Translation of Encephalomyocarditis Virus RNA by Internal Ribosomal Entry

  • C. U. T. Hellen
  • E. Wimmer
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 203)

Abstract

The positive-sense genomic RNAs of picornaviruses such as encephalomyocarditis virus (EMCV) have been widely used in studies of translation, resulting in significant advances, such as identification of mammalian Met-tRNA (Smith and Marcker 1970) and recognition of the initiation factor elF-4A (Wigle and Smith 1973; Blair etal. 1977). Analysis of picornavirus translation also revealed a fundamental difference between eukaryotic and prokaryotic mRNAs: initiation of translation is limited to a single 5’ proximal site (Jacobson and Baltimore 1968; Smith 1973), indicating that picornavirus genomes, and by implication all other eukaryotic mRNAs, are monocistronic. The EMCV genome does indeed contain a single large open reading frame, but further studies of picornavirus mRNAs revealed fundamental differences from standard eukaryotic mRNAs (such as the absence of a 5’ terminal capping group, and the presence of multiple AUG triplets and stable secondary structure upstream of the initiation codon) that proved incompatible with conventional models for the initiation of eukaryotic translation (Kozak 1991). The discovery that EMCV initiation results from entry of ribosomes into an internal segment of the 5’NCR (Jang et al. 1988) has revitalized studies of EMCV translation, and its internal ribosome entry site (IRES) is now used both as a model for analysis of this novel mechanism of eukaryotic gene expression, and as a genetic element, for example in expression vectors, to promote cap-independent internal initiation of translation.This review shall focus on EMCV translation, but will also consider translation of other cardioviruses and of the related aphtho-viruses and hepatoviruses.

Keywords

Hepatitis Codon adenOSine Polypeptide Methionine 

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References

  1. Abramson RD, Dever TE, Lawson TG, Ray BK, Thach RE, Merrick WC (1987) The ATP-dependent interaction of eukaryotic initiation factors with mRNA. J Biol Chem 262: 3826–3832PubMedGoogle Scholar
  2. Abramson RD, Dever TE, Merrick WC (1988) Biochemical evidence supporting a mechanism for cap- independent and internal initiation of eukaryotic mRNA. J Biol Chem 263:6016–6019.PubMedGoogle Scholar
  3. Adam MA, Ramesh N, Miller AD, Osbourne WRA,(1991) Internal initiation of translation in retroviral vectors carrying picornavirus 5’ nontranslated regions. J Virol 65: 4985–4990PubMedGoogle Scholar
  4. Alexander L, Lu HH, Wimmer E (1994) Polioviruses containing picornavirus type 1 and/or type 2 internal ribosomal entry site elements: genetic hybrids and the expression of a foreign gene. Proc Natl Acad Sci USA 91: 1406–1410PubMedGoogle Scholar
  5. Alonso MA, Carrasco L (1981) Reversion by hypotonic medium of the shutoff of protein synthesis induced by encephalomyocarditis virus. J Virol 37: 535–540PubMedGoogle Scholar
  6. Anthony DD, Merrick WC (1991) Eukaryotic intiation factor (elF)-4F. Implications for a role in internal initiation of translation. J Biol Chem 266: 10218–10226.PubMedGoogle Scholar
  7. Baglioni C, Simili M, Shafritz DA (1978) Initiation activity of EMCV virus RNA, binding to initiation factor elF-4B and shut-off of host cell protein synthesis. Nature 275: 240–243PubMedGoogle Scholar
  8. Bandyopadhyay PK, Wang C, Lipton HL (1992) Cap-independent translation by the 5’ untranslated region of Theiler’s murine encephalomyelitis virus. J Virol 66: 6249–6256PubMedGoogle Scholar
  9. Bandyopadhyay PK, Pritchard A, Jensen K, Lipton HL (1993) A three-nucleotide insertion in the H stem- loop of the 5’ untranslated region of Theiler’s virus attenuates neurovirulence. J Virol 67: 3691–3695PubMedGoogle Scholar
  10. Beck E, Forss S, Strebel K, Cattaneo R, Feil G (1983) Structure of the FMDV translation initiation site and of the structural proteins. Nucleic Acids Res 11: 7873–7885PubMedGoogle Scholar
  11. Belsham GJ (1992) Dual initiation sites of protein synthesis on foot-and-mouth disease virus RNA are selected following internal entry and scanning of ribosomes in vivo. EMBO J 11: 1105–1110PubMedGoogle Scholar
  12. Belsham GJ, Brangwyn JK (1990) A region of the 5’ noncoding region of foot-and-mouth disease virus RNA directs efficient internal initiation of protein synthesis within cells: involvement with the role of L protease in translational control. J Virol 64: 5389–5395PubMedGoogle Scholar
  13. Bennett M, Michaud S, Kingston J, Reed R (1992a) Protein components specifically associated with prespliceosome and spliceosome complexes. Genes Dev 6: 1986–2000PubMedGoogle Scholar
  14. Bennett M, Pinol-Roma S, Staknis D, Dreyfuss G, Reed R (1992b) Differential binding of heterogenous nuclear ribonucleoproteins to mRNA precursors prior to spliceosome assembly in vitro. Mol Cell Biol 12:3165–3175PubMedGoogle Scholar
  15. Black DN, Stephenson P, Rowlands DJ, Brown F (1979) Sequence and location of the poly (C) tract in aphtho- and cardiovirus RNA. Nucleic Acids Res 6: 2381–2390PubMedGoogle Scholar
  16. Blair GE, Dahl HHM, Truelsen E, Lelong JC (1977) Functional identity of a mouse ascites and a rabbit reticulocyte initiation factor required for natural mRNA translation. Nature 265: 651–653PubMedGoogle Scholar
  17. Borman A, Jackson RJ (1992) Initiation of translation of human rhinovirus RNA: mapping internal ribosomal entry site. Virology 88: 685–696Google Scholar
  18. Borman A, Howell MT, Patton JG, Jackson RJ (1993) The involvement of a spliceosome component in internal initiation of human rhinovirus RNA translation. J Gen Virol 74: 1775–1778PubMedGoogle Scholar
  19. Borovjagin AV, Evstafieva AG, Ugarova TY, Shatsky IN (1990) A factor that specifically binds to the 5-untranslated region of encephalomyocarditis virus RNA. FEBS Lett 261: 237–240PubMedGoogle Scholar
  20. Borovjagin AV, Ezrokhi MV, Rostapshov VM, Ugarova TY, Bystrova TF, Shatsky IN (1991) RNA-protein interactions within the internal translation initiation region of encephalomyocarditis virus RNA. Nucleic Acids Res 19: 4999–5005PubMedGoogle Scholar
  21. Borovjagin AV, Pestova TV, Shatsky IN (1994) Pyrimidine tract binding protein strongly stimulates in vitro encephalomyocarditis virus RNA translation at the level of preinitiation complex formation. FEBS Letts 351: 299–302Google Scholar
  22. Bothwell ALM, Ballard DW, Philbrick WM, Lindwall G, Maher SE, Bridgett MM, Jamison SF, Garcia-Blanco MA (1991) Murine polypyrimidine tract binding protein. Purification, cloning, and mapping of the RNA binding domain. J Biol Chem 266: 24657–24663PubMedGoogle Scholar
  23. Brahms J, Maurizot JC, Michelson AM (1967) Conformation and thermodynamic properties of oligo- cytidylic acids. J Mol Biol 25: 465–480PubMedGoogle Scholar
  24. Brown EA, Day SP, Jansen RW, Lemon SM (1991) The 5’ nontranslated region of hepatitis A virus RNA: secondary structure and elements required for translation in vitro. J Virol 65: 5828–5838PubMedGoogle Scholar
  25. Brown EA, Zajac AJ, Lemon SM (1994) In vitro characterization of an internal ribosomal entry site (IRES) present within the 5’ nontranslated region of hepatitis A virus RNA: comparison with the IRES of encephalomyocarditis virus. J Virol 68: 1066–1074PubMedGoogle Scholar
  26. Brown F, Newman J, Stott J, Porter A, Frisby D, Newton C, Carey N, Fellner P (1974) Poly (C) in animal viral RNAs. Nature 251: 342–344Google Scholar
  27. Brunei F, Alzari PM, Ferrara P, Zakin MM (1991) Cloning and sequencing of a PYBP, a pyrimidine - rich specific single strand DNA binding protein. Nucl Acid Res 19: 5237–5245Google Scholar
  28. Burd, C, Matunis E, Dreyfuss G (1991) The multiple RNA-binding domains of the mRNA poly (A)-binding protein have different RNA-binding activities. Mol Cell Biol 11: 3419–3424Google Scholar
  29. Butterworth BE, Hall L, Stoltzfus CM, Rueckert RR (1971) Virus-specific proteins synthesized in encephalomyocarditis virus-infected cells. Proc Natl Acad Sci USA 68:3083–3087PubMedGoogle Scholar
  30. Canaani D, Revel M, Groner Y (1976) Translational discrimination of ‘capped’ and ‘noncapped’ mRNAs: inhibition by a series of chemical analogs of m7GpppX. FEBS Lett 64: 326–331PubMedGoogle Scholar
  31. Chang KH, Brown EA, Lemon SM (1993) Cell type-specific proteins which interact with the 5’ nontranslated region hepatitis A virus RNA. J Virol 67: 6716–6725PubMedGoogle Scholar
  32. Chumakov KM, Agol VI (1976) Poly (C) sequence is located near the 5’-end of encephalomyocarditis virus RNA. Biochem Biophys Res Commun 71: 551–557PubMedGoogle Scholar
  33. Chumakov KM, Chichkova NV, Agol VI (1979) 5’-terminal sequence of encephalomyocarditis virus RNA: localization of the poly (C) tract, and role in translation. Dokl Akad Nauk SSSR 246: 994–996Google Scholar
  34. Clarke BE, Sangar DV, Burroughs JN, Newton SE, Carroll AR, Rowlands DJ (1985) Two initiation sites for foot-and mouth disease virus polyprotein in vivo. J Gen virol 66: 2615–2626PubMedGoogle Scholar
  35. Clarke BE, Brown AL, Currey KL, Newton SE, Rowlands DJ, Carroll AR (1987) Potential secondary and tertiary interactions in the genomic RNA of foot and mouth disease virus. Nucleic Acids Res 15: 7067–7079PubMedGoogle Scholar
  36. Coller B-AG, Chapman NM, Beck MA, Pallansch MA, Gauntt CJ, Tracy SM (1990) Echovirus 22 is an atypical enterovirus. J Virol 64: 2692–2701PubMedGoogle Scholar
  37. Dalgarno L, Cox RA, Martin EM (1967) Polyribosomes in normal Krebs 2 ascites tumor cells and in cells infected with encephalomyocarditis virus. Biochim Biophys Acta 138: 316–328PubMedGoogle Scholar
  38. Daniels-McQueen S, Detjen BM, Grifo JA, Merrick WG, Thach RE (1983) Unusual requirements for optimum translation of polio viral RNA in vitro. J Biol Chem 258: 7195–7199PubMedGoogle Scholar
  39. Davies MV, Kaufman RJ (1992) The sequence context of the initiation codon in the encephalomyocarditis virus leader modulates efficiency of internal translation initiation. J Virol 66: 1924–1932PubMedGoogle Scholar
  40. Deng H, Wang C, Ascadi G, Wolff JA (1991) High-efficiency protein synthesis from T7 TNA polymerase transcripts in 3T3 fibroblasts. Gene 109: 193–201PubMedGoogle Scholar
  41. Detjen BM, Jen G, Thach RE (1981) Encephalomyocarditis viral RNA can be translated under conditions of poliovirus-induced translation shutoff in vivo. J Virol 38: 777–781PubMedGoogle Scholar
  42. Dorner AJ, Dorner LF, Larsen GR, Wimmer E, Anderson CW (1982) Identification of the initiation site of poliovirus polyprotein synthesis. J Virol 42: 1017–1028PubMedGoogle Scholar
  43. Dorner AJ, Semler BL, Jackson RJ, Hanecak R, Duprey E, Wimmer E (1984) In vitro translation of poliovirus RNA: utilization of internal initiation sites in reticulocyte lysates. J Virol 50: 507–514PubMedGoogle Scholar
  44. Duke GM, Hoffman MA, Palmenberg AC (1992) Sequence and structural elements that contribute to efficient encephalomyocarditis virus RNA translation. J Virol 66: 1602–1609PubMedGoogle Scholar
  45. Edery I, Lee KAW, Sonenberg N (1984) Functional characterization of eukaryotic mRNA cap binding protein complex: effects on translation of capped and naturally uncapped RNAs. Biochemistry 23: 2456–2462PubMedGoogle Scholar
  46. Elroy-Stein O, Moss B (1990) Cytoplasmic expression system based on constitutive synthesis of bacteriophage T7 RNA polymjerase in mammalian cells. Proc Natl Acad Sci USA 87:6743–6747PubMedGoogle Scholar
  47. Elory-Stein O, Fuerst TR, Moss B (1989) Cap-independent translation of mRNA conferred by encephalo- myocarditis virus 5’ sequence improves the performance of the vaccinia virus/baceteriophage T7 hybrid expression system. Proc Natl Acad Sci USA 86: 6126–6130Google Scholar
  48. Escarmis C, Toja M, Medina M, Domingo E (1992) Modifications of the 5’ untranslated region of foot- and-mouth disease virus after prolonged persistence in cell culture. Virus Res. 26: 113–125PubMedGoogle Scholar
  49. Etchison D, Smith K (1990) Variations in cap-binding complexes from uninfected and poliovirus-infected HeLA cells. J Biol Chem 265: 358–362Google Scholar
  50. Etchison D, Milburn SC, Edery I, Sonenberg N, Hershey JWB (1982) Inhibition of HeLa cell protein synthesis following poliovirus infection correlates with the proteolysis of a 220,000 dalton polypeptide associated with eukaryotic initiation factor 3 and a cap-binding protein complex. J Biol Chem 257: 14806–14810PubMedGoogle Scholar
  51. Evstafieva AG, Ugarova TY, Chernov BK, Shatsky IN (1991) A complex RNA sequence determines the internal initiation of encephalomyocarditis virus RNA translation. Nucleic Acids Res 19: 665–671PubMedGoogle Scholar
  52. Evstafieva AG, Beletsky AV, Borovjagin AV, Bogdanov AA (1993) Internal ribosomal entry site of encephalomyocarditis virus RNA is unable to direct translation in Saccharmoyces cerevisiae. FEBS Lett 335: 273–276PubMedGoogle Scholar
  53. Forss S, Strebel K, Beck E, Schaller H (1984) Nucleotide sequence and genome organization of foot-and- mouth disease virus. Nucleic Acids Res 12: 6587–6601PubMedGoogle Scholar
  54. Frisby D, Eaton M, Fellner P (1976) Absence of 5’-terminal capping in encephalomyocarditis virus RNA. Nucleic Acids. Res 3: 2771–2787Google Scholar
  55. Garcia-Blanco MA, Jamison SF, Sharp PA (1989) Identification and purification of a 62 000 dalton protein that binds specifically to the polypyrimidine tract of introns. Genes Dev 3: 1874–1886PubMedGoogle Scholar
  56. Ghattas IR, Sanes JS, Majors JE (1991) The encephalomyocarditis virus internal entry site allows efficient coexpression of two genes from a recombinant provirus in cultured cells and in embryos. Mol Cell Biol 11: 5848–5859PubMedGoogle Scholar
  57. Ghetti A, Pinol-Roma S, Michael WM, Morandi C, Dreyfuss G (1992) hnRNP I, the polypyrimidine tract- binding protein: distinct nuclear localization and association with hnRNAs. Nucleic Acids Res. 20: 3671–3678PubMedGoogle Scholar
  58. Gil A, Sharp PA, Jamison SF, Garcia-Blanco MA (1991) Characterization of cDNAs encoding the polypyrimidine tract-binding protein. Genes Dev 5: 1224–1236PubMedGoogle Scholar
  59. Glass MJ, Jia X-Y, Summers DF (1993) Identification of the hepatitis A virus internal ribosomal entry site: in vivo and in vitro analysis of bicistronic RNAs containing the HAV 5’ noncoding region. Virology 193: 842–852PubMedGoogle Scholar
  60. Golini F, Thach SS, Birge CH, Safer B, Merrick WC, Thach RE (1976) Competition between cellular and viral mRNAs in vitro is regulated by a messenger discriminatory initiation factor. Proc Natl Acad Sci USA 73:3040–3043PubMedGoogle Scholar
  61. Golini F, Nomoto A, Wimmer E (1978) The genome-linked protein of picornaviruses. IV. Difference in the VPg’s of encephalomyocarditis virus and poliovirus as evidence that the genome-linked proteins are virus-coded. Virology 89: 112–118Google Scholar
  62. Hackett PB, Egberts E, Traub P (1978) Selective translation of mengovirus RNA over host mRNA in homologous, fractionated, cell-free translational systems from Ehrlich-ascites-tumor cells. Eur J Biochem 83: 353–361PubMedGoogle Scholar
  63. Hellen CUT, Witherell GW, Schmid M, Shin SH, Pestova TV, Gil A, Wimmer E (1993) A cytoplasmic protein (p57) that is required for translation of picornavirus RNA by internal ribosomal entry is identical to the nuclear pyrimidine-tract-binding protein. Proc Natl Acad Sci USA 90: 7642–7646PubMedGoogle Scholar
  64. Hellen CUT, Pestova TV, Litterst M, Wimmer E (1994) The cellular polypeptide p57 (pyrimidine- tract binding protein) binds to multiple site in the poliovirus 5’ nontranslated region. J Virol 68: 941–950PubMedGoogle Scholar
  65. Hershey JWB (1991) Translational control in mammalian cells. Annu Rev Biochem 60: 717–755PubMedGoogle Scholar
  66. Hruby DE, Roberts WK (1978) Encephalomyocarditis virus RNA III. Presence of a genome-associated protein. J Virol 25: 413–415Google Scholar
  67. Hunt SL, Kaminski A, Jackson RJ (1993) The influence of viral coding sequences on the efficiency of internal initiation of translational of cardiovirus RNAs. Virology 197: 801–807PubMedGoogle Scholar
  68. Hyppia T, Horsnell C, Maaronen M, Khan M, Kalkkinen N, Auvinen P, Kinnunen L, Stanway G (1992) A distinct picornavirus group identified by sequence analysis. Proc Natl Acad Sci USA 89: 8847–4451Google Scholar
  69. Jackson RJ (1989) Comparison of encephalomyocarditis virus and poliovirus with respect to translation initiation and processing in vitro. In: Semler BL, Ehrenfeld E (eds) Molecular aspects of picornavirus infection and detection. American Society for Microbiology, WashingtonGoogle Scholar
  70. Jackson RJ (1990) Binding of Met-tRNA. In: Trachsel H(ed) Translation in eukaryotes. CRC Press, Boca Raton pp 193–242Google Scholar
  71. Jackson RJ (1991a) Potassium salts influence the fidelity of mRNA translation initiation in rabbit reticulocytes: unique features of encephalomyocarditis virus RNA translation. Biochem Biophys Acta 1088: 345–358PubMedGoogle Scholar
  72. Jackson RJ (1991b) The ATP requirement for initiation of eukaryotic translation varies according to the mRNA species. Eur J Biochem 200: 285–294PubMedGoogle Scholar
  73. Jackson RJ, Howell MT, Kaminski A (1990) The novel mechanism of initiation of picornavirus RNA translation. Trends Biochim Sci 15: 477–483Google Scholar
  74. Jacobson MF, Baltimore D (1968) Polypeptide cleavages in the formation of poliovirus polyproteins. Proc Natl Acad Sci USA 61: 77–84PubMedGoogle Scholar
  75. Jamison SF, Crow A, Garcia-Blanco MA (1992) The spliceosome assembly pathway in mammalian extracts. Mol Cell Biol 12: 4279–4287PubMedGoogle Scholar
  76. Jang SK (1989) Translation of picornaviral mRNAs: initiation of protein synthesis by internal entry of ribosomes into the 5’ nontranslated region of picornavirus mRNAs. PhD thesis, State University of New York, Stony BrookGoogle Scholar
  77. Jang SK, Wimmer E (1990) 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 4: 1560–1572PubMedGoogle Scholar
  78. Jang SK, Krausslich H-G, Nicklin MJH, Duke GM, Palmenberg AC, Wimmer E (1988) A segment of the 5’ nontranslated region of encephalomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation. J Virol 62: 2636–2643PubMedGoogle Scholar
  79. Jang SK, Davies MV, Kaufman RJ, Wimmer E (1989) Initiation of protein synthesis by internal entry of ribosomes into the 5’ nontranslated region of encephalomyocarditis virus RNA in vivo. J Virol 63: 1651–1660PubMedGoogle Scholar
  80. Jang SK, Pestova TV, Hellen CUT, Witherell GW, Wimmer E (1990) Cap-independent translation of picornavirus RNAs: structure and function of the internal ribosomal entry site. Enzyme 44: 292–309PubMedGoogle Scholar
  81. Jen G, Thach RE (1982) Inhibition of host translation in encephalomyocarditis virus-infected L cells: a novel mechanism. J Virol 43: 250–261PubMedGoogle Scholar
  82. Jen G, Birge CH, Thach RE (1978) Comparison of initiation rates of encephalomyocarditis virus and host protein synthesis in infected cells. J Virol 27: 640–647PubMedGoogle Scholar
  83. Jen G, Detjen BM, Thach RE (1980) Shutoff of HeLa cell protein synthesis by encephalomyocarditis virus and poliovirus: a comparative study. J Virol 35: 150–156PubMedGoogle Scholar
  84. Kaminski A, Howell MT, Jackson RJ (1990) Initiation of encephalomyocarditis virus RNA translation: the authentic initiation site is not selected by a scanning mechanism. EMBO J 9: 3753–3759PubMedGoogle Scholar
  85. Kaminski A, Belsham GJ, Jackson RJ (1994) Translation of encephalomyocarditis virus RNA: parameters influencing the selection of the internal initiation site. EMBO J 13: 1673–1681PubMedGoogle Scholar
  86. Kaufman RJ, Davies MV, Walsay LC, Michnick D (1991) Improved vectors for stable expression of foreign genes in mammalian cells by use of the untranslated leader sequence from EMC virus. Nucleic Acids. Res 19: 4485–4490Google Scholar
  87. Kenan DJ, Query CC, Keene J (1991) RNA recognition: towards identifying determinants of specificity. Trends Biochem Sci 16: 214–220PubMedGoogle Scholar
  88. Kim DG, Kang HM, Jang SK, Shin H-S (1992) Construction of a bifunctional mRNA in the mouse by using the internal ribosomal entry site of the encephalomyocarditis virus. Mol Cell Biol 12: 3636–3643PubMedGoogle Scholar
  89. Kong W-P, Roos RP (1991) Alternative translation initiation site in the DA strain of Theiler’s murine encephalomyocarditis virus. J Virol 65: 3395–3399PubMedGoogle Scholar
  90. Kozak M (1989) Structural features in eukaryotic mRNAs that modulate the efficiency of translation. J Biol Chem 266: 19867–19870Google Scholar
  91. Kozak M (1991) The scanning model for translation: an update. J Cell Biol 108: 229–241Google Scholar
  92. Kozak M (1992) A consideration of alternative models for the initiation of translation in eukaryotes Crit Rev Biochem Mol Biol 27: 385–402PubMedGoogle Scholar
  93. Kozak M (1994) Features in the 5’ non-coding sequences of rabbit a-and p-globin mRNAs that affect translational efficiency. J Mol Biol 235: 95–110PubMedGoogle Scholar
  94. Krausslich H-G, Nicklin MJH, Toyoda H, Etchison D, Wimmer E (1987) Poliovirus proteinase 2A induces cleavage of eukaryotic initiation factor 4F polypeptide p220. J Virol 61: 2711–2718PubMedGoogle Scholar
  95. Kuhn R, Luz N, Beck E (1990) Functional analysis of the internal initiation site of foot-and-mouth disease virus. J Virol 64: 4625–4631PubMedGoogle Scholar
  96. Laskey RA, Gurdon JB, Crawford LV (1972) Translation of encephalomyocarditis viral RNA in oocytes of Xenopus laevis. Proc Natl Acad Sci USA 69: 3665–3669PubMedGoogle Scholar
  97. Law KM, Brown TDK (1990) The complete nucleotide sequence of the GDVII strain of Theiler’s murine encephalomyocarditis virus (TMEV). Nucleic Acids Res 18: 6707Google Scholar
  98. Lawrence C, Thach RE (1974) Encephalomyocarditis virus infection of mouse plasmacytoma cells. I. Inhibition of cellular protein synthesis. J Virol 14: 598–610Google Scholar
  99. Le S-Y, Zuker M (1990) Common structures of the 5’ non-coding RNA in enteroviruses and rhinoviruses. Thermodynamical stability and statistical significance. J Mol Biol 216: 729–741Google Scholar
  100. Le S-Y, Chen J-H, Sonenberg N, Maizel JV (1993) Conserved tertiary structural elements in the 5’ nontranslated region of cardiovirus, aphthovirus and hepatitis A virus RNAs. Nucleic Acids Res 21: 2445–2451PubMedGoogle Scholar
  101. Luz N, Beck E (1990) A cellular 57 kDa protein binds to two regions of the internal translation initiation region of foot-and-mouth disease virus. FEBS Lett 269: 311–314PubMedGoogle Scholar
  102. Luz N, Beck E (1991) Interaction of a cellular 57-kilodalton protein with the internal translation initiation site of foot-and-mouth disease virus. J Virol 65: 6486–6494PubMedGoogle Scholar
  103. Martinez-Salas E, Saiz J-C, Davila M, Belsham GJ, Domingo E (1993) A single nucleotide substitution in the internal ribosome entry site of foot-and-mouth disease virus leads to enhanced cap-independent translation in vivo. J Virol 67: 3748–3755PubMedGoogle Scholar
  104. Mathews MB, Korner A (1970) Mammalian cell-free protein synthesis directed by viral ribonucleic acid. Eur J Biochem 17: 328–338PubMedGoogle Scholar
  105. Meerovitch K, Pelletier J, Sonenberg N (1989) A cellular protein that binds to the 5’-noncoding region of poliovirus RNA: implications for internal translation initiation. Genes Dev 3: 1026–1034PubMedGoogle Scholar
  106. Meerovitch K, Svitkin YV, Lee HS, Lejbkowicz F, Kenan DJ, Chan EKL, Agol VI, Keene JD, Sonenberg N (1993) La autoantigen enhances and corrects aberrant translation of poliovirus RNA in reticulocyte lysate. J Virol 67: 3798–3807PubMedGoogle Scholar
  107. Merrick WC (1992) Mechanism and regulation of eukaryotic protein synthesis. Microbiol Rev 56: 291–315PubMedGoogle Scholar
  108. Michaud S, Reed R, (1991) An ATP-independent complex commits pre-mRNA to the mammalian- spliceosome assembly pathway. Genes Dev 5: 2534–2546PubMedGoogle Scholar
  109. Mirochnitchenko O, Inouye S, Inouye M (1994) Production of a single-stranded DNA in mammalian cells by means of a bacterial retron. J Biol Chem 269: 2380–2383PubMedGoogle Scholar
  110. Molla A, Jang SK, Paul AV, Reuer Q, Wimmer E (1993) Cardioviral internal ribosomal entry site is functional in a genetically engineered dicistronic poliovirus. Nature 356: 255–257Google Scholar
  111. Molla A, Paul AV, Schmid M, Jang SK, Wimmer E (1994) Studies on dicistronic polioviruses implicate proteinase 2Apro in RNA replication. Virology 196: 739–747Google Scholar
  112. Moore M, Query C, Sharp PM (1993) Splicing of precursors to mRNAs by the spliceosome. In: Gestland RF, Atkins JF (eds) The RNA world. Cold Spring Harbor Laboratory Press, Plainview, pp 303–357Google Scholar
  113. Morgan RA, Couture L, Elroy-Stein O, Ragheb J, Moss B, Anderson WF (1992) Retroviral vectors containing putative internal ribosome entry sites: development of a polycistronic gene transfer system and applications to human gene therapy. Nucleic Acids Res 20: 1293–1299PubMedGoogle Scholar
  114. Mosenkis J, Daniels-McQueen S, Janovec S, Duncan R, Hershey JWB, Grifo JA, Merrick WC, Thach RE (1985) Shutoff of host translation by encephalomyocarditis virus infection does not involve cleavage of the eukaryotic initiation factor 4F polypeptide that accompanies poliovirus infection. J Virol 54: 43–645Google Scholar
  115. Mullen MP, Smith CW, Patton JG, Nadal-Ginard B (1991) oc-tropomyosin mutually exclusive exon selection: competition between barnchpoint/polyprimidine tract determines default exon choice. Genes Dev 5: 642–655PubMedGoogle Scholar
  116. Mulligan GJ, Guo W, Wormsley S, Helfman DM (1992) Polypyrimidine tract binding protein interacts with sequences involved in alternative splicing of p-tropomyosin pre-mRNA. J Biol Chem 267: 25480–25487PubMedGoogle Scholar
  117. Newton SE, Carroll AR, Campbell RO, Clarke BE, Rowlands DJ (1985) The sequence of foot-and-month disease virus RNA to the 5’side of the poly(C) tract. Gene 40: 331–336PubMedGoogle Scholar
  118. Nicholson R, Pelletier J, Le S-Y, Sonenberg N (1991) Structural and functional analysis of the ribosome landing pad of poliovirus type 2: in vivo translation studies. J Virol 65: 5886–5894PubMedGoogle Scholar
  119. Nietfeld W, Metzel H, Pieler T (1990) The Xenopus laevis poly(A) binding protein is composed of multiple functionally independent RNA binding domains. EMBO J 9:3699–3705PubMedGoogle Scholar
  120. Norton PA, Hynes RO (1993) Characterization of HeLa nuclear factors which interact with a conditionally processed rat fibronectin pre-mRNA. Biochem Biophys Res Commun 195: 215–221PubMedGoogle Scholar
  121. Ohara Y, Stein S, Lu J, Stillman L, Klaman L, Roos R (1988) Molecular cloning and sequence determination of DA strain of Theiler’s murine encephalomyocarditis viruses. Virology 164: 245–255PubMedGoogle Scholar
  122. Oudshoorn P, Thomas A, Scheper G, Voorma HO (1990) An initiation signal in the 5’untranslated leader sequence of encephalomyocarditis virus RNA. Biochim Biophys Acta 1050: 124–128PubMedGoogle Scholar
  123. Palmenberg AC (1989) Sequence alignments of picornaviral capsid proteins. In: Semler BL, Ehrenfeld E (eds) Molecular aspects of picornavirus infection and detection. American Society for Microbiology, WashingtonGoogle Scholar
  124. Palmenberg AC, Duke GM (1993) The genomic sequence of mengovirus and its relationship to other cardioviruses. Genebank, no L22089Google Scholar
  125. Palmenberg AC, Kirby EM, Janda MR, Drake NL, Duke GM, Potratz KF, Collett MS (1984) The nucleotide and deduced amino acid sequences of the encephalomyocarditis viral polyprotein coding region. Nucleic Acids Res. 12:2969–2985PubMedGoogle Scholar
  126. Parks GD, Duke GM, Palmenberg AC (1986) Encephalomyocarditis 3C protease: efficient cell- free expression from clones which link viral 5’ noncoding sequences to the P3 region. J Virol 60: 376–384PubMedGoogle Scholar
  127. Patton JG, Meyer SA, Tempst P, Nadal-Ginard B (1991) Characterization and molecular cloning of polypyrimidine tract-binding protein: a component of a complex necessary for pre-mRNA splicing. Genes Dev.5: 1237–1251PubMedGoogle Scholar
  128. Patton JG, Porro EB, Galceran J, Tempst P, Nadal-Ginard B (1993) Cloning and characterization of PSF, a novel pre-mRNA splicing factor. Genes Dev.7: 393–406PubMedGoogle Scholar
  129. Pause A, Methot N, Svitkin Y, Merrick WC, Sonenberg N (1994) Dominant negative mutants of mammalian translation initiation factor elF-4A define a critical role for elF-4F in cap-dependent and cap-independent initiation of translation. EMBO J 13: 1205–1215PubMedGoogle Scholar
  130. Pelham HRB (1978) Translation of encephalomyocarditis virus RNA in vitro yields an active proteolytic processing enzyme. Eur J Biochem 85:457–462PubMedGoogle Scholar
  131. Pelham HRB, Jackson RJ (1976) An efficient mRNA-dependent translation system from reticulocyte lysates Eur J Biochem 67:247–256PubMedGoogle Scholar
  132. Pelletier J, Sonenberg N (1988) Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature 334: 320–325PubMedGoogle Scholar
  133. Pelletier J, Kaplan G, Racaniello VR, Sonenberg N (1988) Translational efficiency of poliovirus mRNA: mapping of inhibitory cis-acting element within the 5’ noncoding region. J Virol 62: 2219–2227PubMedGoogle Scholar
  134. Perez-Bercoff R, Gander M (1978) In vitro translation of mengovirus RNA deprived of the terminally- linked (capping?) protein. FEBS Lett 96: 306–312PubMedGoogle Scholar
  135. Perez-Bercoff R, Kaempfer R (1982) Genomic RNA of mengovirus. V. Recognition of common features by ribosomes and eucaryotic initiation factor 2. J Virol 41: 30–41PubMedGoogle Scholar
  136. Pestova TV, Hellen CUT, Wimmer E (1991) 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 J Virol 65: 6194–6204PubMedGoogle Scholar
  137. Pestova TV, Hellen CUT, Wimmer E (1994) A conserved AUG triplet in the 5’ nontranslated region of poliovirus can function as an initiation codon in vitro and in vivo. Virology 204: 729–737PubMedGoogle Scholar
  138. Pevear DC, Calenoff M, Rozhon E, Lipton HL (1987) Analysis of the complete nucleotide sequence of the picornavirus Theiler’s murine encephalomyocarditis virus indicates that it is closely related to cardioviruses. J Virol 61: 1507–1516PubMedGoogle Scholar
  139. Pilipenko EV, Blinov VM, Chernov BK, Dimitrieva TM, Agol VI (1989) Conservation of the secondary structure elements of the 5’-untranslated region of cardio- and aphthovirus RNAs. Nucl Acids Res 17: 5701–5711PubMedGoogle Scholar
  140. Pilipenko EV, Gmyl AP, Maslova SV, Belov GA, Singakov AN, Huang M, Brown TDK, Agol VI (1994) Starting window, a distinct element in the cap-independent internal initiation of translation on picornaviral RNA. J Mol Biol 241: 398–414PubMedGoogle Scholar
  141. Porter A, Carey N, Fellner P (1974) Presence of a larger poly(rC) tract within the RNA of encephalomyocarditis virus. Nature 243: 675–678Google Scholar
  142. Poyry T, Kinnunen L, Hovi T (1992) Genetic variation in vivo and proposed functional domains of the 5’ noncoding region of poliovirus RNA. J Virol 66: 5313–5319PubMedGoogle Scholar
  143. Pritchard AE, Calenoff MA, Simpson S, Jensen K, Lipton HL (1992) A single base deletion in the 5’ noncoding region of Theiler’s virus attenuates neurovirulence. J Virol 66: 1951–1958PubMedGoogle Scholar
  144. Rivera VM, Walsh JD, Maizel JV (1988) Comparative sequence analysis of the 51 noncoding region of enteroviruses and rhinoviruses. Virology 185: 42–50Google Scholar
  145. Rosen H, Di Segni G, Kaempfer R (1982) Translational control by messenger RNA competition for eukaryotic initiation factor 2. J Biol Chem 257: 946–952PubMedGoogle Scholar
  146. Sangar DV, Black DN, Rowlands DJ, Harris TJR, Brown F (1980) Location of the initiation site for protein synthesis on foot-and-mouth disease virus RNA by in vitro translation of defined fragments of the RNA. J Virol 33: 59–68PubMedGoogle Scholar
  147. Sangar DV, Newton SE, Rowlands DJ, Clarke BE (1987) All foot and mouth disease virus serotypes initiate protein synthesis at two separate AUGs. Nucl Acids Res 15: 3305–3315PubMedGoogle Scholar
  148. Sankar S, Cheah K-C, Porter AG (1989) Antisense oligonucleotide inhibition of encephalomyocarditis virus RNA translation. Eur J Biochem 184: 465–480Google Scholar
  149. Scheper GC, Thomas AAM, Voorma HO (1991) The 5’ untranslated region of encephalomyocarditis virus contains a sequence for very efficient binding of eukaryotic initiation factor elF2/2B. Biochem Biophys Acta 1089: 220–226PubMedGoogle Scholar
  150. Scheper GC, Voorma HO, Thomas AAM (1992) Eukaryotic initiation factors-4E and-4F stimulate 5’ cap- dependent as well as internal initiation of protein synthesis. J Biol Chem 267: 7269–7274PubMedGoogle Scholar
  151. Shih DS, Park I-W, Evans CL, Jaynes JM, Palmenberg AC (1987) Effects of cDNA hybridization on translation of encephalomyocarditis virus RNA. J Virol 61: 233–2037Google Scholar
  152. Smith AE (1973) The initiation of protein synthesis directed by the RNA from encephalomyocarditis virus. Eur J Biochem 33: 301–313PubMedGoogle Scholar
  153. Smith AE, Marcker KA (1970) Cytoplasmic methionine transfer RNAs from eukaryotes. Nature 226: 607–610PubMedGoogle Scholar
  154. Sonenberg N (1987) Regulation of translation of poliovirus. Adv Virus Res 33: 175–204.PubMedGoogle Scholar
  155. Sonenberg N, Trachsel H, Hecht S, Shatkin AJ (1980) Differential stimulation of capped mRNA translation in vitro by cap binding protein. Nature 285: 331–333PubMedGoogle Scholar
  156. Sosnovtsev SV, Onischenko AM, Petrov NA, Kalashnikova Tl, Mamaeva NV, Drygin VY, Perevozchikova NA, Vasilenko SK (1993) Sequence of the L fragment of foot-and-mouth disease virus A strain A22/550 Azerbaijan 65. Genbank, no.X74812Google Scholar
  157. Stanway G (1990) Structure, function, and evolution of picornaviruses. J Gen Virol 71: 2483–2501PubMedGoogle Scholar
  158. Svitkin YV, Agol VI (1978) Complete translation of encephalomyocarditis virus RNA and faithful cleavage of virus-specific proteins in a cell-free system from Krebs-2 cells. FEBS Lett 87: 7–11PubMedGoogle Scholar
  159. Svitkin YV, Pestova TV, Maslova SV, Agol VI (1988) Point mutations modify the response of poliovirus RNA to a translation initiation factor: a comparison of neurovirulent and attenuated strains. Virology 166: 394–404PubMedGoogle Scholar
  160. Svitkin YV, Meerovitch K, Lee HS, Dholakia JN, Kenan DJ, Agol VI, Sonenberg N (1994) Internal translation initiation on poliovirus RNA: further characterization of La function in poliovirus translation in vitro J Virol 68: 1544–1550PubMedGoogle Scholar
  161. Tesar M, Harmon SA, Summers DF, Ehrenfeld E (1991) Hepatitis A virus polyprotein synthesis initiates from two alternative AUG codons. Virology 186: 609–618Google Scholar
  162. Trachsel H (ed) (1991) Translation in eukaryotes. Telford, CaldwellGoogle Scholar
  163. Tsukiyama-Kohara K, Iizuka N, Kohara M, Nomoto A (1992) Internal ribosome entry site within hepatitis C virus RNA. J Virol 66: 1476–1483PubMedGoogle Scholar
  164. Ugarova TY (1987) Primary structure of mRNA and the translation strategy of eukaryotes Mol Biol 21: 888–914Google Scholar
  165. Ugarova TY, Siyanova EY, Svitkin YV, Kazachkov YA, Baratova LA, Agol VI (1984) Partial N-terminal amino acid sequences of polypeptides p14 and p12 of encephalomyocarditis virus are identical and correspond to the N-terminus of the polyprotein. FEBS Lett 170: 339–342PubMedGoogle Scholar
  166. Vartapetian AB, Drygin YF, Chumakov KM, Bogdanov AA (1980) The structure of the covalent linkage between proteins and RNA in encephalomyocarditis virus. Nucleic Acid Res 8: 3729–3742PubMedGoogle Scholar
  167. Vartapetian AB, Mankin AS, Skripkin EA, Chumakov KM, Smirnov VD, Bogdanov AA (1983) The primary and secondary structure of the 5’-end region of encephalomyocarditis virus RNA. A novel approach to sequencing long RNA molecules. Gene 26: 189–195Google Scholar
  168. Vennema H, Rijnbrand R, Heijnen L, Horzinek MC, Spaan WJM (1991) Enhancement of the vaccinia virus/phage T7 RNA polymerase expression system using encephalomyocarditis virus 5’-un- translated region sequences. Gene 108: 201–210PubMedGoogle Scholar
  169. Villa-Komaroff L, Guttman N, Baltimore D, Lodish H (1975) Complete translation of poliovirus RNA in a eukaryotic cell-free system. Proc Natl Acad Sci USA 83: 2330–2334Google Scholar
  170. Wigle DT (1973) Purification of a messenger-specific initiation factor from ascites-cell supernatant. Eur J Biochem 35: 11–17PubMedGoogle Scholar
  171. Wigle DT, Smith AE (1973) Specificity in initiation in a fractionated mammalian cell-free system. Nature New Biol 242: 136–140PubMedGoogle Scholar
  172. Wimmer E (1982) Genome-linked proteins of viruses. Cell 28: 199–201PubMedGoogle Scholar
  173. Wimmer E, Hellen CUT, Cao X (1993) Genetics of poliovirus. Annu Rev Genet 27: 353–435PubMedGoogle Scholar
  174. Wimmer E, Murdin AD (1991) Hepatitis A virus and the molecular biology of picornaviruses: a case for a new genus of the family picornaviridae. In: Hollinger FB, Lemon SM, Margolis HS (eds) Viral hepatitis and liver disease. Williams and Wilkins, BaltimoreGoogle Scholar
  175. Witherell GW, Gil A, Wimmer E (1993) Interaction of polypyrimidine tract binding protein with the encephalomyocarditis virus mRNA internal ribosomal entry site. Biochemistry 32: 8268–8275PubMedGoogle Scholar
  176. Witherell GW, Wimmer E (1994) Encephalomyocarditis virus internal ribosomal entry site RNA-protein interactions. J Virol 68: 3183–3192PubMedGoogle Scholar
  177. Witherell GW, Wimmer E (1993) Cap-independent translation of picornavirus mRNAs. In: Doefler W, Bom P (eds) Virus strategies. Molecular biology and pathogenesis VCH, Weinheim, pp 237–248Google Scholar
  178. Wood CR, Morris GE, Alderman EM, Fouser L, Kaufman RJ (1991) An internal ribosome binding site can be used to select for homologous recombinants at an immunoglobulin heavy-chain locus. Proc Natl Acad Sci USA 88: 8006–8010PubMedGoogle Scholar
  179. Zhou Y, Giordano TJ, Durbin RK, McAllister WT (1990) Synthesis of functional mRNA in mammalian cells by bacteriophage T3 RNA polymerase. Mol Cell Biol 10: 4529–4537PubMedGoogle Scholar
  180. Zimmerman A, Nelsen-Salz B, Kruppenbacher JP, Eggers HJ (1994) The complete nucleotide sequence and construction of an infectious cDNA clone of a highly virulent encephalomyocarditis virus. Virology 203: 366–372Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1995

Authors and Affiliations

  • C. U. T. Hellen
    • 1
  • E. Wimmer
    • 2
  1. 1.Department of Microbiology and ImmunologySUNY Health Sciences Center at BrooklynBrooklynUSA
  2. 2.Department of MicrobiologyState University of New York at Stony BrookBrooklynUSA

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