Regulation Mechanisms of Viral IRES-Driven Translation

Trends in Microbiology

Volumn 25, Issue 7, 2017, Pages 546-561

  Lee, Kuo Ming ^a   Chen, Chi Jene ^a   Shih, Shin Ru ^a,b  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^b CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

Author keywords

EV A71; IRES dependent translation; ITAFs; Picornaviruses

Indexed keywords

INITIATION FACTOR; MESSENGER RNA; NUCLEAR PROTEIN; TRANS ACTING FACTOR; VIRAL PROTEIN;

APHTHOVIRUS; CARDIOVIRUS; CELL NUCLEUS; CRICKET PARALYSIS VIRUS; CYTOPLASM; DICISTROVIRIDAE; ENTEROVIRUS; HEPATITIS C VIRUS; HOST CELL; HUMAN; INTERNAL RIBOSOME ENTRY SITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN RNA BINDING; PROTEIN SECONDARY STRUCTURE; PROTEIN SYNTHESIS; REVIEW; RHINOVIRUS; RNA TRANSLATION; RNA VIRUS; RNA VIRUS INFECTION; TAURA SYNDROME VIRUS; TRANSLATION REGULATION; VIRAL GENETICS; VIROGENESIS; VIRUS CELL INTERACTION; VIRUS IDENTIFICATION; VIRUS STRAIN; GENE EXPRESSION REGULATION; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; PICORNAVIRIDAE;

GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERNAL RIBOSOME ENTRY SITES; PICORNAVIRIDAE; PROTEIN BIOSYNTHESIS; RNA VIRUSES;

EID: 85013679239     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2017.01.010     Document Type: Review

References (137)

1. Walsh, D., Mohr, I., Viral subversion of the host protein synthesis machinery. Nat. Rev. Microbiol. 9 (2011), 860–875.
2. Jackson, R.J., The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell. Biol. 11 (2010), 113–127.
3. Komar, A.A., Hatzoglou, M., Cellular IRES-mediated translation: the war of ITAFs in pathophysiological states. Cell Cycle 10 (2011), 229–240.
4. Martinez-Salas, E., RNA-binding proteins impacting on internal initiation of translation. Int. J. Mol. Sci. 14 (2013), 21705–21726.
5. Walters, B., Thompson, S.R., Cap-independent translational control of carcinogenesis. Front. Oncol., 6, 2016, 128.
6. Filbin, M.E., Kieft, J.S., Toward a structural understanding of IRES RNA function. Curr. Opin. Struct. Biol. 19 (2009), 267–276.
7. Jang, S.K., A segment of the 5' nontranslated region of encephalomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation. J. Virol. 62 (1988), 2636–2643.
8. Pelletier, J., Sonenberg, N., Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature 334 (1988), 320–325.
9. Komar, A.A., Hatzoglou, M., Exploring internal ribosome entry sites as therapeutic targets. Front. Oncol., 5, 2015, 233.
10. Hinnebusch, A.G., The scanning mechanism of eukaryotic translation initiation. Annu. Rev. Biochem. 83 (2014), 779–812.
11. Jan, E., A Cap-to-tail guide to mRNA translation strategies in virus-infected cells. Annu. Rev. Virol. 3 (2016), 283–307.
12. Visweswaraiah, J., The beta-hairpin of 40S exit channel protein Rps5/uS7 promotes efficient and accurate translation initiation in vivo. Elife, 4, 2015, e07939.
13. Parsyan, A., mRNA helicases: the tacticians of translational control. Nat. Rev. Mol. Cell. Biol. 12 (2011), 235–245.
14. Lloyd, R.E., Translational control by viral proteinases. Virus Res. 119 (2006), 76–88.
15. Lozano, G., Martinez-Salas, E., Structural insights into viral IRES-dependent translation mechanisms. Curr. Opin. Virol. 12 (2015), 113–120.
16. Kolekar, P., IRESPred: Web server for prediction of cellular and viral internal ribosome entry site (IRES). Sci. Rep., 6, 2016, 27436.
17. Weingarten-Gabbay, S., et al. Comparative genetics. Systematic discovery of cap-independent translation sequences in human and viral genomes. Science, 2016, 10.1126/science.aad4939 Published online January 15, 2016.
18. Shatsky, I.N., Transcriptome-wide studies uncover the diversity of modes of mRNA recruitment to eukaryotic ribosomes. Crit. Rev. Biochem. Mol. Biol. 49 (2014), 164–177.
19. Anderson, E.C., Internal initiation of translation from the human rhinovirus-2 internal ribosome entry site requires the binding of Unr to two distinct sites on the 5' untranslated region. J. Gen. Virol. 88 (2007), 3043–3052.
20. Bailey, J.M., Tapprich, W.E., Structure of the 5' nontranslated region of the coxsackievirus b3 genome: Chemical modification and comparative sequence analysis. J. Virol. 81 (2007), 650–668.
21. Lin, J.Y., Far upstream element binding protein 2 interacts with enterovirus 71 internal ribosomal entry site and negatively regulates viral translation. Nucleic Acids Res. 37 (2009), 47–59.
22. Rivera, V.M., Comparative sequence analysis of the 5' noncoding region of the enteroviruses and rhinoviruses. Virology 165 (1988), 42–50.
23. Pilipenko, E.V., Conserved structural domains in the 5'-untranslated region of picornaviral genomes: an analysis of the segment controlling translation and neurovirulence. Virology 168 (1989), 201–209.
24. Skinner, M.A., New model for the secondary structure of the 5' non-coding RNA of poliovirus is supported by biochemical and genetic data that also show that RNA secondary structure is important in neurovirulence. J. Mol. Biol. 207 (1989), 379–392.
25. Burrill, C.P., Global RNA structure analysis of poliovirus identifies a conserved RNA structure involved in viral replication and infectivity. J. Virol. 87 (2013), 11670–11683.
26. Andino, R., A functional ribonucleoprotein complex forms around the 5' end of poliovirus RNA. Cell 63 (1990), 369–380.
27. Andino, R., Poliovirus RNA synthesis utilizes an RNP complex formed around the 5'-end of viral RNA. EMBO J. 12 (1993), 3587–3598.
28. Lamphear, B.J., et al. Mapping of functional domains in eukaryotic protein synthesis initiation factor 4G (eIF4G) with picornaviral proteases. Implications for cap-dependent and cap-independent translational initiation. J. Biol. Chem. 270 (1995), 21975–21983.
29. Gradi, A., Proteolysis of human eukaryotic translation initiation factor eIF4GII, but not eIF4GI, coincides with the shutoff of host protein synthesis after poliovirus infection. Proc. Natl. Acad. Sci. U.S.A. 95 (1998), 11089–11094.
30. Fletcher, S.P., Jackson, R.J., Pestivirus internal ribosome entry site (IRES) structure and function: elements in the 5' untranslated region important for IRES function. J. Virol. 76 (2002), 5024–5033.
31. Guest, S., Molecular mechanisms of attenuation of the Sabin strain of poliovirus type 3. J. Virol. 78 (2004), 11097–11107.
32. de Breyne, S., Direct functional interaction of initiation factor eIF4G with type 1 internal ribosomal entry sites. Proc. Natl. Acad. Sci. U.S.A. 106 (2009), 9197–9202.
33. King, H.A., The role of IRES trans-acting factors in regulating translation initiation. Biochem. Soc. Trans. 38 (2010), 1581–1586.
34. Martinez-Salas, E., et al. Picornavirus IRES elements: RNA structure and host protein interactions. Virus Res. 206 (2015), 62–73.
35. Kaminski, A., Mechanism of initiation site selection promoted by the human rhinovirus 2 internal ribosome entry site. J. Virol. 84 (2010), 6578–6589.
36. Kafasla, P., Polypyrimidine tract-binding protein stimulates the poliovirus IRES by modulating eIF4G binding. EMBO J. 29 (2010), 3710–3722.
37. Perera, R., Cellular protein modification by poliovirus: the two faces of poly(rC)-binding protein. J. Virol. 81 (2007), 8919–8932.
38. Toyoda, H., Replication of poliovirus requires binding of the poly(rC) binding protein to the cloverleaf as well as to the adjacent C-rich spacer sequence between the cloverleaf and the internal ribosomal entry site. J. Virol. 81 (2007), 10017–10028.
39. Sweeney, T.R., The mechanism of translation initiation on Type 1 picornavirus IRESs. EMBO J. 33 (2014), 76–92.
40. Malnou, C.E., Poliovirus internal ribosome entry segment structure alterations that specifically affect function in neuronal cells: molecular genetic analysis. J. Virol. 76 (2002), 10617–10626.
41. Fiore, J.L., Nesbitt, D.J., An RNA folding motif: GNRA tetraloop-receptor interactions. Q. Rev. Biophys. 46 (2013), 223–264.
42. Lopez de Quinto, S., Martinez-Salas, E., 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 (1997), 4171–4175.
43. Robertson, M.E., 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 (1999), 1167–1179.
44. Gao, Y., Biological function of Foot-and-mouth disease virus non-structural proteins and non-coding elements. Virol J., 13, 2016, 107.
45. Imai, S., An accurately preorganized IRES RNA structure enables eIF4G capture for initiation of viral translation. Nat. Struct. Mol. Biol. 23 (2016), 859–864.
46. Lopez de Quinto, S., IRES interaction with translation initiation factors: functional characterization of novel RNA contacts with eIF3, eIF4B, and eIF4GII. RNA 7 (2001), 1213–1226.
47. Kafasla, P., Polypyrimidine tract binding protein stabilizes the encephalomyocarditis virus IRES structure via binding multiple sites in a unique orientation. Mol. Cell. 34 (2009), 556–568.
48. Jackson, R.J., Alternative mechanisms of initiating translation of mammalian mRNAs. Biochem. Soc. Trans. 33 (2005), 1231–1241.
49. Andreev, D.E., Differential factor requirement to assemble translation initiation complexes at the alternative start codons of foot-and-mouth disease virus RNA. RNA 13 (2007), 1366–1374.
50. Pilipenko, E.V., A cell cycle-dependent protein serves as a template-specific translation initiation factor. Genes Dev. 14 (2000), 2028–2045.
51. Belsham, G.J., Divergent picornavirus IRES elements. Virus Res. 139 (2009), 183–192.
52. Khawaja, A., Understanding the potential of hepatitis C virus internal ribosome entry site domains to modulate translation initiation via their structure and function. Wiley Interdiscip. Rev. RNA 6 (2015), 211–224.
53. Quade, N., et al. Cryo-EM structure of hepatitis C virus IRES bound to the human ribosome at 3.9-A resolution. Nat. Commun., 6, 2015, 7646.
54. Spahn, C.M., Hepatitis C virus IRES RNA-induced changes in the conformation of the 40s ribosomal subunit. Science 291 (2001), 1959–1962.
55. Filbin, M.E., HCV IRES manipulates the ribosome to promote the switch from translation initiation to elongation. Nat. Struct. Mol. Biol. 20 (2013), 150–158.
56. Bhat, P., The beta hairpin structure within ribosomal protein S5 mediates interplay between domains II and IV and regulates HCV IRES function. Nucleic Acids Res. 43 (2015), 2888–2901.
57. Niepmann, M., Hepatitis C virus RNA translation. Curr. Top. Microbiol. Immunol. 369 (2013), 143–166.
58. Hashem, Y., Hepatitis-C-virus-like internal ribosome entry sites displace eIF3 to gain access to the 40S subunit. Nature 503 (2013), 539–543.
59. Jopling, C.L., Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA. Science 309 (2005), 1577–1581.
60. Shimakami, T., Stabilization of hepatitis C virus RNA by an Ago2-miR-122 complex. Proc. Natl. Acad. Sci. U.S.A. 109 (2012), 941–946.
61. Sedano, C.D., Sarnow, P., Hepatitis C virus subverts liver-specific miR-122 to protect the viral genome from exoribonuclease Xrn2. Cell Host Microbe 16 (2014), 257–264.
62. Henke, J.I., microRNA-122 stimulates translation of hepatitis C virus RNA. EMBO J. 27 (2008), 3300–3310.
63. Roberts, A.P., miR-122 activates hepatitis C virus translation by a specialized mechanism requiring particular RNA components. Nucleic Acids Res. 39 (2011), 7716–7729.
64. Goergen, D., Niepmann, M., Stimulation of Hepatitis C Virus RNA translation by microRNA-122 occurs under different conditions in vivo and in vitro. Virus Res. 167 (2012), 343–352.
65. Diaz-Toledano, R., In vitro characterization of a miR-122-sensitive double-helical switch element in the 5' region of hepatitis C virus RNA. Nucleic Acids Res. 37 (2009), 5498–5510.
66. Masaki, T., et al. miR-122 stimulates hepatitis C virus RNA synthesis by altering the balance of viral RNAs engaged in replication versus translation. Cell Host Microbe 17 (2015), 217–228.
67. Luna, J.M., Hepatitis C virus RNA functionally sequesters miR-122. Cell 160 (2015), 1099–1110.
68. Kerr, C.H., Jan, E., Commandeering the ribosome: lessons learned from Dicistroviruses about translation. J. Virol. 90 (2016), 5538–5540.
69. Wilson, J.E., Initiation of protein synthesis from the A site of the ribosome. Cell 102 (2000), 511–520.
70. Muhs, M., Cryo-EM of ribosomal 80S complexes with termination factors reveals the translocated cricket paralysis virus IRES. Mol. Cell 57 (2015), 422–432.
71. Fernandez, I.S., Initiation of translation by cricket paralysis virus IRES requires its translocation in the ribosome. Cell 157 (2014), 823–831.
72. Ruehle, M.D., A dynamic RNA loop in an IRES affects multiple steps of elongation factor-mediated translation initiation. Elife, 4, 2015, e08146.
73. Landry, D.M., RPS25 is essential for translation initiation by the Dicistroviridae and hepatitis C viral IRESs. Genes Dev. 23 (2009), 2753–2764.
74. Muhs, M., Structural basis for the binding of IRES RNAs to the head of the ribosomal 40S subunit. Nucleic Acids Res. 39 (2011), 5264–5275.
75. Colussi, T.M., Initiation of translation in bacteria by a structured eukaryotic IRES RNA. Nature 519 (2015), 110–113.
76. Meerovitch, K., A cellular protein that binds to the 5'-noncoding region of poliovirus RNA: implications for internal translation initiation. Genes Dev. 3 (1989), 1026–1034.
77. Luz, N., Beck, E., Interaction of a cellular 57-kilodalton protein with the internal translation initiation site of foot-and-mouth disease virus. J. Virol. 65 (1991), 6486–6494.
78. Singh, G., The cellular EJC interactome reveals higher-order mRNP structure and an EJC-SR protein nexus. Cell 151 (2012), 750–764.
79. Flather, D., Semler, B.L., Picornaviruses and nuclear functions: targeting a cellular compartment distinct from the replication site of a positive-strand RNA virus. Front. Microbiol., 6, 2015, 594.
80. Pilipenko, E.V., Cell-specific proteins regulate viral RNA translation and virus-induced disease. EMBO J. 20 (2001), 6899–6908.
81. Hunt, S.L., 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. 13 (1999), 437–448.
82. Boussadia, O., Unr is required in vivo for efficient initiation of translation from the internal ribosome entry sites of both rhinovirus and poliovirus. J. Virol. 77 (2003), 3353–3359.
83. Bedard, K.M., A nucleo-cytoplasmic SR protein functions in viral IRES-mediated translation initiation. EMBO J. 26 (2007), 459–467.
84. Lin, J.Y., mRNA decay factor AUF1 binds the internal ribosomal entry site of enterovirus 71 and inhibits virus replication. PLoS One, 9, 2014, e103827.
85. Lin, J.Y., HuR and Ago2 bind the internal ribosome entry site of Enterovirus 71 and promote virus translation and replication. PLoS One, 10, 2015, e0140291.
86. Lin, J.Y., Heterogeneous nuclear ribonuclear protein K interacts with the enterovirus 71 5' untranslated region and participates in virus replication. J. Gen. Virol. 89 (2008), 2540–2549.
87. Lin, J.Y., hnRNP A1 interacts with the 5' untranslated regions of enterovirus 71 and Sindbis virus RNA and is required for viral replication. J. Virol. 83 (2009), 6106–6114.
88. Huang, P.N., Far upstream element binding protein 1 binds the internal ribosomal entry site of enterovirus 71 and enhances viral translation and viral growth. Nucleic Acids Res. 39 (2011), 9633–9648.
89. Weng, K.F., A cytoplasmic RNA virus generates functional viral small RNAs and regulates viral IRES activity in mammalian cells. Nucleic Acids Res. 42 (2014), 12789–12805.
90. Doronina, V.A., Dissection of a co-translational nascent chain separation event. Biochem. Soc. Trans. 36 (2008), 712–716.
91. Kempf, B.J., Barton, D.J., Poliovirus 2A(Pro) increases viral mRNA and polysome stability coordinately in time with cleavage of eIF4G. J. Virol. 82 (2008), 5847–5859.
92. Sun, D., Roles of the picornaviral 3C proteinase in the viral life cycle and host cells. Viruses, 8, 2016, 82.
93. Zhang, B., RNA interaction and cleavage of poly(C)-binding protein 2 by hepatitis A virus protease. Biochem. Biophys. Res. Commun. 364 (2007), 725–730.
94. Hung, C.T., Additive promotion of viral internal ribosome entry site-mediated translation by Far Upstream Element-Binding Protein 1 and an Enterovirus 71-induced cleavage product. PLoS Pathog., 12, 2016, e1005959.
95. Lloyd, R.E., Enterovirus control of translation and RNA granule stress responses. Viruses, 8, 2016, 93.
96. Reineke, L.C., Large G3BP-induced granules trigger eIF2alpha phosphorylation. Mol. Biol. Cell 23 (2012), 3499–3510.
97. Fung, G., Production of a dominant-negative fragment due to G3BP1 cleavage contributes to the disruption of mitochondria-associated protective stress granules during CVB3 infection. PLoS One, 8, 2013, e79546.
98. Pineiro, D., Gemin5 promotes IRES interaction and translation control through its C-terminal region. Nucleic Acids Res. 41 (2013), 1017–1028.
99. Chen, L.L., Enterovirus 71 infection cleaves a negative regulator for viral internal ribosomal entry site-driven translation. J. Virol. 87 (2013), 3828–3838.
100. Kung, Y.A., et al. Control of the negative IRES trans-acting factor KHSRP by ubiquitination. Nucleic Acids Res. 45 (2017), 271–287.
101. Kim, C.S., An RNA-binding protein, hnRNP A1, and a scaffold protein, septin 6, facilitate hepatitis C virus replication. J. Virol. 81 (2007), 3852–3865.
102. Rozovics, J.M., et al. Picornavirus modification of a host mRNA decay protein. mBio, 3, 2012 e00431-12.
103. Cathcart, A.L., Cellular mRNA decay protein AUF1 negatively regulates enterovirus and human rhinovirus infections. J. Virol. 87 (2013), 10423–10434.
104. Lawrence, P., The nuclear protein Sam68 is cleaved by the FMDV 3C protease redistributing Sam68 to the cytoplasm during FMDV infection of host cells. Virology 425 (2012), 40–52.
105. McBride, A.E., Human protein Sam68 relocalization and interaction with poliovirus RNA polymerase in infected cells. Proc. Natl. Acad. Sci. U.S.A. 93 (1996), 2296–2301.
106. Zhang, H., Nuclear protein Sam68 interacts with the Enterovirus 71 internal ribosome entry site and positively regulates viral protein translation. J. Virol. 89 (2015), 10031–10043.
107. Liberman, N., DAP5 associates with eIF2beta and eIF4AI to promote Internal Ribosome Entry Site driven translation. Nucleic Acids Res. 43 (2015), 3764–3775.
108. Hanson, P.J., Cleavage of DAP5 by coxsackievirus B3 2A protease facilitates viral replication and enhances apoptosis by altering translation of IRES-containing genes. Cell Death Differ. 23 (2016), 828–840.
109. Nicholson, B.L., White, K.A., Functional long-range RNA-RNA interactions in positive-strand RNA viruses. Nat. Rev. Microbiol. 12 (2014), 493–504.
110. Paek, K.Y., Translation initiation mediated by RNA looping. Proc. Natl. Acad. Sci. U.S.A. 112 (2015), 1041–1046.
111. Chamond, N., 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. 42 (2014), 10373–10384.
112. Asnani, M., PCBP2 enables the cadicivirus IRES to exploit the function of a conserved GRNA tetraloop to enhance ribosomal initiation complex formation. Nucleic Acids Res. 44 (2016), 9902–9917.
113. Chen, J., Coupling of mRNA structure rearrangement to ribosome movement during bypassing of non-coding regions. Cell 163 (2015), 1267–1280.
114. Nair, V.P., Endoplasmic reticulum stress induced synthesis of a novel viral factor mediates efficient replication of Genotype-1 Hepatitis E Virus. PLoS Pathog., 12, 2016, e1005521.
115. Pirakitikulr, N., The coding region of the HCV genome contains a network of regulatory RNA structures. Mol. Cell 62 (2016), 111–120.
116. Spitale, R.C., RNA structural analysis by evolving SHAPE chemistry. Wiley Interdiscip. Rev. RNA 5 (2014), 867–881.
117. Brown, M.C., Gromeier, M., Cytotoxic and immunogenic mechanisms of recombinant oncolytic poliovirus. Curr. Opin. Virol. 13 (2015), 81–85.
118. Kaufman, H.L., Oncolytic viruses: a new class of immunotherapy drugs. Nat. Rev. Drug Discov. 14 (2015), 642–662.
119. Paek, K.Y., RNA-binding protein hnRNP D modulates internal ribosome entry site-dependent translation of hepatitis C virus RNA. J. Virol. 82 (2008), 12082–12093.
120. Hellen, C.U., A cytoplasmic 57-kDa protein 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. U.S.A. 90 (1993), 7642–7646.
121. Hunt, S.L., Jackson, R.J., Polypyrimidine-tract binding protein (PTB) is necessary, but not sufficient, for efficient internal initiation of translation of human rhinovirus-2 RNA. RNA 5 (1999), 344–359.
122. Yi, M., Functional significance of the interaction of hepatitis A virus RNA with glyceraldehyde 3-phosphate dehydrogenase (GAPDH): opposing effects of GAPDH and polypyrimidine tract binding protein on internal ribosome entry site function. J. Virol. 74 (2000), 6459–6468.
123. Verma, B., Polypyrimidine tract-binding protein interacts with coxsackievirus B3 RNA and influences its translation. J. Gen. Virol. 91 (2010), 1245–1255.
124. Sean, P., Altered interactions between stem-loop IV within the 5' noncoding region of coxsackievirus RNA and poly(rC) binding protein 2: effects on IRES-mediated translation and viral infectivity. Virology 389 (2009), 45–58.
125. Walter, B.L., Differential utilization of poly(rC) binding protein 2 in translation directed by picornavirus IRES elements. RNA 5 (1999), 1570–1585.
126. Kim, Y.K., Jang, S.K., La protein is required for efficient translation driven by encephalomyocarditis virus internal ribosomal entry site. J. Gen. Virol. 80 (1999), 3159–3166.
127. Ali, N., Human La antigen is required for the hepatitis C virus internal ribosome entry site-mediated translation. J. Biol. Chem. 275 (2000), 27531–27540.
128. Ray, P.S., Das, S., La autoantigen is required for the internal ribosome entry site-mediated translation of Coxsackievirus B3 RNA. Nucleic Acids Res. 30 (2002), 4500–4508.
129. Cordes, S., La autoantigen suppresses IRES-dependent translation of the hepatitis A virus. Biochem. Biophys. Res. Commun. 368 (2008), 1014–1019.
130. Jiang, X., Suppression of La antigen exerts potential antiviral effects against hepatitis A virus. PLoS One, 9, 2014, e101993.
131. Andreev, D.E., Glycyl-tRNA synthetase specifically binds to the poliovirus IRES to activate translation initiation. Nucleic Acids Res. 40 (2012), 5602–5614.
132. Pacheco, A., A novel role for Gemin5 in mRNA translation. Nucleic Acids Res. 37 (2009), 582–590.
133. Hwang, B., hnRNP L is required for the translation mediated by HCV IRES. Biochem. Biophys. Res. Commun. 378 (2009), 584–588.
134. Kim, J.H., A cellular RNA-binding protein enhances internal ribosomal entry site-dependent translation through an interaction downstream of the hepatitis C virus polyprotein initiation codon. Mol. Cell. Biol. 24 (2004), 7878–7890.
135. Waggoner, S., Sarnow, P., Viral ribonucleoprotein complex formation and nucleolar-cytoplasmic relocalization of nucleolin in poliovirus-infected cells. J. Virol. 72 (1998), 6699–6709.
136. Izumi, R.E., Nucleolin stimulates viral internal ribosome entry site-mediated translation. Virus Res. 76 (2001), 17–29.
137. Fitzgerald, K.D., Viral proteinase requirements for the nucleocytoplasmic relocalization of cellular splicing factor SRp20 during picornavirus infections. J. Virol. 87 (2013), 2390–2400.