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Cited by 23Chromosomal and Genetic VariationsInfectious Diseases and MycologyEvolution and Genetic Dynamics

Multiple invasions of an infectious retrovirus in cat genomes

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Shimode, Sayumi, Nakagawa, So, Miyazawa, Takayuki·2015·Scientific Reports
DOI 10.1038/srep08164PMC PMC4313119
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Abstract

Endogenous retroviruses (ERVs) are remnants of ancient retroviral infections of host germ-line cells. While most ERVs are defective, some are active and express viral proteins. The RD-114 virus is a replication-competent feline ERV and several feline cell lines produce infectious RD-114 viral particles. All domestic cats are considered to have an ERV locus encoding a replication-competent RD-114 virus in their genomes; however, the locus has not been identified. In this study, we investigated RD-114 virus-related proviral loci in genomes of domestic cats and found that none were capable of producing infectious viruses. We also found that all domestic cats have an RD-114 virus-related sequence on chromosome C2, termed RDRS C2a, but populations of the other RDRSs are different depending on the regions where cats live or breed. Our results indicate that RDRS C2a, the oldest RD-114-related provirus, entered the host genome before an ancestor of domestic cats started diverging and the other new RDRSs might have integrated into migrating cats in Europe. We also show that infectious RD-114 virus can be resurrected by the recombination between two non-infectious RDRSs. From these data, we conclude that cats do not harbor infectious RD-114 viral loci in their genomes and RD-114-related viruses invaded cat genomes multiple times.

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Research works printed but not linked: 55

  1. Gifford R. & Tristem M. The evolution, distribution and diversity of endogenous retroviruses. Virus Genes 26, 291– 315 (2003). 12876457
  2. Reeves R. H. & O'Brien S. J. Molecular genetic characterization of the RD-114 gene family of endogenous feline retroviral sequences. J Virol 52, 164– 171 (1984). 6090693 PMC254502
  3. Okada M., Yoshikawa R., Shojima T., Baba K. & Miyazawa T. Susceptibility and production of a feline endogenous retrovirus (RD-114 virus) in various feline cell lines. Virus Res 155, 268– 273 (2011). 21029758
  4. McAllister R. M. et al. C-type virus released from cultured human rhabdomyosarcoma cells. Nat New Biol 235, 3– 6 (1972). 4111969
  5. Okabe H., Gilden R. V. & Hatanaka M. Extensive homology of RD114 virus DNA with RNA of feline cell origin. Nat New Biol 244, 54– 56 (1973). 4352701
  6. Okabe H., Gilden R. V. & Hatanaka M. RD 114 virus-specific sequences in feline cellular RNA: detection and characterization. J Virol 12, 984– 994 (1973). 4358169 PMC356727
  7. Baluda M. A. & Roy-Burman P. Partial characterization of RD114 virus by DNA-RNA hybridization studies. Nat New Biol 244, 59– 62 (1973). 4352702
  8. Neiman P. E. Measurement of RD114 virus nucleotide sequences in feline cellular DNA. Nat New Biol 244, 62– 64 (1973). 4352703
  9. Gillespie D., Gillespie S., Gallo R. C., East J. L. & Dmochowski L. Genetic origin of RD114 and other RNA tumour viruses assayed by molecular hybridization. Nat New Biol 244, 51– 54 (1973). 4352700
  10. Benveniste R. E. & Todaro G. J. Segregation of RD-114 and FeL-V-related sequences in crosses between domestic cat and leopard cat. Nature 257, 506– 508 (1975). 170535 PMC7086506
  11. Livingston D. M. & Todaro G. J. Endogenous type C virus from a cat cell clone with properties distinct from previously described feline type C virus. Virology 53, 142– 151 (1973). 4122424
  12. Fischinger P. J., Peebles P. T., Nomura S. & Haapala D. K. Isolation of RD-114-like oncornavirus from a cat cell line. J Virol 11, 978– 985 (1973). 4123287 PMC355206
  13. Todaro G. J., Benveniste R. E., Lieber M. M. & Livingston D. M. Infectious type C viruses released by normal cat embryo cells. Virology 55, 506– 515 (1973). 4126409
  14. Spodick D. A., Soe L. H. & Roy-Burman P. Genetic analysis of the feline RD-114 retrovirus-related endogenous elements. Virus Res 1, 543– 555 (1984). 6085439
  15. Reeves R. H., Nash W. G. & O'Brien S. J. Genetic mapping of endogenous RD-114 retroviral sequences of domestic cats. J Virol 56, 303– 306 (1985). 4032538 PMC252532
  16. van der Kuyl A. C., Dekker J. T. & Goudsmit J. Discovery of a new endogenous type C retrovirus (FcEV) in cats: Evidence for RD-114 being an FcEVGag-Pol/baboon endogenous virus BaEVEnv recombinant. J Virol 73, 7994– 8002 (1999). 10482547 PMC112814
  17. Kim F. J., Battini J. L., Manel N. & Sitbon M. Emergence of vertebrate retroviruses and envelope capture. Virology 318, 183– 191 (2004). 14972546
  18. Pearson W. R. Searching protein sequence libraries: comparison of the sensitivity and selectivity of the Smith-Waterman and FASTA algorithms. Genomics 11, 635– 650 (1991). 1774068
  19. Yoshikawa R., Sato E., Igarashi T. & Miyazawa T. Characterization of RD-114 virus isolated from a commercial canine vaccine manufactured using CRFK cells. J Clin Microbiol 48, 3366– 3369 (2010). 20631117 PMC2937671
  20. Shimode S. et al. Sequence comparison of three infectious molecular clones of RD-114 virus. Virus Genes 45, 393– 397 (2012). 22639102
  21. Tamazian G. et al. Annotated features of domestic cat - Felis catus genome. Gigascience 3, 13 (2014). 25143822 PMC4138527
  22. Martins H. & Villesen P. Improved integration time estimation of endogenous retroviruses with phylogenetic data. PLoS One 6, e14745 (2011). 21394200 PMC3048862
  23. Lopez J. V., Culver M., Stephens J. C., Johnson W. E. & O'Brien S. J. Rates of nuclear and cytoplasmic mitochondrial DNA sequence divergence in mammals. Mol Biol Evol 14, 277– 286 (1997). 9066795
  24. Driscoll C. A. et al. The Near Eastern origin of cat domestication. Science 317, 519– 523 (2007). 17600185 PMC5612713
  25. Okada N. SINEs: Short interspersed repeated elements of the eukaryotic genome. Trends Ecol Evol 6, 358– 361 (1991). 21232509
  26. Okada N., Hamada M., Ogiwara I. & Ohshima K. SINEs and LINEs share common 3′ sequences: a review. Gene 205, 229– 243 (1997). 9461397
  27. Anai Y. et al. Infectious endogenous retroviruses in cats and emergence of recombinant viruses. J Virol 86, 8634– 8644 (2012). 22674983 PMC3421742
  28. Johnson W. E. et al. The late Miocene radiation of modern Felidae: a genetic assessment. Science 311, 73– 77 (2006). 16400146
  29. Beaumont M. et al. Genetic diversity and introgression in the Scottish wildcat. Mol Ecol 10, 319– 336 (2001). 11298948
  30. Randi E., Pierpaoloni M., Beaumont M., Ragni B. & Sforzi A. Genetic identification of wild and domestic cats (Felis silvestris) and their hybrids using Bayesian clustering methods. Mol Biol Evol 18, 1679– 1693 (2001). 11504848
  31. Crandell R. A., Fabricant C. G. & Nelson-Ress W. A. Development, characterization, and viral susceptibility of a feline (Felis catus) renal cell line (CRFK). In Vitro 9, 176– 185 (1973). 4130570
  32. Rojko J. L. et al. Feline lymphomas: immunological and cytochemical characterization. Nature 19, 656– 658 (1978). 2535958
  33. Jarrett O., Laid H. M. & Hay D. Determinants of the host range of feline leukemia viruses. J Gen Virol 20, 169– 175 (1973). 4127732
  34. Sakaguchi S., Okada M., Shojima T., Baba K. & Miyazawa T. Establishment of a LacZ marker rescue assay to detect infectious RD114 virus. J Vet Med Sci 70, 785– 790 (2008). 18772552
  35. Li S. & Wilkinson M. F. Site-directed mutagenesis: a two-step method using PCR and DpnI. Biotechniques 23, 588– 590 (1997). 9343667
  36. Craigie R. HIV integrase, a brief overview from chemistry to therapeutics. J Biol Chem 276, 23213– 23216 (2001). 11346660
  37. Palmarini M., Mura M. & Spencer T. E. Endogenous betaretroviruses of sheep: teaching new lessons in retroviral interference and adaptation. J Gen Virol 85, 1– 13 (2004). 14718613
  38. Driscoll C. A., Clutton-Brock J., Kitchener A. C. & O'Brien S. J. The Taming of the cat. Genetic and archaeological findings hint that wildcats became housecats earlier--and in a different place--than previously thought. Sci Am 300, 68– 75 (2009). 19485091 PMC5790555
  39. Menotti-Raymond M. et al. Patterns of molecular genetic variation among cat breeds. Genomics 91, 1– 11 (2008). 17964115
  40. Henzy J. E., Gifford R. J., Johnson W. E. & Coffin J. M. A novel recombinant retrovirus in the genomes of modern birds combines features of avian and mammalian retroviruses. J Virol 88, 2398– 2405 (2014). 24352464 PMC3958055
  41. Delviks-Frankenberry K. et al. Generation of multiple replication-competent retroviruses through recombination between PreXMRV-1 and PreXMRV-2. J Virol 87, 11525– 11537 (2013). 23966380 PMC3807343
  42. Denner J., Specke V., Thiesen U., Karlas A. & Kurth R. Genetic alterations of the long terminal repeat of an ecotropic porcine endogenous retrovirus during passage in human cells. Virology 314, 125– 133 (2003). 14517066
  43. Denner J. Recombinant porcine endogenous retroviruses (PERV-A/C): a new risk for xenotransplantation? Arch Virol 153, 1421– 1426 (2008). 18584115
  44. Delviks-Frankenberry K. A., Nikolenko G. N. & Pathak V. K. The "Connection" Between HIV Drug Resistance and RNase H. Viruses 2, 1476– 1503 (2010). 21088701 PMC2982141
  45. Takeuchi Y. et al. Host range and interference studies of three classes of pig endogenous retrovirus. J Virol 72, 9986– 9991 (1998). 9811736 PMC110514
  46. Arias M. & Fan H. The saga of XMRV: a virus that infects human cells but is not a human virus. Emerg Microbes Infect 3, e25 (2014). PMC4008767 26038516
  47. Shimode S., Nakaoka R., Shogen H. & Miyazawa T. Characterization of feline ASCT1 and ASCT2 as RD-114 virus receptor. J Gen Virol 94, 1608– 1612 (2013). 23580426
  48. Odaka T. Genetic transmission of endogenous N- and B-tropic murine leukemia viruses in low-leukemic strain C57BL/6. J Virol 15, 332– 337 (1975). 163359 PMC354457
  49. Kozak C. A. & Rowe W. P. Genetic mapping of ecotropic murine leukemia virus-inducing loci in six inbred strains. J Exp Med 155, 524– 534 (1982). 6276492 PMC2186586
  50. McCubrey J. & Risser R. Genetic interactions in the spontaneous production of endogenous murine leukemia virus in low leukemic mouse strains. J Exp Med 156, 337– 349 (1982). 6284854 PMC2186749
  51. King S. R., Berson B. J. & Risser R. Mechanism of interaction between endogenous ecotropic murine leukemia viruses in (BALB/c X C57BL/6) hybrid cells. Virology 162, 1– 11 (1988). 2447699
  52. Nakamura K. et al. Comparison of prevalence of feline herpesvirus type 1, calicivirus and parvovirus infections in domestic and leopard cats in Vietnam. J Vet Med Sci 61, 1313– 1315 (1999). 10651052
  53. Sassa Y. et al. Successive deaths of a captive snow leopard (Uncia uncia) and a serval (Leptailurus serval) by infection with feline panleukopenia virus at Sapporo Maruyama Zoo. J Vet Med Sci 73, 491– 494 (2011). 21116104
  54. Katoh K. & Standley D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30, 772– 780. (2013). 23329690 PMC3603318
  55. Stamatakis A. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 2688– 2690 (2006). 16928733

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Authors
Shimode, S., Nakagawa, S., & Miyazawa, T.
Affiliations
  • Kyoto University (JP)
  • Tokai University (JP)
Corresponding author
Miyazawa, Takayuki
ORCID
Venue
Scientific Reports
Publisher
Springer Science and Business Media LLC
Published
2015-02-02
Volume
5
Issue
1
Pages
8164-8164
ISSN
2045-2322 (ISSN-L)
DOI
10.1038/srep08164
PMC
PMC4313119
OpenAlex
W2019178666
Cited by
23
References
3
Citations by year
2026: 1 · 2025: 1 · 2024: 3 · 2023: 1 · 2022: 2 · 2021: 3 · 2020: 2 · 2019: 2 · 2018: 1 · 2017: 2 · 2016: 3 · 2015: 2
FWCI
3.22
Type
journal article
Language
en
Open access
Licence
Locations
  • Scientific Reports (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Kyoto University Research Information Repository (Kyoto University) (submittedVersion)
Funders
  • University College London
  • Japan Society for the Promotion of Science (25891023, 14J05589)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Chromosomal and Genetic Variations
  • Health Sciences › Veterinary › Small Animals › Infectious Diseases and Mycology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
Keywords
endogenous retroviruses, feline retroviruses, cats, viral recombination, multiple invasions, retroviral evolution
MeSH terms
Animals, Base Sequence, Cats, Cell Line, Chromosomes, Humans, Molecular Sequence Data, Proviruses, RNA, Viral, Blotting, Southern, Genome, Endogenous Retroviruses, Genetic Loci, HEK293 Cells

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