Coxsackievirus cloverleaf RNA containing a 5′ triphosphate triggers an antiviral response via RIG-I activation

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Feng, Qian ^a   Langereis, Martijn A ^a   Olagnier, David ^b   Chiang, Cindy ^b   Van De Winkel, Roel ^c   Van Essen, Peter ^c   Zoll, Jan ^c   Hiscott, John ^b   Van Kuppeveld, Frank J M ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b Vaccine and Gene Therapy Institute of Florida   (United States)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

5' TRIPHOSPHATE; ALPHA INTERFERON; ANTIVIRUS AGENT; BETA INTERFERON; CLOVERLEAF RNA; CYTOKINE; HYDROLASE; PATTERN RECOGNITION RECEPTOR; PROTEIN MDA5; RETINOIC ACID INDUCIBLE PROTEIN I; UNCLASSIFIED DRUG; VIRUS RNA; 5'PPP-RNA; DEAD BOX PROTEIN; POLYPHOSPHATE; RETINOIC ACID RECEPTOR; TRIPHOSPHORIC ACID;

AMINO ACID SEQUENCE; ANTIVIRAL ACTIVITY; ARTICLE; CELL PROTECTION; COMPLEX FORMATION; CONTROLLED STUDY; COXSACKIE VIRUS B3; DENGUE VIRUS; ENTEROVIRUS 71; IMMUNE RESPONSE; IMMUNOREGULATION; IN VITRO STUDY; INFECTION PREVENTION; INFECTION RESISTANCE; NONHUMAN; PROTEIN DOMAIN; PROTEIN RNA BINDING; RNA ANALYSIS; RNA STRUCTURE; RNA TRANSCRIPTION; SIGNAL TRANSDUCTION; VESICULAR STOMATITIS VIRUS; VIRUS GENOME; ANIMAL; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; CYTOLOGY; FIBROBLAST; GENETICS; HELA CELL LINE; HUMAN; IMMUNOLOGY; METABOLISM; MOUSE; PICORNAVIRIDAE; RNA VIRUS INFECTIONS; VIROLOGY;

ANIMALS; ANTIVIRAL AGENTS; CELL LINE; CYTOKINES; DEAD-BOX RNA HELICASES; FIBROBLASTS; HELA CELLS; HUMANS; MICE; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PICORNAVIRIDAE; POLYPHOSPHATES; RECEPTORS, RETINOIC ACID; RNA VIRUS INFECTIONS; RNA, VIRAL;

EID: 84899736643     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095927     Document Type: Article

References (30)

1. Kato H, Takahasi K, Fujita T (2011) RIG-I-like receptors: cytoplasmic sensors for non-self RNA. Immunol Rev 243: 91-98.
2. Goubau D, Deddouche S, Reis E Sousa C (2013) Cytosolic sensing of viruses. Immunity 38: 855-869.
3. Schlee M (2013) Master sensors of pathogenic RNA - RIG-I like receptors. Immunobiology 218: 1322-1335.
4. Stackaruk ML, Lee AJ, Ashkar AA (2013) Type I interferon regulation of natural killer cell function in primary and secondary infections. Expert Rev Vaccines 12: 875-884.
5. Chen Y-L, Chen T-T, Pai L-M, Wesoly J, Bluyssen HAR, et al. (2013) A type I IFN-Flt3 ligand axis augments plasmacytoid dendritic cell development from common lymphoid progenitors. J Exp Med 210: 2515-2522.
6. Ploss A, Dubuisson J (2012) New advances in the molecular biology of hepatitis C virus infection: towards the identification of new treatment targets. Gut 61 Suppl 1: i25-35.
7. Dogan UB, Golge N, Akin MS (2013) The comparison of the efficacy of pegylated interferon α-2a and α-2b in chronic hepatitis B patients. Eur J Gastroenterol Hepatol 25: 1312-1316.
8. Sleijfer S, Bannink M, Van Gool AR, Kruit WHJ, Stoter G (2005) Side effects of interferon-alpha therapy. Pharm World Sci 27: 423-431.
9. Zhao T, Wu X, Song D, Fang M, Guo S, et al. (2012) Effect of prophylactically applied CpG ODN on the development of myocarditis in mice infected with Coxsackievirus B3. Int Immunopharmacol 14: 665-673.
10. McCaskill JL, Marsh GA, Monaghan P, Wang L-F, Doran T, et al. (2013) Potent inhibition of Hendra virus infection via RNA interference and poly I:C immune activation. PLoS One 8: e64360.
11. Rodríguez-Pulido M, Borrego B, Sobrino F, Sáiz M (2011) RNA structural domains in noncoding regions of the foot-and-mouth disease virus genome trigger innate immunity in porcine cells and mice. J Virol 85: 6492-6501.
12. Martínez-Gil L, Goff PH, Hai R, García-Sastre A, Shaw ML, et al. (2013) A Sendai virus-derived RNA agonist of RIG-I as a virus vaccine adjuvant. J Virol 87: 1290-1300.
13. Goulet M-L, Olagnier D, Xu Z, Paz S, Belgnaoui SM, et al. (2013) Systems Analysis of a RIG-I Agonist Inducing Broad Spectrum Inhibition of Virus Infectivity. PLoS Pathog 9: e1003298.
14. Schlee M, Roth A, Hornung V, Hagmann CA, Wimmenauer V, et al. (2009) Recognition of 5 9 triphosphate by RIG-I helicase requires short blunt double-stranded RNA as contained in panhandle of negative-strand virus. Immunity 31: 25-34.
15. Binder M, Eberle F, Seitz S, Mücke N, Hüber CM, et al. (2011) Molecular mechanism of signal perception and integration by the innate immune sensor retinoic acid-inducible gene-I (RIG-I). J Biol Chem 286: 27278-27287.
16. Samanta M, Iwakiri D, Kanda T, Imaizumi T, Takada K (2006) EB virus-encoded RNAs are recognized by RIG-I and activate signaling to induce type I IFN. EMBO J 25: 4207-4214. (Pubitemid 44435218)
17. Plumet S, Herschke F, Bourhis J-M, Valentin H, Longhi S, et al. (2007) Cytosolic 5′-triphosphate ended viral leader transcript of measles virus as activator of the RIG I-mediated interferon response. PLoS One 2: e279.
18. Saito T, Owen DM, Jiang F, Marcotrigiano J, Gale Jr M (2008) Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature 454: 523-527.
19. Cheong HK, Cheong C, Choi BS (1996) Secondary structure of the panhandle RNA of influenza virus A studied by NMR spectroscopy. Nucleic Acids Res 24: 4197-4201. (Pubitemid 26377335)
20. Glickman JN, Howe JG, Steitz JA (1988) Structural analyses of EBER1 and EBER2 ribonucleoprotein particles present in Epstein-Barr virus-infected cells. J Virol 62: 902-911. (Pubitemid 18068649)
21. Feng Q, Hato S V, Langereis MA, Zoll J, Virgen-Slane R, et al. (2012) MDA5 detects the double-stranded RNA replicative form in picornavirus-infected cells. Cell Rep 2: 1187-1196.
22. Wimmer E, Hellen CU, Cao X (1993) Genetics of poliovirus. Annu Rev Genet 27: 353-436. (Pubitemid 24011358)
23. Witwer C, Rauscher S, Hofacker IL, Stadler PF (2001) Conserved RNA secondary structures in Picornaviridae genomes. Nucleic Acids Res 29: 5079-5089. (Pubitemid 34065425)
24. Schmidt A, Schwerd T, Hamm W, Hellmuth JC, Cui S, et al. (2009) 5′-triphosphate RNA requires base-paired structures to activate antiviral signaling via RIG-I. Proc Natl Acad Sci U S A 106: 12067-12072.
25. Hornung V, Ellegast J, Kim S, Brzózka K, Jung A, et al. (2006) 5′-Triphosphate RNA is the ligand for RIG-I. Science 314: 994-997.
26. Klump WM, Bergmann I, Müller BC, Ameis D, Kandolf R (1990) Complete nucleotide sequence of infectious Coxsackievirus B3 cDNA: two initial 5′ uridine residues are regained during plus-strand RNA synthesis. J Virol 64: 1573-1583. (Pubitemid 20104893)
27. Kato H, Sato S, Yoneyama M, Yamamoto M, Uematsu S, et al. (2005) Cell type-specific involvement of RIG-I in antiviral response. Immunity 23: 19-28. (Pubitemid 41019654)
28. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, et al. (2006) Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441: 101-105.
29. Kumar H, Kawai T, Kato H, Sato S, Takahashi K, et al. (2006) Essential role of IPS-1 in innate immune responses against RNA viruses. J Exp Med 203: 1795-1803. (Pubitemid 44036284)
30. Olagnier D, Scholte FEM, Chiang C, Albulescu IC, Nichols C, et al. (2014) Inhibition of dengue and chikungunya virus infection by RIG-I-mediated type I IFN-independent stimulation of the innate antiviral response. J Virol 88: 4180-4194.