1887

Abstract

Among the six envelope subgroups of avian leukosis virus (ALV) that infect chickens, subgroups A (ALV-A) and J (ALV-J) are the most pathogenic and widespread among commercial chicken populations. While ALV-A is predominantly associated with lymphoid leukosis (LL) and less frequently with erythroblastosis (EB), ALV-J mainly induces tumours of the myeloid lineage. In order to examine the basis for the lineage specificity of tumour induction by these two ALV subgroups, we constructed two chimeric viruses by substituting the genes into the reciprocal proviral clones. The chimeric HPRS-103(A) virus carrying the subgroup A gene is identical to ALV-J prototype virus HPRS-103 except for the gene, and the chimeric RCAS(J) virus carrying the subgroup J gene is identical to the parent replication-competent ALV-A vector RCAS except for the gene. In experimentally inoculated chickens, HPRS-103(A) virus induced LL and EB similar to ALV-A isolates such as RAV-1, while RCAS(J) virus induced myeloid leukosis (ML) and EB, similar to ALV-J, suggesting that the gene is the major determinant for the lineage-specific oncogenicity. There were genetic differences in susceptibility to tumour induction between line 0 and line 15 chickens, indicating that in addition to the gene, other viral or host factors could also serve as determinants for oncogenicity. Induction of both LL and ML by the two chimeric viruses occurred through the activation of c-, while the EB tumours were induced by activation of the c-B oncogene.

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2002-10-01
2020-08-11
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References

  1. Adkins H. B., Blacklow S. C., Young J. A.. 2001; Two functionally distinct forms of a retroviral receptor explain the nonreciprocal receptor interference among subgroups B, D, and E avian leukosis viruses. Journal of Virology75:3520–3526
    [Google Scholar]
  2. Arshad S. S., Howes K., Barron G. S., Smith L. M., Russell P. H., Payne L. N.. 1997; Tissue tropism of the HPRS-103 strain of J subgroup avian leukosis virus and of a derivative acutely transforming virus. Veterinary Pathology34:127–137
    [Google Scholar]
  3. Astrin S. M., Buss E. G., Haywards W. S.. 1979; Endogenous viral genes are non-essential in the chicken. Nature282:339–341
    [Google Scholar]
  4. Bacon L. D., Hunt H. D., Cheng H. H.. 2000; A review of the development of chicken lines to resolve genes determining resistance to diseases. Poultry Science79:1082–1093
    [Google Scholar]
  5. Bai J., Payne L. N., Skinner M. A.. 1995; HPRS-103 (exogenous avian leukosis virus, subgroup J) has an env gene related to those of endogenous elements EAV-0 and E51 and an E element found previously only in sarcoma viruses. Journal of Virology69:779–784
    [Google Scholar]
  6. Bates P., Young J. A., Varmus H. E.. 1993; A receptor for subgroup A Rous sarcoma virus is related to the low density lipoprotein receptor. Cell74:1043–1051
    [Google Scholar]
  7. Benson S. J., Ruis B. L., Fadly A. M., Conklin K. F.. 1998; The unique envelope gene of the subgroup J avian leukosis virus derives from ev/J proviruses, a novel family of avian endogenous viruses. Journal of Virology72:10157–10164
    [Google Scholar]
  8. Bieth E., Darlix J. L.. 1992; Complete nucleotide sequence of a highly infectious avian leukosis virus. Nucleic Acids Research20:367
    [Google Scholar]
  9. Bird K. J., Semus H. L., Ruddell A.. 1999; Resistance to avian leukosis virus lymphomagenesis occurs subsequent to proviral c-myc integration. Oncogene18:201–209
    [Google Scholar]
  10. Brown D. W., Robinson H. L.. 1988; Influence of env and long terminal repeat sequences on the tissue tropism of avian leukosis viruses. Journal of Virology62:4828–4831
    [Google Scholar]
  11. Brown D. W., Blais B. P., Robinson H. L.. 1988; Long terminal repeat (LTR) sequences, env, and a region near the 5′ LTR influence the pathogenic potential of recombinants between Rous-associated virus types 0 and 1. Journal of Virology62:3431–3437
    [Google Scholar]
  12. Bruskin A., Jackson J., Bishop J. M., McCarley D. J., Schatzman R. C.. 1990; Six amino acids from the retroviral gene gag greatly enhance the transforming potential of the oncogene v-erb-B. Oncogene5:15–24
    [Google Scholar]
  13. Chesters P. M., Howes K., McKay J. C., Payne L. N., Venugopal K.. 2001; Acutely transforming avian leukosis virus subgroup J strain 966: defective genome encodes a 72-kilodalton Gag–Myc fusion protein. Journal of Virology75:4219–4225
    [Google Scholar]
  14. Crittenden L. B., Salter D. W.. 1992; A transgene, alv6, that expresses the envelope of subgroup A avian leukosis virus reduces the rate of congenital transmission of a field strain of avian leukosis virus. Poultry Science71:799–806
    [Google Scholar]
  15. Curristin S. M., Bird K. J., Tubbs R. J., Ruddell A.. 1997; VBP and RelA regulate avian leukosis virus long terminal repeat-enhanced transcription in B cells. Journal of Virology71:5972–5981
    [Google Scholar]
  16. Fadly A., Witter R. L.. 1998; Oncornaviruses: leukosis/sarcoma and reticuloendotheliosis. In A Laboratory Manual for the Isolation and Identification of Avian Pathogens . pp185–196 Edited by Swayne D. E., Glisson J. R., Jackwood M. W., Pearson J. E., Reed W. M.. Kennet Square, PA: American Association of Avian Pathologists;
  17. Fung Y. K., Lewis W. G., Crittenden L. B., Kung H. J.. 1983; Activation of the cellular oncogene c-erbB by LTR insertion: molecular basis for induction of erythroblastosis by avian leukosis virus. Cell33:357–368
    [Google Scholar]
  18. Fynan E., Block T. M., DuHadaway J., Olson W., Ewert D. L.. 1992; Persistence of Marek’s disease virus in a subpopulation of B cells that is transformed by avian leukosis virus, but not in normal bursal B cells. Journal of Virology66:5860–5866
    [Google Scholar]
  19. Gazzolo L., Moscovici M. G., Moscovici C.. 1975; Susceptibility and resistance of chicken macrophages to avian RNA tumor viruses. Virology67:553–565
    [Google Scholar]
  20. Gong M., Semus H. L., Bird K. J., Stramer B. J., Ruddell A.. 1998; Differential selection of cells with proviral c-myc and c-erbB integrations after avian leukosis virus infection. Journal of Virology72:5517–5525
    [Google Scholar]
  21. Hayward W. S., Neel B. G., Astrin S. M.. 1981; Activation of a cellular onc gene by promoter insertion in ALV-induced lymphoid leukosis. Nature290:475–480
    [Google Scholar]
  22. Hughes S. H., Greenhouse J. J., Petropoulos C. J., Sutrave P.. 1987; Adaptor plasmids simplify the insertion of foreign DNA into helper-independent retroviral vectors. Journal of Virology61:3004–3012
    [Google Scholar]
  23. Klempnauer K. H., Gonda T. J., Bishop J. M.. 1982; Nucleotide sequence of the retroviral leukemia gene v-myb and its cellular progenitor c-myb: the architecture of a transduced oncogene. Cell31:453–463
    [Google Scholar]
  24. Kung H.-J., Liu J.-L.. 1997; Retroviral oncogenesis. In Viral Pathogenesis pp235–266 Edited by Nathanson N.. Philadelphia: Lippincott–Raven;
    [Google Scholar]
  25. Lupiani B., Hunt H., Silva R., Fadly A.. 2000; Identification and characterization of recombinant subgroup J avian leukosis viruses (ALV) expressing subgroup A ALV envelope. Virology276:37–43
    [Google Scholar]
  26. Miles B. D., Robinson H. L.. 1985; High-frequency transduction of c-erbB in avian leukosis virus-induced erythroblastosis. Journal of Virology54:295–303
    [Google Scholar]
  27. Payne L. N.. 1998; HPRS-103: a retrovirus strikes back. The emergence of subgroup J avian leukosis virus. Avian Pathology27:S36–S45
    [Google Scholar]
  28. Payne L. N., Crittenden L. B., Okazaki W.. 1968; Influence of host genotype on responses to four strains of avian leukosis virus. Journal of the National Cancer Institute40:907–916
    [Google Scholar]
  29. Payne L. N., Gillespie A. M., Howes K.. 1991; Induction of myeloid leukosis and other tumours with the HPRS-103 strain of ALV. Veterinary Record129:447–448
    [Google Scholar]
  30. Payne L. N., Gillespie A. M., Howes K.. 1992a; Myeloid leukaemogenicity and transmission of the HPRS-103 strain of avian leukosis virus. Leukemia6:1167–1176
    [Google Scholar]
  31. Payne L. N., Howes K., Gillespie A. M., Smith L. M.. 1992b; Host range of Rous sarcoma virus pseudotype RSV(HPRS-103) in 12 avian species: support for a new avian retrovirus envelope subgroup, designated J. Journal of General Virology 73:2995–2997
    [Google Scholar]
  32. Payne L. N., Gillespie A. M., Howes K.. 1993; Recovery of acutely transforming viruses from myeloid leukosis induced by the HPRS-103 strain of avian leukosis virus. Avian Diseases37:438–450
    [Google Scholar]
  33. Purchase H. G., Okazaki W., Vogt P. K., Hanafusa H., Burmester B. R., Crittenden L. B.. 1977; Oncogenicity of avian leukosis viruses of different subgroups and of mutants of sarcoma viruses. Infection and Immunity15:423–428
    [Google Scholar]
  34. Raines M. A., Maihle N. J., Moscovici C., Crittenden L., Kung H. J.. 1988; Mechanism of c-erbB transduction: newly released transducing viruses retain poly(A) tracts of erbB transcripts and encode C-terminally intact erbB proteins. Journal of Virology62:2437–2443
    [Google Scholar]
  35. Robinson H. L., Gagnon G. C.. 1986; Patterns of proviral insertion and deletion in avian leukosis virus-induced lymphomas. Journal of Virology57:28–36
    [Google Scholar]
  36. Ruddell A., Linial M. L., Groudine M.. 1989; Tissue-specific lability and expression of avian leukosis virus long terminal repeat enhancer-binding proteins. Molecular and Cellular Biology9:5660–5668
    [Google Scholar]
  37. Sacco M. A., Flannery D. M., Howes K., Venugopal K.. 2000; Avian endogenous retrovirus EAV-HP shares regions of identity with avian leukosis virus subgroup J and the avian retrotransposon ART-CH. Journal of Virology74:1296–1306
    [Google Scholar]
  38. Smith E. J., Fadly A., Okazaki W.. 1979; An enzyme-linked immunosorbent assay for detecting avian leukosis–sarcoma viruses. Avian Diseases23:698–707
    [Google Scholar]
  39. Smith L. M., Toye A. A., Howes K., Bumstead N., Payne L. N., Venugopal K.. 1999; Novel endogenous retroviral sequences in the chicken genome closely related to HPRS-103 (subgroup J) avian leukosis virus. Journal of General Virology80:261–268
    [Google Scholar]
  40. Tam W., Hughes S. H., Hayward W. S., Besmer P.. 2002; Avian bic , a gene isolated from a common retroviral site in avian leukosis virus-induced lymphomas that encodes a noncoding RNA, cooperates with c- myc in lymphomagenesis and erythroleukemogenesis. Journal of Virology76:4275–4286
    [Google Scholar]
  41. Venugopal K.. 1999; Avian leukosis virus subgroup J: a rapidly evolving group of oncogenic retroviruses. Research in Veterinary Science67:113–119
    [Google Scholar]
  42. Venugopal K., Howes K., Flannery D. M. J., Payne L. N.. 2000; Isolation of acutely transforming subgroup J avian leukosis viruses that induce erythroblastosis and myelocytomatosis. Avian Pathology29:327–332
    [Google Scholar]
  43. Weiss R. A.. 1992; Cellular receptors and viral glycoproteins involved in retrovirus entry. In The Retroviridae pp1–72 Edited by Levy J. A.. New York: Plenum;
    [Google Scholar]
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