1887

Abstract

The vinegar fly, , is a popular model for the study of invertebrate antiviral immune responses. Several picorna-like viruses are commonly found in both wild and laboratory populations of . The best-studied and most pathogenic of these is the dicistrovirus Drosophila C virus. Among the uncharacterized small RNA viruses of , Drosophila A virus (DAV) is the least pathogenic. Historically, DAV has been labelled as a picorna-like virus based on its particle size and the content of its RNA genome. Here, we describe the characterization of both the genome and the virion structure of DAV. Unexpectedly, the DAV genome was shown to encode a circular permutation in the palm-domain motifs of the RNA-dependent RNA polymerase. This arrangement has only been described previously for a subset of viruses from the double-stranded RNA virus family and the =4 single-stranded RNA virus family . The 8 Å (0.8 nm) DAV virion structure computed from cryo-electron microscopy and image reconstruction indicates that the virus structural protein forms two discrete domains within the capsid. The inner domain is formed from a clear =3 lattice with similarity to the -sandwich domain of tomato bushy stunt virus, whilst the outer domain is not ordered icosahedrally, but forms a cage-like structure that surrounds the core domain. Taken together, this indicates that DAV is highly divergent from previously described viruses.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.012104-0
2009-09-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/90/9/2191.html?itemId=/content/journal/jgv/10.1099/vir.0.012104-0&mimeType=html&fmt=ahah

References

  1. Agrawal, D. K. & Johnson, J. E.(1992). Sequence and analysis of the capsid protein of Nudaurelia capensisω virus, an insect virus with T=4 icosahedral symmetry. Virology 190, 806–814.[CrossRef] [Google Scholar]
  2. Brun, G. & Plus, N.(1980). The viruses of Drosophila. In The Genetics and Biology of Drosophila, pp. 625–702. Edited by M. Ashburner & T. F. R. Wright. New York: Academic Press.
  3. Cherry, S. & Perrimon, N.(2004). Entry is a rate-limiting step for viral infection in a Drosophila melanogaster model of pathogenesis. Nat Immunol 5, 81–87. [Google Scholar]
  4. Cherry, S., Doukas, T., Armknecht, S., Whelan, S., Wang, H., Sarnow, P. & Perrimon, N.(2005). Genome-wide RNAi screen reveals a specific sensitivity of IRES-containing RNA viruses to host translation inhibition. Genes Dev 19, 445–452.[CrossRef] [Google Scholar]
  5. Christian, P. D.(1992). A simple vacuum dot-blot hybridisation assay for the detection of Drosophila A and C viruses in single Drosophila. J Virol Methods 38, 153–165.[CrossRef] [Google Scholar]
  6. Christian, P. D. & Scotti, P. D.(1998). The picorna-like viruses of insects. In The Viruses: Insect Viruses II, pp. 301–336. Edited by L. K. Miller & L. A. Ball. New York: Plenum.
  7. Christian, P. D., Carstens, E. B., Domier, L., Johnson, J. E., Johnson, K. N., Nakashima, N., Scotti, P. D. & van der Wilk, F.(2005).Dicistroviridae. In Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses, pp. 783–788. Edited by C. M. Fauquet, M. A. Mayo, J. Maniloff, U. Desselberger & L. A. Ball. San Diego, CA: Elsevier Academic Press.
  8. Deddouche, S., Matt, N., Budd, A., Mueller, S., Kemp, C., Galiana-Arnoux, D., Dostert, C., Antoniewski, C., Hoffmann, J. A. & Imler, J. L.(2008). The DExD/H-box helicase Dicer-2 mediates the induction of antiviral activity in Drosophila. Nat Immunol 9, 1425–1432.[CrossRef] [Google Scholar]
  9. Ding, S. W. & Voinnet, O.(2007). Antiviral immunity directed by small RNAs. Cell 130, 413–426.[CrossRef] [Google Scholar]
  10. Dormitzer, P. R., Nason, E. B., Prasad, B. V. & Harrison, S. C.(2004). Structural rearrangements in the membrane penetration protein of a non-enveloped virus. Nature 430, 1053–1058.[CrossRef] [Google Scholar]
  11. Dostert, C., Jouanguy, E., Irving, P., Troxler, L., Galiana-Arnoux, D., Hetru, C., Hoffmann, J. A. & Imler, J. L.(2005). The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of Drosophila. Nat Immunol 6, 946–953.[CrossRef] [Google Scholar]
  12. Fauquet, C. M., Mayo, M. A., Maniloff, J., Desselberger, U. & Ball, L. A. (editors)(2005).Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses. San Diego, CA: Academic Press.
  13. Galiana-Arnoux, D., Dostert, C., Schneemann, A., Hoffmann, J. A. & Imler, J. L.(2006). Essential function in vivo for Dicer-2 in host defense against RNA viruses in Drosophila. Nat Immunol 7, 590–597.[CrossRef] [Google Scholar]
  14. Garriga, D., Navarro, A., Querol-Audi, J., Abaitua, F., Rodriguez, J. F. & Verdaguer, N.(2007). Activation mechanism of a noncanonical RNA-dependent RNA polymerase. Proc Natl Acad Sci U S A 104, 20540–20545.[CrossRef] [Google Scholar]
  15. Gateff, E., Gissmann, L., Shrestha, R., Plus, N., Pfister, H., Schröder, J. & Zur Hausen, H.(1980). Characterization of two tumorous blood cell lines of Drosophila melanogaster and the viruses they contain. In Invertebrate Systems In Vitro, pp. 517–533. Edited by E. Kurstak, K. Maramorosch & F. Dübendorfer. Amsterdam: Elsevier/North-Holland Biomedical Press.
  16. Ginalski, K., Elofsson, A., Fischer, D. & Rychlewski, L.(2003). 3D-Jury: a simple approach to improve protein structure predictions. Bioinformatics 19, 1015–1018.[CrossRef] [Google Scholar]
  17. Gorbalenya, A. E., Pringle, F. M., Zeddam, J. L., Luke, B. T., Cameron, C. E., Kalmakoff, J., Hanzlik, T. N., Gordon, K. H. & Ward, V. K.(2002). The palm subdomain-based active site is internally permuted in viral RNA-dependent RNA polymerases of an ancient lineage. J Mol Biol 324, 47–62.[CrossRef] [Google Scholar]
  18. Gordon, K. H. J. & Hanzlik, T. N.(1998). Tetraviruses. In The Viruses: Insect Viruses II, pp. 269–299. Edited by L. K. Miller & L. A. Ball. New York: Plenum.
  19. Gordon, K. H. J., Johnson, K. N. & Hanzlik, T. N.(1995). The larger genomic RNA of Helicoverpa armigera stunt tetravirus encodes the viral RNA polymerase and has a novel 3′-terminal tRNA-like structure. Virology 208, 84–98.[CrossRef] [Google Scholar]
  20. Gordon, K. H., Williams, M. R., Hendry, D. A. & Hanzlik, T. N.(1999). Sequence of the genomic RNA of Nudaurelia beta virus (Tetraviridae) defines a novel virus genome organization. Virology 258, 42–53.[CrossRef] [Google Scholar]
  21. Habayeb, M. S., Ekengren, S. K. & Hultmark, D.(2006). Nora virus, a persistent virus in Drosophila, defines a new picorna-like virus family. J Gen Virol 87, 3045–3051.[CrossRef] [Google Scholar]
  22. Hanzlik, T. N., Dorrian, S. J., Johnson, K. N., Brooks, E. M. & Gordon, K. H. J.(1995). Sequence of RNA2 of the Helicoverpa armigera stunt virus (Tetraviridae) and bacterial expression of its genes. J Gen Virol 76, 799–811.[CrossRef] [Google Scholar]
  23. Hartley, C. J., Greenwood, D. R., Gilbert, R. J., Masoumi, A., Gordon, K. H., Hanzlik, T. N., Fry, E. E., Stuart, D. I. & Scotti, P. D.(2005). Kelp fly virus: a novel group of insect picorna-like viruses as defined by genome sequence analysis and a distinctive virion structure. J Virol 79, 13385–13398.[CrossRef] [Google Scholar]
  24. Hedges, L. M. & Johnson, K. N.(2008). The induction of host defence responses by Drosophila C virus. J Gen Virol 89, 1497–1501.[CrossRef] [Google Scholar]
  25. Hedges, L. M., Brownlie, J. C., O'Neill, S. L. & Johnson, K. N.(2008).Wolbachia and virus protection in insects. Science 322, 702[CrossRef] [Google Scholar]
  26. Huszar, T. & Imler, J. L.(2008).Drosophila viruses and the study of antiviral host-defense. Adv Virus Res 72, 227–265. [Google Scholar]
  27. Johnson, K. N. & Ball, L. A.(2003). Virions of Pariacoto virus contain a minor protein translated from the second AUG codon of the capsid protein open reading frame. J Gen Virol 84, 2847–2852.[CrossRef] [Google Scholar]
  28. Johnson, K. N. & Christian, P. D.(1998). The novel genome organization of the insect picorna-like virus Drosophila C virus suggests this virus belongs to a previously undescribed virus family. J Gen Virol 79, 191–203. [Google Scholar]
  29. Johnson, J. E. & Reddy, V.(1998). Structural studies of nodaviruses and tetraviruses. In The Insect Viruses, pp. 171–223. Edited by L. K. Miller & L. A. Ball. New York: Plenum.
  30. Johnson, K. N., Johnson, K. L., Dasgupta, R., Gratsch, T. & Ball, L. A.(2001). Comparisons among the larger genome segments of six nodaviruses and their encoded RNA replicases. J Gen Virol 82, 1855–1866. [Google Scholar]
  31. Jousset, F. X. & Plus, N.(1975). Étude de la transmission horizontale et de la transmission verticale des picornavirus de Drosophila melanogaster et de Drosophila immigrans. Ann Microbiol (Paris) 126, 231–249 (in French). [Google Scholar]
  32. Jousset, F. X., Plus, N., Croizier, G. & Thomas, M.(1972). Existence chez Drosophila de deux groupes de picornavirus de propriétés sérologiques et biologiques différentes. C R Acad Sci Hebd Seances Acad Sci D 275, 3043–3046 (in French). [Google Scholar]
  33. Koonin, E. V., Wolf, Y. I., Nagasaki, K. & Dolja, V. V.(2008). The big bang of picorna-like virus evolution antedates the radiation of eukaryotic supergroups. Nat Rev Microbiol 6, 925–939.[CrossRef] [Google Scholar]
  34. Lander, G. C., Stagg, S., Voss, N. R., Cheng, A., Fellmann, D., Pulokas, J., Yoshioka, C., Irving, C., Mulder, A. & other authors(2009). Appion: an integrated, database-driven pipeline to facilitate EM image processing. J Struct Biol 166, 95–102.[CrossRef] [Google Scholar]
  35. Ludtke, S. J., Baldwin, P. R. & Chiu, W.(1999).eman: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128, 82–97.[CrossRef] [Google Scholar]
  36. Mallick, S. P., Carragher, B., Potter, C. S. & Kriegman, D. J.(2005).ace: automated CTF estimation. Ultramicroscopy 104, 8–29.[CrossRef] [Google Scholar]
  37. Plus, N.(1978). Endogenous viruses of Drosophila melanogaster cell lines: their frequency, identification and origin. In Vitro Cell Dev Biol Plant 14, 1015–1021.[CrossRef] [Google Scholar]
  38. Plus, N., Croizier, G., Jousset, F. X. & David, J.(1975). Picornaviruses of laboratory and wild Drosophila melanogaster: geographical distribution and serotypic composition. Ann Microbiol (Paris) 126, 107–117. [Google Scholar]
  39. Plus, N., Croizier, G., Veyrunes, J. & David, J.(1976). A comparison of buoyant density and polypeptides of Drosophila P, C and A viruses. Intervirology 7, 346–350.[CrossRef] [Google Scholar]
  40. Poch, O., Sauvaget, I., Delarue, M. & Tordo, N.(1989). Identification of four conserved motifs among the RNA-dependent polymerase encoding elements. EMBO J 8, 3867–3874. [Google Scholar]
  41. Pringle, F. M., Kalmakoff, J. & Ward, V. K.(2001). Analysis of the capsid processing strategy of Thosea asigna virus using baculovirus expression of virus-like particles. J Gen Virol 82, 259–266. [Google Scholar]
  42. Pringle, F. M., Johnson, K. N., Goodman, C. L., McIntosh, A. H. & Ball, L. A.(2003).Providence virus: a new member of the Tetraviridae that infects cultured insect cells. Virology 306, 359–370.[CrossRef] [Google Scholar]
  43. Roseman, A. M.(2003). Particle finding in electron micrographs using a fast local correlation algorithm. Ultramicroscopy 94, 225–236.[CrossRef] [Google Scholar]
  44. Roxstrom-Lindquist, K., Terenius, O. & Faye, I.(2004). Parasite-specific immune response in adult Drosophila melanogaster: a genomic study. EMBO Rep 5, 207–212.[CrossRef] [Google Scholar]
  45. Sabatier, L., Jouanguy, E., Dostert, C., Zachary, D., Dimarcq, J. L., Bulet, P. & Imler, J. L.(2003). Pherokine-2 and -3. Eur J Biochem 270, 3398–3407.[CrossRef] [Google Scholar]
  46. Schneider, I.(1972). Cell lines derived from late embryonic stages of Drosophila melanogaster. J Embryol Exp Morphol 27, 353–365. [Google Scholar]
  47. Sousa, D. & Grigorieff, N.(2007).Ab initio resolution measurement for single particle structures. J Struct Biol 157, 201–210.[CrossRef] [Google Scholar]
  48. Suloway, C., Pulokas, J., Fellmann, D., Cheng, A., Guerra, F., Quispe, J., Stagg, S., Potter, C. S. & Carragher, B.(2005). Automated molecular microscopy: the new Leginon system. J Struct Biol 151, 41–60.[CrossRef] [Google Scholar]
  49. Tang, L., Johnson, K. N., Ball, L. A., Lin, T., Yeager, M. & Johnson, J. E.(2001). The structure of Pariacoto virus reveals a dodecahedral cage of duplex RNA. Nat Struct Biol 8, 77–83.[CrossRef] [Google Scholar]
  50. Tang, L., Lin, C. S., Krishna, N. K., Yeager, M., Schneemann, A. & Johnson, J. E.(2002). Virus-like particles of a fish nodavirus display a capsid subunit domain organization different from that of insect nodaviruses. J Virol 76, 6370–6375.[CrossRef] [Google Scholar]
  51. Tate, J., Liljas, L., Scotti, P., Christian, P., Lin, T. & Johnson, J. E.(1999). The crystal structure of cricket paralysis virus: the first view of a new virus family. Nat Struct Biol 6, 765–774.[CrossRef] [Google Scholar]
  52. Teixeira, L., Ferreira, A. & Ashburner, M.(2008). The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6, e2 [Google Scholar]
  53. van der Wilk, F., Dullemans, A. M., Verbeek, M. & Van den Heuvel, J. F.(1997). Nucleotide sequence and genomic organization of Acyrthosiphon pisum virus. Virology 238, 353–362.[CrossRef] [Google Scholar]
  54. van Rij, R. P., Saleh, M. C., Berry, B., Foo, C., Houk, A., Antoniewski, C. & Andino, R.(2006). The RNA silencing endonuclease Argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster. Genes Dev 20, 2985–2995.[CrossRef] [Google Scholar]
  55. Venter, P. A., Marshall, D. & Schneemann, A.(2009). Dual roles for an arginine-rich motif in specific genome recognition and localization of viral coat protein to RNA replication sites in flock house virus-infected cells. J Virol 83, 2872–2882.[CrossRef] [Google Scholar]
  56. Zambon, R. A., Nandakumar, M., Vakharia, V. N. & Wu, L. P.(2005). The Toll pathway is important for an antiviral response in Drosophila. Proc Natl Acad Sci U S A 102, 7257–7262.[CrossRef] [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.012104-0
Loading
/content/journal/jgv/10.1099/vir.0.012104-0
Loading

Data & Media loading...

Supplements

vol. , part 9, pp. 2191–2200

Alignment of RdRP showing C–A–B arrangement of RdRP motifs.

Alignment of deduced capsid protein sequence of DAV with those of other RNA viruses.

[ Single PDF file] (142 KB)



PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error