Host-dependent roles of the viral 5′ untranslated region (UTR) in RNA stabilization and cap-independent translational enhancement mediated by the 3′ UTR of Red clover necrotic mosaic virus RNA1

Virology

Volumn 391, Issue 1, 2009, Pages 107-118

  Sarawaneeyaruk, Siriruk ^a   Iwakawa, Hiro oki ^a   Mizumoto, Hiroyuki ^a   Murakami, Hiromi ^a   Kaido, Masanori ^a   Mise, Kazuyuki ^a   Okuno, Tetsuro ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

3 UTR; 5 UTR; Cap independent translation; Dianthovirus; Host dependent; IRES; Positive strand RNA virus; Ribosomal scanning; RNA stability; Tombusviridae

Indexed keywords

LUCIFERASE; MESSENGER RNA; UNCLASSIFIED DRUG; VIRUS RNA; VIRUS RNA 1;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; COWPEA; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTOPLAST; RED CLOVER NECROTIC MOSAIC VIRUS; REPORTER GENE; RIBOSOME; RNA CAPPING; RNA STABILITY; RNA TRANSLATION; RNA VIRUS; TOBACCO; TRANSLATION REGULATION; VIRUS MUTATION;

3' UNTRANSLATED REGIONS; 5' UNTRANSLATED REGIONS; BASE SEQUENCE; CELLS, CULTURED; FABACEAE; GENOME, VIRAL; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PROTEIN BIOSYNTHESIS; RNA CAPS; RNA STABILITY; RNA, VIRAL; TOBACCO; TOMBUSVIRIDAE; VIRAL PROTEINS;

DIANTHOVIRUS; NICOTIANA TABACUM; RED CLOVER NECROTIC MOSAIC VIRUS; RNA VIRUSES; TOMBUSVIRIDAE;

EID: 67650762447     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2009.05.037     Document Type: Article

References (50)

1. Babendure J.R., Babendure J.L., Ding J.H., and Tsien R.Y. Control of mammalian translation by mRNA structure near caps. RNA 12 (2006) 851-861
2. Barton D.J., O'Donnell B.J., and Flanegan J.B. 5′ cloverleaf in poliovirus RNA is a cis-acting replication element required for negative-strand synthesis. EMBO J. 20 (2001) 1439-1448
3. Cheng S., and Gallie D.R. eIF4G, eIFiso4G, and eIF4B bind the poly(A)-binding protein through overlapping sites within the RNA recognition motif domains. J. Biol. Chem. 282 (2007) 25247-25258
4. Damayanti T.A., Nagano H., Mise K., Furusawa I., and Okuno T. Positional effect of deletions on viability, especially on encapsidation, of Brome mosaic virus D-RNA in barley protoplasts. Virology 293 (2002) 314-319
5. Dreher T.W., and Miller W.A. Translational control in positive strand RNA plant viruses. Virology 344 (2006) 185-197
6. Fabian M.R., and White K.A. 5′-3′ RNA-RNA interaction facilitates cap- and poly(A) tail-independent translation of Tomato bushy stunt virus mRNA: a potential common mechanism for tombusviridae. J. Biol. Chem. 279 (2004) 28862-28872
7. Gallie D.R. Cap-independent translation conferred by the 5′ leader of Tobacco etch virus is eukaryotic initiation factor 4G dependent. J. Virol. 75 (2001) 12141-12152
8. Gallie D.R. The 5′-leader of tobacco mosaic virus promotes translation through enhanced recruitment of eIF4F. Nucleic Acids Res. 30 (2002) 3401-3411
9. Guo L., Allen E., and Miller W.A. Structure and function of a cap-independent translation element that functions in either the 3′ or the 5′ untranslated region. RNA 6 (2000) 1808-1820
10. Hartley C.J., Greenwood D.R., Gilbert R.J.C., Masoumi A., Gordon K.H.J., Hanzlik T.N., Fry E.E., Stuart D.J., and Scotti P.D. Kelp fly virus: a novel group of insect picorna-like viruses as defined by genome sequence analysis and a distinctive virion structure. J. Virol. 79 (2005) 13385-13398
11. Higgs D.C., Shapiro R.S., Kindle K.L., and Stern D.B. Small cis-acting sequences that specify secondary structures in a chloroplast mRNA are essential for RNA stability and translation. Mol. Cell. Biol. 19 (1999) 8479-8491
12. Iwakawa H.O., Kaido M., Mise K., and Okuno T. 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 (2007) 168-181
13. Iwakawa H.O., Mizumoto H., Nagano H., Imoto Y., Takigawa K., Sarawaneeyaruk S., Kaido M., Mise K., and Okuno T. A viral noncoding RNA generated by cis-element-mediated protection against 5′ → 3′ RNA decay represses both cap-independent and cap-dependent translation. J. Virol. 82 (2008) 10162-10174
14. Kim K.H., and Lommel S.A. Identification and analysis of the site of -1 ribosomal frameshifting in Red clover necrotic mosaic virus. Virology 200 (1994) 574-582
15. Kneller E.L., Rakotondrafara A.M., and Miller W.A. Cap-independent translation of plant viral RNAs. Virus Res. 119 (2006) 63-75
16. Komoda K., Naito S., and Ishikawa M. Replication of plant RNA virus genomes in a cell-free extract of evacuolated plant protoplasts. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 1863-1867
17. Kozak M. The scanning model for translation: an update. J. Cell Biol. 108 (1989) 229-241
18. Li W., and Wong S.M. Host-dependent effects of the 3′ untranslated region of turnip crinkle virus RNA on accumulation in Hibiscus and Arabidopsis. J. Gen. Virol. 88 (2007) 680-687
19. Lommel S.A., Weston-Fina M., Xiong Z., and Lomonossoff G.P. The nucleotide sequence and gene organization of Red clover necrotic mosaic virus RNA-2. Nucleic Acids Res. 16 (1988) 8587-8602
20. Luo G., Xin S., and Cai Z. Role of the 5′-proximal stem-loop structure of the 5′ untranslated region in replication and translation of hepatitis C virus RNA. J. Virol. 77 (2003) 3312-3318
21. Masoumi A., Hanzlik T.N., and Christian P.D. Functionality of the 5′- and intergenic IRES elements of Cricket paralysis virus in a range of insect cell lines, and its relationship with viral activities. Virus Res. 94 (2003) 113-120
22. Mathews D.H., and Turner D.H. Dynalign: an algorithm for finding the secondary structure common to two RNA sequences. J. Mol. Biol. 317 (2002) 191-203
23. McCormack J.C., Yuan X., Yingling Y.G., Kasprzak W., Zamora R.E., Shapiro B.A., and Simon A.E. Structural domains within the 3′ untranslated region of Turnip crinkle virus. J. Virol. 82 (2008) 8706-8720
24. Meulewaeter F., Danthinne X., Van Montagu M., and Cornelissen M. 5′- and 3′-sequences of Satellite tobacco necrosis virus RNA promoting translation in tobacco. Plant J. 14 (1998) 169-176
25. Miller W.A., and White K.A. Long-distance RNA-RNA interactions in plant virus gene expression and replication. Annu. Rev. Phytopathol. 44 (2006) 447-467
26. Mizumoto H., Hikichi Y., and Okuno T. The 3′-untranslated region of RNA1 as a primary determinant of temperature sensitivity of Red clover necrotic mosaic virus Canadian strain. Virology 293 (2002) 320-327
27. Mizumoto H., Tatsuta M., Kaido M., Mise K., and Okuno T. Cap-independent translational enhancement by the 3′ untranslated region of red clover necrotic mosaic virus RNA1. J. Virol. 77 (2003) 12113-12121
28. Mizumoto H., Iwakawa H.O., Kaido M., Mise K., and Okuno T. Cap-independent translation mechanism of Red clover necrotic mosaic virus RNA2 differs from that of RNA1 and is linked to RNA replication. J. Virol. 80 (2006) 3781-3791
29. Morino S., Imataka H., Svitkin Y.V., Pestova T.V., and Sonenberg N. Eukaryotic translation initiation factor 4E (eIF4E) binding site and the middle one-third of eIF4GI constitute the core domain for cap-dependent translation, and the C-terminal one-third functions as a modulatory region. Mol. Cell. Biol. 20 (2000) 468-477
30. Okamoto K., Nagano H., Iwakawa H.O., Mizumoto H., Takeda A., Kaido M., Mise K., and Okuno T. cis-Preferential requirement of a-1 frameshift product p88 for the replication of Red clover necrotic mosaic virus RNA1. Virology 375 (2008) 205-212
31. Ongus J.R., Roode E.C., Pleij C.W.A., Vlak J.M., and van Oers M.M. The 5′ non-translated region of Varroa destructor virus 1 (genus Iflavirus): structure prediction and IRES activity in Lymantria dispar cells. J. Gen. Virol. 87 (2006) 3397-3407
32. Pestova T.V., and Kolupaeva V.G. The roles of individual eukaryotic translation initiation factors in ribosomal scanning and initiation codon selection. Genes Dev. 16 (2002) 2906-2922
33. Pfingsten J.S., and Kieft J.S. RNA structure-based ribosome recruitment: lessons from the Dicistroviridae intergenic region IRESes. RNA 14 (2008) 1255-1263
34. Pisarev A.V., Kolupaeva V.G., Pisareva V.P., Merrick W.C., Hellen C.U.T., and Pestova T.V. Specific functional interactions of nucleotides at key (-)3 and (+)4 positions flanking the initiation codon with components of the mammalian 48S translation initiation complex. Genes Dev. 20 (2006) 624-636
35. Qu F., and Morris T.J. Cap-independent translational enhancement of turnip crinkle virus genomic and subgenomic RNAs. J. Virol. 74 (2000) 1085-1093
36. Rakotondrafara A.M., Polacek C., Harris E., and Miller W.A. Oscillating kissing stem-loop interactions mediate 5′ scanning-dependent translation by a viral 3′ cap-independent translation element. RNA 12 (2006) 1893-1906
37. Ross J. mRNA stability in mammalian cells. Microbiol. Rev. 59 (1995) 423-450
38. Scholthof H.B., and Jackson A.O. The enigma of pX: a host-dependent cis-acting element with variable effects on tombusvirus RNA accumulation. Virology 237 (1997) 56-65
39. Sharp J.S., and Bechhofer D.H. Effect of 5′-proximal elements on decay of a model mRNA in Bacillus subtilis. Mol. Microbiol. 57 (2005) 484-495
40. Shen R., and Miller W.A. The 3′ untranslated region of Tobacco necrosis virus RNA contains a Barley yellow dwarf virus-like cap-independent translation element. J. Virol. 78 (2004) 4655-4664
41. Stupina V.A., Meskauskas A., McCormack J.C., Yingling Y.G., Shapiro B.A., Dinman J.D., and Simon A.E. The 3′ proximal translational enhancer of Turnip crinkle virus binds to 60S ribosomal subunits. RNA 14 (2008) 2379-2393
42. Suay L., Salvador M.L., Abesha E., and Klein U. Specific roles of 5′ RNA secondary structures in stabilizing transcripts in chloroplasts. Nucleic Acids Res. 33 (2005) 4754-4761
43. Svitkin Y.V., Imataka H., Khaleghpour K., Kahvejian A., Liebig H.-D., and Sonenberg N. Poly(A)-binding protein interaction with elF4G stimulates picornavirus IRES-dependent translation. RNA 7 (2001) 1743-1752
44. Takeda A., Tsukuda M., Mizumoto H., Okamoto K., Kaido M., Mise K., and Okuno T. A plant RNA virus suppresses RNA silencing through viral RNA replication. EMBO J. 24 (2005) 3147-3157
45. Treder K., Kneller E.L., Allen E.M., Wang Z., Browning K.S., and Miller W.A. The 3′ cap-independent translation element of Barley yellow dwarf virus binds eIF4F via the eIF4G subunit to initiate translation. RNA 14 (2008) 134-147
46. Wang S., Browning K.S., and Miller W.A. A viral sequence in the 3′-untranslated region mimics a 5′ cap in facilitating translation of uncapped mRNA. EMBO J. 16 (1997) 4107-4116
47. Wang G., Guo X., and Floros J. Differences in the translation efficiency and mRNA stability mediated by 5′-UTR splice variants of human SP-A1 and SP-A2 genes. Am. J. Physiol. Lung. Cell. Mol. Physiol. 289 (2005) L497-L508
48. Xiong Z., and Lommel S.A. Red clover necrotic mosaic virus infectious transcripts synthesized in vitro. Virology 182 (1991) 388-392
49. Zavriev S.K., Hickey C.M., and Lommel S.A. Mapping of the Red clover necrotic mosaic virus subgenomic RNA. Virology 216 (1996) 407-410
50. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31 (2003) 3406-3415