Abstract
Singapore grouper iridovirus (SGIV), as a causative agent of serious systemic disease, causes significant economic losses in grouper aquaculture. In this study, a novel ICP18 homolog encoded by SGIV ORF086R was identified and characterized. Strikingly, ICP18 homologs can be found in all ranaviruses, but not in other sequenced large DNA viruses. SGIV ICP18 is an immediate-early gene and begins to be transcribed as early as 2 h post-infection (p.i.). Western blotting indicated that SGIV ICP18 is translated as early as 6 h p.i. and is a viral non-envelope protein. Subcellular localization analysis revealed that the SGIV ICP18 displays a finely punctate cytoplasmic pattern. Furthermore, overexpression of SGIV ICP18 can promote the growth of grouper embryonic cells (GP) and contribute to SGIV replication. These results should offer important insights into the pathogenesis of ranaviruses.
Similar content being viewed by others
References
Ahne WHJ, Schlotfeldt HJ, Thomsen I (1989) Fish viruses: isolation of an icosahedral cytoplasmic deoxyribovirus from sheatfish (Silurus glanis). J Vet Med 36:333–336
Alzhanova D, Hruby DE (2006) A trans-Golgi network resident protein, golgin-97, accumulates in viral factories and incorporates into virions during poxvirus infection. J Virol 80:11520–11527
Castillo JP, Kowalik TF (2002) Human cytomegalovirus immediate early proteins and cell growth control. Gene 290:19–34
Castillo JP, Yurochko AD, Kowalik TF (2000) Role of human cytomegalovirus immediate-early proteins in cell growth control. J Virol 74:8028–8037
Chen M, Goorha R, Murti KG (1986) Interaction of frog virus-3 with the cytomatrix. IV: phosphorylation of vimentin precedes the reorganisation of intermediate filaments around the virus assembly sites. J Gen Virol 67:915–922
Chinchar VG, Essbauer S, He JG, Hyatt A, Miyazaki T, Seligy D, Williams T (2005) In: Fauqet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA (eds) Iridovirade. Virus taxonomy, VIIIth report of the international committee on taxonomy of viruses. Academic Press, London, pp 163–175
Everett RD (2000) ICP0, a regulator of herpes simplex virus during lytic and latent infection. Bioessays 22:761–770
Hampl H, Ben-Porat T, Ehrlicher L, Habermehl KO, Kaplan AS (1984) Characterization of the envelope proteins of pseudorabies virus. J Virol 52:583–590
Hobbs WE, DeLuca NA (1999) Perturbation of cell cycle progression and cellular gene expression as a function of herpes simplex virus ICP0. J Virol 73:8245–8255
Hyatt AD, Gould AR, Zupanovic Z, Cummingham AA, Hengstberger S, Whittington RJ, Kattenbelt J, Coupar BEH (2000) Comparative studies of piscine and amphibian iridoviruses. Arch Virol 145:301–331
Kalejta RF (2008) Tegument proteins of human cytomegalovirus. Microbiol Mol Biol Rev 72:249–265
Kinchington PR, Fite K, Seman A, Turse SE (2001) Virion Association of IE62, the varicella-zoster virus (VZV) major transcriptional regulatory protein, requires expression of the VZV open reading frame 66 protein kinase. J Virol 75:9106–9113
Kinchington PR, Hougland JK, Arvin AM, Ruyechan WT, Hay J (1992) The varicella-zoster virus immediate-early protein IE62 is a major component of virus particles. J Virol 66:359–366
Moss B, Shisler JL (2001) Immunology 101 at poxvirus U: immune evasion genes. Semin Immunol 13:59–66
Murti KG, Goorha R (1983) Interaction of frog virus-3 with the cytoskeleton.I: altered organization of microtubules, intermediate filaments, and microfilaments. J Cell Biol 96:1248–1257
Pallister J, Goldie S, Coupar B, Hyatt A (2005) Promoter activity in the 5′ flanking regions of the Bohle iridovirus ICP18, ICP46 and major capsid protein genes. Arch Virol 150:1911–1919
Piaskoski TO, Plumb JA (1999) Characterization of the largemouth bass virus in cell culture. J Aquat Anim Health 11:45–51
Qin QW, Chang SF, Ngoh-Lim GH, Gibson-Kueh S, Shi C, Lam TJ (2003) Characterization of a novel ranavirus isolated from grouper Epinephelus tauvina. Dis Aquat Organ 53:1–9
Qin QW, Lam TJ, Sin YM, Shen H, Chang SF, Ngoh GH, Chen CL (2001) Electron microscopic observations of a marine fish iridovirus isolated from brown-spotted grouper, Epinepheous tauvina. J Virol Methods 98:17–24
Reed LJ, Muench H (1938) A simple method of estimating fifty per cent endpoints. Am J Epidemiol 27:493–497
Sample R, Bryan L, Long S, Majji S, Hoskins G, Sinning A, Olivier J, Chinchar VG (2007) Inhibition of iridovirus protein synthesis and virus replication by antisense morpholino oligonucleotides targeted to the major capsid protein, the 18 kDa immediate-early protein, and a viral homolog of RNA polymerase II. Virology 358:311–320
Song SW, Lin Q, Joshi SB, Lim TK, Hew CL (2006) Proteomic studies of the Singapore grouper iridovirus. Mol Cell Proteomics 5:256–264
Song WJ, Qin QW, Qiu J, Huang CH, Wang F, Hew CL (2004) Functional genomics analysis of Singapore grouper iridovirus: complete sequence determination and proteomic analysis. J Virol 78:12576–12590
Stinski MF, Petrik DT (2008) Functional roles of the human cytomegalovirus essential IE86 protein. Curr Top Microbiol Immunol 325:133–152
Teng Y, Hou ZW, Gong J, Liu H, Xie X, Zhang L, Chen XH, Qin QW (2008) Whole-genome transcriptional pro.les of a novel marine fish iridovirus, Singapore grouper iridovirus (SGIV) in virus-infected grouper spleen cell cultures and in orange-spotted grouper, Epinephulus coioides. Virology 377:39–48
VanSlyke JK, Hruby DE (1994) Immunolocalization of vaccinia virus structural proteins during virion formation. Virology 198:624–635
Varnum SM, Streblow DN, Monroe ME, Smith P, Auberry KJ, Pasa-Tolic L, Wang D, Camp DG, Rodland K, Wiley S, Britt W, Shenk T, Smith RD, Nelson J (2004) Identification of proteins in human cytomegalovirus (HCMV) particles: the HCMV proteome. J Virol 78:10960–10966
Wang F, Bi X, Chen LM, Hew CL (2008) ORF018R, a highly abundant virion protein from Singapore grouper iridovirus, is involved in serine/threonine phosphorylation and virion assembly. J Gen Virol 89:1169–1178
Wang YQ, Lu L, Weng SP, Huang JN, Chan SM, He JG (2007) Molecular epidemiology and phylogenetic analysis of a marine fish infectious spleen and kidney necrosis virus-like (ISKNV-like) virus. Arch Virol 152:763–773
Wiebusch L, Neuwirth A, Grabenhenrich L, Voigt S, Hagemeier C (2008) Cell cycle-independent expression of immediate-early gene 3 results in G1 and G2 arrest in murine cytomegalovirus-infected cells. J Virol 82:10188–10198
Wileman T (2006) Aggresomes and autophagy generate sites for virus replication. Science 312:875–878
Williams T (1996) The iridoviruses. Adv Virus Res 46:347–412
Williams T, Barbosa-Solomieu V, Chinchar VG (2005) A decade of advances in iridovirus research. Adv Virus Res 65:173–248
Willis D, Foglesong D, Granoff A (1984) Nucleotide sequence of an immediate-early frog virus 3 gene. J Virol 53:905–912
Willis DB, Granoff A (1985) Trans activation of an immediate-early frog virus 3 promoter by a virion protein. J Virol 56:495–501
Yao F, Courtney RJ (1989) A major transcriptional regulatory protein (ICP4) of herpes simplex virus type 1 is associated with purified virions. J Virol 63:3338–3344
Yao F, Courtney RJ (1992) Association of ICP0 but not ICP27 with purified virions of herpes simplex virus type 1. J Virol 66:2709–2716
Zhao Z, Ke F, Gui JF, Zhang QY (2007) Characterization of an early gene encoding for dUTPase in Rana grylio virus. Virus Res 123:128–137
Zhou YF, Yu ZX, Wanishsawad C, Shou M, Epstein SE (1999) The immediate early gene products of human cytomegalovirus increase vascular smooth muscle cell migration, proliferation, and expression of PDGF β-receptor. Biochem Biophys Res Commun 256:608–613
Acknowledgments
This work was supported by grants from the National Basic Research Program of China (973) (2006CB101802), the National High Technology Development Program of China (863) (2006AA09Z445, 2006AA09Z411), National Natural Science Foundation of China (30700616, 30725027) and Chinese Academy of Sciences (KZCX2-YW-BR-08). We thank Professor Zaohe Wu and Jichang Jian, Guangdong Provincial Key Laboratory of Pathogenic Biology and Epidemiology for Aquatic Economic Animals, for providing facilities to perform the work of gene cloning, plasmid construction and antibody preparation.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Xia, L., Cao, J., Huang, X. et al. Characterization of Singapore grouper iridovirus (SGIV) ORF086R, a putative homolog of ICP18 involved in cell growth control and virus replication. Arch Virol 154, 1409–1416 (2009). https://doi.org/10.1007/s00705-009-0457-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-009-0457-y