Conserved RNA secondary structures and long-range interactions in hepatitis C viruses

RNA

Volumn 21, Issue 7, 2015, Pages 1219-1232

  Fricke, Markus ^a   Dünnes, Nadia ^b   Zayas, Margarita ^c   Bartenschlager, Ralf ^c   Niepmann, Michael ^b   Marz, Manja ^a,d  

^a FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^b JUSTUS LIEBIG UNIVERSITY GIESSEN   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d FRITZ LIPMANN INSTITUTE   (Germany)

Author keywords

Bioinformatics; Circularization; HCV; RNA long range interaction prediction; RNA secondary structure prediction

Indexed keywords

DIMER; INITIATION FACTOR 3; MICRORNA 122; RNA; RNA DIRECTED RNA POLYMERASE; VIRUS RNA; 3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; BASE PAIRING; BINDING SITE; CYCLIZATION; GENOTYPE; HEPACIVIRUS; INTERACTIONS WITH RNA; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PRIORITY JOURNAL; PROTEIN SECONDARY STRUCTURE; RIBOSOME SUBUNIT; RNA CONFORMATION; RNA REPLICATION; RNA SYNTHESIS; START CODON; STOP CODON; TERMINAL SEQUENCE; VIRUS REPLICATION; CHEMISTRY; CONFORMATION; GENETICS; MOLECULAR GENETICS; PHYSIOLOGY;

HEPACIVIRUS; HEPATITIS C VIRUS;

3' UNTRANSLATED REGIONS; 5' UNTRANSLATED REGIONS; BASE SEQUENCE; HEPACIVIRUS; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; RNA, VIRAL; VIRUS REPLICATION;

EID: 84931026734     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.049338.114     Document Type: Article

References (100)

1. Alvarez DE, Lodeiro MF, Ludueña SJ, Pietrasanta LI, Gamarnik AV. 2005. Long-range RNA-RNA interactions circularize the dengue virus genome. J Virol 79: 6631-6643.
2. Alvarez DE, Filomatori CV, Gamarnik AV. 2008. Functional analysis of dengue virus cyclization sequences located at the 5' and 3' UTRs. Virology 375: 223-235.
3. Anandam P, Torarinsson E, Ruzzo WL. 2009. Multiperm: shuffling multiple sequence alignments while approximately preserving dinucleotide frequencies. Bioinformatics 25: 668-669.
4. Ariumi Y, Kuroki M, Abe K, Dansako H, Ikeda M, Wakita T, Kato N. 2007. DDX3 DEAD-box RNA helicase is required for hepatitis C virus RNA replication. J Virol 81: 13922-13926.
5. Astier-Gin T, Bellecave P, Litvak S, Ventura M. 2005. Template requirements and binding of hepatitis C virus NS5B polymerase during in vitro RNA synthesis from the 3'-end of virus minus-strand RNA. FEBS J 272: 3872-3886.
6. Bai Y, Zhou K, Doudna JA. 2013. Hepatitis C virus 3' UTR regulates viral translation through direct interactions with the host translation machinery. Nucleic Acids Res 41: 7861-7874.
7. Bauer M, Klau GW, Reinert K. 2007. Accurate multiple sequence-structure alignment of RNA sequences using combinatorial optimization. BMC Bioinformatics 8: 271.
8. Beerens N, Kjems J. 2010. Circularization of the HIV-1 genome facilitates strand transfer during reverse transcription. RNA 16: 1226-1235.
9. Beguiristain N, Robertson HD, Gómez J. 2005. RNase III cleavage demonstrates a long range RNA: RNA duplex element flanking the hepatitis C virus internal ribosome entry site. Nucleic Acids Res 33: 5250-5261.
10. Berry KE, Waghray S, Mortimer SA, Bai Y, Doudna JA. 2011. Crystal structure of the HCV IRES central domain reveals strategy for start-codon positioning. Structure 19: 1456-1466.
11. Blight KJ, Rice CM. 1997. Secondary structure determination of the conserved 98-base sequence at the 3' terminus of hepatitis C virus genome RNA. J Virol 71: 7345-7352.
12. Boehringer D, Thermann R, Ostareck-Lederer A, Lewis JD, Stark H. 2005. Structure of the hepatitis C virus IRES bound to the human 80S ribosome: remodeling of the HCV IRES. Structure 13: 1695-1706.
13. Brown EA, Zhang H, Ping LH, Lemon SM. 1992. Secondary structure of the 5' nontranslated regions of hepatitis C virus and pestivirus genomic RNAs. Nucleic Acids Res 20: 5041-5045.
14. Buratti E, Tisminetzky S, Zotti M, Baralle FE. 1998. Functional analysis of the interaction between HCV 5' UTR and putative subunits of eukaryotic translation initiation factor eIF3. Nucleic Acids Res 26: 3179-3187.
15. Corver J, Lenches E, Smith K, Robison RA, Sando T, Strauss EG, Strauss JH. 2003. Fine mapping of a cis-acting sequence element in yellow fever virus RNA that is required for RNA replication and cyclization. J Virol 77: 2265-2270.
16. Díaz-Toledano R, Ariza-Mateos A, Birk A, Martínez-García B, Gómez J. 2009. In vitro characterization of a miR-122-sensitive double-helical switch element in the 5' region of hepatitis C virus RNA. Nucleic Acids Res 37: 5498-5510.
17. Diviney S, Tuplin A, Struthers M, Armstrong V, Elliott RM, Simmonds P, Evans DJ. 2008. A hepatitis C virus cis-acting replication element forms a long-range RNA-RNA interaction with upstream RNA sequences in NS5B. J Virol 82: 9008-9022.
18. Dutkiewicz M, Swiatkowska A, Figlerowicz M, Ciesiołka J. 2008. Structural domains of the 3'-terminal sequence of the hepatitis C virus replicative strand. Biochemistry 47: 12197-12207.
19. Edgil D, Harris E. 2006. End-to-end communication in the modulation of translation by mammalian RNA viruses. Virus Res 119: 43-51.
20. Filbin ME, Kieft JS. 2011. HCV IRES domain IIb affects the configuration of coding RNA in the 40S subunit's decoding groove. RNA 17: 1258-1273.
21. Fraser CS, Doudna JA. 2007. Structural and mechanistic insights into hepatitis C viral translation initiation. Nat Rev Microbiol 5: 29-38.
22. Friebe P, Bartenschlager R. 2002. Genetic analysis of sequences in the 3' nontranslated region of hepatitis C virus that are important for RNA replication. J Virol 76: 5326-5338.
23. Friebe P, Bartenschlager R. 2009. Role of RNA structures in genome terminal sequences of the hepatitis C virus for replication and assembly. J Virol 83: 11989-11995.
24. Friebe P, Lohmann V, Krieger N, Bartenschlager R. 2001. Sequences in the 5' nontranslated region of hepatitis C virus required for RNA replication. J Virol 75: 12047-12057.
25. Friebe P, Boudet J, Simorre JP, Bartenschlager R. 2005. Kissing-loop interaction in the 3' end of the hepatitis C virus genome essential for RNA replication. J Virol 79: 380-392.
26. Friebe P, Shi PY, Harris E. 2011. The 5' and 3' downstream AUG region elements are required for mosquito-borne flavivirus RNA replication. J Virol 85: 1900-1905.
27. Goergen D, Niepmann M. 2012. Stimulation of Hepatitis C Virus RNA translation by microRNA-122 occurs under different conditions in vivo and in vitro. Virus Res 167: 343-352.
28. Hajdin CE, Bellaousov S, Huggins W, Leonard CW, Mathews DH, Weeks KM. 2013. Accurate SHAPE-directed RNA secondary structure modeling, including pseudoknots. Proc Natl Acad Sci 110: 5498-5503.
29. Harris D, Zhang Z, Chaubey B, Pandey VN. 2006. Identification of cellular factors associated with the 3'-nontranslated region of the hepatitis C virus genome. Mol Cell Proteomics 5: 1006-1018.
30. Henke JI, Goergen D, Zheng J, Song Y, Schüttler CG, Fehr C, Jünemann C, Niepmann M. 2008. microRNA-122 stimulates translation of hepatitis C virus RNA. EMBO J 27: 3300-3310.
31. Herold J, Andino R. 2001. Poliovirus RNA replication requires genome circularization through a protein-protein bridge. Mol Cell 7: 581-591.
32. Honda M, Brown EA, Lemon SM. 1996. 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.
33. Honda M, Beard MR, Ping LH, Lemon SM. 1999a. A phylogenetically conserved stem-loop structure at the 5' border of the internal ribosome entry site of hepatitis C virus is required for cap-independent viral translation. J Virol 73: 1165-1174.
34. Honda M, Rijnbrand R, Abell G, Kim D, Lemon SM. 1999b. 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.
35. Isken O, Baroth M, Grassmann CW, Weinlich S, Ostareck DH, Ostareck-Lederer A, Behrens SE. 2007. Nuclear factors are involved in hepatitis C virus RNA replication. RNA 13: 1675-1692.
36. Ito T, Lai MM. 1997. Determination of the secondary structure of and cellular protein binding to the 3' -untranslated region of the hepatitis C virus RNA genome. J Virol 71: 8698-8706.
37. Ivanyi-Nagy R, Kanevsky I, Gabus C, Lavergne JP, Ficheux D, Penin F, Fossé P, Darlix JL. 2006. Analysis of hepatitis C virus RNA dimerization and core-RNA interactions. Nucleic Acids Res 34: 2618-2633.
38. Jackowiak P, Kuls K, Budzko L, Mania A, Figlerowicz M, Figlerowicz M. 2014. Phylogeny and molecular evolution of the hepatitis C virus. Infect Genet Evol 21: 67-82.
39. Jangra RK, Yi M, Lemon SM. 2010. DDX6 (Rck/p54) is required for efficient hepatitis C virus replication but not for internal ribosome entry site-directed translation. J Virol 84: 6810-6824.
40. Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P. 2005. Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science 309: 1577-1581.
41. Katoh K, Misawa K, Kuma K, Miyata T. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30: 3059-3066.
42. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, et al. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28: 1647-1649.
43. Kieft JS, Zhou K, Jubin R, Doudna JA. 2001. Mechanism of ribosome recruitment by hepatitis C IRES RNA. RNA 7: 194-206.
44. Kieft JS, Zhou K, Grech A, Jubin R, Doudna JA. 2002. Crystal structure of an RNA tertiary domain essential to HCV IRES-mediated translation initiation. Nat Struct Biol 9: 370-374.
45. Kim YK, Lee SH, Kim CS, Seol SK, Jang SK. 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.
46. Kolupaeva VG, Pestova TV, Hellen CU. 2000. An enzymatic footprinting analysis of the interaction of 40S ribosomal subunits with the internal ribosomal entry site of hepatitis C virus. J Virol 74: 6242-6250.
47. Kolykhalov AA, Feinstone SM, Rice CM. 1996. Identification of a highly conserved sequence element at the 3' terminus of hepatitis C virus genome RNA. J Virol 70: 3363-3371.
48. Kuiken C, Yusim K, Boykin L, Richardson R. 2005. The Los Alamos hepatitis C sequence database. Bioinformatics 21: 379-384.
49. Lee H, Shin H, Wimmer E, Paul AV. 2004. cis-acting RNA signals in the NS5B C-terminal coding sequence of the hepatitis C virus genome. J Virol 78: 10865-10877.
50. Liu Y, Wimmer E, Paul AV. 2009. Cis-acting RNA elements in human and animal plus-strand RNA viruses. Biochim Biophys Acta 1789: 495-517.
51. Lohmann V. 2013. Hepatitis C virus RNA replication, Vol. 369 of Current topics in microbiology and immunology. Springer, Berlin, Heidelberg.
52. Lorenz R, Bernhart SH, Höner zu Siederdissen C, Tafer H, Flamm C, Stadler PF, Hofacker IL. 2011. ViennaRNA Package 2.0. Algorithms Mol Biol 6: 26.
53. Lu H, Li W, Noble WS, Payan D, Anderson DC. 2004. Riboproteomics of the hepatitis C virus internal ribosomal entry site. J Proteome Res 3: 949-957.
54. Lukavsky PJ, Otto GA, Lancaster AM, Sarnow P, Puglisi JD. 2000. Structures of two RNA domains essential for hepatitis C virus internal ribosome entry site function. Nat Struct Biol 7: 1105-1110.
55. Lukavsky PJ, Kim I, Otto GA, Puglisi JD. 2003. Structure of HCV IRES domain II determined by NMR. Nat Struct Biol 10: 1033-1038.
56. Mahias K, Ahmed-El-Sayed N, Masante C, Bitard J, Staedel C, Darfeuille F, Ventura M, Astier-Gin T. 2010. Identification of a structural element of the hepatitis C virus minus strand RNA involved in the initiation of RNA synthesis. Nucleic Acids Res 38: 4079-4091.
57. Masante C, Mahias K, Lourenço S, Dumas E, Cahour A, Trimoulet P, Fleury H, Astier-Gin T, Ventura M. 2008. Seven nucleotide changes characteristic of the hepatitis C virus genotype 3 5' untranslated region: correlation with reduced in vitro replication. J Gen Virol 89: 212-221.
58. McMullan LK, Grakoui A, Evans MJ, Mihalik K, Puig M, Branch AD, Feinstone SM, Rice CM. 2007. Evidence for a functional RNA element in the hepatitis C virus core gene. Proc Natl Acad Sci 104: 2879-2884.
59. Moradpour D, Penin F. 2013. Hepatitis C virus proteins: from structure to function. Curr Top Microbiol Immunol 369: 113-142.
60. Narberhaus F. 2010. Translational control of bacterial heat shock and virulence genes by temperature-sensing mRNAs. RNA Biol 7: 84-89.
61. Nasheri N, Singaravelu R, Goodmurphy M, Lyn RK, Pezacki JP. 2011. Competing roles of microRNA-122 recognition elements in hepatitis C virus RNA. Virology 410: 336-344.
62. Niepmann M. 2013. Hepatitis C virus RNA translation. Curr Top Microbiol Immunol 369: 143-166.
63. Odreman-Macchioli FE, Tisminetzky SG, Zotti M, Baralle FE, Buratti E. 2000. Influence of correct secondary and tertiary RNA folding on the binding of cellular factors to the HCV IRES. Nucleic Acids Res 28: 875-885.
64. Ooms M, Abbink TE, Pham C, Berkhout B. 2007. Circularization of the HIV-1 RNA genome. Nucleic Acids Res 35: 5253-5261.
65. Pang PS, Elazar M, Pham EA, Glenn JS. 2011. Simplified RNA secondary structure mapping by automation of SHAPE data analysis. Nucleic Acids Res 39: e151.
66. Pérard J, Leyrat C, Baudin F, Drouet E, Jamin M. 2013. Structure of the full-length HCV IRES in solution. Nat Commun 4: 1612.
67. Pestova TV, Shatsky IN, Fletcher SP, Jackson RJ, Hellen CU. 1998. A prokaryotic-like mode of cytoplasmic eukaryotic ribosome binding to the initiation codon during internal translation initiation of hepatitis C and classical swine fever virus RNAs. Genes Dev 12: 67-83.
68. Romero-López C, Berzal-Herranz A. 2009. A long-range RNA-RNA interaction between the 5' and 3' ends of the HCV genome. RNA 15: 1740-1752.
69. Romero-López C, Berzal-Herranz A. 2012. The functional RNA domain 5BSL3.2 within the NS5B coding sequence influences hepatitis C virus IRES-mediated translation. Cell Mol Life Sci 69: 103-113.
70. Romero-López C, Barroso-Deljesus A, García-Sacristán A, Briones C, Berzal-Herranz A. 2014. End-to-end crosstalk within the hepatitis C virus genome mediates the conformational switch of the 3' X-tail region. Nucleic Acids Res 42: 567-582.
71. Sato K, Kato Y, Akutsu T, Asai K, Sakakibara Y. 2012. DAFS: simultaneous aligning and folding of RNA sequences via dual decomposition. Bioinformatics 28: 3218-3224.
72. Schuster C, Isel C, Imbert I, Ehresmann C, Marquet R, Kieny MP. 2002. Secondary structure of the 3' terminus of hepatitis C virus minusstrand RNA. J Virol 76: 8058-8068.
73. Sedano CD, Sarnow P. 2014. Hepatitis C virus subverts liver-specific miR-122 to protect the viral genome from exoribonuclease Xrn2. Cell Host Microbe 16: 257-264.
74. Seemann SE, Richter AS, Gesell T, Backofen R, Gorodkin J. 2011. PETcofold: predicting conserved interactions and structures of two multiple alignments of RNA sequences. Bioinformatics 27: 211-219.
75. Shetty S, Kim S, Shimakami T, Lemon SM, Mihailescu MR. 2010. Hepatitis C virus genomic RNA dimerization is mediated via a kissing complex intermediate. RNA 16: 913-925.
76. Shimakami T, Yamane D, Jangra RK, Kempf BJ, Spaniel C, Barton DJ, Lemon SM. 2012. Stabilization of hepatitis C virus RNA by an Ago2- miR-122 complex. Proc Natl Acad Sci 109: 941-946.
77. Simmonds P. 2013. The origin of hepatitis C virus. Curr Top Microbiol Immunol 369: 1-15.
78. Siridechadilok B, Fraser CS, Hall RJ, Doudna JA, Nogales E. 2005. Structural roles for human translation factor eIF3 in initiation of protein synthesis. Science 310: 1513-1515.
79. Sizova DV, Kolupaeva VG, Pestova TV, Shatsky IN, Hellen CU. 1998. Specific interaction of eukaryotic translation initiation factor 3 with the 5' nontranslated regions of hepatitis C virus and classical swine fever virus RNAs. J Virol 72: 4775-4782.
80. Smith RM, Wu GY. 2004. Secondary structure and hybridization accessibility of the hepatitis C virus negative strand RNA 5' -terminus. J Viral Hepat 11: 115-123.
81. Smith RM, Walton CM, Wu CH, Wu GY. 2002. Secondary structure and hybridization accessibility of hepatitis C virus 3'-terminal sequences. J Virol 76: 9563-9574.
82. Song Y, Friebe P, Tzima E, Jünemann C, Bartenschlager R, Niepmann M. 2006. The hepatitis C virus RNA 3'-untranslated region strongly enhances translation directed by the internal ribosome entry site. J Virol 80: 11579-11588.
83. Spahn CM, Kieft JS, Grassucci RA, Penczek PA, Zhou K, Doudna JA, Frank J. 2001. Hepatitis C virus IRES RNA-induced changes in the conformation of the 40s ribosomal subunit. Science 291: 1959-1962.
84. Tamura K, Nei M. 1993. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10: 512-526.
85. Tanaka T, Kato N, Cho MJ, Shimotohno K. 1995. A novel sequence found at the 3' terminus of hepatitis C virus genome. Biochem Biophys Res Commun 215: 744-749.
86. Tuplin A, Wood J, Evans DJ, Patel AH, Simmonds P. 2002. Thermodynamic and phylogenetic prediction of RNA secondary structures in the coding region of hepatitis C virus. RNA 8: 824-841.
87. Tuplin A, Struthers M, Simmonds P, Evans DJ. 2012. A twist in the tail: SHAPE mapping of long-range interactions and structural rearrangements of RNA elements involved in HCV replication. Nucleic Acids Res 40: 6908-6921.
88. Vassilaki N, Friebe P, Meuleman P, Kallis S, Kaul A, Paranhos-Baccalà G, Leroux-Roels G, Mavromara P, Bartenschlager R. 2008. Role of the hepatitis C virus core+1 open reading frame and core cis-acting RNA elements in viral RNA translation and replication. J Virol 82: 11503-11515.
89. Wang C, Le SY, 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.
90. Wang TH, Rijnbrand RC, Lemon SM. 2000. Core protein-coding sequence, but not core protein, modulates the efficiency of cap-independent translation directed by the internal ribosome entry site of hepatitis C virus. J Virol 74: 11347-11358.
91. Will S, Joshi T, Hofacker IL, Stadler PF, Backofen R. 2012. LocARNA-P: accurate boundary prediction and improved detection of structural RNAs. RNA 18: 900-914.
92. Yamamoto H, Unbehaun A, Loerke J, Behrmann E, Collier M, Bürger J, Mielke T, Spahn CM. 2014. Structure of the mammalian 80S initiation complex with initiation factor 5B on HCV-IRES RNA. Nat Struct Mol Biol 21: 721-727.
93. Yamane D, McGivern DR, Masaki T, Lemon SM. 2013. Liver injury and disease pathogenesis in chronic hepatitis C. Curr Top Microbiol Immunol 369: 263-288.
94. Yanagi M, St Claire M, Emerson SU, Purcell RH, Bukh J. 1999. In vivo analysis of the 3' untranslated region of the hepatitis C virus after in vitro mutagenesis of an infectious cDNA clone. Proc Natl Acad Sci 96: 2291-2295.
95. Yi M, Lemon SM. 2003. 3' Nontranslated RNA signals required for replication of hepatitis C virus RNA. J Virol 77: 3557-3568.
96. You S, Rice CM. 2008. 3' RNA elements in hepatitis C virus replication: kissing partners and long poly(U) . J Virol 82: 184-195.
97. You S, Falgout B, Markoff L, Padmanabhan R. 2001. In vitro RNA synthesis from exogenous dengue viral RNA templates requires long range interactions between 5'- and 3'-terminal regions that influence RNA structure. J Biol Chem 276: 15581-15591.
98. Zeisel MB, Felmlee DJ, Baumert TF. 2013. Hepatitis C virus entry. Curr Top Microbiol Immunol 369: 87-112.
99. Zhang B, Dong H, Stein DA, Shi PY. 2008. Co-selection of West Nile virus nucleotides that confer resistance to an antisense oligomer while maintaining long-distance RNA/RNA base pairings. Virology 382: 98-106.
100. Zhao WD, Wimmer E. 2001. Genetic analysis of a poliovirus/hepatitis C virus chimera: new structure for domain II of the internal ribosomal entry site of hepatitis C virus. J Virol 75: 3719-3730.