1887

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Volume 94, Issue 7

Identification and classification of feline endogenous retroviruses in the cat genome using degenerate PCR and data analysis Free

Abstract

The purpose of this study was to identify and classify endogenous retroviruses (ERVs) in the cat genome. Pooled DNA from five domestic cats was subjected to degenerate PCR with primers specific to the conserved retroviral / region. The 59 amplified retroviral sequences were used for analysis of the cat genome (-6.2). We identified 219 ERV γ and β elements from cat genome contigs, which were classified into 42 ERV γ and 4 β families and further analysed. Among them, 99 γ and 5 β ERV elements contained the complete retroviral structure. Furthermore, we identified 757 spuma-like ERV elements based on the sequence homology to murine (Mu)ERV-L and human (H)ERV-L. To the best of our knowledge, this is the first detailed genome-scale analysis examining endogenous retroviruses (FcERV) and providing advanced insights into their structural characteristics, localization in the genome, and diversity.

  • Received:
  • Accepted:
  • Published Online:
© 2013 SGM
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2013-07-01
2024-04-26
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References

  1. Anai Y., Ochi H., Watanabe S., Nakagawa S., Kawamura M., Gojobori T., Nishigaki K. 2012; Infectious endogenous retroviruses in cats and emergence of recombinant viruses. J Virol 86:8634–8644 [View Article][PubMed]
     [Google Scholar]
  2. Baillie G. J., Wilkins R. J. 2001; Endogenous type D retrovirus in a marsupial, the common brushtail possum (Trichosurus vulpecula). J Virol 75:2499–2507 [View Article][PubMed]
     [Google Scholar]
  3. 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]
  4. Bénit L., Dessen P., Heidmann T. 2001; Identification, phylogeny, and evolution of retroviral elements based on their envelope genes. J Virol 75:11709–11719 [View Article][PubMed]
     [Google Scholar]
  5. Beyer W., Möhring R., Drescher B., Nötzel U., Rosenthal S. 1987; Molecular cloning of an endogenous cat retroviral element (ECE 1)–a recombinant between RD-114 and FeLV-related sequences. Brief report. Arch Virol 96:297–301 [View Article][PubMed]
     [Google Scholar]
  6. Blikstad V., Benachenhou F., Sperber G. O., Blomberg J. 2008; Evolution of human endogenous retroviral sequences: a conceptual account. Cell Mol Life Sci 65:3348–3365 [View Article][PubMed]
     [Google Scholar]
  7. Blomberg J., Benachenhou F., Blikstad V., Sperber G., Mayer J. 2009; Classification and nomenclature of endogenous retroviral sequences (ERVs): problems and recommendations. Gene 448:115–123 [View Article][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. Bonner T. I., Todaro G. J. 1979; Carnivores have sequences in their cellular DNA distantly related to the primate endogenous virus, MAC-1. Virology 94:224–227 [View Article][PubMed]
     [Google Scholar]
  10. Boonyaratanakornkit J., Chew A., Ryu D. D., Greenhalgh D. G., Cho K. 2004; Murine endogenous retroviruses and their transcriptional potentials. Mamm Genome 15:914–923 [View Article][PubMed]
     [Google Scholar]
  11. Chakrabarti R., Hofman F. M., Pandey R., Mathes L. E., Roy-Burman P. 1994; Recombination between feline exogenous and endogenous retroviral sequences generates tropism for cerebral endothelial cells. Am J Pathol 144:348–358[PubMed]
     [Google Scholar]
  12. Chenna R., Sugawara H., Koike T., Lopez R., Gibson T. J., Higgins D. G., Thompson J. D. 2003; Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31:3497–3500 [View Article][PubMed]
     [Google Scholar]
  13. Craven R. C., Leure-duPree A. E., Weldon R. A. Jr, Wills J. W. 1995; Genetic analysis of the major homology region of the Rous sarcoma virus Gag protein. J Virol 69:4213–4227[PubMed]
     [Google Scholar]
  14. Cui J., Holmes E. C. 2012; Endogenous lentiviruses in the ferret genome. J Virol 86:3383–3385 [View Article][PubMed]
     [Google Scholar]
  15. Dangel A. W., Baker B. J., Mendoza A. R., Yu C. Y. 1995; Complement component C4 gene intron 9 as a phylogenetic marker for primates: long terminal repeats of the endogenous retrovirus ERV-K(C4) are a molecular clock of evolution. Immunogenetics 42:41–52 [View Article][PubMed]
     [Google Scholar]
  16. Driscoll C. A., Menotti-Raymond M., Roca A. L., Hupe K., Johnson W. E., Geffen E., Harley E. H., Delibes M., Pontier D. other authors 2007; The Near Eastern origin of cat domestication. Science 317:519–523 [View Article][PubMed]
     [Google Scholar]
  17. 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]
  18. Garcia-Etxebarria K., Jugo B. M. 2010; Genome-wide detection and characterization of endogenous retroviruses in Bos taurus . J Virol 84:10852–10862 [View Article][PubMed]
     [Google Scholar]
  19. Gifford R., Tristem M. 2003; The evolution, distribution and diversity of endogenous retroviruses. Virus Genes 26:291–315 [View Article][PubMed]
     [Google Scholar]
  20. Greenwood A. D., Englbrecht C. C., MacPhee R. D. 2004; Characterization of an endogenous retrovirus class in elephants and their relatives. BMC Evol Biol 4:38 [View Article][PubMed]
     [Google Scholar]
  21. Haapala D. K., Robey W. G., Oroszlan S. D., Tsai W. P. 1985; Isolation from cats of an endogenous type C virus with a novel envelope glycoprotein. J Virol 53:827–833[PubMed]
     [Google Scholar]
  22. Hall T. A. 1999; BioEdit:a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
     [Google Scholar]
  23. Han G.-Z., Worobey M. 2012a; An endogenous foamy virus in the aye-aye (Daubentonia madagascariensis). J Virol 86:7696–7698 [View Article][PubMed]
     [Google Scholar]
  24. Han G.-Z., Worobey M. 2012b; An endogenous foamy-like viral element in the coelacanth genome. PLoS Pathog 8:e1002790 [View Article][PubMed]
     [Google Scholar]
  25. Han G.-Z., Worobey M. 2012c; Endogenous lentiviral elements in the weasel family (Mustelidae). Mol Biol Evol 29:2905–2908 [View Article][PubMed]
     [Google Scholar]
  26. Harada F., Tsukada N., Kato N. 1987; Isolation of three kinds of human endogenous retrovirus-like sequences using tRNAPro as a probe. Nucleic Acids Res 15:9153–9162 [View Article][PubMed]
     [Google Scholar]
  27. 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]
  28. Hughes J. F., Coffin J. M. 2001; Evidence for genomic rearrangements mediated by human endogenous retroviruses during primate evolution. Nat Genet 29:487–489 [View Article][PubMed]
     [Google Scholar]
  29. Jo H., Choi H., Choi M. K., Song N., Kim J. H., Oh J. W., Seo K., Seo H. G., Chun T. other authors 2012; Identification and classification of endogenous retroviruses in the canine genome using degenerative PCR and in-silico data analysis. Virology 422:195–204 [View Article][PubMed]
     [Google Scholar]
  30. Johnson W. E., Coffin J. M. 1999; Constructing primate phylogenies from ancient retrovirus sequences. Proc Natl Acad Sci U S A 96:10254–10260 [View Article][PubMed]
     [Google Scholar]
  31. Katzourakis A., Tristem M., Pybus O. G., Gifford R. J. 2007; Discovery and analysis of the first endogenous lentivirus. Proc Natl Acad Sci U S A 104:6261–6265 [View Article][PubMed]
     [Google Scholar]
  32. Kimura M. 1980; A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120 [View Article][PubMed]
     [Google Scholar]
  33. Klymiuk N., Müller M., Brem G., Aigner B. 2002; Characterization of porcine endogenous retrovirus γ pro-pol nucleotide sequences. J Virol 76:11738–11743 [View Article][PubMed]
     [Google Scholar]
  34. Klymiuk N., Müller M., Brem G., Aigner B. 2003; Characterization of endogenous retroviruses in sheep. J Virol 77:11268–11273 [View Article][PubMed]
     [Google Scholar]
  35. Kröger B., Horak I. 1987; Isolation of novel human retrovirus-related sequences by hybridization to synthetic oligonucleotides complementary to the tRNA(Pro) primer-binding site. J Virol 61:2071–2075[PubMed]
     [Google Scholar]
  36. Lebedev Y. B., Belonovitch O. S., Zybrova N. V., Khil P. P., Kurdyukov S. G., Vinogradova T. V., Hunsmann G., Sverdlov E. D. 2000; Differences in HERV-K LTR insertions in orthologous loci of humans and great apes. Gene 247:265–277 [View Article][PubMed]
     [Google Scholar]
  37. Lindblad-Toh K., Wade C. M., Mikkelsen T. S., Karlsson E. K., Jaffe D. B., Kamal M., Clamp M., Chang J. L., Kulbokas E. J. III other authors 2005; Genome sequence, comparative analysis and haplotype structure of the domestic dog. Nature 438:803–819 [View Article][PubMed]
     [Google Scholar]
  38. Löwer R., Löwer J., Kurth R. 1996; The viruses in all of us: characteristics and biological significance of human endogenous retrovirus sequences. Proc Natl Acad Sci U S A 93:5177–5184 [View Article][PubMed]
     [Google Scholar]
  39. Lueders K. K., Kuff E. L. 1980; Intracisternal A-particle genes: identification in the genome of Mus musculus and comparison of multiple isolates from a mouse gene library. Proc Natl Acad Sci U S A 77:3571–3575 [View Article][PubMed]
     [Google Scholar]
  40. McAllister R. M., Nicolson M., Gardner M. B., Rongey R. W., Rasheed S., Sarma P. S., Huebner R. J., Hatanaka M., Oroszlan S. other authors 1972; C-type virus released from cultured human rhabdomyosarcoma cells. Nat New Biol 235:3–6[PubMed] [CrossRef]
     [Google Scholar]
  41. McDonald J. F. 1993; Evolution and consequences of transposable elements. Curr Opin Genet Dev 3:855–864 [View Article][PubMed]
     [Google Scholar]
  42. Mi S., Lee X. H., Li X. P., 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]
  43. Miller S. A., Dykes D. D., Polesky H. F. 1988; A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16:1215 [View Article][PubMed]
     [Google Scholar]
  44. Mullikin J. C., Hansen N. F., Shen L., Ebling H., Donahue W. F., Tao W., Saranga D. J., Brand A., Rubenfield M. J. other authors 2010; Light whole genome sequence for SNP discovery across domestic cat breeds. BMC Genomics 11:406[PubMed] [CrossRef]
     [Google Scholar]
  45. O’Brien S. J., Johnson W., Driscoll C., Pontius J., Pecon-Slattery J., Menotti-Raymond M. 2008; State of cat genomics. Trends Genet 24:268–279 [View Article][PubMed]
     [Google Scholar]
  46. Ono M., Toh H., Miyata T., Awaya T. 1985; Nucleotide sequence of the Syrian hamster intracisternal A-particle gene: close evolutionary relationship of type A particle gene to types B and D oncovirus genes. J Virol 55:387–394[PubMed]
     [Google Scholar]
  47. Patience C., Switzer W. M., Takeuchi Y., Griffiths D. J., Goward M. E., Heneine W., Stoye J. P., Weiss R. A. 2001; Multiple groups of novel retroviral genomes in pigs and related species. J Virol 75:2771–2775 [View Article][PubMed]
     [Google Scholar]
  48. Pontius J. U., Mullikin J. C., Smith D. R., Lindblad-Toh K., Gnerre S., Clamp M., Chang J., Stephens R., Neelam B. other authors 2007; Initial sequence and comparative analysis of the cat genome. Genome Res 17:1675–1689 [View Article][PubMed]
     [Google Scholar]
  49. Ruebner M., Langbein M., Strissel P. L., Henke C., Schmidt D., Goecke T. W., Faschingbauer F., Schild R. L., Beckmann M. W., Strick R. 2012; Regulation of the human endogenous retroviral Syncytin-1 and cell-cell fusion by the nuclear hormone receptors PPARγ/RXRα in placentogenesis. J Cell Biochem 113:2383–2396 [View Article][PubMed]
     [Google Scholar]
  50. Sheets R. L., Pandey R., Jen W. C., Roy-Burman P. 1993; Recombinant feline leukemia virus genes detected in naturally occurring feline lymphosarcomas. J Virol 67:3118–3125[PubMed]
     [Google Scholar]
  51. Soe L. H., Devi B. G., Mullins J. I., Roy-Burman P. 1983; Molecular cloning and characterization of endogenous feline leukemia virus sequences from a cat genomic library. J Virol 46:829–840[PubMed]
     [Google Scholar]
  52. Stewart M. A., Warnock M., Wheeler A., Wilkie N., Mullins J. I., Onions D. E., Neil J. C. 1986; Nucleotide sequences of a feline leukemia virus subgroup A envelope gene and long terminal repeat and evidence for the recombinational origin of subgroup B viruses. J Virol 58:825–834[PubMed]
     [Google Scholar]
  53. Stewart H., Jarrett O., Hosie M. J., Willett B. J. 2011; Are endogenous feline leukemia viruses really endogenous?. Vet Immunol Immunopathol 143:325–331 [View Article][PubMed]
     [Google Scholar]
  54. Tamura K., Dudley J., Nei M., Kumar S. 2007; MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599 [View Article][PubMed]
     [Google Scholar]
  55. Tönjes R. R., Niebert M. 2003; Relative age of proviral porcine endogenous retrovirus sequences in Sus scrofa based on the molecular clock hypothesis. J Virol 77:12363–12368 [View Article][PubMed]
     [Google Scholar]
  56. Tristem M., Kabat P., Lieberman L., Linde S., Karpas A., Hill F. 1996; Characterization of a novel murine leukemia virus-related subgroup within mammals. J Virol 70:8241–8246[PubMed]
     [Google Scholar]
  57. van der Kuyl A. C., Dekker J. T., Goudsmit J. 1999; Discovery of a new endogenous type C retrovirus (FcEV) in cats: evidence for RD-114 being an FcEV(Gag-Pol)/baboon endogenous virus BaEV(Env) recombinant. J Virol 73:7994–8002[PubMed]
     [Google Scholar]
  58. Weiss R. A. 2006; The discovery of endogenous retroviruses. Retrovirology 3:67 [View Article][PubMed]
     [Google Scholar]
  59. Weiss R. A., Friis R. R., Katz E., Vogt P. K. 1971; Induction of avian tumor viruses in normal cells by physical and chemical carcinogens. Virology 46:920–938 [View Article][PubMed]
     [Google Scholar]
  60. Xiao R., Park K., Oh Y., Kim J.-H., Park C. 2008a; Structural characterization of the genome of BERV γ4, the most abundant endogenous retrovirus family in cattle. Mol Cells 26:404–408[PubMed]
     [Google Scholar]
  61. Xiao R., Park K., Lee H., Kim J., Park C. 2008b; Identification and classification of endogenous retroviruses in cattle. J Virol 82:582–587 [View Article][PubMed]
     [Google Scholar]
  62. Xiong Y., Eickbush T. H. 1990; Origin and evolution of retroelements based upon their reverse transcriptase sequences. EMBO J 9:3353–3362[PubMed]
     [Google Scholar]
  63. Yi J.-M., Kim T.-H., Huh J.-W., Park K. S., Jang S. B., Kim H.-M., Kim H.-S. 2004; Human endogenous retroviral elements belonging to the HERV-S family from human tissues, cancer cells, and primates: expression, structure, phylogeny and evolution. Gene 342:283–292 [View Article][PubMed]
     [Google Scholar]
  64. Yuhki N., Mullikin J. C., Beck T., Stephens R., O’Brien S. J. 2008; Sequences, annotation and single nucleotide polymorphism of the major histocompatibility complex in the domestic cat. PLoS ONE 3:e2674 [View Article][PubMed]
     [Google Scholar]
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Identification and classification of feline endogenous retroviruses in the cat genome using degenerate PCR and in silico data analysis
J. Gen. Virol. 94, 1587 (2013); https://doi.org/10.1099/vir.0.051862-0
/content/journal/jgv/10.1099/vir.0.051862-0
/content/journal/jgv/10.1099/vir.0.051862-0
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