1887

Abstract

The early phase after hepatitis B virus infection could play a crucial role in clearance and/or persistence of the virus, particularly in neonates. This work compared the early phase of duck hepatitis B virus infection in 1-day-old (D1) and 28-day-old (D28) ducks to determine whether differences in viral or host innate immune response can be related to the difference in outcome. In the first phase, almost immediately after inoculation, virus was taken up by components of the reticulo-endothelial systems, particularly liver-specific macrophages, Kupffer cells. Very early after infection, the induction of alpha interferon by infected hepatocytes occurred and was rapidly reinforced by recruitment of effector lymphocytes, which directly or indirectly caused apoptosis, eliminating infected hepatocytes, as was seen in mature birds. In addition, a lack of lymphocytic infiltration of the liver was found in D1 ducks, which supports the suggestion that the innate immune network is less effective in D1 ducks. Taken together, these results suggest that failure of the co-ordinated innate immune response rather than a defect in induced antiviral cell-mediated immunity may be the key factor which makes baby ducks vulnerable to persistence of hepadnavirus infection.

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2010-02-01
2019-11-19
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References

  1. Anderson, D. A., Grgacic, E. V., Luscombe, C. A., Gu, X. & Dixon, R. ( 1997; ). Quantification of infectious duck hepatitis B virus by radioimmunofocus assay. J Med Virol 52, 354–361.[CrossRef]
    [Google Scholar]
  2. Breiner, K. M., Schaller, H. & Knolle, P. A. ( 2001; ). Endothelial cell-mediated uptake of a hepatitis B virus: a new concept of liver targeting of hepatotropic microorganisms. Hepatology 34, 803–808.[CrossRef]
    [Google Scholar]
  3. Brunner, K. T., Hurez, D., Mc, C. R. & Benacerraf, B. ( 1960; ). Blood clearance of P32-labeled vesicular stomatitis and Newcastle disease viruses by the reticuloendothelial system in mice. J Immunol 85, 99–105.
    [Google Scholar]
  4. Chisari, F. V. ( 1995; ). Hepatitis B virus transgenic mice: insights into the virus and the disease. Hepatology 22, 1316–1325.
    [Google Scholar]
  5. Cogger, V. C., Warren, A., Fraser, R., Ngu, M., McLean, A. J. & Le Couteur, D. G. ( 2003; ). Hepatic sinusoidal pseudocapillarization with aging in the non-human primate. Exp Gerontol 38, 1101–1107.[CrossRef]
    [Google Scholar]
  6. Couderc, T., Chrétien, F., Schilte, C., Disson, O., Brigitte, M., Guivel-Benhassine, F., Touret, Y., Barau, G., Cayet, N. & other authors ( 2008; ). A mouse model for Chikungunya: young age and inefficient type-I interferon signaling are risk factors for severe disease. PLoS Pathog 4, e29 [CrossRef]
    [Google Scholar]
  7. Dobson, E. L. & Jones, H. B. ( 1952; ). The behavior of intravenously injected particulate material; its rate of disappearance from the blood stream as a measure of liver blood flow. Acta Med Scand Suppl 273, 1–71.
    [Google Scholar]
  8. Freiman, J. S., Jilbert, A. R., Dixon, R. J., Holmes, M., Gowans, E. J., Burrell, C. J., Wills, E. J. & Cossart, Y. E. ( 1988; ). Experimental duck hepatitis B virus infection: pathology and evolution of hepatic and extrahepatic infection. Hepatology 8, 507–513.[CrossRef]
    [Google Scholar]
  9. Freiman, J. S., Murray, S. M., Vickery, K., Lim, D. & Cossart, Y. E. ( 1990; ). Postexposure treatment of experimental DHBV infection: a new therapeutic strategy. J Med Virol 30, 272–276.[CrossRef]
    [Google Scholar]
  10. Fukuda, R., Fukumoto, S. & Shimada, Y. ( 1987; ). A sequential study of viral DNA in serum in experimental transmission of duck hepatitis B virus. J Med Virol 21, 311–320.[CrossRef]
    [Google Scholar]
  11. Galle, P. R., Schlicht, H. J., Kuhn, C. & Schaller, H. ( 1989; ). Replication of duck hepatitis B virus in primary duck hepatocytes and its dependence on the state of differentiation of the host cell. Hepatology 10, 459–465.[CrossRef]
    [Google Scholar]
  12. Heuss, L. T., Heim, M. H., Schultz, U., Wissmann, D., Offensperger, W. B., Staeheli, P. & Blum, H. E. ( 1998; ). Biological efficacy and signal transduction through STAT proteins of recombinant duck interferon in duck hepatitis B virus infection. J Gen Virol 79, 2007–2012.
    [Google Scholar]
  13. Jeurissen, S. H., Claassen, E. & Janse, E. M. ( 1992; ). Histological and functional differentiation of non-lymphoid cells in the chicken spleen. Immunology 77, 75–80.
    [Google Scholar]
  14. Jilbert, A. R., Wu, T. T., England, J. M., Hall, P. M., Carp, N. Z., O'Connell, A. P. & Mason, W. S. ( 1992; ). Rapid resolution of duck hepatitis B virus infections occurs after massive hepatocellular involvement. J Virol 66, 1377–1388.
    [Google Scholar]
  15. Jilbert, A. R., Miller, D. S., Scougall, C. A., Turnbull, H. & Burrell, C. J. ( 1996; ). Kinetics of duck hepatitis B virus infection following low dose virus inoculation: one virus DNA genome is infectious in neonatal ducks. Virology 226, 338–345.[CrossRef]
    [Google Scholar]
  16. Keating, G. M. & Noble, S. ( 2003; ). Recombinant hepatitis B vaccine (Engerix-B): a review of its immunogenicity and protective efficacy against hepatitis B. Drugs 63, 1021–1051.[CrossRef]
    [Google Scholar]
  17. Kuroki, K., Eng, F., Ishikawa, T., Turck, C., Harada, F. & Ganem, D. ( 1995; ). gp180, a host cell glycoprotein that binds duck hepatitis B virus particles, is encoded by a member of the carboxypeptidase gene family. J Biol Chem 270, 15022–15028.[CrossRef]
    [Google Scholar]
  18. Lavine, J. E. & Ganem, D. ( 1993; ). Inhibition of duck hepatitis B virus replication by interferon-gamma. J Med Virol 40, 59–64.[CrossRef]
    [Google Scholar]
  19. Le Couteur, D. G., Cogger, V. C., Markus, A. M., Harvey, P. J., Yin, Z. L., Ansselin, A. D. & McLean, A. J. ( 2001; ). Pseudocapillarization and associated energy limitation in the aged rat liver. Hepatology 33, 537–543.[CrossRef]
    [Google Scholar]
  20. Lehmann-Grube, F., Tijerina, R., Zeller, W., Chaturvedi, U. C. & Lohler, J. ( 1983; ). Age-dependent susceptibility of murine T lymphocytes to lymphocytic choriomeningitis virus. J Gen Virol 64, 1157–1166.[CrossRef]
    [Google Scholar]
  21. Le Mire, M. F., Miller, D. S., Foster, W. K., Burrell, C. J. & Jilbert, A. R. ( 2005; ). Covalently closed circular DNA is the predominant form of duck hepatitis B virus DNA that persists following transient infection. J Virol 79, 12242–12252.[CrossRef]
    [Google Scholar]
  22. MacDonald, M. R., Xia, J., Smith, A. L. & Magor, K. E. ( 2008; ). The duck toll like receptor 7: genomic organization, expression and function. Mol Immunol 45, 2055–2061.[CrossRef]
    [Google Scholar]
  23. Marion, P. L., Knight, S. S., Ho, B. K., Guo, Y. Y., Robinson, W. S. & Popper, H. ( 1984; ). Liver disease associated with duck hepatitis B virus infection of domestic ducks. Proc Natl Acad Sci U S A 81, 898–902.[CrossRef]
    [Google Scholar]
  24. McLean, A. J., Cogger, V. C., Chong, G. C., Warren, A., Markus, A. M., Dahlstrom, J. E. & Le Couteur, D. G. ( 2003; ). Age-related pseudocapillarization of the human liver. J Pathol 200, 112–117.[CrossRef]
    [Google Scholar]
  25. Mims, C. A. ( 1959; ). The response of mice to large intravenous injections of ectromelia virus. I. The fate of injected virus. Br J Exp Pathol 40, 533–542.
    [Google Scholar]
  26. Murray, J. M., Wieland, S. F., Purcell, R. H. & Chisari, F. V. ( 2005; ). Dynamics of hepatitis B virus clearance in chimpanzees. Proc Natl Acad Sci U S A 102, 17780–17785.[CrossRef]
    [Google Scholar]
  27. Narayan, R., Buronfosse, T., Schultz, U., Chevallier-Gueyron, P., Guerret, S., Chevallier, M., Saade, F., Ndeboko, B., Trepo, C. & other authors ( 2006; ). Rise in gamma interferon expression during resolution of duck hepatitis B virus infection. J Gen Virol 87, 3225–3232.[CrossRef]
    [Google Scholar]
  28. Portman, O. W., McConnell, K. P. & Rigdon, R. H. ( 1952; ). Blood volumes of ducks using human serum albumin labeled with radio-iodine. Proc Soc Exp Biol Med 81, 599–601.[CrossRef]
    [Google Scholar]
  29. Pugh, J. C. & Summers, J. W. ( 1989; ). Infection and uptake of duck hepatitis B virus by duck hepatocytes maintained in the presence of dimethyl sulfoxide. Virology 172, 564–572.[CrossRef]
    [Google Scholar]
  30. Pugh, J. C., Di, Q., Mason, W. S. & Simmons, H. ( 1995; ). Susceptibility to duck hepatitis B virus infection is associated with the presence of cell surface receptor sites that efficiently bind viral particles. J Virol 69, 4814–4822.
    [Google Scholar]
  31. Qiao, M., Gowans, E. J. & Burrell, C. J. ( 1992; ). Intracellular factors, but not virus receptor levels, influence the age-related outcome of DHBV infection of ducks. Virology 186, 517–523.[CrossRef]
    [Google Scholar]
  32. Schultz, U. & Chisari, F. V. ( 1999; ). Recombinant duck interferon gamma inhibits duck hepatitis B virus replication in primary hepatocytes. J Virol 73, 3162–3168.
    [Google Scholar]
  33. Schultz, U., Kock, J., Schlicht, H. J. & Staeheli, P. ( 1995; ). Recombinant duck interferon: a new reagent for studying the mode of interferon action against hepatitis B virus. Virology 212, 641–649.[CrossRef]
    [Google Scholar]
  34. Srivastava, A. S., Kaido, T. & Carrier, E. ( 2004; ). Immunological factors that affect the in vivo fate of T7 phage in the mouse. J Virol Methods 115, 99–104.[CrossRef]
    [Google Scholar]
  35. Thimme, R., Wieland, S., Steiger, C., Ghrayeb, J., Reimann, K. A., Purcell, R. H. & Chisari, F. V. ( 2003; ). CD8(+) T cells mediate viral clearance and disease pathogenesis during acute hepatitis B virus infection. J Virol 77, 68–76.[CrossRef]
    [Google Scholar]
  36. Uchida, T., Suzuki, K., Okuda, Y. & Shikata, T. ( 1988; ). In vitro transmission of duck hepatitis B virus to primary duck hepatocyte cultures. Hepatology 8, 760–765.[CrossRef]
    [Google Scholar]
  37. Vickery, K. ( 1994; ). The humoral and cellular responses to duck hepatitis B virus. PhD thesis, University of Sydney.
  38. Vickery, K. & Cossart, Y. ( 1996; ). DHBV manipulation and prediction of the outcome of infection. J Hepatol 25, 504–509.[CrossRef]
    [Google Scholar]
  39. Vickery, K., Freiman, J. S., Dixon, R. J., Kearney, R., Murray, S. & Cossart, Y. E. ( 1989; ). Immunity in Pekin ducks experimentally and naturally infected with duck hepatitis B virus. J Med Virol 28, 231–236.[CrossRef]
    [Google Scholar]
  40. Vickery, K., Tohidi-Esfahani, R., Pouliopoulos, J., Welschinger, R., Dixon, R., Deva, A. & Cossart, Y. ( 2006; ). The effect of surgical immunomodulation on liver inflammation and clearance of DHBV infection. J Med Virol 78, 1572–1578.[CrossRef]
    [Google Scholar]
  41. Walter, E., Teubner, K., Blum, H. E., Offensperger, W. B., Offensperger, S. & Gerok, W. ( 1991; ). Duck hepatitis B virus infection of non-hepatocytes. Liver 11, 53–62.
    [Google Scholar]
  42. Warren, A., Bertolino, P., Cogger, V. C., McLean, A. J., Fraser, R. & Le Couteur, D. G. ( 2005; ). Hepatic pseudocapillarization in aged mice. Exp Gerontol 40, 807–812.[CrossRef]
    [Google Scholar]
  43. White, R. G. ( 1969; ). Recognition mechanisms in the chicken spleen. Antibiot Chemother 15, 24–39.
    [Google Scholar]
  44. Zhang, Y. Y. & Summers, J. ( 2004; ). Rapid production of neutralizing antibody leads to transient hepadnavirus infection. J Virol 78, 1195–1201.[CrossRef]
    [Google Scholar]
  45. Zhang, Y. Y., Theele, D. P. & Summers, J. ( 2005; ). Age-related differences in amplification of covalently closed circular DNA at early times after duck hepatitis B virus infection of ducks. J Virol 79, 9896–9903.[CrossRef]
    [Google Scholar]
  46. Zhang, X., Deriaud, E., Jiao, X., Braun, D., Leclerc, C. & Lo-Man, R. ( 2007; ). Type I interferons protect neonates from acute inflammation through interleukin 10-producing B cells. J Exp Med 204, 1107–1118.[CrossRef]
    [Google Scholar]
  47. Zilversmit, D. B., Boyd, G. A. & Brucer, M. ( 1952; ). The effect of particle size on blood clearance and tissue distribution of radioactive gold colloids. J Lab Clin Med 40, 255–260.
    [Google Scholar]
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