1887

Abstract

The members of the family are small positive-sense insect RNA viruses that exhibit stringent host specificity and a high degree of tissue tropism, suggesting that complex virus–host interactions are likely to occur during infection and viral replication. The alpha-like replicase of stunt virus (HaSV) (genus ) has been proposed to associate with membranes of the endocytic pathway, which is similar to Semliki Forest virus, Sindbis virus and rubella virus. Here, we have used replicase–EGFP fusion proteins and recombinant baculovirus expression to demonstrate that the HaSV replicase associates strongly with cellular membranes, including detergent-resistant membranes, and that this association is maintained through a novel membrane targeting domain within the C-terminal region of the RNA-dependent RNA polymerase domain. We show a similar subcellular localization and strong association with detergent-resistant membranes for the carmo-like replicase of another tetravirus, Providence virus, in replicating cells, suggesting a common site of replication for these two tetraviruses.

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2012-08-01
2019-10-23
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References

  1. Ambrose R. L., Lander G. C., Maaty W. S., Bothner B., Johnson J. E., Johnson K. N.. ( 2009;). Drosophila A virus is an unusual RNA virus with a T = 3 icosahedral core and permuted RNA-dependent RNA polymerase. . J Gen Virol 90:, 2191–2200. [CrossRef][PubMed]
    [Google Scholar]
  2. Anderson R. G. W., Jacobson K.. ( 2002;). A role for lipid shells in targeting proteins to caveolae, rafts, and other lipid domains. . Science 296:, 1821–1825. [CrossRef][PubMed]
    [Google Scholar]
  3. Banerjee M., Speir J. A., Johnson J. E.. ( 2010;). Structural comparison of insect RNA viruses. . In Insect Virology, pp. 327–346. Edited by Asgari S., Johnson K... Norfolk, UK:: Caister Academic Press;.
    [Google Scholar]
  4. Bawden A. L., Gordon K. H. J., Hanzlik T. N.. ( 1999;). The specificity of Helicoverpa armigera stunt virus infectivity. . J Invertebr Pathol 74:, 156–163. [CrossRef][PubMed]
    [Google Scholar]
  5. Berditchevski F.. ( 2001;). Complexes of tetraspanins with integrins: more than meets the eye. . J Cell Sci 114:, 4143–4151.[PubMed]
    [Google Scholar]
  6. Blachly-Dyson E., Zambronicz E. B., Yu W. H., Adams V., McCabe E. R. B., Adelman J., Colombini M., Forte M.. ( 1993;). Cloning and functional expression in yeast of two human isoforms of the outer mitochondrial membrane channel, the voltage-dependent anion channel. . J Biol Chem 268:, 1835–1841.[PubMed]
    [Google Scholar]
  7. Brooks E. M., Gordon K. H. J., Dorrian S. J., Hines E. R., Hanzlik T. N.. ( 2002;). Infection of its lepidopteran host by the Helicoverpa armigera stunt virus (Tetraviridae). . J Invertebr Pathol 80:, 97–111. [CrossRef][PubMed]
    [Google Scholar]
  8. Christian P. D., Dorrian S. J., Gordon K. H. J., Hanzlik T. N.. ( 2001;). Pathology and properties of the tetravirus Helicoverpa armigera stunt virus. . Biol Control 20:, 65–75. [CrossRef]
    [Google Scholar]
  9. Claas C., Stipp C. S., Hemler M. E.. ( 2001;). Evaluation of prototype transmembrane 4 superfamily protein complexes and their relation to lipid rafts. . J Biol Chem 276:, 7974–7984. [CrossRef][PubMed]
    [Google Scholar]
  10. Dorrington R. A., Short J. R.. ( 2010;). The tetraviruses. . In Insect Virology, pp. 283–306. Edited by Asgari S., Johnson K... Norfolk, UK:: Caister Academic Press;.
    [Google Scholar]
  11. Dorrington R. A., Gorbalenya A. E., Gordon K. H. J., Lauber C., Ward V. K.. ( 2011;). Tetraviridae. . In Virus Taxonomy: Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses, pp. 1091–1102. Edited by King A. M. Q., Adams M. J., Carstens E. B., Lefkowitz E. J... San Diego:: Elsevier;.
    [Google Scholar]
  12. Froshauer S., Kartenbeck J., Helenius A.. ( 1988;). Alphavirus RNA replicase is located on the cytoplasmic surface of endosomes and lysosomes. . J Cell Biol 107:, 2075–2086. [CrossRef][PubMed]
    [Google Scholar]
  13. Gey G. O., Coffman W. D., Kubicek M. T.. ( 1952;). Tissue culture studies of the proliferative capacity of cervical carcinoma and normal epithelium. . Cancer Res 12:, 264.
    [Google Scholar]
  14. Gorbalenya A. E., Pringle F. M., Zeddam J.-L., Luke B. T., Cameron C. E., Kalmakoff J., Hanzlik T. N., Gordon K. H. J., 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][PubMed]
    [Google Scholar]
  15. 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][PubMed]
    [Google Scholar]
  16. Gordon K. H. J., Williams M. R., Hendry D. A., Hanzlik T. N.. ( 1999;). Sequence of the genomic RNA of Nudaurelia β virus (Tetraviridae) defines a novel virus genome organization. . Virology 258:, 42–53. [CrossRef][PubMed]
    [Google Scholar]
  17. Johannes L., Lamaze C.. ( 2002;). Clathrin-dependent or not: is it still the question?. Traffic 3:, 443–451. [CrossRef][PubMed]
    [Google Scholar]
  18. Koonin E. V.. ( 1991;). The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. . J Gen Virol 72:, 2197–2206. [CrossRef][PubMed]
    [Google Scholar]
  19. Kurzchalia T. V., Parton R. G.. ( 1999;). Membrane microdomains and caveolae. . Curr Opin Cell Biol 11:, 424–431. [CrossRef][PubMed]
    [Google Scholar]
  20. Levy S., Shoham T.. ( 2005;). The tetraspanin web modulates immune-signalling complexes. . Nat Rev Immunol 5:, 136–148. [CrossRef][PubMed]
    [Google Scholar]
  21. MacPherson I. A., Stoker M.. ( 1962;). Polyoma transformation of hamster cell clones–an investigation of genetic factors affecting cell competence. . Virology 16:, 147–151. [CrossRef][PubMed]
    [Google Scholar]
  22. Magliano D., Marshall J. A., Bowden D. S., Vardaxis N., Meanger J., Lee J.-Y.. ( 1998;). Rubella virus replication complexes are virus-modified lysosomes. . Virology 240:, 57–63. [CrossRef][PubMed]
    [Google Scholar]
  23. Matthews J. D., Tzeng W.-P., Frey T. K.. ( 2009;). Determinants of subcellular localization of the rubella virus nonstructural replicase proteins. . Virology 390:, 315–323. [CrossRef][PubMed]
    [Google Scholar]
  24. Mayor S., Pagano R. E.. ( 2007;). Pathways of clathrin-independent endocytosis. . Nat Rev Mol Cell Biol 8:, 603–612. [CrossRef][PubMed]
    [Google Scholar]
  25. Moffat K., Howell G., Knox C., Belsham G. J., Monaghan P., Ryan M. D., Wileman T.. ( 2005;). Effects of foot-and-mouth disease virus nonstructural proteins on the structure and function of the early secretory pathway: 2BC but not 3A blocks endoplasmic reticulum-to-Golgi transport. . J Virol 79:, 4382–4395. [CrossRef][PubMed]
    [Google Scholar]
  26. Pelkmans L., Helenius A.. ( 2003;). Insider information: what viruses tell us about endocytosis. . Curr Opin Cell Biol 15:, 414–422. [CrossRef][PubMed]
    [Google Scholar]
  27. Pelkmans L., Kartenbeck J., Helenius A.. ( 2001;). Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. . Nat Cell Biol 3:, 473–483. [CrossRef][PubMed]
    [Google Scholar]
  28. 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][PubMed]
    [Google Scholar]
  29. Sabanadzovic S., Ghanem-Sabanadzovic N. A., Gorbalenya A. E.. ( 2009;). Permutation of the active site of putative RNA-dependent RNA polymerase in a newly identified species of plant alpha-like virus. . Virology 394:, 1–7. [CrossRef][PubMed]
    [Google Scholar]
  30. Sandvig K., Torgersen M. L., Raa H. A., van Deurs B.. ( 2008;). Clathrin-independent endocytosis: from nonexisting to an extreme degree of complexity. . Histochem Cell Biol 129:, 267–276. [CrossRef][PubMed]
    [Google Scholar]
  31. Short J. R.. ( 2010;). An investigation into the replication biology of Helicoverpa armigera stunt virus. PhD thesis. . Rhodes University, Grahamstown, South Africa.
    [Google Scholar]
  32. Short J. R., Knox C., Dorrington R. A.. ( 2010;). Subcellular localization and live-cell imaging of the Helicoverpa armigera stunt virus replicase in mammalian and Spodoptera frugiperda cells. . J Gen Virol 91:, 1514–1523. [CrossRef][PubMed]
    [Google Scholar]
  33. Simons K., Ikonen E.. ( 1997;). Functional rafts in cell membranes. . Nature 387:, 569–572. [CrossRef][PubMed]
    [Google Scholar]
  34. Spuul P., Balistreri G., Kääriäinen L., Ahola T.. ( 2010;). Phosphatidylinositol 3-kinase-, actin-, and microtubule-dependent transport of Semliki Forest virus replication complexes from the plasma membrane to modified lysosomes. . J Virol 84:, 7543–7557. [CrossRef][PubMed]
    [Google Scholar]
  35. Thomsen P., Roepstorff K., Stahlhut M., van Deurs B.. ( 2002;). Caveolae are highly immobile plasma membrane microdomains, which are not involved in constitutive endocytic trafficking. . Mol Biol Cell 13:, 238–250. [CrossRef][PubMed]
    [Google Scholar]
  36. Tomasicchio M., Venter P. A., Gordon K. H. J., Hanzlik T. N., Dorrington R. A.. ( 2007;). Induction of apoptosis in Saccharomyces cerevisiae results in the spontaneous maturation of tetravirus procapsids in vivo. . J Gen Virol 88:, 1576–1582. [CrossRef][PubMed]
    [Google Scholar]
  37. Vaughn J. L., Goodwin R. H., Tompkins G. J., McCawley P.. ( 1977;). The establishment of two cell lines from the insect Spodoptera frugiperda (Lepidoptera; Noctuidae). . In Vitro 13:, 213–217. [CrossRef][PubMed]
    [Google Scholar]
  38. Walter C. T.. ( 2008;). Establishment of experimental systems for studying the replication biology of Providence virus. PhD thesis, Rhodes University. .
  39. Walter C. T., Pringle F. M., Nakayinga R., de Felipe P., Ryan M. D., Ball L. A., Dorrington R. A.. ( 2010;). Genome organization and translation products of Providence virus: insight into a unique tetravirus. . J Gen Virol 91:, 2826–2835. [CrossRef][PubMed]
    [Google Scholar]
  40. Yi F., Zhang J., Yu H., Liu C., Wang J., Hu Y.. ( 2005;). Isolation and identification of a new tetravirus from Dendrolimus punctatus larvae collected from Yunnan Province, China. . J Gen Virol 86:, 789–796. [CrossRef][PubMed]
    [Google Scholar]
  41. Zeddam J.-L., Gordon K. H. J., Lauber C., Alves C. A., Luke B. T., Hanzlik T. N., Ward V. K., Gorbalenya A. E.. ( 2010;). Euprosterna elaeasa virus genome sequence and evolution of the Tetraviridae family: emergence of bipartite genomes and conservation of the VPg signal with the dsRNA Birnaviridae family. . Virology 397:, 145–154. [CrossRef][PubMed]
    [Google Scholar]
  42. Zheng Y. Z., Foster L. J.. ( 2009;). Biochemical and proteomic approaches for the study of membrane microdomains. . J Proteomics 72:, 12–22. [CrossRef][PubMed]
    [Google Scholar]
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