Abstract
The predicted open reading frame 167L (ORF 167L) of lymphocystis disease virus (LCDV, Iridoviridae) isolated from plaice, dab and flounder was investigated. The ORF 167L corresponding genes of the three LCDV isolates were amplified, cloned and sequenced. A comparison of the LCDV strains showed that the nucleotide sequence of ORF 167L and its deduced amino acid sequence were highly conserved in the genus lymphocystivirus (a homology of 80% in dab and flounder/plaice, 97% in plaice and flounder). The N-terminus protein predicted from the ORF 167L suggests similarities to the tumor necrosis factor receptor (TNFR)-family, and to TNFR-like proteins, which play an important role in various poxvirus species. Further, homology to the CUB-domain was shown at the C-terminus of the LCDV protein. Phylogenetic analyses of partial LCDV protein sequences identified two clusters: one cluster containing the flounder and plaice LCDV isolate (LCDV-1), and another cluster, containing the dab LCDV isolate (LCDV-2). The ORF 167L of plaice LCDV was expressed in Escherichia coli, and in fish cells. The expressed ORF resulted in a 30-kDa cytoplasmic protein lacking a signal peptide. An established monoclonal antibody (mAb 18) was used to detect LCDV proteins in skin explants of flounders and cryosections of dab skin. Specific fluorescence was found in the cytoplasm of intact epitheloid cells of the lymphocystis capsule and in the epidermis skin covering the lymphocystic nodules. LCDV-specific labelling of mAb 18 was also shown in spleen and liver tissue of LCDV-positive flounders. The ORF 167L protein seemed not to have the extracellular receptor function predicted from the usual cellular TNFR. The myxomavirus M-T2 protein, a poxviral TNFR homologue, was also shown not to have TNFR-like functions but to be involved in the apoptosis signal cascade.
Similar content being viewed by others
References
Lowe K., Trans Norfolk Norwich Nat Soc Fish, pp. 21–56, 1874.
Woodcock H.M., Trans Liverpool Biol Soc 18, 143–152, 1904.
Madeley C.R., Smail D.A. and Egglestone S.I., J Gen Virol 40, 421–431, 1978.
Darai G., Anders K., Koch H., Delius H., Gelderblom H., Samalecos C. and Flügel R.M., Virology 126, 466–479, 1983.
Yamamoto T., Mac Donald R.D., Gillespie D.C. and Kelly R.K., J Fish Res Board Can 33, 2408–2419, 1976.
Anders K. in Ahne W., Kurstak E. (eds), Viruses of Lower Vertebrates. Springer Verlag, Berlin Heidelberg New York, 1989, pp. 141–160.
Williams T., Chinchar G., Darai G., Hyatt A., Kalmakoff J. and Seligy V., in Van Regenmortel M.H.V., Fauquet C.M., Bishop D.H.L., Carstens E.B., Estes M.K., Lemon S.M., Maniloff J., Mayo M.A., McGeoch D.J., Pringle C.R. and Wickner R.B. (eds), Virus Taxonomy. Seventh Report of the International Committee on Taxonomy of Viruses. Academic Press, New York, San Diego, 2000, pp. 167–182.
Essbauer S. and Ahne W., J Vet Med B 48, 403–475, 2001.
Nigrelli R.F. and Ruggieri G.D., Zoologica NY 50, 83–95, 1965.
Wolf K., Virology 18, 249–262, 1962.
Grinwis G.C.M., Wester P.W., Kamstra A., Van de Brandhof E.F.J., Van Dijk J.E., Leewis R.J., Vaal M.A., Vethaak A.D. and Vos J.G., Laboratory Maintenance, Topographical Anatomy and Histology of Flounder, Platichthys flesus. Nat. Inst. Public Health and Environmental Protection, Bilthoven, Netherlands, Rapp No. 732402 001, 1995.
Sindermann C.J., Ocean Pollution: Effects on Living Resources and Humans. CRC Press, Boca Raton, FL, 1996, pp. 1–275.
Dethlefsen V., Lang T. and Köves P., Dis Aquat Org 42, 119–132, 2000.
Tidona C.A. and Darai G., Arch Virol (Suppl) 13, 49–56, 1997.
Tidona C.A. and Darai G., Virology 230, 207–216, 1997.
Upton C., Machen J.L., Schreiber M. and Mc Fadden G., Virology 18, 370–382, 1991.
McFadden G., Viroceptors, Virokines and Related Immune Modulators Encoded by DNA Viruses. Springer-Verlag, New York, 1994.
Smith C.A. and Godwin R.G., in McFadden G. (ed.), Viroceptors, virokines and related immune modulators encoded by DNA viruses. Springer-Verlag, New York, 1994.
Sedger L. and Mc Fadden G., Immunol Cell Biol 74, 538–545, 1996.
Schreiber M., Sedger L. and McFadden G., J Virol 71, 2171–2181, 1997.
Bazan J.F., Curr Biol 3, 603–606, 1993.
Smith C.A., Farrah T. and Goodwin R.G., Cell 76, 959–962, 1994.
Beutler B. and Van Huffel C., Science 264, 667–668, 1994.
Herbein G. and O'Brien W.A., Proc Soc Exp Biol Med 223, 241–257, 2000.
Schnitzler P. and Darai G., J Gen Virol 74, 2143–2150, 1993.
Mao J., Hedrick R.P. and Chinchar V.G., Virology 229, 212–220, 1997.
Kyte J. and Doolittle R.F., J Mol Biol 157, 105–132, 1982.
Higgins D.G., Methods Mol Biol 25, 307–318, 1994.
Altschul S.F., Madden T.L., Schäffer A.A., Zhang J., Zhang Z., Miller W. and Lipman D.J., Nucleic Acids Res 25, 3389–3402, 1997.
Bairoch A., Bucher P. and Hofmann K., Nucleic Acids Res 25, 217–221, 1997.
Bailey T.L. and Grandy W.N., Classifying proteins by family using the product of correlated p-values. Proc. 3rd International Conference on Computational Molecular Biology (RECOMB99), 1999.
Sonnhammer E.L.L., von Heijne G. and Krogh A. in Glasgow J., Littlejohn T., Major F., Lathrop R., Sankoff D. and Sensen C. (eds), Proc. 6th Conf. on Intelligent Systems for Molecular Biology, 1998, pp. 175–182.
Nielsen H., Engelbrecht J., Brunak S. and von Heinje G., Protein Eng 10, 1–6, 1997.
Lodish H., Baltimore D., Berk A., Zipursky S.L., Matsudeira P. and Darnell J., Molecular Cell Biology. Scientific American Books Inc. (Scientific American Inc.), New York–Oxford, 1995.
Hansen J.E., Lund O., Rapacki K. and Brunak S., Nucleic Acids Res 25, 278–282, 1997.
Hansen J.E., Lund O., Tolstrup N., Gooley A.A. and Williams K.L., Glycoconjugate J 15, 115–130, 1998.
Hansen J.E., Lund O., Engelbrecht J., Bohr H., Nielsen J.O., Hansen J-E.S. and Brunak S., Biochem J 308, 801–813, 1995.
Felsenstein J., Cladistics 5, 164–166, 1989.
Felsenstein J., PHYLIP (Phylogeny Inference Package) version 3.5c. Distributed by the author. Department of Genetics, University of Washington, Seattle, 1993.
Sambrook J., Fritsch E.F. and Maniatis T., Molecular Cloning – A Laboratory Manual. Cold Spring Harbor Laboratory Press, 1989.
Coligan J.E., Kruisbeek A.M., Marguliesn D.H., Shevach E.M., Strober W. and Coico R., Current Protocols in Immunology. John Wiley & Sons Inc., USA, 1994.
Fijan N., Sulimanovic D., Bearzotti M., Muzinic D., Zwillenberg L.O., Chilmonczyk S., Vautherot J.F. and de Kinkelin P., Ann Virol 134E, 207–220, 1983.
Araki K., Nagoya H. and Onozato H., Bull Natl Inst Aquaculture 10, 1–9, 1991.
Howard S.T., Chan S.Y. and Smith G.L., Virology 180, 633–647, 1991.
Smith C.A., Davis T., Anderson D., Solam L., Beckmann P., Jerzey R., Dower S.K., Cosman D. and Goodwin R.G., Science 248, 1019–1023, 1990.
Lee T.H., Wisniewski H.-G. and Vilcek J., J Cell Biol 116, 545–557, 1992.
Bork P., FEBS Lett 282, 9–12, 1991.
Bork P. and Beckmann G., J Mol Biol 231, 539–545, 1993.
Mallett S. and Barclay A.N., Immunol Today 12, 220–223, 1991.
Armitage R.J., Curr Biol 6, 407–413, 1994.
Sprang S.R., Trends Biochem Sci 15, 366–368, 1990.
Brojatsch J., Naughton J., Rolls M.M., Zingler K. and Young J.A.T., Cell 87, 845–855, 1996.
Banner D.W., d'Arcy A., Janes W., Gentz R., Schoenfeld H.-J., Broger C., Loetscher H. and Lesslauer W., Cell 73, 431–445, 1993.
Gooding L.R., Cell 71, 5–7, 1992.
Spriggs M.K., Virus Res 33, 1–10, 1994.
Spriggs M.K., Annu Rev Immunol 14, 101–130, 1996.
McFadden G., Schreiber M. and Sedger L., J Neuroimmunol 72, 119–126, 1997.
Alcami A. and Koszinowski U.H., Immunol Today 21, 447–455, 2000.
Loparev V.N., Parsons J.M., Knight J.C., Panus J.F., Ray C.A., Buller R.M., Pickup D.J. and Esposito J.J., Proc Nat Aca Sci USA 95, 3786–3791, 1998.
Ahne W., Bull Eur Ass Fish Pathol 13, 106–107, 1993.
Ahne W., Immunol Today 115, 137, 1994.
Hardie L.J., Vet Imm Immunpath 40, 73–84, 1994.
Hirono I., Nam B.-H., Kurobe T. and Aoki T., J Immunol 165(8), 423–427, 2000.
Laing K.J., Wang T., Zou J., Holland J., Hong S., Bols N., Hirono I., Aoki T. and Secombes C.J., Eur J Biochem 268(5), 1315–1322, 2001.
Secombes C.J., Hardie L.J. and Daniels G., Fish Shellfish Imm 6, 291–304, 1996.
Hughes T.K.Jr., Smith E.M., Chin R., Cadet P., Sinisterra J., Leung M.R., Shipp M.A., Scharrer B. and Stefano G.B., Proc Nat Aca Sci USA 87, 4426–4429, 1990.
Jang S.I., Mulero V., Hardie L.J. and Secombes C.J., Fish Shellfish Imm 5, 61–69, 1995.
Lurain N.S., Kapell K.S., Huang D.D., Short J.A., Paintsil J., Winkfield E., Benedict C.A., Ware C.F. and Bremer J.W., J Virol 73, 10040–10050, 1999.
Benedict C.A., Butrovich K.D., Lurain N.S., Corbeil J., Rooney I., Schneider P., Tschopp J. and Ware C.F., J Immunol 162, 6967–6970, 1999.
Cascino I., Fiucci G., Papoff G. and Ruberti G., J Immunol 154, 2706–2713, 1995.
Cascino I., Papoff G., De Maria R. and Ruberti G., J Immunol 156, 13–17, 1996.
Opata I., Auster A.S., Matsui A., Greenwel P., Geerts A., D 'Amico T., Fujiwra K., Kessler E. and Rojkind M., Hepatology 26, 611–617, 1997.
Hulmes D.J., Mould A.P. and Kessler E., Matrix Biol. 16(1), 41–45, 1997.
Weissenberg R., Cancer Res 11, 608–613, 1951.
Walker R., Virology 18, 503–505, 1962.
Dunbar C.E. and Wolf K., J Inf Dis 116, 466–472, 1962.
Wolf K., Gravell M. and Malsberger R.G., Science 151, 1004–1005, 1966.
Walker R. and Weissenberg R., Ann NY Acad Sci 126, 375–385, 1965.
Howse H.D. and Christmas J.Y., Trans Am Microscop Soc 89, 276–282, 1970.
Howse H.D. and Christmas J.Y., Virol 44, 211–214, 1971.
Gonzales de Canales M.L., Munoz-Cueto J.A., Arellano J.M., Garci G.A. and Sarsquete M.C., Eur J Histochem 40, 143–152, 1996.
Toole B.P., Tissue Res 10, 93–100, 1982.
Sarasquete C., Gonzales de Canales M.L., Arellano J., Perez-Prieto S., Garcia-Rosada E. and Borrego J.J., Histol Histopathol 13, 37–45, 1998.
Flügel R.M., Darai G. and Gelderblom H., Virol 122, 48–55, 1982.
Robin J., Laperiere A. and Berthiaume L., Arch Virol 87, 297–305, 1986.
Fiedler K., in Starck, D. (ed.), 2. Lehrbuch der speziellen Zoologie begründet von Alfred Kästner. Band II: Wirbeltiere Teil: Fische. Gustav Fischer Verlag Jena, 1991, pp. 21–35.
Bullock A.M. and Roberts R.J., Ocenogr Mar Biol Ann Rev 13, 383–411, 1974.
Roberts R.J., Grundlagen der Fischpathologie mit einer Einführung in die Anatomie, Physiologie, Pathophysiologie und Immunologie sowie in den aquatischen Lebensraum der Knochenfische. Verlag Paul Parey, Berlin, Hamburg, 1985.
Whitear M., J Zool 160, 437–454, 1970.
Whitear M., in Bereiter-Hahn J., Matoltsy A.G. and Richards S.K. (eds), Biology of the Integument. 2 Vertebrates. Springer Verlag, Berlin Heidelberg New York Tokyo, 1986, p. 8ff.
Watermann B., Zur Histologie und Genese von Geschwüren und Papillomen bei Klieschen (Limanda limanda L.) der deutschen Bucht. Diploma thesis in biology, University of Hamburg, 1979.
Fujii R. in Hoar W.S. and Randall D.J. (eds.), Fish Physiology. Volume III: Reproduction, Growth, Pigments, and Poisons. Academic Press, New York, London, 1969.
Starck D., Vergleichende Anatomie der Wirbeltiere auf evolutionsbiologischer Grundlage. Band 3: Organe des aktiven Bewegungsapparates, der Koordination, der Umweltbeziehung, des Stoffwechsels und der Fortpflanzung. Springer Verlag, Berlin, 1992, p. 139ff.
Weissenberg R., in Prowazek S. and von Möller W. (eds), Handbuch der pathogenen Protozoen 3. J.A. Barth, Leipzig, 1921, 1344–1380.
Russell P.H., J Fish Biol 6, 771–778, 1974.
Schacht V., Untersuchungen zur Lymphocystiskrankheit in inneren Organen der Kliesche (Limanda limanda L.). Diploma thesis in biology, University of Hamburg, 1988.
Tanaka M., Yoshimizu M., Kusakari M. and Kimura T., Bull Jpn Soc Sci Fish 50, 37–42, 1984.
Weissenberg R. and Zoologica N.Y. 30, 169–184, 1945.
Möller H. and Anders K., Krankheiten und Parasiten der Meeresfische, Verlag Heino Möller, Kiel, 1983, p. 45–50.
Bogovskii S., Eesti nsv tead akad toim biol 31, 310–312, 1982.
Alcami A., Khanna A., Paul N.L. and Smith G.L., J Gen Virol 80, 949–959, 1999.
Macen J.L., Graham K.A., Lee M., Schreiber M., Boshkov L.K. and Mc Fadden G., Virology 218, 232–237, 1996.
Kessler E., Mould A.P. and Hulmes D.J., Biochem Biophys Res Comm 173, 81–86, 1990.
Langdon J.S. and Humphrey J.D., J Fish Dis 10, 289–297, 1987.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Essbauer, S., Fischer, U., Bergmann, S. et al. Investigations on the ORF 167L of Lymphocystis Disease Virus (Iridoviridae). Virus Genes 28, 19–39 (2004). https://doi.org/10.1023/B:VIRU.0000012261.96217.fe
Issue Date:
DOI: https://doi.org/10.1023/B:VIRU.0000012261.96217.fe