1887

Abstract

Endogenous retroviruses (ERVs) are widespread in vertebrate genomes. The recent availability of whole eukaryotic genomes has enabled their characterization in many organisms, including (red jungle fowl), the progenitor of the domesticated chicken. Our bioinformatics analysis of a ERV previously designated GGERV20 identified 35 proviruses with complete long terminal repeats (LTRs) and open reading frames (ORFs) in the Genome Reference Consortium Chicken Build 6a, of which 8 showed potential for translation of functional retroviral polyproteins, including the integrase and reverse transcriptase enzymes. No elements were discovered with an gene. Fifteen loci had LTR sequences with 100 % identity, indicative of recent integration. Chicken embryo fibroblast RNA-seq datasets showed reads representing the entire length of the GGERV20 provirus, supporting their potential for expressing viral proteins. To investigate the possibility that GGERV20 elements may not be fixed in the genome, we assessed the integration status of five loci in a meat-type chicken. PCRs targeting a GGERV20 locus on chromosome one (GGERV20) reproducibly amplified both LTRs and the preintegration state, indicating that the bird from which the DNA was sampled was hemizygous at this locus. The four other loci examined only produced the preintegration state amplicons. These results reveal that GGERV20 is not fixed in the population, and taken together with the lack of mutations seen in several provirus LTRs and their transcriptional activity, suggest that GGERV20 retroviruses have recently been and continue to be active in the chicken genome.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001379
2020-01-09
2024-10-03
Loading full text...

Full text loading...

/deliver/fulltext/jgv/101/3/299.html?itemId=/content/journal/jgv/10.1099/jgv.0.001379&mimeType=html&fmt=ahah

References

  1. Temin HM. Reverse transcription in the eukaryotic genome: retroviruses, pararetroviruses, retrotransposons, and retrotranscripts. Mol Biol Evol 1985; 2:455–468 [View Article]
    [Google Scholar]
  2. Arkhipova IR, Mazo AM, Cherkasova VA, Gorelova TV, Schuppe NG et al. The steps of reverse transcription of Drosophila mobile dispersed genetic elements and U3-R-U5 structure of their LTRs. Cell 1986; 44:555–563 [View Article]
    [Google Scholar]
  3. Weiss RA. The discovery of endogenous retroviruses. Retrovirology 2006; 3:67 [View Article]
    [Google Scholar]
  4. Hayward A, Cornwallis CK, Jern P. Pan-vertebrate comparative genomics unmasks retrovirus macroevolution. Proc Natl Acad Sci U S A 2015; 112:464–469 [View Article]
    [Google Scholar]
  5. Magiorkinis G, Gifford RJ, Katzourakis A, De Ranter J, Belshaw R. Env-less endogenous retroviruses are genomic superspreaders. Proc Natl Acad Sci U S A 2012; 109:7385–7390 [View Article]
    [Google Scholar]
  6. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC et al. Initial sequencing and analysis of the human genome. Nature 2001; 409:860–921 [View Article]
    [Google Scholar]
  7. Johnson WE, Coffin JM. Constructing primate phylogenies from ancient retrovirus sequences. Proc Natl Acad Sci U S A 1999; 96:10254–10260 [View Article]
    [Google Scholar]
  8. Resnick RM, Boyce-Jacino MT, Fu Q, Faras AJ. Phylogenetic distribution of the novel avian endogenous provirus family EAV-0. J Virol 1990; 64:4640–4653
    [Google Scholar]
  9. Sacco MA, Venugopal K. Segregation of EAV-HP ancient endogenous retroviruses within the chicken population. J Virol 2001; 75:11935–11938 [View Article]
    [Google Scholar]
  10. Rivas-Carrillo SD, Pettersson ME, Rubin CJ, Jern P. Whole-genome comparison of endogenous retrovirus segregation across wild and domestic host species populations. Proc Natl Acad Sci U S A 2018; 115:11012–11017 [View Article]
    [Google Scholar]
  11. Crittenden LB, Astrin SM. Independent segregation of eV 2 and eV 10, genetic loci for spontaneous production of endogenous avian retroviruses. Virology 1981; 110:120–127 [View Article]
    [Google Scholar]
  12. Crittenden LB, Astrin SM, Smith EJ. Independent segregation of eV 10 and eV 11, genetic loci for spontaneous production of endogenous avian retroviruses. Virology 1983; 129:514–516 [View Article]
    [Google Scholar]
  13. Wildschutte JH, Williams ZH, Montesion M, Subramanian RP, Kidd JM et al. Discovery of unfixed endogenous retrovirus insertions in diverse human populations. Proc Natl Acad Sci U S A 2016; 113:E2326–E2334 [View Article]
    [Google Scholar]
  14. Astrin SM, Buss EG, Haywards WS. Endogenous viral genes are non-essential in the chicken. Nature 1979; 282:339–341 [View Article]
    [Google Scholar]
  15. Payne LN, Chubb RC. Studies on the nature and genetic control of an antigen in normal chick embryos which reacts in the COFAL test. J Gen Virol 1968; 3:379–391 [View Article]
    [Google Scholar]
  16. Vogt PK, Friis RR. An avian leukosis virus related to RSV(O): properties and evidence for helper activity. Virology 1971; 43:223–234 [View Article]
    [Google Scholar]
  17. Zhang H, Bacon LD, Fadly AM. Development of an endogenous virus-free line of chickens susceptible to all subgroups of avian leukosis virus. Avian Dis 2008; 52:412–418 [View Article]
    [Google Scholar]
  18. Huda A, Polavarapu N, Jordan IK, McDonald JF. Endogenous retroviruses of the chicken genome. Biol Direct 2008; 3:9 [View Article]
    [Google Scholar]
  19. Bolisetty M, Blomberg J, Benachenhou F, Sperber G, Beemon K. Unexpected diversity and expression of avian endogenous retroviruses. MBio 2012; 3:e00344–00312 [View Article]
    [Google Scholar]
  20. Smith LM, Toye AA, Howes K, Bumstead N, Payne LN et al. Novel endogenous retroviral sequences in the chicken genome closely related to HPRS-103 (subgroup J) avian leukosis virus. J Gen Virol 1999; 80:261–268 [View Article]
    [Google Scholar]
  21. Robertson JS, Nicolson C, Riley AM, Bentley M, Dunn G et al. Assessing the significance of reverse transcriptase activity in chick cell-derived vaccines. Biologicals 1997; 25:403–414 [View Article]
    [Google Scholar]
  22. Böni J, Stalder J, Reigel F, Schüpbach J. Detection of reverse transcriptase activity in live attenuated virus vaccines. Clin Diagn Virol 1996; 5:43–53 [View Article]
    [Google Scholar]
  23. Weissmahr RN, Schüpbach J, Böni J. Reverse transcriptase activity in chicken embryo fibroblast culture supernatants is associated with particles containing endogenous avian retrovirus EAV-0 RNA. J Virol 1997; 71:3005–3012
    [Google Scholar]
  24. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990; 215:403–410 [View Article]
    [Google Scholar]
  25. Jurka J. Repbase update: a database and an electronic journal of repetitive elements. Trends Genet 2000; 16:418–420 [View Article]
    [Google Scholar]
  26. Goujon M, McWilliam H, Li W, Valentin F, Squizzato S et al. A new bioinformatics analysis tools framework at EMBL-EBI. Nucleic Acids Res 2010; 38:W695–W699 [View Article]
    [Google Scholar]
  27. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 2011; 7:539 [View Article]
    [Google Scholar]
  28. Gouy M, Guindon S, Gascuel O. SeaView version 4: a multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol Biol Evol 2010; 27:221–224 [View Article]
    [Google Scholar]
  29. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC et al. Primer3-new capabilities and interfaces. Nucleic Acids Res 2012; 40:e115 [View Article]
    [Google Scholar]
  30. Benkel B, Rutherford K. Endogenous avian leukosis viral loci in the red jungle fowl genome assembly. Poult Sci 2014; 93:2988–2990 [View Article]
    [Google Scholar]
  31. Linial ML. Foamy viruses are unconventional retroviruses. J Virol 1999; 73:1747–1755
    [Google Scholar]
  32. Sacco MA, Nair VK. Prototype endogenous avian retroviruses of the genus Gallus. J Gen Virol 2014; 95:2060–2070 [View Article]
    [Google Scholar]
  33. Sacco MA, Howes K, Smith LP, Nair VK. Assessing the roles of endogenous retrovirus EAV-HP in avian leukosis virus subgroup J emergence and tolerance. J Virol 2004; 78:10525–10535 [View Article]
    [Google Scholar]
  34. Payne LN. HPRS‐103: a retro virus strikes back. The emergence of subgroup J avian leukosis virus. Avian Pathology 1998; 27:S36–S45 [View Article]
    [Google Scholar]
  35. Wang Z, Qu L, Yao J, Yang X, Li G et al. An EAV-HP insertion in 5' Flanking region of SLCO1B3 causes blue eggshell in the chicken. PLoS Genet 2013; 9:e1003183 [View Article]
    [Google Scholar]
  36. Belshaw R, Watson J, Katzourakis A, Howe A, Woolven-Allen J et al. Rate of recombinational deletion among human endogenous retroviruses. J Virol 2007; 81:9437–9442 [View Article]
    [Google Scholar]
  37. Gifford RJ, Blomberg J, Coffin JM, Fan H, Heidmann T et al. Nomenclature for endogenous retrovirus (Erv) loci. Retrovirology 2018; 15:59 [View Article]
    [Google Scholar]
  38. Lee J, Mun S, Kim DH, Cho C-S, Oh D-Y et al. Chicken (Gallus gallus) endogenous retrovirus generates genomic variations in the chicken genome. Mob DNA 2017; 8:2 [View Article]
    [Google Scholar]
  39. Naville M, Volff J-N. Endogenous retroviruses in fish genomes: from relics of past infections to evolutionary innovations?. Front Microbiol 2016; 7:1197 [View Article]
    [Google Scholar]
  40. Vargiu L, Rodriguez-Tomé P, Sperber GO, Cadeddu M, Grandi N et al. Classification and characterization of human endogenous retroviruses; mosaic forms are common. Retrovirology 2016; 13:7 [View Article]
    [Google Scholar]
  41. Aiewsakun P, Katzourakis A. Marine origin of retroviruses in the early Palaeozoic era. Nat Commun 2017; 8:13954 [View Article]
    [Google Scholar]
  42. Weiss RA, Boettiger D, Murphy HM. Pseudotypes of avian sarcoma viruses with the envelope properties of vesicular stomatitis virus. Virology 1977; 76:808–825 [View Article]
    [Google Scholar]
  43. Johnson JA, Heneine W. Characterization of endogenous avian leukosis viruses in chicken embryonic fibroblast substrates used in production of measles and mumps vaccines. J Virol 2001; 75:3605–3612 [View Article]
    [Google Scholar]
  44. Hussain AI, Johnson JA, Da Silva Freire M, Heneine W. Identification and characterization of avian retroviruses in chicken embryo-derived yellow fever vaccines: investigation of transmission to vaccine recipients. J Virol 2003; 77:1105–1111 [View Article]
    [Google Scholar]
  45. Hussain AI, Shanmugam V, Switzer WM, Tsang SX, Fadly A et al. Lack of evidence of endogenous avian leukosis virus and endogenous avian retrovirus transmission to measles, mumps, and rubella vaccine recipients. Emerg Infect Dis 2001; 7:66–72 [View Article]
    [Google Scholar]
  46. Shahabuddin M, Sears JF, Khan AS. No evidence of infectious retroviruses in measles virus vaccines produced in chicken embryo cell cultures. J Clin Microbiol 2001; 39:675–684 [View Article]
    [Google Scholar]
  47. Martin J, Herniou E, Cook J, O'Neill RW, Tristem M. Interclass transmission and phyletic host tracking in murine leukemia virus-related retroviruses. J Virol 1999; 73:2442–2449
    [Google Scholar]
/content/journal/jgv/10.1099/jgv.0.001379
Loading
/content/journal/jgv/10.1099/jgv.0.001379
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