1887

Abstract

Many fish undergo betanodavirus infection. To study the infection process of dragon grouper nervous necrosis virus (DGNNV), native virus and virus-like particles (VLPs) were used to analyse the binding and internalization in SSN-1 cells. The binding of DGNNV and VLPs to SSN-1 cells was demonstrated using Western blotting and immunofluorescence microscopy. As estimated by indirect ELISA, the DGNNV particles bound SSN-1 cells in a dose-dependent manner up to 8×10 particles per cell. The binding of VLPs was sensitive to neuraminidase and tunicamycin, suggesting that cell-surface sialic acid is involved in binding. The penetration of DGNNV into cells, which was monitored by electron microscopy, appeared to occur mainly via the spherical pit and membrane ruffling pathways. Occasionally, a spherical pit was engulfed by membrane ruffling so as to form a large figure-of-eight-shaped vesicle with an open connection. Our observations suggest that DGNNV utilizes both micro- and macropinocytosis pathways to enter SSN-1 cells.

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2005-09-01
2019-11-14
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References

  1. Belnap, D. M., Filman, D. J., Trus, B. L. & 8 other authors ( 2000; ). Molecular tectonic model of virus structural transitions: the putative cell entry states of poliovirus. J Virol 74, 1342–1354.[CrossRef]
    [Google Scholar]
  2. Bibb, J. A., Witherell, G., Bernhardt, G. & Wimmer, E. ( 1994; ). Interaction of poliovirus with its cell-surface binding site. Virology 201, 107–115.[CrossRef]
    [Google Scholar]
  3. Bousarghin, L., Touzé, A., Sizaret, P. Y. & Coursaget, P. ( 2003; ). Human papillomavirus types 16, 31, and 58 use different endocytosis pathways to enter cells. J Virol 77, 3846–3850.[CrossRef]
    [Google Scholar]
  4. Comps, M., Trindade, M. & Delsert, C. ( 1996; ). Investigation of fish encephalitis viruses (FEV) expression in marine fishes using DIG-labelled probes. Aquaculture 143, 113–121.[CrossRef]
    [Google Scholar]
  5. Dimitrov, D. S. ( 2000; ). Cell biology of virus entry. Cell 101, 697–702.[CrossRef]
    [Google Scholar]
  6. Frerichs, G. N., Morgan, D., Hart, D., Skerrow, C., Roberts, R. J. & Onions, D. E. ( 1991; ). Spontaneously productive C-type retrovirus infection of fish cell lines. J Gen Virol 72, 2537–2539.[CrossRef]
    [Google Scholar]
  7. Greve, J. M., Davis, G., Meyer, A. M., Forte, C. P., Yost, S. C., Marlor, C. W., Kamarck, M. E. & McClelland, A. ( 1989; ). The major human rhinovirus receptor is ICAM-1. Cell 56, 839–847.[CrossRef]
    [Google Scholar]
  8. Hatton, M. W. & Regoeczi, E. ( 1973; ). A simple method for the purification of commercial neuraminidase preparations free from proteases. Biochim Biophys Acta 327, 114–120.[CrossRef]
    [Google Scholar]
  9. Hurley, J. H. & Meyer, T. ( 2001; ). Subcellular targeting by membrane lipids. Curr Opin Cell Biol 13, 146–152.[CrossRef]
    [Google Scholar]
  10. Iwamoto, T., Okinaka, Y., Mise, K., Mori, K. I., Arimoto, M., Okuno, T. & Nakai, T. ( 2004; ). Identification of host-specificity determinants in betanodaviruses by using reassortants between striped jack nervous necrosis virus and sevenband grouper nervous necrosis virus. J Virol 78, 1256–1262.[CrossRef]
    [Google Scholar]
  11. Johnson, J. E. & Rueckert, R. R. ( 1997; ). Packaging and release of viral genome. In Structural Biology of Viruses, pp. 269–287. Edited by W. Chiu, R. M. Burnett & R. L. Garcea. New York: Oxford University Press.
  12. Kirchhausen, T. ( 2000; ). Three ways to make a vesicle. Nat Rev Mol Cell Biol 1, 187–198.[CrossRef]
    [Google Scholar]
  13. Lai, Y. S., Chiu, H. C., Murali, S., Guo, I. C., Chen, S. C., Fang, K. & Chang, C. Y. ( 2001; ). In vitro neutralization by monoclonal antibodies against yellow grouper nervous necrosis virus (YGNNV) and immunolocalization of virus infection in yellow grouper, Epinephelus awoara (Temminck & Schlegel). J Fish Dis 24, 237–244.[CrossRef]
    [Google Scholar]
  14. Lin, C. S., Lu, M. W., Tang, L., Liu, W., Chao, C. B., Lin, C. J., Krishna, N. K., Johnson, J. E. & Schneemann, A. ( 2001; ). Characterization of virus-like particles assembled in a recombinant baculovirus system expressing the capsid protein of a fish nodavirus. Virology 290, 50–58.[CrossRef]
    [Google Scholar]
  15. Lu, M. W. & Lin, C. S. ( 2003; ). Involvement of the terminus of grouper betanodavirus capsid protein in virus-like particle assembly. Arch Virol 148, 345–355.[CrossRef]
    [Google Scholar]
  16. Lu, M. W., Liu, W. & Lin, C. S. ( 2003; ). Infection competition against grouper nervous necrosis virus by virus-like particles produced in Escherichia coli. J Gen Virol 84, 1577–1582.[CrossRef]
    [Google Scholar]
  17. Mañes, S., Mira, E., Gómez-Moutón, C., Lacalle, R. A., Keller, P., Labrador, J. P. & Martínez-A, C. ( 1999; ). Membrane raft microdomains mediate front–rear polarity in migrating cells. EMBO J 18, 6211–6220.[CrossRef]
    [Google Scholar]
  18. Maniak, M. ( 2003; ). Macropinocytosis. In Endocytosis, pp. 78–93. Edited by M. Marsh. New York: Oxford University Press.
  19. McPherson, P. S., Kay, B. K. & Hussain, N. K. ( 2001; ). Signaling on the endocytic pathway. Traffic 2, 375–384.[CrossRef]
    [Google Scholar]
  20. Meier, O. & Greber, U. F. ( 2004; ). Adenovirus endocytosis. J Gene Med 6, S152–S163.[CrossRef]
    [Google Scholar]
  21. Meier, O., Boucke, K., Hammer, S. V., Keller, S., Stidwill, R. P., Hemmi, S. & Greber, U. F. ( 2002; ). Adenovirus triggers macropinocytosis and endosomal leakage together with its clathrin-mediated uptake. J Cell Biol 158, 1119–1131.[CrossRef]
    [Google Scholar]
  22. Mori, K. I., Nakai, T., Muroga, K., Arimoto, M., Mushiake, K. & Furusawa, I. ( 1992; ). Properties of a new virus belonging to nodaviridae found in larval striped jack (Pseudocaranx dentex) with nervous necrosis. Virology 187, 368–371.[CrossRef]
    [Google Scholar]
  23. Mori, K., Mangyoku, T., Iwamoto, T., Arimoto, M., Tanaka, S. & Nakai, T. ( 2003; ). Serological relationships among genotypic variants of betanodavirus. Dis Aquat Organ 57, 19–26.[CrossRef]
    [Google Scholar]
  24. Müller, M., Gissmann, L., Cristiano, R. J., Sun, X. Y., Frazer, I. H., Jenson, A. B., Alonso, A., Zentgraf, H. & Zhou, J. ( 1995; ). Papillomavirus capsid binding and uptake by cells from different tissues and species. J Virol 69, 948–954.
    [Google Scholar]
  25. Munday, B. L. & Nakai, T. ( 1997; ). Special topic review: nodaviruses as pathogens in larval and juvenile marine finfish. World J Microbiol Biotechnol 13, 375–381.[CrossRef]
    [Google Scholar]
  26. Munday, B. L., Kwang, J. & Moody, N. ( 2002; ). Betanodavirus infections of teleost fish: a review. J Fish Dis 25, 127–142.[CrossRef]
    [Google Scholar]
  27. Nemerow, G. R. ( 2000; ). Cell receptors involved in adenovirus entry. Virology 274, 1–4.[CrossRef]
    [Google Scholar]
  28. Rittig, M. G., Jagoda, J. C., Wilske, B., Murgia, R., Cinco, M., Repp, R., Burmester, G. R. & Krause, A. ( 1998; ). Coiling phagocytosis discriminates between different spirochetes and is enhanced by phorbol myristate acetate and granulocyte-macrophage colony-stimulating factor. Infect Immun 66, 627–635.
    [Google Scholar]
  29. Sieczkarski, S. B. & Whittaker, G. R. ( 2002; ). Dissecting virus entry via endocytosis. J Gen Virol 83, 1535–1545.
    [Google Scholar]
  30. Smith, A. E. & Helenius, A. ( 2004; ). How viruses enter animal cells. Science 304, 237–242.[CrossRef]
    [Google Scholar]
  31. Tang, L., Lin, C. S., Krishna, N. K., Yeager, M., Schneemann, A. & Johnson, J. E. ( 2002; ). Virus-like particles of a fish nodavirus display a capsid subunit domain organization different from that of insect nodaviruses. J Virol 76, 6370–6375.[CrossRef]
    [Google Scholar]
  32. Volpers, C., Unckell, F., Schirmacher, P., Streeck, R. E. & Sapp, M. ( 1995; ). Binding and internalization of human papillomavirus type 33 virus-like particles by eukaryotic cells. J Virol 69, 3258–3264.
    [Google Scholar]
  33. White, J. M. ( 1993; ). Integrins as virus receptors. Curr Biol 3, 596–599.[CrossRef]
    [Google Scholar]
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