mRNAs that specifically interact with eukaryotic ribosomal subunits

Biochimie

Volumn 114, Issue , 2015, Pages 48-57

  Deforges, Jules ^a,b   Locker, Nicolas ^c   Sargueil, Bruno ^a,b  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c UNIVERSITY OF SURREY   (United Kingdom)

Author keywords

3 CITE; IRES; Ribosome; Shine Dalgarno; Translation; Virus

Indexed keywords

GENOMIC RNA; MESSENGER RNA; RNA 16S; RNA 18S; TRANSFER RNA;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; BASE PAIRING; CALICIVIRIDAE; CODON; EUKARYOTE; HUMAN HERPESVIRUS 8; HUMAN IMMUNODEFICIENCY VIRUS; INTERACTIONS WITH RNA; INTERNAL RIBOSOME ENTRY SITE; LARGE RIBOSOMAL SUBUNIT; MOLECULAR MIMICRY; NONHUMAN; OPEN READING FRAME; PLANT VIRUS; RIBOSOME SUBUNIT; RNA STRUCTURE; RNA TRANSLATION; SMALL RIBOSOMAL SUBUNIT; TRANSLATION INITIATION; ANIMAL; BINDING SITE; HUMAN; PHYSIOLOGY; PROTEIN SYNTHESIS; RNA TRANSPORT;

EUKARYOTA; PROKARYOTA;

ANIMALS; BINDING SITES; HUMANS; PROTEIN BIOSYNTHESIS; RIBOSOME SUBUNITS, LARGE, EUKARYOTIC; RIBOSOME SUBUNITS, SMALL, EUKARYOTIC; RNA TRANSPORT; RNA, MESSENGER; RNA, TRANSFER;

EID: 84930654162     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2014.12.008     Document Type: Review

References (105)

1. G.Z. Yusupova, M.M. Yusupov, J.H.D. Cate, and H.F. Noller The path of messenger RNA through the ribosome Cell 106 2001 233 241 10.1016/S0092-8674(01)00435-4
2. A. Simonetti, S. Marzi, L. Jenner, A. Myasnikov, P. Romby, and G. Yusupova A structural view of translation initiation in bacteria Cell. Mol. Life Sci. 66 2009 423 436 10.1007/s00018-008-8416-4
3. M. Kozak Initiation of translation in prokaryotes and eukaryotes Gene 234 1999 187 208 10.1016/S0378-1119(99)00210-3
4. L.S. Valasek "Ribozoomin" - translation initiation from the perspective of the ribosome-bound eukaryotic initiation factors (eIFs) Curr. Protein Pept. Sci. 13 2012 305 330 10.2174/138920312801619385
5. C.E. Aitken, and J.R. Lorsch A mechanistic overview of translation initiation in eukaryotes Nat. Struct. Mol. Biol. 19 2012 568 576 10.1038/nsmb.2303
6. R.J. Jackson, C.U.T. Hellen, and T.V. Pestova The mechanism of eukaryotic translation initiation and principles of its regulation Nat. Rev. Mol. Cell. Biol. 11 2010 113 127 10.1038/nrm2838
7. T.V. Pestova, C.U. Hellen, and I.N. Shatsky Canonical eukaryotic initiation factors determine initiation of translation by internal ribosomal entry Mol. Cell. Biol. 16 1996 6859 6869
8. T.V. Pestova, I.N. Shatsky, S.P. Fletcher, R.J. Jackson, and C.U.T. Hellen 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. 12 1998 67 83 10.1101/gad.12.1.67
9. J.E. Wilson, M.J. Powell, S.E. Hoover, and P. Sarnow Naturally occurring dicistronic cricket paralysis virus RNA is regulated by two internal ribosome entry sites Mol. Cell. Biol. 20 2000 4990 4999 10.1128/MCB.20.14.4990-4999.2000
10. C.U.T. Hellen IRES-induced conformational changes in the ribosome and the mechanism of translation initiation by internal ribosomal entry Biochim. Biophys. Acta 1789 2009 558 570 10.1016/j.bbagrm.2009.06.001
11. D.A. Costantino, J.S. Pfingsten, R.P. Rambo, and J.S. Kieft tRNA-mRNA mimicry drives translation initiation from a viral IRES Nat. Struct. Mol. Biol. 15 2008 57 64 10.1038/nsmb1351
12. J.S. Pfingsten, D.A. Costantino, and J.S. Kieft Structural basis for ribosome recruitment and manipulation by a viral IRES RNA Science 314 2006 1450 1454 10.1126/science.1133281
13. C.M.T. Spahn, E. Jan, A. Mulder, R.A. Grassucci, P. Sarnow, and J. Frank Cryo-EM visualization of a viral internal ribosome entry site bound to human ribosomes: the IRES functions as an RNA-based translation factor Cell 118 2004 465 475 10.1016/j.cell.2004.08.001
14. M. Schüler, S.R. Connell, A. Lescoute, J. Giesebrecht, M. Dabrowski, and B. Schroeer Structure of the ribosome-bound cricket paralysis virus IRES RNA Nat. Struct. Mol. Biol. 13 2006 1092 1096 10.1038/nsmb1177
15. C.M.T. Spahn, J.S. Kieft, R.A. Grassucci, P.A. Penczek, K. Zhou, and J.A. Doudna Hepatitis C virus IRES RNA-induced changes in the conformation of the 40S ribosomal subunit Science 291 2001 1959 1962 10.1126/science.1058409
16. B. Siridechadilok, C.S. Fraser, R.J. Hall, J.A. Doudna, and E. Nogales Structural roles for human translation factor eIF3 in initiation of protein synthesis Science 310 2005 1513 1515 10.1126/science.1118977
17. H. Yamamoto, A. Unbehaun, J. Loerke, E. Behrmann, M. Collier, and J. Bürger Structure of the mammalian 80S initiation complex with initiation factor 5B on HCV-IRES RNA Nat. Struct. Mol. Biol. 21 2014 721 727 10.1038/nsmb.2859
18. C.S. Koh, A.F. Brilot, N. Grigorieff, and A.A. Korostelev Taura syndrome virus IRES initiates translation by binding its tRNA-mRNA-like structural element in the ribosomal decoding center Proc. Natl. Acad. Sci. 111 2014 9139 9144 10.1073/pnas.1406335111
19. I.S. Fernandez, X.-C. Bai, G. Murshudov, S.H.W. Scheres, and V. Ramakrishnan Initiation of translation by cricket paralysis virus IRES requires its translocation in the ribosome Cell 157 2014 823 831 10.1016/j.cell.2014.04.015
20. Y. Hashem, A. des Georges, V. Dhote, R. Langlois, H.Y. Liao, and R.A. Grassucci Hepatitis-C-virus-like internal ribosome entry sites displace eIF3 to gain access to the 40S subunit Nature 503 2013 539 543 10.1038/nature12658
21. A.E. Simon, and W.A. Miller 3′ Cap-independent translation enhancers of plant viruses Annu. Rev. Microbiol. 67 2013 21 42 10.1146/annurev-micro-092412-155609
22. L. Balvay, R.S. Rifo, E.P. Ricci, D. Decimo, and T. Ohlmann Structural and functional diversity of viral IRESes Biochim. Biophys. Acta BBA - Gene Regul. Mech. 1789 2009 542 557 10.1016/j.bbagrm.2009.07.005
23. W.A. Miller, Z. Wang, and K. Treder The amazing diversity of cap-independent translation elements in the 3′-untranslated regions of plant viral RNAs Biochem. Soc. Trans. 35 2007 1629 10.1042/BST0351629
24. B.L. Nicholson, and K.A. White 3′ Cap-independent translation enhancers of positive-strand RNA plant viruses Curr. Opin. Virol. 1 2011 373 380 10.1016/j.coviro.2011.10.002
25. J.E. Wilson, T.V. Pestova, C.U.T. Hellen, and P. Sarnow Initiation of protein synthesis from the A site of the ribosome Cell 102 2000 511 520 10.1016/S0092-8674(00)00055-6
26. C.U.T. Hellen, and P. Sarnow Internal ribosome entry sites in eukaryotic mRNA molecules Genes Dev. 15 2001 1593 1612 10.1101/gad.891101
27. E. Jan, and P. Sarnow Factorless ribosome assembly on the internal ribosome entry site of cricket paralysis virus J.Mol. Biol. 324 2002 889 902 10.1016/S0022-2836(02)01099-9
28. T.V. Pestova, and C.U.T. Hellen Translation elongation after assembly of ribosomes on the Cricket paralysis virus internal ribosomal entry site without initiation factors or initiator tRNA Genes Dev. 17 2003 181 186 10.1101/gad.1040803
29. H. Yamamoto, N. Nakashima, Y. Ikeda, and T. Uchiumi Binding mode of the first aminoacyl-tRNA in translation initiation mediated by Plautia stali intestine virus internal ribosome entry site J.Biol. Chem. 282 2007 7770 7776 10.1074/jbc.M610887200
30. X. Zuo, J. Wang, P. Yu, D. Eyler, H. Xu, and M.R. Starich Solution structure of the cap-independent translational enhancer and ribosome-binding element in the 3′ UTR of turnip crinkle virus Proc. Natl. Acad. Sci. 107 2010 1385 1390 10.1073/pnas.0908140107
31. F. Gao, W. Kasprzak, V.A. Stupina, B.A. Shapiro, and A.E. Simon A ribosome-binding, 3′ translational enhancer has a T-shaped structure and engages in a long-distance RNA-RNA interaction J. Virol. 86 2012 9828 9842 10.1128/JVI.00677-12
32. T.M. Colussi, D.A. Costantino, J.A. Hammond, G.M. Ruehle, J.C. Nix, and J.S. Kieft The structural basis of transfer RNA mimicry and conformational plasticity by a viral RNA Nature 511 2014 366 369 10.1038/nature13378
33. F. Gao, S.P. Gulay, W. Kasprzak, J.D. Dinman, B.A. Shapiro, and A.E. Simon The kl-TSS translational enhancer of PEMV can bind simultaneously to ribosomes and a 5′ proximal hairpin J. Virol. 2013 JVI.02005 JVI.02013 10.1128/JVI.02005-13
34. T.V. Pestova, I.B. Lomakin, J.H. Lee, S.K. Choi, T.E. Dever, and C.U.T. Hellen The joining of ribosomal subunits in eukaryotes requires eIF5B Nature 403 2000 332 335 10.1038/35002118
35. N. Locker, L.E. Easton, and P.J. Lukavsky HCV and CSFV IRES domain II mediate eIF2 release during 80S ribosome assembly EMBO J. 26 2007 795 805 10.1038/sj.emboj.7601549
36. I.M. Terenin, S.E. Dmitriev, D.E. Andreev, and I.N. Shatsky Eukaryotic translation initiation machinery can operate in a bacterial-like mode without eIF2 Nat. Struct. Mol. Biol. 15 2008 836 841 10.1038/nsmb.1445
37. T.V. Pestova, S. de Breyne, A.V. Pisarev, I.S. Abaeva, and C.U.T. Hellen eIF2-dependent and eIF2-independent modes of initiation on the CSFV IRES: a common role of domain II EMBO J. 27 2008 1060 1072 10.1038/emboj.2008.49
38. M.A. Skabkin, O.V. Skabkina, V. Dhote, A.A. Komar, C.U.T. Hellen, and T.V. Pestova Activities of ligatin and MCT-1/DENR in eukaryotic translation initiation and ribosomal recycling Genes Dev. 24 2010 1787 1801 10.1101/gad.1957510
39. S.E. Dmitriev, I.M. Terenin, D.E. Andreev, P.A. Ivanov, J.E. Dunaevsky, and W.C. Merrick GTP-independent tRNA delivery to the ribosomal P-site by a novel eukaryotic translation factor J. Biol. Chem. 285 2010 26779 26787 10.1074/jbc.M110.119693
40. J.S. Kieft, K. Zhou, R. Jubin, and J.A. Doudna Mechanism of ribosome recruitment by hepatitis C IRES RNA RNA 7 2001 194 206
41. V.G. Kolupaeva, T.V. Pestova, and C.U.T. Hellen An enzymatic footprinting analysis of the interaction of 40S ribosomal subunits with the internal ribosomal entry site of hepatitis C virus J. Virol. 74 2000 6242 6250 10.1128/JVI.74.14.6242-6250.2000
42. V.G. Kolupaeva, T.V. Pestova, and C.U. Hellen Ribosomal binding to the internal ribosomal entry site of classical swine fever virus RNA 6 2000 1791 1807
43. A.A. Malygin, O.A. Kossinova, I.N. Shatsky, and G.G. Karpova HCV IRES interacts with the 18S rRNA to activate the 40S ribosome for subsequent steps of translation initiation Nucleic Acids Res. 41 2013 8706 8714 10.1093/nar/gkt632
44. D. Matsuda, and V.P. Mauro Base pairing between hepatitis C virus RNA and 18S rRNA is required for IRES-dependent translation initiation in vivo Proc. Natl. Acad. Sci. 2014 201413472 10.1073/pnas.1413472111
45. M.E. Filbin, B.S. Vollmar, D. Shi, T. Gonen, and J.S. Kieft HCV IRES manipulates the ribosome to promote the switch from translation initiation to elongation Nat. Struct. Mol. Biol. 20 2013 150 158 10.1038/nsmb.2465
46. M. Honda, E.A. Brown, and S.M. Lemon Stability of a stem-loop involving the initiator AUG controls the efficiency of internal initiation of translation on hepatitis C virus RNA RNA 2 1996 955 968
47. V.G. Kolupaeva, T.V. Pestova, C.U.T. Hellen, and I.N. Shatsky Translation eukaryotic initiation factor 4G recognizes a specific structural element within the internal ribosome entry site of encephalomyocarditis virus RNA J. Biol. Chem. 273 1998 18599 18604 10.1074/jbc.273.29.18599
48. I.B. Lomakin, C.U.T. Hellen, and T.V. Pestova Physical association of eukaryotic initiation factor 4G (eIF4G) with eIF4A strongly enhances binding of eIF4G to the internal ribosomal entry site of encephalomyocarditis virus and is required for internal initiation of translation Mol. Cell. Biol. 20 2000 6019 6029 10.1128/MCB.20.16.6019-6029.2000
49. N. Chamond, J. Deforges, N. Ulryck, and B. Sargueil 40S recruitment in the absence of eIF4G/4A by EMCV IRES refines the model for translation initiation on the archetype of Type II IRESs Nucleic Acids Res. 2014 gku720 10.1093/nar/gku720
50. V.G. Kolupaeva, I.B. Lomakin, T.V. Pestova, and C.U.T. Hellen Eukaryotic initiation factors 4G and 4A mediate conformational changes downstream of the initiation codon of the encephalomyocarditis virus internal ribosomal entry site Mol. Cell. Biol. 23 2003 687 698 10.1128/MCB.23.2.687-698.2003
51. P. Kafasla, N. Morgner, T.A.A. Pöyry, S. Curry, C.V. Robinson, and R.J. Jackson Polypyrimidine tract binding protein stabilizes the encephalomyocarditis virus IRES structure via binding multiple sites in a unique orientation Mol. Cell. 34 2009 556 568 10.1016/j.molcel.2009.04.015
52. J.-C. Paillart, M. Dettenhofer, X. Yu, C. Ehresmann, B. Ehresmann, and R. Marquet First snapshots of the HIV-1 RNA structure in infected cells and in virions J. Biol. Chem. 279 2004 48397 48403 10.1074/jbc.M408294200
53. A.M.G. Dirac, H. Huthoff, J. Kjems, and B. Berkhout Regulated HIV-2 RNA dimerization by means of alternative RNA conformations Nucleic Acids Res. 30 2002 2647 2655 10.1093/nar/gkf381
54. L. James, and B. Sargueil RNA secondary structure of the feline immunodeficiency virus 5′UTR and Gag coding region Nucleic Acids Res. 36 2008 4653 4666 10.1093/nar/gkn447
55. J. Deforges, N. Chamond, and B. Sargueil Structural investigation of HIV-1 genomic RNA dimerization process reveals a role for the Major Splice-site Donor stem loop Biochimie 94 2012 1481 1489 10.1016/j.biochi.2012.02.009
56. B. Berkhout, and J.L. van Wamel The leader of the HIV-1 RNA genome forms a compactly folded tertiary structure RNA 6 2000 282 295
57. K.A. Wilkinson, R.J. Gorelick, S.M. Vasa, N. Guex, A. Rein, and D.H. Mathews High-throughput SHAPE analysis reveals structures in HIV-1 genomic RNA strongly conserved across distinct biological states PLoS Biol. 6 2008 883 899 10.1371/journal.pbio.0060096
58. A. Sharma, A. Yilmaz, K. Marsh, A. Cochrane, and K. Boris-Lawrie Thriving under stress: selective translation of HIV-1 structural protein mRNA during Vpr-mediated impairment of eIF4E translation activity PLoS Pathog. 8 2012 e1002612 10.1371/journal.ppat.1002612
59. R. Soto-Rifo, P.S. Rubilar, and T. Ohlmann The DEAD-box helicase DDX3 substitutes for the cap-binding protein eIF4E to promote compartmentalized translation initiation of the HIV-1 genomic RNA Nucleic Acids Res. 41 2013 6286 6299 10.1093/nar/gkt306
60. A. Brasey, M. Lopez-Lastra, T. Ohlmann, N. Beerens, B. Berkhout, and J.-L. Darlix 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. 77 2003 3939 3949 10.1128/JVI.77.7.3939-3949.2003
61. M. Vallejos, J. Deforges, T.-D.M. Plank, A. Letelier, P. Ramdohr, and C.G. Abraham Activity of the human immunodeficiency virus type 1 cell cycle-dependent internal ribosomal entry site is modulated by IRES trans-acting factors Nucleic Acids Res. 39 2011 6186 6200 10.1093/nar/gkr189
62. T.-D.M. Plank, J.T. Whitehurst, and J.S. Kieft Cell type specificity and structural determinants of IRES activity from the 5′ leaders of different HIV-1 transcripts Nucleic Acids Res. 41 2013 6698 6714 10.1093/nar/gkt358
63. C.B. Buck, X. Shen, M.A. Egan, T.C. Pierson, C.M. Walker, and R.F. Siliciano The human immunodeficiency virus type 1gag gene encodes an internal ribosome entry site J. Virol. 75 2001 181 191 10.1128/JVI.75.1.181-191.2001
64. C.H. Herbreteau, L. Weill, D. Décimo, D. Prévôt, J.-L. Darlix, and B. Sargueil HIV-2 genomic RNA contains a novel type of IRES located downstream of its initiation codon Nat. Struct. Mol. Biol. 12 2005 1001 1007 10.1038/nsmb1011
65. N. Chamond, N. Locker, and B. Sargueil The different pathways of HIV genomic RNA translation Biochem. Soc. Trans. 38 2010 1548 10.1042/BST0381548
66. N. Locker, N. Chamond, and B. Sargueil A conserved structure within the HIV gag open reading frame that controls translation initiation directly recruits the 40S subunit and eIF3 Nucleic Acids Res. 39 2011 2367 2377 10.1093/nar/gkq1118
67. L. Weill, L. James, N. Ulryck, N. Chamond, C.H. Herbreteau, and T. Ohlmann A new type of IRES within gag coding region recruits three initiation complexes on HIV-2 genomic RNA Nucleic Acids Res. 38 2009 1367 1381 10.1093/nar/gkp1109
68. S. de Breyne, N. Chamond, D. Décimo, M.-A. Trabaud, P. André, and B. Sargueil In vitro studies reveal that different modes of initiation on HIV-1 mRNA have different levels of requirement for eukaryotic initiation factor 4F FEBS J. 279 2012 3098 3111 10.1111/j.1742-4658.2012.08689.x
69. Y. Chang, E. Cesarman, M.S. Pessin, F. Lee, J. Culpepper, and D.M. Knowles Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma Science 266 1994 1865 1869
70. L. Bieleski, and S.J. Talbot Kaposi's sarcoma-associated herpesvirus vCyclin open reading frame contains an internal ribosome entry site J. Virol. 75 2001 1864 1869 10.1128/JVI.75.4.1864-1869.2001
71. A. Grundhoff, and D. Ganem Mechanisms governing expression of the v-FLIP gene of Kaposi's sarcoma-associated herpesvirus J. Virol. 75 2001 1857 1863 10.1128/JVI.75.4.1857-1863.2001
72. W. Low, M. Harries, H. Ye, M.-Q. Du, C. Boshoff, and M. Collins Internal ribosome entry site regulates translation of Kaposi's sarcoma-associated herpesvirus FLICE inhibitory protein J. Virol. 75 2001 2938 2945 10.1128/JVI.75.6.2938-2945.2001
73. Z. Othman, M.K. Sulaiman, M.M. Willcocks, N. Ulryck, D.J. Blackbourn, and B. Sargueil Functional analysis of Kaposi's sarcoma-associated herpesvirus vFLIP expression reveals a new mode of IRES-mediated translation RNA 20 2014 1803 1814 10.1261/rna.045328.114
74. A.M. Borman, Y.M. Michel, and K.M. Kean Detailed analysis of the requirements of hepatitis A virus internal ribosome entry segment for the eukaryotic initiation factor complex eIF4F J. Virol. 75 2001 7864 7871 10.1128/JVI.75.17.7864-7871.2001
75. I.K. Ali, L. McKendrick, S.J. Morley, and R.J. Jackson Activity of the hepatitis A virus IRES requires association between the CAP-binding translation initiation factor (eIF4E) and eIF4G J. Virol. 75 2001 7854 7863 10.1128/JVI.75.17.7854-7863.2001
76. G. Meyers Translation of the minor capsid protein of a calicivirus is initiated by a novel termination-dependent reinitiation mechanism J. Biol. Chem. 278 2003 34051 34060 10.1074/jbc.M304874200
77. T.A.A. Pöyry, A. Kaminski, E.J. Connell, C.S. Fraser, and R.J. Jackson 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. 21 2007 3149 3162 10.1101/gad.439507
78. C. Luttermann, and G. Meyers A bipartite sequence motif induces translation reinitiation in feline calicivirus RNA J. Biol. Chem. 282 2007 7056 7065 10.1074/jbc.M608948200
79. M.L. Powell Translational termination-reinitiation in RNA viruses Biochem. Soc. Trans. 38 2010 1558 10.1042/BST0381558
80. C. Luttermann, and G. Meyers The importance of inter- and intramolecular base pairing for translation reinitiation on a eukaryotic bicistronic mRNA Genes Dev. 23 2009 331 344 10.1101/gad.507609
81. M.L. Powell, K.E. Leigh, T.A.A. Pöyry, R.J. Jackson, T.D.K. Brown, and I. Brierley Further characterisation of the translational termination-reinitiation signal of the influenza B virus segment 7 RNA PLoS One 6 2011 e16822 10.1371/journal.pone.0016822
82. C. Luttermann, and G. Meyers Two alternative ways of start site selection in human norovirus reinitiation of translation J. Biol. Chem. 289 2014 11739 11754 10.1074/jbc.M114.554030
83. S. Napthine, R.A. Lever, M.L. Powell, R.J. Jackson, T.D.K. Brown, and I. Brierley Expression of the VP2 protein of murine norovirus by a translation termination-reinitiation strategy PLoS One 4 2009 e8390 10.1371/journal.pone.0008390
84. G. Meyers Characterization of the sequence element directing translation reinitiation in RNA of the calicivirus rabbit hemorrhagic disease virus J. Virol. 81 2007 9623 9632 10.1128/JVI.00771-07
85. M.L. Powell, S. Napthine, R.J. Jackson, I. Brierley, and T.D.K. Brown Characterization of the termination-reinitiation strategy employed in the expression of influenza B virus BM2 protein RNA 14 2008 2394 2406 10.1261/rna.1231008
86. C.M. Horvath, M.A. Williams, and R.A. Lamb Eukaryotic coupled translation of tandem cistrons: identification of the influenza B virus BM2 polypeptide EMBO J. 9 1990 2639 2647
87. S.A. Chappell, G.M. Edelman, and V.P. Mauro A 9-nt segment of a cellular mRNA can function as an internal ribosome entry site (IRES) and when present in linked multiple copies greatly enhances IRES activity Proc. Natl. Acad. Sci. 97 2000 1536 1541 10.1073/pnas.97.4.1536
88. M.C.-Y. Hu, P. Tranque, G.M. Edelman, and V.P. Mauro rRNA-complementarity in the 5′ untranslated region of mRNA specifying the Gtx homeodomain protein: evidence that base- pairing to 18S rRNA affects translational efficiency Proc. Natl. Acad. Sci. 96 1999 1339 1344 10.1073/pnas.96.4.1339
89. M. Niepel, and D.R. Gallie Identification and characterization of the functional elements within the tobacco etch virus 5′ leader required for cap-independent translation J. Virol. 73 1999 9080 9088
90. D.R. Gallie Cap-independent translation conferred by the 5′ leader of tobacco etch virus is eukaryotic initiation factor 4G dependent J. Virol. 75 2001 12141 12152 10.1128/JVI.75.24.12141-12152.2001
91. V. Zeenko, and D.R. Gallie Cap-independent translation of tobacco etch virus is conferred by an RNA pseudoknot in the 5′-leader J. Biol. Chem. 280 2005 26813 26824 10.1074/jbc.M503576200
92. J. Rabl, M. Leibundgut, S.F. Ataide, A. Haag, and N. Ban Crystal structure of the eukaryotic 40S ribosomal subunit in complex with initiation factor 1 Science 331 2011 730 736 10.1126/science.1198308
93. A. Ben-Shem, N.G. de Loubresse, S. Melnikov, L. Jenner, G. Yusupova, and M. Yusupov The structure of the eukaryotic ribosome at 3.0 Å resolution Science 334 2011 1524 1529 10.1126/science.1212642
94. D.C.-Y. Koh, D.X. Liu, and S.-M. Wong A six-nucleotide segment within the 3′ untranslated region of hibiscus chlorotic ringspot virus plays an essential role in translational enhancement J. Virol. 76 2002 1144 1153 10.1128/JVI.76.3.1144-1153.2002
95. Z. Meng, N.L. Jackson, O.D. Shcherbakov, H. Choi, and S.W. Blume The human IGF1R IRES likely operates through a Shine-Dalgarno-like interaction with the G961 loop (E-site) of the 18S rRNA and is kinetically modulated by a naturally polymorphic polyU loop J. Cell. Biochem. 110 2010 531 544 10.1002/jcb.22569
96. R.Z. Akbergenov, S.S. Zhanybekova, R.V. Kryldakov, A. Zhigailov, N.S. Polimbetova, and T. Hohn ARC-1, a sequence element complementary to an internal 18S rRNA segment, enhances translation efficiency in plants when present in the leader or intercistronic region of mRNAs Nucleic Acids Res. 32 2004 239 247 10.1093/nar/gkh176
97. S.A. Chappell, G.M. Edelman, and V.P. Mauro Ribosomal tethering and clustering as mechanisms for translation initiation Proc. Natl. Acad. Sci. 103 2006 18077 18082 10.1073/pnas.0608212103
98. J. Pánek, M. Kolář, J. Vohradský, and L.S. Valášek An evolutionary conserved pattern of 18S rRNA sequence complementarity to mRNA 5′ UTRs and its implications for eukaryotic gene translation regulation Nucleic Acids Res. 41 2013 7625 7634 10.1093/nar/gkt548
99. Y. Yu, T.R. Sweeney, P. Kafasla, R.J. Jackson, T.V. Pestova, and C.U. Hellen The mechanism of translation initiation on Aichivirus RNA mediated by a novel type of picornavirus IRES EMBO J. 30 2011 4423 4436 10.1038/emboj.2011.306
100. T.R. Cech Crawling out of the RNA world Cell 136 2009 599 602 10.1016/j.cell.2009.02.002
101. N. Lehman RNA in evolution Wiley Interdiscip. Rev. - RNA 1 2010 202 213 10.1002/wrna.37
102. E. Martínez-Salas, G. Lozano, J. Fernandez-Chamorro, R. Francisco-Velilla, A. Galan, and R. Diaz RNA-binding proteins impacting on internal initiation of translation Int. J. Mol. Sci. 14 2013 21705 21726 10.3390/ijms141121705
103. M.I. Hertz, D.M. Landry, A.E. Willis, G. Luo, and S.R. Thompson Ribosomal protein S25 dependency reveals a common mechanism for diverse internal ribosome entry sites and ribosome shunting Mol. Cell. Biol. 33 2013 1016 1026 10.1128/MCB.00879-12
104. J.S. Kieft Viral IRES RNA structures and ribosome interactions Trends Biochem. Sci. 33 2008 274 283 10.1016/j.tibs.2008.04.007
105. M. Selmer, C.M. Dunham, F.V. Murphy, A. Weixlbaumer, S. Petry, and A.C. Kelley Structure of the 70S ribosome complexed with mRNA and tRNA Science 313 2006 1935 1942 10.1126/science.1131127