Poly(A)-binding protein facilitates translation of an uncapped/nonpolyadenylated viral rna by binding to the 3' untranslated region

Journal of Virology

Volumn 86, Issue 15, 2012, Pages 7836-7849

  Iwakawa, Hiro Oki ^a,b   Tajima, Yuri ^a   Taniguchi, Takako ^c   Kaido, Masanori ^a   Mise, Kazuyuki ^a   Tomari, Yukihide ^b   Taniguchi, Hisaaki ^c   Okuno, Tetsuro ^a  

^a KYOTO UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c UNIVERSITY OF TOKUSHIMA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; POLYADENYLIC ACID BINDING PROTEIN; RIBOSOME RNA; RNA 40S; UNCLASSIFIED DRUG; VIRUS RNA;

3' UNTRANSLATED REGION; AFFINITY CHROMATOGRAPHY; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; MOLECULAR EVOLUTION; MOSAIC VIRUS; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN RNA BINDING; RED CLOVER NECROTIC MOSAIC VIRUS; RNA TRANSCRIPTION; SEQUENCE ANALYSIS; TANDEM MASS SPECTROMETRY; TOBACCO; VIRUS GENOME; VIRUS TRANSCRIPTION;

3' UNTRANSLATED REGIONS; CELL-FREE SYSTEM; EUKARYOTIC INITIATION FACTOR-4F; PLANT PROTEINS; POLY(A)-BINDING PROTEINS; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RIBOSOME SUBUNITS, SMALL, EUKARYOTIC; RNA, VIRAL; TOMBUSVIRIDAE; TRITICUM;

EUKARYOTA; RED CLOVER NECROTIC MOSAIC VIRUS; RNA VIRUSES;

EID: 84864387263     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00538-12     Document Type: Article

References (70)

1. Bachler M, Schroeder R, von Ahsen U. 1999. StreptoTag: a novel method for the isolation of RNA-binding proteins. RNA 5:1509-1516.
2. Baer BW, Kornberg RD. 1983. The protein responsible for the repeating structure of cytoplasmic poly(A)-ribonucleoprotein. J. Cell Biol. 96:717-721.
3. Balvay L, Soto Rifo R, Ricci EP, Decimo D, Ohlmann T. 2009. Structural and functional diversity of viral IRESes. Biochim. Biophys. Acta 1789: 542-557.
4. Belostotsky DA. 2003. Unexpected complexity of poly(A)-binding protein gene families in flowering plants: three conserved lineages that are at least 200 million years old and possible auto- and cross-regulation. Genetics 163:311-319.
5. Borman AM, Michel YM, Kean KM. 2000. Biochemical characterisation of cap-poly(A) synergy in rabbit reticulocyte lysates: the eIF4G-PABP interaction increases the functional affinity of eIF4E for the capped mRNA 5'-end. Nucleic Acids Res. 28:4068-4075.
6. Brook M, Smith JW, Gray NK. 2009. The DAZL and PABP families: RNA-binding proteins with interrelated roles in translational control in oocytes. Reproduction 137:595-617.
7. Browning KS. 1996. The plant translational apparatus. Plant Mol. Biol. 32:107-144.
8. Browning KS, Webster C, Roberts JK, Ravel JM. 1992. Identification of an isozyme form of protein synthesis initiation factor 4F in plants. J. Biol. Chem. 267:10096-10100.
9. Burd CG, Matunis EL, Dreyfuss G. 1991. The multiple RNA-binding domains of the mRNA poly(A)-binding protein have different RNAbinding activities. Mol. Cell. Biol. 11:3419-3424.
10. Chattopadhyay M, Shi K, Yuan X, Simon AE. 2011. Long-distance kissing loop interactions between a 3' proximal Y-shaped structure and apical loops of 5' hairpins enhance translation of Saguaro cactus virus. Virology 417:113-125.
11. Cheng S, Gallie DR. 2007. eIF4G, eIFiso4G, and eIF4B bind the poly(A)-binding protein through overlapping sites within the RNA recognition motif domains. J. Biol. Chem. 282:25247-25258.
12. Dangerfield JA, Windbichler N, Salmons B, Gunzburg WH, Schroder R. 2006. Enhancement of the StreptoTag method for isolation of endogenously expressed proteins with complex RNA binding targets. Electrophoresis 27:1874-1877.
13. De Gregorio E, Preiss T, Hentze MW. 1998. Translational activation of uncapped mRNAs by the central part of human eIF4G is 5' enddependent. RNA 4:828-836.
14. Dufresne PJ, Ubalijoro E, Fortin MG, Laliberte JF. 2008. Arabidopsis thaliana class II poly(A)-binding proteins are required for efficient multiplication of turnip mosaic virus. J. Gen. Virol. 89:2339-2348.
15. Duprat A, et al. 2002. The Arabidopsis eukaryotic initiation factor (iso)4E is dispensable for plant growth but required for susceptibility to potyviruses. Plant J. 32:927-934.
16. Fabian MR, White KA. 2004. 5'-3' RNA-RNA interaction facilitates capand poly(A) tail-independent translation of tomato bushy stunt virus mRNA: a potential common mechanism for Tombusviridae. J. Biol. Chem. 279:28862-28872.
17. Fabian MR, White KA. 2006. Analysis of a 3'-translation enhancer in a tombusvirus: a dynamic model for RNA-RNA interactions of mRNA termini. RNA 12:1304-1314.
18. Fitzgerald KD, Semler BL. 2009. Bridging IRES elements in mRNAs to the eukaryotic translation apparatus. Biochim. Biophys. Acta 1789:518-528.
19. Gallie DR. 1991. The cap and poly(A) tail function synergistically to regulate mRNA translational efficiency. Genes Dev. 5:2108-2116.
20. Gallie DR, Browning KS. 2001. eIF4G functionally differs from eIFiso4G in promoting internal initiation, cap-independent translation, and translation of structured mRNAs. J. Biol. Chem. 276:36951-36960.
21. Gazo BM, Murphy P, Gatchel JR, Browning KS. 2004. A novel interaction of Cap-binding protein complexes eukaryotic initiation factor (eIF) 4F and eIF(iso)4F with a region in the 3'-untranslated region of satellite tobacco necrosis virus. J. Biol. Chem. 279:13584-13592.
22. Gorlach M, Burd CG, Dreyfuss G. 1994. The mRNA poly(A)-binding protein: localization, abundance, and RNA-binding specificity. Exp. Cell Res. 211:400-407.
23. Gray NK, Hentze MW. 1994. Iron regulatory protein prevents binding of the 43S translation pre-initiation complex to ferritin and eALAS mRNAs. EMBO J. 13:3882-3891.
24. Guo L, Allen EM, Miller WA. 2001. Base-pairing between untranslated regions facilitates translation of uncapped, nonpolyadenylated viral RNA. Mol. Cell 7:1103-1109.
25. Hinnebusch AG. 2006. eIF3: a versatile scaffold for translation initiation complexes. Trends Biochem. Sci. 31:553-562.
26. Iwakawa HO, Kaido M, Mise K, Okuno T. 2007. cis-Acting core RNA elements required for negative-strand RNA synthesis and cap-independent translation are separated in the 3'-untranslated region of Red clover necrotic mosaic virus RNA1. Virology 369:168-181.
27. Iwakawa HO, et al. 2011. Template recognition mechanisms by replicase proteins differ between bipartite positive-strand genomic RNAs of a plant virus. J. Virol. 85:497-509.
28. Iwakawa HO, et al. 2008. A viral noncoding RNA generated by ciselement-mediated protection against 5'¡3' RNA decay represses both cap-independent and cap-dependent translation. J. Virol. 82:10162-10174.
29. Iwasaki S, Kawamata T, Tomari Y. 2009. Drosophila argonaute1 and argonaute2 employ distinct mechanisms for translational repression. Mol. Cell 34:58-67.
30. 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.
31. Kahvejian A, Svitkin YV, Sukarieh R, M'Boutchou MN, Sonenberg N. 2005. Mammalian poly(A)-binding protein is a eukaryotic translation initiation factor, which acts via multiple mechanisms. Genes Dev. 19:104-113.
32. Kneller EL, Rakotondrafara AM, Miller WA. 2006. Cap-independent translation of plant viral RNAs. Virus Res. 119:63-75.
33. Komoda K, Naito S, Ishikawa M. 2004. Replication of plant RNA virus genomes in a cell-free extract of evacuolated plant protoplasts. Proc. Natl. Acad. Sci. U. S. A. 101:1863-1867.
34. Kuhn U, Pieler T. 1996. Xenopus poly(A) binding protein: functional domains in RNA binding and protein-protein interaction. J. Mol. Biol. 256:20-30.
35. Lax SR, Lauer SJ, Browning KS, Ravel JM. 1986. Purification and properties of protein synthesis initiation and elongation factors from wheat germ. Methods Enzymol. 118:109-128.
36. Le H, Browning KS, Gallie DR. 2000. The phosphorylation state of poly(A)-binding protein specifies its binding to poly(A) RNA and its interaction with eukaryotic initiation factor (eIF) 4F, eIFiso4F, and eIF4B. J. Biol. Chem. 275:17452-17462.
37. Lellis AD, et al. 2010. Deletion of the eIFiso4G subunit of the Arabidopsis eIFiso4F translation initiation complex impairs health and viability. Plant Mol. Biol. 74:249-263.
38. Li J, Chorba JS, Whelan SP. 2007. Vesicular stomatitis viruses resistant to the methylase inhibitor sinefungin upregulate RNA synthesis and reveal mutations that affect mRNA cap methylation. J. Virol. 81:4104-4115.
39. Miller WA, Wang Z, Treder K. 2007. The amazing diversity of capindependent translation elements in the 3'-untranslated regions of plant viral RNAs. Biochem. Soc. Trans. 35:1629-1633.
40. Mine A, et al. 2010. Interactions between p27 and p88 replicase proteins of Red clover necrotic mosaic virus play an essential role in viral RNA replication and suppression of RNA silencing via the 480-kDa viral replicase complex assembly. Virology 407:213-224.
41. Mine A, et al. 2010. Identification and characterization of the 480-kilodalton template-specific RNA-dependent RNA polymerase complex of red clover necrotic mosaic virus. J. Virol. 84:6070-6081.
42. Mizumoto H, Iwakawa HO, Kaido M, Mise K, Okuno T. 2006. Capindependent translation mechanism of red clover necrotic mosaic virus RNA2 differs from that of RNA1 and is linked to RNA replication. J. Virol. 80:3781-3791.
43. Mizumoto H, Tatsuta M, Kaido M, Mise K, Okuno T. 2003. Capindependent translational enhancement by the 3' untranslated region of red clover necrotic mosaic virus RNA1. J. Virol. 77:12113-12121.
44. Narabayashi T, Iwahashi F, Kaido M, Okuno T, Mise K. 2009. Melandrium yellow fleck bromovirus infects Arabidopsis thaliana and has genomic RNA sequence characteristics that are unique among bromoviruses. Arch. Virol. 154:1381-1389.
45. Nicholson BL, White KA. 2008. Context-influenced cap-independent translation of Tombusvirus mRNAs in vitro. Virology 380:203-212.
46. Nicholson BL, White KA. 2011. 3' Cap-independent translation enhancers of positive-strand RNA plant viruses. Curr. Opin. Virol. 1:373-380.
47. Nicholson BL, Wu B, Chevtchenko I, White KA. 2010. Tombusvirus recruitment of host translational machinery via the 3' UTR. RNA 16: 1402-1419.
48. Nietfeld W, Mentzel H, Pieler T. 1990. The Xenopus laevis poly(A) binding protein is composed of multiple functionally independent RNA binding domains. EMBO J. 9:3699-3705.
49. 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.
50. Polacek C, Friebe P, Harris E. 2009. Poly(A)-binding protein binds to the non-polyadenylated 3' untranslated region of dengue virus and modulates translation efficiency. J. Gen. Virol. 90:687-692.
51. Sachs AB, Bond MW, Kornberg RD. 1986. A single gene from yeast for both nuclear and cytoplasmic polyadenylate-binding proteins: domain structure and expression. Cell 45:827-835.
52. Sachs AB, Davis RW, Kornberg RD. 1987. A single domain of yeast poly(A)-binding protein is necessary and sufficient for RNA binding and cell viability. Mol. Cell. Biol. 7:3268-3276.
53. Sarawaneeyaruk S, et al. 2009. Host-dependent roles of the viral 5' untranslated region (UTR) in RNA stabilization and cap-independent translational enhancement mediated by the 3'UTRof Red clover necrotic mosaic virus RNA1. Virology 391:107-118.
54. Shen R, Miller WA. 2007. Structures required for poly(A) tailindependent translation overlap with, but are distinct from, capindependent translation and RNA replication signals at the 3' end of Tobacco necrosis virus RNA. Virology 358:448-458.
55. Shen X, et al. 1999. Poly [G] improved protein productivity of cell-free translation by inhibiting mRNase in wheat germ extract. J. Biotechnol. 75:221-228.
56. Skabkina OV, et al. 2003. Poly(A)-binding protein positively affects YB-1 mRNA translation through specific interaction with YB-1 mRNA. J. Biol. Chem. 278:18191-18198.
57. Sonenberg N, Hinnebusch AG. 2009. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136:731-745.
58. Stupina VA, et al. 2008. The 3' proximal translational enhancer of Turnip crinkle virus binds to 60S ribosomal subunits. RNA. 14:2379-2393.
59. Takeda A, et al. 2005. A plant RNA virus suppresses RNA silencing through viral RNA replication. EMBO J. 24:3147-3157.
60. Taniguchi T, et al. 2010. Induction of endosomal/lysosomal pathways in differentiating osteoblasts as revealed by combined proteomic and transcriptomic analyses. FEBS Lett. 584:3969-3974.
61. Treder K, et al. 2008. The 3' cap-independent translation element of Barley yellow dwarf virus binds eIF4F via the eIF4G subunit to initiate translation. RNA. 14:134-147.
62. Vazquez-Pianzola P, Urlaub H, Suter B. 2011. Pabp binds to the osk 3'UTR and specifically contributes to osk mRNA stability and oocyte accumulation. Dev. Biol. 357:404-418.
63. von Der Haar T, Ball PD, McCarthy JE. 2000. Stabilization of eukaryotic initiation factor 4E binding to the mRNA 5'-Cap by domains of eIF4G. J. Biol. Chem. 275:30551-30555.
64. Wallace ST, Schroeder R. 1998. In vitro selection and characterization of streptomycin-binding RNAs: recognition discrimination between antibiotics. RNA 4:112-123.
65. Wang S, Browning KS, Miller WA. 1997. A viral sequence in the 3'-untranslated region mimics a 5' cap in facilitating translation of uncapped mRNA. EMBO J. 16:4107-4116.
66. 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.
67. Wang Z, Parisien M, Scheets K, Miller WA. 2011. The cap-binding translation initiation factor, eIF4E, binds a pseudoknot in a viral capindependent translation element. Structure 19:868-880.
68. Wang Z, Treder K, Miller WA. 2009. Structure of a viral cap-independent translation element that functions via high-affinity binding to the eIF4E subunit of eIF4F. J. Biol. Chem. 284:14189-14202.
69. Xu W, White KA. 2009. RNA-based regulation of transcription and translation of aureusvirus subgenomic mRNA1. J. Virol. 83:10096-10105.
70. Zhang F, Simon AE. 2003. A novel procedure for the localization of viral RNAs in protoplasts and whole plants. Plant J. 35:665-673.