Influenza Virus RNA Structure: Unique and Common Features

REFERENCES

• Cox NJ, Subbarao K. Global epidemiology of influenza: Past and present. Annu Rev Med 2000;51:407–421.
   PubMed Web of Science ®Google Scholar
• Horimoto T, Kawaoka Y. Influenza: Lessons from past pandemics, warnings from current incidents. Nature Rev Microbiol 2005;3:591–600.
   PubMed Web of Science ®Google Scholar
• Nelson MI, Holmes EC. The evolution of epidemic influenza. Nature Rev Genet 2007;8:196–204.
   PubMed Web of Science ®Google Scholar
• Parrish CR, Kawaoka Y. The origins of new pandemic viruses: The acquisition of new host ranges by canine parvovirus and influenza A viruses. Annu Rev Microbiol 2005;59:553–586.
   PubMed Web of Science ®Google Scholar
• Finkelstein DB, Mukatira S, Mehta PK, Persistent host markers in pandemic and H5N1 influenza viruses. J Virol 2007;81:10292–10299.
   PubMed Web of Science ®Google Scholar
• de Wit E, Fouchier RAM. Emerging influenza. J Clin Virol 2008;41:1–6.
   PubMed Web of Science ®Google Scholar
• Basler CF, Aguilar PV. Progress in identifying virulence determinants of the 1918 H1N1 and the Southeast Asian H5N1 influenza A viruses. Antiviral Res 2008;79:166–178.
   PubMed Web of Science ®Google Scholar
• Brierley I, Pennell S, Gilbert RJ. Viral RNA pseudoknots: Versatile motifs in gene expression and replication. Nature Rev Microbiol 2007;5: 598–610.
   PubMed Web of Science ®Google Scholar
• Liu Y, Wimmer E, Paul AV. Cis-acting RNA elements in human and animal plus-strand RNA viruses. Biochim Biophys Acta 2009;1789:495–517.
   Google Scholar
• Schroeder S. Advances in RNA structure prediction from sequence: New tools for generating hypotheses about viral RNA structure-function relationships. J Virol 2009;83:6326–6334.
   Google Scholar
• Simmonds P, Tuplin A, and Evans DJ. Detection of genome-scale ordered RNA structure (GORS) in genomes of positive-stranded RNA viruses: Implications for virus evolution and host persistence. RNA 2004;10:1337–1351.
   Google Scholar
• Ortin J, Parra F. Structure and function of RNA replication. Annu Rev Microbiol 2006;60:305–326.
   PubMed Web of Science ®Google Scholar
• Coloma R, Valpuesta JM, Arranz R, The structure of a biologically active influenza virus ribonucleoprotein complex. PLoS Pathogens 2009;5:e1000491.
   PubMed Web of Science ®Google Scholar
• Baudin F, Bach C, Cusack S, Ruigrok RWH. Structure of influenza virus RNP. I. Influenza virus nucleoprotein melts secondary structure in panhandle RNA and exposes the bases to the solvent. EMBO J 1994;13:3158–3165.
   Google Scholar
• Klumpp K, Ruigrok RWH, Baudin F. Roles of the influenza virus polymerase and nucleoprotein in forming a functional RNP structure. EMBO J 1997;16:1248–1257.
   PubMed Web of Science ®Google Scholar
• Brower-Sinning R, Carter DM, Crevar CJ, The role of RNA folding free energy in the evolution of the polymerase genes of the influenza A virus. Genome Biol 2009;10:R18.
   PubMed Web of Science ®Google Scholar
• Rabadan R, Levine AJ, Robins H. Comparison of avian and human influenza A viruses reveals a mutational bias on the viral genomes. J Virol 2006;80:11887–11891.
   Google Scholar
• Greenbaum BD, Levine AJ, Bhanot G, Rabadan R. Patterns of evolution and host gene mimicry in influenza and other RNA viruses. PLoS Pathogens 2008;4:e1000079.
   PubMed Web of Science ®Google Scholar
• Rivas E, Eddy SR. Secondary structure alone is generally not statistically significant for the detection of noncoding RNAs. Bioinformatics 2000;16:583–605.
   Google Scholar
• Skehel JJ, Hay AJ. Nucleotide sequences at the 5′ termini of influenza virus RNAs and their transcripts. Nucleic Acids Res 1978;5:1207–1219.
   Google Scholar
• Robertson JS. 5′ and 3′ terminal nucleotide sequences of the RNA genome segments of influenza virus. Nucleic Acids Res 1979;6:3745–3757.
   PubMed Web of Science ®Google Scholar
• Neumann G, Brownlee GG, Fodor E, Kawaoka Y. Orthomyxovirus replication, transcription, and polyadenylation. Curr Top Microbiol Immunol 2004;283:121–143.
   PubMed Web of Science ®Google Scholar
• Hsu, M-T, Parvin JD, Gupta S, 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 U S A 1987;84:8140–8144.
   PubMed Web of Science ®Google Scholar
• Flick R, Elgh F, Hobom G, Pettersson RF. Mutational analysis of the Uukuniemi virus (Bunyaviridae family) promoter reveals two elements of functional importance. J Virol 2002;76:10849–10860.
   Google Scholar
• Perez M, de la Torre JC. Characterization of the genomic promoter of the prototypic arenavirus lymphocytic choriomeningitis virus. J Virol 2003;77:1184–1194.
   Google Scholar
• Barr JN, Wertz GW. Role of the conserved nucleotide mismatch within 3′- and 5′-terminal regions of Bunyamwera virus in signaling transcription. J Virol 2005;79:3586–3594.
   Google Scholar
• Fodor E, Pritlove DC, Brownlee GG. The influenza virus panhandle is involved in the initiation of transcription. J Virol 1994;68:4092–4096.
   PubMed Web of Science ®Google Scholar
• Kim HJ, Fodor E, Brownlee GG, Seong BL. Mutational analysis of the RNA-fork model of the influenza A virus vRNA promoter. J Gen Virol 1997;78:353–357.
   PubMedGoogle Scholar
• Flick R, Neumann G, Hoffmann E, Promoter elements in the influenza vRNA terminal structure. RNA 1996;2:1046–1057.
   PubMed Web of Science ®Google Scholar
• Leahy MB, Dobbyn HC, Brownlee GG. Hairpin loop structure in the 3′ arm of the influenza A virus virion RNA promoter is required for endonuclease activity. J Virol 2001;75:7042–7049.
   Google Scholar
• Brownlee GG, Sharps JL. The RNA polymerase of influenza A virus is stabilized by interaction with its viral RNA promoter. J Virol 2002;76:7103–7113.
   PubMed Web of Science ®Google Scholar
• Pritlove DC, Poon LLM, Devenish LN, A hairpin loop at the 5′ end of influenza A virus virion RNA is required for synthesis of poly(A)+ mRNA in vitro. J Virol 1999;73:2109–2114.
   Google Scholar
• Robertson JS, Schubert M, Lazzarini RA. Polyadenylation sites for influenza virus mRNA. J Virol 1981;38:157–163.
   PubMed Web of Science ®Google Scholar
• Poon LLM, Pritlove DC, Fodor E, Brownlee GG. Direct evidence that the poly(A) tail of influenza A virus mRNA is synthesized by reiterative copying of a U track in the virion RNA template. J Virol 1999;73:3473–3476.
   PubMed Web of Science ®Google Scholar
• Leahy MB, Dessens JT, Nuttall PA. Striking conformational similarities between the transcription promoters of Thogoto and influenza A viruses: Evidence for intrastrand base pairing in the 5′ promoter arm. J Virol 1997;71:8352–8356.
   Google Scholar
• Mir MA, Panganiban AT. Characterization of the RNA chaperone activity of hantavirus nucleocapsid protein. J Virol 2006;80:6276–6285.
   PubMed Web of Science ®Google Scholar
• Wertz GW, Whelan S, LeGrone A, Ball LA. Extent of terminal complementarity modulates the balance between transcription and replication of vesicular stomatitis virus RNA. Proc Natl Acad Sci U S A 1994;91:8587–8591.
   Google Scholar
• Gritsun TS, Gould EA. Origin and evolution of flavivirus 5′UTRs and panhandles: Trans-terminal duplications? Virology 2007;366:8–15.
   Google Scholar
• Van Den Born E, Posthuma CC, Gultyaev AP, Snijder EJ. Discontinuous subgenomic RNA synthesis in arteriviruses is guided by an RNA hairpin structure located in the genomic leader region. J Virol 2005;79:6312–6324.
   PubMedGoogle Scholar
• Olsthoorn RCL, Mertens S, Brederode FT, Bol JF. A conformational switch at the 3′ end of a plant virus RNA regulates viral replication. EMBO J 1999;18:4856–4864.
   PubMed Web of Science ®Google Scholar
• Chen S-C, Olsthoorn RCL. In vitro and in vivo studies of the RNA conformational switch in alfalfa mosaic virus. J Virol 2010;84:1423–1429.
   Google Scholar
• Ortega J, Martin-Benito J, Zürcher T, Ultrastructural and functional analyses of recombinant influenza virus ribonucleoproteins suggest dimerization of nucleoprotein during virus amplification. J Virol 2000;74:156–163.
   PubMed Web of Science ®Google Scholar
• Hutchinson A, von Kirchbach JC, Gog JR, Digard P. Genome packaging in influenza A virus. J Gen Virol 2010;91:313–328.
   PubMed Web of Science ®Google Scholar
• Tchatalbachev S, Flick R, Hobom G. The packaging signal of influenza viral RNA molecules. RNA 2001;7:979–989.
   Google Scholar
• Noda T, Sagara H, Yen A, Architecture of ribonucleoprotein complexes in influenza A virus particles. Nature 2006;439:490–492.
   PubMed Web of Science ®Google Scholar
• de Wit E, Spronken MIJ, Rimmelzwaan GF, Evidence for specific packaging of the influenza A virus genome from conditionally defective virus particles lacking a polymerase gene. Vaccine 2006;24:6647–6650.
   Google Scholar
• Gao Q, Brydon EWA, Palese P. A seven-segmented influenza A virus expressing the influenza C virus glycoprotein HEF. J Virol 2008;82:6419–6426.
   Google Scholar
• Gao Q, Palese P. Rewiring the RNAs of influenza virus to prevent reassortment. Proc Natl Acad Sci U S A 2009;106:15891–15896.
   Google Scholar
• Muramoto Y, Takada A, Fijii K, Hierarchy among viral RNA (vRNA) segments in their role in vRNA incorporation into influenza A virions. J Virol 2006;80:2318–2325.
   Google Scholar
• Marsh GA, Hatami R, Palese P. Specific residues of the influenza A virus hemagglutinin viral RNA are important for efficient packaging into budding virions. J Virol 2007;81:9727–9736.
   PubMed Web of Science ®Google Scholar
• Marsh GA, Rabadan R, Levine AJ, Palese P. Highly conserved regions of influenza A virus polymerase gene segments are critical for efficient viral RNA packaging. J Virol 2008;82:2295–2304.
   Google Scholar
• Hutchinson EC, Wise HM, Kudryavtseva K, Characterisation of influenza A viruses with mutations in segment 5 packaging signals. Vaccine 2009;27:6270–6275.
   Google Scholar
• Fujii Y, Goto H, Watanabe T, Selective incorporation of influenza virus RNA segments into virions. Proc Natl. Acad. Sci. U S A 2003;100:2002–2007.
   PubMed Web of Science ®Google Scholar
• Ruigrok RWH, Baudin F. Structure of influenza virus ribonucleoprotein particles. II. Purified RNA-free influenza virus ribonucleoprotein forms structures that are indistinguishable from the intact influenza virus ribonucleoprotein particles. J Gen Virol 1995;76:1009–1014.
   PubMed Web of Science ®Google Scholar
• Yamanaka K, Ishihama A, Nagata K. Reconstitution of influenza virus RNA-nucleoprotein complexes structurally resembling native viral ribonucleoprotein cores. J Biol Chem 1990;265:11151–11155.
   PubMed Web of Science ®Google Scholar
• Fujii K, Ozawa M, Iwatsuki-Horimoto K, Incorporation of influenza A virus genome segments does not absolutely require wild-type sequences. J Gen Virol 2009;90:1734–1740.
   Google Scholar
• Liang, Y, Huang T, Ly H, Mutational analysis of packaging signals in influenza virus PA, PB1, and PB2 genomic RNA segments. J Virol 2008;82:229–236.
   PubMedGoogle Scholar
• Ortin J. Multiple levels of posttranscriptional regulation of influenza virus gene expression. Semin Virol 1998;8:335–342.
   Google Scholar
• Kash JC, Goodman AG, Korth MJ, Katze MG. Hijacking of the host-cell response and translational control during influenza virus infection. Virus Res 2006;119:111–120.
   Google Scholar
• Garfinkel MS, Katze MG. Translational control by influenza virus. J Biol Chem 1993;268:22223–22226.
   PubMed Web of Science ®Google Scholar
• Enami K, Sato TA, Nakada S, Enami M. Influenza virus NS1 protein stimulates translation of the M1 protein. J Virol 1994;68:1432–1437.
   PubMedGoogle Scholar
• de la Luna S, Fortes P, Beloso A, Ortin J. Influenza virus NS1 protein enhances the rate of translation initiation of viral mRNAs. J Virol 1995;69:2427–2433.
   PubMedGoogle Scholar
• Park YW, Wilusz J, Katze MG. Regulation of eukaryotic protein synthesis: Selective influenza viral mRNA translation is mediated by the cellular RNA-binding protein GRSF-1. Proc Natl Acad Sci U S A 1999;96:6694–6699.
   PubMedGoogle Scholar
• Kash JC, Cunningham DM, Smit MW, Selective translation of eukaryotic mRNAs: Functional molecular analysis of GRSF-1, a positive regulator of influenza virus protein synthesis. J Virol 2002;76:10417–10426.
   PubMedGoogle Scholar
• Watts JM, Dang KK, Gorelick RJ, Architecture and secondary structure of an entire HIV-1 RNA genome. Nature 2009;460:711–716.
   PubMed Web of Science ®Google Scholar
• Guisez Y, Robbens J, Remaut E, Fiers W. Folding of the MS2 coat protein in Escherichia coli is modulated by translational pauses resulting from mRNA secondary structure and codon usage: A hypothesis. J Theor Biol 1993;162:243–252.
   PubMed Web of Science ®Google Scholar
• Lamb RA, Horvath CM. Diversity of coding strategies in influenza viruses. Trends Genet 1991;7:261–266.
   PubMedGoogle Scholar
• Gultyaev AP, Heus HA, Olsthoorn RCL. An RNA conformational shift in recent H5N1 influenza A viruses. Bioinformatics 2007;23:272–276.
   Google Scholar
• Gultyaev AP, Olsthoorn RCL. A family of non-classical pseudoknots in influenza A and B viruses. RNA Biol 2010;7:125–129.
   PubMed Web of Science ®Google Scholar
• Ducatez MF, Olinger CM, Owoade AA, Molecular and antigenic evolution and geographical spread of H5N1 highly pathogenic avian influenza viruses in western Africa. J Gen Virol 2007;88:2297–2306.
   PubMed Web of Science ®Google Scholar
• Plotch SJ, Krug RM. In vitro splicing of influenza viral NS1 mRNA and NS1-β-globin chimeras: Possible mechanisms for the control of viral mRNA splicing. Proc Natl Acad Sci U S A 1986;83:5444–5448.
   PubMedGoogle Scholar
• Nemeroff ME, Utans U, Krämer A, Krug RM. Identification of cis-acting intron and exon regions in influenza virus NS1 mRNA that inhibit splicing and cause the formation of aberrantly sedimenting presplicing complexes. Mol Cell Biol 1992;12:962–970.
   PubMedGoogle Scholar
• Fortes P, Beloso A, J. Ortin J. Influenza virus NS1 protein inhibits pre-mRNA splicing and blocks mRNA nucleocytoplasmic transport. EMBO J 1994;13:704–712.
   PubMed Web of Science ®Google Scholar
• Lu Y, Qian XY, Krug RM. The influenza virus NS1 protein: A novel inhibitor of pre-mRNA splicing. Genes Dev 1994;8:1817–1828.
   PubMed Web of Science ®Google Scholar
• Muraki Y, Furukawa T, Kohno Y, Influenza C virus NS1 protein upregulates the splicing of viral mRNAs. J Virol 2010;84:1957–1966.
   Google Scholar
• Garaigorta U, Ortin J. Mutation analysis of a recombinant NS replicon shows that influenza virus NS1 protein blocks the splicing and nucleo-cytoplasmic transport of its own viral mRNA. Nucleic Acids Res 2007;35:4573–4582.
   Google Scholar
• Horvath CM, Williams MA, Lamb RA. Eukaryptic coupled translation of tandem cistrons: Identification of the influenza B virus BM2 polypeptide. EMBO J 1990;9:2639–2647.
   PubMedGoogle Scholar
• Powell ML, Napthine S, Jackson RJ, Characterization of the termination-reinitiation strategy employed in the expression of influenza B virus BM2 protein. RNA 2008;14:2394–2406.
   Google Scholar
• Hatta M, Kohlmeier CK, Hatta Y, Region required for protein expression from the stop-start pentanucleotide in the M gene of influenza B virus. J Virol 2009;83:5939–5942.
   Google Scholar
• Luttermann C, Meyers G. The importance of inter- and intramolecular base pairing for translation reinitiation on a eukaryotic bicistronic mRNA. Genes Dev 2009;23:331–344.
   Google Scholar
• Napthine S, Lever RA, Powell ML, Expression of the VP2 protein of murine norovirus by a translation termination-reinitiation strategy. PLoS One 2009;4:e8390.
   Google Scholar
• Domingo E, Escarmis C, Sevilla N, Basic concepts in RNA virus evolution. FASEB J 1996;10:859–864.
   PubMed Web of Science ®Google Scholar
• Holmes EC. Error thresholds and the constraints to RNA virus evolution. Trends Microbiol 2003;11:543–546.
   PubMed Web of Science ®Google Scholar
• Gog JR, Dos Santos Afonso E, Dalton RM, Codon conservation in the influenza A virus genome defines RNA packaging signals. Nucleic Acids Res 2007;35:1897–1907.
   Google Scholar
• Smith DJ, Lapedes AS, de Jong JC, Mapping the antigenic and genetic evolution of influenza virus. Science 2004;305:371–376.
   PubMed Web of Science ®Google Scholar
• Koelle K, Cobey S, Grenfell B, Pascual M. Epochal evolution shapes the phylodynamics of interpandemic influenza A (H3N2) in humans. Science 2006;314:1898–1903.
   PubMed Web of Science ®Google Scholar
• Wolf YI, Viboud C, Holmes EC, Long intervals of stasis punctuated by bursts of positive selection in the seasonal evolution of influenza A virus. Biol Direct 2006;1:34.
   Google Scholar
• Huynen MA, Stadler PF, Fontana W. Smoothness within ruggedness: The role of neutrality in adaptation. Proc Natl Acad Sci U S A 1996;93:397–401.
   PubMed Web of Science ®Google Scholar
• Fontana W, Schuster P. Continuity in evolution: On the nature of transitions. Science 1998;280:1451–1455.
   PubMed Web of Science ®Google Scholar
• Ilyinskii PO, Schmidt T, Lukashev D, Importance of mRNA secondary structural elements for the expression of influenza virus genes. OMICS 2009;13:421–430.
   Google Scholar
• Ghosh A, Nandy A, Nandy P. Computational analysis and determination of a highly conserved surface exposed segment in H5N1 avian flu and H1N1 swine flu neuraminidase. BMC Struct Biol 2010;10:6.
   Google Scholar
• Beekwilder MJ, Nieuwenhuizen R, van Duin J. Secondary structure model for the last two domains of single-stranded RNA phage Q beta. J Mol Biol 1995;247:903–917.
   PubMedGoogle Scholar
• Enami M, Enami K. Characterization of influenza virus NS1 protein by using a novel helper-virus-free reverse genetic system. J Virol 2000;74:5556–5561.
   PubMedGoogle Scholar
• Pley HW, Flaherty KM, McKay DB. Model for an RNA tertiary interaction from the structure of an intermolecular complex between a GAAA tetraloop and an RNA helix. Nature 1994;372:111–113.
   PubMed Web of Science ®Google Scholar
• Costa M, Michel F. Rules for RNA recognition of GNRA tetraloops deduced by in vitro selection: Comparison with in vivo evolution. EMBO J 1997;16:3289–3302.
   PubMed Web of Science ®Google Scholar
• Geary C, Baudrey S, Jaeger L. Comprehensive features of natural and in vitro selected GNRA tetraloop-binding receptors. Nucleic Acids Res 2008;36:1138–1152.
   PubMed Web of Science ®Google Scholar
• Franch T, Gerdes K. U-turns and regulatory RNAs. Curr Opin Microbiol 2000;3:159–164.
   Google Scholar
• Brunel C, Marquet R, Romby P, Ehresmann C. RNA loop-loop interactions as dynamic functional motifs. Biochimie 2002;84:925–944.
   PubMed Web of Science ®Google Scholar
• Aldaz-Carroll L, Tallet B, Dausse E, Apical loop–internal loop interactions: A new RNA-RNA recognition motif identified through in vitro selection against RNA hairpins of the hepatitis C virus mRNA. Biochemistry 2002;41:5883–5893.
   PubMed Web of Science ®Google Scholar
• Clever JL, Wong ML, Parslow TG. Requirements for kissing-loop-mediated dimerization of human immunodeficiency virus RNA. J Virol 1996;70:5902–5908.
   PubMed Web of Science ®Google Scholar
• De Tapia M, Metzler V, Mougel M, Dimerization of MoMuLV genomic RNA: Redefinition of the role of the palindromic stem-loop H1 (278–303) and new roles for stem-loops H2 (310–352) and H3 (355–374). Biochemistry 1998;37:6077–6085.
   PubMedGoogle Scholar
• Huthoff H, Berkhout B. Multiple secondary structure reaarangements during HIV-1 RNA dimerization. Biochemistry 2002;41:10439–10445.
   PubMed Web of Science ®Google Scholar
• Gherghe C, Leonard CW, Gorelick RJ, Weeks KM. Secondary structure of the mature ex virio Moloney murine leukemia virus genomic RNA dimerization domain. J Virol 2010;84:898–906.
   Google Scholar
• Miyazaki Y, Garcia EL, King SR, An RNA structural switch regulates diploid genome packaging by Moloney murine leukemia virus. J Mol Biol 2010;396:141–152.
   Google Scholar
• Basnayake VR, Sit TL, Lommel SA. The Red clover necrotic mosaic virus origin of assembly is delimited to the RNA-2 trans-activator. Virology 2009;384:169–178.
   Google Scholar
• Kim CH, Tinoco Jr. I. A retroviral RNA kissing complex containing only two G.C base pairs. Proc Natl Acad Sci U S A 2000;97:9396–9401.
   Google Scholar
• Li PTX, Bustamante C, Tinoco Jr. I. Unusual mechanical stability of a minimal RNA kissing complex. Proc Natl Acad Sci U S A 2006;103:15847–15852.
   PubMed Web of Science ®Google Scholar
• Boucard D, Toulmé J-J, Di Primo C. Bimodal loop-loop interactions increase the affinity of RNA aptamers for HIV-1 RNA structures. Biochemistry 2006;45:1518–1524.
   Google Scholar
• Lodmell JS, Ehresmann C, Ehresmann B, Marquet R. Convergence of natural and artificial evolution of an RNA loop-loop interaction: The HIV-1 dimerization initiation site. RNA 2000;6:1267–1276.
   PubMed Web of Science ®Google Scholar
• Ducongé F, Di Primo C, Toulmé JJ. Is a closing “GA pair” a rule for stable loop-loop RNA complexes? J Biol Chem 2000;275:21287–21294.
   PubMed Web of Science ®Google Scholar
• Meulewaeter F, van Lipzig R, Gultyaev AP, Conservation of RNA structures enables TNV and BYDV 5′ and 3′ elements to cooperate synergistically in cap-independent translation. Nucleic Acids Res 2004;32:1721–1730.
   Google Scholar
• Osborne JC, Elliott RM. RNA binding properties of Bunyamwera virus nucleocapsid protein and selective binding to an element in the 5′ terminus of the negative-sense S segment. J Virol 2000;74:9946–9952.
   PubMed Web of Science ®Google Scholar
• Kohl A, Lowen AC, Leonard VHJ, Elliott RM. Genetic elements regulating packaging of the Bunyamwera orthobunyavirus genome. J Gen Virol 2006;87:177–187.
   PubMed Web of Science ®Google Scholar
• Severson WE, Xu X, Jonsson CB. Cis-acting signals in encapsidation of hantaan virus S-segment viral genomic RNA by its N protein. J Virol 2001;75:2646–2652.
   Google Scholar
• Gultyaev AP, van Batenburg FHD, Pleij CWA. The computer simulation of RNA folding pathways using a genetic algorithm. J Mol Biol 1995;250:37–51.
   PubMed Web of Science ®Google Scholar
• Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 2003;31:3406–3415.
   PubMed Web of Science ®Google Scholar
• Gruber AR, Lorenz R, Bernhart SH, The Vienna RNA Websuite. Nucleic Acids Res 2008;36:W70–W74.
   PubMed Web of Science ®Google Scholar
• Jacquenet S, Ropers D, Bilodeau PS, Conserved stem-loop structures in the HIV-1 RNA region containing the A3 3′ splice site and its cis-regulatory element: Possible involvement in RNA splicing. Nucleic Acids Res 2001;29:464–468.
   PubMedGoogle Scholar
• Ryabova LA, Pooggin MM, Hohn T. Translation reinitiation and leaky scanning in plant viruses. Virus Res 2006;119:52–62.
   Google Scholar
• Abbink TEM, Berkhout B. RNA structure modulates splicing efficiency at the human immunodeficiency virus type 1 major splice donor. J Virol 2008;82:3090–3098.
   Google Scholar
• Plant EP, Rakauskaite R, Taylor DR, Dinman JD. Achieving a golden mean: Mechanisms by which coronaviruses ensure synthesis of the correct stoichiometric ratios of viral proteins. J Virol 2010;84:4330–4340.
   PubMed Web of Science ®Google Scholar
• Shih S-R, Krug RM. Novel exploitation of a nuclear function by influenza virus: the cellular SF2/ASF splicing factor controls the amount of the essential viral M2 ion channel protein in infected cells. EMBO J 1996;15:5415–5427.
   PubMedGoogle Scholar
• Buratti E, Muro AF, Giombi M, RNA folding affects the recruitment of SR proteins by mouse and human polypurinic enhancer elements in the fibronectin EDA exon. Mol Cell Biol 2004;24:1387–1400.
   PubMed Web of Science ®Google Scholar
• Karlas A, Machuy N, Shin Y, Genome-wide RNAi screen identifies human host factors crucial for influenza virus replication. Nature 2010;463:818–822.
   PubMed Web of Science ®Google Scholar
• Chen W, Calvo PA, Malide D, A novel influenza A virus mitochondrial protein that induces cell death. Nature Med 2001;7:1306–1312.
   PubMed Web of Science ®Google Scholar
• Wise HM, Foeglein A, Sun J, A complicated message: Identification of a novel PB1-related protein translated from influenza A virus segment 2 mRNA. J Virol 2009;83:8021–8031.
   PubMed Web of Science ®Google Scholar
• Zamarin D, Ortigoza MB, Palese P. Influenza A virus PB1-F2 protein contributes to viral pathogenesis. J Virol 2006;80:7976–7983.
   PubMed Web of Science ®Google Scholar
• Amorim MJ, Read EK, Dalton RM, Nuclear export of influenza A virus mRNAs requires ongoing RNA polymeraze II activity. Traffic 2007;8:1–11.
   PubMed Web of Science ®Google Scholar
• Wang W, Cui ZQ, Han H, Imaging and characterizing influenza A virus mRNA transport in living cells. Nucleic Acids Res 2008;36:4913–4928.
   Google Scholar
• Schneider J, Wolff T. Nuclear functions of the influenza A and B viruses NS proteins: Do they play a role in viral mRNA export? Vaccine 2009;27:6312–6316.
   PubMedGoogle Scholar
• Read EKC, Digard P. Individual influenza A virus mRNAs show differential dependence on cellular NXF1/TAP for their nuclear export. J Gen Virol 2010;91:1290–1301.
   Google Scholar
• Ludwig S, Schultz U, Mandler J, Phylogenetic relationship of the nonstructural (NS) genes of influenza A viruses. Virology 1991;183:566–577.
   PubMedGoogle Scholar