Hostile takeovers: viral appropriation of the NF-kB pathway

John Hiscott, Hakju Kwon, and Pierre Génin

Supplemental references

Briant, L., et al. 1998. The protein tyrosine kinase p56lck is required for triggering NF-kB activation upon interaction of human immunodeficiency virus type 1 envelope glycoprotein gp120 with cell surface CD4. J. Virol. 72:6207—6214.

Demarchi, F., d'Adda di Fagagna, F., Falaschi, A., and Giacca, M. 1996. Activation of transcription factor NF-kB by the Tat protein of human immunodeficiency virus type 1. J. Virol. 70:4427—4437.

Demarchi, F., Gutierrez, M.I., and Giacca, M. 1999. HIV-1 Tat protein activates transcription factor NF-kB through the cellular interferon-inducible, double stranded RNA-dependent protein kinase PKR. J. Virol. 73:7080—7086.

Montano, M.A., et al. 2000. Elevated tumor necrosis factor-alpha activation of human immunodeficiency virus type 1 subtype C in Southern Africa is associated with an NF-kappaB enhancer gain-of-function. J. Infect. Dis. 181:76—81.

Nabel, G., and Baltimore, D. 1987. An inducible transcription factor activates expression of human immunodeficiency virus in T cells. Nature. 326:711—713.

Naghavi, M.H., Salminen, M.O., Sonnerborg, A., and Vahlne, A. 1999. DNA sequence of the long terminal repeat of human immunodeficiency virus type 1 subtype A through G. AIDS Res. Hum. Retroviruses. 15:485—488.

Poli, G. 1999. Laureate ESCI award for excellence in clinical science 1999. Cytokines and the human immunodeficiency virus: from bench to bedside. European Society for Clinical Investigation. Eur. J. Clin. Invest. 29:723—732.

Westendorp, M.O., et al. 1995. HIV-1 Tat potentiates TNF-induced NF-kB activation and cytotoxicity by altering the cellular redox state. EMBO J. 14:546—554.

Wu, B.-Y., Woffendin, C., Duckett, C.S., Ohno, T., and Nabel, G.J. 1995. Regulation of human retroviral latency by the NF-kB/IkB family: inhibition of human immunodeficiency virus replication by IkB through a Rev-dependent mechanism. Proc. Natl. Acad. Sci. USA. 92:1480—1484.

Beraud, C., and Greene, W.C. 1996. Interaction of HTLV-I Tax with the human proteasome: implications for NF-kB induction. AIDS Res. Hum. Retroviruses. 13(Suppl.):S76—S84.

Hiscott, J., Petropoulos, L., and Lacoste, J. 1995. Molecular interactions between HTLV-1 Tax protein and the NF-kB /IkB transcription complex. Virology. 214:3—11.

Maggirwar, S.B., Harhaj, E., and Sun, S.C. 1995. Activation of NF-kB/Rel by Tax involves degradation of IkBa and is blocked by a proteasome inhibitor. Oncogene. 11:993—998.

McKinsey, T.A., et al. 1996. Inactivation of IkBb by the Tax protein of human T-cell leukemia virus type 1: a potential mechanism for constitutive induction of NF-kB. Mol. Cell. Biol. 16:2083—2090.

Petropoulos, L., Lin, R., and Hiscott, J. 1996. Human T cell leukemia virus type 1 Tax protein increases NF-kB dimer formation and antagonizes the inhibitory activity of the IkBa regulatory protein. Virology. 225:52—64.

Petropoulos, L., and Hiscott, J. 1998. Association between HTLV-1 Tax and IkBa is dependent on the IkBa phosphorylation state. Virology. 252:189—199.

Poiez, B.F., et al. 1980. Detection and isolation of type C retrovirus particles from fresh cultured lymphocytes of a patient with cutaneous T-cell lymphoma. Proc. Natl. Acad. Sci. USA. 77:7415—7419.

Rousset, R., Desbois, C., Bantignies, F., and Jalinot, P. 1996. Effects on NF-kB1/p105 processing of the interaction between the HTLV-1 transactivator Tax and the proteasome. Nature. 381:328—331.

Semmes, O.J., and Jeang, K.-T. 1992. Mutational analysis of human T-cell leukemia virus type I Tax: regions necessary for function determined with 47 mutant proteins. J. Virol. 66:7183—7192.

Smith, M.R., and Greene, W.C. 1990. Identification of HTLV-I tax trans-activator mutants exhibiting novel transcriptional phenotypes [errata 1991, 5:150, and 1995, 9:2324]. Genes Dev. 4:1875—1885.

Tanaka, Y., Hayashi, M., Takagi, S., and Yoshie, O. 1996. Differential transactivation of the intercellular adhesion molecule 1 gene promoter by Tax1 and Tax2 of human T-cell leukemia viruses. J. Virol. 70:8508—8517.

Tsukahara, T., et al. 1999. Induction of Bcl-x(L) expression by human T-cell leukemia virus type 1 Tax through NF-kappaB in apoptosis-resistant T-cell transfectants with Tax. J. Virol. 73:7981—7987.

Yin, M.-J., et al. 1998. HTLV-I Tax protein binds to MEKK1 to stimulate IkB kinase activity and NF-kB activation. Cell. 93:875—884.

Yoshida, M., Miyoshi, I., and Hinuma, Y. 1982. Isolation and characterization of retrovirus from cell lines of human adult T-cell leukemia and its implication in the disease. Proc. Natl. Acad. Sci. USA. 79:2031—2035.

Yoshida, M. 1995. HTLV-1 oncoprotein Tax deregulates transcription of cellular genes through multiple mechanisms. J. Cancer Res. Clin. Oncol. 121:521—528.

Chaudhary, P.M., Jasmin, A., Eby, M.T., and Hood, L. 1999. Modulation of the NF-kappa B pathway by virally encoded death effector domains-containing proteins. Oncogene. 18:5738—5746.

He, Z., Xin, B., Yang, X., Chan, C., and Cao, L. 2000. Nuclear factor-kappaB activation is involved in LMP1-mediated transformation and tumorigenesis of rat-1 fibroblasts. Cancer Res. 60:1845—1848.

Keller, S.A., Schattner, E.J., and Cesarman, E. 2000. Inhibition of NF-kappaB induces apoptosis of KSHV-infected primary effusion lymphoma cells. Blood. 96:2537—2542.

Mosialos, G. 1997. The role of Rel/NF-kappa B proteins in viral oncogenesis and the regulation of viral transcription. Semin. Cancer Biol. 8:121—129.

Rickinson, A.B., and Kieff, E. 1996. Epstein-Barr virus. In Virology. B.N. Fields, D.M. Knipe, and P.M. Howley, editors. Raven Press. New York, New York, USA. 2397—2446.

Scala, G., et al. 1993. Epstein-Barr virus nuclear antigen 2 transactivates the long terminal repeat of human immunodeficiency virus type 1. J. Virol. 67:2853—2861.

Schafer, S.L., Hiscott, J., and Pitha, P.M. 1996. Differential regulation of the HIV-1 LTR by specific NF-kappa B subunits in HSV-1-infected cells. Virology. 224:214—223.

Yao, Z., et al. 1995. Herpesvirus Saimiri encodes a new cytokine, IL-17, which binds to a novel cytokine receptor. Immunity. 3:811—821.

Zhou, Y., Chang, C.K., Quian, G., Chandran, B., and Wood, C. 1994. Trans-activation of the HIV promoter by a cDNA and its genomic clones of human herpesvirus-6. Virology. 199:311—322.

Hepatitis and NF-kB

Hildt, E., Saher, G., Bruss, V., and Hofschneider, P.H. 1996. The hepatitis B virus large surface protein (LHBs) is a transcriptional activator. Virology. 225:235—239.

Marusawa, H., Hijikata, M., Chiba, T., and Shimotohno, K. 1999. Hepatitis C virus core protein inhibits Fas- and tumor necrosis factor alpha-mediated apoptosis via NF-kappaB activation. J. Virol. 73:4713—4720.

Meyer, M., et al. 1992. Hepatitis B virus transactivator MHBst: activation of NF-kappa B, selective inhibition by antioxidants and integral membrane localization. EMBO J. 11:2991—3001.

Shrivastava, A., Manna, S.K., Ray, R., and Aggarwal, B.B. 1998. Ectopic expression of hepatitis C virus core protein differentially regulates nuclear transcription factors. J. Virol. 72:9722—9728.

Su, F., and Schneider, R.J. 1996. Hepatitis B virus HBx protein activates transcription factor NF-kappaB by acting on multiple cytoplasmic inhibitors of rel-related proteins. J. Virol. 70:4558—4566.

Zhu, N., et al. 1998. Hepatitis C virus core protein binds to the cytoplasmic domain of tumor necrosis factor (TNF) receptor 1 and enhances TNF-induced apoptosis. J. Virol. 72:3691—3697.

Cheng, G., Nazar, A.S., Shin, H.S., Vanguri, P., and Shin, M.L. 1998. IP-10 gene transcription by virus in astrocytes requires cooperation of ISRE with adjacent kappaB site but not IRF-1 or viral transcription. J. Interferon Cytokine Res. 18:987—997.

Dhib-Jalbut, S., Xia, J., Rangaviggula, H., Fang, Y.Y., and Lee, T. 1999. Failure of measles virus to activate nuclear factor-kappa B in neuronal cells: implications on the immune response to viral infections in the central nervous system. J. Immunol. 162:4024—4029.

Flory, E., et al. 2000. Influenza virus-induced NF-kappaB-dependent gene expression is mediated by overexpression of viral proteins and involves oxidative radicals and activation of IkappaB kinase. J. Biol. Chem. 275:8307—8314.

Harcourt, B.H., Rota, P.A., Hummel, K.B., Bellini, W.J., and Offermann, M.K. 1999. Induction of intercellular adhesion molecule 1 gene expression by measles virus in human umbilical vein endothelial cells. J. Med. Virol. 57:9—16.

Pahl, H.L., and Baeuerle, P.A. 1995. Expression of influenza virus hemagglutinin activates transcription factor NF-kappa-B. J. Virol. 69:1480—1484.

Pahl, H.L., Sester, M., Burgert, H.G., and Baeuerle, P.A. 1996. Activation of transcription factor NF-kappaB by the adenovirus E3/19K protein requires its ER retention. J. Cell Biol. 132:511—522.

Pak, J., and Faller, D.V. 1996. Moloney murine leukemia virus activates NF-kappa B. J. Virol. 70:4167—4172.

Powell, P.P., Dixon, L.K., and Parkhouse, R.M. 1996. An IkappaB homolog encoded by African swine fever virus provides a novel mechanism for downregulation of proinflammatory cytokine responses in host macrophages. J. Virol. 70:8527—8533.

Rager, K.J., et al. 1998. Activation of antiviral protein kinase leads to immunoglobulin E class switching in human B cells. J. Virol. 72:1171—1176.

Schwarz, E.M., et al. 1998. NF-kappaB-mediated inhibition of apoptosis is required for encephalomyocarditis virus virulence: a mechanism of resistance in p50 knockout mice. J. Virol. 72:5654—5660.

Thompson, J.E., Phillips, R.J., Erdjument-Bromage, H., Tempst, P., and Ghosh, S. 1995. IkB-b regulates the persistent response in a biphasic activation of NF-kB. Cell. 80:573—582.

Baichwal, V.R., and Baeuerle, P.A. 1997. Apoptosis: activate NF-kB or die? Curr. Biol. 7:R94—R96.

Beg, A.A., and Baltimore, D. 1996. An essential role for NF-kB in preventing TNF-a-induced cell death. Science. 274:782—784.

Chen, C., Edelstein, L.C., and Gelinas, C. 2000. The Rel/NF-kappaB family directly activates expression of the apoptosis inhibitor Bcl-x(L). Mol. Cell. Biol. 20:2687—2695.

Gil, J., Alcami, J., and Esteban, M. 1999. Induction of apoptosis by double-stranded-RNA-dependent protein kinase (PKR) involves the alpha subunit of eukaryotic translation initiation factor 2 and NF-kappaB. Mol. Cell. Biol. 19:4653—4663.

Kaufman, R.J. 1999. Double-stranded RNA-activated protein kinase mediates virus-induced apoptosis: a new role for an old actor. Proc. Natl. Acad. Sci. USA. 96:11693—11695.

Lin, K.I., DiDonato, J.A., Hoffmann, A., Hardwick, J.M., and Ratan, R.R. 1998. Suppression of steady-state, but not stimulus-induced NF-kappaB activity inhibits alphavirus-induced apoptosis. J. Cell Biol. 141:1479—1487.

Lin, K.I., Baraban, J.M., and Ratan, R.R. 1998. Inhibition versus induction of apoptosis by proteasome inhibitors depends on concentration. Cell Death Differ. 5:577—583.

Lin, B., et al. 1999. NF-kappaB functions as both a proapoptotic and antiapoptotic regulatory factor within a single cell type. Cell Death Differ. 6:570—582.

Lin, Y., Devin, A., Rodriguez, Y., and Liu, Z.G. 1999. Cleavage of the death domain kinase RIP by caspase-8 prompts TNF-induced apoptosis. Genes Dev. 13:2514—2526.

Marianneau, R., Cardona, A., Edelman, L., Deubel, V., and Despres, P. 1997. Dengue virus replication in human hepatoma cells activates NF-kappa B which in turn induces apoptotic cell death. J. Virol. 71:3244—3249.

Mayo, M.W., et al. 1997. Requirement of NF-kappaB activation to suppress p53-independent apoptosis induced by oncogenic Ras. Science. 278:1812—1815.

Moffatt, S., Yaegashi, N., Tada, K., Tanaka, N., and Sugamura, K. 1998. Human parvovirus B19 nonstructural (NS1) protein induces apoptosis in erythroid lineage cells. J. Virol. 72:3018—3028.

Shao, R., et al. 1997. Inhibition of nuclear factor-kappaB activity is involved in E1A-mediated sensitization of radiation-induced apoptosis. J. Biol. Chem. 272:32739—32742.

Van Antwerp, D.J., Martin, S.J., Kafri, T., Green, D.R., and Verma, I.M. 1996. Suppression of TNF-a-induced apoptosis by NF-kB. Science. 274:787—789.

Wang, C.Y., Mayo, M.W., and Baldwin, A.S. 1996. TNF- and cancer therapy-induced apoptosis: potentiation by inhibition of NF-kB. Science. 274:784—787.

Wang, C.Y., Guttridge, D.C., Mayo, M.W., and Baldwin, A.S., Jr. 1999. NF-kappaB induces expression of the Bcl-2 homologue A1/Bfl-1 to preferentially suppress chemotherapy-induced apoptosis. Mol. Cell. Biol. 19:5923—5929.

Wu, M., et al. 1996. Inhibition of NF-kB/Rel induces apoptosis of murine B cells. EMBO J. 15:4682—4690.