Abstract
All cellular cytoplasmic mRNAs carry a 7-methylguanylate cap attached to their 5' ends. This cap structure is recognized by cap-binding proteins that then direct the binding of ribosomal subunits to this 5'-end complex. Poliovirus, a plus-stranded RNA virus, interferes with this cellular translation process by proteolytically inactivating the cap-binding protein complex. Subsequently the viral mRNA can be translated by an initiation process in which ribosomes bind internally to the mRNA [Pelletier, J. & Sonenberg, N. (1988) Nature (London) 334, 320-325], obviating cap-dependent translation. At least one cellular mRNA, encoding a heat shock-like protein, glucose-regulated protein 78/immunoglobulin heavy-chain binding protein, has been discovered to be translated at an increased rate in poliovirus-infected cells at a time when the translation of other cellular mRNAs is inhibited. The glucose-regulated protein 78/immunoglobulin heavy-chain binding protein mRNA thus exemplifies a cellular mRNA that is translated at a specifically enhanced rate by an as-yet-unresolved cap-independent initiation process in cells when the cap-binding protein complex is not functional.
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Selected References
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- Berget S. M., Moore C., Sharp P. A. Spliced segments at the 5' terminus of adenovirus 2 late mRNA. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3171–3175. doi: 10.1073/pnas.74.8.3171. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bernstein H. D., Sarnow P., Baltimore D. Genetic complementation among poliovirus mutants derived from an infectious cDNA clone. J Virol. 1986 Dec;60(3):1040–1049. doi: 10.1128/jvi.60.3.1040-1049.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bernstein H. D., Sonenberg N., Baltimore D. Poliovirus mutant that does not selectively inhibit host cell protein synthesis. Mol Cell Biol. 1985 Nov;5(11):2913–2923. doi: 10.1128/mcb.5.11.2913. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berstein H. D., Baltimore D. Poliovirus mutant that contains a cold-sensitive defect in viral RNA synthesis. J Virol. 1988 Aug;62(8):2922–2928. doi: 10.1128/jvi.62.8.2922-2928.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bole D. G., Hendershot L. M., Kearney J. F. Posttranslational association of immunoglobulin heavy chain binding protein with nascent heavy chains in nonsecreting and secreting hybridomas. J Cell Biol. 1986 May;102(5):1558–1566. doi: 10.1083/jcb.102.5.1558. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bonneau A. M., Sonenberg N. Proteolysis of the p220 component of the cap-binding protein complex is not sufficient for complete inhibition of host cell protein synthesis after poliovirus infection. J Virol. 1987 Apr;61(4):986–991. doi: 10.1128/jvi.61.4.986-991.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chow L. T., Gelinas R. E., Broker T. R., Roberts R. J. An amazing sequence arrangement at the 5' ends of adenovirus 2 messenger RNA. Cell. 1977 Sep;12(1):1–8. doi: 10.1016/0092-8674(77)90180-5. [DOI] [PubMed] [Google Scholar]
- Cleveland D. W., Fischer S. G., Kirschner M. W., Laemmli U. K. Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis. J Biol Chem. 1977 Feb 10;252(3):1102–1106. [PubMed] [Google Scholar]
- Collins P. L., Hightower L. E. Newcastle disease virus stimulates the cellular accumulation of stress (heat shock) mRNAs and proteins. J Virol. 1982 Nov;44(2):703–707. doi: 10.1128/jvi.44.2.703-707.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DALES S., EGGERS H. J., TAMM I., PALADE G. E. ELECTRON MICROSCOPIC STUDY OF THE FORMATION OF POLIOVIRUS. Virology. 1965 Jul;26:379–389. doi: 10.1016/0042-6822(65)90001-2. [DOI] [PubMed] [Google Scholar]
- Dolph P. J., Racaniello V., Villamarin A., Palladino F., Schneider R. J. The adenovirus tripartite leader may eliminate the requirement for cap-binding protein complex during translation initiation. J Virol. 1988 Jun;62(6):2059–2066. doi: 10.1128/jvi.62.6.2059-2066.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Etchison D., Milburn S. C., Edery I., Sonenberg N., Hershey J. W. Inhibition of HeLa cell protein synthesis following poliovirus infection correlates with the proteolysis of a 220,000-dalton polypeptide associated with eucaryotic initiation factor 3 and a cap binding protein complex. J Biol Chem. 1982 Dec 25;257(24):14806–14810. [PubMed] [Google Scholar]
- Gruss P., Dhar R., Khoury G. Simian virus 40 tandem repeated sequences as an element of the early promoter. Proc Natl Acad Sci U S A. 1981 Feb;78(2):943–947. doi: 10.1073/pnas.78.2.943. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hanecak R., Semler B. L., Anderson C. W., Wimmer E. Proteolytic processing of poliovirus polypeptides: antibodies to polypeptide P3-7c inhibit cleavage at glutamine-glycine pairs. Proc Natl Acad Sci U S A. 1982 Jul;79(13):3973–3977. doi: 10.1073/pnas.79.13.3973. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jang S. K., Kräusslich H. G., Nicklin M. J., Duke G. M., Palmenberg A. C., Wimmer E. A segment of the 5' nontranslated region of encephalomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation. J Virol. 1988 Aug;62(8):2636–2643. doi: 10.1128/jvi.62.8.2636-2643.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kitamura N., Semler B. L., Rothberg P. G., Larsen G. R., Adler C. J., Dorner A. J., Emini E. A., Hanecak R., Lee J. J., van der Werf S. Primary structure, gene organization and polypeptide expression of poliovirus RNA. Nature. 1981 Jun 18;291(5816):547–553. doi: 10.1038/291547a0. [DOI] [PubMed] [Google Scholar]
- Kozutsumi Y., Segal M., Normington K., Gething M. J., Sambrook J. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature. 1988 Mar 31;332(6163):462–464. doi: 10.1038/332462a0. [DOI] [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- Lee A. S., Delegeane A. M., Baker V., Chow P. C. Transcriptional regulation of two genes specifically induced by glucose starvation in a hamster mutant fibroblast cell line. J Biol Chem. 1983 Jan 10;258(1):597–603. [PubMed] [Google Scholar]
- Lee A. S., Delegeane A., Scharff D. Highly conserved glucose-regulated protein in hamster and chicken cells: preliminary characterization of its cDNA clone. Proc Natl Acad Sci U S A. 1981 Aug;78(8):4922–4925. doi: 10.1073/pnas.78.8.4922. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Munro S., Pelham H. R. An Hsp70-like protein in the ER: identity with the 78 kd glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell. 1986 Jul 18;46(2):291–300. doi: 10.1016/0092-8674(86)90746-4. [DOI] [PubMed] [Google Scholar]
- Muñoz A., Alonso M. A., Carrasco L. Synthesis of heat-shock proteins in HeLa cells: inhibition by virus infection. Virology. 1984 Aug;137(1):150–159. doi: 10.1016/0042-6822(84)90018-7. [DOI] [PubMed] [Google Scholar]
- Pelham H. R. Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell. 1986 Sep 26;46(7):959–961. doi: 10.1016/0092-8674(86)90693-8. [DOI] [PubMed] [Google Scholar]
- Pelletier J., Sonenberg N. Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature. 1988 Jul 28;334(6180):320–325. doi: 10.1038/334320a0. [DOI] [PubMed] [Google Scholar]
- Peluso R. W., Lamb R. A., Choppin P. W. Infection with paramyxoviruses stimulates synthesis of cellular polypeptides that are also stimulated in cells transformed by Rous sarcoma virus or deprived of glucose. Proc Natl Acad Sci U S A. 1978 Dec;75(12):6120–6124. doi: 10.1073/pnas.75.12.6120. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Racaniello V. R., Baltimore D. Cloned poliovirus complementary DNA is infectious in mammalian cells. Science. 1981 Nov 20;214(4523):916–919. doi: 10.1126/science.6272391. [DOI] [PubMed] [Google Scholar]
- Racaniello V. R., Meriam C. Poliovirus temperature-sensitive mutant containing a single nucleotide deletion in the 5'-noncoding region of the viral RNA. Virology. 1986 Dec;155(2):498–507. doi: 10.1016/0042-6822(86)90211-4. [DOI] [PubMed] [Google Scholar]
- Sarnow P., Bernstein H. D., Baltimore D. A poliovirus temperature-sensitive RNA synthesis mutant located in a noncoding region of the genome. Proc Natl Acad Sci U S A. 1986 Feb;83(3):571–575. doi: 10.1073/pnas.83.3.571. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sarnow P., Hearing P., Anderson C. W., Reich N., Levine A. J. Identification and characterization of an immunologically conserved adenovirus early region 11,000 Mr protein and its association with the nuclear matrix. J Mol Biol. 1982 Dec 15;162(3):565–583. doi: 10.1016/0022-2836(82)90389-8. [DOI] [PubMed] [Google Scholar]
- Sarnow P., Ho Y. S., Williams J., Levine A. J. Adenovirus E1b-58kd tumor antigen and SV40 large tumor antigen are physically associated with the same 54 kd cellular protein in transformed cells. Cell. 1982 Feb;28(2):387–394. doi: 10.1016/0092-8674(82)90356-7. [DOI] [PubMed] [Google Scholar]
- Schneider R. J., Safer B., Munemitsu S. M., Samuel C. E., Shenk T. Adenovirus VAI RNA prevents phosphorylation of the eukaryotic initiation factor 2 alpha subunit subsequent to infection. Proc Natl Acad Sci U S A. 1985 Jul;82(13):4321–4325. doi: 10.1073/pnas.82.13.4321. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Semler B. L., Dorner A. J., Wimmer E. Production of infectious poliovirus from cloned cDNA is dramatically increased by SV40 transcription and replication signals. Nucleic Acids Res. 1984 Jun 25;12(12):5123–5141. doi: 10.1093/nar/12.12.5123. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Semler B. L., Johnson V. H., Tracy S. A chimeric plasmid from cDNA clones of poliovirus and coxsackievirus produces a recombinant virus that is temperature-sensitive. Proc Natl Acad Sci U S A. 1986 Mar;83(6):1777–1781. doi: 10.1073/pnas.83.6.1777. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sonenberg N., Guertin D., Lee K. A. Capped mRNAs with reduced secondary structure can function in extracts from poliovirus-infected cells. Mol Cell Biol. 1982 Dec;2(12):1633–1638. doi: 10.1128/mcb.2.12.1633. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sonenberg N. Regulation of translation by poliovirus. Adv Virus Res. 1987;33:175–204. doi: 10.1016/s0065-3527(08)60318-8. [DOI] [PubMed] [Google Scholar]
- Stoeckle M. Y., Sugano S., Hampe A., Vashistha A., Pellman D., Hanafusa H. 78-kilodalton glucose-regulated protein is induced in Rous sarcoma virus-transformed cells independently of glucose deprivation. Mol Cell Biol. 1988 Jul;8(7):2675–2680. doi: 10.1128/mcb.8.7.2675. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ting J., Lee A. S. Human gene encoding the 78,000-dalton glucose-regulated protein and its pseudogene: structure, conservation, and regulation. DNA. 1988 May;7(4):275–286. doi: 10.1089/dna.1988.7.275. [DOI] [PubMed] [Google Scholar]
- Toyoda H., Nicklin M. J., Murray M. G., Anderson C. W., Dunn J. J., Studier F. W., Wimmer E. A second virus-encoded proteinase involved in proteolytic processing of poliovirus polyprotein. Cell. 1986 Jun 6;45(5):761–770. doi: 10.1016/0092-8674(86)90790-7. [DOI] [PubMed] [Google Scholar]
- Trono D., Andino R., Baltimore D. An RNA sequence of hundreds of nucleotides at the 5' end of poliovirus RNA is involved in allowing viral protein synthesis. J Virol. 1988 Jul;62(7):2291–2299. doi: 10.1128/jvi.62.7.2291-2299.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zala C. A., Salas-Prato M., Yan W. T., Banjo B., Perdue J. F. In cultured chick embryo fibroblasts the hexose transport components are not the 75 000 and 95 000 dalton polypeptides synthesized following glucose deprivation. Can J Biochem. 1980 Oct;58(10):1179–1188. doi: 10.1139/o80-158. [DOI] [PubMed] [Google Scholar]