Translation and Replication of FMDV RNA

  • G. J. Belsham
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 288)

Abstract

Foot-and-mouth disease virus (FMDV) RNA is infectious. After delivery of the RNA (about 8.3 kb) into the cytoplasm of a cell, the RNA must initially be translated to produce the viral proteins required for RNA replication and for the packaging of the RNA into new virions. Subsequently there has to be a switch in the function of the RNA; translation has to be stopped to permit RNA replication. The signals required for the control of the different roles of viral RNA must be included within the viral RNA sequence. Many cellular proteins interact with the viral RNA and probably also with the virus-encoded proteins. The functions of different RNA elements within the viral RNA and the various virus-encoded proteins in determining the efficiency of virus replication are discussed. Unique aspects of FMDV RNA translation and replication are emphasised.

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References

  1. Abrams C., King A.M.Q. and Belsham G.J. 1995. Assembly of foot-and-mouth disease virus empty capsids synthesized by a vaccinia virus expression system. J. Gen. Virol. 76:3089–3098PubMedGoogle Scholar
  2. Ali, I.K., McKendrick, L., Morley, S.J. and Jackson, R.J. 2001. Activity of the Hepatitis A virus IRES requires association between the cap-binding translation initiation factor (eIF4E) and eIF4G. J. Virol. 75:7854–7863CrossRefPubMedGoogle Scholar
  3. Andino, R., Rieckhof, G.E. and Baltimore, D. 1990. A functional ribonucleoprotein complex forms around the 5’ end of poliovirus RNA. Cell 63:369–380CrossRefPubMedGoogle Scholar
  4. Belsham, G.J. and Bostock, C.J. 1988. Studies on the infectivity of foot-and-mouth disease virus RNA using microinjection. J. Gen. Virol. 69:265–274PubMedGoogle Scholar
  5. Belsham, G.J. and Brangwyn, J.K. 1990. A region of the 5’ non-coding region of foot-and-mouth disease virus RNA directs efficient internal initiation of protein synthesis within cells; interaction with the role of the L protease in translational control. J. Virol. 64:5389–5395PubMedGoogle Scholar
  6. Belsham, G.J. 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
  7. Belsham, G.J. and Sonenberg, N. 1996. RNA-protein interactions in regulation of picornavirus RNA translation. Microbiol. Rev. 60:499–511PubMedGoogle Scholar
  8. Belsham, G.J. and Jackson, R.J. 2000. Translation initiation on picornavirus RNA. In: ‘Translational Control of Gene Expression’ Monograph 39. Eds. N. Sonenberg, J.W.B. Hershey and M.B. Mathews. pp869–900. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NYGoogle Scholar
  9. Belsham, G.J. and Sonenberg, N. 2000. Picornavirus RNA translation: roles for cellular proteins. Trends Microbiol. 8:330–335CrossRefPubMedGoogle Scholar
  10. Belsham, G.J., McInerney, G.M. and Ross-Smith, N. 2000. Foot-and-mouth disease virus 3C protease induces cleavage of translation initiation factors eIF4A and eIF4G within infected cells. J. Virol. 74:272–280PubMedGoogle Scholar
  11. Bienz, K., Egger, D., and Pasamontes, L. 1987. Association of polioviral proteins of the P2 genomic region with the viral replication complex and virus-induced membrane synthesis as visualized by electron microscopic immunocytochemistry and autoradiography. Virology 160:220–226CrossRefPubMedGoogle Scholar
  12. Bienz, K., Egger, D., Troxler, M. and Pasamontes, L. 1990. Structural organization of poliovirus RNA replication is mediated by viral proteins of the P2 genomic region. J. Virol. 64:1156–1163PubMedGoogle Scholar
  13. Borman, A.M., Le Mercier, P., Girard, M. and Kean, K.M. 1997. Comparison of picornaviral IRES-driven internal initiation in cultured cells of different origins. Nucl. Acids Res. 25:925–932CrossRefPubMedGoogle Scholar
  14. Borman, A.M. and Kean, K.M. 1997. Intact eukaryotic initiation factor 4G is required for hepatitis A virus internal initiation of translation. Virology 237:129–136CrossRefPubMedGoogle Scholar
  15. Brown, F., Newman, J., Stott, J., Porter, A., Frisby, D., Newton, C., Carey, N. and Fellner, P. 1974. Poly(C) in animal viral RNAs. Nature (London) 251:342–344CrossRefPubMedGoogle Scholar
  16. Brown, E.A., Zajac, A.J. and Lemon, S.M. 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. 1994 68:1066–1074PubMedGoogle Scholar
  17. Brown, C.C., Piccone, M.E., Mason, P.W., McKenna, T.S.C. and Grubman, M.J. 1996. Pathogenesis of wild-type and leaderless foot-and-mouth disease virus in cattle. J. Virol. 70:5638–5641PubMedGoogle Scholar
  18. Cao, X.M., Bergmann, I.E., Fullkrug, R. and Beck, E. 1995. Functional analysis of the two alternative translation initiation sites of foot-and-mouth-disease virus. J. Virol. 69:560–563PubMedGoogle Scholar
  19. Chinsangaram, J., Piccone, M.E. and Grubman, M.J. 1999. Ability of foot-and-mouth disease virus to form plaques in cell culture is associated with suppression of α/β interferon. J. Virol. 73:9891–9898PubMedGoogle Scholar
  20. Chow, M., Newman, J.F.E., Filman, D., Hogle, J.M., Rowlands, D.J. and Brown, F. 1987. Myristylation of picornavirus capsid protein VP4 and its structural significance. Nature 327:482–486CrossRefPubMedGoogle Scholar
  21. Clarke, B.E., Brown, A.L., Currey, K.M., Newton, S.E., Rowlands, D.J. and Carroll, A.R. 1987. Potential secondary and tertiary structure in the genomic RNA of FMDV. Nucl. Acids Res. 15:7067–7079PubMedGoogle Scholar
  22. Costa, M. and Michel, F. 1995. Frequent use of the same tertiary motif by self-folding RNAs. EMBO J. 14:1276–1285PubMedGoogle Scholar
  23. Crawford, N.M. and Baltimore, D. 1983. Genome-linked protein VPg of poliovirus is present as free VPg and VPgpUpU in poliovirus-infected cells. Proc. Natl. Acad. Sci. USA. 80:7452–7455PubMedGoogle Scholar
  24. Curry, S., Abrams, C.C., Fry, E., Crowther, J.C., Belsham, G.J., Stuart, D.I. and King, A.M.Q. 1995. Viral RNA modulates the acid sensitivity of foot-and-mouth disease virus capsids. J. Virol. 69:430–438PubMedGoogle Scholar
  25. Devaney, M.A., Vakharia, V.N., Lloyd, R.E., Ehrenfeld, E. and Grubman, M.J. 1988. Leader protein of foot-and-mouth-disease virus is required for cleavage of the p220 component of the cap-binding protein complex. J. Virol. 62:4407–4409PubMedGoogle Scholar
  26. Doedens, J.R. and Kirkegaard, K. 1995. Inhibition of cellular protein secretion by poliovirus proteins 2B and 3A. EMBO J. 14:894–907PubMedGoogle Scholar
  27. Donnelly, M.L., Gani, D., Flint, M., Monaghan, S. and Ryan, M.D. 1997. The cleavage activities of aphthovirus and cardiovirus 2A proteins. J. Gen. Virol. 78:13–21PubMedGoogle Scholar
  28. Donnelly, M.L.L., Luke, G., Mehrotra, A., Li, X., Hughes, L.E., Gani, G. and Ryan, M.D. 2001. Analysis of the aphthovirus 2A/2B polyprotein ‘cleavage’ mechanism indicates not a proteolytic reaction, but a novel translational effect: a putative ribosomal 'skip'. J. Gen. Virol. 82:1013–1025PubMedGoogle Scholar
  29. Duke, G.M., Osorio, J.E. and Palmenberg, A.C. 1990. Attenuation of mengo-virus through genetic-engineering of the 5’ noncoding poly(C) tract. Nature 343:474–476CrossRefPubMedGoogle Scholar
  30. Duque, H. and Palmenberg, A.C. 2001. Phenotypic characterization of three phylogenetically conserved stem-loop motifs in the mengovirus 3’ untranslated region. J. Virol. 75:3111–3120CrossRefPubMedGoogle Scholar
  31. Escarmis, C., Toja, M., Medina, M. and Domingo, E. 1992. Modifications of the 5’ untranslated region of foot-and-mouth disease virus after prolonged persistence in cell culture. Virus Res. 26:113–125CrossRefPubMedGoogle Scholar
  32. Escarmis, C., Dopazo, J., Davila, M., Palma, E.L. and Domingo, E. 1995. Large deletions in the 5'-untranslated region of foot-and-mouth-disease virus of serotype-C. Virus Res. 35:155–167CrossRefPubMedGoogle Scholar
  33. Falk, M.M., Grigera, P.R., Bergmann, I.E., Zibert, A., Multhaup, G. and Beck, E. 1990. Foot-and-mouth-disease virus protease-3C induces specific proteolytic cleavage of host-cell histone-H3. J. Virol. 64:748–756PubMedGoogle Scholar
  34. Fernandez-Miragall, O. and Martinez-Salas, F. 2003. Structured organization of a viral IRES depends on the integrity of the GNRA motif. RNA 9:1333–1344CrossRefPubMedGoogle Scholar
  35. Falk, M.M., Sobrino, F. and Beck, E. 1992. VPg-gene amplification correlates with infective particle formation in foot-and-mouth-disease virus J. Virol. 66:2251–2260Google Scholar
  36. Gamarnik, A.V. and Andino, R.. 1997. Two functional complexes formed by KH domain containing proteins with the 5’ noncoding region of poliovirus RNA. RNA 3:882–892PubMedGoogle Scholar
  37. Gamarnik, A.V. and Andino, R. 1998. Switch from translation to RNA replication in a positive-stranded RNA virus. Genes Dev. 12:2293–2304PubMedGoogle Scholar
  38. Gerber, K., Wimmer, E. and Paul, A.V. 2001. Biochemical and genetic studies of the initiation of human rhinovirus 2 RNA replication: identification of a cis-replicating element in the coding sequence of 2Apro. J Virol. 75:10979–10990CrossRefPubMedGoogle Scholar
  39. Gingras, A.C., Raught, B. and Sonenberg, N. 1999. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu. Rev. Biochem. 68:913–963CrossRefPubMedGoogle Scholar
  40. Glaser, W., Cencic, R. and Skern, T. 2001. Foot-and-mouth disease virus Leader proteinase: involvement of C-terminal residues in self-processing and cleavage of eIF4GI. J. Biol. Chem. 276:35473–35481CrossRefPubMedGoogle Scholar
  41. Goodfellow, I., Chaudhry, Y., Richardson, A., Meredith, J., Almond, J.W., Barclay, W. and Evans, D.J. 2000. Identification of a cis-acting replication element within the poliovirus coding region. J. Virol. 74:4590–4600CrossRefPubMedGoogle Scholar
  42. Gradi, A., Imataka, H., Svitkin, Y.V., Rom, E., Raught, B., Morino, S. and Sonenberg, N. 1998. A novel functional human eukaryotic translation initiation factor 4G. Mol. Cell. Biol. 18:334–342PubMedGoogle Scholar
  43. Gradi, A., Foeger, N., Strong, R., Svitkin, Y.V., Sonenberg, N., Skern, T., and Belsham, G.J. 2004. Cleavage of enkaryotic translation initiation factor 4GII within foot-and-mouth disease virus-effected cells: identification of the L-protease cleavage site in vitro. J. Virol. 78:3271–3278CrossRefPubMedGoogle Scholar
  44. Grubman, M.J., Zellner, M., Bablanian, G., Mason, P.W. and Piccone, M.E. 1995. Identification of the active-site residues of the 3C proteinase of foot-and-mouth-disease virus. Virology 213:581–589CrossRefPubMedGoogle Scholar
  45. Guarne, A., Tormo, J., Kirchweger, R., Pfistermueller, D., Fita, I. and Skern, T. 1998. Structure of the foot-and-mouth disease virus leader protease: a papain-like fold adapted for self-processing and eIF4G recognition. EMBO J. 17:7469–7479CrossRefPubMedGoogle Scholar
  46. Haghighat, A., Svitkin, Y., Novoa, I., Kuechler, E., Skern, T. and Sonenberg, N. 1996. The eIF4G-eIF4E complex is the target for direct cleavage by the rhinovirus 2A proteinase. J. Virol. 70:8444–8450PubMedGoogle Scholar
  47. Hahn, H. and Palmenberg. A.C. 1995. Encephalomyocarditis viruses with short poly(C) tracts are more virulent than their mengovirus counterparts. J. Virol. 69:2697–2699PubMedGoogle Scholar
  48. Hambidge, S.J. and Sarnow, P. 1992. Translational enhancement of the poliovirus 5’ noncoding region mediated by virus-encoded polypeptide 2A. Proc. Natl. Acad. Sci. USA. 89:10272–10276PubMedGoogle Scholar
  49. Harris, T.J.R. and Brown, F. 1977. Biochemical analysis of a virulent and an avirulent strain of foot-and-mouth disease virus. J. Gen. Virol. 34:87–105PubMedGoogle Scholar
  50. Herold, J. and Andino, R. 2001. Poliovirus RNA replication requires genome circularization through a protein-protein bridge. Mol. Cell 7:581–591CrossRefPubMedGoogle Scholar
  51. Hinton, T.M., Li, F. and Crabb, B.S. 2000. Internal ribosomal entry site-mediated translation initiation in equine rhinitis A virus: similarities to and differences from that of foot-and-mouth disease virus. J. Virol. 74:11708–11716CrossRefPubMedGoogle Scholar
  52. Hinton, T., Ross-Smith, N., Warner, S., Belsham, G.J. and Crabb, B. 2002. Conservation of L and 3C proteinase activities across distantly related aphthoviruses. J. Gen. Virol. 83:3111–3121PubMedGoogle Scholar
  53. Hobson, S.D., Rosenblum, E.S., Richards, O.C., Richmond, K., Kirkegaard, K., and Schultz S.C. 2001. Oligomeric structures of poliovirus polymerase are important for function. EMBO J 20:1153–1163CrossRefPubMedGoogle Scholar
  54. Imataka, H., Gradi, A. and Sonenberg N. 1998. A newly identified N-terminal amino acid sequence of human eIF4G binds poly(A)-binding protein and functions in poly(A)-dependent translation. EMBO J. 17:7480–7489CrossRefPubMedGoogle Scholar
  55. Irurzun, A., Perez, L. and Carrasco, L. 1992. Involvement of membrane traffic in the replication of poliovirus genomes: effects of brefeldin A. Virology 191:166–175CrossRefPubMedGoogle Scholar
  56. Jang, S.K., Krausslich, H.G., Nicklin, M.J., Duke, G.M., Palmenberg, A.C. and Wimmer, E. 1998. A segment of the 5’ nontranslated region of encephalomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation. J. Virol. 62:2636–2643Google Scholar
  57. Kaku, Y., Chard, L.S., Inoue, T. and Belsham, G.J. 2002. Unique characteristics of a picornavirus internal ribosome entry site from the Porcine Teschovirus-1 Talfan. J. Virol. 76:11721–11728CrossRefPubMedGoogle Scholar
  58. Kaminski, A., Howell, M.T. and Jackson, R.J. 1990. Initiation of encephalomyocarditis virus RNA translation: the authentic initiation site is not selected by a scanning mechanism. EMBO J. 9:3753–3759PubMedGoogle Scholar
  59. Kaminski, A., Belsham, G.J. and Jackson, R.J. 1994. Translation of encephalomyocarditis virus RNA: parameters influencing the selection of the internal initiation site. EMBO J. 13:1673–1681PubMedGoogle Scholar
  60. Kaminski, A. and Jackson, R.J. 1998. The polypyrimidine tract binding protein (PTB) requirement for internal initiation of translation of cardiovirus RNAs is conditional rather than absolute. RNA 4:626–638CrossRefPubMedGoogle Scholar
  61. King, A.M.Q., Sangar, D.V., Harris, T.J.R. and Brown F. 1980. Heterogeneity of the genome-linked protein of FMDV. J. Virol. 34:627–634PubMedGoogle Scholar
  62. Kirchweger, R., Ziegler, E., Lamphear, B.J., Waters, D., Liebig, H.D., Sommergruber, W., Sobrino, F., Hohenadl, C., Blaas, D., Rhoads, R.E. and Skern, T. 1994. Foot-and-mouth disease virus leader proteinase: purification of the Lb form and determination of its cleavage site on eIF-4γ. J. Virol. 61:2711–2718Google Scholar
  63. Kolupaeva, V.G., Hellen, C.U.T. and Shatsky, I.N. 1996. Structural analysis of the interaction of the pyrimidine tract-binding protein with the internal ribosomal entry site of encephalomyocarditis virus and foot-and-mouth disease virus RNAs. RNA 2:1199–1212PubMedGoogle Scholar
  64. Kolupaeva, V.G., Pestova, T.V., Hellen, C.U.T. and Shatsky I.N. 1998. Translation eukaryotic initiation factor 4G recognizes a specific structural element within the internal ribosome entry site of encephalomyocarditis virus RNA. J. Biol. Chem. 273:18599–18604CrossRefPubMedGoogle Scholar
  65. Kozak, M. 1989. The scanning model for translation: an update. J. Cell Biol. 108:229–241CrossRefPubMedGoogle Scholar
  66. Kuhn, R., Luz, N. and Beck, E. 1990. Functional analysis of the internal translation initiation site of foot-and-mouth disease virus. J. Virol. 64:4625–4631PubMedGoogle Scholar
  67. Lamphear, B.J., Yan, R.Q., Yang, F., Waters, D., Liebig, H.D., Klump, H., Kuechler, E., Skern, T. and R.E. Rhoads. 1993. Mapping the cleavage site in protein synthesis initiation factor eIF-4γ of the 2A proteases from human coxsackievirus and rhinovirus. J. Biol. Chem. 268:19200–19203PubMedGoogle Scholar
  68. Li, W., Ross-Smith, N., Proud, C.G. and Belsham, G.J. 2001. Cleavage of translation initiation factor 4AI (eIF4AI) but not eIF4AII by foot-and-mouth disease virus 3C protease: determination of the eIF4AI cleavage site. FEBS Lett. 507:1–5CrossRefPubMedGoogle Scholar
  69. López de Quinto, S. and Martínez-Salas, E. 1997. Conserved structural motifs located in distal loops of aphthovirus internal ribosome entry site domain 3 are required for internal initiation of translation. J. Virol. 71:4171–4175PubMedGoogle Scholar
  70. López de Quinto, S. and Martinez-Salas, E. 1999. Involvement of the aphthovirus RNA region located between the two functional AUGs in start codon selection. Virology 255:324–336CrossRefPubMedGoogle Scholar
  71. López de Quinto, S. and Martínez-Salas, E. 2000. Interaction of the eIF4G initiation factor with the aphthovirus IRES is essential for internal translation initiation in vivo. RNA 6:1380–1392CrossRefPubMedGoogle Scholar
  72. López de Quinto, S., Lafuente, E. and Martínez-Salas, E. 2001. IRES interaction with translation initiation factors: functional characterization of novel RNA contacts with eIF3, eIF4B, and eIF4GII. RNA 7:1213–1226CrossRefPubMedGoogle Scholar
  73. López de Quinto, S., Saiz, M., de la Morena, D., Sobrino, F. and Martínez-Salas, E. 2002. IRES-driven translation is stimulated separately by the FMDV 3’ NCR and poly(A) sequences. Nucl. Acids Res. 30:4398–4405CrossRefPubMedGoogle Scholar
  74. Martin, L.R. and Palmenberg, A.C. 1996. Tandem mengovirus 5’ pseudoknots are linked to viral RNA synthesis, not poly(C)-mediated virulence. J. Virol. 70:8182–8186PubMedGoogle Scholar
  75. Mason, P.W., Bezborodova, S.V. and Henry, T.M. 2002. Identification and characterization of a cis-acting replication element (cre) adjacent to the IRES of foot-and-mouth disease virus. J. Virol. 76:9686–9694CrossRefPubMedGoogle Scholar
  76. Maynell, L. A., Kirkegaard, K. and Klymkowsky, M.W. 1992. Inhibition of poliovirus RNA synthesis by brefeldin A. J. Virol. 66:1985–1994PubMedGoogle Scholar
  77. McKnight, K.L. and Lemon. S.M. 1996. Capsid coding sequence is required for efficient replication of human rhinovirus-14 RNA. J. Virol. 70:1941–1952PubMedGoogle Scholar
  78. McKnight, K. L. and Lemon, S.M. 1998. The rhinovirus type 14 genome contains and internally located RNA structure that is required for viral replication. RNA 4:1569–1584CrossRefPubMedGoogle Scholar
  79. Medina, M., Domingo, E., Brangwyn, J.K. and Belsham, G.J. 1993. The two species of the foot-and-mouth disease virus leader protein, expressed individually, exhibit the same activities. Virology 194:355–359CrossRefPubMedGoogle Scholar
  80. Meerovitch, K. and Sonenberg, N. 1993. Internal initiation of picornavirus RNA translation. Semin. Virol. 4:217–227CrossRefGoogle Scholar
  81. Meyer, K., Petersen, A., Niepmann, M. and Beck, E. 1995. Interaction of eukaryotic initiation factor eIF-4B with a picornavirus internal translation initiation site. J. Virol. 69:2819–2824PubMedGoogle Scholar
  82. Miller, L.C., Blakemore, W., Sheppard, D., Atakilit, A., King, A.M.Q. and Jackson, T. 2001. Role of the cytoplasmic domain of the β-subunit of integrin αvβ6 in infection by foot-and-mouth disease virus. J. Virol. 75:4158–4164CrossRefPubMedGoogle Scholar
  83. Molla, A., Paul, A.V. and Wimmer E. 1991. Cell-free, de novo synthesis of poliovirus. Science 254:1647–1651PubMedGoogle Scholar
  84. Murray, K.E., Roberts, A.W. and Barton, D.J. 2001. Poly(rC) binding proteins mediate poliovirus mRNA stability. RNA 7:1126–1141CrossRefPubMedGoogle Scholar
  85. Niepmann, M., Petersen, A., Meyer, K. and Beck, E. 1997. Functional involvement of polypyrimidine tract-binding protein in translation initiation complexes with the internal ribosome entry site of foot-and-mouth disease virus. J. Virol. 71:8330–8339PubMedGoogle Scholar
  86. O'Donnell, V.K., Pacheco, J.M., Henry, T.M. and Mason, P.W. 2001. Subcellular distribution of the foot-and-mouth disease virus 3A protein in cells infected with viruses encoding wild-type and bovine-attenuated forms of 3A. Virology 287:151–162CrossRefPubMedGoogle Scholar
  87. Ohlmann, T., Pain, V.M., Wood, W., Rau, M. and Morley, S.J. 1997. The proteolytic cleavage of eukaryotic initiation factor (eIF) 4G is prevented by eIF4E binding protein (PHAS-I; 4E-BP1) in the reticulocyte lysate. EMBO J. 16:844–855CrossRefPubMedGoogle Scholar
  88. Ohlmann T. and Jackson, R.J. 1999. The properties of chimeric picornavirus IRESes show that discrimination between internal translation initiation sites is influenced by the identity of the IRES and not just the context of the AUG codon. RNA 5:764–778CrossRefPubMedGoogle Scholar
  89. Parsley, T.B., Towner, J.S., Blyn, L.B., Ehrenfeld, E. and Semler, BL. 1997. Poly (rC) binding protein 2 forms a ternary complex with the 5'-terminal sequences of poliovirus RNA and the viral 3CD proteinase. RNA 3:1124–1134PubMedGoogle Scholar
  90. Pata, J.D., Schultz, S.C. and Kirkegaard, K. 1995. Functional oligomerization of poliovirus RNA-dependent RNA-polymerase. RNA 1:466–477PubMedGoogle Scholar
  91. Paul, A.V., Rieder, E., Kim, D.W., van Boom, J.H. and Wimmer, E. 2000. Identification of an RNA hairpin in poliovirus RNA that serves as the primary template in the in vitro uridylylation of VPg. J. Virol. 74:10359–10370CrossRefPubMedGoogle Scholar
  92. Pause, A., Belsham, G.J., Gingras, A-C., Donze, O., Lin, T-A., Lawrence, J.C. Jr. and Sonenberg, N. 1994a. Insulin dependent stimulation of protein synthesis by phosphorylation of a novel regulator of 5'-cap function. Nature (London) 371:762–767CrossRefPubMedGoogle Scholar
  93. Pause, A., Methot, N., Svitkin, Y.V., Merrick, W.C. and Sonenberg. 1994b. Dominant negative mutants of mammalian translation initiation factor eIF-4A define a critical role for eIF-4F in cap-dependent and cap-independent initiation of translation. EMBO J. 13:1205–1215PubMedGoogle Scholar
  94. Pelletier, J., and Sonenberg, N. 1998. Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature (London) 334:320–325CrossRefGoogle Scholar
  95. Pestova, T.V., Hellen, C.U.T. and Shatsky, I.N. 1996. Canonical eukaryotic initiation factors determine initiation of translation by internal ribosomal entry. Mol. Cell. Biol. 16:6859–6869PubMedGoogle Scholar
  96. Piccone, M.E., Rieder, E., Mason, P.W. and Grubman, M.J. 1995a. The foot-and-mouth-disease virus leader proteinase gene is not required for viral replication. J. Virol. 69:5376–5382PubMedGoogle Scholar
  97. Piccone, M.E., Zellner, M., Kumosinski, T.F., Mason, P.W. and Grubman, M.J. 1995b. Identification of the active-site residues of the L-proteinase of foot-and-mouth-disease virus. J. Virol. 69:4950–4956PubMedGoogle Scholar
  98. Pilipenko, E.V., Blinov, V.M., Chernov, B.K., Dmitrieva, T.M. and Agol, V.I. 1989. Conservation of the secondary structure elements of the 5'-untranslated region of cardiovirus and aphthovirus RNAs. Nucl. Acids Res. 17:5701–5711PubMedGoogle Scholar
  99. Pilipenko, E.V., Pestova, T.V., Kolupaeva, V.G., Khitrina, E.V., Poperechnaya, A.N., Agol, V.I. and Hellen, C.U.T. 2000. A cell cycle-dependent protein serves as a template-specific translation initiation factor. Gen. Dev. 14:2028–2045Google Scholar
  100. Pisarev,. A.Y., Charch, L.S., Kaku, Y., Johns, H.L., Shatsky, I.N., and Belsham, G.J. 2004. Functional and structural similarities between the internal ribosome entry sites of hepatitis C virus and porcine teschovirus, a picornavirus. J. Virol. 78:4487–4497CrossRefPubMedGoogle Scholar
  101. Poyry, T.A.A., Hentze, M.W. and Jackson, R.J. 2001. Construction of regulatable picornavirus IRESes as a test of current models of the mechanism of internal translation initiation. RNA 7:647–660CrossRefPubMedGoogle Scholar
  102. Ramos, R. and Martínez-Salas, E. 1999. Long-range RNA interactions between structural domains of the aphthovirus internal ribosome entry site (IRES). RNA 5:1374–1383CrossRefPubMedGoogle Scholar
  103. Rieder, E., Bunch, T., Brown, F. and Mason, P.W. 1993. Genetically-engineered foot-and-mouth-disease viruses with poly(C) tracts of 2 nucleotides are virulent in mice. J. Virol. 67:5139–5145PubMedGoogle Scholar
  104. Roberts, P. and Belsham, G.J. 1995. Identification of critical amino acids within the foot-and-mouth disease virus Leader protein, a cysteine protease. Virology 213:140–146CrossRefPubMedGoogle Scholar
  105. Roberts, L.O. and Belsham G.J. 1997. Complementation of defective picornavirus internal ribosome entry site (IRES) elements by the coexpression of fragments of the IRES. Virology 227:53–62CrossRefPubMedGoogle Scholar
  106. Roberts, L.O., Seamons, R.A. and Belsham, G.J. 1998. Recognition of picornavirus internal ribosome entry sites within cells; influence of cellular and viral proteins. RNA 4:520–529CrossRefPubMedGoogle Scholar
  107. Robertson, M.E., Seamons, R.A. and Belsham, G.J. 1999. A selection system for functional internal ribosome entry site (IRES) elements: analysis of the requirement for a conserved GNRA tetraloop in the encephalomyocarditis virus IRES. RNA 5:1167–1179CrossRefPubMedGoogle Scholar
  108. Saiz, M., Gomez, S., Martinez-Salas, E. and Sobrino, F. 2001. Deletion or substitution of the aphthovirus 3’ NCR abrogates infectivity and virus replication. J. Gen. Virol. 82:93–101PubMedGoogle Scholar
  109. Sakoda, Y., Ross-Smith, N., Inoue, T. and Belsham, G.J. 2001. An attenuating mutation in the 2A protease of swine vesicular disease virus, a picornavirus, regulates cap-and internal ribosome entry site-dependent protein synthesis. J Virol. 75, 10643–10650CrossRefPubMedGoogle Scholar
  110. Sangar, D.V., Newton, S.E., Rowlands, D.J. and Clarke, B.E. 1987. All foot and mouth disease serotypes initiate protein synthesis at two separate AUGs. Nucl. Acids Res. 15:3305–3315PubMedGoogle Scholar
  111. Saunders, K. and King, A.M.Q. 1982. Guanidine-resistant mutants of aphthovirus induce the synthesis of an altered non-structural polypeptide, p34. J. Virol. 42:389–394PubMedGoogle Scholar
  112. Spector, D.H. and Baltimore, D. 1974. Requirement of 3’ terminal polyadenylic acid for the infectivity of poliovirus RNA. Proc. Natl. Acad. Sci. USA 71:2983–2987PubMedGoogle Scholar
  113. Stassinopoulos, I.A. and Belsham, G.J. 2001. A novel protein-RNA binding assay: functional interactions of the foot-and-mouth disease virus internal ribosome entry site with cellular proteins. RNA 7:114–122CrossRefPubMedGoogle Scholar
  114. Strebel, K., and Beck, E. 1986. A second protease of foot-and-mouth-disease virus. J. Virol. 58:893–899PubMedGoogle Scholar
  115. Strong, R., and Belsham, G.J. 2004. Sequential modification of translation initiation factor elF4GI by two different foot-and-mouth disease protease within infected baby hamster kidney cells: identification of the 3epro cleavage site. J. Gen. Virol. 85 (in press)Google Scholar
  116. Svitkin, Y.V., Pause, A., Haghighat, A., Pyronnet, S., Witherell, G., Belsham, G.J. and Sonenberg, N. 2001a. The requirement for eukaryotic initiation factor 4A (eIF4A) in translation is directly proportional to the degree of mRNA 5’ secondary structure. RNA 7:382–394CrossRefPubMedGoogle Scholar
  117. Svitkin, Y.V., Imataka, H., Khaleghpour, K., Kahvejian, A., Liebig, H.D. and Sonenberg, N. 2001b. Poly(A)-binding protein interaction with eIF4G stimulates picornavirus IRES-dependent translation. RNA 7:1743–52CrossRefPubMedGoogle Scholar
  118. Tiley, L., King, A.M.Q. and Belsham, G.J. 2003. The foot-and-mouth disease virus cis-acting replication element (cre) can be complemented in trans within infected cells. J. Virol. (in press)Google Scholar
  119. Todd, S., Towner, J.S., Brown, D.M. and Semler, B.L. 1997. Replication-competent picornaviruses with complete genomic RNA 3’ noncoding region deletions. J. Virol. 71:8868–8874PubMedGoogle Scholar
  120. van Kuppeveld, F.J.M., Melchers, W.J.G, Kirkegaard, K. and Doedens, J.R. 1997. Structure-function analysis of coxsackie B3 virus protein 2B. Virology 227:111–118CrossRefPubMedGoogle Scholar
  121. Walter, B.L., Nguyen, J.H., Ehrenfeld, E. and Semler, B.L. 1999. Differential utilization of poly(rC) binding protein 2 in translation directed by picornavirus IRES elements. RNA 5:1570–1585CrossRefPubMedGoogle Scholar
  122. Woese, C.R., Winker, S. and Gutell, R.R. 1990. Architecture of ribosomal-RNA—constraints on the sequence of tetra-loops. Proc. Natl. Acad. Sci. USA 87:8467–8471PubMedGoogle Scholar
  123. Ypma-Wong, M.F., Dewalt, P.G., Johnson, V.H., Lamb, J.G., and Semler, B.L. 1988. Protein 3CD is the major poliovirus proteinase responsible for the cleavage of the P1 capsid precursor. Virology 166:265–270CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • G. J. Belsham
    • 1
  1. 1.BBSRC Institute for Animal Health, Pirbright, WokingSurreyUK

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