Self-folding of naked segment 8 genomic RNA of influenza a virus

PLoS ONE

Volumn 11, Issue 2, 2016, Pages

  Lenartowicz, Elzbieta ^a   Kesy, Julita ^a   Ruszkowska, Agnieszka ^a   Soszynska Jozwiak, Marta ^a   Michalak, Paula ^a   Moss, Walter N ^b   Turner, Douglas H ^b   Kierzek, Ryszard ^a   Kierzek, Elzbieta ^a  

^a INSTITUTE OF BIOORGANIC CHEMISTRY   (Poland)

^b UNIVERSITY OF ROCHESTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS PROTEIN NEP; VIRUS PROTEIN NS1; VIRUS RNA;

ARTICLE; BASE PAIRING; BIOINFORMATICS; CONTROLLED STUDY; GENETIC CODE; IN VITRO STUDY; INFLUENZA A VIRUS; NONHUMAN; PROTEIN BINDING; PROTEIN STRUCTURE; RNA FOLDING; RNA SEQUENCE; RNA STRUCTURE; SEQUENCE ANALYSIS; THERMODYNAMICS; VIRUS GENOME; VIRUS STRAIN; CHEMISTRY; COMPUTER SIMULATION; GENETICS; INFLUENZA A VIRUS (H5N1); MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE;

BASE PAIRING; BASE SEQUENCE; COMPUTER SIMULATION; GENOME, VIRAL; INFLUENZA A VIRUS, H5N1 SUBTYPE; MOLECULAR SEQUENCE DATA; RNA FOLDING; RNA, VIRAL;

EID: 84959233783     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0148281     Document Type: Article

References (83)

1. Shapshak P, Chiappelli F, Somboonwit C, Sinnott J. The Influenza Pandemic of 2009 Lessons and Implications. Molecular Diagnosis & Therapy. 2011; 15: 63-81.
2. Nguyen-Van-Tam JS, Hampson AW. The epidemiology and clinical impact of pandemic influenza. Vaccine. 2003; 21: 1762-1768. PMID: 12686091
3. Bouvier NM, Palese P. The biology of influenza viruses. Vaccine. 2008; 26: D49-D53. PMID: 19230160
4. Moeller A, Kirchdoerfer RN, Potter CS, Carragher B, Wilson IA. Organization of the Influenza Virus Replication Machinery. Science. 2012; 338: 1631-1634. doi: 10.1126/science.1227270 PMID: 23180774
5. Suzuki Y, Kobayashi Y. Evolution of complementary nucleotides in 5' and 3' untranslated regions of influenza A virus genomic segments. Infection, Genetics and Evolution. 2013; 13: 175-179. doi: 10.1016/j.meegid.2012.10.007 PMID: 23146832
6. Hsu MT, Parvin JD, Gupta S, Krystal M, Palese P. 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. PMID: 2446318
7. Pflug A, Guilligay D, Reich S, Cusack S. Structure of influenza A polymerase bound to the viral RNA promoter. Nature. 2014; 516: 355-360 doi: 10.1038/nature14008 PMID: 25409142
8. Reich S, Guilligay D, Pflug A, Malet H, Berger I, Crepin T, et al. Structural insight into cap-snatching and RNA synthesis by influenza polymerase. Nature. 2014; 516: 361-366 doi: 10.1038/nature14009 PMID: 25409151
9. Flick R, Hobom G. Interaction of influenza virus polymerase with viral RNA in the 'corkscrew' conformation. J Gen Virol. 1999; 80: 2565-2572. PMID: 10573148
10. Bae SH, Cheong HK, Lee JH, Cheong C, Kainosho M, Choi BS. Structural features of an influenza virus promoter and their implications for viral RNA synthesis. Proceedings of the National Academy of Sciences of the United States of America. 2001; 98: 10602-10607. PMID: 11553808
11. Gultyaev AP, Fouchier RAM, Olsthoorn RCL. Influenza Virus RNA Structure: Unique and Common Features. International Reviews of Immunology. 2010; 29: 533-556. doi: 10.3109/08830185.2010. 507828 PMID: 20923332
12. Gultyaev A, Tsyganov-Bodounov A, Spronken M, van der Kooij S, Fouchier R, Olsthoorn R. RNA structural constraints in the evolution of the influenza A virus genome NP segment. RNA Biology 2014; 11: 942-952. doi: 10.4161/rna.29730 PMID: 25180940
13. Gavazzi C, Isel C, Fournier E, Moules V, Cavalier A, Thomas D, et al. An in vitro network of intermolecular interactions between viral RNA segments of an avian H5N2 influenza A virus: comparison with a human H3N2 virus. Nucleic Acids Res. 2013; 41: 1241-1254. doi: 10.1093/nar/gks1181 PMID: 23221636
14. Fournier E, Moules V, Essere B, Paillart J-C, Sirbat J-D, Cavalier A, et al. Interaction network linking the human H3N2 influenza A virus genomic RNA segments. Vaccine. 2012 2012; 30: 7359-7367. doi: 10.1016/j.vaccine.2012.09.079 PMID: 23063835
15. Fournier E, Moules V, Essere B, Paillart J-C, Sirbat J-D, Isel C, et al. A supramolecular assembly formed by influenza A virus genomic RNA segments. Nucleic Acids Res. 2012; 40: 2197-2209. doi: 10.1093/nar/gkr985 PMID: 22075989
16. Essere B, Yver M, Gavazzi C, Terrier O, Isel C, Fournier E, et al. Critical role of segment-specific packaging signals in genetic reassortment of influenza A viruses. Proc Natl Acad Sci U S A. 2013; 110: E3840-E3848. doi: 10.1073/pnas.1308649110 PMID: 24043788
17. Eggington JM, Greene T, Bass BL. Predicting sites of ADAR editing in double-stranded RNA. Nature Communications. 2011; 2: 319. doi: 10.1038/ncomms1324 PMID: 21587236
18. Tenoever BR, Ng SL, Chua MA, McWhirter SM, Garcia-Sastre A, Maniatis T. Multiple functions of the IKK-related kinase IKK epsilon in interferon-mediated antiviral immunity. Science. 2007; 315: 1274-1278. PMID: 17332413
19. Suspene R, Petit V, Puyraimond-Zemmour D, Aynaud M-M, Henry M, Guetard D, et al. Double-Stranded RNA Adenosine Deaminase ADAR-1-Induced Hypermutated Genomes among Inactivated Seasonal Influenza and Live Attenuated Measles Virus Vaccines. J Virol. 2011; 85: 2458-2462. doi: 10.1128/JVI.02138-10 PMID: 21159878
20. Ward SV, George CX, Welch MJ, Liou L-Y, Hahm B, Lewicki H, et al. RNA editing enzyme adenosine deaminase is a restriction factor for controlling measles virus replication that also is required for embryogenesis. Proc Natl Acad Sci U S A. 2011; 108: 331-336. doi: 10.1073/pnas.1017241108 PMID: 21173229
21. Hofacker IL, Stadler PF, Stocsits RR. Conserved RNA secondary structures in viral genomes: a survey. Bioinformatics. 2004; 20: 1495-1499. PMID: 15231541
22. Priore SF, Moss WN, Turner DH. Influenza A Virus Coding Regions Exhibit Host-Specific Global Ordered RNA Structure. PLOS ONE. 2012; 7: e35989. doi: 10.1371/journal.pone.0035989 PMID: 22558296
23. Moss WN, Priore SF, Turner DH. Identification of potential conserved RNA secondary structure throughout influenza A coding regions. RNA-Publ RNA Soc. 2011; 17: 991-1011.
24. Gultyaev AP, Olsthoorn RCL. A family of non-classical pseudoknots in influenza A and B viruses. Rna Biology. 2010; 7: 125-129. PMID: 20200490
25. Moss WN, Dela-Moss LI, Kierzek E, Kierzek R, Priore SF, Turner DH. The 3' splice site of influenza A segment 7 mRNA can exist in two conformations: a pseudoknot and a hairpin. PLOS ONE. 2012; 7: e38323. doi: 10.1371/journal.pone.0038323 PMID: 22685560
26. Jiang T, Kennedy SD, Moss WN, Kierzek E, Turner DH. Secondary structure of a conserved domain in an intron of influenza A M1 mRNA. Biochemistry. 2014; 53: 5236-5248. doi: 10.1021/bi500611j PMID: 25026548
27. Priore SF, Kierzek E, Kierzek R, Baman JR, Moss WN, Dela-Moss LI, et al. Secondary structure of a conserved domain in the intron of influenza A NS1 mRNA. PLOS ONE. 2013; 8: e70615. doi: 10.1371/ journal.pone.0070615 PMID: 24023714
28. Priore SF, Kauffmann AD, Baman JR, Turner DH. The Influenza A PB1-F2 and N40 Start Codons Are Contained within an RNA Pseudoknot. Biochemistry. 2015; 54: 3413-3415. doi: 10.1021/bi501564d PMID: 25996464
29. Soszynska-Jozwiak M, Michalak P, Moss WN, Kierzek R, Kierzek E. A Conserved Secondary Structural Element in the Coding Region of the Influenza A Virus Nucleoprotein (NP) mRNA Is Important for the Regulation of Viral Proliferation. PLOS ONE. 2015; 10: e0141132. doi: 10.1371/journal.pone. 0141132 PMID: 26488402
30. Arranz R, Coloma R, Javier Chichon F, Javier Conesa J, Carrascosa JL, Valpuesta JM, et al. The Structure of Native Influenza Virion Ribonucleoproteins. Science. 2012; 338: 1634-1637. doi: 10.1126/ science.1228172 PMID: 23180776
31. Coloma R, Valpuesta JM, Arranz R, Carrascosa JL, Ortin J, Martin-Benito J. The Structure of a Biologically Active Influenza Virus Ribonucleoprotein Complex. PLOS Pathogens. 2009; 5: e1000491 doi: 10.1371/journal.ppat.1000491 PMID: 19557158
32. Baudin F, Bach C, Cusack S, Ruigrok RWH. Structure of Influenza-Virus Rnp.1. Influenza-Virus Nucleoprotein Melts Secondary Structure in Panhandle Rna and Exposes the Bases to the Solvent. Embo J. 1994; 13: 3158-3165. PMID: 8039508
33. 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. PMID: 9135141
34. Portela A, Digard P. The influenza virus nucleoprotein: a multifunctional RNA-binding protein pivotal to virus replication. J Gen Virol. 2002; 83: 723-734. PMID: 11907320
35. Zheng W, Olson J, Vakharia V, Tao YJ. The Crystal Structure and RNA-Binding of an Orthomyxovirus Nucleoprotein. PLOS Pathogens. 2013; 9: e1003657.
36. 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. PMID: 2358455
37. Xia TB, SantaLucia J, Burkard ME, Kierzek R, Schroeder SJ, Jiao XQ, et al. Thermodynamic parameters for an expanded nearest-neighbor model for formation of RNA duplexes with Watson-Crick base pairs. Biochemistry. 1998; 37: 14719-14735. PMID: 9778347
38. Crothers DM. The molecular mechanism of thermal unfolding. J Mol Biol. 1974; 87: 63-88. PMID: 4610153
39. Zhang T, Wang T-C, Zhao P-S, Liang M, Gao Y-W, Yang S-T, et al. Antisense oligonucleotides targeting the RNA binding region of the NP gene inhibit replication of highly pathogenic avian influenza virus H5N1. International Immunopharmacology. 2011; 11: 2057-2061. doi: 10.1016/j.intimp.2011.08.019 PMID: 21933722
40. Ge Q, Pastey M, Kobasa D, Puthavathana P, Lupfer C, Bestwick RK, et al. Inhibition of multiple subtypes of influenza A virus in cell cultures with morpholino oligomers. Antimicrob Agents Chemother. 2006; 50: 3724-3733. PMID: 16966399
41. Poland GA, Jacobson RM, Targonski PV. Avian and pandemic influenza: An overview. Vaccine. 2007; 25: 3057-3061. PMID: 17289227
42. Imai M, Watanabe T, Hatta M, Das SC, Ozawa M, Shinya K, et al. Experimental adaptation of an influenza H5 HA confers respiratory droplet transmission to a reassortant H5 HA/H1N1 virus in ferrets. Nature. 2012; 486: 420-428. doi: 10.1038/nature10831 PMID: 22722205
43. Pasternak A, Kierzek E, Pasternak K, Turner DH, Kierzek R. A chemical synthesis of LNA-2,6-diaminopurine riboside, and the influence of 2'-O-methyl-2,6-diaminopurine and LNA-2,6-diaminopurine ribosides on the thermodynamic properties of 2'-O-methyl RNA/RNA heteroduplexes. Nucleic Acids Res. 2007; 35: 4055-4063. PMID: 17567607
44. Kierzek E, Kierzek R. The synthesis of oligoribonucleotides containing N-6-alkyladenosines and 2-methylthio-N-6-alkyladenosines via post-synthetic modification of precursor oligomers. Nucleic Acids Res. 2003; 31: 4461-4471. PMID: 12888506
45. Fujii K, Fujii Y, Noda T, Muramoto Y, Watanabe T, Takada A, et al. 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. 2005; 79: 3766-3774. PMID: 15731270
46. Merino EJ, Wilkinson KA, Coughlan JL, Weeks KM. RNA structure analysis at single nucleotide resolution by selective 2 '-hydroxyl acylation and primer extension (SHAPE). J Am Chem Soc. 2005; 127: 4223-4231. PMID: 15783204
47. Fratczak A, Kierzek R, Kierzek E. LNA-Modified Primers Drastically Improve Hybridization to Target RNA and Reverse Transcription. Biochemistry. 2009; 48: 514-516. doi: 10.1021/bi8021069 PMID: 19119855
48. Reuter JS, Mathews DH. RNAstructure: software for RNA secondary structure prediction and analysis. BMC Bioinformatics. 2010; 11: 129. doi: 10.1186/1471-2105-11-129 PMID: 20230624
49. Mathews DH, Disney MD, Childs JL, Schroeder SJ, Zuker M, Turner DH. Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. Proc Natl Acad Sci U S A. 2004; 101: 7287-7292. PMID: 15123812
50. Bao Y, Bolotov P, Dernovoy D, Kiryutin B, Zaslavsky L, Tatusova T, et al. The influenza virus resource at the national center for biotechnology information. J Virol. 2008; 82: 596-601. PMID: 17942553
51. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series. 1999; 41: 95-98.
52. Hofacker IL, Fontana W, Stadler PF, Bonhoeffer S, Tacker M, Schuster P. Fast Folding and Comparison of RNA Secondary Structures. Monatshefte für Chemie. 1994; 125: 167-188.
53. Gruber AR, Lorenz R, Bernhart SH, Neuboeck R, Hofacker IL. The Vienna RNA Websuite. Nucleic Acids Res. 2008; 36: W70-W74. doi: 10.1093/nar/gkn188 PMID: 18424795
54. Katoh K, Misawa K, Kuma K, Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucl Acids Res. 2002; 30: 3059-3066. PMID: 12136088
55. Turner DH, Mathews DH. NNDB: the nearest neighbor parameter database for predicting stability of nucleic acid secondary structure. Nucleic Acids Res. 2010; 38: D280-D282. doi: 10.1093/nar/gkp892 PMID: 19880381
56. Zuker M, Stiegler P. Optimal Computer Folding of Large RNA Sequences Using Thermodynamics and Auxiliary Information. Nucleic Acids Res. 1981; 9: 133-148. PMID: 6163133
57. Schroeder SJ. Probing Viral Genomic Structure: Alternative Viewpoints and Alternative Structures for Satellite Tobacco Mosaic Virus RNA. Biochemistry. 2014; 53: 6728-6737. doi: 10.1021/bi501051k PMID: 25320869
58. Schroeder SJ, Stone JW, Bleckley S, Gibbons T, Mathews DM. Ensemble of secondary structures for encapsidated satellite tobacco mosaic virus RNA consistent with chemical probing and crystallography constraints. Biophys J. 2011; 101: 167-175. doi: 10.1016/j.bpj.2011.05.053 PMID: 21723827
59. Kierzek E, Kierzek R, Moss WN, Christensen SM, Eickbush TH, Turner DH. Isoenergetic penta-and hexanucleotide microarray probing and chemical mapping provide a secondary structure model for an RNA element orchestrating R2 retrotransposon protein function. Nucleic Acids Res. 2008; 36: 1770-1782. doi: 10.1093/nar/gkm1085 PMID: 18252773
60. Kierzek E. Binding of Short Oligonucleotides to RNA: Studies of the Binding of Common RNA Structural Motifs to Isoenergetic Microarrays. Biochemistry. 2009; 48: 11344-11356. doi: 10.1021/bi901264v PMID: 19835418
61. Fratczak A, Kierzek R, Kierzek E. Isoenergetic Microarrays To Study the Structure and Interactions of DsrA and OxyS RNAs in Two-and Three-Component Complexes. Biochemistry. 2011; 50:7647-7665. doi: 10.1021/bi200463p PMID: 21793590
62. Kierzek R, Turner DH, Kierzek E. Microarrays for identifying binding sites and probing structure of RNAs. Nucleic Acids Res. 2015; 43: 1-12. doi: 10.1093/nar/gku1303 PMID: 25505162
63. Pasternak A, Kierzek E, Pasternak K, Fratczak A, Turner DH, Kierzek R. The thermodynamics of 3'-terminal pyrene and guanosine for the design of isoenergetic 2'-O-methyl-RNA-LNA chimeric oligonucleotide probes of RNA structure. Biochemistry. 2008; 47: 1249-1258. doi: 10.1021/bi701758z PMID: 18177022
64. Kierzek E, Ciesielska A, Pasternak K, Mathews DH, Turner DH, Kierzek R. The influence of locked nucleic acid residues on the thermodynamic properties of 2'-O-methyl RNA/RNA heteroduplexes. Nucleic Acids Res. 2005; 33: 5082-5093. PMID: 16155181
65. Afanassiev V, Hanemann V, Wolfl S. Preparation of DNA and protein micro arrays on glass slides coated with an agarose film. Nucleic Acids Res. 2000; 28: e66. PMID: 10871389
66. Kierzek E, Christensen SM, Eickbush TH, Kierzek R, Turner DH, Moss WN. Secondary structures for 5' regions of R2 retrotransposon RNAs reveal a novel conserved pseudoknot and regions that evolve under different constraints. J Mol Biol. 2009; 390: 428-442. doi: 10.1016/j.jmb.2009.04.048 PMID: 19397915
67. Kierzek E, Kierzek R, Turner DH, Catrina IE. Facilitating RNA structure prediction with microarrays. Biochemistry. 2006; 45: 581-593. PMID: 16401087
68. Deigan KE, Li TW, Mathews DH, Weeks KM. Accurate SHAPE-directed RNA structure determination. Proc Natl Acad Sci U S A. 2009; 106: 97-102. doi: 10.1073/pnas.0806929106 PMID: 19109441
69. Lu ZJ, Gloor JW, Mathews DH. Improved RNA secondary structure prediction by maximizing expected pair accuracy. RNA-Publ RNA Soc. 2009; 15: 1805-1813.
70. Gruber AR, Findeiss S, Washietl S, Hofacker IL, Stadler PF. RNAz 2.0: improved noncoding RNA detection. Pac Symp Biocomput. 2010: 69-79. PMID: 19908359
71. Gavazzi C, Yver M, Isel C, Smyth RP, Rosa-Calatrava M, Lina B, et al. A functional sequence-specific interaction between influenza A virus genomic RNA segments. Proc Natl Acad Sci U S A. 2013; 110: 16604-16609. doi: 10.1073/pnas.1314419110 PMID: 24067651
72. Shao Y, Chan CY, Maliyekkel A, Lawrence CE, Roninson IB, Ding Y. Effect of target secondary structure on RNAi efficiency. RNA. 2007; 13: 1631-1640. PMID: 17684233
73. Lu ZJ, Mathews DH. Fundamental differences in the equilibrium considerations for siRNA and antisense oligodeoxynucleotide design. Nucleic Acids Res. 2008; 36: 3738-3745. doi: 10.1093/nar/ gkn266 PMID: 18483081
74. Wilkinson KA, Merino EJ, Weeks KM. RNA SHAPE chemistry reveals nonhierarchical interactions dominate equilibrium structural transitions in tRNA(Asp) transcripts. J Am Chem Soc. 2005; 127: 4659-4667. PMID: 15796531
75. Wilkinson KA, Merino EJ, Weeks KM. Selective 2'-hydroxyl acylation analyzed by primer extension (SHAPE): quantitative RNA structure analysis at single nucleotide resolution. Nature Protocols. 2006; 1: 1610-1616. PMID: 17406453
76. Ehresmann C, Baudin F, Mougel M, Romby P, Ebel JP, Ehresmann B. Probing the structure of RNAs in solution. Nucleic Acids Res. 1987; 15: 9109-9128. PMID: 2446263
77. Liang RT, Kierzek E, Kierzek R, Turner DH. Comparisons between Chemical Mapping and Binding to Isoenergetic Oligonucleotide Microarrays Reveal Unexpected Patterns of Binding to the Bacillus subtilis RNase P RNA Specificity Domain. Biochemistry. 2010; 49: 8155-8168. doi: 10.1021/bi100286n PMID: 20557101
78. Kladwang W, Mann TH, Becka A, Tian S, Kim H, Yoon S, et al. Standardization of RNA Chemical Mapping Experiments. Biochemistry. 2014; 53: 3063-3065. doi: 10.1021/bi5003426 PMID: 24766159
79. Znosko BM, Burkard ME, Schroeder SJ, Krugh TR, Turner DH. Sheared A(anti)center dot A(anti) base pairs in a destabilizing 2x2 internal loop: The NMR structure of 5 '(rGGCAAGCCU)(2). Biochemistry. 2002; 41: 14969-14977. PMID: 12475246
80. Cate JH, Gooding AR, Podell E, Zhou KH, Golden BL, Kundrot CE, et al. Crystal structure of a group I ribozyme domain: Principles of RNA packing. Science. 1996; 273: 1678-1685. PMID: 8781224
81. Krasilnikov AS, Yang X, Pan T, Mondragón A. Crystal structure of the specificity domain of ribonuclease P. Nature. 2003; 421: 760-764. PMID: 12610630
82. Lerman YV, Kennedy SD, Shankar N, Parisien M, Major F, Turner DH. NMR structure of a 4 × 4 nucleotide RNA internal loop from an R2 retrotransposon: Identification of a three purine-purine sheared pair motif and comparison to MC-SYM predictions. RNA. 2011; 17: 1664-1677. doi: 10.1261/rna.2641911 PMID: 21778280
83. Zheng W, Olson J, Vakharia V, Tao YJ. The crystal structure and RNA-binding of an orthomyxovirus nucleoprotein. PLOS Pathogens. 2013; 9: e1003624. doi: 10.1371/journal.ppat.1003624 PMID: 24068932