-encoded IκB-like protein. J. Biol. Chem., 273, 5405-5411.
67. Rong, B.L. et al. (1992) HSV-1-inducible proteins bind to NF-κB-like sites in the HSV-1 genome. Virology, 189, 750-756.
68. Rossi, A., Elia, G. and Santoro, M.G. (1996) 2-Cyclopenten-l-one, a new inducer of heat shock protein 70 with antiviral activity. J. Biol. Chem., 271, 32192-32196.
69. 1: an effect associated with heat shock transcription factor activation. Proc. Natl Acad. Sci. USA, 94, 746-750.
70. Rossi, A., Kapahi, P., Natoli, G., Takahashi, T., Chen, Y., Karin, M. and Santoro, M.G. (2000) Anti-inflammatory cyclopentenone prostaglandins are direct inhibitors of IκB kinase. Nature, 403, 103-108.
71. Rothwarf, D.M., Zandi, E., Natoli, G. and Karin, M. (1998) IKK-γ is an essential regulatory subunit of the IκB kinase complex. Nature, 395, 297-300.
72. Roulston, A., Marcellus, R.C. and Branton, P.E. (1999) Viruses and apoptosis. Annu. Rev. Microbiol., 53, 577-628.
73. Rozera, C., Carattoli, A., De Marco, A., Amici, C., Giorgi, C. and Santoro, M.G. (1996) Inhibition of HIV-1 replication by cyclopentenone prostaglandins in acutely infected human cells: evidence for a transcriptional block. J. Clin. Invest., 97, 1795-1803.
74. Sambucetti, L.C., Cherrington, J.M., Wilkinson, G.W. and Mocarski, E.S. (1989) NF-κB activation of the cytomegalovirus enhancer is mediated by a viral transactivator and by T cell stimulation. EMBO J., 8, 4251-4258.
75. Santoro, M.G. (1997) Antiviral activity of cyclopentenone prostanoids. Trends Microbiol., 5, 276-281.
76. Santoro, M.G., Benedetto, A., Carruba, G., Garaci, E. and Jaffe, B.M. (1980) Prostaglandin A compounds as antiviral agents. Science, 209, 1032-1034.
77. Sassone-Corsi, P., Wildeman, A. and Chambon, P. (1985) A trans-acting factor is responsible for the simian virus 40 enhancer activity in vitro. Nature, 313, 458-463.
78. Schwarz, E.M. et al. (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.
79. Senftleben, U. et al. (2001) Activation by IKKα of a second, evolutionarily conserved, NF-κB signaling pathway. Science, 293, 1495-1499.
80. Sha, W.C., Liou, H.C., Tuomanen, E.I. and Baltimore, D. (1995) Targeted disruption of the p50 subunit of NF-κB leads to multifocal defects in immune responses. Cell, 80, 321-330.
81. Shoji, S. et al. (1998) An allosteric drug, o,o′-bismyristoyl thiamine disulfide, suppresses HIV-1 replication through prevention of nuclear translocation of both HIV-1 Tat and NF-κB. Biochem. Biophys. Res. Commun., 249, 745-753.
82. Silverman, N. and Maniatis, T. (2001) NF-κB signaling pathways in mammalian and insect innate immunity. Genes Dev., 15, 2321-2342.
83. Su, F. and Schneider, R.J. (1996) Hepatitis B virus HBx protein activates transcription factor NF-κB by acting on multiple cytoplasmic inhibitors of rel-related proteins. J. Virol., 70, 4558-4566.
84. Sugano,N., Chen, W., Roberts, M.L. and Cooper, N.R. (1997) Epstein-Barr virus binding to CD21 activates the initial viral promoter via NF-κB induction. J. Exp. Med., 186, 731-737.
85. Surabhi, R.M. and Gaynor, R.B. (2002) RNA interference directed against viral and cellular targets inhibits human immunodeficiency virus type 1 replication. J. Virol., 76, 12963-12973.
86. Sylla, B.S. et al. (1998) Epstein-Barr virus-transforming protein latent infection membrane protein I activates transcription factor NF-κB through a pathway that includes the NF-κB-inducing kinase and the IκB kinases IKKα and IKKβ. Proc. Natl Acad. Sci. USA, 95, 10106-10111.
87. Tai, D.I. et al. (2000a) Constitutive activation of nuclear factor κB in hepatocellular carcinoma. Cancer, 89, 2274-2281.
88. Tai, D.I. et al. (2000b) Activation of nuclear factor κB in hepatitis C virus infection: implications for pathogenesis and hepatocarcinogenesis. Hepatology, 31, 656-664.
89. Tak, P.P. and Firestein, G.S. (2001) NF-κB: a key role in inflammatory diseases. J. Clin. Invest., 107, 7-11.
90. Tanner, J.E., Alfieri, C., Chatila, T.A. and Diaz-Mitoma, F. (1996) Induction of interleukin-6 after stimulation of human B-cell CD21 by Epstein-Barr virus glycoproteins gp350 and gp220. J. Virol., 70, 570-575.
91. Tato, C.M. and Hunter, C.A. (2002) Host-pathogen interactions: subversion and utilization of the NF-κB pathway during infection. Infect. Immun., 70, 3311-3317.
92. Weil, R. et al. (1999) Direct association and nuclear import of the hepatitis B virus X protein with the NF-κB inhibitor IκBα. Mol. Cell. Biol., 19, 6345-6354.
93. Williams, B.R. (2001) Signal integration via PKR. Sci. STKE, 2001, RE2.
94. Xiao, G. et al. (2001) Retroviral oncoprotein Tax induces processing of NF-κB2/p100 in T cells: evidence for the involvement of IKKα. EMBO J., 20, 6805-6815.
95. Yin, M.J., Yamamoto, Y. and Gaynor, R.B. (1998) The anti-inflammatory agents aspirin and salicylate inhibit the activity of IκB kinase-β. Nature, 396, 77-80.
96. Yoshida, H. et al. (2001) Hepatitis C virus core protein activates nuclear factor κB-dependent signaling through tumor necrosis factor receptor-associated factor. J. Biol. Chem., 276, 16399-16405.
97. You, L.R., Chen, C.M. and Lee, Y.H. (1999) Hepatitis C virus core protein enhances NF-κB signal pathway triggering by lymphotoxin-β receptor ligand and tumor necrosis factor α. J. Virol., 73, 1672-1681.
98. Yurochko, A.D., Mayo, M.W., Poma, E.E., Baldwin, A.S., Jr and Huang, E.S. (1997) Induction of the transcription factor Sp1 during human cytomegalovirus infection mediates upregulation of the p65 and p105/p50 NF-κB promoters. J. Virol., 71, 4638-4648.
99. Zhong, H., Voll, R.E. and Ghosh, S. (1998) Phosphorylation of NF-κB p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300. Mol. Cell, 1, 661-671.