The mechanism of translation initiation on type 1 picornavirus IRESs

EMBO Journal

Volumn 33, Issue 1, 2014, Pages 76-92

  Sweeney, Trevor R ^a   Abaeva, Irina S ^a   Pestova, Tatyana V ^a   Hellen, Christopher U T ^a  

^a Downstate Health Sciences University   (United States)

Author keywords

EIF4G; IRES; PCBP2; Poliovirus; Translation initiation

Indexed keywords

INITIATION FACTOR 1; INITIATION FACTOR 1A; INITIATION FACTOR 2; INITIATION FACTOR 3; INITIATION FACTOR 4A; INITIATION FACTOR 4B; MESSENGER RNA; INITIATION FACTOR; RNA BINDING PROTEIN;

ARTICLE; BASE PAIRING; BINDING SITE; BOVINE ENTEROVIRUS; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; ENTEROVIRUS 71; IN VITRO STUDY; INTERNAL RIBOSOME ENTRY SITE; PESTIVIRUS; PICORNAVIRUS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; RIBOSOME; RNA BINDING; START CODON; STEREOSPECIFICITY; TRANSLATION INITIATION; ENTEROVIRUS; GENETICS; METABOLISM; PHYSIOLOGY; POLIOMYELITIS VIRUS; RNA TRANSLATION;

CODON, INITIATOR; ENTEROVIRUS A, HUMAN; ENTEROVIRUS, BOVINE; EUKARYOTIC INITIATION FACTORS; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; POLIOVIRUS; RIBOSOMES; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 84894646564     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1002/embj.201386124     Document Type: Article

References (64)

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. Anderson EC, Hunt SL, Jackson RJ (2007) 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: 3043 - 3052
3. Andreev DE, Fernandez-Miragall O, Ramajo J, Dmitriev SE, Terenin IM, Martinez-Salas E, Shatsky IN (2007) Differential factor requirement to assemble translation initiation complexes at the alternative start codons of foot-and-mouth disease virus RNA. RNA 13: 1366 - 1374
4. Andreev D, Hauryliuk V, Terenin I, Dmitriev S, Ehrenberg M, Shatsky I (2008) The bacterial toxin RelE induces specific mRNA cleavage in the A site of the eukaryote ribosome. RNA 14: 233 - 239
5. Andreev DE, Hirnet J, Terenin IM, Dmitriev SE, Niepmann M, Shatsky IN (2012) Glycyl-tRNA synthetase specifically binds to the poliovirus IRES to activate translation initiation. Nucleic Acids Res 40: 5602 - 5614
6. Bedard KM, Daijogo S, Semler BL (2007) A nucleo-cytoplasmic SR protein functions in viral IRES-mediated translation initiation. EMBO J 26: 459 - 467
7. Blyn LB, Swiderek KM, Richards O, Stahl DC, Semler BL, Ehrenfeld E (1996) Poly(rC) binding protein 2 binds to stem-loop IV of the poliovirus RNA 5′ noncoding region: identification by automated liquid chromatography-tandem mass spectrometry. Proc Natl Acad Sci USA 93: 11115 - 11120
8. Blyn LB, Towner JS, Semler BL, Ehrenfeld E (1997) Requirement of poly(rC) binding protein 2 for translation of poliovirus RNA. J Virol 71: 6243 - 6246
9. Borman A, Howell MT, Patton JG, Jackson RJ (1993) The involvement of a spliceosome component in internal initiation of human rhinovirus RNA translation. J Gen Virol 74: 1775 - 1788
10. Borman AM, Bailly JL, Girard M, Kean KM (1995) Picornavirus internal ribosome entry segments: comparison of translation efficiency and the requirements for optimal internal initiation of translation in vitro. Nucleic Acids Res 23: 3656 - 3663
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 USA 106: 9197 - 9202
12. Choi K, Kim JH, Li X, Paek KY, Ha SH, Ryu SH, Wimmer E, Jang SK (2004) Identification of cellular proteins enhancing activities of internal ribosomal entry sites by competition with oligodeoxynucleotides. Nucleic Acids Res 32: 1308 - 1317
13. Cuesta R, Laroia G, Schneider RJ (2000) Chaperone hsp27 inhibits translation during heat shock by binding eIF4G and facilitating dissociation of cap-initiation complexes. Genes Dev 14: 1460 - 1470
14. Dhote V, Sweeney TR, Kim N, Hellen CU, Pestova TV (2012) Roles of individual domains in the function of DHX29, an essential factor required for translation of structured mammalian mRNAs. Proc Natl Acad Sci USA 109: E3150 - E3159
15. Du Z, Fenn S, Tjhen R, James TL (2008) Structure of a construct of a human poly(C)-binding protein containing the first and second KH domains reveals insights into its regulatory mechanisms. J Biol Chem 283: 28757 - 28766
16. Funke B, Zuleger B, Benavente R, Schuster T, Goller M, Stévenin J, Horak I (1996) The mouse poly(C)-binding protein exists in multiple isoforms and interacts with several RNA-binding proteins. Nucleic Acids Res 24: 3821 - 3828
17. Gamarnik AV, Andino R (1997) Two functional complexes formed by KH domain containing proteins with the 5′ noncoding region of poliovirus RNA. RNA 3: 882 - 892
18. 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
19. Gradi A, Svitkin YV, Imataka H, Sonenberg N (1998) 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 USA 95: 11089 - 11094
20. Hellen CU, Pestova TV, Wimmer E (1994) Effect of mutations downstream of the internal ribosome entry site on initiation of poliovirus protein synthesis. J Virol 68: 6312 - 6322
21. Hellen CU, Witherell GW, Schmid M, Shin SH, Pestova TV, Gil A, Wimmer E (1993) 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 USA 90: 7642 - 7646
22. Hunt SL, Hsuan JJ, Totty N, Jackson RJ (1999) 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: 437 - 448
23. Iizuka N, Yonekawa H, Nomoto A (1991) Nucleotide sequences important for translation initiation of enterovirus RNA. J Virol 65: 4867 - 4873
24. Jackson RJ (1991) Potassium salts influence the fidelity of mRNA translation initiation in rabbit reticulocyte lysates: unique features of encephalomyocarditis virus RNA translation. Biochim Biophys Acta 1088: 345 - 358
25. Jackson RJ, Hellen CU, Pestova TV (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11: 113 - 127
26. Jackson RJ, Kaminski A (1995) Internal initiation of translation in eukaryotes: the picornavirus paradigm and beyond. RNA 1: 985 - 1000
27. Kafasla P, Morgner N, Pöyry TA, Curry S, Robinson CV, Jackson RJ (2009) Polypyrimidine tract binding protein stabilizes the encephalomyocarditis virus IRES structure via binding multiple sites in a unique orientation. Mol Cell 34: 556 - 568
28. 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
29. Kaminski A, Pöyry TA, Skene PJ, Jackson RJ (2010) Mechanism of initiation site selection promoted by the human rhinovirus 2 internal ribosome entry site. J Virol 84: 6578 - 6589
30. 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
31. Lamichhane R, Daubner GM, Thomas-Crusells J, Auweter SD, Manatschal C, Austin KS, Valniuk O, Alain FH-T, Rueda D (2010) RNA looping by PTB: evidence using FRET and NMR spectroscopy for a role in splicing repression. Proc Natl Acad Sci USA 107: 4105 - 4110
32. Lamphear BJ, Kirchweger R, Skern T, Rhoads RE (1995) 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: 21975 - 21983
33. Lomakin IB, Hellen CU, 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
34. López-Rivas A, Castrillo JL, Carrasco L (1987) Cation content in poliovirus-infected HeLa cells. J Gen Virol 68: 335 - 342
35. Meerovitch K, Nicholson R, Sonenberg N (1991) In vitro mutational analysis of cis-acting RNA translational elements within the poliovirus type 2 5′ untranslated region. J Virol 65: 5895 - 5901
36. Meerovitch K, Svitkin YV, Lee HS, Lejbkowicz F, Kenan DJ, Chan EK, Agol VI, Keene JD, Sonenberg N (1993) La autoantigen enhances and corrects aberrant translation of poliovirus RNA in reticulocyte lysate. J Virol 67: 3798 - 3807
37. Merrill MK, Gromeier M (2006) The double-stranded RNA binding protein 76: NF45 heterodimer inhibits translation initiation at the rhinovirus type 2 internal ribosome entry site. J Virol 80: 6936 - 6942
38. Neubauer C, Gao YG, Andersen KR, Dunham CM, Kelley AC, Hentschel J, Gerdes K, Ramakrishnan V, Brodersen DE (2009) The structural basis for mRNA recognition and cleavage by the ribosome-dependent endonuclease RelE. Cell 139: 1084 - 1095
39. Nicholson R, Pelletier J, Le SY, Sonenberg N (1991) Structural and functional analysis of the ribosome landing pad of poliovirus type 2: in vivo translation studies. J Virol 65: 5886 - 5894
40. Oberstrass FC, Auweter SD, Erat M, Hargous Y, Henning A, Wenter P, Reymond L, Amir-Ahmady B, Pitsch S, Black DL, Allain FH (2005) Structure of PTB bound to RNA: specific binding and implications for splicing regulation. Science 309: 2054 - 2057
41. Pause A, Méthot 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 cap-independent initiation of translation. EMBO J 13: 1205 - 1215
42. Pestova TV, Hellen CU (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
43. Pestova TV, Hellen CU, Shatsky IN (1996a) Canonical eukaryotic initiation factors determine initiation of translation by internal ribosomal entry. Mol Cell Biol 16: 6859 - 6869
44. 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
45. 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
46. Pestova TV, Kolupaeva VG (2002) The roles of individual eukaryotic translation initiation factors in ribosomal scanning and initiation codon selection. Genes Dev 16: 2906 - 2922
47. Pestova TV, Lomakin IB, Lee JH, Choi SK, Dever TE, Hellen CU (2000) The joining of ribosomal subunits in eukaryotes requires eIF5B. Nature 403: 332 - 335
48. Pestova TV, Shatsky IN, Fletcher SP, Jackson RJ, Hellen CU (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
49. Pestova TV, Shatsky IN, Hellen CU (1996b) 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
50. Pilipenko EV, Gmyl AP, Maslova SV, Svitkin YV, Sinyakov AN, Agol VI (1992) Prokaryotic-like cis elements in the cap-independent internal initiation of translation on picornavirus RNA. Cell 68: 119 - 131
51. Pilipenko EV, Pestova TV, Kolupaeva VG, Khitrina EV, Poperechnaya AN, Agol VI, Hellen CU (2000) A cell cycle-dependent protein serves as a template-specific translation initiation factor. Genes Dev 14: 2028 - 2045
52. Pisarev AV, Unbehaun A, Hellen CU, Pestova TV (2007) Assembly and analysis of eukaryotic translation initiation complexes. Methods Enzymol 430: 147 - 177
53. 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
54. Sean P, Nguyen JH, Semler BL (2009) 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: 45 - 58
55. Sidiqi M, Wilce JA, Vivian JP, Porter CJ, Barker A, Leedman PJ, Wilce MC (2005) Structure and RNA binding of the third KH domain of poly(C)-binding protein 1. Nucleic Acids Res 33: 1213 - 1221
56. Silvera D, Gamarnik AV, Andino R (1999) The N-terminal K homology domain of the poly(rC)-binding protein is a major determinant for binding to the poliovirus 5′-untranslated region and acts as an inhibitor of viral translation. J Biol Chem 274: 38163 - 38170
57. Sizova DV, Kolupaeva VG, Pestova TV, Shatsky IN, Hellen CU (1998) 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 72: 4775 - 4782
58. Sweeney TR, Dhote V, Yu Y, Hellen CU (2012) A distinct class of internal ribosomal entry site in members of the Kobuvirus and proposed Salivirus and Paraturdivirus genera of the Picornaviridae. J Virol 86: 1468 - 1486
59. Thompson SR, Sarnow P (2003) Enterovirus 71 contains a type I IRES element that functions when eukaryotic initiation factor eIF4G is cleaved. Virology 315: 259 - 266
60. Unbehaun A, Borukhov SI, Hellen CU, Pestova TV (2004) 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 18: 3078 - 3093
61. Yu Y, Abaeva IS, Marintchev A, Pestova TV, Hellen CU (2011a) Common conformational changes induced in type 2 picornavirus IRESs by cognate trans-acting factors. Nucleic Acids Res 39: 4851 - 4865
62. Yu Y, Sweeney TR, Kafasla P, Jackson RJ, Pestova TV, Hellen CU (2011b) The mechanism of translation initiation on Aichivirus RNA mediated by a novel type of picornavirus IRES. EMBO J 30: 4423 - 4436
63. Zell R, Ihle Y, Effenberger M, Seitz S, Wutzler P, Görlach M (2008) Interaction of poly(rC)-binding protein 2 domains KH1 and KH3 with coxsackievirus RNA. Biochem Biophys Res Commun 377: 500 - 503
64. Zell R, Sidigi K, Henke A, Schmidt-Brauns J, Hoey E, Martin S, Stelzner A (1999) Functional features of the bovine enterovirus 5′-non-translated region. J Gen Virol 80: 2299 - 2309