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J Virol. Nov 1991; 65(11): 6194–6204.
PMCID: PMC250311

Translation of poliovirus RNA: role of an essential cis-acting oligopyrimidine element within the 5' nontranslated region and involvement of a cellular 57-kilodalton protein.

Abstract

Translation of poliovirus RNA is initiated by cap-independent internal entry of ribosomes into the 5' nontranslated region. This process is dependent on elements within the 5' nontranslated region (the internal ribosomal entry site) and may involve novel translation factors. Systematic mutation of a conserved oligopyrimidine tract has revealed a cis-acting element that is essential for translation in vitro. The function of this element is related to its position relative to other cis-acting domains. This element is part of a more complex structure that interacts with several cellular factors, but changes in protein binding after mutation of this element were not detected in a UV cross-linking assay. A 57-kDa protein from the ribosomal salt wash fraction of HeLa cells was identified that binds upstream of the oligopyrimidine tract. Translation of poliovirus mRNA in vitro was strongly and specifically inhibited by competition with the p57-binding domain (nucleotides 260 to 488) of the 5' nontranslated region of encephalomyocarditis virus, indicating a probable role for p57 in poliovirus translation. p57 is likely to be identical to the ribosome-associated factor that binds to and is necessary for the function of the internal ribosomal entry site of encephalomyocarditis virus RNA.

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  • Agol VI, Drozdov SG, Ivannikova TA, Kolesnikova MS, Korolev MB, Tolskaya EA. Restricted growth of attenuated poliovirus strains in cultured cells of a human neuroblastoma. J Virol. 1989 Sep;63(9):4034–4038. [PMC free article] [PubMed]
  • Almond JW. The attenuation of poliovirus neurovirulence. Annu Rev Microbiol. 1987;41:153–180. [PubMed]
  • Alsaadi S, Hassard S, Stanway G. Sequences in the 5' non-coding region of human rhinovirus 14 RNA that affect in vitro translation. J Gen Virol. 1989 Oct;70(Pt 10):2799–2804. [PubMed]
  • Andino R, Rieckhof GE, Baltimore D. A functional ribonucleoprotein complex forms around the 5' end of poliovirus RNA. Cell. 1990 Oct 19;63(2):369–380. [PubMed]
  • Beck E, Forss S, Strebel K, Cattaneo R, Feil G. Structure of the FMDV translation initiation site and of the structural proteins. Nucleic Acids Res. 1983 Nov 25;11(22):7873–7885. [PMC free article] [PubMed]
  • Bienkowska-Szewczyk K, Ehrenfeld E. An internal 5'-noncoding region required for translation of poliovirus RNA in vitro. J Virol. 1988 Aug;62(8):3068–3072. [PMC free article] [PubMed]
  • Borovjagin AV, Evstafieva AG, Ugarova TYu, Shatsky IN. A factor that specifically binds to the 5'-untranslated region of encephalomyocarditis virus RNA. FEBS Lett. 1990 Feb 26;261(2):237–240. [PubMed]
  • Brown BA, Ehrenfeld E. Translation of poliovirus RNA in vitro: changes in cleavage pattern and initiation sites by ribosomal salt wash. Virology. 1979 Sep;97(2):396–405. [PubMed]
  • Chapman NM, Tracy S, Gauntt CJ, Fortmueller U. Molecular detection and identification of enteroviruses using enzymatic amplification and nucleic acid hybridization. J Clin Microbiol. 1990 May;28(5):843–850. [PMC free article] [PubMed]
  • del Angel RM, Papavassiliou AG, Fernández-Tomás C, Silverstein SJ, Racaniello VR. Cell proteins bind to multiple sites within the 5' untranslated region of poliovirus RNA. Proc Natl Acad Sci U S A. 1989 Nov;86(21):8299–8303. [PMC free article] [PubMed]
  • de Moor CH, van Heugten HA, Voorma HO. Characterization of messenger ribonucleoprotein particles. Mol Biol Rep. 1990;14(2-3):57–60. [PubMed]
  • Dorner AJ, Dorner LF, Larsen GR, Wimmer E, Anderson CW. Identification of the initiation site of poliovirus polyprotein synthesis. J Virol. 1982 Jun;42(3):1017–1028. [PMC free article] [PubMed]
  • Dorner AJ, Semler BL, Jackson RJ, Hanecak R, Duprey E, Wimmer E. In vitro translation of poliovirus RNA: utilization of internal initiation sites in reticulocyte lysate. J Virol. 1984 May;50(2):507–514. [PMC free article] [PubMed]
  • Dreyfuss G. Structure and function of nuclear and cytoplasmic ribonucleoprotein particles. Annu Rev Cell Biol. 1986;2:459–498. [PubMed]
  • Dunn JJ, Studier FW. Complete nucleotide sequence of bacteriophage T7 DNA and the locations of T7 genetic elements. J Mol Biol. 1983 Jun 5;166(4):477–535. [PubMed]
  • Hellen CU, Kräusslich HG, Wimmer E. Proteolytic processing of polyproteins in the replication of RNA viruses. Biochemistry. 1989 Dec 26;28(26):9881–9890. [PubMed]
  • Iizuka N, Kohara M, Hagino-Yamagishi K, Abe S, Komatsu T, Tago K, Arita M, Nomoto A. Construction of less neurovirulent polioviruses by introducing deletions into the 5' noncoding sequence of the genome. J Virol. 1989 Dec;63(12):5354–5363. [PMC free article] [PubMed]
  • Jackson RJ, Howell MT, Kaminski A. The novel mechanism of initiation of picornavirus RNA translation. Trends Biochem Sci. 1990 Dec;15(12):477–483. [PubMed]
  • Jang SK, Davies MV, Kaufman RJ, Wimmer E. Initiation of protein synthesis by internal entry of ribosomes into the 5' nontranslated region of encephalomyocarditis virus RNA in vivo. J Virol. 1989 Apr;63(4):1651–1660. [PMC free article] [PubMed]
  • Jang SK, Kräusslich HG, Nicklin MJ, Duke GM, Palmenberg AC, 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. [PMC free article] [PubMed]
  • Jang SK, Wimmer E. Cap-independent translation of encephalomyocarditis virus RNA: structural elements of the internal ribosomal entry site and involvement of a cellular 57-kD RNA-binding protein. Genes Dev. 1990 Sep;4(9):1560–1572. [PubMed]
  • Kozak M. Influences of mRNA secondary structure on initiation by eukaryotic ribosomes. Proc Natl Acad Sci U S A. 1986 May;83(9):2850–2854. [PMC free article] [PubMed]
  • Kozak M. An analysis of 5'-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res. 1987 Oct 26;15(20):8125–8148. [PMC free article] [PubMed]
  • Kräusslich HG, Hölscher C, Reuer Q, Harber J, Wimmer E. Myristoylation of the poliovirus polyprotein is required for proteolytic processing of the capsid and for viral infectivity. J Virol. 1990 May;64(5):2433–2436. [PMC free article] [PubMed]
  • Kuge S, Nomoto A. Construction of viable deletion and insertion mutants of the Sabin strain of type 1 poliovirus: function of the 5' noncoding sequence in viral replication. J Virol. 1987 May;61(5):1478–1487. [PMC free article] [PubMed]
  • Kühn R, Luz N, Beck E. Functional analysis of the internal translation initiation site of foot-and-mouth disease virus. J Virol. 1990 Oct;64(10):4625–4631. [PMC free article] [PubMed]
  • Kunkel TA. Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc Natl Acad Sci U S A. 1985 Jan;82(2):488–492. [PMC free article] [PubMed]
  • La Monica N, Racaniello VR. Differences in replication of attenuated and neurovirulent polioviruses in human neuroblastoma cell line SH-SY5Y. J Virol. 1989 May;63(5):2357–2360. [PMC free article] [PubMed]
  • Larsen GR, Semler BL, Wimmer E. Stable hairpin structure within the 5'-terminal 85 nucleotides of poliovirus RNA. J Virol. 1981 Jan;37(1):328–335. [PMC free article] [PubMed]
  • Le SY, Zuker M. Common structures of the 5' non-coding RNA in enteroviruses and rhinoviruses. Thermodynamical stability and statistical significance. J Mol Biol. 1990 Dec 5;216(3):729–741. [PubMed]
  • Lee CK, Wimmer E. Proteolytic processing of poliovirus polyprotein: elimination of 2Apro-mediated, alternative cleavage of polypeptide 3CD by in vitro mutagenesis. Virology. 1988 Oct;166(2):405–414. [PubMed]
  • Lee KA, Sonenberg N. Inactivation of cap-binding proteins accompanies the shut-off of host protein synthesis by poliovirus. Proc Natl Acad Sci U S A. 1982 Jun;79(11):3447–3451. [PMC free article] [PubMed]
  • López-Guerrero JA, Carrasco L, Martínez-Abarca F, Fresno M, Alonso MA. Restriction of poliovirus RNA translation in a human monocytic cell line. Eur J Biochem. 1989 Dec 22;186(3):577–582. [PubMed]
  • Luz N, Beck E. A cellular 57 kDa protein binds to two regions of the internal translation initiation site of foot-and-mouth disease virus. FEBS Lett. 1990 Sep 3;269(2):311–314. [PubMed]
  • McCallum FS, Maden BE. Human 18 S ribosomal RNA sequence inferred from DNA sequence. Variations in 18 S sequences and secondary modification patterns between vertebrates. Biochem J. 1985 Dec 15;232(3):725–733. [PMC free article] [PubMed]
  • Meerovitch K, Pelletier J, Sonenberg N. A cellular protein that binds to the 5'-noncoding region of poliovirus RNA: implications for internal translation initiation. Genes Dev. 1989 Jul;3(7):1026–1034. [PubMed]
  • Milligan JF, Groebe DR, Witherell GW, Uhlenbeck OC. Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucleic Acids Res. 1987 Nov 11;15(21):8783–8798. [PMC free article] [PubMed]
  • Najita L, Sarnow P. Oxidation-reduction sensitive interaction of a cellular 50-kDa protein with an RNA hairpin in the 5' noncoding region of the poliovirus genome. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5846–5850. [PMC free article] [PubMed]
  • Nicklin MJ, Kräusslich HG, Toyoda H, Dunn JJ, Wimmer E. Poliovirus polypeptide precursors: expression in vitro and processing by exogenous 3C and 2A proteinases. Proc Natl Acad Sci U S A. 1987 Jun;84(12):4002–4006. [PMC free article] [PubMed]
  • Palmenberg AC, Kirby EM, Janda MR, Drake NL, Duke GM, Potratz KF, Collett MS. The nucleotide and deduced amino acid sequences of the encephalomyocarditis viral polyprotein coding region. Nucleic Acids Res. 1984 Mar 26;12(6):2969–2985. [PMC free article] [PubMed]
  • Paul AV, Tada H, von der Helm K, Wissel T, Kiehn R, Wimmer E, Deinhardt F. The entire nucleotide sequence of the genome of human hepatitis A virus (isolate MBB). Virus Res. 1987 Aug;8(2):153–171. [PubMed]
  • Pelletier J, Flynn ME, Kaplan G, Racaniello V, Sonenberg N. Mutational analysis of upstream AUG codons of poliovirus RNA. J Virol. 1988 Dec;62(12):4486–4492. [PMC free article] [PubMed]
  • Pelletier J, Kaplan G, Racaniello VR, Sonenberg N. Cap-independent translation of poliovirus mRNA is conferred by sequence elements within the 5' noncoding region. Mol Cell Biol. 1988 Mar;8(3):1103–1112. [PMC free article] [PubMed]
  • Pelletier J, Kaplan G, Racaniello VR, Sonenberg N. Translational efficiency of poliovirus mRNA: mapping inhibitory cis-acting elements within the 5' noncoding region. J Virol. 1988 Jul;62(7):2219–2227. [PMC free article] [PubMed]
  • Pelletier J, Sonenberg N. Insertion mutagenesis to increase secondary structure within the 5' noncoding region of a eukaryotic mRNA reduces translational efficiency. Cell. 1985 Mar;40(3):515–526. [PubMed]
  • 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. [PubMed]
  • Phillips BA, Emmert A. Modulation of the expression of poliovirus proteins in reticulocyte lysates. Virology. 1986 Jan 30;148(2):255–267. [PubMed]
  • Pilipenko EV, Blinov VM, Chernov BK, Dmitrieva TM, Agol VI. Conservation of the secondary structure elements of the 5'-untranslated region of cardio- and aphthovirus RNAs. Nucleic Acids Res. 1989 Jul 25;17(14):5701–5711. [PMC free article] [PubMed]
  • Rhoads RE. Cap recognition and the entry of mRNA into the protein synthesis initiation cycle. Trends Biochem Sci. 1988 Feb;13(2):52–56. [PubMed]
  • Rose JK, Trachsel H, Leong K, Baltimore D. Inhibition of translation by poliovirus: inactivation of a specific initiation factor. Proc Natl Acad Sci U S A. 1978 Jun;75(6):2732–2736. [PMC free article] [PubMed]
  • Ruiz-Linares A, Bouloy M, Girard M, Cahour A. Modulations of the in vitro translational efficiencies of Yellow Fever virus mRNAs: interactions between coding and noncoding regions. Nucleic Acids Res. 1989 Apr 11;17(7):2463–2476. [PMC free article] [PubMed]
  • Sangar DV, Newton SE, Rowlands DJ, Clarke BE. All foot and mouth disease virus serotypes initiate protein synthesis at two separate AUGs. Nucleic Acids Res. 1987 Apr 24;15(8):3305–3315. [PMC free article] [PubMed]
  • Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. [PMC free article] [PubMed]
  • Schreier MH, Staehelin T. Initiation of mammalian protein synthesis: the importance of ribosome and initiation factor quality for the efficiency of in vitro systems. J Mol Biol. 1973 Feb 19;73(3):329–349. [PubMed]
  • Seechurn P, Knowles NJ, McCauley JW. The complete nucleotide sequence of a pathogenic swine vesicular disease virus. Virus Res. 1990 Jul;16(3):255–274. [PubMed]
  • Shih DS, Shih CT, Kew O, Pallansch M, Rueckert R, Kaesberg P. Cell-free synthesis and processing of the proteins of poliovirus. Proc Natl Acad Sci U S A. 1978 Dec;75(12):5807–5811. [PMC free article] [PubMed]
  • Skinner MA, Racaniello VR, Dunn G, Cooper J, Minor PD, Almond JW. New model for the secondary structure of the 5' non-coding RNA of poliovirus is supported by biochemical and genetic data that also show that RNA secondary structure is important in neurovirulence. J Mol Biol. 1989 May 20;207(2):379–392. [PubMed]
  • Sonenberg N. Regulation of translation by poliovirus. Adv Virus Res. 1987;33:175–204. [PubMed]
  • Sonenberg N. Poliovirus translation. Curr Top Microbiol Immunol. 1990;161:23–47. [PubMed]
  • Stanway G. Structure, function and evolution of picornaviruses. J Gen Virol. 1990 Nov;71(Pt 11):2483–2501. [PubMed]
  • Svitkin YV, Cammack N, Minor PD, Almond JW. Translation deficiency of the Sabin type 3 poliovirus genome: association with an attenuating mutation C472----U. Virology. 1990 Mar;175(1):103–109. [PubMed]
  • Svitkin YV, Lyapustin VN, Lashkevich VA, Agol VI. Differences between translation products of tick-borne encephalitis virus RNA in cell-free systems from Krebs-2 cells and rabbit reticulocytes: involvement of membranes in the processing of nascent precursors of flavivirus structural proteins. Virology. 1984 Jun;135(2):536–541. [PubMed]
  • Svitkin YV, Maslova SV, Agol VI. The genomes of attenuated and virulent poliovirus strains differ in their in vitro translation efficiencies. Virology. 1985 Dec;147(2):243–252. [PubMed]
  • Svitkin YV, Pestova TV, Maslova SV, Agol VI. Point mutations modify the response of poliovirus RNA to a translation initiation factor: a comparison of neurovirulent and attenuated strains. Virology. 1988 Oct;166(2):394–404. [PubMed]
  • Toyoda H, Kohara M, Kataoka Y, Suganuma T, Omata T, Imura N, Nomoto A. Complete nucleotide sequences of all three poliovirus serotype genomes. Implication for genetic relationship, gene function and antigenic determinants. J Mol Biol. 1984 Apr 25;174(4):561–585. [PubMed]
  • van der Werf S, Bradley J, Wimmer E, Studier FW, Dunn JJ. Synthesis of infectious poliovirus RNA by purified T7 RNA polymerase. Proc Natl Acad Sci U S A. 1986 Apr;83(8):2330–2334. [PMC free article] [PubMed]
  • Wimmer E. Genome-linked proteins of viruses. Cell. 1982 Feb;28(2):199–201. [PubMed]

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