A long-distance RNA-RNA interaction plays an important role in programmed -1 ribosomal frameshifting in the translation of p88 replicase protein of Red clover necrotic mosaic virus

Virology

Volumn 417, Issue 1, 2011, Pages 169-178

  Tajima, Yuri ^a   Iwakawa, Hiro oki ^a,b   Kaido, Masanori ^a   Mise, Kazuyuki ^a   Okuno, Tetsuro ^a  

^a KYOTO UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

Author keywords

Bulged stem loop; Cap independent translation; Dianthovirus; Frameshifting; Long distance RNA RNA interaction; Positive strand RNA virus; Red clover necrotic mosaic virus; RNA structure; RNA dependent RNA polymerase

Indexed keywords

PROTEIN P27; PROTEIN P88; UNCLASSIFIED DRUG; VIRUS ENZYME; VIRUS RNA;

3' UNTRANSLATED REGION; ARTICLE; BASE PAIRING; CONTROLLED STUDY; GENE INTERACTION; GENE MAPPING; GENE SWITCHING; LONG DISTANCE RNA RNA INTERACTION; MOSAIC VIRUS; NONHUMAN; PRIORITY JOURNAL; RED CLOVER NECROTIC MOSAIC VIRUS; RIBOSOMAL FRAMESHIFTING; RNA REPLICATION; RNA SEQUENCE; RNA TRANSLATION; SITE DIRECTED MUTAGENESIS; VIRUS TRANSCRIPTION;

CELL-FREE SYSTEM; FRAMESHIFTING, RIBOSOMAL; GENE EXPRESSION REGULATION, VIRAL; MUTAGENESIS, SITE-DIRECTED; OPEN READING FRAMES; PROTEIN BIOSYNTHESIS; RNA REPLICASE; RNA, VIRAL; TOMBUSVIRIDAE;

DIANTHOVIRUS; RED CLOVER NECROTIC MOSAIC VIRUS; RNA VIRUSES;

EID: 79960940357     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2011.05.012     Document Type: Article

References (51)

1. Barry J.K., Miller W.A. A -1 ribosomal frameshift element that requires base pairing across four kilobases suggests a mechanism of regulating ribosome and replicase traffic on a viral RNA. Proc. Natl Acad. Sci. U. S. A. 2002, 99:11133-11138.
2. Bates H.J., Farjah M., Osman T.A., Buck K.W. Isolation and characterization of an RNA-dependent RNA polymerase from Nicotiana clevelandii plants infected with red clover necrotic mosaic dianthovirus. J. Gen. Virol. 1995, 76:1483-1491.
3. Blobel G., Sabatini D. Dissociation of mammalian polyribosomes into subunits by puromycin. Proc. Natl Acad. Sci. U. S. A. 1971, 68:390-394.
4. Brierley I. Ribosomal frameshifting viral RNAs. J. Gen. Virol. 1995, 76:1885-1892.
5. Brierley I., Pennell S. Structure and function of the stimulatory RNAs involved in programmed eukaryotic -1 ribosomal frameshifting. Cold Spring Harb. Symp. Quant. Biol. 2001, 66:233-248.
6. Brierley I., Digard P., Inglis S.C. Characterization of an efficient coronavirus ribosomal frameshifting signal: requirement for an RNA pseudoknot. Cell 1989, 57:537-547.
7. Dreher T.W., Miller W.A. Translational control in positive strand RNA plant viruses. Virology 2006, 344:185-197.
8. Fabian M.R., 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. 2004, 279:28862-28872.
9. Fabian M.R., White K.A. Solution structure probing of RNA structures. Methods Mol. Biol. 2008, 451:243-250.
10. Giedroc D.P., Cornish P.V. Frameshifting RNA pseudoknots: structure and mechanism. Virus Res. 2009, 139:193-208.
11. Guo L., Allen E.M., Miller W.A. Base-pairing between untranslated regions facilitates translation of uncapped, nonpolyadenylated viral RNA. Mol. Cell 2001, 7:1103-1109.
12. Hyodo K., Mine A., Iwakawa H.O., Kaido M., Mise K., Okuno T. Identification of amino acids in auxiliary replicase protein p27 critical for its RNA-binding activity and the assembly of the replicase complex in Red clover necrotic mosaic virus. Virology 2011, 413:300-309.
13. Iwakawa H.O., Kaido M., Mise K., 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 2007, 369:168-181.
14. Iwakawa H.O., Mizumoto H., Nagano H., Imoto Y., Takigawa K., Sarawaneeyaruk S., Kaido M., Mise K., 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. 2008, 82:10162-10174.
15. Iwakawa H.O., Mine A., Hyodo K., An M., Kaido M., Mise K., Okuno T. Template recognition mechanisms by replicase proteins differ between bipartite positive-strand genomic RNAs of a plant virus. J. Virol. 2011, 85:497-509.
16. Jacks T., Madhani H.D., Masiarz F.R., Varmus H.E. Signals for ribosomal frameshifting in the Rous sarcoma virus gag-pol region. Cell 1988, 55:447-458.
17. Kim K.H., Hemenway C.L. Long-distance RNA-RNA interactions and conserved sequence elements affect potato virus X plus-strand RNA accumulation. RNA 1999, 5:636-645.
18. Kim K.H., Lommel S.A. Identification and analysis of the site of -1 ribosomal frameshifting in red clover necrotic mosaic virus. Virology 1994, 200:574-582.
19. Kim K.H., Lommel S.A. Sequence element required for efficient -1 ribosomal frameshifting in red clover necrotic mosaic dianthovirus. Virology 1998, 250:50-59.
20. Klovins J., Berzins V., van Duin J. A long-range interaction in Qbeta RNA that bridges the thousand nucleotides between the M-site and the 3' end is required for replication. RNA 1998, 4:948-957.
21. Komoda K., Naito S., Ishikawa M. Replication of plant RNA virus genomes in a cell-free extract of evacuolated plant protoplasts. Proc. Natl Acad. Sci. U. S. A. 2004, 101:1863-1867.
22. Koonin E.V. The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. J. Gen. Virol. 1991, 72:2197-2206.
23. Lehninger A.L., Nelson D.L., Cox M.M. Principles of Biochemistry 1993, 927-928. World Publishers, New York, NY.
24. Lindenbach B.D., Sgro J.Y., Ahlquist P. Long-distance base pairing in flock house virus RNA1 regulates subgenomic RNA3 synthesis and RNA2 replication. J. Virol. 2002, 76:3905-3919.
25. Lobanov A.V., Turanov A.A., Hatfield D.L., Gladyshev V.N. Dual functions of codons in the genetic code. Crit. Rev. Biochem. Mol. Biol. 2010, 45:257-265.
26. Lommel S.A., Weston-Fina M., Xiong Z., Lomonossoff G.P. The nucleotide sequence and gene organization of red clover necrotic mosaic virus RNA-2. Nucleic Acids Res. 1988, 16:8587-8602.
27. Mazauric M.H., Licznar P., Prere M.F., Canal I., Fayet O. Apical loop-internal loop RNA pseudoknots: a new type of stimulator of -1 translational frameshifting in bacteria. J. Biol. Chem. 2008, 283:20421-20432.
28. Miller W.A., Koev G. Synthesis of subgenomic RNAs by positive-strand RNA viruses. Virology 2000, 273:1-8.
29. Mine A., Takeda A., Taniguchi T., Taniguchi H., Kaido M., Mise K., Okuno T. Identification and characterization of the 480-kilodalton template-specific RNA-dependent RNA polymerase complex of red clover necrotic mosaic virus. J. Virol. 2010, 84:6070-6081.
30. Mine A., Hyodo K., Takeda A., Kaido M., Mise K., Okuno T. 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 2010, 407:213-224.
31. Mizumoto H., Hikichi Y., Okuno T. The 3'-untranslated region of RNA1 as a primary determinant of temperature sensitivity of Red clover necrotic mosaic virus Canadian strain. Virology 2002, 293:320-327.
32. Mizumoto H., Tatsuta M., Kaido M., Mise K., Okuno T. Cap-independent translational enhancement by the 3' untranslated region of red clover necrotic mosaic virus RNA1. J. Virol. 2003, 77:12113-12121.
33. Moreno J.L., Zuniga S., Enjuanes L., Sola I. Identification of a coronavirus transcription enhancer. J. Virol. 2008, 82:3882-3893.
34. Namy O., Moran S.J., Stuart D.I., Gilbert R.J., Brierley I. A mechanical explanation of RNA pseudoknot function in programmed ribosomal frameshifting. Nature 2006, 441:244-247.
35. Nicholson B.L., Wu B., Chevtchenko I., White K.A. Tombusvirus recruitment of host translational machinery via the 3' UTR. RNA 2010, 16:1402-1419.
36. Okamoto K., Nagano H., Iwakawa H., Mizumoto H., Takeda A., Kaido M., Mise K., Okuno T. cis-Preferential requirement of a -1 frameshift product p88 for the replication of Red clover necrotic mosaic virus RNA1. Virology 2008, 375:205-212.
37. Panavas T., Nagy P.D. Mechanism of stimulation of plus-strand synthesis by an RNA replication enhancer in a tombusvirus. J. Virol. 2005, 79:9777-9785.
38. Paul C.P., Barry J.K., Dinesh-Kumar S.P., Brault V., Miller W.A. A sequence required for -1 ribosomal frameshifting located four kilobases downstream of the frameshift site. J. Mol. Biol. 2001, 310:987-999.
39. Sarawaneeyaruk S., Iwakawa H.O., Mizumoto H., Murakami H., Kaido M., Mise K., Okuno T. 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 2009, 391:107-118.
40. Sit T.L., Vaewhongs A.A., Lommel S.A. RNA-mediated trans-activation of transcription from a viral RNA. Science 1998, 281:828-832.
41. Takeda A., Tsukuda M., Mizumoto H., Okamoto K., Kaido M., Mise K., Okuno T. A plant RNA virus supresses RNA silencing through viral RNA replication. EMBO J. 2005, 24:3147-3157.
42. Treder K., Kneller E.L., Allen E.M., Wang Z., Browning K.S., Miller W.A. The 3' cap-independent translation element of Barley yellow dwarf virus binds eIF4F via the eIF4G subunit to initiate translation. RNA 2008, 14:134-147.
43. Weixlbaumer A., Werner A., Flamm C., Westhof E., Schroeder R. Determination of thermodynamic parameters for HIV DIS type loop-loop kissing complexes. Nucleic Acids Res. 2004, 32:5126-5133.
44. Wu B., Vanti W.B., White K.A. An RNA domain within the 5' untranslated region of tomato bushy stunt virus genome modulates viral RNA replication. J. Mol. Biol. 2001, 305:741-756.
45. Xiong Z., Lommel S.A. The complete nucleotide sequence and genome organization of red clover necrotic mosaic virus RNA-1. Virology 1989, 171:543-554.
46. Xiong Z., Lommel S.A. Red clover necrotic mosaic virus infectious transcripts synthesized in vitro. Virology 1991, 193:213-221.
47. Xiong Z., Kim K.H., Giesman-Cookmeyer D., Lommel S.A. The roles of the red clover necrotic mosaic virus capsid and cell-to-cell movement proteins in systemic infection. Virology 1993, 192:27-32.
48. Xiong Z., Kim K.H., Kendall T.L., Lommel S.A. Synthesis of the putative red clover necrotic mosaic virus RNA polymerase by ribosomal frameshifting in vitro. Virology 1993, 193:213-221.
49. Yuan X., Shi K., Meskauskas A., Simon A.E. The 3' end of Turnip crinkle virus contains a highly interactive structure including a translational enhancer that is disrupted by binding to the RNA-dependent RNA polymerase. RNA 2009, 15:1849-1864.
50. Zavriev S.K., Hickey C.M., Lommel S.A. Mapping of the red clover necrotic mosaic virus subgenomic RNA. Virology 1996, 216:407-410.
51. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 2003, 31:3406-3415.