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

Volumn 10, Issue 10, 2015, Pages

  Soszynska Jozwiak, Marta ^a   Michalak, Paula ^a   Moss, Walter N ^b   Kierzek, Ryszard ^a   Kierzek, Elzbieta ^a  

^a INSTITUTE OF BIOORGANIC CHEMISTRY   (Poland)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; GENOMIC RNA; MESSENGER RNA; SHORT HAIRPIN RNA; VIRUS NUCLEOPROTEIN; PROTEIN BINDING; VIRAL PROTEIN; VIRUS RNA;

ALTERNATIVE RNA SPLICING; ANALYTICAL PARAMETERS; ANIMAL CELL; ARTICLE; BIOINFORMATICS; COMPARATIVE STUDY; CONTROLLED STUDY; ENERGY MINIMIZATION; GENETIC CONSERVATION; IN VITRO STUDY; INFLUENZA A VIRUS; INFLUENZA A VIRUS (H5N1); MICROARRAY ANALYSIS; NONHUMAN; PROTEIN SECONDARY STRUCTURE; RNA FOLDING; RNA SEQUENCE; RNA STRUCTURAL MOTIF; RNA STRUCTURE; THERMODYNAMICS; VIRAL FITNESS; VIRAL PHENOMENA AND FUNCTIONS; VIRAL PROLIFERATION REGULATION; VIRUS GENOME; ANIMAL; CELL LINE; CONFORMATION; DOG; GENETICS; MDCK CELL LINE; OPEN READING FRAME; VIRUS REPLICATION;

ALTERNATIVE SPLICING; ANIMALS; CELL LINE; DOGS; INFLUENZA A VIRUS, H5N1 SUBTYPE; MADIN DARBY CANINE KIDNEY CELLS; NUCLEIC ACID CONFORMATION; OPEN READING FRAMES; PROTEIN BINDING; RNA, MESSENGER; RNA, VIRAL; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 84949523890     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0141132     Document Type: Article

References (50)

1. Shapshak P, Chiappelli F, Somboonwit C, Sinnott J. The Influenza Pandemic of 2009 Lessons and Implications. Molecular Diagnosis & Therapy. 2011 2011; 15(2):63-81.
2. Franco-Paredes C, Hernandez-Ramos I, Del Rio C, Alexander KT, Tapia-Conyer R, Santos-Preciado JI. H1N1 Influenza Pandemics: Comparing the Events of 2009 in Mexico with those of 1976 and 1918-1919. Archives of Medical Research. 2009 Nov; 40(8):669-72. doi: 10.1016/j.arcmed.2009.10.004 PMID: 20304254
3. Van Kerkhove MD, Asikainen T, Becker NG, Bjorge S, Desenclos J-C, dos Santos T, et al. Studies Needed to Address Public Health Challenges of the 2009 H1N1 Influenza Pandemic: Insights from Modeling. Plos Medicine. 2010 Jun; 7(6).
4. Neumann G, Noda T, Kawaoka Y. Emergence and pandemic potential of swine-origin H1N1 influenza virus. Nature. 2009 Jun 18; 459(7249):931-9. doi: 10.1038/nature08157 PMID: 19525932
5. York A, Fodor E. Biogenesis, assembly, and export of viral messenger ribonucleoproteins in the influenza A virus infected cell. Rna Biology. 2013 Aug 1; 10(8):1274-82. doi: 10.4161/rna.25356 PMID: 23807439
6. Bouvier NM, Palese P. The biology of influenza viruses. Vaccine. 2008 Sep; 26:D49-D53. PMID: 19230160
7. Gultyaev AP, Fouchier RAM, Olsthoorn RCL. Influenza Virus RNA Structure: Unique and Common Features. International Reviews of Immunology. 2010 Dec; 29(6):533-56. doi: 10.3109/08830185. 2010.507828 PMID: 20923332
8. Gultyaev AP, Olsthoorn RCL. A family of non-classical pseudoknots in influenza A and B viruses. RNA Biology. 2010 Mar-Apr; 7(2):125-9. PMID: 20200490
9. 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; 11:942-52. doi: 10.4161/rna.29730 PMID: 25180940
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. Proc Natl Acad Sci U S A. 2001 Sep 11; 98(19):10602-7. PMID: 11553808
11. 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(6): e38323-e. doi: 10.1371/journal.pone.0038323 PMID: 22685560
12. Moss WN, Priore SF, Turner DH. Identification of potential conserved RNA secondary structure throughout influenza A coding regions. RNA. 2011 Jun; 17(6):991-1011. doi: 10.1261/rna.2619511 PMID: 21536710
13. 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; 53:5236-48. doi: 10.1021/bi500611j PMID: 25026548
14. Priore SF, Kierzek E, Kierzek R, Baman J, 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(9):e70615. doi: 10.1371/journal.pone.0070615 PMID: 24023714
15. Priore SF, Moss WN, Turner DH. Influenza A Virus Coding Regions Exhibit Host-Specific Global Ordered RNA Structure. Plos One. 2012 Apr; 7(4):e35989. doi: 10.1371/journal.pone.0035989 PMID: 22558296
16. Dela-Moss LI, Moss WN, Turner DH. Identification of conserved RNA secondary structures at influenza B and C splice sites reveals similarities and differences between influenza A, B, and C. BMC Research Notes. 2014 2014 Jan; 7:22-. doi: 10.1186/1756-0500-7-22 PMID: 24405943
17. Chiang C, Chen G-W, Shih S-R. Mutations at Alternative 5′ Splice Sites of M1 mRNA Negatively Affect Influenza A Virus Viability and Growth Rate. J Virol. 2008 Nov; 82(21):10873-86. doi: 10.1128/JVI. 00506-08 PMID: 18768984
18. 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 Oct; 37(42):14719-35. PMID: 9778347
19. Kierzek E, Kierzek R. The thermodynamic stability of RNA duplexes and hairpins containing N-6-alkyladenosines and 2-methylthio-N-6-alkyladenosines. Nucleic Acids Res. 2003 Aug; 31(15):4472-80. PMID: 12888507
20. Ehresmann C, Baudin F, Mougel M, Romby P, Ebel JP, Ehresmann B. Probing the structure of RNAs in solution. Nucleic Acids Res. 1987; 15:9109-28. PMID: 2446263
21. 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 Mar; 127 (12):4223-31. PMID: 15783204
22. 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 Apr; 36 (6):1770-82. doi: 10.1093/nar/gkm1085 PMID: 18252773
23. Kierzek E. Binding of short oligonucleotides to RNA: studies of the binding of common RNA structural motifs to isoenergetic microarrays. Biochemistry. 2009 Dec; 48(48):11344-56. doi: 10.1021/bi901264v PMID: 19835418
24. 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 Sep; 50 (35):7647-65. doi: 10.1021/bi200463p PMID: 21793590
25. 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 Jan; 82(2):596-601. PMID: 17942553
26. Gruber AR, Findeiss S, Washietl S, Hofacker IL, Stadler PF. RNAz 2.0: improved noncoding RNA detection. Pac Symp Biocomp. 2010; 15:69-79.
27. Gruber AR, Neuboeck R, Hofacker IL, Washietl S. The RNAz web server: prediction of thermodynamically stable and evolutionarily conserved RNA structures. Nucleic Acids Res. 2007 Jul; 35:W335-W8. PMID: 17452347
28. Bernhart SH, Hofacker IL, Will S, Gruber AR, Stadler PF. RNAalifold: improved consensus structure prediction for RNA alignments. Bmc Bioinformatics. 2008 Nov 11; 9:474. doi: 10.1186/1471-2105-9-474 PMID: 19014431
29. Martinez-Sobrido L, Cadagan R, Steel J, Basler CF, Palese P, Moran TM, et al. Hemagglutinin-Pseudotyped Green Fluorescent Protein-Expressing Influenza Viruses for the Detection of Influenza Virus Neutralizing Antibodies. J Virol. 2010 Feb 15; 84(4):2157-63. doi: 10.1128/JVI.01433-09 PMID: 19939917
30. Baker SF, Guo H, Albrecht RA, Garcia-Sastre A, Topham DJ, Martinez-Sobrido L. Protection against Lethal Influenza with a Viral Mimic. J Virol. 2013 Aug; 87(15):8591-605. doi: 10.1128/JVI.01081-13 PMID: 23720727
31. 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 Dec; 11(12):2057-61. doi: 10.1016/j.intimp.2011.08. 019 PMID: 21933722
32. Washietl S, Hofacker IL, Stadler PF. Fast and reliable prediction of noncoding RNAs. Proc Natl Acad Sci U S A. 2005 Feb 15; 102(7):2454-9. PMID: 15665081
33. Reuter JS, Mathews DH. RNAstructure: software for RNA secondary structure prediction and analysis. Bmc Bioinformatics. 2010 Mar; 11.
34. 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 May; 101(19):7287-92. PMID: 15123812
35. 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; 390:428-42. doi: 10.1016/j.jmb.2009.04.048 PMID: 19397915
36. 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(12):4055-63. PMID: 17567607
37. 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 Feb; 47(5):1249-58. doi: 10.1021/bi701758z PMID: 18177022
38. 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(16):5082-93. PMID: 16155181
39. Kierzek E, Fratczak A, Pasternak A, Turner DH, Kierzek R. Isoenergetic RNA microarrays, a new method to study the structure and interactions of RNA. International Proceedings Division. 2007:25-30.
40. Kierzek E, Kierzek R, Turner DH, Catrina IE. Facilitating RNA structure prediction with microarrays. Biochemistry. 2006 Jan; 45(2):581-93. PMID: 16401087
41. Mizuta T, Fujiwara M, Hatta T, Abe T, Miyano-Kurosaki N, Shigeta S, et al. Antisense oligonucleotides directed against the viral RNA polymerase gene enhance survival of mice infected with influenza A. Nature Biotechnology. 1999 Jun; 17(6):583-7. PMID: 10385324
42. 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 Nov; 50(11):3724-33. PMID: 16966399
43. Wu Y, Zhang G, Li Y, Jin Y, Dale R, Sun L-Q, et al. Inhibition of highly pathogenic avian H5N1 influenza virus replication by RNA oligonucleotides targeting NS1 gene. Biochem Biophys Res Commun. 2008; 365:369-74. PMID: 17996729
44. Kumar B, Khanna M, Kumar P, Sood V, Vyas R, Banerjea AC. Nucleic Acid-Mediated Cleavage of M1 Gene of Influenza A Virus Is Significantly Augmented by Antisense Molecules Targeted to Hybridize Close to the Cleavage Site. Molecular Biotechnology. 2012 May; 51(1):27-36. doi: 10.1007/s12033-011-9437-z PMID: 21744034
45. Li W, Yang X, Jiang Y, Wang B, Yang Y, Jiang Z, et al. Inhibition of influenza A virus replication by RNA interference targeted against the PB1 subunit of the RNA polymerase gene. Archives of Virology. 2011 Nov; 156(11):1979-87. doi: 10.1007/s00705-011-1087-8 PMID: 21837415
46. Ge Q, Filip L, Bai AL, Nguyen T, Eisen HN, Chen J. Inhibition of influenza virus production in virusinfected mice by RNA interference. Proc Natl Acad Sci U S A. 2004 Jun 8; 101(23):8676-81. PMID: 15173599
47. Ge Q, McManus MT, Nguyen T, Shen CH, Sharp PA, Eisen HN, et al. RNA interference of influenza virus production by directly targeting rnRNA for degradation and indirectly inhibiting all viral RNA transcription. Proc Natl Acad Sci U S A. 2003 Mar; 100(5):2718-23. PMID: 12594334
48. Martelli F, Salata C, Calistri A, Parolin C, Azzi A, Palù G, et al. Small RNAs targeting the 5′ end of the viral polymerase gene segments specifically interfere with influenza type A virus replication. J Biotechnol 2015; 210:85-90. doi: 10.1016/j.jbiotec.2015.06.391 PMID: 26091771
49. Zhang T, Zhao P-S, Zhang W, Liang M, Gao Y-W, Yang S-T, et al. Antisense oligonucleotide inhibits avian influenza virus H5N1 replication by single chain antibody delivery system. Vaccine. 2011 Feb 11; 29(8):1558-64. doi: 10.1016/j.vaccine.2010.12.088 PMID: 21215341
50. Giannecchini S, Wise HM, Digard P, Clausi V, Del Poggetto E, Vesco L, et al. Packaging signals in the 5 '-ends of influenza virus PA, PB1, and PB2 genes as potential targets to develop nucleic-acid based antiviral molecules. Antiviral Res. 2011 Oct; 92(1):64-72. doi: 10.1016/j.antiviral.2011.06.013 PMID: 21741410