A distinct class of internal ribosomal entry site in members of the Kobuvirus and proposed Salivirus and Paraturdivirus genera of the Picornaviridae

Journal of Virology

Volumn 86, Issue 3, 2012, Pages 1468-1486

  Sweeney, Trevor R ^a   Dhote, Vidya ^a   Yu, Yingpu ^a   Hellen, Christopher U T ^a  

^a SUNY DOWNSTATE MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 4G; MESSENGER RNA;

5' UNTRANSLATED REGION; ARTICLE; BINDING AFFINITY; CODON; INTERNAL RIBOSOME ENTRY SITE; KOBUVIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PARATURDIVIRUS; PICORNAVIRUS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; RNA BINDING; RNA SEQUENCE; SALIVIRUS; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; TRANSLATION INITIATION; VIRUS GENOME; VIRUS ISOLATION; VIRUS MORPHOLOGY;

5' UNTRANSLATED REGIONS; ANIMALS; BASE SEQUENCE; HUMANS; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PICORNAVIRIDAE; PROTEIN BIOSYNTHESIS; RIBOSOMES; RNA, VIRAL;

AICHI VIRUS; BK POLYOMAVIRUS; BOVINE KOBUVIRUS; KOBUVIRUS; OVIS ARIES; PICORNAVIRIDAE;

EID: 84857069886     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.05862-11     Document Type: Article

References (96)

1. Abaeva IS, Marintchev A, Pisareva VP, Hellen CU, Pestova TV. 2011. Bypassing of stems versus linear base-by-base inspection of mammalian mRNAs during ribosomal scanning. EMBO J. 30:115-129
2. Ali IK, McKendrick L, Morley SJ, Jackson RJ. 2001. Activity of the hepatitis A virus IRES requires association between the cap-binding translation initiation factor (eIF4E) and eIF4G. J. Virol. 75:7854 -7863.
3. Bailey JM, Tapprich WE. 2007. Structure of the 5′ nontranslated region of the coxsackievirus B3 genome: chemical modification and comparative sequence analysis. J. Virol. 81:650-668.
4. Bassili G, et al. 2004. Sequence and secondary structure requirements in a highly conserved element for foot-and-mouth disease virus internal ribosome entry site activity and eIF4G binding. J. Gen. Virol. 85:2555-2565.
5. Belsham GJ, Jackson RJ. 2000. Translation initiation on picornavirus RNA, p. 869-900. In Sonenberg N, Hershey JWB, Mathews MB (ed.), Translational control of gene expression. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
6. Botstein D. 1980. A theory of modular evolution for bacteriophages. Ann. N. Y. Acad. Sci. 354:484-490.
7. Brown EA, Zajac AJ, Lemon SM. 1994. In vitro characterization of an internal ribosomal entry site (IRES) present within the 5′ nontranslated region of hepatitis A virus RNA: comparison with the IRES of encephalomyocarditis virus. J. Virol. 68:1066 -1074.
8. Chard LS, Bordeleau ME, Pelletier J, Tanaka J, Belsham GJ. 2006. Hepatitis C virus-related internal ribosome entry sites are found in multiple genera of the family Picornaviridae. J. Gen. Virol. 87:927-936.
9. Clark AT, Robertson ME, Conn GL, Belsham GJ. 2003. Conserved nucleotides within the J domain of the encephalomyocarditis virus internal ribosome entry site are required for activity and for interaction with eIF4G. J. Virol. 77:12441-12449.
10. de Breyne S, Yu Y, Pestova TV, Hellen CU. 2008. Factor requirementsfor translation initiation on the Simian picornavirus internal ribosomal entry site. RNA 14:367-380.
11. de Breyne S, Yu Y, Unbehaun A, Pestova TV, Hellen CUT. 2009. Direct functional interaction of initiation factor eIF4G with type 1 internal ribosomal entry sites. Proc. Natl. Acad. Sci. U. S. A. 106:9197-9202.
12. Dildine SL, Semler BL. 1989. The deletion of 41 proximal nucleotides reverts a poliovirus mutant containing a temperature-sensitive lesion in the 5′ noncoding region of genomic RNA. J. Virol. 63:847- 862.
13. Drexler JF, et al. 2011. Aichi virus shedding in high concentrations in patients with acute diarrhea. Emerg. Infect. Dis. 17:1544-1548.
14. Easton LE, Locker N, Lukavsky PJ. 2009. Conserved functional domains and a novel tertiary interaction near the pseudoknot drive translational activity of hepatitis C virus and hepatitis C virus-like internal ribosome entry sites. Nucleic Acids Res. 37:5537-5549.
15. Evstafieva AG, Ugarova TY, Chernov BK, Shatsky IN. 1991. A complex RNA sequence determines the internal initiation of encephalomyocarditis virus RNA translation. Nucleic Acids Res. 19:665- 671.
16. Gamarnik AV, Andino R. 2000. Interactions of viral protein 3CD and poly(rC) binding protein with the 5′ untranslated region of the poliovirus genome. J. Virol. 74:2219-2226.
17. Greninger AL, et al. 2009. The complete genome of klassevirus-a novel picornavirus in pediatric stool. Virol. J. 6:82.
18. Gruber AR, Lorenz R, Bernhart SH, Neuböck R, Hofacker IL. The Vienna RNA websuite. Nucleic Acids Res. 36:W70-W74.
19. Haller AA, Semler BL. 1992. Linker scanning mutagenesis of the internal ribosome entry site of poliovirus RNA. J. Virol. 66:5075-5086.
20. Han X, Zhang W, Xue Y, Shao S. 2011. Sequence analysis reveals mosaic genome of Aichi virus. Virol. J. 8:390.
21. Hellen CU, de Breyne S. 2007. A distinct group of hepacivirus/pestiviruslike internal ribosomal entry sites in members of diverse picornavirus genera: evidence for modular exchange of functional noncoding RNA elements by recombination. J. Virol. 81:5850 -5863.
22. Heuser W, Kaleta E, Giesow K, Keil GM, Knowles NJ. 2010. Genome sequence of virus X, a picornavirus isolated from a spur-thighed tortoise (Testudo graeca). Abstr. 16th Meet. Eur. Study Group Mol. Biol. Picornaviruses, abstr. H15.
23. Hollister JR, Vagnozzi A, Knowles NJ, Rieder E. 2008. Molecular and phylogenetic analyses of bovine rhinovirus type 2 shows it is closely related to foot-and-mouth disease virus. Virology 373:411- 425.
24. Holmes EC. 2009. The evolution and emergence of RNA viruses. Oxford series in ecology and evolution (OSEE). Oxford University Press, Oxford, United Kingdom.
25. Holtz LR, et al. 2009. Klassevirus 1, a previously undescribed member of the family Picornaviridae, is globally widespread. Virol. J. 6:86.
26. Honkavuori KS, et al. 2011. Novel picornavirus in Turkey poults with hepatitis, California, U. S. A. Emerg. Infect. Dis. 17:480-487.
27. Huang T, et al. 2009. Evidence of recombination and genetic diversity in human rhinoviruses in children with acute respiratory infection. PLoS One 4:e6355.
28. Jackson RJ, Hellen CUT, Pestova TV. 2010. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell Biol. 11:113-127.
29. Jang SK, Pestova TV, Hellen CUT, Witherell GW, Wimmer E. 1990. Cap-independent translation of picornavirus RNAs: structure and function of the internal ribosomal entry site. Enzyme 44:292-309.
30. Kafasla P, et al. 2009. Polypyrimidine tract binding protein stabilizes the encephalomyocarditis virus IRES structure via binding multiple sites in a unique orientation. Mol. Cell 34:556-568.
31. Kafasla P, Morgner N, Robinson CV, Jackson RJ. 2010. Polypyrimidine tract-binding protein stimulates the poliovirus IRES by modulating eIF4G binding. EMBO J. 29:3710-3722.
32. Kaminski A, Hunt SL, Gibbs CL, Jackson RJ. 1994. Internal initiation of mRNA translation in eukaryote, p. 115-155. In Setlow JK (ed.), Genetic engineering, vol. 16. Plenum Press, New York, NY.
33. Kapoor A, et al. 2011. Characterization of a canine homolog of human Aichivirus. J. Virol. 85:11520-11525.
34. Kapoor A, et al. 2008. A highly prevalent and genetically diversified Picornaviridae genus in south Asian children. Proc. Natl. Acad. Sci. U. S. A. 105:20482-20487.
35. Kapoor A, et al. 2008. A highly divergent picornavirus in a marine mammal. J. Virol. 82:311-320.
36. Knudsen B, Hein J. 2003. Pfold: RNA secondary structure prediction using stochastic context-free grammars. Nucleic Acids Res. 31:3423-3428.
37. Kofstad T, Jonassen CM. 2011. Screening of feral and wood pigeons for viruses harbouring a conserved mobile viral element: characterization of novel astroviruses and picornaviruses. PLoS One 6:e25964.
38. Kolupaeva VG, de Breyne S, Pestova TV, Hellen CU. 2007. In vitro reconstitution and biochemical characterization of translation initiation by internal ribosomal entry. Methods Enzymol. 430:409-439.
39. Kolupaeva VG, Lomakin IB, Pestova TV, Hellen CU. 2003. 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. 23:687-698.
40. Le Gall O, Candresse T, Dunez J. 1995. Transfer of the 3′ non-translated region of grapevine chrome mosaic virus RNA-1 by recombination to tomato black ring virus RNA-2 in pseudorecombinant isolates. J. Gen. Virol. 76:1285-1289.
41. Li L, et al. 2011. Viruses in diarrhetic dogs include novel kobuviruses and sapoviruses. J. Gen. Virol. 92:2534 -2541.
42. Li L, et al. 2009. A novel picornavirus associated with gastroenteritis. J. Virol. 83:12002-12006.
43. Lomakin IB, Shirokikh NE, Yusupov MM, Hellen CU, Pestova TV. 2006. The fidelity of translation initiation: reciprocal activities of eIF1, IF3 and YciH. EMBO J. 25:196 -210.
44. Lomakin IB, Hellen CUT, Pestova TV. 2000. 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. 20:6019-6029.
45. López de Quinto S, 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- 4175.
46. Lukashev AN, et al. 2005. Recombination in circulating human enterovirus B: independent evolution of structural and non-structural genome regions. J. Gen. Virol. 86:3281-3290.
47. Lukavsky PJ. 2009. Structure and function of HCV IRES domains. Virus Res. 139:166 -171.
48. Marcotrigiano J, et al. 2001. A conserved HEAT domain within eIF4G directs assembly of the translation initiation machinery. Mol. Cell 7:193-203.
49. McIntyre CL, McWilliam Leitch EC, Savolainen-Kopra C, Hovi T, Simmonds P. 2010. Analysis of genetic diversity and sites of recombination in human rhinovirus species C. J. Virol. 84:10297-10310.
50. Meulewaeter F, et al. 2004. Conservation of RNA structures enables TNV and BYDV 5′ and 3′ elements to cooperate synergistically in capindependent translation. Nucleic Acids Res. 32:1721-1730.
51. Nagashima S, Sasaki J, Taniguchi K. 2005. The 5′-terminal region of the Aichi virus genome encodes cis-acting replication elements required for positive- and negative-strand RNA synthesis. J. Virol. 79:6918-6931.
52. Nakashima N, Uchiumi T. 2009. Functional analysis of structural motifs in dicistroviruses. Virus Res. 139:137-147.
53. Nicholson BL, Wu B, Chevtchenko I, White KA. 2010. Tombusvirus recruitment of host translational machinery via the 3′ UTR. RNA 16: 1402-1419.
54. Niepmann M. 2009. Internal translation initiation of picornaviruses and hepatitis C virus. Biochim. Biophys. Acta 1789:529-541.
55. Oberste MS, Peñaranda S, Pallansch MA. 2004. RNA recombination plays a major role in genomic change during circulation of coxsackie B viruses. J. Virol. 78:2948-2955.
56. Pause A, Methot N, Svitkin Y, Merrick WC, Sonenberg N. 1994. Dominant negative mutants of mammalian translation initiation factor eIF-4A define a critical role for eIF-4F in cap-dependent and capindependent initiation of translation. EMBO J. 13:1205-1215.
57. Pestova TV, Borukhov SI, Hellen CU. 1998. Eukaryotic ribosomes require initiation factors 1 and 1A to locate initiation codons. Nature 394: 854-859.
58. Pestova TV, de Breyne S, Pisarev AV, Abaeva IS, Hellen CUT. 2008. eIF2-dependent and eIF2-independent modes of initiation on the CSFV IRES: a common role of domain II. EMBO J. 27:1060-1072.
59. Pestova TV, Hellen CUT. 1999. Internal initiation of translation of bovine viral diarrhea virus RNA. Virology 258:249 -256.
60. Pestova TV, Hellen CUT. 2001. Preparation and activity of synthetic unmodified mammalian tRNAi(Met) in initiation of translation in vitro. RNA 7:1496 -1505.
61. Pestova TV, Hellen CUT. 2003. Translation elongation after assembly of ribosomes on the Cricket paralysis virus internal ribosomal entry site without initiation factors or initiator tRNA. Genes Dev. 17:181-186.
62. Pestova TV, Hellen CUT, Shatsky IN. 1996. Canonical eukaryotic initiation factors determine initiation of translation by internal ribosomal entry. Mol. Cell. Biol. 16:6859-6869.
63. Pestova TV, Hellen CU, Wimmer E. 1991. Translation of poliovirus RNA: role of an essential cis-acting oligopyrimidine element within the 5′ nontranslated region and involvement of a cellular 57-kilodalton protein. J. Virol. 65:6194-6204.
64. Pestova TV, Hellen CU, Wimmer E. 1994. A conserved AUG triplet in the 5′ nontranslated region of poliovirus can function as an initiation codon in vitro and in vivo. Virology 204:729 -737.
65. Pestova TV, Shatsky IN, Hellen CUT. 1996. Functional dissection of eukaryotic initiation factor 4F: the 4A subunit and the central domain of the 4G subunit are sufficient to mediate internal entry of 43S preinitiation complexes. Mol. Cell. Biol. 16:6870-6878.
66. Pestova TV, Shatsky IN, Fletcher SP, Jackson RJ, Hellen CUT. 1998. 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. 12:67-83.
67. Phan TG, et al. 2011. The fecal viral flora of wild rodents. PLoS Pathog. 7:e1002218.
68. Pilipenko EV, et al. 2000. A cell cycle-dependent protein serves as a template-specific translation initiation factor. Genes Dev. 14:2028-2045.
69. Pisarev AV, et al. 2004. Functional and structural similarities between the internal ribosome entry sites of hepatitis C virus and porcine teschovirus, a picornavirus. J. Virol. 78:4487- 4497.
70. Pisarev AV, Unbehaun A, Hellen CU, Pestova TV. 2007. Assembly and analysis of eukaryotic translation initiation complexes. Methods Enzymol. 430:147-177.
71. Pisareva VP, Pisarev AV, Komar AA, Hellen CU, Pestova TV. 2008. Translation initiation on mammalian mRNAs with structured 5′ UTRs requires DExH-box protein DHX29. Cell 135:1237-1250.
72. Reeder J, Steffen P, Giegerich R. 2007. pknotsRG: RNA pseudoknot folding including near-optimal structures and sliding windows. Nucleic Acids Res. 35:W320-W324.
73. Reuter G, Boldizsár A, Pankovics P. 2009. Complete nucleotide and amino acid sequences and genetic organization of porcine kobuvirus, a member of a new species in the genus Kobuvirus, family Picornaviridae. Arch. Virol. 154:101-108.
74. Reuter G, Boros A, Pankovics P. 2011. Kobuviruses-a comprehensive review. Rev. Med. Virol. 21:32-41.
75. Reuter G, Boros A, Pankovics P, Egyed L. 2010. Kobuvirus in domestic sheep, Hungary. Emerg. Infect. Dis. 16:869-870.
76. Robertson ME, Seamons RA, Belsham GJ. 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 5:1167-1179.
77. Robertson MP, Igel H, Baertsch R, Haussler D, Ares M, Jr., Scott WG. 2005. The structure of a rigorously conserved RNA element within the SARS virus genome. PLoS Biol. 3:e5.
78. Sasaki J, et al. 2001. Construction of an infectious cDNA clone of Aichi virus (a new member of the family Picornaviridae) and mutational analysis of a stem-loop structure at the 5′ end of the genome. J. Virol. 75: 8021-8030.
79. Sasaki J, Taniguchi K. 2003. The 5′-end sequence of the genome of Aichi virus, a picornavirus, contains an element critical for viral RNA encapsidation. J. Virol. 77:3542-3548.
80. Sato K, Hamada M, Asai K, Mituyama T. 2009. CENTROIDFOLD: a web server for RNA secondary structure prediction. Nucleic Acids Res. 37:W277-W280.
81. Shan T, et al. 2010. Picornavirus salivirus/klassevirus in children with diarrhea, China. Emerg. Infect. Dis. 16:1303-1305.
82. Simmonds P. 2006. Recombination and selection in the evolution of picornaviruses and other mammalian positive-stranded RNA viruses. J. Virol. 80:11124 -11140.
83. Skabkin MA, et al. 2010. Activities of Ligatin and MCT-1/DENR in eukaryotic translation initiation and ribosomal recycling. Genes Dev. 24: 1787-1801.
84. Smura T, et al. 2007. Enterovirus surveillance reveals proposed new serotypes and provides new insight into enterovirus 5′-untranslated region evolution. J. Gen. Virol. 88:2520 -2526.
85. Wagner A, Stadler PF. 1999. Viral RNA and evolved mutational robustness. J. Exp. Zool. 285:119-127.
86. Wang Z, Kraft JJ, Hui AY, Miller WA. 2010. Structural plasticity of Barley yellow dwarf virus-like cap-independent translation elements in four genera of plant viral RNAs. Virology 402:177-186.
87. Willcocks MM, et al. 2011. Structural features of the Seneca Valley virus internal ribosome entry site element; a picornavirus with a pestivirus-like IRES. J. Virol. 85:4452- 4461.
88. Wilson JE, Pestova TV, Hellen CUT, Sarnow P. 2000. Initiation of protein synthesis from the A site of the ribosome. Cell 102:511-520.
89. Woo PC, et al. 2010. Comparative analysis of six genome sequences of three novel picornaviruses, turdiviruses 1, 2 and 3, in dead wild birds, and proposal of two novel genera, Orthoturdivirus and Paraturdivirus, in the family Picornaviridae. J. Gen. Virol. 91:2433-2448.
90. Yamashita T, et al. 2003. Isolation and characterization of a new species of kobuvirus associated with cattle. J. Gen. Virol. 84:3069-3077.
91. Yamashita T, et al. 1998. Complete nucleotide sequence and genetic organization of Aichi virus, a distinct member of the Picornaviridae associated with acute gastroenteritis in humans. J. Virol. 72: 8408 - 8412.
92. Yozwiak NL, et al. 2010. Human enterovirus 109: a novel interspecies recombinant enterovirus isolated from a case of acute pediatric respiratory illness in Nicaragua. J. Virol. 84:9047-9058.
93. Yu JM, et al. 2011. Analysis and characterization of the complete genome of a member of a new species of kobuvirus associated with swine. Arch. Virol. 156:747-751.
94. Yu Y, Abaeva IS, Marintchev A, Pestova TV, Hellen CUT. 2011. Common conformational changes induced in type 2 picornavirus IRESs by cognate trans-acting factors. Nucleic Acids Res. 39:4851- 4865.
95. Yu Y, et al. 2011. The mechanism of translation initiation on Aichi virus RNA mediated by a novel type of picornavirus IRES. EMBO J. 30: 4423-4436.
96. Zuker M. 2003. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31:3406-3415.