Genomic analysis of codon, sequence and structural conservation with selective biochemical-structure mapping reveals highly conserved and dynamic structures in rotavirus RNAs with potential cis-acting functions

Nucleic Acids Research

Volumn 38, Issue 21, 2010, Pages 7718-7735

  Li, Wilson ^a   Manktelow, Emily ^a   Von Kirchbach, Johann C ^b   Gog, Julia R ^b   Desselberger, Ulrich ^a   Lever, Andrew M ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS RNA;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; CODON; GENE FUNCTION; GENE MAPPING; GENOME ANALYSIS; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; RNA REPLICATION; RNA SEQUENCE; RNA STRUCTURE; RNA TRANSLATION; ROTAVIRUS; STRUCTURE ANALYSIS;

BASE SEQUENCE; CODON; CONSERVED SEQUENCE; GENOME, VIRAL; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; OPEN READING FRAMES; PROTEIN BIOSYNTHESIS; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RIBONUCLEASES; RNA, VIRAL; ROTAVIRUS; UNTRANSLATED REGIONS;

MAMMALIA; ROTAVIRUS; ROTAVIRUS A;

EID: 78649901487     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkq663     Document Type: Article

References (85)

1. Parashar, U. D., Gibson, C. J., Bresse, J. S. and Glass, R. I. (2006) Rotavirus and severe childhood diarrhea. Emerg. Infect. Dis., 12, 304-306.
2. Ruiz-Palacios, G. M., Perez-Schael, I., Velazquez, F. R., Abate, H., Breuer, T., Clemens, S. C., Cheuvart, B., Espinoza, F., Gillard, P., Innis, B. L. et al. (2006) Safety and efficacy of an attenuated vaccine against severe rotavirus gastroenteritis. N. Engl. J. Med., 354, 11-22.
3. Vesikari, T., Matson, D. O., Dennehy, P., Van Damme, P., Santosham, M., Rodriguez, Z., Dallas, M. J., Heyse, J. F., Goveia, M. G., Black, S. B. et al. (2006) Safety and efficacy of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine. N. Engl. J. Med., 354, 23-33.
4. Estes, M. K. and Kapikian, A. Z. (2007) In Knipe, D. M. and Howley, P. M. (eds), Fields' Virology, Vol. II, 5th edn. Wolters Kluwer Health/Lippincott Williams & Wilkins, Philadelphia, pp. 1917-1974.
5. Cheung, W., Gill, M., Esposito, A., Kaminski, C., Courousse, N., Chwetzoff, S., Trugnan, G., Keshavan, N., Lever, A. and Desselberger, U. (2010) Rotaviruses associate with cellular lipid droplet components to replicate in viroplasms, and compounds disrupting or blocking lipid droplets inhibit viroplasm formation and viral replication. J. Virol., 84, 6782-6798.
6. Gale, M. Jr and Katze, M. G. (1998) Molecular mechanisms of interferon resistance mediated by viral-directed inhibition of PKR, the interferon-induced protein kinase. Pharmacol. Ther., 78, 29-46.
7. Reeves, M. B., Davies, A. A., McSharry, B. P., Wilkinson, G. W. and Sinclair, J. H. (2007) Complex I binding by a virally encoded RNA regulates mitochondria-induced cell death. Science, 316, 1345-1348.
8. Wentz, M. J., Patton, J. T. and Ramig, R. F. (1996) The 3′-terminal consensus sequence of rotavirus mRNA is the minimal promoter of negative-strand RNA synthesis. J. Virol., 70, 7833-7841.
9. 0 consensus sequence of rotavirus plus-strand RNAs promotes replication of the double-stranded RNA genome segments. RNA, 12, 133-146.
10. Chen, D. and Patton, J. T. (1998) Rotavirus RNA replication requires a single-stranded 3′ end for efficient minus-strand synthesis. J. Virol., 72, 7387-7396.
11. Lukavsky, P. J. (2009) Structure and function of HCV IRES domains. Virus Res., 139, 166-171.
12. Olsen, H. S., Nelbock, P., Cochrane, A. W. and Rosen, C. A. (1990) Secondary structure is the major determinant for interaction of HIV rev protein with RNA. Science, 247, 845-848.
13. Lever, A. M. (2007) HIV-1 RNA packaging. Adv. Pharmacol., 55, 1-32.
14. Hundley, F., Biryahwaho, B., Gow, M. and Desselberger, U. (1985) Genome rearrangements of bovine rotavirus after serial passage at high multiplicity of infection. Virology, 143, 88-103.
15. Gog, J. R., Afonso Edos, S., Dalton, R. M., Leclercq, I., Tiley, L., Elton, D., von Kirchbach, J. C., Naffakh, N., Escriou, N. and Digard, P. (2007) Codon conservation in the influenza A virus genome defines RNA packaging signals. Nucleic Acids Res., 35, 1897-1907.
16. Mathews, D. H., Sabina, J., Zuker, M. and Turner, D. H. (1999) Expanded sequence dependence of thermodynamic parameters improves prediction of RNA secondary structure. J. Mol. Biol., 288, 911-940.
17. Zuker, M. (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res., 31, 3406-3415.
18. Gruber, A. R., Lorenz, R., Bernhart, S. H., Neubock, R. and Hofacker, I. L. (2008) The Vienna RNA websuite. Nucleic Acids Res., 36, W70-W74.
19. Ruan, J., Stormo, G. D. and Zhang, W. (2004) An iterated loop matching approach to the prediction of RNA secondary structures with pseudoknots. Bioinformatics, 20, 58-66.
20. Knudsen, B. and Hein, J. (2003) Pfold: RNA secondary structure prediction using stochastic context-free grammars. Nucleic Acids Res., 31, 3423-3428.
21. Bernhart, S. H., Hofacker, I. L., Will, S., Gruber, A. R. and Stadler, P. F. (2008) RNAalifold: improved consensus structure prediction for RNA alignments. BMC Bioinformatics, 9, 474.
22. Thurner, C., Witwer, C., Hofacker, I. L. and Stadler, P. F. (2004) Conserved RNA secondary structures in Flaviviridae genomes. J. Gen. Virol., 85, 1113-1124.
23. Witwer, C., Rauscher, S., Hofacker, I. L. and Stadler, P. F. (2001) Conserved RNA secondary structures in Picornaviridae genomes. Nucleic Acids Res., 29, 5079-5089.
24. Hofacker, I. L., Stadler, P. F. and Stocsits, R. R. (2004) Conserved RNA secondary structures in viral genomes: a survey. Bioinformatics, 20, 1495-1499.
25. Wilm, A., Linnenbrink, K. and Steger, G. (2008) ConStruct: improved construction of RNA consensus structures. BMC Bioinformatics, 9, 219.
26. Gruber, A. R., Findeiss, S., Washietl, S., Hofacker, I. L. and Stadler, P. F. (2010) RNAz 2. 0: Improved Noncoding RNA Detection. Pac. Symp. Biocomput., 15, 69-79.
27. Benson, D. A., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J. and Wheeler, D. L. (2008) GenBank. Nucleic Acids Res., 36, D25-D30.
28. Hofacker, I. L. (2009) RNA secondary structure analysis using the Vienna RNA package. Curr. Protoc. Bioinformatics, 26, 12. 2. 1-12. 2. 16.
29. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R. et al. (2007) Clustal W and Clustal X version 2. 0. Bioinformatics, 23, 2947-2948.
30. Hofacker, I. L. (2003) Vienna RNA secondary structure server. Nucleic Acids Res., 31, 3429-3431.
31. Lowman, H. B. and Draper, D. E. (1986) On the recognition of helical RNA by cobra venom V1 nuclease. J. Biol. Chem., 261, 5396-5403.
32. Klarmann, G. J., Schauber, C. A. and Preston, B. D. (1993) Template-directed pausing of DNA synthesis by HIV-1 reverse transcriptase during polymerization of HIV-1 sequences in vitro. J. Biol. Chem., 268, 9793-9802.
33. 0 and 3′ of the catalytic site. Nucleic Acids Res., 26, 3433-3442.
34. Klasens, B. I., Huthoff, H. T., Das, A. T., Jeeninga, R. E. and Berkhout, B. (1999) The effect of template RNA structure on elongation by HIV-1 reverse transcriptase. Biochim. Biophys. Acta., 1444, 355-370.
35. Lopez, T., Rojas, M., Ayala-Breton, C., Lopez, S. and Arias, C. F. (2005) Reduced expression of the rotavirus NSP5 gene has a pleiotropic effect on virus replication. J. Gen. Virol., 86, 1609-1617.
36. Matthijnssens, J., Ciarlet, M., Rahman, M., Attoui, H., Banyai, K., Estes, M. K., Gentsch, J. R., Iturriza-Gomara, M., Kirkwood, C. D., Martella, V. et al. (2008) Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch. Virol., 153, 1621-1629.
37. Yang, A. D., Barro, M., Gorziglia, M. I. and Patton, J. T. (2004) Translation enhancer in the 3′-untranslated region of rotavirus gene 6 mRNA promotes expression of the major capsid protein VP6. Arch. Virol., 149, 303-321.
38. Imai, M., Akatani, K., Ikegami, N. and Furuichi, Y. (1983) Capped and conserved terminal structures in human rotavirus genome double-stranded RNA segments. J. Virol., 47, 125-136.
39. Tortorici, M. A., Broering, T. J., Nibert, M. L. and Patton, J. T. (2003) Template recognition and formation of initiation complexes by the replicase of a segmented double-stranded RNA virus. J. Biol. Chem., 278, 32673-32682.
40. Chen, D., Barros, M., Spencer, E. and Patton, J. T. (2001) Features of the 3′-consensus sequence of rotavirus mRNAs critical to minus strand synthesis. Virology, 282, 221-229.
41. Poncet, D., Aponte, C. and Cohen, J. (1993) Rotavirus protein NSP3 (NS34) is bound to the 3′ end consensus sequence of viral mRNAs in infected cells. J. Virol., 67, 3159-3165.
42. Poncet, D., Laurent, S. and Cohen, J. (1994) Four nucleotides are the minimal requirement for RNA recognition by rotavirus non-structural protein NSP3. EMBO J., 13, 4165-4173.
43. Greatorex, J. S., Laisse, V., Dockhelar, M. C. and Lever, A. M. (1996) Sequences involved in the dimerisation of human T cell leukaemia virus type-1 RNA. Nucleic Acids Res., 24, 2919-2923.
44. Shetty, S., Kim, S., Shimakami, T., Lemon, S. M. and Mihailescu, M. R. (2010) Hepatitis C virus genomic RNA dimerization is mediated via a kissing complex intermediate. RNA, 16, 913-925.
45. Ooms, M., Abbink, T. E., Pham, C. and Berkhout, B. (2007) Circularization of the HIV-1 RNA genome. Nucleic Acids Res., 35, 5253-5261.
46. 0 -terminal sequences of influenza A, B and C virus RNA segments are highly conserved and show partial inverted complementarity. Gene, 8, 315-328.
47. Fodor, E., Pritlove, D. C. and Brownlee, G. G. (1994) The influenza virus panhandle is involved in the initiation of transcription. J. Virol., 68, 4092-4096.
48. Hsu, M. T., Parvin, J. D., Gupta, S., Krystal, M. and Palese, P. (1987) Genomic RNAs of influenza viruses are held in a circular conformation in virions and in infected cells by a terminal panhandle. Proc. Natl Acad. Sci. USA, 84, 8140-8144.
49. Leahy, M. B., Dessens, J. T., Pritlove, D. C. and Nuttall, P. A. (1998) The Thogoto orthomyxovirus cRNA promoter functions as a panhandle but does not stimulate cap snatching in vitro. J. Gen. Virol., 79, 457-460.
50. Lee, Y. S. and Seong, B. L. (1998) Nucleotides in the panhandle structure of the influenza B virus virion RNA are involved in the specificity between influenza A and B viruses. J. Gen. Virol., 79, 673-681.
51. Pritlove, D. C., Fodor, E., Seong, B. L. and Brownlee, G. G. (1995) In vitro transcription and polymerase binding studies of the termini of influenza A virus cRNA: evidence for a cRNA panhandle. J. Gen. Virol., 76, 2205-2213.
52. Weber, F., Haller, O. and Kochs, G. (1997) Conserved vRNA end sequences of Thogoto-orthomyxovirus suggest a new panhandle structure. Arch. Virol., 142, 1029-1033.
53. Herold, J. and Andino, R. (2001) Poliovirus RNA replication requires genome circularization through a protein-protein bridge. Mol. Cell, 7, 581-591.
54. Martinez-Salas, E., Pacheco, A., Serrano, P. and Fernandez, N. (2008) New insights into internal ribosome entry site elements relevant for viral gene expression. J. Gen. Virol., 89, 611-626.
55. Patton, J. T. (2001) Rotavirus RNA replication and gene expression. Novartis Found Symp., 238, 64-77.
56. Vende, P., Piron, M., Castagne, N. and Poncet, D. (2000) Efficient translation of rotavirus mRNA requires simultaneous interaction of NSP3 with the eukaryotic translation initiation factor eIF4G and the mRNA 3′ end. J. Virol., 74, 7064-7071.
57. Lu, X., McDonald, S. M., Tortorici, M. A., Tao, Y. J., Vasquez-Del Carpio, R., Nibert, M. L., Patton, J. T. and Harrison, S. C. (2008) Mechanism for coordinated RNA packaging and genome replication by rotavirus polymerase VP1. Structure, 16, 1678-1688.
58. Guglielmi, K. M., McDonald, S. M. and Patton, J. T. (2010) Mechanism of intraparticle synthesis of the rotavirus double-stranded RNA genome. J. Biol. Chem., 285, 18123-18128.
59. Barro, M., Mandiola, P., Chen, D., Patton, J. T. and Spencer, E. (2001) Identification of sequences in rotavirus mRNAs important for minus strand synthesis using antisense oligonucleotides. Virology, 288, 71-80.
60. Hellen, C. U. and Sarnow, P. (2001) Internal ribosome entry sites in eukaryotic mRNA molecules. Genes Dev., 15, 1593-1612.
61. Vagner, S., Galy, B. and Pyronnet, S. (2001) Irresistible IRES. Attracting the translation machinery to internal ribosome entry sites. EMBO Rep., 2, 893-898.
62. Miller, W. A., Wang, Z. and Treder, K. (2007) The amazing diversity of cap-independent translation elements in the 3′-untranslated regions of plant viral RNAs. Biochem. Soc. Trans., 35, 1629-1633.
63. Rainsford, E. W. and McCrae, M. A. (2007) Characterization of the NSP6 protein product of rotavirus gene 11. Virus Res., 130, 193-201.
64. Kozak, M. (1987) Effects of intercistronic length on the efficiency of reinitiation by eucaryotic ribosomes. Mol. Cell Biol., 7, 3438-3445.
65. Kozak, M. (1989) Context effects and inefficient initiation at non-AUG codons in eucaryotic cell-free translation systems. Mol. Cell Biol., 9, 5073-5080.
66. Ryabova, L. A., Pooggin, M. M. and Hohn, T. (2006) Translation reinitiation and leaky scanning in plant viruses. Virus Res., 119, 52-62.
67. Schmidt-Puchta, W., Dominguez, D., Lewetag, D. and Hohn, T. (1997) Plant ribosome shunting in vitro. Nucleic Acids Res., 25, 2854-2860.
68. 0-UTR identifies essential elements of a ribosomal shunt. Nucleic Acids Res., 37, 5838-5847.
69. Latorre, P., Kolakofsky, D. and Curran, J. (1998) Sendai virus Y proteins are initiated by a ribosomal shunt. Mol. Cell Biol., 18, 5021-5031.
70. Yueh, A. and Schneider, R. J. (2000) Translation by ribosome shunting on adenovirus and hsp70 mRNAs facilitated by complementarity to 18S rRNA. Genes Dev., 14, 414-421.
71. Olkkonen, V. M., Gottlieb, P., Strassman, J., Qiao, X. Y., Bamford, D. H. and Mindich, L. (1990) In vitro assembly of infectious nucleocapsids of bacteriophage phi 6: formation of a recombinant double-stranded RNA virus. Proc. Natl Acad. Sci. USA, 87, 9173-9177.
72. Poranen, M. M., Paatero, A. O., Tuma, R. and Bamford, D. H. (2001) Self-assembly of a viral molecular machine from purified protein and RNA constituents. Mol. Cell, 7, 845-854.
73. Mindich, L. (1999) Precise packaging of the three genomic segments of the double-stranded-RNA bacteriophage phi6. Microbiol. Mol. Biol. Rev., 63, 149-160.
74. Huiskonen, J. T., de Haas, F., Bubeck, D., Bamford, D. H., Fuller, S. D. and Butcher, S. J. (2006) Structure of the bacteriophage phi6 nucleocapsid suggests a mechanism for sequential RNA packaging. Structure, 14, 1039-1048.
75. Taraporewala, Z. F. and Patton, J. T. (2001) Identification and characterization of the helix-destabilizing activity of rotavirus nonstructural protein NSP2. J. Virol., 75, 4519-4527.
76. Zou, S. and Brown, E. G. (1992) Identification of sequence elements containing signals for replication and encapsidation of the reovirus M1 genome segment. Virology, 186, 377-388.
77. Ni, Y. and Kemp, M. C. (1994) Subgenomic S1 segments are packaged by avian reovirus defective interfering particles having an S1 segment deletion. Virus Res., 32, 329-342.
78. Fujii, Y., Goto, H., Watanabe, T., Yoshida, T. and Kawaoka, Y. (2003) Selective incorporation of influenza virus RNA segments into virions. Proc. Natl Acad. Sci. USA, 100, 2002-2007.
79. Watanabe, T., Watanabe, S., Noda, T., Fujii, Y. and Kawaoka, Y. (2003) Exploitation of nucleic acid packaging signals to generate a novel influenza virus-based vector stably expressing two foreign genes. J. Virol., 77, 10575-10583.
80. Marsh, G. A., Hatami, R. and Palese, P. (2007) Specific residues of the influenza A virus hemagglutinin viral RNA are important for efficient packaging into budding virions. J. Virol., 81, 9727-9736.
81. Fujii, K., Fujii, Y., Noda, T., Muramoto, Y., Watanabe, T., Takada, A., Goto, H., Horimoto, T. and Kawaoka, Y. (2005) Importance of both the coding and the segment-specific noncoding regions of the influenza A virus NS segment for its efficient incorporation into virions. J. Virol., 79, 3766-3774.
82. Liang, Y., Hong, Y. and Parslow, T. G. (2005) cis-Acting packaging signals in the influenza virus PB1, PB2, and PA genomic RNA segments. J. Virol., 79, 10348-10355.
83. Muramoto, Y., Takada, A., Fujii, K., Noda, T., Iwatsuki-Horimoto, K., Watanabe, S., Horimoto, T., Kida, H. and Kawaoka, Y. (2006) Hierarchy among viral RNA (vRNA) segments in their role in vRNA incorporation into influenza A virions. J. Virol., 80, 2318-2325.
84. Marsh, G. A., Rabadan, R., Levine, A. J. and Palese, P. (2008) Highly conserved regions of influenza a virus polymerase gene segments are critical for efficient viral RNA packaging. J. Virol., 82, 2295-2304.
85. Gao, Q. and Palese, P. (2009) Rewiring the RNAs of influenza virus to prevent reassortment. Proc. Natl Acad. Sci. USA, 106, 15891-15896.