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Cell Growth and Development

Defects in Translational Regulation Mediated by the α Subunit of Eukaryotic Initiation Factor 2 Inhibit Antiviral Activity and Facilitate the Malignant Transformation of Human Fibroblasts

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Pages 2025-2040 | Received 19 Aug 2003, Accepted 04 Dec 2003, Published online: 27 Mar 2023

REFERENCES

  • Anand, N., Murthy S., Amann G., Wernick M., Porter L. A., Cukier I. H., Collins H. C., Gray J. W., Diebold J., Demetrick D. J., and Lee J. M.. 2002. Protein elongation factor EEF1A2 is a putative oncogene in ovarian cancer. Nat. Genet. 31:301–305.
  • Anthony, T. G., Fabian J. R., Kimball S. R., and Jefferson L. S.. 2000. Identification of domains within the epsilon-subunit of the translation initiation factor eIF2B that are necessary for guanine nucleotide exchange activity and eIF2B holoprotein formation. Biochim. Biophys. Acta 1492:56–62.
  • Asano, K., and Hinnebusch A. G.. 2001. Protein interactions important in eukaryotic translation initiation. Methods Mol. Biol. 177:179–198.
  • Asano, K., Shalev A., Phan L., Nielsen K., Clayton J., Valasek L., Donahue T. F., and Hinnebusch A. G.. 2001. Multiple roles for the C-terminal domain of eIF5 in translation initiation complex assembly and GTPase activation. EMBO J. 20:2326–2337.
  • Balachandran, S., Kim C. N., Yeh W. C., Mak T. W., Bhalla K., and Barber G. N.. 1998. Activation of the dsRNA-dependent protein kinase, PKR, induces apoptosis through FADD-mediated death signaling. EMBO J. 17:6888–6902.
  • Balachandran, S., Roberts P. C., Brown L. E., Truong H., Pattnaik A. K., Archer D. R., and Barber G. N.. 2000. Essential role for the dsRNA-dependent protein kinase PKR in innate immunity to viral infection. Immunity 13:129–141.
  • Barber, G. N., Tomita J., Hovanessian A. G., Meurs E., and Katze M. G.. 1991. Functional expression and characterization of the interferon-induced double-stranded RNA activated P68 protein kinase from Escherichia coli. Biochemistry 30:10356–10361.
  • Boileau, G., Butler P., Hershey J. W., and Traut R. R.. 1983. Direct cross-links between initiation factors 1, 2, and 3 and ribosomal proteins promoted by 2-iminothiolane. Biochemistry 22:3162–3170.
  • Brewer, J. W., and Diehl J. A.. 2000. PERK mediates cell-cycle exit during the mammalian unfolded protein response. Proc. Natl. Acad. Sci. USA 97:12625–12630.
  • Brewer, J. W., Hendershot L. M., Sherr C. J., and Diehl J. A.. 1999. Mammalian unfolded protein response inhibits cyclin D1 translation and cell-cycle progression. Proc. Natl. Acad. Sci. USA 96:8505–8510.
  • Chen, J. J., Crosby J. S., and London I. M.. 1994. Regulation of heme-regulated eIF2 alpha kinase and its expression in erythroid cells. Biochimie 76:761–769.
  • Chen, J. J., Throop M. S., Gehrke L., Kuo I., Pal J. K., Brodsky M., and London I. M.. 1991. Cloning of the cDNA of the heme-regulated eukaryotic initiation factor 2 alpha (eIF2α) kinase of rabbit reticulocytes: homology to yeast GCN2 protein kinase and human double-stranded-RNA-dependent eIF2α kinase. Proc. Natl. Acad. Sci. USA 88:7729–7733.
  • Clemens, M. J. 2001. Initiation factor eIF2α phosphorylation in stress responses and apoptosis. Prog. Mol. Subcell. Biol. 27:57–89.
  • Clemens, M. J., Safer B., Merrick W. C., Anderson W. F., and London I. M.. 1975. Inhibition of protein synthesis in rabbit reticulocyte lysates by double-stranded RNA and oxidized glutathione: indirect mode of action on polypeptide chain initiation. Proc. Natl. Acad. Sci. USA 72:1286–1290.
  • De Benedetti, A., Joshi-Barve S., Rinker-Schaeffer C., and Rhoads R. E.. 1991. Expression of antisense RNA against initiation factor eIF-4E mRNA in HeLa cells results in lengthened cell division times, diminished translation rates, and reduced levels of both eIF-4E and the p220 component of eIF-4F. Mol. Cell. Biol. 11:5435–5445.
  • DeGracia, D. J., Sullivan J. M., Neumar R. W., Alousi S. S., Hikade K. R., Pittman J. E., White B. C., Rafols J. A., and Krause G. S.. 1997. Effect of brain ischemia and reperfusion on the localization of phosphorylated eukaryotic initiation factor 2 alpha. J. Cereb. Blood Flow Metab. 17:1291–1302.
  • Dever, T. E. 1997. Using GCN4 as a reporter of eIF2 alpha phosphorylation and translational regulation in yeast. Methods (Duluth) 11:403–417.
  • Dever, T. E. 1999. Translation initiation: adept at adapting. Trends Biochem. Sci. 24:398–403.
  • Dever, T. E. 2002. Gene-specific regulation by general translation factors. Cell 108:545–556.
  • Dever, T. E., Chen J. J., Barber G. N., Cigan A. M., Feng L., Donahue T. F., London I. M., Katze M. G., and Hinnebusch A. G.. 1993. Mammalian eukaryotic initiation factor 2 alpha kinases functionally substitute for GCN2 protein kinase in the GCN4 translational control mechanism of yeast. Proc. Natl. Acad. Sci. USA 90:4616–4620.
  • Dever, T. E., Feng L., Wek R. C., Cigan A. M., Donahue T. F., and Hinnebusch A. G.. 1992. Phosphorylation of initiation factor 2 alpha by protein kinase GCN2 mediates gene-specific translational control of GCN4 in yeast. Cell 68:585–596.
  • Donze, O., Dostie J., and Sonenberg N.. 1999. Regulatable expression of the interferon-induced double-stranded RNA dependent protein kinase PKR induces apoptosis and fas receptor expression. Virology 256:322–329.
  • Donze, O., Jagus R., Koromilas A. E., Hershey J. W., and Sonenberg N.. 1995. Abrogation of translation initiation factor eIF2 phosphorylation causes malignant transformation of NIH 3T3 cells. EMBO J. 14:3828–3834.
  • Fernandez, M., Porosnicu M., Markovic D., and Barber G. N.. 2002. Genetically engineered vesicular stomatitis virus in gene therapy: application for treatment of malignant disease. J. Virol. 76:895–904.
  • Filipowicz, W., Furuichi Y., Sierra J. M., Muthukrishnan S., Shatkin A. J., and Ochoa S.. 1976. A protein binding the methylated 5′-terminal sequence, m7GpppN, of eukaryotic messenger RNA. Proc. Natl. Acad. Sci. USA 73:1559–1563.
  • Gerlitz, G., Jagus R., and Elroy-Stein O.. 2002. Phosphorylation of initiation factor-2 alpha is required for activation of internal translation initiation during cell differentiation. Eur. J. Biochem. 269:2810–2819.
  • Gil, J., Alcami J., and Esteban M.. 1999. Induction of apoptosis by double-stranded-RNA-dependent protein kinase (PKR) involves the α subunit of eukaryotic translation initiation factor 2 and NF-κB. Mol. Cell. Biol. 19:4653–4663.
  • Gossen, M., and Bujard H.. 1995. Efficacy of tetracycline-controlled gene expression is influenced by cell type. BioTechniques 19:213–216.
  • Hahn, W. C., Counter C. M., Lundberg A. S., Beijersbergen R. L., Brooks M. W., and Weinberg R. A.. 1999. Creation of human tumour cells with defined genetic elements. Nature 400:464–468.
  • Han, A. P., Yu C., Lu L., Fujiwara Y., Browne C., Chin G., Fleming M., Leboulch P., Orkin S. H., and Chen J. J.. 2001. Heme-regulated eIF2α kinase (HRI) is required for translational regulation and survival of erythroid precursors in iron deficiency. EMBO J. 20:6909–6918.
  • Harding, H. P., Novoa I., Zhang Y., Zeng H., Wek R., Schapira M., and Ron D.. 2000. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6:1099–1108.
  • Harding, H. P., Zhang Y., Bertolotti A., Zeng H., and Ron D.. 2000. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 5:897–904.
  • Harding, H. P., Zhang Y., and Ron D.. 1999. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397:271–274. (Erratum, 398:90.)
  • Hershey, J. W. 1989. Protein phosphorylation controls translation rates. J. Biol. Chem. 264:20823–20826.
  • Hinnebusch, A. G. 1994. The eIF2 alpha kinases: regulators of protein synthesis in starvation and stress. Semin. Cell Biol. 5:417–426.
  • Imoto, M., Doki Y., Jiang W., Han E. K., and Weinstein I. B.. 1997. Effects of cyclin D1 overexpression on G1 progression-related events. Exp. Cell Res. 236:173–180.
  • Kimball, S. R. 1999. Eukaryotic initiation factor eIF2. Int. J. Biochem. Cell Biol. 31:25–29.
  • Kimball, S. R. 2001. Regulation of translation initiation by amino acids in eukaryotic cells. Prog. Mol. Subcell. Biol. 26:155–184.
  • Kimball, S. R., Fabian J. R., Pavitt G. D., Hinnebusch A. G., and Jefferson L. S.. 1998. Regulation of guanine nucleotide exchange through phosphorylation of eukaryotic initiation factor eIF2α. Role of the alpha- and delta-subunits of eiF2b. J. Biol. Chem. 273:12841–12845.
  • Kimball, S. R., Heinzinger N. K., Horetsky R. L., and Jefferson L. S.. 1998b. Identification of interprotein interactions between the subunits of eukaryotic initiation factors eIF2 and eIF2B. J. Biol. Chem. 273:3039–3044.
  • Kimball, S. R., Horetsky R. L., Ron D., Jefferson L. S., and Harding H. P.. 2003. Mammalian stress granules represent sites of accumulation of stalled translation initiation complexes. Am. J. Physiol. Cell Physiol. 284:C273–C284.
  • Knappik, A., and Pluckthun A.. 1994. An improved affinity tag based on the FLAG peptide for the detection and purification of recombinant antibody fragments. BioTechniques 17:754–761.
  • Kostura, M., and Mathews M. B.. 1989. Purification and activation of the double-stranded RNA-dependent eIF2 kinase DAI. Mol. Cell. Biol. 9:1576–1586.
  • Kozak, M. 1987. At least six nucleotides preceding the AUG initiator codon enhance translation in mammalian cells. J. Mol. Biol. 196:947–950.
  • Kumar, A., Haque J., Lacoste J., Hiscott J., and Williams B. R.. 1994. Double-stranded RNA-dependent protein kinase activates transcription factor NF-κB by phosphorylating IκB. Proc. Natl. Acad. Sci. USA 91:6288–6292.
  • Lazaris-Karatzas, A., Smith M. R., Frederickson R. M., Jaramillo M. L., Liu Y. L., Kung H. F., and Sonenberg N.. 1992. Ras mediates translation initiation factor 4E-induced malignant transformation. Genes Dev. 6:1631–1642.
  • Lazaris-Karatzas, A., and Sonenberg N.. 1992. The mRNA 5′ cap-binding protein, eIF-4E, cooperates with v-myc or E1A in the transformation of primary rodent fibroblasts. Mol. Cell. Biol. 12:1234–1238.
  • Manchester, K. L. 1987. eIF2B and the exchange of guanine nucleotides bound to eIF2. Int. J. Biochem. 19:245–251.
  • Mayeur, G. L., and Hershey J. W.. 2002. Malignant transformation by the eukaryotic translation initiation factor 3 subunit p48 (eIF3e). FEBS Lett. 514:49–54.
  • Merrick, W. C. 1990. Overview: mechanism of translation initiation in eukaryotes. Enzyme 44:7–16.
  • Merrick, W. C. 1992. Mechanism and regulation of eukaryotic protein synthesis. Microbiol. Rev. 56:291–315.
  • Meurs, E. F., Watanabe Y., Kadereit S., Barber G. N., Katze M. G., Chong K., Williams B. R., and Hovanessian A. G.. 1992. Constitutive expression of human double-stranded RNA-activated p68 kinase in murine cells mediates phosphorylation of eukaryotic initiation factor 2 and partial resistance to encephalomyocarditis virus growth. J. Virol. 66:5804–5814.
  • Muthukrishnan, S., Both G. W., Furuichi Y., and Shatkin A. J.. 1975. 5′-Terminal 7-methylguanosine in eukaryotic mRNA is required for translation. Nature 255:33–37.
  • Nika, J., Rippel S., and Hannig E. M.. 2001. Biochemical analysis of the eIF2β gamma complex reveals a structural function for eIF2α in catalyzed nucleotide exchange. J. Biol. Chem. 276:1051–1056.
  • Novoa, I., Zeng H., Harding H. P., and Ron D.. 2001. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2α. J. Cell Biol. 153:1011–1022.
  • Pestova, T. V., Kolupaeva V. G., Lomakin I. B., Pilipenko E. V., Shatsky I. N., Agol V. I., and Hellen C. U.. 2001. Molecular mechanisms of translation initiation in eukaryotes. Proc. Natl. Acad. Sci. USA 98:7029–7036.
  • Petryshyn, R., Rosa F., Fagard R., Levin D., and London I. M.. 1984. Control of protein synthesis in human reticulocytes by heme-regulated and double-stranded RNA dependent eIF2 alpha kinases. Biochem. Biophys. Res. Commun. 119:891–899.
  • Polunovsky, V. A., Gingras A. C., Sonenberg N., Peterson M., Tan A., Rubins J. B., Manivel J. C., and Bitterman P. B.. 2000. Translational control of the antiapoptotic function of Ras. J. Biol. Chem. 275:24776–24780.
  • Proud, C. G. 2001. Regulation of eukaryotic initiation factor eIF2B. Prog. Mol. Subcell. Biol. 26:95–114.
  • Quelle, D. E., Ashmun R. A., Shurtleff S. A., Kato J. Y., Bar-Sagi D., Roussel M. F., and Sherr C. J.. 1993. Overexpression of mouse D-type cyclins accelerates G1 phase in rodent fibroblasts. Genes Dev. 7:1559–1571.
  • Ramaiah, K. V. A., Davies M. V., Chen J.-J., and Kaufman R. J.. 1994. Expression of mutant eukaryotic initiation factor 2 α subunit (eIF2α) reduces inhibition of guanine nucleotide exchange activity of eIF2B mediated by eIF2α phosphorylation. Mol. Cell. Biol. 14:4546–4553.
  • Roy, A. L., Chakrabarti D., and Gupta N. K.. 1987. Protein synthesis in rabbit reticulocytes: Mg2+-inhibition of ternary complex (Met-tRNA(f) · eIF2 · GTP) formation by reticulocyte eIF2. Biochem. Biophys. Res. Commun. 146:114–120.
  • Samuel, C. E. 1993. The eIF2 alpha protein kinases, regulators of translation in eukaryotes from yeasts to humans. J. Biol. Chem. 268:7603–7606.
  • Saunders, L. R., Perkins D. J., Balachandran S., Michaels R., Ford R., Mayeda A., and Barber G. N.. 2001. Characterization of two evolutionarily conserved, alternatively spliced nuclear phosphoproteins, NFAR-1 and -2, that function in mRNA processing and interact with the double-stranded RNA-dependent protein kinase, PKR. J. Biol. Chem. 276:32300–32312.
  • Scheuner, D., Song B., McEwen E., Liu C., Laybutt R., Gillespie P., Saunders T., Bonner-Weir S., and Kaufman R. J.. 2001. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 7:1165–1176.
  • Sherr, C. J. 2001. The INK4a/ARF network in tumour suppression. Nat. Rev. Mol. Cell Biol. 2:731–737.
  • Shi, Y., Vattem K. M., Sood R., An J., Liang J., Stramm L., and Wek R. C.. 1998. Identification and characterization of pancreatic eukaryotic initiation factor 2 α-subunit kinase, PEK, involved in translational control. Mol. Cell. Biol. 18:7499–7509.
  • Srivastava, S. P., Kumar K. U., and Kaufman R. J.. 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.
  • Tolan, D. R., Hershey J. W., and Traut R. T.. 1983. Crosslinking of eukaryotic initiation factor eIF3 to the 40S ribosomal subunit from rabbit reticulocytes. Biochimie 65:427–436.
  • Wek, S. A., Zhu S., and Wek R. C.. 1995. The histidyl-tRNA synthetase-related sequence in the eIF2α protein kinase GCN2 interacts with tRNA and is required for activation in response to starvation for different amino acids. Mol. Cell. Biol. 15:4497–4506.
  • Williams, B. R. 1999. PKR; a sentinel kinase for cellular stress. Oncogene 18:6112–6120.
  • Wong, C., Luedi M., Hershey J. W., and Issinger O. G.. 1976. Phosphorylation in vitro of eukaryotic initiation factors IF-E2 and IF-E3 by protein kinases. J. Biol. Chem. 251:7675–7681.

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