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Cell Growth and Development

Activation of NF-κB by Double-Stranded RNA (dsRNA) in the Absence of Protein Kinase R and RNase L Demonstrates the Existence of Two Separate dsRNA-Triggered Antiviral Programs

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Pages 61-72 | Received 27 Jun 2000, Accepted 22 Sep 2000, Published online: 28 Mar 2023

REFERENCES

  • Abraham, N., D. F. Stojdl, P. I. Duncan, N. Methot, T. Ishii, M. Dube, B. C. Vanderhyden, H. L. Atkins, D. A. Gray, M. W. McBurney, A. E. Koromilas, E. G. Brown, N. Sonenberg, and J. C. Bell. 1999. Characterization of transgenic mice with targeted disruption of the catalytic domain of the double-stranded RNA-dependent protein kinase, PKR. J. Biol. Chem. 274:5953–5962.
  • Balachandran, S., C. N. Kim, W. C. Yeh, T. W. Mak, K. Bhalla, and G. N. Barber. 1998. Activation of the dsRNA-dependent protein kinase, PKR, induces apoptosis through FADD-mediated death signaling. EMBO J. 17:6888–6902.
  • Balachandran, S., P. C. Roberts, T. Kipperman, K. N. Bhalla, R. W. Compans, D. R. Archer, and G. N. Barber. 2000. Alpha/beta interferons potentiate virus-induced apoptosis through activation of the FADD/caspase-8 death signaling pathway. J. Virol. 74:1513–1523.
  • Bender, K., M. Gottlicher, S. Whiteside, H. J. Rahmsdorf, and P. Herrlich. 1998. Sequential DNA damage-independent and -dependent activation of NF-kappaB by UV. EMBO J. 17:5170–5181.
  • Birnbaum, M. J., R. J. Clem, and L. K. Miller. 1994. An apoptosis-inhibiting gene from a nuclear polyhedrosis virus encoding a polypeptide with Cys/His sequence motifs. J. Virol. 68:2521–2528.
  • Bonnet, M. C., R. Weil, E. Dam, A. G. Hovanessian, and E. F. Meurs. 2000. PKR stimulates NF-κB irrespective of its kinase function by interacting with the IκB kinase complex. Mol. Cell. Biol. 20:4532–4542.
  • Castelli, J., K. A. Wood, and R. J. Youle. 1998. The 2-5A system in viral infection and apoptosis. Biomed. Pharmacother. 52:386–390.
  • Castelli, J. C., B. A. Hassel, A. Maran, J. Paranjape, J. A. Hewitt, X. L. Li, Y. T. Hsu, R. H. Silverman, and R. J. Youle. 1998. The role of 2′-5′ oligoadenylate-activated ribonuclease L in apoptosis. Cell Death Differ. 5:313–320.
  • Castelli, J. C., B. A. Hassel, K. A. Wood, X. L. Li, K. Amemiya, M. C. Dalakas, P. F. Torrence, and R. J. Youle. 1997. A study of the interferon antiviral mechanism: apoptosis activation by the 2-5A system. J. Exp. Med. 186:967–972.
  • Chen, C., L. C. Edelstein, and C. Gelinas. 2000. The Rel/NF-κB family directly activates expression of the apoptosis inhibitor Bcl-x(L). Mol. Cell. Biol. 20:2687–2695.
  • Chu, W. M., D. Ostertag, Z. W. Li, L. Chang, Y. Chen, Y. Hu, B. Williams, J. Perrault, and M. Karin. 1999. JNK2 and IKKbeta are required for activating the innate response to viral infection. Immunity 11:721–731.
  • Chu, Z. L., T. A. McKinsey, L. Liu, J. J. Gentry, M. H. Malim, and D. W. Ballard. 1997. Suppression of tumor necrosis factor-induced cell death by inhibitor of apoptosis c-IAP2 is under NF-kappaB control. Proc. Natl. Acad. Sci. USA 94:10057–10062.
  • Diaz-Guerra, M., C. Rivas, and M. Esteban. 1997. Activation of the IFN-inducible enzyme RNase L causes apoptosis of animal cells. Virology 236:354–363.
  • DiDonato, J. A., M. Hayakawa, D. M. Rothwarf, E. Zandi, and M. Karin. 1997. A cytokine-responsive IkappaB kinase that activates the transcription factor NF-kappaB. Nature 388:548–554.
  • Donze, O., J. Dostie, and N. Sonenberg. 1999. Regulatable expression of the interferon-induced double-stranded RNA dependent protein kinase PKR induces apoptosis and fas receptor expression. Virology 256:322–329.
  • Foster, G. R., and N. B. Finter. 1998. Are all type I human interferons equivalent?. J. Viral Hepatol. 5:143–152.
  • Gagliardini, V., P. A. Fernandez, R. K. Lee, H. C. Drexler, R. J. Rotello, M. C. Fishman, and J. Yuan. 1994. Prevention of vertebrate neuronal death by the crmA gene. Science 263:826–828.
  • Garoufalis, E., I. Kwan, R. Lin, A. Mustafa, N. Pepin, A. Roulston, J. Lacoste, and J. Hiscott. 1994. Viral induction of the human beta interferon promoter: modulation of transcription by NF-kappa B/rel proteins and interferon regulatory factors. J. Virol. 68:4707–4715.
  • Gil, J., J. Alcami, and M. Esteban. 2000. Activation of NF-kappa B by the dsRNA-dependent protein kinase, PKR involves the I kappa B kinase complex. Oncogene 19:1369–1378.
  • Gil, J., J. Alcami, and M. Esteban. 1999. Induction of apoptosis by double-stranded-RNA-dependent protein kinase (PKR) involves the alpha subunit of eukaryotic translation initiation factor 2 and NF-κB. Mol. Cell. Biol. 19:4653–4663.
  • Gilmore, T. D.. 1999. The Rel/NF-kappaB signal transduction pathway: introduction. Oncogene 18:6842–6844.
  • Gross, M., W. M. Knish, and A. Kwan. 1981. Rabbit reticulocyte double-stranded RNA-activated protein kinase and the hemin-controlled translational repressor phosphorylate the same Mr 1500 peptide of eukaryotic initiation factor 2 alpha. FEBS Lett. 125:223–226.
  • Hosenpud, J. D., R. J. Novick, L. E. Bennett, B. M. Keck, B. Fiol, and O. P. Daily. 1996. The Registry of the International Society for Heart and Lung Transplantation: thirteenth official report—1996. J. Heart Lung Transplant. 15:655–674.
  • Hovanessian, A. G.. 1991. Interferon-induced and double-stranded RNA-activated enzymes: a specific protein kinase and 2′,5′-oligoadenylate synthetases. J. Interferon Res. 11:199–205.
  • Hu, Y., V. Baud, M. Delhase, P. Zhang, T. Deerinck, M. Ellisman, R. Johnson, and M. Karin. 1999. Abnormal morphogenesis but intact IKK activation in mice lacking the IKKalpha subunit of IkappaB kinase. Science 284:316–320.
  • Iordanov, M. S., J. M. Paranjape, A. Zhou, J. Wong, B. R. Williams, E. F. Meurs, R. H. Silverman, and B. E. Magun. 2000. Activation of p38 mitogen-activated protein kinase and c-Jun NH2-terminal kinase by double-stranded RNA and encephalomyocarditis virus: involvement of RNase L, protein kinase R, and alternative pathways. Mol. Cell. Biol. 20:617–627.
  • Iordanov, M. S., O. P. Ryabinina, J. Wong, T. H. Dinh, D. L. Newton, S. M. Rybak, and B. E. Magun. 2000. Molecular determinants of apoptosis induced by the cytotoxic ribonuclease onconase: evidence for cytotoxic mechanisms different from inhibition of protein synthesis. Cancer Res. 60:1983–1994.
  • Jagus, R., B. Joshi, and G. N. Barber. 1999. PKR, apoptosis and cancer. Int. J. Biochem. Cell Biol. 31:123–138.
  • Jeffrey, I. W., S. Kadereit, E. F. Meurs, T. Metzger, M. Bachmann, M. Schwemmle, A. G. Hovanessian, and M. J. Clemens. 1995. Nuclear localization of the interferon-inducible protein kinase PKR in human cells and transfected mouse cells. Exp. Cell Res. 218:17–27.
  • Karin, M.. 1999. The beginning of the end: IkappaB kinase (IKK) and NF-kappaB activation. J. Biol. Chem. 274:27339–27342.
  • Karin, M.. 1999. How NF-kappaB is activated: the role of the IkappaB kinase (IKK) complex. Oncogene 18:6867–6874.
  • LaCasse, E. C., S. Baird, R. G. Korneluk, and A. E. MacKenzie. 1998. The inhibitors of apoptosis (IAPs) and their emerging role in cancer. Oncogene 17:3247–3259.
  • Lee, H. H., H. Dadgostar, Q. Cheng, J. Shu, and G. Cheng. 1999. NF-kappaB-mediated up-regulation of Bcl-x and Bfl-1/A1 is required for CD40 survival signaling in B lymphocytes. Proc. Natl. Acad. Sci. USA 96:9136–9141.
  • Lee, S. B., D. Rodriguez, J. R. Rodriguez, and M. Esteban. 1997. The apoptosis pathway triggered by the interferon-induced protein kinase PKR requires the third basic domain, initiates upstream of Bcl-2, and involves ICE-like proteases. Virology 231:81–88.
  • Levin, D. H., R. Petryshyn, and I. M. London. 1981. Characterization of purified double-stranded RNA-activated eIF-2 alpha kinase from rabbit reticulocytes. J. Biol. Chem. 256:7638–7641.
  • Li, Z. W., W. Chu, Y. Hu, M. Delhase, T. Deerinck, M. Ellisman, R. Johnson, and M. Karin. 1999. The IKKbeta subunit of IkappaB kinase (IKK) is essential for nuclear factor kappaB activation and prevention of apoptosis. J. Exp. Med. 189:1839–1845.
  • Maniatis, T., J. V. Falvo, T. H. Kim, T. K. Kim, C. H. Lin, B. S. Parekh, and M. G. Wathelet. 1998. Structure and function of the interferon-beta enhanceosome. Cold Spring Harbor Symp. Quant. Biol. 63:609–620.
  • Mercurio, F., H. Zhu, B. W. Murray, A. Shevchenko, B. L. Bennett, J. Li, D. B. Young, M. Barbosa, M. Mann, A. Manning, and A. Rao. 1997. IKK-1 and IKK-2: cytokine-activated IkappaB kinases essential for NF-kappaB activation. Science 278:860–866.
  • Meurs, E., K. Chong, J. Galabru, N. S. Thomas, I. M. Kerr, B. R. Williams, and A. G. Hovanessian. 1990. Molecular cloning and characterization of the human double-stranded RNA-activated protein kinase induced by interferon. Cell 62:379–390.
  • Muller, U., U. Steinhoff, L. F. Reis, S. Hemmi, J. Pavlovic, R. M. Zinkernagel, and M. Aguet. 1994. Functional role of type I and type II interferons in antiviral defense. Science 264:1918–1921.
  • Nilsen, T. W., D. L. Wood, and C. Baglioni. 1981. 2′,5′-Oligo(A)-activated endoribonuclease. Tissue distribution and characterization with a binding assay. J. Biol. Chem. 256:10751–10754.
  • Pahl, H. L.. 1999. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 18:6853–6866.
  • Player, M. R., and P. F. Torrence. 1998. The 2-5A system: modulation of viral and cellular processes through acceleration of RNA degradation. Pharmacol. Ther. 78:55–113.
  • Rabizadeh, S., D. J. LaCount, P. D. Friesen, and D. E. Bredesen. 1993. Expression of the baculovirus p35 gene inhibits mammalian neural cell death. J. Neurochem. 61:2318–2321.
  • Rao, L., M. Debbas, P. Sabbatini, D. Hockenbery, S. Korsmeyer, and E. White. 1992. The adenovirus E1A proteins induce apoptosis, which is inhibited by the E1B 19-kDa and Bcl-2 proteins. Proc. Natl. Acad. Sci. USA 89:7742–7746.
  • Rudolph, D., W. C. Yeh, A. Wakeham, B. Rudolph, D. Nallainathan, J. Potter, A. J. Elia, and T. W. Mak. 2000. Severe liver degeneration and lack of NF-kappaB activation in NEMO/IKKgamma-deficient mice. Genes Dev. 14:854–862.
  • Rueckert, R.. 1996. Picornaviridae: the viruses and their replication. Virology, 3rd ed. B. Fields, D. Knipe, and P. Howley. 477–522. Lippincott-Raven, Philadelphia, Pa
  • 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.
  • Sha, W. C., H. C. Liou, E. I. Tuomanen, and D. Baltimore. 1995. Targeted disruption of the p50 subunit of NF-kappa B leads to multifocal defects in immune responses. Cell 80:321–330.
  • Siekierka, J., V. Manne, and S. Ochoa. 1984. Mechanism of translational control by partial phosphorylation of the alpha subunit of eukaryotic initiation factor 2. Proc. Natl. Acad. Sci. USA 81:352–356.
  • Silverman, R. H., P. J. Cayley, D. H. Wreschner, M. Knight, C. S. Gilbert, R. E. Brown, and I. M. Kerr. 1981. 2-5A(pppA2′p5′A2′p5′A) in interferon-treated encephalomyocarditis virus-infected mouse L-cells. Tex. Rep. Biol. Med. 41:479–486.
  • Silverman, R. H., J. J. Skehel, T. C. James, D. H. Wreschner, and I. M. Kerr. 1983. rRNA cleavage as an index of ppp(A2′p)nA activity in interferon-treated encephalomyocarditis virus-infected cells. J. Virol. 46:1051–1055.
  • Srivastava, S. P., K. U. Kumar, and R. J. Kaufman. 1998. Phosphorylation of eukaryotic translation initiation factor 2 mediates apoptosis in response to activation of the double-stranded RNA-dependent protein kinase. J. Biol. Chem. 273:2416–2423.
  • Stark, G. R., I. M. Kerr, B. R. Williams, R. H. Silverman, and R. D. Schreiber. 1998. How cells respond to interferons. Annu. Rev. Biochem. 67:227–264.
  • Stehlik, C., R. de Martin, I. Kumabashiri, J. A. Schmid, B. R. Binder, and J. Lipp. 1998. Nuclear factor (NF)-kappaB-regulated X-chromosome-linked iap gene expression protects endothelial cells from tumor necrosis factor alpha-induced apoptosis. J. Exp. Med. 188:211–216.
  • Stein, B., H. J. Rahmsdorf, A. Steffen, M. Litfin, and P. Herrlich. 1989. UV-induced DNA damage is an intermediate step in UV-induced expression of human immunodeficiency virus type 1, collagenase, c-fos, and metallothionein. Mol. Cell. Biol. 9:5169–5181.
  • Stroka, D. M., A. Z. Badrichani, F. H. Bach, and C. Ferran. 1999. Overexpression of A1, an NF-kappaB-inducible anti-apoptotic bcl gene, inhibits endothelial cell activation. Blood 93:3803–3810.
  • Sugimoto, A., P. D. Friesen, and J. H. Rothman. 1994. Baculovirus p35 prevents developmentally programmed cell death and rescues a ced-9 mutant in the nematode Caenorhabditis elegans. EMBO J. 13:2023–2028.
  • Takeda, K., O. Takeuchi, T. Tsujimura, S. Itami, O. Adachi, T. Kawai, H. Sanjo, K. Yoshikawa, N. Terada, and S. Akira. 1999. Limb and skin abnormalities in mice lacking IKKalpha. Science 284:313–316.
  • Tam, P. E., and R. P. Messner. 1999. Molecular mechanisms of coxsackievirus persistence in chronic inflammatory myopathy: viral RNA persists through formation of a double-stranded complex without associated genomic mutations or evolution. J. Virol. 73:10113–10121.
  • Tanaka, M., M. E. Fuentes, K. Yamaguchi, M. H. Durnin, S. A. Dalrymple, K. L. Hardy, and D. V. Goeddel. 1999. Embryonic lethality, liver degeneration, and impaired NF-kappa B activation in IKK-beta-deficient mice. Immunity 10:421–429.
  • Teodoro, J. G., and P. E. Branton. 1997. Regulation of apoptosis by viral gene products. J. Virol. 71:1739–1746.
  • Tewari, M., and V. M. Dixit. 1995. Fas- and tumor necrosis factor-induced apoptosis is inhibited by the poxvirus crmA gene product. J. Biol. Chem. 270:3255–3260.
  • Thanos, D., and T. Maniatis. 1992. The high mobility group protein HMG I(Y) is required for NF-kappa B-dependent virus induction of the human IFN-beta gene. Cell 71:777–789.
  • Thanos, D., and T. Maniatis. 1995. Identification of the rel family members required for virus induction of the human beta interferon gene. Mol. Cell. Biol. 15:152–164.
  • Thome, M., P. Schneider, K. Hofmann, H. Fickenscher, E. Meinl, F. Neipel, C. Mattmann, K. Burns, J. L. Bodmer, M. Schroter, C. Scaffidi, P. H. Krammer, M. E. Peter, and J. Tschopp. 1997. Viral FLICE-inhibitory proteins (FLIPs) prevent apoptosis induced by death receptors. Nature 386:517–521.
  • Traenckner, E. B., H. L. Pahl, T. Henkel, K. N. Schmidt, S. Wilk, and P. A. Baeuerle. 1995. 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. 14:2876–2883.
  • Tsukahara, T., M. Kannagi, T. Ohashi, H. Kato, M. Arai, G. Nunez, Y. Iwanaga, N. Yamamoto, K. Ohtani, M. Nakamura, and M. Fujii. 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.
  • Wang, C. Y., D. C. Guttridge, M. W. Mayo, and A. S. Baldwin 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.
  • Wang, C. Y., M. W. Mayo, R. G. Korneluk, D. V. Goeddel, and A. S. Baldwin Jr.. 1998. NF-kappaB antiapoptosis: induction of TRAF1 and TRAF2 and c-IAP1 and c-IAP2 to suppress caspase-8 activation. Science 281:1680–1683.
  • Wessely, R., K. Klingel, L. F. Santana, N. Dalton, M. Hongo, W. Jonathan Lederer, R. Kandolf, and K. U. Knowlton. 1998. Transgenic expression of replication-restricted enteroviral genomes in heart muscle induces defective excitation-contraction coupling and dilated cardiomyopathy. J. Clin. Investig. 102:1444–1453.
  • White, E., P. Sabbatini, M. Debbas, W. S. Wold, D. I. Kusher, and L. R. Gooding. 1992. The 19-kilodalton adenovirus E1B transforming protein inhibits programmed cell death and prevents cytolysis by tumor necrosis factor alpha. Mol. Cell. Biol. 12:2570–2580.
  • Williams, B. R.. 1999. PKR: a sentinel kinase for cellular stress. Oncogene 18:6112–6120.
  • Wreschner, D. H., T. C. James, R. H. Silverman, and I. M. Kerr. 1981. Ribosomal RNA cleavage, nuclease activation and 2-5A(ppp(A2′p)nA) in interferon-treated cells. Nucleic Acids Res. 9:1571–1581.
  • Yamaoka, S., G. Courtois, C. Bessia, S. T. Whiteside, R. Weil, F. Agou, H. E. Kirk, R. J. Kay, and A. Israel. 1998. Complementation cloning of NEMO, a component of the IkappaB kinase complex essential for NF-kappaB activation. Cell 93:1231–1240.
  • Yang, Y. L., L. F. Reis, J. Pavlovic, A. Aguzzi, R. Schafer, A. Kumar, B. R. Williams, M. Aguet, and C. Weissmann. 1995. Deficient signaling in mice devoid of double-stranded RNA-dependent protein kinase. EMBO J. 14:6095–6106.
  • 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 96:11860–11860.
  • Yeung, M. C., J. Liu, and A. S. Lau. 1996. An essential role for the interferon-inducible, double-stranded RNA-activated protein kinase PKR in the tumor necrosis factor-induced apoptosis in U937 cells. Proc. Natl. Acad. Sci. USA 93:12451–12455.
  • Zamanian-Daryoush, M., T. H. Mogensen, J. A. DiDonato, and B. R. Williams. 2000. NF-κB activation by double-stranded-RNA-activated protein kinase (PKR) is mediated through NF-κB-inducing kinase and IκB kinase. Mol. Cell. Biol. 20:1278–1290.
  • Zandi, E., and M. Karin. 1999. Bridging the gap: composition, regulation, and physiological function of the IκB kinase complex. Mol. Cell. Biol. 19:4547–4551.
  • Zandi, E., D. M. Rothwarf, M. Delhase, M. Hayakawa, and M. Karin. 1997. The IkappaB kinase complex (IKK) contains two kinase subunits, IKKalpha and IKKbeta, necessary for IkappaB phosphorylation and NF-kappaB activation. Cell 91:243–252.
  • Zhou, A., B. A. Hassel, and R. H. Silverman. 1993. Expression cloning of 2-5A-dependent RNAase: a uniquely regulated mediator of interferon action. Cell 72:753–765.
  • Zhou, A., J. Paranjape, T. L. Brown, H. Nie, S. Naik, B. Dong, A. Chang, B. Trapp, R. Fairchild, C. Colmenares, and R. H. Silverman. 1997. Interferon action and apoptosis are defective in mice devoid of 2′,5′-oligoadenylate-dependent RNase L. EMBO J. 16:6355–6363.
  • Zhou, A., J. M. Paranjape, S. D. Der, B. R. Williams, and R. H. Silverman. 1999. Interferon action in triply deficient mice reveals the existence of alternative antiviral pathways. Virology 258:435–440.
  • Zhou, A., J. M. Paranjape, B. A. Hassel, H. Nie, S. Shah, B. Galinski, and R. H. Silverman. 1998. Impact of RNase L overexpression on viral and cellular growth and death. J. Interferon Cytokine Res. 18:953–961.
  • Zong, W. X., L. C. Edelstein, C. Chen, J. Bash, and C. Gelinas. 1999. The prosurvival Bcl-2 homolog Bfl-1/A1 is a direct transcriptional target of NF-kappaB that blocks TNFalpha-induced apoptosis. Genes Dev. 13:382–387.

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