1,731
Views
1
CrossRef citations to date
0
Altmetric
Research Paper

Insights into the secondary and tertiary structure of the Bovine Viral Diarrhea Virus Internal Ribosome Entry Site

, , , ORCID Icon, , ORCID Icon & ORCID Icon show all
Pages 496-506 | Received 22 Nov 2021, Accepted 23 Mar 2022, Published online: 05 Apr 2022

References

  • Khodakaram-Tafti A, Farjanikish GH. Persistent bovine viral diarrhea virus (BVDV) infection in cattle herds. Iran J Vet Res. 2017;18:154–163.
  • Simmonds P, Becher P, Bukh J, et al. ICTV virus taxonomy profile: flaviviridae. J Gen Virol. 2017;98:2–3.
  • Houe H. Epidemiological features and economical importance of bovine virus diarrhoea virus (BVDV) infections. Vet Microbiol. 1999;64:89–107.
  • Vilček Š, Paton DJ, Durkovic B, et al. Bovine viral diarrhoea virus genotype 1 can be separated into at least eleven genetic groups. Arch Virol. 2001;146:99–115.
  • Burks JM, Zwieb C, Müller F, et al. Comparative structural studies of bovine viral diarrhea virus IRES RNA. Virus Res. 2011;160:136–142.
  • Eterhans EP, Achofen CB, Talder HS, et al. Cytopathic bovine viral diarrhea viruses (BVDV): emerging pestiviruses doomed to extinction. Vet Res. 2010;41:44.
  • Tsukiyama-Kohara K, Iizuka N, Kohara M, et al. Internal ribosome entry site within hepatitis C virus RNA. J Virol. 1992;66:1476–1483.
  • Rijnbrand R, Bredenbeek P, van der Straaten T, et al. Almost the entire 5′ non-translated region of hepatitis C virus is required for cap-independent translation. FEBS Lett. 1995;365:115–119.
  • Wilson JE, Powell MJ, Hoover SE, et al. Naturally occurring dicistronic cricket Paralysis virus RNA is regulated by two Internal Ribosome Entry Sites. Mol Cell Biol. 2000;20:4990–4999.
  • Kühn R, Luz N, Beck E. Functional analysis of the internal translation initiation site of foot-and-mouth disease virus. J Virol. 1990;64:4625–4631.
  • Pelletier J, Sonenberg N. Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature. 1988;334:320–325.
  • Thakor N, Holcik M. IRES-mediated translation of cellular messenger RNA operates in eIF2 a -independent manner during stress. Nucleic Acids Res. 2011;40:541–552.
  • Martinez-salas E, Francisco-Velilla R, Fernandez-Chamorro J. Insights into structural and mechanistic features of viral IRES elements. Front Microbiol. 2018;8:1–15.
  • Burks JM, Zwieb C, Müller F, et al. In silico analysis of IRES RNAs of foot-and-mouth disease virus and related picornaviruses. Arch Virol. 2011;156:1737–1747.
  • Komar AA, Hatzoglou M. Exploring internal ribosome entry sites as therapeutic targets. Front Oncol. 2015;5:1–10.
  • Ghassemi F, Madadgar O, Roohvand F, et al. Translational efficiency of BVDV IRES and EMCV IRES for T7 RNA polymerase driven cytoplasmic expression in mammalian cell lines. Mol Biol. 2017;51:324–333.
  • Yu Y, Abaeva IS, Marintchev A, et al. Common conformational changes induced in type 2 picornavirus IRESs by cognate trans-acting factors. Nucleic Acids Res. 2011;39:4851–4865.
  • Yamamoto H, Collier M, Loerke J, et al. Molecular architecture of the ribosome‐bound hepatitis C virus internal ribosomal entry site RNA. EMBO J. 2015;34:3042–3058.
  • Lukavsky PJ. Structure and function of HCV IRES domains. Virus Res. 2009;139:166–171.
  • Shen LX, Tinoco I. The structure of an RNA pseudoknot that causes efficient frameshifting in mouse mammary tumor virus. J Mol Biol. 1995;247:963–978.
  • Brierley I, Pennell S, Gilbert RJC. Viral RNA pseudoknots: versatile motifs in gene expression and replication. Nat Rev Microbiol. 2007;5:598–610.
  • Moes L, Wirth M. The internal initiation of translation in bovine viral diarrhea virus RNA depends on the presence of an RNA pseudoknot upstream of the initiation codon. Virol J. 2007;4:124.
  • Pestova TV, Hellen CUT. Internal initiation of translation of bovine viral diarrhea virus rna. Virology. 1999;258:249–256.
  • Fukushi S, Okada M, Stahl J, et al. Ribosomal protein S5 interacts with the internal ribosomal entry site of hepatitis C virus. J Biol Chem. 2001;276:20824–20826.
  • Otto GA, Lukavsky PJ, Lancaster AM, et al. Ribosomal proteins mediate the hepatitis C virus IRES-HeLa 40S interaction. RNA. 2002;8:913–923.
  • Laletina E, Graifer D, Malygin A, et al. Proteins surrounding hairpin IIIe of the hepatitis C virus internal ribosome entry site on the human 40S ribosomal subunit. Nucleic Acids Res. 2006;34:2027–2036.
  • Babaylova E, Graifer D, Malygin A, et al. Positioning of subdomain IIId and apical loop of domain II of the hepatitis C IRES on the human 40S ribosome. Nucleic Acids Res. 2009;37:1141–1151.
  • Smola MJ, Calabrese JM, Weeks KM. Detection of RNA-protein interactions in living cells with SHAPE. Biochemistry. 2015;54:6867–6875.
  • Smola MJ, Rice GM, Busan S, et al. Selective 2’-hydroxyl acylation analyzed by primer extension and mutational profiling (SHAPE-MaP) for direct, versatile and accurate RNA structure analysis. Nat Protoc. 2015;10:1643–1669.
  • Le SY, Siddiqui A, Maizel JV. A common structural core in the internal ribosome entry sites of picornavirus, hepatitis C virus, and pestivirus. Virus Genes. 1996;12:135–147.
  • Le SY, Sonenberg N, Maizel JV. Unusual folding regions and ribosome landing pad within hepatitis C virus and pestivirus RNAs. Gene. 1995;154:137–143.
  • Kerpedjiev P, Höner Zu Siederdissen C, Hofacker IL. Predicting RNA 3D structure using a coarse-grain helix-centered model. RNA. 2015;21:1110–1121.
  • Boniecki MJ, Lach G, Dawson WK, et al. SimRNA: a coarse-grained method for RNA folding simulations and 3D structure prediction. Nucleic Acids Res. 2015;44:1–20.
  • Mortimer SA, Weeks KM. A fast-acting reagent for accurate analysis of RNA secondary and tertiary structure by SHAPE chemistry. J Am Chem Soc. 2007;129:4144–4145.
  • Sztuba-Solinska J, Rausch JW, Smith R, et al. Kaposi’s sarcoma-associated herpesvirus polyadenylated nuclear RNA: a structural scaffold for nuclear, cytoplasmic and viral proteins. Nucleic Acids Res. 2017;45:6805–6821.
  • Siegfried NA, Busan S, Rice GM, et al. RNA motif discovery by SHAPE and mutational profiling (SHAPE-MaP). Nat Methods. 2014;11:959–965.
  • Ghassemi F, Madadgar O, Roohvand F, et al. Translational efficiency of BVDV IRES and EMCV IRES for T7 RNA polymerase driven cytoplasmic expression in mammalian cell lines. Mol Biol. 2017;51:283–292.
  • Ghaderi M, Sabahi F, Sadeghi-Zadeh M, et al. Construction of an eGFP expression plasmid under control of T7 promoter and IRES sequence for assay of T7 RNA polymerase activity in mammalian cell lines. Iran J Cancer Prev. 2014;7:137–141.
  • Mendez E, Ruggli N, Collett MS, et al. Infectious Bovine viral Diarrhea virus (Strain NADL) RNA from stable cDNA clones: a cellular insert determines ns3 production and viral cytopathogenicity. J Virol. 1998;72:4737–4745.
  • Hurst T, Xu X, Zhao P, et al. Quantitative understanding of SHAPE mechanism from RNA structure and dynamics analysis. J Phys Chem B. 2018;122:4771–4783.
  • Stallings SC, Moore PB. The structure of an essential splicing element: stem loop IIa from yeast U2 snRNA. Structure. 1997;5:1173–1185.
  • Moore PB. Structural motifs in RNA. Annu Rev Biochem. 1999;68:287–300.
  • Proctor DJ, Schaak JE, Bevilacqua JM, et al. Isolation and characterization of a family of stable RNA tetraloops with the motif YNMG that participate in tertiary interactions. Biochemistry. 2002;41:12062–12075.
  • Paoletti AC, Shubsda MF, Hudson BS, et al. Affinities of the nucleocapsid protein for variants of SL3 RNA in HIV-1. Biochemistry. 2002;41:15423–15428.
  • Wilkinson KA, Vasa SM, Deigan KE, et al. Influence of nucleotide identity on ribose 2′-hydroxyl reactivity in RNA. RNA. 2009;15:1314–1321.
  • Mlýnský V, Bussi G. Molecular dynamics simulations reveal an interplay between SHAPE reagent binding and RNA flexibility. J Phys Chem Lett. 2018;9:313–318.
  • McGinnis JL, Dunkle JA, Cate JHD, et al. The mechanisms of RNA SHAPE chemistry. J Am Chem Soc. 2012;134:6617–6624.
  • Vicens Q, Gooding AR, Laederach A, et al. Local RNA structural changes induced by crystallization are revealed by SHAPE. RNA. 2007;13:536–548.
  • Deigan KE, Li TW, Mathews DH, et al. Accurate SHAPE-directed RNA structure determination. Proc Natl Acad Sci. U S A. 2009;106:97–102.
  • Huynen M, Gutell R, Konings D. Assessing the reliability of RNA folding using statistical mechanics. J Mol Biol. 1997;267:1104–1112.
  • Huber RG, Lim XN, Ng WC, et al. Structure mapping of dengue and Zika viruses reveals functional long-range interactions. Nat Commun. 2019;10:1408.
  • Mauger DM, Golden M, Yamane D, et al. Functionally conserved architecture of hepatitis C virus RNA genomes. Proc Natl Acad Sci U S A. 2015;112:3692–3697.
  • Deng R, Brock KV. 5′ and 3′ untranslated regions of pestivirus genome: primary and secondary structure analyses. Nucleic Acids Res. 1993;21:1949–1957.
  • Thiel BC, Beckmann IK, Kerpedjiev P, et al. 3D based on 2D: calculating helix angles and stacking patterns using forgi 2.0, an RNA Python library centered on secondary structure elements. F1000Res. 2019;8:1–16.
  • Holland JA, Hansen MR, Du Z, et al. An examination of coaxial stacking of helical stems in a pseudoknot motif: the gene 32 messenger RNA pseudoknot of bacteriophage T2. RNA. 1999;5:257–271.
  • Dumas P, Moras D, Florentz C, et al. 3-d graphics modelling of the tRNA-like 3’-end of turnip yellow mosaic virus RNA: structural and functional implications. J Biomol Struct Dyn. 1987;4:707–728.
  • Sung D, Kang H. Mutational analysis of the RNA pseudoknot involved in efficient ribosomal frameshifting in simian retrovirus-1. Nucleic Acids Res. 1998;26:1369–1372.
  • Fletcher SP, Jackson RJ. Pestivirus Internal Ribosome Entry Site (IRES) structure and function: elements in the 5′ untranslated region important for IRES function. J Virol. 2002;76:5024–5033.
  • Wang C, Le SY, Ali N, et al. An RNA pseudoknot is an essential structural element of the internal ribosome entry site located within the hepatitis C virus 5′ noncoding region. RNA. 1995;1:526–537.
  • Spahn CMT, Kieft JS, Grassucci RA, et al. Hepatitis C virus IRES RNA-induced changes in the conformation of the 40S ribosomal subunit. Science. 2001;291:1959–1962.
  • Grassmann CW, Yu H, Isken O, et al. Hepatitis C virus and the related bovine viral diarrhea virus considerably differ in the functional organization of the 5′ non-translated region: implications for the viral life cycle. Virology. 2005;333(2):349–366.
  • Lemon SM, Honda M. Internal ribosome entry sites within the RNA genomes of hepatitis C virus and other flaviviruses. Semin Virol. 1997;8:274–288.
  • Berry KE, Waghray S, Doudna JA. The HCV IRES pseudoknot positions the initiation codon on the 40S ribosomal subunit. RNA. 2010;16(8):1559–1569.
  • Berry KE, Waghray S, Mortimer SA, et al. Crystal structure of the HCV IRES central domain reveals strategy for start-codon positioning. Structure. 2011;19(10):1456–1466.
  • Pawlotsky JM, Chevaliez S, McHutchison JG. The hepatitis C virus life cycle as a target for new antiviral therapies. Gastroenterology. 2007;132(5):1979–1998.
  • Busan S, Weeks KM. Accurate detection of chemical modifications in RNA by mutational profiling (MaP) with ShapeMapper 2. RNA. 2018;24(2):143–148.
  • Bellaousov S, Reuter JS, Seetin MG, et al. RNAstructure: web servers for RNA secondary structure prediction and analysis. Nucleic Acids Res. 2013;41(W1):W471–W474.
  • Tsybulskyi V, Mounir M, Meyer IM. R-chie: a web server and R package for visualizing cis and trans RNA–RNA, RNA–DNA and DNA–DNA interactions. Nucleic Acids Res. 2020;48(18):E105–E105.
  • Nawrocki EP, Eddy SR. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics. 2013;29(22):2933–2935.
  • Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772–780.
  • Bernhart SH, Hofacker IL, Will S, et al. RNAalifold: improved consensus structure prediction for RNA alignments. In: BMC bioinformatics. BioMed Central Ltd. 2008. p. 9.
  • Lorenz R, Bernhart SH, Höner Zu Siederdissen C, et al. ViennaRNA package 2.0. Algorithms Mol Biol. 2011;6(1). DOI:10.1186/1748-7188-6-26
  • Rivas E, Clements J, Eddy SR. A statistical test for conserved RNA structure shows lack of evidence for structure in lncRNAs. Nat Methods. 2017;14(1):45–48.
  • Janssen S, Giegerich R. The RNA shapes studio. Bioinformatics. 2015;31(3):423–425.
  • Yuan S, Chan HCS, Hu Z. Using PyMOL as a platform for computational drug design. Wiley Interdiscip Rev Comput Mol Sci. 2017;7(2):1–17.