1887

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Volume 71, Issue 9

Ducks: a new experimental host system for studying persistent infection with avian leukaemia retroviruses Free

Abstract

Long-term persistence of the avian leukosis virus (ALV), the transformation-defective mutant of Prague strain Rous sarcoma virus subgroup C ( PR-C) was established in heterologous duck hosts after infection in mid-embryogenesis. Transient viraemia was observed for about 4 weeks after hatching and was lost in most of the infected ducks by about 6 months. Loss of viraemia was accompanied by the increasing synthesis of virus-neutralizing antibodies. In spite of strong virus-neutralizing antibodies, virus was detected by the cocultivation assay in duck tissues throughout the observation period up to 5 years. In the viraemic phase of infection, we found integrated proviruses in various tissues, preferentially in stomach muscle tissue and in the thymus. The long-term persistence of virus was frequently accompanied by liver necrosis and neoplastic diseases. Injection of PR-C virus into early embryos resulted in more pronounced infection accompanied by an increased copy number of viral DNA per cell, high mortality and remarkable atrophy of thymus tissue in infected ducklings.

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© Society for General Microbiology 1990
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1990-09-01
2024-04-19
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References

  1. Akroyd J., Fincham V. J., Green A. R., Levantis P., Searle S., Wyke J. A. 1987; Transcription of Rous sarcoma proviruses in rat cells is determined by chromosomal position effects that fluctuate and can operate over long distances. Oncogene 1:347–354
     [Google Scholar]
  2. Baba T. W., Humphries E. H. 1984; Avian leukosis virus infection: analysis of viremia and DNA integration in susceptible and resistant chicken lines. Journal of Virology 51:123–130
     [Google Scholar]
  3. Baba T. W., Humphries E. H. 1986; Selective integration of avian leukosis virus in different hematopoietic tissues. Virology 155:557–566
     [Google Scholar]
  4. Chambers J. A., Cywinski A., Chen P. -J., Taylor J. M. 1986; Characterization of Rous sarcoma virus-related sequences in the Japanese quail. Journal of Virology 59:354–362
     [Google Scholar]
  5. Cooper G. M., Temin H. M. 1976; Lack of infectivity of the endogenous avian leukosis virus-related genes in the DNA of uninfected chicken cells. Journal of Virology 17:422–430
     [Google Scholar]
  6. Cullen B. R., Greene W. C. 1989; Regulatory pathways governing HIV-1 replication. Cell 58:423–426
     [Google Scholar]
  7. De Boer G. F., Maas H. J. L., Van Vloten J., Groenendal J. E. 1981; Horizontal transmission of lymphoid leukosis virus. Influence of age, maternal antibodies and degree of contact exposure. Avian Pathology 10:343–358
     [Google Scholar]
  8. Duran-Reynals F. 1942; The reciprocal infection of ducks and chickens with tumor-inducing viruses. Cancer Research 2:343–369
     [Google Scholar]
  9. Dyson P. J., Cook P. R., Searle S., Wyke J. A. 1985; The chromatin structure of Rous sarcoma proviruses is changed by factors that act in trans in cell hybrids. EMBO Journal 4:413–420
     [Google Scholar]
  10. Flamant F., Le Guellec D., Verdier G., Nigon V. M. 1987; Tissue specificity of retrovirus expression in inoculated avian embryos revealed by in situ hybridization to whole-body section. Virology 160:301–304
     [Google Scholar]
  11. Frisby D. P., Weiss R. A., Roussel M., Stéhelin D. 1979; The distribution of endogenous chicken retrovirus sequences in the DNA of galliform birds does not coincide with avian phylogenetic relationships. Cell 17:623–634
     [Google Scholar]
  12. Fritsch E. F., Temin H. M. 1977; Inhibition of viral DNA synthesis in stationary chicken embryo fibroblasts infected with avian retroviruses. Journal of Virology 24:461–469
     [Google Scholar]
  13. Gazzolo L., Moscovici M. G., Moscovici C. 1975; Susceptibility and resistance of chicken macrophages to avian RNA tumor viruses. Virology 67:553–565
     [Google Scholar]
  14. Geryk J., Mazo A., Svoboda J., Hložánek I. 1980; Replication of transformation-defective mutants of the Prague strain of Rous sarcoma virus and isolation of td mutant from duck-adapted PR-RSV-C. Folia biologica (Praha) 26:34–41
     [Google Scholar]
  15. Guntaka R. V., Mitsialis S. A. 1980; Cloning of avian tumor virus DNA fragments in plasmid pBR322: evidence for efficient transcription in E. coli from a virus-coded promoter. Gene 12:113–121
     [Google Scholar]
  16. Haase A. T. 1986; Pathogenesis of lentivirus infections. Nature; London: 322130–136
     [Google Scholar]
  17. Halpern M. S., Ewert D. L., Flores L. J., Crittenden L. B. 1983; The influence of the ev 3 locus on the inducibility of serum antibody reactivity for envelope glycoprotein group-specific determinants. Virology 128:502–504
     [Google Scholar]
  18. Hložánek I., Svoboda J. 1972; Characterization of viruses obtained after cell fusion or transfection of chicken cells with DNA from virogenic mammalian Rous sarcoma cells. Journal of General Virology 17:55–59
     [Google Scholar]
  19. Howlett A. R., Cullen B., Hertle M., Bissell M. J. 1987; Tissue tropism and temporal expression of Rous sarcoma virus in embryonic avian limb in ovo . Oncogene Research 1:255–267
     [Google Scholar]
  20. Humphries E. H., Temin H. M. 1974; Requirement for cell division for initiation of transcription of Rous sarcoma virus RNA. Journal of Virology 14:531–546
     [Google Scholar]
  21. Humphries E. H., Glover C., Reichmann M. E. 1981; Rous sarcoma virus infection of synchronized cells establishes provirus integration during S-phase DNA synthesis prior to cellular division. Proceedings of the National Academy of Sciences, U.S.A 78:2601–2605
     [Google Scholar]
  22. Karakoz I., Geryk J., Svoboda J. 1980; In vivoeffect of three transformation-defective mutants of subgroup C avian sarcoma viruses. Folia biologica (Praha) 26:62–69
     [Google Scholar]
  23. Karlson P., Gerok W., Gross W. 1987; Connective tissue. In Pathobiochemistry pp. 342–358 Karlson P., Gerok W., Gross W. Edited by Prague: Academia; In Czech
    [Google Scholar]
  24. Katz R. A., Mitsialis S. A., Guntaka R. V. 1983; Studies on the methylation of avian sarcoma proviruses in permissive and nonpermissive cells. Journal of General Virology 64:429–435
     [Google Scholar]
  25. Levy J. A., Oleszko O., Dimpfl J., Lau D., Rigdon R. H., Jones J., Avery R. 1982; Murine xenotropic type C viruses. IV. Replication and pathogenesis in ducks. Journal of General Virology 61:65–74
     [Google Scholar]
  26. Loan R. W., Whiteaker R. S. 1986; Immune response to avian leukosis virus determined by the cell-mediated focus-reduction (CEMFOR) assay. Journal of the National Cancer Institute 77:757–762
     [Google Scholar]
  27. Meyers P., Ritts G. D., Johnson D. R. 1976; Phytohemagglutinin-induced leukocyte blastogenesis in normal and avian leukosis virus-infected chickens. Cellular Immunology 27:140–146
     [Google Scholar]
  28. Murphy H. M. 1977; A new replication-defective variant of the Bryan high-titre strain Rous sarcoma virus. Virology 77:705–721
     [Google Scholar]
  29. Narayan O., Clements J. E. 1989; Biology and pathogenesis of lentiviruses. Journal of General Virology 70:1617–1639
     [Google Scholar]
  30. Narayan O., Wolinsky J. S., Clements J. E., Strandberg J. D., Griffin D. E., Cork L. C. 1982; Slow virus replication: the role of macrophages in the persistence and expression of visna viruses of sheep and goats. Journal of General Virology 59:345–356
     [Google Scholar]
  31. Peluso R., Haase A., Stowring L., Edwards M., Ventura P. 1985; A Trojan horse mechanism for the spread of visna virus in monocytes. Virology 147:231–236
     [Google Scholar]
  32. Purchase H. G., Burmester B. R. 1978; Leukosis/sarcomagroup. In Diseases of Poultry pp. 418–468 Hofstad M. F., Calnek B. W., Reid W. M., Yoder H. W. Edited by Ames, Iowa: Iowa State University Press;
     [Google Scholar]
  33. Purdy W. J. 1932; The propagation of the Rous sarcoma No. 1 in ducklings. British Journal of Experimental Pathology 13:473–479
     [Google Scholar]
  34. Qualtiere L. F., Meyers P. 1979; A reexamination of humoral tolerance in chickens congenitally infected with an avian leukosis virus. Journal of Immunology 122:825–829
     [Google Scholar]
  35. Rigdon R. H., Leibovitz L. 1970; Spontaneous-occurring tumors in the duck: review of the literature and report of three cases. Avian Diseases 14:431–444
     [Google Scholar]
  36. Rubin H. 1962; Conditions for establishing immunological tolerance to a tumor virus. Nature; London: 195342–345
     [Google Scholar]
  37. Rubin H., Fanshier L., Cornelius A., Hughes W. F. 1962; Tolerance and immunity in chickens after congenital and contact infection with an avian leukosis virus. Virology 17:143–156
     [Google Scholar]
  38. Shimakage M. I., Kamahora T., Hakura A., Toyoshima K. 1979; Selective replication of transformation-defective avian sarcoma virus mutants in duck embryo fibroblasts. Journal of General Virology 45:99–105
     [Google Scholar]
  39. Spencer J. L. 1984; Progress towards eradication of lymphoid leukosis viruses. Avian Pathology 13:599–619
     [Google Scholar]
  40. Svoboda J. 1960; Presence of chicken tumour virus in the sarcoma of the adult rat inoculated after birth with Rous sarcoma tissue. Nature; London: 186980–981
     [Google Scholar]
  41. Svoboda J., Geryk J., Karakoz I. 1980; Long-term persistence of transformation-defective mutants of subgroup C in chickens and ducks inoculated early in life. Archiv für Geschwulstforschung 50:429–434
     [Google Scholar]
  42. Svoboda J., Lhoták V., Geryk J., Saule S., Raes M. B., Stéhelin D. 1983; Characterization of exogenous proviral sequences in hamster tumor cell lines transformed by Rous sarcoma virus rescued from XC cells. Virology 128:195–209
     [Google Scholar]
  43. Varmus H. E., Bishop J. M., Vogt P. K. 1973; Appearance of virus-specific DNA in mammalian cells following transformation by Rous sarcoma virus. Journal of Molecular Biology 74:613–626
     [Google Scholar]
  44. Vilhelmová M., Hála K., Hašek M., Karakoz I., Plachý J. 1972; Inbreeding of Khaki-Campbell ducks. In Proceedings of a conference on genetics and reproduction of farm animals pp. 163–165 Matoušek J., Valenta M. Edited by Praha: Academia; In Czech
    [Google Scholar]
  45. Vogt P. K. 1971; Spontaneous segregation of nontransforming viruses from cloned sarcoma viruses. Virology 46:939–946
     [Google Scholar]
  46. Vogt P. K., Friis R. R. 1971; An avian leukosis virus related to RSV(O): properties and evidence for helper activity. Virology 43:223–234
     [Google Scholar]
  47. Weller S. K., Temin H. M. 1981; Cell killing by avian leukosis viruses. Journal of Virology 39:713–721
     [Google Scholar]
  48. Welt S., Purchase H. G., Thorbecke G. J. 1977; Viral protein synthesis by tissues from avian leukosis virus-infected chickens. I. Susceptible chickens infected after hatching. Journal of Immunology 119:1800–1805
     [Google Scholar]
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Ducks: a new experimental host system for studying persistent infection with avian leukaemia retroviruses
J. Gen. Virol. 71, 1937 (1990); https://doi.org/10.1099/0022-1317-71-9-1937
/content/journal/jgv/10.1099/0022-1317-71-9-1937
/content/journal/jgv/10.1099/0022-1317-71-9-1937
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