1887

Abstract

Ancient endogenous retroviruses (ERVs), designated endogenous avian retrovirus (EAVs), are present in all spp. including the chicken, and resemble the modern avian sarcoma and leukosis viruses (ASLVs). The EAVs comprise several distinct retroviruses, including EAV-0, EAV-E51 and EAV-HP, as well as a putative member previously named the avian retrotransposon of chickens (ART-CH). Thus far, only the EAV-HP elements have been well characterized. Here, we determined sequences of representative EAV-0 and EAV-E51 proviruses by cloning and data mining of the 2011 assembly of the genome. Although the EAV-0 elements are primarily deleted in the region, we identified two complete EAV-0 genes within the genome and prototype elements sharing identity with an EAV-E51-related clone previously designated EAV-E33. Prototype EAV-0, EAV-E51 and EAV-E33 , and gene sequences used for phylogenetic analysis of deduced proteins showed that the EAVs formed three distinct clades, with EAV-0 sharing the last common ancestor with the ASLVs. The EAV-E51 clade showed the greatest level of divergence compared with other EAVs or ASLVs, suggesting that these ERVs represented exogenous retroviruses that evolved and integrated into the germline over a long period of time. Moreover, the degree of divergence between the chicken and red jungle fowl EAV-E51 sequences suggested that they were more ancient than the other EAVs and may have diverged through mutations that accumulated post-integration. Finally, we showed that the ART-CH elements were chimeric defective ERVs comprising portions of EAV-E51 and EAV-HP rather than authentic retrotransposons.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.066852-0
2014-09-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/95/9/2060.html?itemId=/content/journal/jgv/10.1099/vir.0.066852-0&mimeType=html&fmt=ahah

References

  1. Arad G., Chorev M., Shtorch A., Goldblum A., Kotler M. 1995; Point mutation in avian sarcoma leukaemia virus protease which increases its activity but impairs infectious virus production. J Gen Virol 76:1917–1925 [View Article][PubMed]
    [Google Scholar]
  2. Axelsson E., Smith N. G., Sundström H., Berlin S., Ellegren H. 2004; Male-biased mutation rate and divergence in autosomal, Z-linked and W-linked introns of chicken and Turkey. Mol Biol Evol 21:1538–1547 [View Article][PubMed]
    [Google Scholar]
  3. Bacon L. D., Smith E., Crittenden L. B., Havenstein G. B. 1988; Association of the slow feathering (K) and an endogenous viral (ev21) gene on the Z chromosome of chickens. Poult Sci 67:191–197 [View Article][PubMed]
    [Google Scholar]
  4. Bacon L. D., Fulton J. E., Kulkarni G. B. 2004; Methods for evaluating and developing commercial chicken strains free of endogenous subgroup E avian leukosis virus. Avian Pathol 33:233–243 [View Article][PubMed]
    [Google Scholar]
  5. Bai J., Howes K., Payne L. N., Skinner M. A. 1995; Sequence of host-range determinants in the env gene of a full-length, infectious proviral clone of exogenous avian leukosis virus HPRS-103 confirms that it represents a new subgroup (designated J). J Gen Virol 76:181–187 [View Article][PubMed]
    [Google Scholar]
  6. Barr S. D., Leipzig J., Shinn P., Ecker J. R., Bushman F. D. 2005; Integration targeting by avian sarcoma-leukosis virus and human immunodeficiency virus in the chicken genome. J Virol 79:12035–12044 [View Article][PubMed]
    [Google Scholar]
  7. Bénit L., Lallemand J. B., Casella J. F., Philippe H., Heidmann T. 1999; ERV-L elements: a family of endogenous retrovirus-like elements active throughout the evolution of mammals. J Virol 73:3301–3308[PubMed]
    [Google Scholar]
  8. Bolisetty M., Blomberg J., Benachenhou F., Sperber G., Beemon K. 2012; Unexpected diversity and expression of avian endogenous retroviruses. MBio 3:e00344-12 [View Article][PubMed]
    [Google Scholar]
  9. Böni J., Stalder J., Reigel F., Schüpbach J. 1996; Detection of reverse transcriptase activity in live attenuated virus vaccines. Clin Diagn Virol 5:43–53 [View Article][PubMed]
    [Google Scholar]
  10. Bova C. A., Olsen J. C., Swanstrom R. 1988; The avian retrovirus env gene family: molecular analysis of host range and antigenic variants. J Virol 62:75–83[PubMed]
    [Google Scholar]
  11. Bowles N., Bonnet D., Mulhauser F., Spahr P. F. 1994; Site-directed mutagenesis of the P2 region of the Rous sarcoma virus gag gene: effects on Gag polyprotein processing. Virology 203:20–28 [View Article][PubMed]
    [Google Scholar]
  12. Boyce-Jacino M. T., Resnick R., Faras A. J. 1989; Structural and functional characterization of the unusually short long terminal repeats and their adjacent regions of a novel endogenous avian retrovirus. Virology 173:157–166 [View Article][PubMed]
    [Google Scholar]
  13. Boyce-Jacino M. T., O’Donoghue K., Faras A. J. 1992; Multiple complex families of endogenous retroviruses are highly conserved in the genus Gallus. J Virol 66:4919–4929[PubMed]
    [Google Scholar]
  14. Cantrell M. A., Ederer M. M., Erickson I. K., Swier V. J., Baker R. J., Wichman H. A. 2005; MysTR: an endogenous retrovirus family in mammals that is undergoing recent amplifications to unprecedented copy numbers. J Virol 79:14698–14707 [View Article][PubMed]
    [Google Scholar]
  15. Coffin J. M., Tsichlis P. N., Conklin K. F., Senior A., Robinson H. L. 1983; Genomes of endogenous and exogenous avian retroviruses. Virology 126:51–72 [View Article][PubMed]
    [Google Scholar]
  16. Crittenden L. B. 1991; Retroviral elements in the genome of the chicken: implications for poultry genetics and breeding. Crit Rev Poultry Biol 3:73–91
    [Google Scholar]
  17. Dorner A. J., Stoye J. P., Coffin J. M. 1985; Molecular basis of host range variation in avian retroviruses. J Virol 53:32–39[PubMed]
    [Google Scholar]
  18. Dunwiddie C., Faras A. J. 1985; Presence of retrovirus reverse transcriptase-related gene sequences in avian cells lacking endogenous avian leukosis viruses. Proc Natl Acad Sci U S A 82:5097–5101 [View Article][PubMed]
    [Google Scholar]
  19. Dunwiddie C. T., Resnick R., Boyce-Jacino M., Alegre J. N., Faras A. J. 1986; Molecular cloning and characterization of gag-, pol-, and env-related gene sequences in the ev chicken. J Virol 59:669–675[PubMed]
    [Google Scholar]
  20. Frisby D. P., Weiss R. A., Roussel M., Stehelin 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 [View Article][PubMed]
    [Google Scholar]
  21. Gifford R., Kabat P., Martin J., Lynch C., Tristem M. 2005; Evolution and distribution of class II-related endogenous retroviruses. J Virol 79:6478–6486 [View Article][PubMed]
    [Google Scholar]
  22. Goujon M., McWilliam H., Li W. Z., Valentin F., Squizzato S., Paern J., Lopez R. 2010; A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res 38:Web Server issueW695–W699 [View Article][PubMed]
    [Google Scholar]
  23. Gouy M., Guindon S., Gascuel O. 2010; SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 27:221–224 [View Article][PubMed]
    [Google Scholar]
  24. Groudine M., Eisenman R., Weintraub H. 1981; Chromatin structure of endogenous retroviral genes and activation by an inhibitor of DNA methylation. Nature 292:311–317 [View Article][PubMed]
    [Google Scholar]
  25. Gudkov A. V., Komarova E. A., Nikiforov M. A., Zaitsevskaya T. E. 1992; ART-CH, a new chicken retroviruslike element. J Virol 66:1726–1736[PubMed]
    [Google Scholar]
  26. Herniou E., Martin J., Miller K., Cook J., Wilkinson M., Tristem M. 1998; Retroviral diversity and distribution in vertebrates. J Virol 72:5955–5966[PubMed]
    [Google Scholar]
  27. Hillier L. D. W., Miller W., Birney E., Warren W., Hardison R. C., Ponting C. P., Bork P., Burt D. W., Groenen M. A. M.other authors 2004; Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature 432:695–716 [View Article][PubMed]
    [Google Scholar]
  28. Hughes D. C. 2001; Alternative splicing of the human VEGFGR-3/FLT4 gene as a consequence of an integrated human endogenous retrovirus. J Mol Evol 53:77–79 [View Article][PubMed]
    [Google Scholar]
  29. Hughes S. H., Toyoshima K., Bishop J. M., Varmus H. E. 1981; Organization of the endogenous proviruses of chickens: implications for origin and expression. Virology 108:189–207 [View Article][PubMed]
    [Google Scholar]
  30. Khan A. S., Maudru T., Thompson A., Muller J., Sears J. F., Peden K. W. 1998; The reverse transcriptase activity in cell-free medium of chicken embryo fibroblast cultures is not associated with a replication-competent retrovirus. J Clin Virol 11:7–18 [View Article][PubMed]
    [Google Scholar]
  31. Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H., Valentin F., Wallace I. M., Wilm A.other authors 2007; Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948 [View Article][PubMed]
    [Google Scholar]
  32. Mammano F., Ohagen A., Höglund S., Göttlinger H. G. 1994; Role of the major homology region of human immunodeficiency virus type 1 in virion morphogenesis. J Virol 68:4927–4936[PubMed]
    [Google Scholar]
  33. Martin J., Herniou E., Cook J., O’Neill R. W., Tristem M. 1999; Interclass transmission and phyletic host tracking in murine leukemia virus-related retroviruses. J Virol 73:2442–2449[PubMed]
    [Google Scholar]
  34. Méric C., Spahr P. F. 1986; Rous sarcoma virus nucleic acid-binding protein p12 is necessary for viral 70S RNA dimer formation and packaging. J Virol 60:450–459[PubMed]
    [Google Scholar]
  35. Mi S., Lee X., Li X., Veldman G. M., Finnerty H., Racie L., LaVallie E., Tang X. Y., Edouard P.other authors 2000; Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature 403:785–789 [View Article][PubMed]
    [Google Scholar]
  36. Nelle T. D., Wills J. W. 1996; A large region within the Rous sarcoma virus matrix protein is dispensable for budding and infectivity. J Virol 70:2269–2276[PubMed]
    [Google Scholar]
  37. Pepinsky R. B., Papayannopoulos I. A., Campbell S., Vogt V. M. 1996; Analysis of Rous sarcoma virus Gag protein by mass spectrometry indicates trimming by host exopeptidase. J Virol 70:3313–3318[PubMed]
    [Google Scholar]
  38. Rainey G. J., Natonson A., Maxfield L. F., Coffin J. M. 2003; Mechanisms of avian retroviral host range extension. J Virol 77:6709–6719 [View Article][PubMed]
    [Google Scholar]
  39. Resnick R. M., Boyce-Jacino M. T., Fu Q., Faras A. J. 1990; Phylogenetic distribution of the novel avian endogenous provirus family EAV-0. J Virol 64:4640–4653[PubMed]
    [Google Scholar]
  40. Robertson J. S., Minor P. 1996; Reverse transcriptase activity in vaccines derived from chick cells. Biologicals 24:289–290 [View Article][PubMed]
    [Google Scholar]
  41. Robertson J. S., Nicolson C., Riley A. M., Bentley M., Dunn G., Corcoran T., Schild G. C., Minor P. 1997; Assessing the significance of reverse transcriptase activity in chick cell-derived vaccines. Biologicals 25:403–414 [View Article][PubMed]
    [Google Scholar]
  42. Ruis B. L., Benson S. J., Conklin K. F. 1999; Genome structure and expression of the ev/J family of avian endogenous viruses. J Virol 73:5345–5355[PubMed]
    [Google Scholar]
  43. Ryan F. P. 2004; Human endogenous retroviruses in health and disease: a symbiotic perspective. J R Soc Med 97:560–565 [View Article][PubMed]
    [Google Scholar]
  44. Sacco M. A. 2001; Characterisation of the EAV-HP endogenous retrovirus elements of the Gallus genus. PhD thesis University of London; London, UK:
    [Google Scholar]
  45. 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. J Virol 74:1296–1306 [View Article][PubMed]
    [Google Scholar]
  46. Sacco M. A., Howes K., Venugopal K. 2001; Intact EAV-HP endogenous retrovirus in Sonnerat’s jungle fowl. J Virol 75:2029–2032 [View Article][PubMed]
    [Google Scholar]
  47. Sacco M. A., Howes K., Smith L. P., Nair V. K. 2004; Assessing the roles of endogenous retrovirus EAV-HP in avian leukosis virus subgroup J emergence and tolerance. J Virol 78:10525–10535 [View Article][PubMed]
    [Google Scholar]
  48. Sawai H., Kim H. L., Kuno K., Suzuki S., Gotoh H., Takada M., Takahata N., Satta Y., Akishinonomiya F. 2010; The origin and genetic variation of domestic chickens with special reference to junglefowls Gallus g. gallus and G. varius. PLoS ONE 5:e10639 [View Article][PubMed]
    [Google Scholar]
  49. 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. J Gen Virol 80:261–268[PubMed]
    [Google Scholar]
  50. Sreekumar G. P., Smyth J. R. Jr, Ambady S., Ponce de Leon F. A. 2000; Analysis of the effect of endogenous viral genes in the Smyth line chicken model for autoimmune vitiligo. Am J Pathol 156:1099–1107 [View Article][PubMed]
    [Google Scholar]
  51. Sverdlov E. D. 2000; Retroviruses and primate evolution. Bioessays 22:161–171 [View Article][PubMed]
    [Google Scholar]
  52. Wang Z. P., Qu L. J., Yao J. F., Yang X. L., Li G. Q., Zhang Y. Y., Li J. Y., Wang X. T., Bai J. R.other authors 2013; An EAV-HP insertion in 5′ Flanking region of SLCO1B3 causes blue eggshell in the chicken. PLoS Genet 9:e1003183 [View Article][PubMed]
    [Google Scholar]
  53. Weissmahr R. N., Schüpbach J., Böni J. 1997; Reverse transcriptase activity in chicken embryo fibroblast culture supernatants is associated with particles containing endogenous avian retrovirus EAV-0 RNA. J Virol 71:3005–3012[PubMed]
    [Google Scholar]
  54. Wragg D., Mwacharo J. M., Alcalde J. A., Wang C., Han J. L., Gongora J., Gourichon D., Tixier-Boichard M., Hanotte O. 2013; Endogenous retrovirus EAV-HP linked to blue egg phenotype in Mapuche fowl. PLoS ONE 8:e71393 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.066852-0
Loading
/content/journal/jgv/10.1099/vir.0.066852-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error