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PMID: 2538648 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Initiation of protein synthesis by internal entry of ribosomes into the 5' nontranslated region of encephalomyocarditis virus RNA in vivo.

Journal of virology ·Vol. 63 ·No. 4 ·1989-04-00 ·Pages 1651-60

Jang SK, Davies MV, Kaufman RJ, Wimmer E

Abstract

Expression vectors that yield mono-, di-, and tricistronic mRNAs upon transfection of COS-1 cells were used to assess the influence of the 5' nontranslated regions (5'NTRs) on translation of reporter genes. A segment of the 5'NTR of encephalomyocarditis virus (EMCV) allowed translation of an adjacent downstream reporter gene (CAT) regardless of its position in the mRNAs. A deletion in the EMCV 5'NTR abolishes this effect. Poliovirus infection completely inhibits translation of the first cistron of a dicistronic mRNA that is preceded by the capped globin 5'NTR, whereas the second cistron preceded by the EMCV 5'NTR is still translated. We conclude that the EMCV 5'NTR contains an internal ribosomal entry site that allows cap-independent initiation of translation. mRNA containing the adenovirus tripartite leader is also resistant to inhibition of translation by poliovirus.

MeSH Terms
Animals Cell Line Chloramphenicol O-Acetyltransferase/genetics Cloning, Molecular Encephalomyocarditis virus/genetics Genes Peptide Chain Initiation, Translational Poliovirus/genetics RNA, Messenger/genetics RNA, Viral/genetics Regulatory Sequences, Nucleic Acid Ribosomes/physiology Viral Proteins/biosynthesis
Chemicals
RNA, Messenger RNA, Viral Viral Proteins Chloramphenicol O-Acetyltransferase
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Jang S K
Department of Microbiology, School of Medicine, State University of New York, Stony Brook 11794-8621.
Davies M V
Kaufman R J
Wimmer E
References (61)
61 references, click to expand
  1. Selective translation of mengovirus RNA over Host mRNA in homologous, fractionated, cell-free translational systems from Ehrlich-ascites-tumor cells.
    Eur J Biochem. 1978 Feb;83(2):353-61 PMID: 204478
  2. The enzymatic acetylation of chloramphenicol by extracts of R factor-resistant Escherichia coli.
    J Biol Chem. 1967 Feb 25;242(4):687-93 PMID: 5335032
  3. How do eucaryotic ribosomes select initiation regions in messenger RNA?
    Cell. 1978 Dec;15(4):1109-23 PMID: 215319
  4. Cell-free synthesis and processing of the proteins of poliovirus.
    Proc Natl Acad Sci U S A. 1978 Dec;75(12):5807-11 PMID: 215997
  5. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease.
    Biochemistry. 1979 Nov 27;18(24):5294-9 PMID: 518835
  6. Influence of mRNA secondary structure on binding and migration of 40S ribosomal subunits.
    Cell. 1980 Jan;19(1):79-90 PMID: 7357609
  7. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose.
    Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201-5 PMID: 6159641
  8. SV40-transformed simian cells support the replication of early SV40 mutants.
    Cell. 1981 Jan;23(1):175-82 PMID: 6260373
  9. Transcriptional control in the production of liver-specific mRNAs.
    Cell. 1981 Mar;23(3):731-9 PMID: 7226226
  10. Possible role of flanking nucleotides in recognition of the AUG initiator codon by eukaryotic ribosomes.
    Nucleic Acids Res. 1981 Oct 24;9(20):5233-52 PMID: 7301588
  11. A membrane-associated precursor to poliovirus VPg identified by immunoprecipitation with antibodies directed against a synthetic heptapeptide.
    Cell. 1982 Feb;28(2):405-12 PMID: 6277514
  12. Efficient infection of monkey cells with DNA of simian virus 40.
    Proc Natl Acad Sci U S A. 1981 Dec;78(12):7575-8 PMID: 6278479
  13. 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):14806-10 PMID: 6294080
  14. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells.
    Mol Cell Biol. 1982 Sep;2(9):1044-51 PMID: 6960240
  15. High efficiency polyoma DNA transfection of chloroquine treated cells.
    Nucleic Acids Res. 1983 Mar 11;11(5):1295-308 PMID: 6298741
  16. In vitro translation of poliovirus RNA: utilization of internal initiation sites in reticulocyte lysate.
    J Virol. 1984 May;50(2):507-14 PMID: 6323749
  17. Modulation of the expression of poliovirus proteins in reticulocyte lysates.
    Virology. 1986 Jan 30;148(2):255-67 PMID: 3002037
  18. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes.
    Cell. 1986 Jan 31;44(2):283-92 PMID: 3943125
  19. 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):1777-81 PMID: 3006071
  20. Transient expression of human adenosine deaminase cDNAs: identification of a nonfunctional clone resulting from a single amino acid substitution.
    Mol Cell Biol. 1985 Apr;5(4):762-7 PMID: 3838797
  21. Genetic analysis of the attenuation phenotype of poliovirus type 1.
    J Virol. 1986 May;58(2):348-58 PMID: 3009852
  22. Influences of mRNA secondary structure on initiation by eukaryotic ribosomes.
    Proc Natl Acad Sci U S A. 1986 May;83(9):2850-4 PMID: 3458245
  23. Poliovirus mutant that does not selectively inhibit host cell protein synthesis.
    Mol Cell Biol. 1985 Nov;5(11):2913-23 PMID: 3018486
  24. Bifunctional messenger RNAs in eukaryotes.
    Cell. 1986 Nov 21;47(4):481-3 PMID: 3779834
  25. Role of the avian retrovirus mRNA leader in expression: evidence for novel translational control.
    Mol Cell Biol. 1986 Feb;6(2):372-9 PMID: 3023842
  26. Termination-reinitiation occurs in the translation of mammalian cell mRNAs.
    Mol Cell Biol. 1986 Jul;6(7):2695-703 PMID: 3023945
  27. Replication of SV5 RNA and the effects of superinfection with poliovirus.
    Virology. 1967 Nov;33(3):442-51 PMID: 4168765
  28. Polypeptide cleavages in the formation of poliovirus proteins.
    Proc Natl Acad Sci U S A. 1968 Sep;61(1):77-84 PMID: 4301595
  29. Adenovirus polypeptide synthesis in the presence of non-replicating poliovirus.
    J Gen Virol. 1974 Aug;24(2):261-79 PMID: 4368375
  30. 5'-terminal structure of poliovirus polyribosomal RNA is pUp.
    Proc Natl Acad Sci U S A. 1976 Feb;73(2):327-30 PMID: 174102
  31. The 5' end of poliovirus mRNA is not capped with m7G(5')ppp(5')Np.
    Proc Natl Acad Sci U S A. 1976 Feb;73(2):375-80 PMID: 174106
  32. 5'-Terminal nucleotide sequences of polio virus polyribosomal RNA and virion RNA are identical.
    Nature. 1977 Jul 21;268(5617):270-2 PMID: 196211
  33. The 5'-terminal structures of poliovirion RNA and poliovirus mRNA differ only in the genome-linked protein VPg.
    Proc Natl Acad Sci U S A. 1977 Dec;74(12):5345-9 PMID: 202952
  34. Increased neurovirulence associated with a single nucleotide change in a noncoding region of the Sabin type 3 poliovaccine genome.
    Nature. 1985 Apr 11-17;314(6011):548-50 PMID: 2986004
  35. Human GM-CSF: molecular cloning of the complementary DNA and purification of the natural and recombinant proteins.
    Science. 1985 May 17;228(4701):810-5 PMID: 3923623
  36. The genomes of attenuated and virulent poliovirus strains differ in their in vitro translation efficiencies.
    Virology. 1985 Dec;147(2):243-52 PMID: 3000069
  37. Effect of upstream reading frames on translation efficiency in simian virus 40 recombinants.
    Mol Cell Biol. 1986 Jul;6(7):2704-11 PMID: 3023946
  38. 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 PMID: 3024397
  39. 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):1478-87 PMID: 3033275
  40. Effects of cDNA hybridization on translation of encephalomyocarditis virus RNA.
    J Virol. 1987 Jun;61(6):2033-7 PMID: 3033330
  41. Translational efficiency of polycistronic mRNAs and their utilization to express heterologous genes in mammalian cells.
    EMBO J. 1987 Jan;6(1):187-93 PMID: 3582359
  42. Adenovirus late protein synthesis is resistant to the inhibition of translation induced by poliovirus.
    J Biol Chem. 1987 May 25;262(15):7328-34 PMID: 3034890
  43. Regulation of translation by poliovirus.
    Adv Virus Res. 1987;33:175-204 PMID: 3035905
  44. Discrete elements within the SV40 enhancer region display different cell-specific enhancer activities.
    EMBO J. 1987 Apr;6(4):1017-25 PMID: 3036487
  45. Translational control mediated by eucaryotic initiation factor-2 is restricted to specific mRNAs in transfected cells.
    Mol Cell Biol. 1987 Apr;7(4):1568-71 PMID: 3600637
  46. Poliovirus proteinase 2A induces cleavage of eucaryotic initiation factor 4F polypeptide p220.
    J Virol. 1987 Sep;61(9):2711-8 PMID: 3039165
  47. Effects of intercistronic length on the efficiency of reinitiation by eucaryotic ribosomes.
    Mol Cell Biol. 1987 Oct;7(10):3438-45 PMID: 3683388
  48. The adenovirus tripartite leader may eliminate the requirement for cap-binding protein complex during translation initiation.
    J Virol. 1988 Jun;62(6):2059-66 PMID: 2835510
  49. Cap-independent translation of poliovirus mRNA is conferred by sequence elements within the 5' noncoding region.
    Mol Cell Biol. 1988 Mar;8(3):1103-12 PMID: 2835660
  50. 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):2291-9 PMID: 2836612
  51. 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):2636-43 PMID: 2839690
  52. RNA translation. Picornaviruses break the rules.
    Nature. 1988 Jul 28;334(6180):292-3 PMID: 3393222
  53. Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA.
    Nature. 1988 Jul 28;334(6180):320-5 PMID: 2839775
  54. Cap-binding proteins of eukaryotic messenger RNA: functions in initiation and control of translation.
    Prog Nucleic Acid Res Mol Biol. 1988;35:173-207 PMID: 3065823
  55. Conserved structural domains in the 5'-untranslated region of picornaviral genomes: an analysis of the segment controlling translation and neurovirulence.
    Virology. 1989 Feb;168(2):201-9 PMID: 2536978
  56. Alterations in HeLa cell metabolism resulting from poliovirus infection.
    Virology. 1959 Oct;9:244-59 PMID: 14441181
  57. The nucleotide and deduced amino acid sequences of the encephalomyocarditis viral polyprotein coding region.
    Nucleic Acids Res. 1984 Mar 26;12(6):2969-85 PMID: 6324136
  58. Initiation of translation at internal AUG codons in mammalian cells.
    Nature. 1984 May 3-9;309(5963):82-5 PMID: 6717585
  59. Insertion mutagenesis to increase secondary structure within the 5' noncoding region of a eukaryotic mRNA reduces translational efficiency.
    Cell. 1985 Mar;40(3):515-26 PMID: 2982496
  60. Shutoff of host translation by encephalomyocarditis virus infection does not involve cleavage of the eucaryotic initiation factor 4F polypeptide that accompanies poliovirus infection.
    J Virol. 1985 May;54(2):643-5 PMID: 2985829
  61. Quantitation of dihydrofolate reductase in individual parental and methotrexate-resistant murine cells. Use of a fluorescence activated cell sorter.
    J Biol Chem. 1978 Aug 25;253(16):5852-60 PMID: 670236
Article Info
Journal
Journal of virology
Abbr.
J Virol
ISSN
0022-538X
Published
1989-04-00
Pages
1651-60
Language
English
Region
United States
NLM ID
0113724
PMCID
PMC248413
Subset
IM
Grants
NIAID NIH HHS · AI-15122 · United States
NCI NIH HHS · CA-28146 · United States
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