1887

Abstract

In the present study, the expression, generation and subcellular localization of Torque teno sus virus (TTSuV) proteins were characterized into two genetically distinct TTSuV species (TTSuV1 and TTSuV2). Following transfection of three TTSuV1 and TTSuV2 full-length ORF (ORF1, ORF2 and ORF3) expression constructs into porcine kidney cells, alternative splice variants encoding new TTSuV protein isoforms were identified for the first time. Proteins encoded from ORF1 and ORF3 were localized in the nucleoli of porcine kidney cells and that of ORF2 in the cytoplasm and nucleus excluding the nucleoli. The subcellular localization of the different protein isoforms was not only similar between distinct TTSuV species but also to the ones described in human Torque teno virus (TTV). Results of the present study were not based on full-length viral clones but suggested that alternative splicing strategy to generate TTSuV protein isoforms probably occurs . Obtained data provide new information on molecular biology of TTSuV and anelloviruses, which until now has been solely based on results obtained from human TTV.

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2011-10-01
2020-01-17
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References

  1. Biagini P.. ( 2009; ). Classification of TTV and related viruses (anelloviruses). . Curr Top Microbiol Immunol 331:, 21–33. [CrossRef] [PubMed]
    [Google Scholar]
  2. Biagini P., Gallian P., Attoui H., Touinssi M., Cantaloube J.-F., de Micco P., de Lamballerie X.. ( 2001; ). Genetic analysis of full-length genomes and subgenomic sequences of TT virus-like mini virus human isolates. . J Gen Virol 82:, 379–383.[PubMed]
    [Google Scholar]
  3. Brunak S., Engelbrecht J., Knudsen S.. ( 1991; ). Prediction of human mRNA donor and acceptor sites from the DNA sequence. . J Mol Biol 220:, 49–65. [CrossRef] [PubMed]
    [Google Scholar]
  4. Ching R. W., Dellaire G., Eskiw C. H., Bazett-Jones D. P.. ( 2005; ). PML bodies: a meeting place for genomic loci?. J Cell Sci 118:, 847–854. [CrossRef] [PubMed]
    [Google Scholar]
  5. Cortey M., Macera L., Segalés J., Kekarainen T.. ( 2011; ). Genetic variability and phylogeny of Torque teno sus virus 1 (TTSuV1) and 2 (TTSuV2) based on complete genomes. . Vet Microbiol 148:, 125–131. [CrossRef] [PubMed]
    [Google Scholar]
  6. Ellis J. A., 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. [CrossRef] [PubMed]
    [Google Scholar]
  7. Erker J. C., Leary T. P., Desai S. M., Chalmers M. L., Mushahwar I. K.. ( 1999; ). Analyses of TT virus full-length genomic sequences. . J Gen Virol 80:, 1743–1750.[PubMed]
    [Google Scholar]
  8. Fu L., Gao Y. S., Tousson A., Shah A., Chen T. L., Vertel B. M., Sztul E.. ( 2005; ). Nuclear aggresomes form by fusion of PML-associated aggregates. . Mol Biol Cell 16:, 4905–4917. [CrossRef] [PubMed]
    [Google Scholar]
  9. Hijikata M., Iwata K., Ohta Y., Nakao K., Matsumoto M., Matsumoto H., Kanai K., Baba K., Samokhvalov E. I., Mishiro S.. ( 1999; ). Genotypes of TT virus (TTV) compared between liver disease patients and healthy individuals using a new PCR system capable of differentiating 1a and 1b types from others. . Arch Virol 144:, 2345–2354. [CrossRef] [PubMed]
    [Google Scholar]
  10. Hiscox J. A.. ( 2002; ). The nucleolus–a gateway to viral infection?. Arch Virol 147:, 1077–1089. [CrossRef] [PubMed]
    [Google Scholar]
  11. Huang Y. W., Ni Y. Y., Dryman B. A., Meng X. J.. ( 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. [CrossRef] [PubMed]
    [Google Scholar]
  12. Kakkola L., Tommiska J., Boele L. C. L., Miettinen S., Blom T., Kekarainen T., Qiu J., Pintel D., Hoeben R. C. et al. & other authors ( 2007; ). Construction and biological activity of a full-length molecular clone of human Torque teno virus (TTV) genotype 6. . FEBS J 274:, 4719–4730. [CrossRef] [PubMed]
    [Google Scholar]
  13. Kamahora T., Hino S., Miyata H.. ( 2000; ). Three spliced mRNAs of TT virus transcribed from a plasmid containing the entire genome in COS1 cells. . J Virol 74:, 9980–9986. [CrossRef] [PubMed]
    [Google Scholar]
  14. Kekarainen T., Sibila M., Segalés 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. [CrossRef] [PubMed]
    [Google Scholar]
  15. Kekarainen T., Martínez-Guinó L., Segalés J.. ( 2009; ). Swine Torque teno virus detection in pig commercial vaccines, enzymes for laboratory use and human drugs containing components of porcine origin. . J Gen Virol 90:, 648–653. [CrossRef] [PubMed]
    [Google Scholar]
  16. Kooistra K., Zhang Y.-H., Henriquez N. V., Weiss B., Mumberg D., Noteborn M. H. M.. ( 2004; ). TT virus-derived apoptosis-inducing protein induces apoptosis preferentially in hepatocellular carcinoma-derived cells. . J Gen Virol 85:, 1445–1450. [CrossRef] [PubMed]
    [Google Scholar]
  17. Kopito R. R.. ( 2000; ). Aggresomes, inclusion bodies and protein aggregation. . Trends Cell Biol 10:, 524–530. [CrossRef] [PubMed]
    [Google Scholar]
  18. Leppik L., Gunst K., Lehtinen M., Dillner J., Streker K., de Villiers E. M.. ( 2007; ). In vivo and in vitro intragenomic rearrangement of TT viruses. . J Virol 81:, 9346–9356. [CrossRef] [PubMed]
    [Google Scholar]
  19. Mankertz A., Hillenbrand B.. ( 2001; ). Replication of porcine circovirus type 1 requires two proteins encoded by the viral rep gene. . Virology 279:, 429–438. [CrossRef] [PubMed]
    [Google Scholar]
  20. Mankertz A., Caliskan R., Hattermann K., Hillenbrand B., Kurzendoerfer P., Mueller B., Schmitt C., Steinfeldt T., Finsterbusch T.. ( 2004; ). Molecular biology of porcine circovirus: analyses of gene expression and viral replication. . Vet Microbiol 98:, 81–88. [CrossRef] [PubMed]
    [Google Scholar]
  21. Martínez L., Kekarainen T., Sibila M., Ruiz-Fons F., Vidal D., Gortázar C., Segalés J.. ( 2006; ). Torque teno virus (TTV) is highly prevalent in the European wild boar (Sus scrofa). . Vet Microbiol 118:, 223–229. [CrossRef] [PubMed]
    [Google Scholar]
  22. Müller B., Maerz A., Doberstein K., Finsterbusch T., Mankertz A.. ( 2008; ). Gene expression of the human Torque teno virus isolate P/1C1. . Virology 381:, 36–45. [CrossRef]
    [Google Scholar]
  23. Mushahwar I. K., Erker J. C., Muerhoff A. S., Leary T. P., Simons J. N., Birkenmeyer L. G., Chalmers M. L., Pilot-Matias T. J., Dexai S. M.. ( 1999; ). Molecular and biophysical characterization of TT virus: evidence for a new virus family infecting humans. . Proc Natl Acad Sci U S A 96:, 3177–3182. [CrossRef] [PubMed]
    [Google Scholar]
  24. Nakai K., Horton P.. ( 1999; ). psort: a program for detecting sorting signals in proteins and predicting their subcellular localization. . Trends Biochem Sci 24:, 34–36. [CrossRef] [PubMed]
    [Google Scholar]
  25. Niel C., Diniz-Mendes L., Devalle S.. ( 2005; ). Rolling-circle amplification of Torque teno virus (TTV) complete genomes from human and swine sera and identification of a novel swine TTV genogroup. . J Gen Virol 86:, 1343–1347. [CrossRef] [PubMed]
    [Google Scholar]
  26. Nishizawa T., Okamoto H., Konishi K., Yoshizawa H., Miyakawa Y., Mayumi M.. ( 1997; ). A novel DNA virus (TTV) associated with elevated transaminase levels in posttransfusion hepatitis of unknown etiology. . Biochem Biophys Res Commun 241:, 92–97. [CrossRef] [PubMed]
    [Google Scholar]
  27. Okamoto H.. ( 2009; ). History of discoveries and pathogenicity of TT viruses. . Curr Top Microbiol Immunol 331:, 1–20. [CrossRef] [PubMed]
    [Google Scholar]
  28. Okamoto H., Akahane Y., Ukita M., Fukuda M., Tsuda F., Miyakawa Y., Mayumi M.. ( 1998; ). Fecal excretion of a nonenveloped DNA virus (TTV) associated with posttransfusion non-A-G hepatitis. . J Med Virol 56:, 128–132. [CrossRef] [PubMed]
    [Google Scholar]
  29. Okamoto H., Nishizawa T., Tawara A., Takahashi M., Kishimoto J., Sai T., Sugai Y.. ( 2000; ). TT virus mRNAs detected in the bone marrow cells from an infected individual. . Biochem Biophys Res Commun 279:, 700–707. [CrossRef] [PubMed]
    [Google Scholar]
  30. 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.[PubMed]
    [Google Scholar]
  31. Qiu J., Kakkola L., Cheng F., Ye C., Söderlund-Venermo M., Hedman K., Pintel D. J.. ( 2005; ). Human circovirus TT virus genotype 6 expresses six proteins following transfection of a full-length clone. . J Virol 79:, 6505–6510. [CrossRef] [PubMed]
    [Google Scholar]
  32. Segalés J., Martínez-Guinó L., Cortey M., Navarro N., Huerta E., Sibila M., Pujols J., Kekarainen T.. ( 2009; ). Retrospective study on swine Torque teno virus genogroups 1 and 2 infection from 1985 to 2005 in Spain. . Vet Microbiol 134:, 199–207. [CrossRef] [PubMed]
    [Google Scholar]
  33. Spector D. L., Lamond A. I.. ( 2011; ). Nuclear speckles. . Cold Spring Harb Perspect Biol 3:, a000646. [CrossRef] [PubMed]
    [Google Scholar]
  34. Taira O., Ogawa H., Nagao A., Tuchiya K., Nunoya T., Ueda S.. ( 2009; ). Prevalence of swine Torque teno virus genogroups 1 and 2 in Japanese swine with suspected post-weaning multisystemic wasting syndrome and porcine respiratory disease complex. . Vet Microbiol 139:, 347–350. [CrossRef] [PubMed]
    [Google Scholar]
  35. Wileman T.. ( 2007; ). Aggresomes and pericentriolar sites of virus assembly: cellular defense or viral design?. Annu Rev Microbiol 61:, 149–167. [CrossRef] [PubMed]
    [Google Scholar]
  36. Zheng H., Ye L., Fang X., Li B., Wang Y., Xiang X., Kong L., Wang W., Zeng Y. et al. & other authors ( 2007; ). Torque teno virus (SANBAN isolate) ORF2 protein suppresses NF-κB pathways via interaction with IκB kinases. . J Virol 81:, 11917–11924. [CrossRef] [PubMed]
    [Google Scholar]
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vol. , part 10, pp. 2446 - 2457

Alignment of full-length amino acid sequence of ORF1 and ORF3 TTSuV species from full-length genomes available on the GenBank database

Schematic presentation of alternative splicing strategy from full-length genomes of TTSuV species

. Oligonucleotides primer used for TTSuV viral proteins constructs in-frame with GFP

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