1887

Abstract

virus (RGV) is a pathogenic iridovirus that has resulted in high mortality in cultured frog. Here, an envelope protein gene, , was identified from RGV and its possible role in virus infection was investigated. Database searches found that RGV had homologues in all sequenced iridoviruses and is a core gene of iridoviruses. Western blotting detection of purified RGV virions confirmed that 2L protein was associated with virion membrane. Fluorescence localization revealed that 2L protein co-localized with viral factories in RGV infected cells. In co-transfected cells, 2L protein co-localized with two other viral envelope proteins, 22R and 53R. However, 2L protein did not co-localize with the major capsid protein of RGV in co-transfected cells. Meanwhile, fluorescence observation showed that 2L protein co-localized with endoplasmic reticulum, but did not co-localize with mitochondria and Golgi apparatus. Moreover, a conditional lethal mutant virus containing the repressor/operator system was constructed to investigate the role of RGV 2L in virus infection. The ability to form plaques and the virus titres were strongly reduced when expression of 2L was repressed. Therefore, the current data showed that 2L protein is essential for virus infection. Our study is the first report, to our knowledge, of co-localization between envelope proteins in iridovirus and provides new insights into the understanding of envelope proteins in iridovirus.

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2014-03-01
2024-04-20
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References

  1. Ao J., Chen X. 2006; Identification and characterization of a novel gene encoding an RGD-containing protein in large yellow croaker iridovirus. Virology 355:213–222 [View Article][PubMed]
    [Google Scholar]
  2. Becker M. M., Peters T. R., Dermody T. S. 2003; Reovirus sigma NS and mu NS proteins form cytoplasmic inclusion structures in the absence of viral infection. J Virol 77:5948–5963 [View Article][PubMed]
    [Google Scholar]
  3. Brandariz-Nuñez A., Menaya-Vargas R., Benavente J., Martinez-Costas J. 2010; IC-tagging and protein relocation to ARV muNS inclusions: a method to study protein-protein interactions in the cytoplasm or nucleus of living cells. PLoS ONE 5:e13785 [View Article][PubMed]
    [Google Scholar]
  4. Broering T. J., Arnold M. M., Miller C. L., Hurt J. A., Joyce P. L., Nibert M. L. 2005; Carboxyl-proximal regions of reovirus nonstructural protein muNS necessary and sufficient for forming factory-like inclusions. J Virol 79:6194–6206 [View Article][PubMed]
    [Google Scholar]
  5. Chang Y. S., Liu W. J., Chou T. L., Lee Y. T., Lee T. L., Huang W. T., Kou G. H., Lo C. F. 2008; Characterization of white spot syndrome virus envelope protein VP51A and its interaction with viral tegument protein VP26. J Virol 82:12555–12564 [View Article][PubMed]
    [Google Scholar]
  6. Chen Z., Gui J., Gao X., Pei C., Hong Y., Zhang Q. 2013; Genome architecture changes and major gene variations of Andrias davidianus ranavirus (ADRV). Vet Res 44:101 [View Article][PubMed]
    [Google Scholar]
  7. Chinchar V. G., Yu K. H., Jancovich J. K. 2011; The molecular biology of frog virus 3 and other iridoviruses infecting cold-blooded vertebrates. Viruses 3:1959–1985 [View Article][PubMed]
    [Google Scholar]
  8. Eaton H. E., Metcalf J., Penny E., Tcherepanov V., Upton C., Brunetti C. R. 2007; Comparative genomic analysis of the family Iridoviridae: re-annotating and defining the core set of iridovirus genes. Virol J 4:11 [View Article][PubMed]
    [Google Scholar]
  9. Gui J. F., Zhu Z. Y. 2012; Molecular basis and genetic improvement of economically important traits in aquaculture animals. Chin Sci Bull 57:1751–1760 [View Article]
    [Google Scholar]
  10. He L. B., Ke F., Zhang Q. Y. 2012; Rana grylio virus as a vector for foreign gene expression in fish cells. Virus Res 163:66–73 [View Article][PubMed]
    [Google Scholar]
  11. He L. B., Gao X. C., Ke F., Zhang Q. Y. 2013; A conditional lethal mutation in Rana grylio virus ORF 53R resulted in a marked reduction in virion formation. Virus Res 177:194–200 [View Article][PubMed]
    [Google Scholar]
  12. Huang X. H., Huang Y. H., Yuan X. P., Zhang Q. Y. 2006; Electron microscopic examination of the viromatrix of Rana grylio virus in a fish cell line. J Virol Methods 133:117–123 [View Article][PubMed]
    [Google Scholar]
  13. Huang Y. H., Huang X. H., Gui J. F., Zhang Q. Y. 2007; Mitochondrion-mediated apoptosis induced by Rana grylio virus infection in fish cells. Apoptosis 12:1569–1577 [View Article][PubMed]
    [Google Scholar]
  14. Huang Y., Huang X., Liu H., Gong J., Ouyang Z., Cui H., Cao J., Zhao Y., Wang X.other authors 2009; Complete sequence determination of a novel reptile iridovirus isolated from soft-shelled turtle and evolutionary analysis of Iridoviridae. BMC Genomics 10:224 [View Article][PubMed]
    [Google Scholar]
  15. Huang Y., Huang X., Cai J., Ye F., Guan L., Liu H., Qin Q. 2011; Construction of green fluorescent protein-tagged recombinant iridovirus to assess viral replication. Virus Res 160:221–229 [View Article][PubMed]
    [Google Scholar]
  16. İnce I. A., Boeren S. A., van Oers M. M., Vervoort J. J., Vlak J. M. 2010; Proteomic analysis of Chilo iridescent virus. Virology 405:253–258 [View Article][PubMed]
    [Google Scholar]
  17. İnce I. A., Ozcan K., Vlak J. M., van Oers M. M. 2013; Temporal classification and mapping of non-polyadenylated transcripts of an invertebrate iridovirus. J Gen Virol 94:187–192 [View Article][PubMed]
    [Google Scholar]
  18. Jacob F., Monod J. 1961; Genetic regulatory mechanisms in the synthesis of proteins. J Mol Biol 3:318–356 [View Article][PubMed]
    [Google Scholar]
  19. Jancovich J. K., Bremont M., Touchman J. W., Jacobs B. L. 2010; Evidence for multiple recent host species shifts among the ranaviruses (family Iridoviridae). J Virol 84:2636–2647 [View Article][PubMed]
    [Google Scholar]
  20. Jancovich J. K., Chinchar V. G., Hyatt A., Miyazaki T., Williams T., Zhang Q. Y. 2012; Family Iridoviridae. In Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses pp. 193–210 Edited by King A. M. Q., Adams M. J., Carstens E. B., Lefkowitz E. J. San Diego, CA: Elsevier;
    [Google Scholar]
  21. Ke F., Zhao Z., Zhang Q. 2009; Cloning, expression and subcellular distribution of a Rana grylio virus late gene encoding ERV1 homologue. Mol Biol Rep 36:1651–1659 [View Article][PubMed]
    [Google Scholar]
  22. Ke F., He L. B., Pei C., Zhang Q. Y. 2011; Turbot reovirus (SMReV) genome encoding a FAST protein with a non-AUG start site. BMC Genomics 12:323 [View Article][PubMed]
    [Google Scholar]
  23. Kim Y. S., Ke F., Lei X. Y., Zhu R., Zhang Q. Y. 2010; Viral envelope protein 53R gene highly specific silencing and iridovirus resistance in fish cells by AmiRNA. PLoS ONE 5:e10308 [View Article][PubMed]
    [Google Scholar]
  24. Lei X. Y., Ou T., Zhu R. L., Zhang Q. Y. 2012a; Sequencing and analysis of the complete genome of Rana grylio virus (RGV). Arch Virol 157:1559–1564 [View Article][PubMed]
    [Google Scholar]
  25. Lei X. Y., Ou T., Zhang Q. Y. 2012b; Rana grylio virus (RGV) 50L is associated with viral matrix and exhibited two distribution patterns. PLoS ONE 7:e43033 [View Article][PubMed]
    [Google Scholar]
  26. Leong J. C., Kurath G. 2011; Novirhabdoviruses. In The Springer Index of Viruses Edited by Tidona C. A., Darai G. Springer-Verlag. (Online.);
    [Google Scholar]
  27. Lo C. F., Aoki T., Bonami J. R., Flegel T., Leu J. H., Lightner D. V., Stentiford G., Söderhäll K., Walker P. J.other authers 2012; Family Nimaviridae . In Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses pp. 229–234Edited by King A. M. Q., Adams M. J., Carstens E. B., Lefkowitz E. J. Elsevier, San Diego, CA: Elsevier;
    [Google Scholar]
  28. Majji S., Thodima V., Sample R., Whitley D., Deng Y., Mao J., Chinchar V. G. 2009; Transcriptome analysis of Frog virus 3, the type species of the genus Ranavirus, family Iridoviridae . Virology 391:293–303 [View Article][PubMed]
    [Google Scholar]
  29. Maruri-Avidal L., Weisberg A. S., Moss B. 2013; Association of the vaccinia virus A11 protein with the endoplasmic reticulum and crescent precursors of immature virions. J Virol 87:10195–10206 [View Article][PubMed]
    [Google Scholar]
  30. Mavian C., López-Bueno A., Fernández Somalo M. P., Alcamí A., Alejo A. 2012; Complete genome sequence of the European sheatfish virus. J Virol 86:6365–6366 [View Article][PubMed]
    [Google Scholar]
  31. Miller C. L., Arnold M. M., Broering T. J., Eichwald C., Kim J., Dinoso J. B., Nibert M. L. 2007; Virus-derived platforms for visualizing protein associations inside cells. Mol Cell Proteomics 6:1027–1038 [View Article][PubMed]
    [Google Scholar]
  32. Netherton C., Moffat K., Brooks E., Wileman T. 2007; A guide to viral inclusions, membrane rearrangements, factories, and viroplasm produced during virus replication. Adv Virus Res 70:101–182 [View Article][PubMed]
    [Google Scholar]
  33. Ring B. A., Ferreira Lacerda A., Drummond D. J., Wangen C., Eaton H. E., Brunetti C. R. 2013; Frog virus 3 open reading frame 97R localizes to the endoplasmic reticulum and induces nuclear invaginations. J Virol 87:9199–9207 [View Article][PubMed]
    [Google Scholar]
  34. Risco C., Rodríguez J. R., López-Iglesias C., Carrascosa J. L., Esteban M., Rodríguez D. 2002; Endoplasmic reticulum-Golgi intermediate compartment membranes and vimentin filaments participate in vaccinia virus assembly. J Virol 76:1839–1855 [View Article][PubMed]
    [Google Scholar]
  35. Shibata Y., Hu J., Kozlov M. M., Rapoport T. A. 2009; Mechanisms shaping the membranes of cellular organelles. Annu Rev Cell Dev Biol 25:329–354 [View Article][PubMed]
    [Google Scholar]
  36. Shuang F., Luo Y., Xiong X. P., Weng S., Li Y., He J., Dong C. 2013; Virions proteins of an RSIV-type megalocytivirus from spotted knifejaw Oplegnathus punctatus (SKIV-ZJ07). Virology 437:89–99 [View Article][PubMed]
    [Google Scholar]
  37. Sun W., Huang Y., Zhao Z., Gui J., Zhang Q. 2006; Characterization of the Rana grylio virus 3β-hydroxysteroid dehydrogenase and its novel role in suppressing virus-induced cytopathic effect. Biochem Biophys Res Commun 351:44–50 [View Article][PubMed]
    [Google Scholar]
  38. Wang Q., Luo Y., Xie J., Dong C., Weng S., Ai H., L., Yang X., Yu X., He J. 2008; Identification of two novel membrane proteins from the Tiger frog virus (TFV). Virus Res 136:35–42 [View Article][PubMed]
    [Google Scholar]
  39. Whitley D. S., Yu K., Sample R. C., Sinning A., Henegar J., Norcross E., Chinchar V. G. 2010; Frog virus 3 ORF 53R, a putative myristoylated membrane protein, is essential for virus replication in vitro. Virology 405:448–456 [View Article][PubMed]
    [Google Scholar]
  40. Whittington R. J., Becker J. A., Dennis M. M. 2010; Iridovirus infections in finfish – critical review with emphasis on ranaviruses. . J Fish Dis 33:95–122 [View Article][PubMed]
    [Google Scholar]
  41. Williams T., Barbosa-Solomieu V., Chinchar V. G. 2005; A decade of advances in iridovirus research. Adv Virus Res 65:173–248 [View Article][PubMed]
    [Google Scholar]
  42. Wong C. K., Young V. L., Kleffmann T., Ward V. K. 2011; Genomic and proteomic analysis of invertebrate iridovirus type 9. J Virol 85:7900–7911 [View Article][PubMed]
    [Google Scholar]
  43. Work T. M., Dagenais J., Balazs G. H., Schumacher J., Lewis T. D., Leong J. A., Casey R. N., Casey J. W. 2009; In vitro biology of fibropapilloma-associated turtle herpesvirus and host cells in Hawaiian green turtles (Chelonia mydas). J Gen Virol 90:1943–1950 [View Article][PubMed]
    [Google Scholar]
  44. Xu W., Zhao Z., Zhang Q. Y. 2007; Identification of a late gene from Rana grylio virus. J Wuhan Univ (Nat Sci Ed) 53:706–710 (in Chinese with English abstract) [View Article]
    [Google Scholar]
  45. Zhang Q. Y., Gui J. F. 2012; Rana grylio virus. In Atlas of Aquatic Viruses and Viral Diseases pp. 200–212 Edited by Zhang Q. Y., Gui J. F. Beijing: Science Press;
    [Google Scholar]
  46. Zhang Q. Y., Li Z. Q., Gui J. F. 1999; Studies on morphogenesis and cellular interactions of Rana grylio virus in an infected fish cell line. Aquaculture 175:185–197 [View Article]
    [Google Scholar]
  47. Zhang Q. Y., Xiao F., Li Z. Q., Gui J. F., Mao J., Chinchar V. G. 2001; Characterization of an iridovirus from the cultured pig frog Rana grylio with lethal syndrome. Dis Aquat Organ 48:27–36 [View Article][PubMed]
    [Google Scholar]
  48. Zhang Q. Y., Xiao F., Xie J., Li Z. Q., Gui J. F. 2004; Complete genome sequence of lymphocystis disease virus isolated from China. J Virol 78:6982–6994 [View Article][PubMed]
    [Google Scholar]
  49. Zhang Q. Y., Zhao Z., Xiao F., Li Z. Q., Gui J. F. 2006; Molecular characterization of three Rana grylio virus (RGV) isolates and Paralichthys olivaceus lymphocystis disease virus (LCDV-C) in iridoviruses. Aquaculture 251:1–10 [View Article]
    [Google Scholar]
  50. Zhao Z., Ke F., Gui J., Zhang Q. 2007; Characterization of an early gene encoding for dUTPase in Rana grylio virus. Virus Res 123:128–137 [View Article][PubMed]
    [Google Scholar]
  51. Zhao Z., Ke F., Huang Y. H., Zhao J. G., Gui J. F., Zhang Q. Y. 2008; Identification and characterization of a novel envelope protein in Rana grylio virus. J Gen Virol 89:1866–1872 [View Article][PubMed]
    [Google Scholar]
  52. Zhao Z., Ke F., Shi Y., Zhou G. Z., Gui J. F., Zhang Q. Y. 2009; Rana grylio virus thymidine kinase gene: an early gene of iridovirus encoding for a cytoplasmic protein. Virus Genes 38:345–352 [View Article][PubMed]
    [Google Scholar]
  53. Zhou Q., Xu L., Li H., Qi Y. P., Yang F. 2009; Four major envelope proteins of white spot syndrome virus bind to form a complex. J Virol 83:4709–4712 [View Article][PubMed]
    [Google Scholar]
  54. Zhou S., Wan Q., Huang Y., Huang X., Cao J., Ye L., Lim T. K., Lin Q., Qin Q. 2011; Proteomic analysis of Singapore grouper iridovirus envelope proteins and characterization of a novel envelope protein VP088. Proteomics 11:2236–2248 [View Article][PubMed]
    [Google Scholar]
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