Detailed mapping of RNA secondary structures in core and NS5B-encoding region sequences of hepatitis C virus by RNase cleavage and novel bioinformatic prediction methods

Journal of General Virology

Volumn 85, Issue 10, 2004, Pages 3037-3047

  Tuplin, A ^a   Evans, D J ^b   Simmonds, Peter ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CIS ACTING ELEMENT; RIBONUCLEASE; VIRUS RNA; NS 5 PROTEIN, HEPATITIS C VIRUS; NS-5 PROTEIN, HEPATITIS C VIRUS; VIRUS PROTEIN;

ARTICLE; BIOINFORMATICS; COMPUTER PROGRAM; CONTROLLED STUDY; GENE FREQUENCY; GENE MAPPING; GENETIC CONSERVATION; GENETIC VARIABILITY; GENOTYPE; HEPATITIS C VIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PREDICTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; RNA CLEAVAGE; RNA SEQUENCE; RNA TRANSCRIPTION; SEQUENCE ANALYSIS; VIRUS GENOME; BIOLOGY; CHEMISTRY; CONFORMATION; GENETICS; METABOLISM;

HEPATITIS C VIRUS; RNA VIRUSES;

COMPUTATIONAL BIOLOGY; HEPACIVIRUS; NUCLEIC ACID CONFORMATION; RIBONUCLEASES; RNA, VIRAL; VIRAL NONSTRUCTURAL PROTEINS;

EID: 5444272324     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.80141-0     Document Type: Article

References (43)

1. Barrera, I., Schuppli, D., Sogo, J. M. & Weber, H. (1993) Different mechanisms of recognition of bacteriophage Qβ plus and minus strand RNAs by Qβ replicase. J Mol Biol 232, 512-521.
2. Boulant, S., Becchi, M., Penin, F. & Lavergne, J.-P. (2003). Unusual multiple recoding events leading to alternative forms of hepatitis C virus core protein from genotype 1b. J Biol Chem 278, 45785-45792.
3. Fletcher, S. P., Ali, I. K., Kaminski, A., Digard, P. & Jackson, R. J. (2002). The influence of viral coding sequences on pestivirus IRES activity reveals further parallels with translation initiation in prokaryotes. RNA 8, 1558-1571.
4. Giedroc, D. P., Theimer, C. A. & Nixon, P. L. (2000). Structure, stability and function of RNA pseudoknots involved in stimulating ribosomal frameshifting. J Mol Biol 298, 167-185.
5. Goodfellow, I., Chaudhry, Y., Richardson, A., Meredith, J., Almond, J. W., Barclay, W. & Evans, D. J. (2000). Identification of a cis-acting replication element within the poliovirus coding region. J Virol 74, 4590-4600.
6. Han, J. H. & Houghton, M. (1992). Group specific sequences and conserved secondary structures at the 3′ end of HCV genome and its implication for viral replication. Nucleic Acids Res 20, 3520.
7. Hofacker, I. L., Fekete, M., Flamm, C., Huynen, M. A., Rauscher, S., Stolorz, P. E. & Stadler, P. F. (1998). Automatic detection of conserved RNA structure elements in complete RNA virus genomes. Nucleic Acids Res 26, 3825-3836.
8. Honda, M., Brown, E. A. & Lemon, S. M. (1996a). Stability of a stem-loop involving the initiator AUG controls the efficiency of internal initiation of translation on hepatitis C virus RNA. RNA 2, 955-968.
9. Honda, M., Ping, L.-H., Rijnbrand, R. C. A., Amphlett, E., Clarke, B., Rowlands, D. & Lemon, S. M. (1996b). Structural requirements for initiation of translation by internal ribosome entry within genome-length hepatitis C virus RNA. Virology 222, 31-42.
10. Honda, M., Rijnbrand, R., Abell, G., Kim, D. & Lemon, S. M. (1999). Natural variation in translational activities of the 5′ nontranslated RNAs of hepatitis C virus genotypes 1a and 1b: evidence for a long-range RNA-RNA interaction outside of the internal ribosomal entry site. J Virol 73, 4941-4951.
11. Ina, Y., Mizokami, M., Ohba, K. & Gojobori, T. (1994). Reduction of synonymous substitutions in the core protein gene of hepatitis C virus. J Mol Evol 38, 50-56.
12. Inoue, T. & Cech, T. R. (1985). Secondary structure of the circular form of the Tetrahymena rRNA intervening sequence: a technique for RNA structure analysis using chemical probes and reverse transcriptase. Proc Natl Acad Sci U S A 82, 648-652.
13. Janda, M. & Ahlquist, P. (1998). Brome mosaic virus RNA replication protein 1a dramatically increases in vivo stability but not translation of viral genomic RNA3. Proc Natl Acad Sci U S A 95 2227-2232.
14. Keskinen, P., Nyqvist, M., Sareneva, T., Pirhonen, J., Melén, K. & Julkunen, I. (1999). Impaired antiviral response in human hepatoma cells. Virology 263, 364-375.
15. Kim, Y. K., Lee, S. H., Kim, C. S., Seol, S. K. & Jang, S. K. (2003). Long-range RNA-RNA interaction between the 5′ nontranslated region and the core-coding sequences of hepatitis C virus modulates the IRES-dependent translation. RNA 9, 599-606.
16. Kolykhalov, A. A., Feinstone, S. M. & Rice, C. M. (1996) Identification of a highly conserved sequence element at the 3′ terminus of hepatitis C virus genome RNA. J Virol 70, 3363-3371.
17. Lee, H., Shin, H., Wimmer, E. & Paul, A. V. (2004). cis-acting RNA signals in the NS5B C-terminal coding sequence of the hepatitis C virus genome. J Virol (in press).
18. Lobert, P.-E., Escriou, N., Ruelle, J. & Michiels, T. (1999). A coding RNA sequence acts as a replication signal in cardioviruses. Proc Natl Acad Sci U S A 96, 11560-11565.
19. Mason, P. W., Bezborodova, S. V. & Henry, T. M. (2002). identification and characterization of a cis-acting replication element (cre) adjacent to the internal ribosome entry site of foot-and-mouth disease virus. J Virol 76, 9686-9694.
20. McKnight, K. L. & Lemon, S. M. (1998). The rhinovirus type 14 genome contains an internally located RNA structure that is required for viral replication. RNA 4, 1569-1584.
21. Reynolds, J. E., Kaminski, A., Kettinen, H. J., Grace, K., Clarke, B. E., Carroll, A. R., Rowlands, D. J. & Jackson, R. J. (1995). Unique features of internal initiation of hepatitis C virus RNA translation. EMBO J 14, 6010-6020.
22. Reynolds, J. E., Kaminski, A., Carroll, A. R., Clarke, B. E., Rowlands, D. J. & Jackson, R. J. (1996). Internal initiation of translation of hepatitis C virus RNA: the ribosome entry site is at the authentic initiation codon. RNA 2, 867-878.
23. Rijnbrand, R., Bredenbeek, P. J., Haasnoot, P. C., Kieft, J. S., Spaan, W. J. M. & Lemon, S. M. (2001). The influence of downstream protein-coding sequence on internal ribosome entry on hepatitis C virus and other flavivirus RNAs. RNA 7, 585-597.
24. Roussel, J., Pillez, A., Montpellier, C., Duverlie, G., Cahour, A., Dubuisson, J. & Wychowski, C. (2003). Characterization of the expression of the hepatitis C virus F protein. J Gen Virol 84, 1751-1759.
25. Shelness, G. S. & Williams, D. L. (1985). Secondary structure analysis of apolipoprotein II mRNA using enzymatic probes and reverse transcriptase. Evaluation of primer extension for high resolution structure mapping of mRNA. J Biol Chem 260, 8637-8646.
26. Simmonds, P. & Smith, D. B. (1999). Structural constraints on RNA virus evolution. J Virol 73, 5787-5794.
27. Simmonds, P., Tuplin, A. & Evans, D. J. (2004). Detection of genome-scale ordered RNA structure (GORS) in genomes of positive-stranded RNA viruses: implications for virus evolution and host persistence. RNA (in press).
28. Smith, D. B. & Simmonds, P. (1997). Characteristics of nucleotide substitution in the hepatitis C virus genome: constraints on sequence change in coding regions at both ends of the genome. J Mol Evol 45, 238-246.
29. Stern, S., Moazed, D. & Noller, H. F. (1988). Structural analysis of RNA using chemical and enzymatic probing monitored by primer extension. Methods Enzymol 164, 481-489.
30. Tsukiyama-Kohara, K., Iizuka, N., Kohara, M. & Nomoto, A. (1992). Internal ribosome entry site within hepatitis C virus RNA. J Virol 66, 1476-1483.
31. Tuplin, A., Wood, J., Evans, D. J., Patel, A. H. & Simmonds, P. (2002). Thermodynamic and phylogenetic prediction of RNA secondary structures in the coding region of hepatitis C virus. RNA 8, 824-841.
32. Varaklioti, A., Vassilaki, N., Georgopoulou, U. & Mavromara, P. (2002). Alternate translation occurs within the core coding region of the hepatitis C viral genome. J Biol Chem 277 17713-17721.
33. Vassilaki, N. & Mavromara, P. (2003). Two alternative translation mechanisms are responsible for the expression of the HCV ARFP/F/core+1 coding open reading frame. J Biol Chem 278, 40503-40513.
34. Walewski, J. L., Keller, T. R., Stump, D. D. & Branch, A. D. (2001). Evidence for a new hepatitis C virus antigen encoded in an overlapping reading frame. RNA 7, 710-721.
35. Walewski, J. L., Gutierrez, J. A., Branch-Elliman, W., Stump, D. D., Keller, T. R., Rodriguez, A., Benson, G. & Branch, A. D. (2002). Mutation Master: profiles of substitutions in hepatitis C virus RNA of the core, alternate reading frame, and NS2 coding regions. RNA 8, 557-571.
36. Wang, C., Sarnow, P. & Siddiqui, A. (1993). Translation of human hepatitis C virus RNA in cultured cells is mediated by an internal ribosome-binding mechanism. J Virol 67, 3338-3344.
37. Wang, C., Le, S. Y., Ali, N. & Siddiqui, A. (1995). An RNA pseudoknot is an essential structural element of the internal ribosome entry site located within the hepatitis C virus 5′ noncoding region. RNA 1, 526-537.
38. Xu, Z., Choi, J., Yen, T. S. B., Lu, W., Strohecker, A., Govindarajan, S., Chien, D., Selby, M. J. & Ou, J. (2001). Synthesis of a novel hepatitis C virus protein by ribosomal frameshift. EMBO J 20, 3840-3848.
39. Xu, Z., Choi, J., Lu, W. & Ou, J. (2003). Hepatitis C virus F protein is a short-lived protein associated with the endoplasmic reticulum. J Virol 77, 1578-1583.
40. Yi, M. & Lemon, S. M. (2003). 3′ nontranslated RNA signals required for replication of hepatitis C virus RNA. J Virol 77, 3557-3568.
41. You, S., Stump, D. D., Branch, A. D. & Rice, C. M. (2004). A cis-acting replication element in the sequence encoding the NS5B RNA-dependent RNA polymerase is required for hepatitis C virus RNA replication. J Virol 78, 1352-1366.
42. Zuker, M. (2000). Calculating nucleic acid secondary structure. Curr Opin Struct Biol 10, 303-310.
43. Zuker, M. (2003). Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31, 3406-3415.