Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses

Journal of Virology

Volumn 80, Issue 10, 2006, Pages 5059-5064

  Weber, Friedemann ^a   Wagner, Valentina ^a   Rasmussen, Simon B ^b   Hartmann, Rune ^b   Paludan, Søren R ^b  

^a UNIVERSITY OF FREIBURG   (Germany)

^b AARHUS UNIVERSITY   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED DNA; DOUBLE STRANDED RNA;

ANIMAL CELL; ANTIBODY SPECIFICITY; ARTICLE; DNA VIRUS; GENOME ANALYSIS; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOFLUORESCENCE; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; RNA ANALYSIS; RNA VIRUS; VIRUS DETECTION; VIRUS DNA CELL DNA INTERACTION; VIRUS GENOME; VIRUS INFECTION; VIRUS REPLICATION;

ANIMALS; ANTIBODIES, MONOCLONAL; CERCOPITHECUS AETHIOPS; CRICETINAE; DNA VIRUSES; FLUORESCENT ANTIBODY TECHNIQUE; HELA CELLS; HUMANS; RNA VIRUSES; RNA, DOUBLE-STRANDED; VERO CELLS;

ANIMALIA; DNA VIRUSES; RNA VIRUSES;

EID: 33646453915     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.80.10.5059-5064.2006     Document Type: Article

References (74)

1. Ahmed, M., M. O. McKenzie, S. Puckett, M. Hojnacki, L. Poliquin, and D. S. Lyles. 2003. Ability of the matrix protein of vesicular stomatitis virus to suppress beta interferon gene expression is genetically correlated with the inhibition of host RNA and protein synthesis. J. Virol. 77:4646-4657.
2. Akira, S., and K. Takeda. 2004. Toll-like receptor signalling. Nat. Rev. Immunol. 4:499-511.
3. Alexopoulou, L., A. C. Holt, R. Medzhitov, and R. A. Flavell. 2001. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413:732-738.
4. Andrejeva, J., K. S. Childs, D. F. Young, T. S. Carlos, N. Stock, S. Goodbourn, and R. E. Randall. 2004. The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFN-beta promoter. Proc. Natl. Acad. Sci. USA 101:17264-17269.
5. Basler, C. F., A. Mikulasova, L. Martinez-Sobrido, J. Paragas, E. Muhlberger, M. Bray, H. D. Klenk, P. Palese, and A. Garcia-Sastre. 2003. The Ebola virus VP35 protein inhibits activation of interferon regulatory factor 3. J. Virol. 77:7945-7956.
6. Belov, G. A., A. G. Evstafieva, Y. P. Rubtsov, O. V. Mikilas, A. B. Vartapetian, and V. I. Agol. 2000. Early alteration of nucleocytoplasmic traffic induced by some RNA viruses. Virology 275:244-248.
7. Bergmann, M., A. Garcia-Sastre, E. Carnero, H. Pehamberger, K. Wolff, P. Palese, and T. Muster. 2000. Influenza virus NS1 protein counteracts PKR-mediated inhibition of replication. J. Virol. 74:6203-6206.
8. Beutler, B. 2004. Inferences, questions and possibilities in Toll-like receptor signalling. Nature 430:257-263.
9. Billecocq, A., M. Spiegel, P. Vialat, A. Kohl, F. Weber, M. Bouloy, and O. Haller. 2004. NSs protein of Rift Valley fever virus blocks interferon production by inhibiting host gene transcription. J. Virol. 78:9798-9806,
10. Black, B. L., and D. S. Lyles. 1992, Vesicular stomatitis virus matrix protein inhibits host cell-directed transcription of target genes in vivo. J. Virol. 66:4058-4064.
11. Bossert, B., S. Marozin, and K. K. Conzelmann. 2003. Nonstructural proteins NS1 and NS2 of bovine respiratory syncytial virus block activation of interferon regulatory factor 3. J. Virol. 77:8661-8668.
12. Brzózka, K., S. Finke, and K.-K. Conzelmann. 2005. Identification of the rabies virus alpha/beta interferon antagonist: phosphoprotein P interferes with phosphorylation of interferon regulatory factor 3. J. Virol. 79:7673-7681.
13. Diebold, S. S., T. Kaisho, H. Hemmi, S. Akira, and C. Reis e Sousa. 2004. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science 303:1529-1531.
14. Donelan, N. R., C. F. Basler, and A. Garcia-Sastre. 2003. 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. 77:13257-13266.
15. Falcon, A. M., R. M. Marion, T. Zurcher, P. Gomez, A. Portela, A. Nieto, and J. Ortin. 2004. Defective RNA replication and late gene expression in temperature-sensitive influenza viruses expressing deleted forms of the NS1 protein. J. Virol. 78:3880-3888,
16. Faria, P. A., P. Chakraborty, A. Levay, G. N. Barber, H. J. Ezelle, J. Enninga, C. Arana, J. van Deursen, and B. M. Fontoura. 2005. VSV disrupts the Rael/mrnp41 mRNA nuclear export pathway. Mol. Cell 17:93-102,
17. Ferran, M. C., and J. M. Lucas-Lenard. 1997. The vesicular stomatitis virus matrix protein inhibits transcription from the human beta interferon promoter. J. Virol. 71:371-377,
18. Garcia-Sastre, A. 2004. Identification and characterization of viral antagonists of type I interferon in negative-strand RNA viruses. Curr. Top. Microbiol. Immunol. 283:249-280.
19. Garcia-Sastre, A. 2001. Inhibition of interferon-mediated antiviral responses by influenza A viruses and other negative-strand RNA viruses. Virology 279:375-384.
20. Geiss, G., G. Jin, J. Guo, R. Bumgarner, M. G. Katze, and G. C. Sen. 2001. A comprehensive view of regulation of gene expression by double-stranded RNA-mediated cell signaling. J. Biol. Chem. 276:30178-30182,
21. Gustin, K. E. 2003. Inhibition of nucleo-cytoplasmic trafficking by RNA viruses: targeting the nuclear pore complex. Virus Res. 95:35-44.
22. Hatada, E., T. Takizawa, and R. Fukuda. 1992. Specific binding of influenza A virus NS1 protein to the virus minus-sense RNA in vitro. J. Gen. Virol. 73:17-25.
23. Hoyt, C. C., R. J. Bouchard, and K. L. Tyler. 2004. Novel nuclear herniations induced by nuclear localization of a viral protein. J. Virol. 78:6360-6369.
24. Ito, T., M. Yang, and W. S. May. 1999. RAX, a cellular activator for double-stranded RNA-dependent protein kinase during stress signaling. J. Biol. Chem. 274:15427-15432.
25. Jacobs, B. L., and J. O. Langland. 1996. When two strands are better than one: the mediators and modulators of the cellular responses to double-stranded RNA. Virology 219:339-349.
26. Jennings, S., L. Martinez-Sobrido, A. Garcia-Sastre, F. Weber, and G. Kochs. 2005. Thogoto virus ML protein suppresses IRF3 function. Virology 331:63-72.
27. Kallman, F., R. C. Williams, R. Dulbecco, and M. Vogt. 1958. Fine structure of changes produced in cultured cells sampled at specified intervals during a single growth cycle of polio virus. J. Biophys. Biochem. Cytol. 4:301-308.
28. Katze, M. G. 1995. Regulation of the interferon-induced PKR: can viruses cope? Trends Microbiol. 3:75-78.
29. Komatsu, T., K. Takeuchi, J. Yokoo, and B. Colon. 2004. C and V proteins of Sendai virus target signaling pathways leading to IRF-3 activation for the negative regulation of interferon-beta production. Virology 325:137-148.
30. Krug, R. M., W. Yuan, D. L. Noah, and A. G. Latham. 2003. Intracellular warfare between human influenza viruses and human cells: the roles of the viral NS1 protein. Virology 309:181-189.
31. Kumar, A., J. Haque, J. Lacoste, J. Hiscott, and B. R. Williams. 1994. Double-stranded RNA-dependent protein kinase activates transcription factor NF-kappa B by phosphorylating I kappa B. Proc. Natl. Acad. Sci, USA 91:6288-6292.
32. Kumar, M., and G. G. Carmichael. 1998. Antisense RNA: function and fate of duplex RNA in cells of higher eukaryotes. Microbiol. Mol. Biol. Rev. 62:1415-1434.
33. Lee, J. Y., J. A. Marshall, and D. S. Bowden. 1994. Characterization of rubella virus replication complexes using antibodies to double-stranded RNA. Virology 200:307-312.
34. Le May, N., S. Dubaele, L. P. De Santis, A. Billecocq, M. Bouloy, and J. M. Egly. 2004. TFIIH transcription factor, a target for the Rift Valley hemorrhagic fever virus. Cell 116:541-550.
35. Lloyd, R. M., and A. J. Shatkin. 1992. Translational stimulation by reovirus polypeptide σ3: substitution for VAI RNA and inhibition of phosphorylation of the α subunit of eukaryotic initiation factor 2. J. Virol. 66:6878-6884.
36. Lu, Y., M. Wambach, M. G. Katze, and R. M. Krug. 1995. Binding of the influenza virus NS1 protein to double-stranded RNA inhibits the activation of the protein kinase that phosphorylates the elF-2 translation initiation factor. Virology 214:222-228.
37. Lukacs, N. 1994. Detection of virus infection in plants and differentiation between coexisting viruses by monoclonal antibodies to double-stranded RNA. J. Virol. Methods 47:255-272.
38. Lund, J. M., L. Alexopoulou, A. Sato, M. Karow, N. C. Adams, N. W. Gale, A. Iwasaki, and R. A. Flavell. 2004. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc. Natl. Acad. Sci. USA 101:5598-5603.
39. Maitra, R. K., N. A. McMillan, S. Desai, J. McSwiggen, A. G. Hovanessian, G. Sen, B. R. Williams, and R. H. Silverman. 1994. HIV-1 TAR RNA has an intrinsic ability to activate interferon-inducible enzymes. Virology 204:823-827.
40. Majde, J. A. 2000. Viral double-stranded RNA, cytokines, and the flu. J. Interferon Cytokine Res. 20:259-272.
41. Majde, J. A., R. K. Brown, M. W. Jones, C. W. Dieffenbach, N. Maitra, J. M. Krueger, A. B. Cady, C. W. Smitka, and H. F. Maassab. 1991. Detection of toxic viral-associated double-stranded RNA (dsRNA) in influenza-infected lung. Microb. Pathog. 10:105-115.
42. Marcus, P. I., and M. J. Sekellick. 1977. Defective interfering particles with covalently linked [+/-]RNA induce interferon. Nature 266:815-819.
43. Mathews, M. B., and T. Shenk. 1991. Adenovirus virus-associated RNA and translation control. J. Virol. 65:5657-5662.
44. McCormack, S. J., and C. E. Samuel. 1995. Mechanism of interferon action: RNA-binding activity of full-length and R-domain forms of the RNA-dependent protein kinase PKR-determination of KD values for VAI and TAR RNAs. Virology 206:511-519.
45. Melchjorsen, J., S. B. Jensen, L. Malmgaard, S. B. Rasmussen, F. Weber, A. G. Bowie, S. Matikainen, and S. R. Paludan. 2005. Activation of innate defense against a paramyxovirus is mediated by RIG-I and TLR 7 and TLR 8 in a cell-type-specific manner. J. Virol. 79:12944-12951.
46. Mogensen, T. H., and S. R. Paludan. 2005. Reading the viral signature by Toll-like receptors and other pattern recognition receptors. J. Mol. Med. 83:180-192.
47. Patel, R. C., and G. C. Sen. 1998, PACT, a protein activator of the interferon-induced protein kinase, PKR. EMBO J. 17:4379-4390.
48. Rothenfusser, S., N. Goutagny, G. DiPerna, M. Gong, B. G. Monks, A. Schoenemeyer, M. Yamamoto, S. Akira, and K. A. Fitzgerald. 2005, The RNA helicase Lgp2 inhibits TLR-independent sensing of viral replication by retinoic acid-inducible gene-I. J. Immunol. 175:5260-5268.
49. Salonen, A., T. Ahola, and L. Kaariainen. 2005. Viral RNA replication in association with cellular membranes. Curr. Top. Microbiol. Immunol. 285:139-173.
50. Samuel, C. E. 2001. Antiviral actions of interferons. Clin. Microbiol. Rev. 14:778-809.
51. Schafer, S. L., R. Lin, P. A. Moore, J. Hiscott, and P. M. Pitha. 1998. Regulation of type I interferon gene expression by interferon regulatory factor-3. J. Biol. Chem. 273:2714-2720.
52. Schonborn, J., J. Oberstrass, E. Breyel, J. Tittgen, J. Schumacher, and N. Lukacs. 1991. Monoclonal antibodies to double-stranded RNA as probes of RNA structure in crude nucleic acid extracts. Nucleic Acids Res. 19:2993-3000.
53. Shaw, M. L., W. B. Cardenas, D. Zamarin, P. Palese, and C. F. Basler. 2005. Nuclear localization of the Nipah virus W protein allows for inhibition of both virus- and Toll-like receptor 3-triggered signaling pathways. J. Virol. 79:6078-6088.
54. Shors, S. T., E. Beattie, E. Paoletti, J. Tartaglia, and B. L. Jacobs. 1998. Role of the vaccinia virus E3L and K3L gene products in rescue of VSV and EMCV from the effects of IFN-alpha. J. Interferon Cytokine Res. 18:721-729.
55. Silverman, R. H. 1994. Fascination with 2-5A-dependent RNase: a unique enzyme that functions in interferon action. J. Interferon Res. 14:101-104.
56. Stojdl, D. F., B. Lichly, S. Knowles, R. Marius, H. Atkins, N. Sonenberg, and J. C. Bell. 2000. Exploiting tumor-specific defects in the interferon pathway with a previously unknown oncolytic virus. Nat. Med. 6:821-825.
57. Stollar, B. D., and V. Stollar. 1970. Immunofluorescent demonstration of double-stranded RNA in the cytoplasm of Sindbis virus-infected cells. Virology 42:276-280.
58. Streitenfeld, H., A. Boyd, J. K. Fazakerley, A. Bridgen, R. M. Elliott, and F. Weber. 2003. Activation of PKR by Bunyamwera virus is independent of the viral interferon antagonist NSs. J. Virol. 77:5507-5511.
59. Sumpter, R., Jr., Y. M. Loo, E. Foy, K. Li, M. Yoneyama, T. Fujita, S. M. Lemon, and M. Gale, Jr. 2005. Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J. Virol. 79:2689-2699.
60. Tabeta, K., P. Georgel, E. Janssen, X. Du, K. Hoebe, K. Crozat, S. Mudd, L. Shamel, S. Sovath, J. Goode, L. Alexopoulou, R. A. Flavell, and B. Beutler. 2004. Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. Proc. Natl. Acad. Sci. USA 101:3516-3521.
61. Takeda, K., and S. Akira. 2005. Toll-like receptors in innate immunity. Int. Immunol. 17:1-14.
62. tenOever, B. R., M. J. Servant, N. Grandvaux, R. Lin, and J. Hiscott. 2002. Recognition of the measles virus nucleocapsid as a mechanism of IRF-3 activation. J. Virol. 76:3659-3669.
63. tenOever, B. R., S. Sharma, W. Zou, Q. Sun, N. Grandvaux, I. Julkunen, H. Hemmi, M. Yamamoto, S. Akira, W. C. Yeh, R. Lin, and J. Hiscott. 2004. Activation of TBK1 and IKKε kinases by vesicular stomatitis virus infection and the role of viral ribonucleoprotein in the development of interferon antiviral immunity. J. Virol. 78:10636-10649.
64. Thomas, D., G. Blakqori, V. Wagner, M. Banholzer, N. Kessler, R. M. Elliott, O. Haller, and F. Weber. 2004. Inhibition of RNA polymerase II phosphorylation by a viral Interferon antagonist. J. Biol. Chem. 279:31471-31477.
65. Unterstab, G., S. Ludwig, A. Anton, O. Planz, B. Dauber, D. Krappmann, G. Heins, C. Ehrhardt, and T. Wolff. 2005. Viral targeting of the interferon-beta-inducing Traf family member-associated NF-κB activator (TANK)-binding kinase-1. Proc. Natl. Acad. Sci. USA 102:13640-13645.
66. Wang, Q., and G. G. Carmichael. 2004. Effects of length and location on the cellular response to double-stranded RNA. Microbiol. Mol. Biol. Rev. 68:432-452.
67. Weaver, B. K., K. P. Kumar, and N. C. Reich. 1998. Interferon regulatory factor 3 and CREB-binding protein/p300 are subunits of double-stranded RNA-activated transcription factor DRAF1. Mol. Cell. Biol. 18:1359-1368.
68. Weber, F., G. Kochs, and O. Haller. 2004. Inverse interference: how viruses fight the interferon system. Viral Immunol. 17:498-515.
69. Westaway, E. G., J. M. Mackenzie, M. T. Kenney, M. K. Jones, and A. A. Khromykh. 1997. Ultrastructure of Kunjin virus-infected cells: colocalization of NS1 and NS3 with double-stranded RNA, and of NS2B with NS3, in virus-induced membrane structures. J. Virol. 71:6650-6661.
70. Williams, B. R. 1999. PKR; a sentinel kinase for cellular stress. Oncogene 18:6112-6120.
71. Yoneyama, M., M. Kikuchi, K. Matsumoto, T. Imaizumi, M. Miyagishi, K. Taira, E. Foy, Y. M. Loo, M. Gale, Jr., S. Akira, S. Yonehara, A. Kato, and T. Fujita. 2005. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J. Immunol. 175:2851-2858.
72. Yoneyama, M., M. Kikuchi, T. Natsukawa, N. Shinobu, T. Imaizumi, M. Miyagishi, K. Taira, S. Akira, and T. Fujita. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5:730-737.
73. Yoneyama, M., W. Suhara, Y. Fukuhara, M. Fukuda, E. Nishida, and T. Fujita. 1998. Direct triggering of the type I interferon system by virus infection: activation of a transcription factor complex containing IRF-3 and CBP/p300. EMBO J. 17:1087-1095.
74. Zamanian-Daryoush, M., T. H. Mogensen, J. A. DiDonato, and B. R. Williams. 2000. NF-κB activation by double-stranded-RNA-activated protein kinase (PKR) is mediated through NF-κB-inducing kinase and IκB kinase. Mol. Cell. Biol. 20:1278-1290.