1887

Abstract

The kinetics of infectious bursal disease virus (IBDV) replication and induction of apoptosis were investigated and After infection of chicken embryo (CE) cells with IBDV strain Cu-1, the proportion of apoptotic cells increased from 5·8% at 4 h post-infection (p.i.) to 64·5% at 48 h p.i. The proportion of apoptotic cells correlated with IBDV replication. UV-inactivated IBDV particles did not induce apoptosis. Double labelling revealed that, early after infection, the majority of antigen-expressing cells were not apoptotic; double-labelled cells appeared more frequently at later times. Remarkably, apoptotic cells were frequently located in the vicinity of antigen-expressing cells. This indicated that an apoptosis-inducing factor(s) might be released by cells that replicate IBDV. Since interferon (IFN) production has been demonstrated after IBDV infection, IFN was considered to be one of several factors. However, supernatants of infected CE cells in which virus infectivity had been neutralized were not sufficient to induce apoptosis.Similar results were observed in the infected bursae of Fabricius: early after infection, most of the cells either showed virus antigens or were apoptotic. Again, double-labelled cells appeared more frequently late after infection. This suggests that indirect mechanisms might also be involved in the induction of apoptosis , contributing to the rapid depletion of cells in the IBDV-infected bursa.

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2001-05-01
2019-10-17
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References

  1. Adler, B., Adler, H., Pfister, H., Jungi, T. W. & Peterhans, E. ( 1997; ). Macrophages infected with cytopathic bovine viral diarrhea virus release a factor(s) capable of priming uninfected macrophages for activation-induced apoptosis. Journal of Virology 71, 3255-3258.
    [Google Scholar]
  2. Becht, H. & Müller, H. ( 1991; ). Infectious bursal disease – a B cell dependent immunodeficiency syndrome in chickens. Behring Institute Mitteilungen 89, 217-225.
    [Google Scholar]
  3. Bergmann, M., Garcia-Sastre, A., Carnero, E., Pehamberger, H., Wolff, K., Palese, P. & Muster, T. ( 2000; ). Influenza virus NS1 protein counteracts PKR-mediated inhibition of replication. Journal of Virology 74, 6203-6206.[CrossRef]
    [Google Scholar]
  4. Birghan, C., Mundt, E. & Gorbalenya, A. E. ( 2000; ). A non-canonical lon proteinase lacking the ATPase domain employs the Ser–Lys catalytic dyad to exercise broad control over the life cycle of a double-stranded RNA virus. EMBO Journal 19, 114-123.[CrossRef]
    [Google Scholar]
  5. Burkhardt, E. & Müller, H. ( 1987; ). Susceptibility of chicken blood lymphoblasts and monocytes to infectious bursal disease virus (IBDV). Archives of Virology 94, 297-303.[CrossRef]
    [Google Scholar]
  6. Cursiefen, D., Käufer, I. & Becht, H. ( 1979; ). Loss of virulence in a small plaque mutant of the infectious bursal disease virus. Archives of Virology 59, 39-46.[CrossRef]
    [Google Scholar]
  7. Fernandez-Arias, A., Martinez, S. & Rodriguez, J. F. ( 1997; ). The major antigenic protein of infectious bursal disease virus, VP2, is an apoptotic inducer. Journal of Virology 71, 8014-8018.
    [Google Scholar]
  8. Gelb, J., Eidson, C. S., Fletcher, O. J. & Kleven, S. H. ( 1979a; ). Studies on interferon induction by infectious bursal disease virus (IBDV). I. Interferon production in chicken embryo cell cultures infected with IBDV. Avian Diseases 23, 485-492.[CrossRef]
    [Google Scholar]
  9. Gelb, J., Eidson, C. S., Fletcher, O. J. & Kleven, S. H. ( 1979b; ). Studies on interferon induction by infectious bursal disease virus (IBDV). II. Interferon production in White Leghorn chickens infected with an attenuated or pathogenic isolate of IBDV. Avian Diseases 23, 634-645.[CrossRef]
    [Google Scholar]
  10. Hong, J. R., Lin, T. L., Hsu, Y. L. & Wu, J. L. ( 1998; ). Apoptosis precedes necrosis of fish cell line with infectious pancreatic necrosis virus infection. Virology 250, 76-84.[CrossRef]
    [Google Scholar]
  11. Hudson, P. J., McKern, N. M., Power, B. E. & Azad, A. A. ( 1986; ). Genomic structure of the large RNA segment of infectious bursal disease virus. Nucleic Acids Research 14, 5001-5012.[CrossRef]
    [Google Scholar]
  12. Inoue, M., Fukuda, M. & Miyano, K. ( 1994; ). Thymic lesions in chicken infected with infectious bursal disease virus. Avian Diseases 38, 839-846.[CrossRef]
    [Google Scholar]
  13. Jacobs, B. L. & Langland, J. O. ( 1996; ). When two strands are better than one: the mediators and modulators of the cellular responses to double-stranded RNA. Virology 219, 339-349.[CrossRef]
    [Google Scholar]
  14. Käufer, I. & Weiss, E. ( 1976; ). Electron-microscope studies on the pathogenesis of infectious bursal disease after intrabursal application of the causal virus. Avian Diseases 20, 483-495.[CrossRef]
    [Google Scholar]
  15. Käufer, I. & Weiss, E. ( 1980; ). Significance of bursa of Fabricius as target organ in infectious bursal disease of chickens. Infection and Immunity 27, 364-367.
    [Google Scholar]
  16. Kibenge, F. S. B., Dhillon, A. S. & Russell, R. G. ( 1988; ). Biochemistry and immunology of infectious bursal disease virus. Journal of General Virology 69, 1757-1775.[CrossRef]
    [Google Scholar]
  17. Kibler, K. V., Shors, T., Perkins, K. B., Zeman, C. C., Banaszak, M. P., Biesterfeldt, J., Langland, J. O. & Jacobs, B. L. ( 1997; ). Double-stranded RNA is a trigger for apoptosis in vaccinia virus-infected cells. Journal of Virology 71, 1992-2003.
    [Google Scholar]
  18. Lam, K. M. ( 1997; ). Morphological evidence of apoptosis in chickens infected with infectious bursal disease virus. Journal of Comparative Pathology 116, 367-377.[CrossRef]
    [Google Scholar]
  19. Lange, H., Müller, H., Käufer, I. & Becht, H. ( 1987; ). Pathogenic and structural properties of wild type infectious bursal disease virus (IBDV) and virus grown in vitro. Archives of Virology 92, 187-196.[CrossRef]
    [Google Scholar]
  20. Lee, S. B. & Esteban, M. ( 1994; ). The interferon-induced double-stranded RNA-activated protein kinase induces apoptosis. Virology 199, 491-496.[CrossRef]
    [Google Scholar]
  21. Lejal, N., Da Costa, B., Huet, J.-C. & Delmas, B. ( 2000; ). Role of Ser-652 and Lys-692 in the protease activity of infectious bursal disease virus VP4 and identification of its substrate cleavage sites. Journal of General Virology 81, 983-992.
    [Google Scholar]
  22. Martin, S. J., Reutelingsperger, C. P., McGahon, A. J., Rader, J. A., van Schie, R. C., LaFace, D. M. & Green, D. R. ( 1995; ). Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. Journal of Experimental Medicine 182, 1545-1556.[CrossRef]
    [Google Scholar]
  23. Müller, H. ( 1986; ). Replication of infectious bursal disease virus in lymphoid cells. Archives of Virology 87, 191-203.[CrossRef]
    [Google Scholar]
  24. Müller, H. & Becht, H. ( 1982; ). Biosynthesis of virus-specific proteins in cells infected with infectious bursal disease virus and their significance as structural elements for infectious virus and incomplete particles. Journal of Virology 44, 384-392.
    [Google Scholar]
  25. Müller, H., Scholtissek, C. & Becht, H. ( 1979; ). The genome of infectious bursal disease virus consists of two segments of double-stranded RNA. Journal of Virology 31, 584-589.
    [Google Scholar]
  26. Mundt, E., Beyer, J. & Müller, H. ( 1995; ). Identification of a novel viral protein in infectious bursal disease virus-infected cells. Journal of General Virology 76, 437-443.[CrossRef]
    [Google Scholar]
  27. Nick, H., Cursiefen, D. & Becht, H. ( 1976; ). Structural and growth characteristics of infectious bursal disease virus. Journal of Virology 18, 227-234.
    [Google Scholar]
  28. Nieper, H. & Müller, H. ( 1996; ). Susceptibility of chicken lymphoid cells to infectious bursal disease virus does not correlate with the presence of specific binding sites. Journal of General Virology 77, 1229-1237.[CrossRef]
    [Google Scholar]
  29. Nieper, H., Teifke, J. P., Jungmann, A., Löhr, C. V. & Müller, H. ( 1999; ). Infected and apoptotic cells in the IBDV-infected bursa of Fabricius, studied by double-labelling techniques. Avian Pathology 28, 279-285.[CrossRef]
    [Google Scholar]
  30. Ojeda, F., Skardova, I., Guarda, M. I., Ulloa, J. & Folch, H. ( 1997; ). Proliferation and apoptosis in infection with infectious bursal disease virus: a flow cytometric study. Avian Diseases 41, 312-316.[CrossRef]
    [Google Scholar]
  31. Öppling, V. (1991). Die Induktion neutralisierender Antikörper durch das Strukturprotein VP2 des Virus der infektiösen Bursitis (IBDV). PhD Thesis, Justus-Liebig-Universität Giessen, Germany.
  32. Perler, L., Schweizer, M., Jungi, T. W. & Peterhans, E. ( 2000; ). Bovine viral diarrhoea virus and bovine herpesvirus-1 prime uninfected macrophages for lipopolysaccharide-triggered apoptosis by interferon-dependent and -independent pathways. Journal of General Virology 81, 881-887.
    [Google Scholar]
  33. Rosenberger, J. K., Cloud, S. S., Gelb, J., Odor, E. & Dohms, J. E. (1985). Sentinel bird survey of Delmarva broiler flocks. In Proceedings of the 20th National Meeting of Poultry Health and Condemnations, pp. 194–202. Ocean City, MD, USA.
  34. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  35. Sanchez, A. B. & Rodriguez, J. F. ( 1999; ). Proteolytic processing in infectious bursal disease virus: identification of the polyprotein cleavage sites by site-directed mutagenesis. Virology 262, 190-199.[CrossRef]
    [Google Scholar]
  36. Sharma, J. M., Dohms, J., Walser, M. & Snyder, D. B. ( 1993; ). Presence of lesions without virus replication in the thymus of chickens exposed to infectious bursal disease virus. Avian Diseases 37, 741-748.[CrossRef]
    [Google Scholar]
  37. Shen, Y. & Shenk, T. E. ( 1995; ). Viruses and apoptosis. Current Opinion in Genetics & Development 5, 105-111.[CrossRef]
    [Google Scholar]
  38. Superti, F., Ammendolia, M. G., Tinari, A., Bucci, B., Giammarioli, A. M., Rainaldi, G., Rivabene, R. & Donelli, G. ( 1996; ). Induction of apoptosis in HT-29 cells infected with SA-11 rotavirus. Journal of Medical Virology 50, 325-334.[CrossRef]
    [Google Scholar]
  39. Tanimura, N. & Sharma, J. M. ( 1998; ). In-situ apoptosis in chicken infected with infectious bursal disease virus. Journal of Comparative Pathology 118, 15-27.[CrossRef]
    [Google Scholar]
  40. Telford, W. G., King, L. E. & Fraker, P. J. ( 1994; ). Rapid quantitation of apoptosis in pure and heterogeneous cell populations using flow cytometry. Journal of Immunological Methods 172, 1-16.[CrossRef]
    [Google Scholar]
  41. Teodoro, J. G. & Branton, P. E. ( 1997; ). Regulation of apoptosis by viral gene products. Journal of Virology 71, 1739-1746.
    [Google Scholar]
  42. Tham, K. M. & Moon, C. D. ( 1996; ). Apoptosis in cell culture induced by infectious bursal disease virus following in vitro infection. Avian Diseases 40, 109-113.[CrossRef]
    [Google Scholar]
  43. Vasconcelos, A. C. & Lam, K. M. ( 1994; ). Apoptosis induced by infectious bursal disease virus. Journal of General Virology 75, 1803-1806.[CrossRef]
    [Google Scholar]
  44. Vasconcelos, A. C. & Lam, K. M. ( 1995; ). Apoptosis in chicken embryos induced by the infectious bursal disease virus. Journal of Comparative Pathology 112, 327-338.[CrossRef]
    [Google Scholar]
  45. Yao, K., Goodwin, M. A. & Vakharia, V. N. ( 1998; ). Generation of a mutant infectious bursal disease virus that does not cause bursal lesions. Journal of Virology 72, 2647-2654.
    [Google Scholar]
  46. Yue, Z. & Shatkin, A. J. ( 1997; ). Double-stranded RNA-dependent protein kinase (PKR) is regulated by reovirus structural proteins. Virology 234, 364-371.[CrossRef]
    [Google Scholar]
  47. Zierenberg, K., Nieper, H., van den Berg, T. P., Ezeokoli, C. D., Voss, M. & Müller, H. ( 2000; ). The VP2 variable region of African and German isolates of infectious bursal disease virus: comparison with very virulent, ‘classical’ virulent, and attenuated tissue culture-adapted strains. Archives of Virology 145, 113-125.[CrossRef]
    [Google Scholar]
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