1887

Abstract

Infectious salmon anaemia virus (ISAV), a pathogen in marine aquaculture, belongs to the genus , family . There is limited information on how ISAV interacts with host defences. To study ISAV–antibody interactions, virus neutralization (VN) assays were performed in the cell lines CHSE-214, SHK-1 and TO using three strains of ISAV and rabbit or fish anti-ISAV sera. Homologous VN titres of >1 : 1280 in CHSE-214 cells corresponded to titres of only 1 : 80 in the macrophage-like fish cell lines SHK-1 and TO, despite using 1000 and 2000 times less virus, respectively. However, rabbit antiserum to infectious pancreatic necrosis virus (IPNV) had a VN titre of 1 : 10 260 against IPNV in both CHSE-214 and TO cells. Poor ISAV neutralization in TO cells was attributed to Fc receptors mediating virus infectivity, because (1) neutralization by rabbit antiserum to ISAV was increased 48-fold in the presence of staphylococcal Protein A and (2) when using FITC-labelled virus and spectrofluorometry, a significant increase (=0·018) in the intensity of fluorescence of intracellular virus was observed in assays of virus–antiserum mixtures in the absence of Protein A as compared to those in the presence of Protein A. Neutralization of ISAV with fish antisera was observed only in CHSE-214 cells, as Protein A could not restore neutralization in TO cells. These findings demonstrate for the first time antibody-mediated infection of macrophage-like fish cell lines by a fish virus, ISAV, and, as ISAV in Atlantic salmon targets leukocytic and endothelial cells, this may have implications for ISA pathogenesis and vaccination.

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2003-07-01
2019-10-24
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References

  1. Anon. ( 2000; ). ISA hits the Faros. Fish Farming Int 27, 47.
    [Google Scholar]
  2. Anon. ( 2001; ). Orthomyxoviridae Study Group proposal to ICTV. 10 September 2001, http://www.danforthcenter.org/iltab/ictvnet/asp_MainePage.asp
  3. Bols, N. C., Ganassin, R. C., Tom, D. J. & Lee, L. E. ( 1994; ). Growth of fish cell lines in glutamine-free media. Cytotechnology 16, 159–166.[CrossRef]
    [Google Scholar]
  4. Bouchard, D., Keleher, W., Opitz, H. M., Blake, S., Edwards, K. C. & Nicholson, B. L. ( 1999; ). Isolation of infectious salmon anaemia virus (ISAV) from Atlantic salmon in New Brunswick, Canada. Dis Aquat Organ 35, 131–137.[CrossRef]
    [Google Scholar]
  5. Bouchard, D., Brockway, K., Giray, C., Keleher, W. & Merril, P. L. ( 2001; ). First report of infectious salmon anemia (ISA) in the United States. Bull Eur Assoc Fish Pathol 21, 86–88.
    [Google Scholar]
  6. Cardosa, M. J., Porterfield, J. S. & Gordon, S. ( 1983; ). Complement receptor mediates enhanced flavivirus replication in macrophages. J Exp Med 158, 258–263.[CrossRef]
    [Google Scholar]
  7. Chanas, A. C., Gould, E. A., Clegg, J. C. & Varma, M. G. ( 1982; ). Monoclonal antibodies to Sindbis virus glycoprotein E1 can neutralize, enhance infectivity, and independently inhibit haemagglutination or haemolysis. J Gen Virol 58, 37–46.[CrossRef]
    [Google Scholar]
  8. Clerx, J. P. M., Horzinek, M. C. & Osterhaus, A. D. M. E. ( 1978; ). Neutralization and enhancement of infectivity of non-salmonid fish rhabdoviruses by rabbit and pike immune sera. J Gen Virol 40, 297–308.[CrossRef]
    [Google Scholar]
  9. Dannevig, B. H., Falk, K. & Namork, E. ( 1995; ). Isolation of the causal virus of infectious salmon anaemia (ISA) in a long-term cell line from Atlantic salmon head kidney. J Gen Virol 76, 1353–1359.[CrossRef]
    [Google Scholar]
  10. Dannevig, B. H., Brudeseth, B. E., Gjøen, T. & n other authors ( 1997; ). Characterisation of a long-term cell line (SHK-1) developed from the head kidney of Atlantic salmon (Salmo salar L.). Fish Shellfish Immunol 7, 213–226.[CrossRef]
    [Google Scholar]
  11. Daughaday, C. C., Brandt, W. E., McCown, J. M. & Russell, P. K. ( 1981; ). Evidence for two mechanisms of dengue virus infection of adherent human monocytes: trypsin-sensitive virus receptors and trypsin-resistant immune complex receptors. Infect Immun 32, 469–473.
    [Google Scholar]
  12. Devold, M., Krossøy, B., Aspehaug, V. & Nylund, A. ( 2000; ). Use of RT-PCR for diagnosis of infectious salmon anaemia virus (ISAV) in carrier sea trout Salmo trutta after experimental infection. Dis Aquat Organ 40, 9–18.[CrossRef]
    [Google Scholar]
  13. Eliassen, T. M., Froystad, M. K., Dannevig, B. H., Jankowska, M., Brech, A., Falk, K., Romoren, K. & Gjøen, T. ( 2000; ). Initial events in infectious salmon anemia virus infection: evidence for the requirement of a low-pH step. J Virol 74, 218–227.[CrossRef]
    [Google Scholar]
  14. Falk, K. & Dannevig, B. H. ( 1995; ). Demonstration of infectious salmon anaemia (ISA) viral antigens in cell cultures and tissue sections. Vet Res 26, 499–504.
    [Google Scholar]
  15. Falk, K., Press, C. M., Landsverk, T. & Dannevig, B. H. ( 1995; ). Spleen and kidney of Atlantic salmon (Salmo salar L.) show histochemical changes early in the course of experimentally induced infectious salmon anaemia (ISA). Vet Immunol Immunopathol 49, 115–126.[CrossRef]
    [Google Scholar]
  16. Falk, K., Namork, E., Rimstad, E., Mjaaland, S. & Dannevig, B. H. ( 1997; ). Characterization of infectious salmon anaemia virus, an orthomyxo-like virus isolated from Atlantic salmon (Salmo salar L.). J Virol 71, 9016–9023.
    [Google Scholar]
  17. Falk, K., Namork, E. & Dannevig, B. H. ( 1998; ). Characterization and applications of a monoclonal antibody against infectious salmon anaemia virus. Dis Aquat Organ 34, 77–85.[CrossRef]
    [Google Scholar]
  18. Falk, K., Johansen, M. B., Ferguson, H. W., Aspehaug, V., Krossøy, B., Biering, E. & Poppe, T. ( 2001; ). Immunohistochemical detection of infectious salmon anaemia virus (ISAV). Proceedings of the European Association of Fish Pathologists (Dublin, Ireland, 10–14 September 2001).
  19. Fujiki, K., Shin, D. H., Nakao, M. & Yano, T. ( 2000; ). Molecular cloning and expression analysis of carp (Cyprinus carpio) interleukin-1β, high affinity immunoglobulin E Fc receptor γ subunit and serum amyloid A. Fish Shellfish Immunol 10, 229–242.[CrossRef]
    [Google Scholar]
  20. Gessner, J. E., Heiken, H., Tamm, A. & Schmidt, R. E. ( 1998; ). The IgG Fc receptor family. Ann Hematol 76, 231–248.[CrossRef]
    [Google Scholar]
  21. Girn, J., Kavoosi, M. & Chantler, J. ( 2002; ). Enhancement of coxsackievirus B3 infection by antibody to a different coxsackievirus strain. J Gen Virol 83, 351–358.
    [Google Scholar]
  22. Griffiths, S., Cook, M., Mallory, B. & Ritchie, R. ( 2001; ). Characterisation of ISAV proteins from cell culture. Dis Aquat Organ 45, 19–24.[CrossRef]
    [Google Scholar]
  23. Halstead, S. B., Venkateshan, C. N., Gentry, M. K. & Larsen, L. K. ( 1984; ). Heterogeneity of infection enhancement of dengue 2 strains by monoclonal antibodies. J Immunol 132, 1529–1532.
    [Google Scholar]
  24. Haynes, L., Fuller, L. & McKinney, E. C. ( 1988; ). Fc receptor for shark IgM. Dev Comp Immunol 12, 561–571.[CrossRef]
    [Google Scholar]
  25. Homsy, J. M., Meyer, M., Tateno, S., Clarkson, S. & Levy, J. A. ( 1989; ). The Fc and not CD4 receptor mediates antibody enhancement of HIV infection in human cells. Science 244, 1357–1360.[CrossRef]
    [Google Scholar]
  26. Kibenge, F. S. B., Lyaku, J. R., Rainnie, D. & Hammell, K. L. ( 2000; ). Growth of infectious salmon anaemia virus in CHSE-214 cells and evidence for phenotypic differences between virus strains. J Gen Virol 81, 143–150.
    [Google Scholar]
  27. Kibenge, F. S. B., Garate, O. N., Johnson, G., Arriagada, R., Kibenge, M. J. T. & Wadowska, D. ( 2001a; ). Isolation and identification of infectious salmon anaemia virus (ISAV) from Coho salmon in Chile. Dis Aquat Organ 45, 9–18.[CrossRef]
    [Google Scholar]
  28. Kibenge, F. S. B., Kibenge, M. J. T., McKenna, P. K., Stothard, P., Marshall, R., Cusack, R. R. & McGeachy, S. ( 2001b; ). Antigenic variation among isolates of infectious salmon anaemia virus correlates with genetic variation of the viral haemagglutinin gene. J Gen Virol 82, 2869–2879.
    [Google Scholar]
  29. Kibenge, M. J. T., Opazo, B., Rojas, A. & Kibenge, F. S. B. ( 2002; ). Serological evidence of infectious salmon anaemia virus (ISAV) infection in farmed fishes, using an indirect enzyme-linked immunosorbent assay (ELISA). Dis Aquat Organ 51, 1–11.[CrossRef]
    [Google Scholar]
  30. Kim, C. H. & Leong, J. A. ( 1999; ). Fish viruses. In Encyclopaedia of Virology, 2nd edn, pp. 558–568. Edited by A. Granoff & R. G. Webster. New York: Academic Press.
  31. King, A. A., Sands, J. J. & Porterfield, J. S. ( 1984; ). Antibody-mediated enhancement of rabies virus infection in a mouse macrophage cell line (P388D1). J Gen Virol 65, 1091–1093.[CrossRef]
    [Google Scholar]
  32. Krilov, L. R., Anderson, L. J., Marcoux, L., Bonagura, V. R. & Wedgwood, J. F. ( 1989; ). Antibody-mediated enhancement of respiratory syncytial virus infection in two monocyte/macrophage cell lines. J Infect Dis 160, 777–782.[CrossRef]
    [Google Scholar]
  33. Krossøy, B., Devold, M., Sanders, L. & 7 other authors ( 2001; ). Cloning and identification of the infectious salmon anaemia haemagglutinin. J Gen Virol 82, 1757–1765.
    [Google Scholar]
  34. Lewis, R. M., Cosgriff, T. M., Griffin, B. Y., Rhoderick, J. & Jahrling, P. B. ( 1988; ). Immune serum increases arenavirus replication in monocytes. J Gen Virol 69, 1735–1739.[CrossRef]
    [Google Scholar]
  35. Mantovani, B., Rabinovitch, M. & Nussenzweig, V. ( 1972; ). Phagocytosis of immune complexes by macrophages: different roles of the macrophage receptor sites for complement (C3) and for immunoglobulin (IgG). J Exp Med 135, 780–792.[CrossRef]
    [Google Scholar]
  36. Mullins, J. E., Groman, D. & Wadowska, D. ( 1998; ). Infectious salmon anaemia in salt water Atlantic salmon in New Brunswick, Canada. Bull Eur Assoc Fish Pathol 18, 110–115.
    [Google Scholar]
  37. Nichols, J. E., Mock, D. J. & Roberts, N. J., Jr ( 1993; ). Use of FITC-labeled influenza virus and flow cytometry to assess binding and internalization of virus by monocytes-macrophages and lymphocytes. Arch Virol 130, 441–445.[CrossRef]
    [Google Scholar]
  38. Nylund, A. & Jakobsen, P. ( 1995; ). Sea trout as a carrier of infectious salmon anaemia virus. J Fish Biol 47, 174–176.[CrossRef]
    [Google Scholar]
  39. Nylund, A., Kvenseth, A. M. & Krossøy, B. ( 1995; ). Susceptibility of wild salmon (Salmo salar L.) to infectious salmon anaemia (ISA). Bull Eur Assoc Fish Pathol 15, 152–156.
    [Google Scholar]
  40. Nylund, A., Kvenseth, A. M., Krossøy, B. & Hodneland, K. ( 1997; ). Replication of the infectious salmon anaemia virus (ISAV) in rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 20, 275–279.[CrossRef]
    [Google Scholar]
  41. Ochiai, H., Kurokawa, M., Hayashi, K. & Niwayama, S. ( 1988; ). Antibody-mediated growth of influenza A NWS virus in macrophagelike cell line P388D1. J Virol 62, 20–26.
    [Google Scholar]
  42. O'Dowd, A. M., Ellis, A. E. & Secombes, C. J. ( 1998; ). Binding of immune complexes to Atlantic salmon peripheral blood leucocytes. Dev Comp Immunol 22, 439–448.[CrossRef]
    [Google Scholar]
  43. Olsen, C. W., Corapi, W. V., Ngichabe, C. K., Baines, J. D. & Scott, F. W. ( 1992; ). Monoclonal antibodies to the spike protein of feline infectious peritonitis virus mediate antibody-dependent enhancement of infection of feline macrophages. J Virol 66, 956–965.
    [Google Scholar]
  44. Peiris, J. S., Gordon, S., Unkeless, J. C. & Porterfield, J. S. ( 1981; ). Monoclonal anti-Fc receptor IgG blocks antibody enhancement of viral replication in macrophages. Nature 289, 189–191.[CrossRef]
    [Google Scholar]
  45. Porterfield, J. S. ( 1986; ). Antibody-dependent enhancement of viral infectivity. Adv Virus Res 31, 335–355.
    [Google Scholar]
  46. Raynard, R. S., Murray, A. G. & Gregory, A. ( 2001; ). Infectious salmon anaemia virus in wild fish from Scotland. Dis Aquat Organ 46, 93–100.[CrossRef]
    [Google Scholar]
  47. Reed, L. J. & Muench, H. ( 1938; ). A simple method of estimating fifty percent endpoints. Am J Hyg 27, 493–497.
    [Google Scholar]
  48. Ritchie, R. J., Heppell, J., Cook, M. B., Jones, S. & Griffiths, S. G. ( 2001; ). Identification and characterization of segment 3 and 4 of the ISAV genome. Virus Genes 22, 289–297.[CrossRef]
    [Google Scholar]
  49. Rodger, H. D. & Richards, R. H. ( 1998; ). Haemorrhagic smolt syndrome: a severe anaemic condition in farmed salmon in Scotland. Vet Rec 142, 538–541.[CrossRef]
    [Google Scholar]
  50. Rolland, J. B., Bouchard, D. A. & Winton, J. R. ( 2002; ). The ASK cell line: an improved diagnostic tool for isolation, propagation and titration of the infectious salmon anaemia virus (ISAV). Proceedings of the ISA Symposium, IVth International Symposium on Aquatic Animal Health (New Orleans, Louisiana, USA, 3–4 September 2002).
  51. Sanchez, L., Abuin, M. & Amaro, R. ( 1993; ). Cytogenetic characterization of the AS cell line derived from the Atlantic salmon (Salmo salar L.). Cytogenet Cell Genet 64, 35–38.[CrossRef]
    [Google Scholar]
  52. Sommer, A. I. & Mennen, S. ( 1997; ). Multiplication and haemadsorbing activity of infectious salmon anaemia virus in the established Atlantic salmon cell line. J Gen Virol 78, 1891–1895.
    [Google Scholar]
  53. Stoddart, C. A. ( 1989; ). Role of virus–macrophage interactions in the pathogenesis of feline coronavirus infection, chapter 4, pp. 125–156. PhD thesis, Cornell University, Ithaca, New York, USA.
  54. Sullivan, N. J. ( 2001; ). Antibody-mediated enhancement of viral disease. Curr Top Microbiol Immunol 260, 145–169.
    [Google Scholar]
  55. Takeda, A., Tuazon, C. U. & Ennis, F. A. ( 1988; ). Antibody-enhanced infection by HIV-1 via Fc receptor-mediated entry. Science 242, 580–583.[CrossRef]
    [Google Scholar]
  56. Thorud, K. & Djupvik, H. O. ( 1988; ). Infectious salmon anaemia in Atlantic salmon (Salmo salar L.). Bull Eur Assoc Fish Pathol 8, 109–111.
    [Google Scholar]
  57. Urabe, M. T., Tanaka, T., Odagiri, M., Tashiro, M. & Tobita, K. ( 1993; ). Persistence of viral genes in a variant of MDBK cell after productive replication of a mutant of influenza virus A/WSN. Arch Virol 128, 97–110.[CrossRef]
    [Google Scholar]
  58. Webster, R. G. ( 1999; ). Influenza viruses (Orthomyxoviridae). In Encyclopaedia of Virology, 2nd edn, pp. 824–829. Edited by A. Granoff & R. G. Webster. New York: Academic Press.
  59. Wergeland, H. I. & Jakobsen, R. A. ( 2001; ). A salmonid cell line (TO) for production of infectious salmon anaemia virus (ISAV). Dis Aquat Organ 44, 183–190.[CrossRef]
    [Google Scholar]
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