Replication protein of tobacco mosaic virus cotranslationally binds the 5′ untranslated region of genomic RNA to enable viral replication

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 16, 2014, Pages

  Kawamura Nagaya, Kazue ^a   Ishibashi, Kazuhiro ^a   Huang, Ying Ping ^a,b   Miyashita, Shuhei ^a   Ishikawa, Masayuki ^a  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

126 KDA REPLICATION PROTEIN; CIS ACTING ELEMENT; GENOMIC RNA; MESSENGER RNA; PREMEMBRANE TARGETING COMPLEX; PROTEIN ANTIBODY; RIBONUCLEOPROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

5' UNTRANSLATED REGION; ARTICLE; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CONTROLLED STUDY; IN VITRO STUDY; MOSAIC VIRUS; NONHUMAN; POTEXVIRUS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROCESSING; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; RNA PROBE; RNA REPLICATION; RNA STRUCTURE; RNA SYNTHESIS; RNA TRANSLATION; SMALL RIBOSOMAL SUBUNIT; TOBACCO MOSAIC VIRUS; TRANSLATION INITIATION; VIRUS REPLICATION; VIRUS TRANSCRIPTION; WESTERN BLOTTING;

5' UNTRANSLATED REGIONS; BASE SEQUENCE; CHROMATOGRAPHY, GEL; GENOME, VIRAL; MICROCOCCAL NUCLEASE; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; MUTATION; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RIBONUCLEASES; RNA, VIRAL; TOBACCO MOSAIC VIRUS; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84899092133     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1321660111     Document Type: Article

References (46)

1. den Boon JA, Ahlquist P (2010) Organelle-like membrane compartmentalization of positive-strand RNA virus replication factories. Annu Rev Microbiol 64(1):241-256.
2. den Boon JA, Diaz A, Ahlquist P (2010) Cytoplasmic viral replication complexes. Cell Host Microbe 8(1):77-85.
3. Liu Y, Wimmer E, Paul AV (2009) Cis-acting RNA elements in human and animal plus-strand RNA viruses. Biochim Biophys Acta 1789(9-10):495-517.
4. Weiland JJ, Dreher TW (1993) Cis-preferential replication of the turnip yellow mosaic virus RNA genome. Proc Natl Acad Sci USA 90(13):6095-6099. (Pubitemid 23191461)
5. Van Bokhoven H, et al. (1993) Cis- and trans-acting elements in cowpea mosaic virus RNA replication. Virology 195(2):377-386.
6. Novak JE, Kirkegaard K (1994) Coupling between genome translation and replication in an RNA virus. Genes Dev 8(14):1726-1737.
7. van Rossum CM, Garcia ML, Bol JF (1996) Accumulation of alfalfa mosaic virus RNAs 1 and 2 requires the encoded proteins in cis. J Virol 70(8):5100-5105.
8. Lewandowski DJ, Dawson WO (2000) Functions of the 126- and 183-kDa proteins of tobacco mosaic virus. Virology 271(1):90-98. (Pubitemid 30341518)
9. Liang Y, Gillam S (2001) Rubella virus RNA replication is cis-preferential and synthesis of negative- and positive-strand RNAs is regulated by the processing of nonstructural protein. Virology 282(2):307-319. (Pubitemid 32881158)
10. Okamoto K, et al. (2008) cis-Preferential requirement of a -1 frameshift product p88 for the replication of Red clover necrotic mosaic virus RNA1. Virology 375(1):205-212.
11. Yi G, Kao C (2008) cis- and trans-acting functions of brome mosaic virus protein 1a in genomic RNA1 replication. J Virol 82(6):3045-3053. (Pubitemid 351329192)
12. Wang J, Yeh H-H, Falk BW (2009) cis preferential replication of Lettuce infectious yellows virus (LIYV) RNA 1: The initial step in the asynchronous replication of the LIYV genomic RNAs. Virology 386(1):217-223.
13. Choi SK, Yoon J-Y, Canto T, Palukaitis P (2011) Replication of cucumber mosaic virus RNA 1 in cis requires functional helicase-like motifs of the 1a protein. Virus Res 158(1-2):271-276.
14. Barton DJ, Morasco BJ, Flanegan JB (1999) Translating ribosomes inhibit poliovirus negative-strand RNA synthesis. J Virol 73(12):10104-10112.
15. Gamarnik AV, Andino R (1998) Switch from translation to RNA replication in a posi-tive- stranded RNA virus. Genes Dev 12(15):2293-2304. (Pubitemid 28371350)
16. Daijogo S, Semler BL (2011) Mechanistic intersections between picornavirus translation and RNA replication. Adv Virus Res 80:1-24.
17. Goelet P, et al. (1982) Nucleotide sequence of tobacco mosaic virus RNA. Proc Natl Acad Sci USA 79(19):5818-5822. (Pubitemid 13199981)
18. Ishikawa M, Okada Y (2004) Replication of tobamovirus RNA. Proc Jpn Acad, Ser B 80(5):215-224.
19. Buck KW (1996) Comparison of the replication of positive-stranded RNA viruses of plants and animals. Adv Virus Res 47:159-251.
20. Yamafuji R, Watanabe Y, Meshi T, Okada Y (1991) Replication of TMV-L and Lta1 RNAs and their recombinants in TMV-resistant Tm-1 tomato protoplasts. Virology 183(1):99-105.
21. Buck KW (1999) Replication of tobacco mosaic virus RNA. Philos Trans R Soc Lond B Biol Sci 354(1383):613-627.
22. Agalarov SC, Sogorin EA, Shirokikh NE, Spirin AS (2011) Insight into the structural organization of the omega leader of TMV RNA: The role of various regions of the sequence in the formation of a compact structure of the omega RNA. Biochem Biophys Res Commun 404(1):250-253.
23. Shirokikh NE, Agalarov SCh, Spirin AS (2010) Chemical and enzymatic probing of spatial structure of the omega leader of tobacco mosaic virus RNA. Biochemistry (Mosc) 75(4):405-411.
24. Gallie DR, Sleat DE, Watts JW, Turner PC, Wilson TMA (1987) The 5′-leader sequence of tobacco mosaic virus RNA enhances the expression of foreign gene transcripts in vitro and in vivo. Nucleic Acids Res 15(8):3257-3273.
25. Sleat DE, et al. (1987) Characterisation of the 5′-leader sequence of tobacco mosaic virus RNA as a general enhancer of translation in vitro. Gene 60(2-3):217-225. (Pubitemid 18043767)
26. Takamatsu N, et al. (1991) Deletion analysis of the 5′ untranslated leader sequence of tobacco mosaic virus RNA. J Virol 65(3):1619-1622.
27. 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 USA 101(7):1863-1867. (Pubitemid 38228982)
28. Komoda K, Mawatari N, Hagiwara-Komoda Y, Naito S, Ishikawa M (2007) Identification of a ribonucleoprotein intermediate of tomato mosaic virus RNA replication complex formation. J Virol 81(6):2584-2591. (Pubitemid 46447024)
29. Nishikiori M, Meshi T, Ishikawa M (2012) Guanylylation-competent replication proteins of Tomato mosaic virus are disulfide-linked. Virology 434(1):118-128.
30. Auweter SD, Oberstrass FC, Allain FH-T (2006) Sequence-specific binding of single-stranded RNA: Is there a code for recognition? Nucleic Acids Res 34(17):4943-4959. (Pubitemid 44605637)
31. Goregaoker SP, Lewandowski DJ, Culver JN (2001) Identification and functional analysis of an interaction between domains of the 126/183-kDa replicase-associated proteins of tobacco mosaic virus. Virology 282(2):320-328. (Pubitemid 32881159)
32. Camborde L, et al. (2010) The ubiquitin-proteasome system regulates the accumulation of Turnip yellow mosaic virus RNA-dependent RNA polymerase during viral infection. Plant Cell 22(9):3142-3152.
33. Li XH, Carrington JC (1995) Complementation of tobacco etch potyvirus mutants by active RNA polymerase expressed in transgenic cells. Proc Natl Acad Sci USA 92(2):457-461.
34. Kubota K, Tsuda S, Tamai A, Meshi T (2003) Tomato mosaic virus replication protein suppresses virus-targeted posttranscriptional gene silencing. J Virol 77(20):11016-11026. (Pubitemid 37204293)
35. Ding XS, et al. (2004) The Tobacco mosaic virus 126-kDa protein associated with virus replication and movement suppresses RNA silencing. Mol Plant Microbe Interact 17(6):583-592. (Pubitemid 38642202)
36. Hagiwara-Komoda Y, et al. (2008) Overexpression of a host factor TOM1 inhibits tomato mosaic virus propagation and suppression of RNA silencing. Virology 376(1):132-139.
37. Osman TAM, Hemenway CL, Buck KW (2000) Role of the 3′ tRNA-like structure in tobacco mosaic virus minus-strand RNA synthesis by the viral RNA-dependent RNA polymerase In vitro. J Virol 74(24):11671-11680. (Pubitemid 32222316)
38. Osman TAM, Buck KW (2003) Identification of a region of the tobacco mosaic virus 126- and 183-kilodalton replication proteins which binds specifically to the viral 3′-terminal tRNA-like structure. J Virol 77(16):8669-8675. (Pubitemid 36936077)
39. Filomatori CV, et al. (2006) A 5′ RNA element promotes dengue virus RNA synthesis on a circular genome. Genes Dev 20(16):2238-2249.
40. Ishikawa M, Meshi T, Watanabe Y, Okada Y (1988) Replication of chimeric tobacco mosaic viruses which carry heterologous combinations of replicase genes and 3′ noncoding regions. Virology 164(1):290-293.
41. Ishikawa M, Kroner P, Ahlquist P, Meshi T (1991) Biological activities of hybrid RNAs generated by 3′-end exchanges between tobacco mosaic and brome mosaic viruses. J Virol 65(7):3451-3459.
42. Yuan X, Shi K, Meskauskas A, Simon AE (2009) 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 15(10):1849-1864.
43. Barry JK, Miller WA (2002) 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 USA 99(17):11133-11138. (Pubitemid 34920891)
44. Nozu Y, Okada Y (1968) Amino acid sequence of a common Japanese strain of tobacco mosaic virus. J Mol Biol 35(3):643-646.
45. Chiba Y, et al. (2003) S-adenosyl-L-methionine is an effector in the posttranscriptional autoregulation of the cystathionine γ-synthase gene in Arabidopsis. Proc Natl Acad Sci USA 100(18):10225-10230. (Pubitemid 37071860)
46. Ishibashi K, Komoda K, Ishikawa M (2006) In vitro translation and replication of tobamovirus RNA in a cell-free extract of evacuolated tobacco BY-2 protoplasts. Tobacco BY-2 Cells: From Cellular Dynamics to Omics, Biotechnology in Agriculture and Forestry, eds Nagata T, Matsuoka K, Inzé D (Springer, Berlin), Vol 58, pp 183-194.