Single-stranded DNA aptamer that specifically binds to the influenza virus NS1 protein suppresses interferon antagonism

Antiviral Research

Volumn 100, Issue 2, 2013, Pages 337-345

  Woo, Hye Min ^a   Kim, Ki Sun ^a   Lee, Jin Moo ^a   Shim, Hee Sup ^a   Cho, Seong Je ^a   Lee, Won Kyu ^a   Ko, Hyuk Wan ^b   Keum, Young Sam ^b   Kim, Soo Youl ^c   Pathinayake, Prabuddha ^d   Kim, Chul Joong ^d   Jeong, Yong Joo ^a  

^a Kookmin University   (South Korea)

^b Dongguk University   (South Korea)

^c National Cancer Center   (South Korea)

^d Chungnam National University   (South Korea)

Author keywords

Aptamer; G quadruplex; Influenza virus; Interferon; NS1

Indexed keywords

APTAMER; BETA INTERFERON; DNA FRAGMENT; GUANINE QUADRUPLEX; INTERFERON; NONSTRUCTURAL PROTEIN 1; SINGLE STRANDED DNA; ANTIVIRUS AGENT; INS1 PROTEIN, INFLUENZA VIRUS; VIRUS PROTEIN;

ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; CELL VIABILITY; CIRCULAR DICHROISM; CYTOKINE RESPONSE; DNA LIBRARY; DNA STRUCTURE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IN VITRO SELECTION; INFLUENZA VIRUS A; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECONDARY STRUCTURE; REPORTER GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA BINDING; VIRUS REPLICATION; ANIMAL; BIOSYNTHESIS; CELL LINE; CELL SURVIVAL; COMBINATORIAL CHEMISTRY; DRUG EFFECT; G-QUADRUPLEX; HUMAN; IMMUNOLOGY; INFLUENZA VIRUS; ISOLATION AND PURIFICATION; KINETICS; METABOLISM; MOUSE; NS1; PHYSIOLOGY; PROTEIN BINDING;

INFLUENZA A VIRUS; ORTHOMYXOVIRIDAE;

APTAMER; G-QUADRUPLEX; INFLUENZA VIRUS; INTERFERON; NS1;

ANIMALS; ANTIVIRAL AGENTS; APTAMERS, NUCLEOTIDE; CELL LINE; CELL SURVIVAL; DNA, SINGLE-STRANDED; HUMANS; INFLUENZA A VIRUS; INTERFERONS; KINETICS; MICE; PROTEIN BINDING; SELEX APTAMER TECHNIQUE; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 84885340369     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2013.09.004     Document Type: Article

References (46)

1. D. Basu, M.P. Walkiewicz, M. Frieman, R.S. Baric, D.T. Auble, and D.A. Engel Novel influenza virus NS1 antagonists block replication and restore innate immune function J. Virol. 83 2009 1881 1891
2. Z.A. Bornholdt, and B.V. Prasad X-ray structure of influenza virus NS1 effector domain Nat. Struct. Mol. Biol. 13 2006 559 560
3. E.N. Brody, and L. Gold Aptamers as therapeutic and diagnostic agents J. Biotechnol. 74 2000 5 13
4. D.H. Bunka, O. Platonova, and P.G. Stockley Development of aptamer therapeutics Curr. Opin. Pharmacol. 10 2010 557 562
5. C. Cheng, J. Dong, L. Yao, A. Chen, R. Jia, L. Huan, J. Guo, Y. Shu, and Z. Zhang Potent inhibition of human influenza H5N1 virus by oligonucleotides derived by SELEX Biochem. Biophys. Res. Commun. 366 2008 670 674
6. C.Y. Chien, R. Tejero, Y. Huang, D.E. Zimmerman, C.B. Rios, R.M. Krug, and G.T. Montelione A novel RNA-binding motif in influenza A virus non-structural protein 1 Nat. Struct. Biol. 4 1997 891 895
7. C.Y. Chien, Y. Xu, R. Xiao, J.M. Aramini, P.V. Sahasrabudhe, R.M. Krug, and G.T. Montelione Biophysical characterization of the complex between double-stranded RNA and the N-terminal domain of the NS1 protein from influenza A virus: evidence for a novel RNA-binding mode Biochemistry 43 2004 1950 1962
8. S.J. Cho, H.M. Woo, K.S. Kim, J.W. Oh, and Y.J. Jeong Novel system for detecting SARS coronavirus nucleocapsid protein using an ssDNA aptamer J. Biosci. Bioeng. 112 2011 535 540
9. N.R. Donelan, C.F. Basler, and A. Garcia-Sastre A recombinant influenza A virus expressing an RNA-binding-defective NS1 protein induces high levels of beta interferon and is attenuated in mice J. Virol. 77 2003 13257 13266
10. A. Egorov, S. Brandt, S. Sereinig, J. Romanova, B. Ferko, D. Katinger, A. Grassauer, G. Alexandrova, H. Katinger, and T. Muster Transfectant influenza A viruses with long deletions in the NS1 protein grow efficiently in Vero cells J. Virol. 72 1998 6437 6441
11. H. Fukuda, M. Katahira, E. Tanaka, Y. Enokizono, N. Tsuchiya, K. Higuchi, M. Nagao, and H. Nakagama Unfolding of higher DNA structures formed by the d(CGG) triplet repeat by UP1 protein Genes Cells 10 2005 953 962
12. M.U. Gack, R.A. Albrecht, T. Urano, K.S. Inn, I.C. Huang, E. Carnero, M. Farzan, S. Inoue, J.U. Jung, and A. Garcia-Sastre Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I Cell Host Microbe 5 2009 439 449
13. U. Garaigorta, A.M. Falcon, and J. Ortin Genetic analysis of influenza virus NS1 gene: a temperature-sensitive mutant shows defective formation of virus particles J. Virol. 79 2005 15246 15257
14. A. Garcia-Sastre, and C.A. Biron Type 1 interferons and the virus-host relationship: a lesson in detente Science 312 2006 879 882
15. A. Garcia-Sastre, A. Egorov, D. Matassov, S. Brandt, D.E. Levy, J.E. Durbin, P. Palese, and T. Muster Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems Virology 252 1998 324 330
16. D. Grimm, P. Staeheli, M. Hufbauer, I. Koerner, L. Martinez-Sobrido, A. Solorzano, A. Garcia-Sastre, O. Haller, and G. Kochs Replication fitness determines high virulence of influenza A virus in mice carrying functional Mx1 resistance gene Proc. Natl. Acad. Sci. USA 104 2007 6806 6811
17. Z. Guo, L.M. Chen, H. Zeng, J.A. Gomez, J. Plowden, T. Fujita, J.M. Katz, R.O. Donis, and S. Sambhara NS1 protein of influenza A virus inhibits the function of intracytoplasmic pathogen sensor, RIG-I Am. J. Respir. Cell Mol. Biol. 36 2007 263 269
18. B.G. Hale, R.E. Randall, J. Ortin, and D. Jackson The multifunctional NS1 protein of influenza A viruses J. Gen. Virol. 89 2008 2359 2376
19. O. Haller, G. Kochs, and F. Weber The interferon response circuit: induction and suppression by pathogenic viruses Virology 344 2006 119 130
20. C.C. Hardin, T. Watson, M. Corregan, and C. Bailey Cation-dependent transition between the quadruplex and Watson-Crick hairpin forms of d(CGCG3GCG) Biochemistry 31 1992 833 841
21. E. Hatada, T. Takizawa, and R. Fukuda Specific binding of influenza A virus NS1 protein to the virus minus-sense RNA in vitro J. Gen. Virol. 73 Pt 1 1992 17 25
22. J.J. Jablonski, D. Basu, D.A. Engel, and H.M. Geysen Design, synthesis, and evaluation of novel small molecule inhibitors of the influenza virus protein NS1 Bioorg. Med. Chem. 20 2012 487 497
23. D. Jackson, M.J. Hossain, D. Hickman, D.R. Perez, and R.A. Lamb A new influenza virus virulence determinant: the NS1 protein four C-terminal residues modulate pathogenicity Proc. Natl. Acad. Sci. USA 105 2008 4381 4386
24. T. Kaisho, and S. Akira Toll-like receptor function and signaling J. Allergy Clin. Immunol. 117 2006 979 987
25. G. Kochs, I. Koerner, L. Thiel, S. Kothlow, B. Kaspers, N. Ruggli, A. Summerfield, J. Pavlovic, J. Stech, and P. Staeheli Properties of H7N7 influenza A virus strain SC35M lacking interferon antagonist NS1 in mice and chickens J. Gen. Virol. 88 2007 1403 1409
26. M. Kurokawa, A.H. Koyama, S. Yasuoka, and A. Adachi Influenza virus overcomes apoptosis by rapid multiplication Int. J. Mol. Med. 3 1999 527 530
27. J. Liu, P.A. Lynch, C.Y. Chien, G.T. Montelione, R.M. Krug, and H.M. Berman Crystal structure of the unique RNA-binding domain of the influenza virus NS1 protein Nat. Struct. Biol. 4 1997 896 899
28. S. Ludwig, X. Wang, C. Ehrhardt, H. Zheng, N. Donelan, O. Planz, S. Pleschka, A. Garcia-Sastre, G. Heins, and T. Wolff The influenza A virus NS1 protein inhibits activation of Jun N-terminal kinase and AP-1 transcription factors J. Virol. 76 2002 11166 11171
29. H.J. Moon, J.S. Lee, Y.K. Choi, J.Y. Park, M.R. Talactac, M.Y. Chowdhury, H. Poo, M.H. Sung, J.H. Lee, J.U. Jung, and C.J. Kim Induction of type I interferon by high-molecular poly-gamma-glutamate protects B6.A2G-Mx1 mice against influenza A virus Antiviral Res. 94 2012 98 102
30. K. Onomoto, M. Jogi, J.S. Yoo, R. Narita, S. Morimoto, A. Takemura, S. Sambhara, A. Kawaguchi, S. Osari, K. Nagata, T. Matsumiya, H. Namiki, M. Yoneyama, and T. Fujita Critical role of an antiviral stress granule containing RIG-I and PKR in viral detection and innate immunity PLoS ONE 7 2012 e43031
31. A. Pichlmair, O. Schulz, C.P. Tan, T.I. Naslund, P. Liljestrom, F. Weber, and C. Reis e Sousa RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates Science 314 2006 997 1001
32. R.E. Randall, and S. Goodbourn Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures J. Gen. Virol. 89 2008 1 47
33. K.T. Shum, and J.A. Tanner Differential inhibitory activities and stabilisation of DNA aptamers against the SARS coronavirus helicase ChemBioChem 9 2008 3037 3045
34. D.L. Suarez, and M.L. Perdue Multiple alignment comparison of the non-structural genes of influenza A viruses Virus Res. 54 1998 59 69
35. J. Talon, C.M. Horvath, R. Polley, C.F. Basler, T. Muster, P. Palese, and A. Garcia-Sastre Activation of interferon regulatory factor 3 is inhibited by the influenza A virus NS1 protein J. Virol. 74 2000 7989 7996
36. J. Talon, M. Salvatore, R.E. O'Neill, Y. Nakaya, H. Zheng, T. Muster, A. Garcia-Sastre, and P. Palese Influenza A and B viruses expressing altered NS1 proteins: a vaccine approach Proc. Natl. Acad. Sci. USA 97 2000 4309 4314
37. K.Y. Twu, D.L. Noah, P. Rao, R.L. Kuo, and R.M. Krug The CPSF30 binding site on the NS1A protein of influenza A virus is a potential antiviral target J. Virol. 80 2006 3957 3965
38. M. Vairamani, and M.L. Gross G-quadruplex formation of thrombin-binding aptamer detected by electrospray ionization mass spectrometry J. Am. Chem. Soc. 125 2003 42 43
39. N.V. Vo, J.W. Oh, and M.M. Lai Identification of RNA ligands that bind hepatitis C virus polymerase selectively and inhibit its RNA synthesis from the natural viral RNA templates Virology 307 2003 301 316
40. M.P. Walkiewicz, D. Basu, J.J. Jablonski, H.M. Geysen, and D.A. Engel Novel inhibitor of influenza non-structural protein 1 blocks multi-cycle replication in an RNase L-dependent manner J. Gen. Virol. 92 2011 60 70
41. X. Wang, M. Li, H. Zheng, T. Muster, P. Palese, A.A. Beg, and A. Garcia-Sastre Influenza A virus NS1 protein prevents activation of NF-kappaB and induction of alpha/beta interferon J. Virol. 74 2000 11566 11573
42. X. Wang, C.F. Basler, B.R. Williams, R.H. Silverman, P. Palese, and A. Garcia-Sastre Functional replacement of the carboxy-terminal two-thirds of the influenza A virus NS1 protein with short heterologous dimerization domains J. Virol. 76 2002 12951 12962
43. S. Weiss, D. Proske, M. Neumann, M.H. Groschup, H.A. Kretzschmar, M. Famulok, and E.L. Winnacker RNA aptamers specifically interact with the prion protein PrP J. Virol. 71 1997 8790 8797
44. M. Yoneyama, M. Kikuchi, T. Natsukawa, N. Shinobu, T. Imaizumi, M. Miyagishi, K. Taira, S. Akira, and T. Fujita The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses Nat. Immunol. 5 2004 730 737
45. M. Zuker Computer prediction of RNA structure Methods Enzymol. 180 1989 262 288
46. M. Zuker Mfold web server for nucleic acid folding and hybridization prediction Nucleic Acids Res. 31 2003 3406 3415