Skip to main content
SpringerLink
Log in

Distribution of infectious endogenous retroviruses in mixed-breed and purebred cats

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Endogenous retroviruses of domestic cats (ERV-DCs) are members of the genus Gammaretrovirus that infect domestic cats (Felis silvestris catus). Uniquely, domestic cats harbor replication-competent proviruses such as ERV-DC10 (ERV-DC18) and ERV-DC14 (xenotropic and nonecotropic viruses, respectively). The purpose of this study was to assess invasion by two distinct infectious ERV-DCs, ERV-DC10 and ERV-DC14, in domestic cats. Of a total sample of 1646 cats, 568 animals (34.5%) were positive for ERV-DC10 (heterozygous: 377; homozygous: 191), 68 animals (4.1%) were positive for ERV-DC14 (heterozygous: 67; homozygous: 1), and 10 animals (0.6%) were positive for both ERV-DC10 and ERV-DC14. ERV-DC10 and ERV-DC14 were detected in domestic cats in Japan as well as in Tanzania, Sri Lanka, Vietnam, South Korea and Spain. Breeding cats, including Singapura, Norwegian Forest and Ragdoll cats, showed high frequencies of ERV-DC10 (60–100%). By contrast, ERV-DC14 was detected at low frequency in breeding cats. Our results suggest that ERV-DC10 is widely distributed while ERV-DC14 is maintained in a minor population of cats. Thus, ERV-DC10 and ERV-DC14 have invaded cat populations independently.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Boeke JD, Stoye JP (1997) Retrotransponsons, endogenous retroviruses and the evolution of retroelements. In: Coffin JM, Hughes SH, Varmus HE (eds) Retroviruses. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  2. Dimmic MW, Rest JS, Mindell DP, Goldstein RA (2002) rtREV: an amino acid substitution matrix for inference of retrovirus and reverse transcriptase phylogeny. J Mol Evol 55(1):65–73. https://doi.org/10.1007/s00239-001-2304-y

    Article  CAS  PubMed  Google Scholar 

  3. Jarrett WF, Crawford EM, Martin WB, Davie F (1964) A virus-like particle associated with leukemia (lymphosarcoma). Nature 202:567–569. https://doi.org/10.1038/202567a0

    Article  CAS  PubMed  Google Scholar 

  4. Pontius JU, Mullikin JC, Smith DR, Team AS, Lindblad-Toh K, Gnerre S, Clamp M, Chang J, Stephens R, Neelam B, Volfovsky N, Schäffer AA, Agarwala R, Narfström K, Murphy WJ, Giger U, Roca AL, Antunes A, Menotti-Raymond M, Yuhki N, Pecon-Slattery J, Johnson WE, Bourque G, Tesler G, Program NCS, O’Brien SJ (2007) Initial sequence and comparative analysis of the cat genome. Genome Res 17(11):1675–1689. https://doi.org/10.1101/gr.6380007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, Funke R, Gage D, Harris K, Heaford A, Howland J, Kann L, Lehoczky J, LeVine R, McEwan P, McKernan K, Meldrim J, Mesirov JP, Miranda C, Morris W, Naylor J, Raymond C, Rosetti M, Santos R, Sheridan A, Sougnez C, Stange-Thomann Y, Stojanovic N, Subramanian A, Wyman D, Rogers J, Sulston J, Ainscough R, Beck S, Bentley D, Burton J, Clee C, Carter N, Coulson A, Deadman R, Deloukas P, Dunham A, Dunham I, Durbin R, French L, Grafham D, Gregory S, Hubbard T, Humphray S, Hunt A, Jones M, Lloyd C, McMurray A, Matthews L, Mercer S, Milne S, Mullikin JC, Mungall A, Plumb R, Ross M, Shownkeen R, Sims S, Waterston RH, Wilson RK, Hillier LW, McPherson JD, Marra MA, Mardis ER, Fulton LA, Chinwalla AT, Pepin KH, Gish WR, Chissoe SL, Wendl MC, Delehaunty KD, Miner TL, Delehaunty A, Kramer JB, Cook LL, Fulton RS, Johnson DL, Minx PJ, Clifton SW, Hawkins T, Branscomb E, Predki P, Richardson P, Wenning S, Slezak T, Doggett N, Cheng JF, Olsen A, Lucas S, Elkin C, Uberbacher E, Frazier M, Gibbs RA, Muzny DM, Scherer SE, Bouck JB, Sodergren EJ, Worley KC, Rives CM, Gorrell JH, Metzker ML, Naylor SL, Kucherlapati RS, Nelson DL, Weinstock GM, Sakaki Y, Fujiyama A, Hattori M, Yada T, Toyoda A, Itoh T, Kawagoe C, Watanabe H, Totoki Y, Taylor T, Weissenbach J, Heilig R, Saurin W, Artiguenave F, Brottier P, Bruls T, Pelletier E, Robert C, Wincker P, Smith DR, Doucette-Stamm L, Rubenfield M, Weinstock K, Lee HM, Dubois J, Rosenthal A, Platzer M, Nyakatura G, Taudien S, Rump A, Yang H, Yu J, Wang J, Huang G, Gu J, Hood L, Rowen L, Madan A, Qin S, Davis RW, Federspiel NA, Abola AP, Proctor MJ, Myers RM, Schmutz J, Dickson M, Grimwood J, Cox DR, Olson MV, Kaul R, Raymond C, Shimizu N, Kawasaki K, Minoshima S, Evans GA, Athanasiou M, Schultz R, Roe BA, Chen F, Pan H, Ramser J, Lehrach H, Reinhardt R, McCombie WR, de la Bastide M, Dedhia N, Blocker H, Hornischer K, Nordsiek G, Agarwala R, Aravind L, Bailey JA, Bateman A, Batzoglou S, Birney E, Bork P, Brown DG, Burge CB, Cerutti L, Chen HC, Church D, Clamp M, Copley RR, Doerks T, Eddy SR, Eichler EE, Furey TS, Galagan J, Gilbert JG, Harmon C, Hayashizaki Y, Haussler D, Hermjakob H, Hokamp K, Jang W, Johnson LS, Jones TA, Kasif S, Kaspryzk A, Kennedy S, Kent WJ, Kitts P, Koonin EV, Korf I, Kulp D, Lancet D, Lowe TM, McLysaght A, Mikkelsen T, Moran JV, Mulder N, Pollara VJ, Ponting CP, Schuler G, Schultz J, Slater G, Smit AF, Stupka E, Szustakowki J, Thierry-Mieg D, Thierry-Mieg J, Wagner L, Wallis J, Wheeler R, Williams A, Wolf YI, Wolfe KH, Yang SP, Yeh RF, Collins F, Guyer MS, Peterson J, Felsenfeld A, Wetterstrand KA, Patrinos A, Morgan MJ, de Jong P, Catanese JJ, Osoegawa K, Shizuya H, Choi S, Chen YJ, Szustakowki J (2001) Initial sequencing and analysis of the human genome. Nature 409(6822):860–921. https://doi.org/10.1038/35057062

    Article  CAS  PubMed  Google Scholar 

  6. Chinwalla AT, Cook LL, Delehaunty KD, Fewell GA, Fulton LA, Fulton RS, Graves TA, Hillier LW, Mardis ER, McPherson JD, Miner TL, Nash WE, Nelson JO, Nhan MN, Pepin KH, Pohl CS, Ponce TC, Schultz B, Thompson J, Trevaskis E, Waterston RH, Wendl MC, Wilson RK, Yang S-P, An P, Berry E, Birren B, Bloom T, Brown DG, Butler J, Daly M, David R, Deri J, Dodge S, Foley K, Gage D, Gnerre S, Holzer T, Jaffe DB, Kamal M, Karlsson EK, Kells C, Kirby A, Kulbokas EJ, Lander ES, Landers T, Leger JP, Levine R, Lindblad-Toh K, Mauceli E, Mayer JH, McCarthy M, Meldrim J, Meldrim J, Mesirov JP, Nicol R, Nusbaum C, Seaman S, Sharpe T, Sheridan A, Singer JB, Santos R, Spencer B, Stange-Thomann N, Vinson JP, Wade CM, Wierzbowski J, Wyman D, Zody MC, Birney E, Goldman N, Kasprzyk A, Mongin E, Rust AG, Slater G, Stabenau A, Ureta-Vidal A, Whelan S, Ainscough R, Attwood J, Bailey J, Barlow K, Beck S, Burton J, Clamp M, Clee C, Coulson A, Cuff J, Curwen V, Cutts T, Davies J, Eyras E, Grafham D, Gregory S, Hubbard T, Hunt A, Jones M, Joy A, Leonard S, Lloyd C, Matthews L, McLaren S, McLay K, Meredith B, Mullikin JC, Ning Z, Oliver K, Overton-Larty E, Plumb R, Potter S, Quail M, Rogers J, Scott C, Searle S, Shownkeen R, Sims S, Wall M, West AP, Willey D, Williams S, Abril JF, Guigó R, Parra G, Agarwal P, Agarwala R, Church DM, Hlavina W, Maglott DR, Sapojnikov V, Alexandersson M, Pachter L, Antonarakis SE, Dermitzakis ET, Reymond A, Ucla C, Baertsch R, Diekhans M, Furey TS, Hinrichs A, Hsu F, Karolchik D, Kent WJ, Roskin KM, Schwartz MS, Sugnet C, Weber RJ, Bork P, Letunic I, Suyama M, Torrents D, Zdobnov EM, Botcherby M, Brown SD, Campbell RD, Jackson I, Bray N, Couronne O, Dubchak I, Poliakov A, Rubin EM, Brent MR, Flicek P, Keibler E, Korf I, Batalov S, Bult C, Frankel WN, Carninci P, Hayashizaki Y, Kawai J, Okazaki Y, Cawley S, Kulp D, Wheeler R, Chiaromonte F, Collins FS, Felsenfeld A, Guyer M, Peterson J, Wetterstrand K, Copley RR, Mott R, Dewey C, Dickens NJ, Emes RD, Goodstadt L, Ponting CP, Winter E, Dunn DM, von Niederhausern AC, Weiss RB, Eddy SR, Johnson LS, Jones TA, Elnitski L, Kolbe DL, Eswara P, Miller W, O’Connor MJ, Schwartz S, Gibbs RA, Muzny DM, Glusman G, Smit A, Green ED, Hardison RC, Yang S, Haussler D, Hua A, Roe BA, Kucherlapati RS, Montgomery KT, Li J, Li M, Lucas S, Ma B, McCombie WR, Morgan M, Pevzner P, Tesler G, Schultz J, Smith DR, Tromp J, Worley KC, Lander ES, Abril JF, Agarwal P, Alexandersson M, Antonarakis SE, Baertsch R, Berry E, Birney E, Bork P, Bray N, Brent MR, Brown DG, Butler J, Bult C, Chiaromonte F, Chinwalla AT, Church DM, Clamp M, Collins FS, Copley RR, Couronne O, Cawley S, Cuff J, Curwen V, Cutts T, Daly M, Dermitzakis ET, Dewey C, Mouse Genome Sequencing C, Genome Sequencing C, Whitehead Institute MITCfGR, European Bioinformatics I, Wellcome Trust Sanger I, Research Group in Biomedical I, Bioinformatics, National Center for Biotechnology I, Department of M, Division of Medical G, Center for Biomolecular S, Engineering, Embl, Consortium UMMS, Lawrence Berkeley National L, Department of Computer S, School of Computer S, The Jackson L, Laboratory for Genome E, Affymetrix I, Departments of S, Health Evaluation S, National Human Genome Research I, Wellcome Trust Centre for Human G, Department of Electrical E, Department of Human A, Genetics, Department of Human G, Howard Hughes Medical I, Department of G, Departments of B, Molecular B, Computer S, Engineering, Department of Computer S, Engineering, Baylor College of M, The Institute for Systems B, Department of B, Molecular B, Howard Hughes Medical I, Department of C, Biochemistry, Departments of G, Medicine, Harvard-Partners Center for G, Genomics, Department of S, Institute UDJG, Cold Spring Harbor L, Wellcome T, Max Planck Institute for Molecular G, Genome Therapeutics C, Bioinformatics Solutions I, Department of M, Human G, Department of B, Members of the Mouse Genome Analysis G (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420(6915):520–562. https://doi.org/10.1038/nature01262

    Article  CAS  PubMed  Google Scholar 

  7. Weiss RA (2006) The discovery of endogenous retroviruses. Retrovirology 3(1):67. https://doi.org/10.1186/1742-4690-3-67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Kozak CA (2014) Origins of the endogenous and infectious laboratory mouse gammaretroviruses. Viruses 7(1):1–26. https://doi.org/10.3390/v7010001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Tarlinton RE, Meers J, Young PR (2006) Retroviral invasion of the koala genome. Nature 442(7098):79–81. https://doi.org/10.1038/nature04841

    Article  CAS  PubMed  Google Scholar 

  10. Hanger JJ, Bromham LD, McKee JJ, O’Brien TM, Robinson WF (2000) The nucleotide sequence of Koala (Phascolarctos cinereus) retrovirus: a novel type C endogenous virus related to gibbon ape leukemia virus. J Virol 74(9):4264–4272. https://doi.org/10.1128/jvi.74.9.4264-4272.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Wilson CA, Wong S, Muller J, Davidson CE, Rose TM, Burd P (1998) Type C retrovirus released from porcine primary peripheral blood mononuclear cells infects human cells. J Virol 72(4):3082–3087

    Article  CAS  Google Scholar 

  12. Le Tissier P, Stoye JP, Takeuchi Y, Patience C, Weiss RA (1997) Two sets of human-tropic pig retrovirus. Nature 389(6652):681–682. https://doi.org/10.1038/39489

    Article  CAS  PubMed  Google Scholar 

  13. Todaro GJ, Benveniste RE, Lieber MM, Sherr CJ (1974) Characterization of a type C virus released from the porcine cell line PK(15). Virology 58(1):65–74. https://doi.org/10.1016/0042-6822(74)90141-X

    Article  CAS  PubMed  Google Scholar 

  14. Moennig V, Frank H, Hunsmann G, Ohms P, Schwarz H, Schäfer W, Strandström H (1974) C-type particles produced by a permanent cell line from a leukemic pig: II. Physical, chemical, and serological characterization of the particles. Virology 57(1):179–188. https://doi.org/10.1016/0042-6822(74)90119-6

    Article  CAS  PubMed  Google Scholar 

  15. Armstrong JA, Porterfield JS, de Madrid AT (1971) C-type virus particles in pig kidney cell lines. J Gen Virol 10(2):195–198. https://doi.org/10.1099/0022-1317-10-2-195

    Article  CAS  PubMed  Google Scholar 

  16. Kuse K, Ito J, Miyake A, Kawasaki J, Watanabe S, Makundi I, Ngo MH, Otoi T, Nishigaki K (2016) Existence of two distinct infectious endogenous retroviruses in domestic cats and their different strategies for adaptation to transcriptional regulation. J Virol 90(20):9029–9045. https://doi.org/10.1128/jvi.00716-16

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. 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(16):8634–8644. https://doi.org/10.1128/jvi.00280-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Driscoll CA, Menotti-Raymond M, Roca AL, Hupe K, Johnson WE, Geffen E, Harley EH, Delibes M, Pontier D, Kitchener AC, Yamaguchi N, O’Brien SJ, Macdonald DW (2007) The near eastern origin of cat domestication. Science 317(5837):519–523. https://doi.org/10.1126/science.1139518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Driscoll CA, Clutton-Brock J, Kitchener AC, O’Brien SJ (2009) The taming of the cat. Sci Am 300(6):68–75

    Article  Google Scholar 

  20. Vella CM, Shelton LM, McGonagle JJ, Stanglein TW (1999) Robinson’s genetics for cat breeders and veterinarians, 4th edn. Butterworth-Heinemann Ltd, Oxford

    Google Scholar 

  21. Salonen M, Vapalahti K, Tiira K, Mäki-Tanila A, Lohi H (2019) Breed differences of heritable behaviour traits in cats. Sci Rep 9(1):7949. https://doi.org/10.1038/s41598-019-44324-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. David VA, Menotti-Raymond M, Wallace AC, Roelke M, Kehler J, Leighty R, Eizirik E, Hannah SS, Nelson G, Schaffer AA, Connelly CJ, O’Brien SJ, Ryugo DK (2014) Endogenous retrovirus insertion in the KIT oncogene determines white and white spotting in domestic cats. G3 (Bethesda, Md) 4(10):1881–1891. https://doi.org/10.1534/g3.114.013425

    Article  CAS  Google Scholar 

  23. Polani S, Roca AL, Rosensteel BB, Kolokotronis SO, Bar-Gal GK (2010) Evolutionary dynamics of endogenous feline leukemia virus proliferation among species of the domestic cat lineage. Virology 405(2):397–407. https://doi.org/10.1016/j.virol.2010.06.010

    Article  CAS  PubMed  Google Scholar 

  24. Roca AL, Nash WG, Menninger JC, Murphy WJ, O’Brien SJ (2005) Insertional polymorphisms of endogenous feline leukemia viruses. J Virol 79(7):3979–3986. https://doi.org/10.1128/JVI.79.7.3979-3986.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Roca AL, Pecon-Slattery J, O’Brien SJ (2004) Genomically intact endogenous feline leukemia viruses of recent origin. J Virol 78(8):4370–4375. https://doi.org/10.1128/JVI.78.8.4370-4375.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Coffin JM (2004) Evolution of retroviruses: fossils in our DNA. Proc Am Philos Soc 148(3):264–280

    PubMed  Google Scholar 

  27. Niman HL, Akhavi M, Gardner MB, Stephenson JR, Roy-Burman P (1980) Differential expression of two distinct endogenous retrovirus genomes in developing tissues of the domestic cat. J Natl Cancer Inst 64(3):587–594

    CAS  PubMed  Google Scholar 

  28. Koshy R, Gallo RC, Wong-Staal F (1980) Characterization of the endogenous feline leukemia virus-related DNA sequences in cats and attempts to identify exogenous viral sequences in tissues of virus-negative leukemic animals. Virology 103(2):434–445. https://doi.org/10.1016/0042-6822(80)90202-0

    Article  CAS  PubMed  Google Scholar 

  29. Benveniste RE, Sherr CJ, Todaro GJ (1975) Evolution of type C viral genes: origin of feline leukemia virus. Science 190(4217):886–888. https://doi.org/10.1126/science.52892

    Article  CAS  PubMed  Google Scholar 

  30. McDougall AS, Terry A, Tzavaras T, Cheney C, Rojko J, Neil JC (1994) Defective endogenous proviruses are expressed in feline lymphoid cells: evidence for a role in natural resistance to subgroup B feline leukemia viruses. J Virol 68(4):2151–2160

    Article  CAS  Google Scholar 

  31. Stewart MA, Warnock M, Wheeler A, Wilkie N, Mullins JI, Onions DE, Neil JC (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(3):825–834

    Article  CAS  Google Scholar 

  32. Ito J, Watanabe S, Hiratsuka T, Kuse K, Odahara Y, Ochi H, Kawamura M, Nishigaki K (2013) Refrex-1, a soluble restriction factor against feline endogenous and exogenous retroviruses. J Virol 87(22):12029–12040. https://doi.org/10.1128/jvi.01267-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Watanabe S, Kawamura M, Odahara Y, Anai Y, Ochi H, Nakagawa S, Endo Y, Tsujimoto H, Nishigaki K (2013) Phylogenetic and structural diversity in the feline leukemia virus env gene. PLoS One 8(4):e61009. https://doi.org/10.1371/journal.pone.0061009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Ngo MH, Arnal M, Sumi R, Kawasaki J, Miyake A, Grant CK, Otoi T, Fernández de Luco D, Nishigaki K (2019) Tracking the fate of endogenous retrovirus segregation in wild and domestic cats. J Virol 93(24):e01324-01319. https://doi.org/10.1128/JVI.01324-19

    Article  Google Scholar 

  35. Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory, Cold Spring Harbor

    Google Scholar 

  36. Kurushima JD, Lipinski MJ, Gandolfi B, Froenicke L, Grahn JC, Grahn RA, Lyons LA (2013) Variation of cats under domestication: genetic assignment of domestic cats to breeds and worldwide random-bred populations. Anim Genet 44(3):311–324. https://doi.org/10.1111/age.12008

    Article  CAS  PubMed  Google Scholar 

  37. Menotti-Raymond M, David VA, Pflueger SM, Lindblad-Toh K, Wade CM, O’Brien SJ, Johnson WE (2008) Patterns of molecular genetic variation among cat breeds. Genomics 91(1):1–11

    Article  CAS  Google Scholar 

  38. Lipinski MJ, Froenicke L, Baysac KC, Billings NC, Leutenegger CM, Levy AM, Longeri M, Niini T, Ozpinar H, Slater MR, Pedersen NC, Lyons LA (2008) The ascent of cat breeds: genetic evaluations of breeds and worldwide random-bred populations. Genomics 91(1):12–21. https://doi.org/10.1016/j.ygeno.2007.10.009

    Article  CAS  PubMed  Google Scholar 

  39. Palmarini M, Mura M, Spencer TE (2004) Endogenous betaretroviruses of sheep: teaching new lessons in retroviral interference and adaptation. J Gen Virol. https://doi.org/10.1099/vir.0.19547-0

    Article  PubMed  Google Scholar 

  40. Greenwood AD, Ishida Y, O’Brien SP, Roca AL, Eiden MV (2018) Transmission, evolution, and endogenization: lessons learned from recent retroviral invasions. Microbiol Mol Biol Rev 82(1):e00044-00017. https://doi.org/10.1128/mmbr.00044-17

    Article  CAS  Google Scholar 

  41. Malfavon-Borja R, Feschotte C (2015) Fighting fire with fire: endogenous retrovirus envelopes as restriction factors. J Virol 89(8):4047–4050. https://doi.org/10.1128/jvi.03653-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Cornelis G, Heidmann O, Bernard-Stoecklin S, Reynaud K, Véron G, Mulot B, Dupressoir A, Heidmann T (2012) Ancestral capture of syncytin-Car1, a fusogenic endogenous retroviral envelope gene involved in placentation and conserved in Carnivora. Proc Natl Acad Sci 109(7):E432–E441. https://doi.org/10.1073/pnas.1115346109

    Article  PubMed  Google Scholar 

  43. Donahue PR, Hoover EA, Beltz GA, Riedel N, Hirsch VM, Overbaugh J, Mullins JI (1988) Strong sequence conservation among horizontally transmissible, minimally pathogenic feline leukemia viruses. J Virol 62(3):722–731

    Article  CAS  Google Scholar 

  44. Pandey R, Ghosh AK, Kumar DV, Bachman BA, Shibata D, Roy-Burman P (1991) Recombination between feline leukemia virus subgroup B or C and endogenous env elements alters the in vitro biological activities of the viruses. J Virol 65(12):6495–6508

    Article  CAS  Google Scholar 

  45. Overbaugh J, Riedel N, Hoover EA, Mullins JI (1988) Transduction of endogenous envelope genes by feline leukaemia virus in vitro. Nature 332(6166):731–734. https://doi.org/10.1038/332731a0

    Article  CAS  PubMed  Google Scholar 

  46. Young GR, Eksmond U, Salcedo R, Alexopoulou L, Stoye JP, Kassiotis G (2012) Resurrection of endogenous retroviruses in antibody-deficient mice. Nature 491(7426):774–778. https://doi.org/10.1038/nature11599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Stoye JP, Moroni C, Coffin JM (1991) Virological events leading to spontaneous AKR thymomas. J Virol 65(3):1273–1285

    Article  CAS  Google Scholar 

  48. Shimode S, Nakagawa S, Miyazawa T (2015) Multiple invasions of an infectious retrovirus in cat genomes. Sci Rep 5:8164. https://doi.org/10.1038/srep08164. https://www.nature.com/articles/srep08164#supplementary-information

Download references

Acknowledgements

We thank Fermín Urra and Veterinary Clinic “Parque Bruil” for providing European domestic cat samples. We thank Edanz Group (http://www.edanzediting.com/ac) for editing a draft of this manuscript.

Funding

This work was supported by the Japan Society for the Promotion of Science KAKENHI to K.N. (Grant Number 15H04602).

Author information

Authors and Affiliations

  1. Laboratory of Molecular Immunology and Infectious Disease, The United Graduate School of Veterinary Science, Yamaguchi University, 1677-1 Yoshida, Yamaguchi, 753-8515, Japan

    Minh Ha Ngo, Isaac Makundi & Kazuo Nishigaki

  2. Veterinary Diagnostic Laboratory, Marupi Lifetech Co., Ltd., 103 Fushiocho, Ikeda, Osaka, 563-0011, Japan

    Takehisa Soma

  3. Department of Veterinary Internal Medicine, Seoul National University Hospital for Animals, College of Veterinary Medicine, Seoul National University, Seoul, South Korea

    Hwa-Young Youn

  4. Laboratory of Molecular Immunology and Infectious Disease, Joint Faculty of Veterinary Medicine, Yamaguchi University, 1677-1 Yoshida, Yamaguchi, 753-8515, Japan

    Taiji Endo, Junna Kawasaki, Ariko Miyake & Kazuo Nishigaki

  5. Department of Veterinary Pathology, Faculty of Veterinary Medicine, Vietnam National University of Agriculture, Hanoi, 100000, Vietnam

    Bui Thi To Nga

  6. Animal Care Clinic, 20/424 Thuy Khue Street, Tay Ho District, Hanoi, 100000, Vietnam

    Huyen Nguyen

  7. Departamento de Patología Animal, Facultad de Veterinaria, Universidad de Zaragoza, Zaragoza, Spain

    MaríaCruz Arnal & Daniel Fernández de Luco

  8. Department of Animal Science, Faculty of Agriculture, University of Peradeniya, Peradeniya, 20400, Sri Lanka

    R. M. C. Deshapriya

  9. Department of Advanced Pathobiology, Graduate School of Life and Environmental Sciences, Osaka Prefecture University, Izumisano, Osaka, 598-8531, Japan

    Shingo Hatoya

Authors
  1. Minh Ha Ngo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Takehisa Soma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hwa-Young Youn
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Taiji Endo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Isaac Makundi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Junna Kawasaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ariko Miyake
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Bui Thi To Nga
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Huyen Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. MaríaCruz Arnal
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Daniel Fernández de Luco
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. R. M. C. Deshapriya
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Shingo Hatoya
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Kazuo Nishigaki
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kazuo Nishigaki.

Ethics declarations

Animal studies were conducted according to the guidelines for the care and use of laboratory animals of the Ministry of Education, Culture, Sports, Science, and Technology, Japan. All experiments were approved by the Genetic Modification Safety Committee of Yamaguchi University.

Conflict of interest

All authors declare that they have no conflicts of interest.

Additional information

Handling Editor: Li Wu.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ngo, M.H., Soma, T., Youn, HY. et al. Distribution of infectious endogenous retroviruses in mixed-breed and purebred cats. Arch Virol 165, 157–167 (2020). https://doi.org/10.1007/s00705-019-04454-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-019-04454-z

Search

Navigation