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Full genome sequences of torque teno sus virus strains that coinfected a pig with postweaning multisystemic wasting syndrome in Japan: implications for genetic diversity

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Abstract

We determined the complete genome sequences of torque teno sus viruses (TTSuVs) detected in pigs with postweaning multisystemic wasting syndrome (PMWS) and in healthy pigs in Japan. Unexpectedly, we found coinfection of a PMWS-affected pig in Japan with one strain of TTSuV1, five strains of TTSuV2, and one strain of PCV2. Full-genome sequencing of each of these strains, followed by phylogenetic analysis, revealed broad genetic diversity in the TTSuV2 strains infecting the PMWS-affected pig. These results suggest that the geographical bias in the available genetic information about TTSuVs has a limited impact on the evaluation of their genetic diversity.

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References

  1. Allan G, Krakowka S, Ellis J, Charreyre C (2012) Discovery and evolving history of two genetically related but phenotypically different viruses, porcine circoviruses 1 and 2. Virus Res 164:4–9

    Article  CAS  PubMed  Google Scholar 

  2. Blomstrom AL, Belak S, Fossum C, Fuxler L, Wallgren P, Berg M (2010) Studies of porcine circovirus type 2, porcine boca-like virus and torque teno virus indicate the presence of multiple viral infections in postweaning multisystemic wasting syndrome pigs. Virus Res 152:59–64

    Article  PubMed  Google Scholar 

  3. Bolin SR, Stoffregen WC, Nayar GP, Hamel AL (2001) Postweaning multisystemic wasting syndrome induced after experimental inoculation of cesarean-derived, colostrum-deprived piglets with type 2 porcine circovirus. J Vet Diagn Invest 13:185–194

    Article  CAS  PubMed  Google Scholar 

  4. Cornelissen-Keijsers V, Jimenez-Melsio A, Sonnemans D, Cortey M, Segales J, van den Born E, Kekarainen T (2012) Discovery of a novel Torque teno sus virus species: genetic characterization, epidemiological assessment and disease association. J Gen Virol 93:2682–2691

    Article  CAS  PubMed  Google Scholar 

  5. de Arruda Leme R, Ribeiro J, Alfieri AF, Alfieri AA (2013) Simultaneous infection with distinct strains of torque teno sus virus (TTSuV) in healthy slaughter-age pigs. Vet Res Commun 37:183–186

    Article  Google Scholar 

  6. de Castro AM, Favero CM, Baldin CM, Borba M, de Castro FG Jr, Miyashiro S, de Moura JC, Dias RA, Brandao PE, Richtzenhain LJ (2012) Preliminary study of Porcine circovirus type 2 and Torque teno sus virus coinfection frequencies in Brazilian pig herds. Can J Vet Res 76:174–179

    PubMed Central  PubMed  Google Scholar 

  7. Ellis J, Krakowka S, Lairmore M, Haines D, Bratanich A, Clark E, Allan G, Konoby C, Hassard L, Meehan B, Martin K, Harding J, Kennedy S, McNeilly F (1999) Reproduction of lesions of postweaning multisystemic wasting syndrome in gnotobiotic piglets. J Vet Diagn Invest 11:3–14

    Article  CAS  PubMed  Google Scholar 

  8. Ellis JA, Allan G, Krakowka S (2008) Effect of coinfection with genogroup 1 porcine torque teno virus on porcine circovirus type 2-associated postweaning multisystemic wasting syndrome in gnotobiotic pigs. Am J Vet Res 69:1608–1614

    Article  PubMed  Google Scholar 

  9. Gallei A, Pesch S, Esking WS, Keller C, Ohlinger VF (2010) Porcine Torque teno virus: determination of viral genomic loads by genogroup-specific multiplex rt-PCR, detection of frequent multiple infections with genogroups 1 or 2, and establishment of viral full-length sequences. Vet Microbiol 143:202–212

    Article  CAS  PubMed  Google Scholar 

  10. Huang YW, Ni YY, Dryman BA, Meng XJ (2010) Multiple infection of porcine Torque teno virus in a single pig and characterization of the full-length genomic sequences of four U.S. prototype PTTV strains: implication for genotyping of PTTV. Virology 396:289–297

    Article  CAS  PubMed  Google Scholar 

  11. Kekarainen T, Sibila M, Segales J (2006) Prevalence of swine Torque teno virus in post-weaning multisystemic wasting syndrome (PMWS)-affected and non-PMWS-affected pigs in Spain. J Gen Virol 87:833–837

    Article  CAS  PubMed  Google Scholar 

  12. Ladekjaer-Mikkelsen AS, Nielsen J, Storgaard T, Botner A, Allan G, McNeilly F (2001) Transplacental infection with PCV-2 associated with reproductive failure in a gilt. Vet Rec 148:759–760

    CAS  PubMed  Google Scholar 

  13. Li K, Wang LQ, Wu YY, Chao AJ, Lu QW, Wei ZY, Cui BA, Chen HY (2013) Molecular detection and genomic characterization of Torque teno sus virus 1 and 2 from domestic pigs in central China. Virus Genes 46:479–486

    Article  CAS  PubMed  Google Scholar 

  14. Liu J, Guo L, Zhang L, Wei Y, Huang L, Wu H, Liu C (2013) Three new emerging subgroups of Torque teno sus viruses (TTSuVs) and co-infection of TTSuVs with porcine circovirus type 2 in China. Virol J 10:189

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Maggi F, Bendinelli M (2009) Immunobiology of the Torque teno viruses and other anelloviruses. Curr Top Microbiol Immunol 331:65–90

    CAS  PubMed  Google Scholar 

  16. McKeown NE, Fenaux M, Halbur PG, Meng XJ (2004) Molecular characterization of porcine TT virus, an orphan virus, in pigs from six different countries. Vet Microbiol 104:113–117

    Article  CAS  PubMed  Google Scholar 

  17. Meng XJ (2012) Spread like a wildfire–the omnipresence of porcine circovirus type 2 (PCV2) and its ever-expanding association with diseases in pigs. Virus Res 164:1–3

    Article  CAS  PubMed  Google Scholar 

  18. O’Connor B, Gauvreau H, West K, Bogdan J, Ayroud M, Clark EG, Konoby C, Allan G, Ellis JA (2001) Multiple porcine circovirus 2-associated abortions and reproductive failure in a multisite swine production unit. Can Vet J 42:551–553

    PubMed Central  PubMed  Google Scholar 

  19. Okamoto H, Takahashi M, Nishizawa T, Tawara A, Fukai K, Muramatsu U, Naito Y, Yoshikawa A (2002) Genomic characterization of TT viruses (TTVs) in pigs, cats and dogs and their relatedness with species-specific TTVs in primates and tupaias. J Gen Virol 83:1291–1297

    Article  CAS  PubMed  Google Scholar 

  20. Opriessnig T, Meng XJ, Halbur PG (2007) Porcine circovirus type 2 associated disease: update on current terminology, clinical manifestations, pathogenesis, diagnosis, and intervention strategies. J Vet Diagn Invest 19:591–615

    Article  PubMed  Google Scholar 

  21. Pallares FJ, Halbur PG, Opriessnig T, Sorden SD, Villar D, Janke BH, Yaeger MJ, Larson DJ, Schwartz KJ, Yoon KJ, Hoffman LJ (2002) Porcine circovirus type 2 (PCV-2) coinfections in US field cases of postweaning multisystemic wasting syndrome (PMWS). J Vet Diagn Invest 14:515–519

    Article  CAS  PubMed  Google Scholar 

  22. Perez LJ, Perera CL, Frias MT, Nunez JI, Ganges L, de Arce HD (2012) A multiple SYBR Green I-based real-time PCR system for the simultaneous detection of porcine circovirus type 2, porcine parvovirus, pseudorabies virus and Torque teno sus virus 1 and 2 in pigs. J Virol Methods 179:233–241

    Article  CAS  PubMed  Google Scholar 

  23. Ramirez A, Wang C, Prickett JR, Pogranichniy R, Yoon KJ, Main R, Johnson JK, Rademacher C, Hoogland M, Hoffmann P, Kurtz A, Kurtz E, Zimmerman J (2012) Efficient surveillance of pig populations using oral fluids. Prev Vet Med 104:292–300

    Article  PubMed  Google Scholar 

  24. Savic B, Milicevic V, Bojkovski J, Kureljusic B, Ivetic V, Pavlovic I (2010) Detection rates of the swine torque teno viruses (TTVs), porcine circovirus type 2 (PCV2) and hepatitis E virus (HEV) in the livers of pigs with hepatitis. Vet Res Commun 34:641–648

    Article  PubMed  Google Scholar 

  25. Segales J, Allan GM, Domingo M (2005) Porcine circovirus diseases. Anim Health Res Rev 6:119–142

    Article  PubMed  Google Scholar 

  26. Zhai SL, Long JX, Wei WK, Chen QL, Luo ML, Lv DH, Wu DC, Gao F, Yuan SS, Tong GZ, Wei ZZ (2013) High prevalence of torque teno sus virus in China and genetic diversity of the 5′ non-coding region. Arch Virol 158:1567–1573

    Article  CAS  PubMed  Google Scholar 

  27. Zheng H, Ye L, Fang X, Li B, Wang Y, Xiang X, Kong L, Wang W, Zeng Y, Ye L, Wu Z, She Y, Zhou X (2007) Torque teno virus (SANBAN isolate) ORF2 protein suppresses NF-kappaB pathways via interaction with IkappaB kinases. J Virol 81:11917–11924

    Article  PubMed Central  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by a Grant-in-Aid for Challenging Exploratory Research from the Japan Society for the Promotion of Science (JSPS) (JSPS KAKENHI Grant Number 26670227) and by the Grant for Joint Research Project of the Institute of Medical Science, the University of Tokyo.

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Authors and Affiliations

  1. Laboratory of Animal Hygiene, Joint Faculty of Veterinary Medicine, Kagoshima University, 1-21-24 Korimoto, Kagoshima, 890-0065, Japan

    Makoto Ozawa, Kosuke Okuya, Takehiro Kanda, Norihiro Kanazawa, Kyoko Tsukiyama-Kohara & Eisaburo Deguchi

  2. Transboundary Animal Diseases Control and Research Center, Joint Faculty of Veterinary Medicine, Kagoshima University, Kagoshima, Japan

    Makoto Ozawa, Toshiko Kawabata, Kiori Nagano & Kyoko Tsukiyama-Kohara

  3. United Graduate School of Veterinary Science, Yamaguchi University, Yamaguchi, Japan

    Makoto Ozawa, Kyoko Tsukiyama-Kohara & Eisaburo Deguchi

  4. Vaxxinova Japan K.K., Tokyo, Japan

    Akira Taneno

  5. Laboratory of Farm Animal Production Medicine, Joint Faculty of Veterinary Medicine, Kagoshima University, Kagoshima, Japan

    Eisaburo Deguchi

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  1. Makoto Ozawa
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  2. Toshiko Kawabata
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  9. Eisaburo Deguchi
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Correspondence to Makoto Ozawa.

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Ozawa, M., Kawabata, T., Okuya, K. et al. Full genome sequences of torque teno sus virus strains that coinfected a pig with postweaning multisystemic wasting syndrome in Japan: implications for genetic diversity. Arch Virol 160, 3067–3074 (2015). https://doi.org/10.1007/s00705-015-2593-x

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  • DOI: https://doi.org/10.1007/s00705-015-2593-x

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