Abstract
Viruses depend on cells for their replication but have evolved mechanisms to achieve this in an efficient and, in some instances, a cell‐type‐specific manner. The expression of viral proteins is frequently subject to translational control. The dominant target of such control is the initiation step of protein synthesis. Indeed, during the early stages of infection, viral mRNAs must compete with their host counterparts for the protein synthetic machinery, especially for the limited pool of eukaryotic translation initiation factors (eIFs) that mediate the recruitment of ribosomes to both viral and cellular mRNAs. To circumvent this competition viruses use diverse strategies so that ribosomes can be recruited selectively to viral mRNAs. In this review we focus on the initiation of protein synthesis and outline some of the strategies used by viruses to ensure efficient translation initiation of their mRNAs. Copyright © 2010 John Wiley & Sons, Ltd.
REFERENCES
- 1. Sonenberg N, Hinnebusch AG. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 2009; 136(4): 731–745. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2. Schoenberg DR, Maquat LE. Re‐capping the message. Trends Biochem Sci 2009; 34(9): 435–442. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3. Hall TM. Poly(A) tail synthesis and regulation: recent structural insights. Curr Opin Struct Biol 2002; 12(1): 82–88. [DOI] [PubMed] [Google Scholar]
- 4. Rogers GW Jr, Richter NJ, Lima WF, Merrick WC. Modulation of the helicase activity of eIF4A by eIF4B, eIF4H, and eIF4F. J Biol Chem 2001; 276(33): 30914–30922. [DOI] [PubMed] [Google Scholar]
- 5. Marintchev A, Edmonds KA, Marintcheva B, et al Topology and regulation of the human eIF4A/4G/4H helicase complex in translation initiation. Cell 2009; 136(3): 447–460. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6. Prevot D, Darlix JL, Ohlmann T. Conducting the initiation of protein synthesis: the role of eIF4G. Biol Cell 2003; 95(3–4): 141–156. [DOI] [PubMed] [Google Scholar]
- 7. Kahvejian A, Roy G, Sonenberg N. The mRNA closed‐loop model: the function of PABP and PABP‐interacting proteins in mRNA translation. Cold Spring Harb Symp Quant Biol 2001; 66: 293–300. [DOI] [PubMed] [Google Scholar]
- 8. Kahvejian A, Svitkin YV, Sukarieh R, M'Boutchou MN, Sonenberg N. Mammalian poly(A)‐binding protein is a eukaryotic translation initiation factor, which acts via multiple mechanisms. Genes Dev 2005; 19(1): 104–113. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9. Pestova TV, Borukhov SI, Hellen CU. Eukaryotic ribosomes require initiation factors 1 and 1A to locate initiation codons. Nature 1998; 394(6696): 854–859. [DOI] [PubMed] [Google Scholar]
- 10. Kozak M. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell 1986; 44(2): 283–292. [DOI] [PubMed] [Google Scholar]
- 11. Unbehaun A, Borukhov SI, Hellen CU, Pestova TV. Release of initiation factors from 48S complexes during ribosomal subunit joining and the link between establishment of codon‐anticodon base‐pairing and hydrolysis of eIF2‐bound GTP. Genes Dev 2004; 18(24): 3078–3093. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12. Schwartz S, Felber BK, Fenyo EM, Pavlakis GN. Env and Vpu proteins of human immunodeficiency virus type 1 are produced from multiple bicistronic mRNAs. J Virol 1990; 64(11): 5448–5456. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13. Chenik M, Chebli K, Blondel D. Translation initiation at alternate in‐frame AUG codons in the rabies virus phosphoprotein mRNA is mediated by a ribosomal leaky scanning mechanism. J Virol 1995; 69(2): 707–712. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14. Stacey SN, Jordan D, Williamson AJ, Brown M, Coote JH, Arrand JR. Leaky scanning is the predominant mechanism for translation of human papillomavirus type 16 E7 oncoprotein from E6/E7 bicistronic mRNA. J Virol 2000; 74(16): 7284–7297. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15. Schaecher SR, Mackenzie JM, Pekosz A. The ORF7b protein of severe acute respiratory syndrome coronavirus (SARS‐CoV) is expressed in virus‐infected cells and incorporated into SARS‐CoV particles. J Virol 2007; 81(2): 718–731. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16. Xu K, Zheng BJ, Zeng R, et al Severe acute respiratory syndrome coronavirus accessory protein 9b is a virion‐associated protein. Virology 2009; 388(2): 279–285. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17. Yang Y, Hussain S, Wang H, Ke M, Guo D. Translational control of the subgenomic RNAs of severe acute respiratory syndrome coronavirus. Virus Genes 2009; 39(1): 10–18. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18. Futterer J, Kiss‐Laszlo Z, Hohn T. Nonlinear ribosome migration on cauliflower mosaic virus 35S RNA. Cell 1993; 73(4): 789–802. [DOI] [PubMed] [Google Scholar]
- 19. Latorre P, Kolakofsky D, Curran J. Sendai virus Y proteins are initiated by a ribosomal shunt. Mol Cell Biol 1998; 18(9): 5021–5031. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20. Sen N, Cao F, Tavis JE. Translation of duck hepatitis B virus reverse transcriptase by ribosomal shunting. J Virol 2004; 78(21): 11751–11757. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21. Remm M, Remm A, Ustav M. Human papillomavirus type 18 E1 protein is translated from polycistronic mRNA by a discontinuous scanning mechanism. J Virol 1999; 73(4): 3062–3070. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22. Yueh A, Schneider RJ. Selective translation initiation by ribosome jumping in adenovirus‐infected and heat‐shocked cells. Genes Dev 1996; 10(12): 1557–1567. [DOI] [PubMed] [Google Scholar]
- 23. Yueh A, Schneider RJ. Translation by ribosome shunting on adenovirus and hsp70 mRNAs facilitated by complementarity to 18S rRNA. Genes Dev 2000; 14(4): 414–421. [PMC free article] [PubMed] [Google Scholar]
- 24. Schepetilnikov M, Schott G, Katsarou K, Thiebeauld O, Keller M, Ryabova LA. Molecular dissection of the prototype foamy virus (PFV) RNA 5′‐UTR identifies essential elements of a ribosomal shunt. Nucleic Acids Res 2009; 37(17): 5838–5847. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25. Xi Q, Cuesta R, Schneider RJ. Regulation of translation by ribosome shunting through phosphotyrosine‐dependent coupling of adenovirus protein 100k to viral mRNAs. J Virol 2005; 79(9): 5676–5683. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26. Cuesta R, Xi Q, Schneider RJ. Structural basis for competitive inhibition of eIF4G‐Mnk1 interaction by the adenovirus 100‐kilodalton protein. J Virol 2004; 78(14): 7707–7716. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27. Saghir AN, Tuxworth WJ Jr., Hagedorn CH, McDermott PJ. Modifications of eukaryotic initiation factor 4F (eIF4F) in adult cardiocytes by adenoviral gene transfer: differential effects on eIF4F activity and total protein synthesis rates. Biochem J 2001; 356(Pt 2): 557–566. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28. Xi Q, Cuesta R, Schneider RJ. Tethering of eIF4G to adenoviral mRNAs by viral 100k protein drives ribosome shunting. Genes Dev 2004; 18(16): 1997–2009. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 29. Poyry TA, Kaminski A, Jackson RJ. What determines whether mammalian ribosomes resume scanning after translation of a short upstream open reading frame? Genes Dev 2004; 18(1): 62–75. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30. Horvath CM, Williams MA, Lamb RA. Eukaryotic coupled translation of tandem cistrons: identification of the influenza B virus BM2 polypeptide. EMBO J 1990; 9(8): 2639–2647. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 31. Powell ML, Napthine S, Jackson RJ, Brierley I, Brown TD. Characterization of the termination‐reinitiation strategy employed in the expression of influenza B virus BM2 protein. RNA 2008; 14(11): 2394–2406. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 32. Ahmadian G, Randhawa JS, Easton AJ. Expression of the ORF‐2 protein of the human respiratory syncytial virus M2 gene is initiated by a ribosomal termination‐dependent reinitiation mechanism. EMBO J 2000; 19(11): 2681–2689. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 33. Meyers G. Translation of the minor capsid protein of a calicivirus is initiated by a novel termination‐dependent reinitiation mechanism. J Biol Chem 2003; 278(36): 34051–34060. [DOI] [PubMed] [Google Scholar]
- 34. Luttermann C, Meyers G. A bipartite sequence motif induces translation reinitiation in feline calicivirus RNA. J Biol Chem 2007; 282(10): 7056–7065. [DOI] [PubMed] [Google Scholar]
- 35. Luttermann C, Meyers G. The importance of inter‐ and intramolecular base pairing for translation reinitiation on a eukaryotic bicistronic mRNA. Genes Dev 2009; 23(3): 331–344. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 36. Daughenbaugh KF, Fraser CS, Hershey JW, Hardy ME. The genome‐linked protein VPg of the Norwalk virus binds eIF3, suggesting its role in translation initiation complex recruitment. EMBO J 2003; 22(11): 2852–2859. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37. Poyry TA, Kaminski A, Connell EJ, Fraser CS, Jackson RJ. The mechanism of an exceptional case of reinitiation after translation of a long ORF reveals why such events do not generally occur in mammalian mRNA translation. Genes Dev 2007; 21(23): 3149–3162. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38. Gallie DR. The cap and poly(A) tail function synergistically to regulate mRNA translational efficiency. Genes Dev 1991; 5(11): 2108–2116. [DOI] [PubMed] [Google Scholar]
- 39. Michel YM, Poncet D, Piron M, Kean KM, Borman AM. Cap‐poly(A) synergy in mammalian cell‐free extracts. Investigation of the requirements for poly(A)‐mediated stimulation of translation initiation. J Biol Chem 2000; 275(41): 32268–32276. [DOI] [PubMed] [Google Scholar]
- 40. Piron M, Vende P, Cohen J, Poncet D. Rotavirus RNA‐binding protein NSP3 interacts with eIF4GI and evicts the poly(A) binding protein from eIF4F. EMBO J 1998; 17(19): 5811–5821. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 41. Vende P, Piron M, Castagne N, Poncet D. Efficient translation of rotavirus mRNA requires simultaneous interaction of NSP3 with the eukaryotic translation initiation factor eIF4G and the mRNA 3′ end. J Virol 2000; 74(15): 7064–7071. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 42. Piron M, Piron M, Delaunay T, Grosclaude J, Poncet D. Identification of the RNA‐binding, dimerization, and eIF4GI‐binding domains of rotavirus nonstructural protein NSP3. J Virol 1999; 73(7): 5411–5421. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 43. Groft CM, Burley SK. Recognition of eIF4G by rotavirus NSP3 reveals a basis for mRNA circularization. Mol Cell 2002; 9(6): 1273–1283. [DOI] [PubMed] [Google Scholar]
- 44. Polacek C, Friebe P, Harris E. Poly(A)‐binding protein binds to the non‐polyadenylated 3′ untranslated region of dengue virus and modulates translation efficiency. J Gen Virol 2009; 90(Pt 3): 687–692. [DOI] [PubMed] [Google Scholar]
- 45. Jang SK, Krausslich 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; 62(8): 2636–2643. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 46. Pelletier J, Sonenberg N. Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature 1988; 334(6180): 320–325. [DOI] [PubMed] [Google Scholar]
- 47. Hellen CU. IRES‐induced conformational changes in the ribosome and the mechanism of translation initiation by internal ribosomal entry. Biochim Biophys Acta 2009; 1789(9–10): 558–570. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 48. Niepmann M. Internal translation initiation of picornaviruses and hepatitis C virus. Biochim Biophys Acta 2009; 1789(9–10): 529–541. [DOI] [PubMed] [Google Scholar]
- 49. Fitzgerald KD, Semler BL. Bridging IRES elements in mRNAs to the eukaryotic translation apparatus. Biochim Biophys Acta 2009; 1789(9–10): 518–528. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 50. Filbin ME, Kieft JS. Toward a structural understanding of IRES RNA function. Curr Opin Struct Biol 2009; 19(3): 267–276. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 51. Balvay L, Soto Rifo R, Ricci EP, Decimo D, Ohlmann T. Structural and functional diversity of viral IRESes. Biochim Biophys Acta 2009; 1789(9–10): 542–557. [DOI] [PubMed] [Google Scholar]
- 52. Semler BL, Waterman ML. IRES‐mediated pathways to polysomes: nuclear versus cytoplasmic routes. Trends Microbiol 2008; 16(1): 1–5. [DOI] [PubMed] [Google Scholar]
- 53. Kieft JS. Viral IRES RNA structures and ribosome interactions. Trends Biochem Sci 2008; 33(6): 274–283. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 54. Baird SD, et al Searching for IRES. RNA 2006; 12(10): 1755–1785. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 55. Sarnow P, Cevallos RC, Jan E. Takeover of host ribosomes by divergent IRES elements. Biochem Soc Trans 2005; 33(Pt 6): 1479–1482. [DOI] [PubMed] [Google Scholar]
- 56. Chen CY, Sarnow P. Initiation of protein synthesis by the eukaryotic translational apparatus on circular RNAs. Science 1995; 268(5209): 415–417. [DOI] [PubMed] [Google Scholar]
- 57. Lukavsky PJ. Structure and function of HCV IRES domains. Virus Res 2009; 139(2): 166–171. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 58. Fraser CS, Doudna JA. Structural and mechanistic insights into hepatitis C viral translation initiation. Nat Rev Microbiol 2007; 5(1): 29–38. [DOI] [PubMed] [Google Scholar]
- 59. Hellen CU, Pestova TV. Translation of hepatitis C virus RNA. J Viral Hepat 1999; 6(2): 79–87. [DOI] [PubMed] [Google Scholar]
- 60. Balvay L, Lopez Lastra M, Sargueil B, Darlix JL, Ohlmann T. Translational control of retroviruses. Nat Rev Microbiol 2007; 5(2): 128–140. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 61. Tahiri‐Alaoui A, Smith LP, Baigent S, et al Identification of an intercistronic internal ribosome entry site in a Marek's disease virus immediate‐early gene. J Virol 2009; 83(11): 5846–5853. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 62. Isaksson A, Berggren M, Ricksten A. Epstein‐Barr virus U leader exon contains an internal ribosome entry site. Oncogene 2003; 22(4): 572–581. [DOI] [PubMed] [Google Scholar]
- 63. Bieleski L, Talbot SJ. Kaposi's sarcoma‐associated herpesvirus vCyclin open reading frame contains an internal ribosome entry site. J Virol 2001; 75(4): 1864–1869. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 64. Wilson JE, et al Naturally occurring dicistronic cricket paralysis virus RNA is regulated by two internal ribosome entry sites. Mol Cell Biol 2000; 20(14): 4990–4999. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 65. Jan E. Divergent IRES elements in invertebrates. Virus Res 2006; 119(1): 16–28. [DOI] [PubMed] [Google Scholar]
- 66. Roberts LO, Groppelli E. An atypical IRES within the 5′ UTR of a dicistrovirus genome. Virus Res 2009; 139(2): 157–165. [DOI] [PubMed] [Google Scholar]
- 67. Wong SM, Koh DC, Liu D. Identification of plant virus IRES. Methods Mol Biol 2008; 451: 125–133. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 68. Ronfort C, De Breyne S, Sandrin V, Darlix JL, Ohlmann T. Characterization of two distinct RNA domains that regulate translation of the Drosophila gypsy retroelement. RNA 2004; 10(3): 504–515. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 69. Meignin C, Bailly JL, Arnaud F, Dastugue B, Vaury C. The 5′ untranslated region and Gag product of Idefix, a long terminal repeat‐retrotransposon from Drosophila melanogaster, act together to initiate a switch between translated and untranslated states of the genomic mRNA. Mol Cell Biol 2003; 23(22): 8246–8254. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 70. Lopez‐Lastra M, Ulrici S, Gabus C, Darlix JL. Identification of an internal ribosome entry segment in the 5′ region of the mouse VL30 retrotransposon and its use in the development of retroviral vectors. J Virol 1999; 73(10): 8393–8402. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 71. Hellen CU, Sarnow P. Internal ribosome entry sites in eukaryotic mRNA molecules. Genes Dev 2001; 15(13): 1593–1612. [DOI] [PubMed] [Google Scholar]
- 72. Stoneley M, Willis AE. Cellular internal ribosome entry segments: structures, trans‐acting factors and regulation of gene expression. Oncogene 2004; 23(18): 3200–3207. [DOI] [PubMed] [Google Scholar]
- 73. Fernandez‐Miragall O, Lopez de Quinto S, Martinez‐Salas E. Relevance of RNA structure for the activity of picornavirus IRES elements. Virus Res 2009; 139(2): 172–182. [DOI] [PubMed] [Google Scholar]
- 74. Martinez‐Salas E, Saiz JC, Davila M, Belsham GJ, Domingo E. 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 1993; 67(7): 3748–3755. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 75. Barria MI, Gonzalez A, Vera‐Otarola J, et al Analysis of natural variants of the hepatitis C virus internal ribosome entry site reveals that primary sequence plays a key role in cap‐independent translation. Nucleic Acids Res 2009; 37(3): 957–971. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 76. Pestova TV, Hellen CU, Shatsky IN. Canonical eukaryotic initiation factors determine initiation of translation by internal ribosomal entry. Mol Cell Biol 1996; 16(12): 6859–6869. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 77. Kolupaeva VG, de Breyne S, Pestova TV, Hellen CU. In vitro reconstitution and biochemical characterization of translation initiation by internal ribosomal entry. Methods Enzymol 2007; 430: 409–439. [DOI] [PubMed] [Google Scholar]
- 78. Pause A, Methot N, Svitkin Y, Merrick WC, Sonenberg N. 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 1994; 13(5): 1205–1215. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 79. Sizova DV, Kolupaeva VG, Pestova TV, Shatsky IN, Hellen CU. Specific interaction of eukaryotic translation initiation factor 3 with the 5′ nontranslated regions of hepatitis C virus and classical swine fever virus RNAs. J Virol 1998; 72(6): 4775– 4782. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 80. Kolupaeva VG, Pestova TV, Hellen CU. An enzymatic footprinting analysis of the interaction of 40S ribosomal subunits with the internal ribosomal entry site of hepatitis C virus. J Virol 2000; 74(14): 6242–6250. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 81. Pestova TV, Lomakin IB, Hellen CU. Position of the CrPV IRES on the 40S subunit and factor dependence of IRES/80S ribosome assembly. EMBO Rep 2004; 5(9): 906–913. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 82. Pestova TV, Shatsky IN, Fletcher SP, Jackson RJ, Hellen CU. A prokaryotic‐like mode of cytoplasmic eukaryotic ribosome binding to the initiation codon during internal translation initiation of hepatitis C and classical swine fever virus RNAs. Genes Dev 1998; 12(1): 67–83. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 83. Jan E, Sarnow P. Factorless ribosome assembly on the internal ribosome entry site of cricket paralysis virus. J Mol Biol 2002; 324(5): 889–902. [DOI] [PubMed] [Google Scholar]
- 84. Jan E, Thompson SR, Wilson JE, Pestova TV, Hellen CU, Sarnow P. Initiator Met‐tRNA‐independent translation mediated by an internal ribosome entry site element in cricket paralysis virus‐like insect viruses. Cold Spring Harb Symp Quant Biol 2001; 66: 285–292. [DOI] [PubMed] [Google Scholar]
- 85. Costantino DA, Pfingsten JS, Rambo RP, Kieft JS. tRNA‐mRNA mimicry drives translation initiation from a viral IRES. Nat Struct Mol Biol 2008; 15(1): 57–64. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 86. Lloyd RE. Translational control by viral proteinases. Virus Res 2006; 119(1): 76–88. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 87. Ohlmann T, Rau M, Pain VM, Morley SJ. The C‐terminal domain of eukaryotic protein synthesis initiation factor (eIF) 4G is sufficient to support cap‐independent translation in the absence of eIF4E. EMBO J 1996; 15(6): 1371–1382. [PMC free article] [PubMed] [Google Scholar]
- 88. Alvarez E, Menendez‐Arias L, Carrasco L. The eukaryotic translation initiation factor 4GI is cleaved by different retroviral proteases. J Virol 2003; 77(23): 12392–12400. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 89. Gingras AC, Svitkin Y, Belsham GJ, Pause A, Sonenberg N. Activation of the translational suppressor 4E‐BP1 following infection with encephalomyocarditis virus and poliovirus. Proc Natl Acad Sci USA 1996; 93(11): 5578– 5583. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 90. Richter JD, Sonenberg N. Regulation of cap‐dependent translation by eIF4E inhibitory proteins. Nature 2005; 433(7025): 477–480. [DOI] [PubMed] [Google Scholar]
- 91. Paulous S, Malnou CE, Michel YM, Kean KM, Borman AM. Comparison of the capacity of different viral internal ribosome entry segments to direct translation initiation in poly(A)‐dependent reticulocyte lysates. Nucleic Acids Res 2003; 31(2): 722– 733. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 92. Bergamini G, Preiss T, Hentze MW. Picornavirus IRESes and the poly(A) tail jointly promote cap‐independent translation in a mammalian cell‐free system. RNA 2000; 6(12): 1781–1790. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 93. Svitkin YV, Costa‐Mattioli M, Herdy B, Perreault S, Sonenberg N. Stimulation of picornavirus replication by the poly(A) tail in a cell‐free extract is largely independent of the poly(A) binding protein (PABP). RNA 2007; 13(12): 2330–2340. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 94. Danthinne X, Seurinck J, Meulewaeter F, Van Montagu M, Cornelissen M. The 3′ untranslated region of satellite tobacco necrosis virus RNA stimulates translation in vitro. Mol Cell Biol 1993; 13(6): 3340–3349. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 95. Ito T, Tahara SM, Lai MM. The 3′‐untranslated region of hepatitis C virus RNA enhances translation from an internal ribosomal entry site. J Virol 1998; 72(11): 8789–8796. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 96. Meulewaeter F, Danthinne X, Van Montagu M, Cornelissen M. 5′‐ and 3′‐sequences of satellite tobacco necrosis virus RNA promoting translation in tobacco. Plant J 1998; 14(2): 169–176. [DOI] [PubMed] [Google Scholar]
- 97. Wang S, Browning KS, Miller WA. A viral sequence in the 3′‐untranslated region mimics a 5′ cap in facilitating translation of uncapped mRNA. EMBO J 1997; 16(13): 4107–4116. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 98. Weinlich S, et al IGF2BP1 enhances HCV IRES‐mediated translation initiation via the 3′UTR. RNA 2009; 15(8): 1528–1542. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 99. Romero‐Lopez C, Berzal‐Herranz A. A long‐range RNA‐RNA interaction between the 5′ and 3′ ends of the HCV genome. RNA 2009; 15(9): 1740–1752. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 100. Guo L, Allen EM, Miller WA. Base‐pairing between untranslated regions facilitates translation of uncapped, nonpolyadenylated viral RNA. Mol Cell 2001; 7(5): 1103–1109. [DOI] [PubMed] [Google Scholar]
- 101. Belsham GJ, Sonenberg N. Picornavirus RNA translation: roles for cellular proteins. Trends Microbiol 2000; 8(7): 330–335. [DOI] [PubMed] [Google Scholar]
- 102. Lewis SM, Holcik M. For IRES trans‐acting factors, it is all about location. Oncogene 2008; 27(8): 1033–1035. [DOI] [PubMed] [Google Scholar]
- 103. Borman A, Howell MT, Patton JG, Jackson RJ. The involvement of a spliceosome component in internal initiation of human rhinovirus RNA translation. J Gen Virol 1993; 74(Pt 9): 1775–1788. [DOI] [PubMed] [Google Scholar]
- 104. Brown BA, Ehrenfeld E. Translation of poliovirus RNA in vitro: changes in cleavage pattern and initiation sites by ribosomal salt wash. Virology 1979; 97(2): 396–405. [DOI] [PubMed] [Google Scholar]
- 105. Dorner AJ, Semler BL, Jackson RJ, Hanecak R, Duprey E, Wimmer E. In vitro translation of polioviru RNA: utilization of internal initiation sites in reticulocyte lysate. J Virol 1984; 50(2): 507–514. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 106. Brasey A, Lopez‐Lastra M, Ohlmann T, et al The leader of human immunodeficiency virus type 1 genomic RNA harbors an internal ribosome entry segment that is active during the G2/M phase of the cell cycle. J Virol 2003; 77(7): 3939–3949. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 107. Monette A, Ajamian L, Lopez‐Lastra M, Mouland AJ. Human immunodeficiency virus type 1 (HIV‐1) induces the cytoplasmic retention of heterogeneous nuclear ribonucleoprotein A1 by disrupting nuclear import: implications for HIV‐1 gene expression. J Biol Chem 2009; 284(45): 31350–31362. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 108. Costa‐Mattioli M, Svitkin Y, Sonenberg N. La autoantigen is necessary for optimal function of the poliovirus and hepatitis C virus internal ribosome entry site in vivo and in vitro. Mol Cell Biol 2004; 24(15): 6861–6870. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 109. Hunt SL, Hsuan JJ, Totty N, Jackson RJ. Unr, a cellular cytoplasmic RNA‐binding protein with five cold‐shock domains, is required for internal initiation of translation of human rhinovirus RNA. Genes Dev 1999; 13(4): 437–448. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 110. Boussadia O, Niepmann M, Creancier L, Prats AC, Dautry F, Jacquemin‐Sablon H. Unr is required in vivo for efficient initiation of translation from the internal ribosome entry sites of both rhinovirus and poliovirus. J Virol 2003; 77(6): 3353–3359. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 111. Andreev DE, Fernandez‐Miragall O, Ramajo J, et al Differential factor requirement to assemble translation initiation complexes at the alternative start codons of foot‐and‐mouth disease virus RNA. RNA 2007; 13(8): 1366–1374. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 112. Hunt SL, Jackson RJ. Polypyrimidine‐tract binding protein (PTB) is necessary, but not sufficient, for efficient internal initiation of translation of human rhinovirus‐2 RNA. RNA 1999; 5(3): 344–359. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 113. Cordes S, Kusov Y, Heise T, Gauss‐Muller V. La autoantigen suppresses IRES‐dependent translation of the hepatitis A virus. Biochem Biophys Res Commun 2008; 368(4): 1014–1019. [DOI] [PubMed] [Google Scholar]
- 114. Rivas‐Aravena A, Ramdohr P, Vallejos M, et al The Elav‐like protein HuR exerts translational control of viral internal ribosome entry sites. Virology 2009; 392(2): 178–185. [DOI] [PubMed] [Google Scholar]
- 115. Lin JY, Li ML, Shih SR. Far upstream element binding protein 2 interacts with enterovirus 71 internal ribosomal entry site and negatively regulates viral translation. Nucleic Acids Res 2009; 37(1): 47–59. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 116. Cristofari G, Darlix JL. The ubiquitous nature of RNA chaperone proteins. Prog Nucleic Acid Res Mol Biol 2002; 72: 223–268. [DOI] [PubMed] [Google Scholar]
- 117. Ivanyi‐Nagy R, Davidovic L, Khandjian EW, Darlix JL. Disordered RNA chaperone proteins: from functions to disease. Cell Mol Life Sci 2005; 62(13): 1409–1417. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 118. Sachs AB. Cell cycle‐dependent translation initiation: IRES elements prevail. Cell 2000; 101(3): 243–245. [DOI] [PubMed] [Google Scholar]
- 119. Kim YK, Jang SK. Continuous heat shock enhances translational initiation directed by internal ribosomal entry site. Biochem Biophys Res Commun 2002; 297(2): 224–231. [DOI] [PubMed] [Google Scholar]
- 120. Qin X, Sarnow P. Preferential translation of internal ribosome entry site‐containing mRNAs during the mitotic cycle in mammalian cells. J Biol Chem 2004; 279(14): 13721–13728. [DOI] [PubMed] [Google Scholar]
- 121. Honda M, Kaneko S, Matsushita E, Kobayashi K, Abell GA, Lemon SM. Cell cycle regulation of hepatitis C virus internal ribosomal entry site‐directed translation. Gastroenterology 2000; 118(1): 152–162. [DOI] [PubMed] [Google Scholar]
- 122. Bonneau AM, Sonenberg N. Involvement of the 24‐kDa cap‐binding protein in regulation of protein synthesis in mitosis. J Biol Chem 1987; 262(23): 11134–11139. [PubMed] [Google Scholar]
- 123. Cormier P, Pyronnet S, Salaun P, Mulner‐Lorillon O, Sonenberg N. Cap‐dependent translation and control of the cell cycle. Prog Cell Cycle Res 2003; 5: 469–475. [PubMed] [Google Scholar]
- 124. Chaudhry Y, Nayak A, Bordeleau ME, et al Caliciviruses differ in their functional requirements for eIF4F components. J Biol Chem 2006; 281(35): 25315–25325. [DOI] [PubMed] [Google Scholar]
- 125. Kash JC, Goodman AG, Korth MJ, Katze MG. Hijacking of the host‐cell response and translational control during influenza virus infection. Virus Res 2006; 119(1): 111–120. [DOI] [PubMed] [Google Scholar]
- 126. Hale BG, Randall RE, Ortin J, Jackson D. The multifunctional NS1 protein of influenza A viruses. J Gen Virol 2008; 89(Pt 10): 2359–2376. [DOI] [PubMed] [Google Scholar]
- 127. Fechter P, Brownlee GG. Recognition of mRNA cap structures by viral and cellular proteins. J Gen Virol 2005; 86(Pt 5): 1239–1249. [DOI] [PubMed] [Google Scholar]
- 128. Burgui I, Aragon T, Ortin J, Nieto A., PABP1 and eIF4GI associate with influenza virus NS1 protein in viral mRNA translation initiation complexes. J Gen Virol 2003; (Pt 12): 3263–3274. [DOI] [PubMed] [Google Scholar]
- 129. Aragon T, de la Luna S, Novoa I, Carrasco L, Ortin J, Nieto A. Eukaryotic translation initiation factor 4GI is a cellular target for NS1 protein, a translational activator of influenza virus. Mol Cell Biol 2000; 20(17): 6259–6268. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 130. Burgui I, Yanguez E, Sonenberg N, Nieto A. Influenza virus mRNA translation revisited: is the eIF4E cap‐binding factor required for viral mRNA translation? J Virol 2007; 81(22): 12427–12438. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 131. Mir MA, Duran WA, Hjelle BL, Ye C, Panganiban AT. Storage of cellular 5′ mRNA caps in P bodies for viral cap‐snatching. Proc Natl Acad Sci USA 2008; 105(49): 19294–19299. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 132. Mir MA, Panganiban AT. A protein that replaces the entire cellular eIF4F complex. EMBO J 2008; 27(23): 3129–3139. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 133. Sarnow P. Viral internal ribosome entry site elements: novel ribosome‐RNA complexes and roles in viral pathogenesis. J Virol 2003; 77(5): 2801–2806. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 134. Gromeier M, Bossert B, Arita M, Nomoto A, Wimmer E. Dual stem loops within the poliovirus internal ribosomal entry site control neurovirulence. J Virol 1999; 73(2): 958–964. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 135. Ohka S, Nomoto A. The molecular basis of poliovirus neurovirulence. Dev Biol (Basel) 2001; 105: 51–58. [PubMed] [Google Scholar]
- 136. Ochs K, Zeller A, Saleh L, et al Impaired binding of standard initiation factors mediates poliovirus translation attenuation. J Virol 2003; 77(1): 115– 122. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 137. Ali IK, McKendrick L, Morley SJ, Jackson RJ. Activity of the hepatitis A virus IRES requires association between the cap‐binding translation initiation factor (eIF4E) and eIF4G. J Virol 2001; 75(17): 7854–7863. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 138. Borman AM, Kean KM. Intact eukaryotic initiation factor 4G is required for hepatitis A virus internal initiation of translation. Virology 1997; 237(1): 129–136. [DOI] [PubMed] [Google Scholar]
- 139. Chang KH, Brown EA, Lemon SM. Cell type‐specific proteins which interact with the 5′ nontranslated region of hepatitis A virus RNA. J Virol 1993; 67(11): 6716–6725. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 140. Funkhouser AW, Purcell RH, D'Hondt E, Emerson SU. Attenuated hepatitis A virus: genetic determinants of adaptation to growth in MRC‐5 cells. J Virol 1994; 68(1): 148–157. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 141. Schultz DE, Honda M, Whetter LE, McKnight KL, Lemon SM. Mutations within the 5′ nontranslated RNA of cell culture‐adapted hepatitis A virus which enhance cap‐independent translation in cultured African green monkey kidney cells. J Virol 1996; 70(2): 1041–1049. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 142. Buratti E, Gerotto M, Pontisso P, Alberti A, Tisminetzky SG, Baralle FE. In vivo translational efficiency of different hepatitis C virus 5′‐UTRs. FEBS Lett 1997; 411(2–3): 275–280. [DOI] [PubMed] [Google Scholar]
- 143. Collier AJ, Tang S, Elliott RM. Translation efficiencies of the 5′ untranslated region from representatives of the six major genotypes of hepatitis C virus using a novel bicistronic reporter assay system. J Gen Virol 1998; 79(Pt 10): 2359– 2366. [DOI] [PubMed] [Google Scholar]
- 144. Yanagiya A, Ohka S, Hashida N, et al Tissue‐specific replicating capacity of a chimeric poliovirus that carries the internal ribosome entry site of hepatitis C virus in a new mouse model transgenic for the human poliovirus receptor. J Virol 2003; 77(19): 10479–10487. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 145. Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P. Modulation of hepatitis C virus RNA abundance by a liver‐specific MicroRNA. Science 2005; 309(5740): 1577–1581. [DOI] [PubMed] [Google Scholar]
- 146. Baek D, Villen J, Shin C, Camargo FD, Gygi SP, Bartel DP. The impact of microRNAs on protein output. Nature 2008; 455(7209): 64–71. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 147. Selbach M, Schwanhausser B, Thierfelder N, Fang Z, Khanin R, Rajewsky N. Widespread changes in protein synthesis induced by microRNAs. Nature 2008; 455(7209): 58–63. [DOI] [PubMed] [Google Scholar]
- 148. Tang G, Tang X, Mendu V, Jia X, Chen QJ, He L. The art of microRNA: various strategies leading to gene silencing via an ancient pathway. Biochim Biophys Acta 2008; 1779(11): 655–662. [DOI] [PubMed] [Google Scholar]
- 149. Grassmann R, Jeang KT. The roles of microRNAs in mammalian virus infection. Biochim Biophys Acta 2008; 1779(11): 706–711. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 150. Cullen BR. Viral and cellular messenger RNA targets of viral microRNAs. Nature 2009; 457(7228): 421–425. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 151. Umbach JL, Cullen BR. The role of RNAi and microRNAs in animal virus replication and antiviral immunity. Genes Dev 2009; 23(10): 1151–1164. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 152. Niepmann M. Activation of hepatitis C virus translation by a liver‐specific microRNA. Cell Cycle 2009; 8(10): 1473–1477. [DOI] [PubMed] [Google Scholar]
- 153. Henke JI, Goergen D, Zheng J, et al microRNA‐122 stimulates translation of hepatitis C virus RNA. EMBO J 2008; 27(24): 3300–3310. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 154. Lanford RE, Hildebrandt‐Eriksen ES, Petri A, et al Therapeutic silencing of microRNA‐122 in primates with chronic hepatitis C virus infection. Science 2010; 327: 198–201. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 155. Bushell M, Sarnow P. Hijacking the translation apparatus by RNA viruses. J Cell Biol 2002; 158(3): 395–399. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 156. Schneider RJ, Mohr I. Translation initiation and viral tricks. Trends Biochem Sci 2003; 28(3): 130–136. [DOI] [PubMed] [Google Scholar]
- 157. Smith RW, Graham SV, Gray NK. Regulation of translation initiation by herpesviruses. Biochem Soc Trans 2008; 36(Pt 4): 701–707. [DOI] [PubMed] [Google Scholar]
- 158. Gebauer F, Hentze MW. Molecular mechanisms of translational control. Nat Rev Mol Cell Biol 2004; 5(10): 827–835. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 159. Sadler AJ, Williams BR. Interferon‐inducible antiviral effectors. Nat Rev Immunol 2008; 8(7): 559–568. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 160. Bolinger C, Boris‐Lawrie K. Mechanisms employed by retroviruses to exploit host factors for translational control of a complicated proteome. Retrovirology 2009; 6: 8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 161. Tallet‐Lopez B, Aldaz‐Carroll L, Chabas S, Dausse E, Staedel C, Toulme JJ. Antisense oligonucleotides targeted to the domain IIId of the hepatitis C virus IRES compete with 40S ribosomal subunit binding and prevent in vitro translation. Nucleic Acids Res 2003; 31(2): 734–742. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 162. Kikuchi K, Umehara T, Fukuda K, Kuno A, Hasegawa T, Nishikawa S. A hepatitis C virus (HCV) internal ribosome entry site (IRES) domain III‐IV‐targeted aptamer inhibits translation by binding to an apical loop of domain IIId. Nucleic Acids Res 2005; 33(2): 683–692. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 163. Alotte C, Martin A, Caldarelli SA, et al Short peptide nucleic acids (PNA) inhibit hepatitis C virus internal ribosome entry site (IRES) dependent translation in vitro. Antiviral Res 2008; 80(3): 280–287. [DOI] [PubMed] [Google Scholar]
- 164. Romero‐Lopez C, Diaz‐Gonzalez R, Barroso‐delJesus A, Berzal‐Herranz A. Inhibition of hepatitis C virus replication and internal ribosome entry site‐dependent translation by an RNA molecule. J Gen Virol 2009; 90(Pt 7): 1659–1669. [DOI] [PubMed] [Google Scholar]
- 165. McCaffrey AP, Meuse L, Karimi M, Contag CH, Kay MA. A potent and specific morpholino antisense inhibitor of hepatitis C translation in mice. Hepatology 2003; 38(2): 503–508. [DOI] [PubMed] [Google Scholar]
- 166. Beaulieu PL, Bos M, Bousquet Y, et al Non‐nucleoside inhibitors of the hepatitis C virus NS5B polymerase: discovery and preliminary SAR of benzimidazole derivatives. Bioorg Med Chem Lett 2004; 14(1): 119–124. [DOI] [PubMed] [Google Scholar]
- 167. Parsons J, Castaldi MP, Dutta S, Dibrov SM, Wyles DL, Hermann T. Conformational inhibition of the hepatitis C virus internal ribosome entry site RNA. Nat Chem Biol 2009; 5(11): 823–825. [DOI] [PMC free article] [PubMed] [Google Scholar]