1887

Abstract

A novel papillomavirus (PV) was isolated from a genital condyloma of a free-ranging bottlenose dolphin inhabiting the coastal waters of Charleston Harbor, SC, USA: papillomavirus type 2 (TtPV2). This novel virus represents the first isolated North American cetacean PV and the first American bottlenose dolphin PV. After the viral genome was cloned, sequenced and characterized genetically, phylogenetic analyses revealed that TtPV2 is most similar to the only published cetacean PV isolated and characterized thus far, PV type 1 (PsPV1). A striking feature of the genome of TtPV2, as well as that of PsPV1, is the lack of an E7 open reading frame, which typically encodes one of the oncogenic proteins believed to be responsible for malignant transformation in the high-risk mucosotropic human papillomaviruses (HPVs). TtPV2 E6 contains a PDZ-binding motif that has been shown to be involved in transformation in the case of high-risk genital HPVs.

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2006-12-01
2019-11-14
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References

  1. Androphy, E. J., Lowy, D. R. & Schiller, J. T. ( 1987; ). Bovine papillomavirus E2 trans-activating gene product binds to specific sites in papillomavirus DNA. Nature 325, 70–73.[CrossRef]
    [Google Scholar]
  2. Anttila, T., Saikku, P., Koskela, P. & 12 other authors ( 2001; ). Serotypes of Chlamydia trachomatis and risk for development of cervical squamous cell carcinoma. JAMA 285, 47–51.[CrossRef]
    [Google Scholar]
  3. Apt, D., Chong, T., Liu, Y. & Bernard, H.-U. ( 1993; ). Nuclear factor I and epithelial cell-specific transcription of human papillomavirus type 16. J Virol 67, 4455–4463.
    [Google Scholar]
  4. Bednarek, P. H., Lee, B. J., Gandhi, S., Lee, E. & Phillips, B. ( 1998; ). Novel binding sites for regulatory factors in the human papillomavirus type 18 enhancer and promoter identified by in vivo footprinting. J Virol 72, 708–716.
    [Google Scholar]
  5. Bossart, G. D., Cray, C., Solorzano, J. L., Decker, S. J., Cornell, L. H. & Altman, N. H. ( 1996; ). Cutaneous papillomaviral-like papillomatosis in a killer whale (Orcinus orca). Mar Mamm Sci 12, 274–281.[CrossRef]
    [Google Scholar]
  6. Bossart, G. D., Ewing, R. Y., Lowe, M., Sweat, M., Decker, S. J., Walsh, C. J., Ghim, S.-j. & Jenson, A. B. ( 2002; ). Viral papillomatosis in Florida manatees (Trichechus manatus latirostris). Exp Mol Pathol 72, 37–48.[CrossRef]
    [Google Scholar]
  7. Bossart, G. D., Ghim, S.-j., Rehtanz, M. & 18 other authors ( 2005; ). Orogenital neoplasia in Atlantic bottlenose dolphins (Tursiops truncatus). Aquat Mamm 31, 473–480.[CrossRef]
    [Google Scholar]
  8. Butz, K. & Hoppe-Seyler, F. ( 1993; ). Transcriptional control of human papillomavirus (HPV) oncogene expression: composition of the HPV type 18 upstream regulatory region. J Virol 67, 6476–6486.
    [Google Scholar]
  9. Castellsagué, X., Bosch, F. X. & Muñoz, N. ( 2002; ). Environmental co-factors in HPV carcinogenesis. Virus Res 89, 191–199.[CrossRef]
    [Google Scholar]
  10. Chan, S.-Y., Delius, H., Halpern, A. L. & Bernard, H.-U. ( 1995; ). Analysis of genomic sequences of 95 papillomavirus types: uniting typing, phylogeny, and taxonomy. J Virol 69, 3074–3083.
    [Google Scholar]
  11. Chong, T., Apt, D., Gloss, B., Isa, M. & Bernard, H.-U. ( 1991; ). The enhancer of human papillomavirus type 16: binding sites for the ubiquitous transcription factors oct-1, NFA, TEF-2, NF1, and AP-1 participate in epithelial cell-specific transcription. J Virol 65, 5933–5943.
    [Google Scholar]
  12. Chow, L. T. & Broker, T. R. ( 1994; ). Papillomavirus DNA replication. Intervirology 37, 150–158.
    [Google Scholar]
  13. DeFilippis, R. A., Goodwin, E. C., Wu, L. & DiMaio, D. ( 2003; ). Endogenous human papillomavirus E6 and E7 proteins differentially regulate proliferation, senescence, and apoptosis in HeLa cervical carcinoma cells. J Virol 77, 1551–1563.[CrossRef]
    [Google Scholar]
  14. Demeret, C., Yaniv, M. & Thierry, F. ( 1994; ). The E2 transcriptional repressor can compensate for SP1 activation of the human papillomavirus type 18 early promoter. J Virol 68, 7075–7082.
    [Google Scholar]
  15. de Villiers, E.-M., Fauquet, C., Broker, T. R., Bernard, H.-U. & zur Hausen, H. ( 2004; ). Classification of papillomaviruses. Virology 324, 17–27.[CrossRef]
    [Google Scholar]
  16. Dick, F. A., Sailhamer, E. & Dyson, N. J. ( 2000; ). Mutagenesis of the pRB pocket reveals that cell cycle arrest functions are separable from binding to viral oncoproteins. Mol Cell Biol 20, 3715–3727.[CrossRef]
    [Google Scholar]
  17. Dostatni, N., Thierry, F. & Yaniv, M. ( 1988; ). A dimer of BPV-1 E2 containing a protease resistant core interacts with its DNA target. EMBO J 7, 3807–3816.
    [Google Scholar]
  18. Flom, J. O., Brown, R. J., Jones, R. E. & Schonewald, J. ( 1980; ). Vaginal fibromas in a beaked whale, Mesoplodon densirostris. J Wildl Dis 16, 99–102.[CrossRef]
    [Google Scholar]
  19. Frattini, M. G. & Laimins, L. A. ( 1994; ). Binding of the human papillomavirus E1 origin-recognition protein is regulated through complex formation with the E2 enhancer-binding protein. Proc Natl Acad Sci U S A 91, 12398–12402.[CrossRef]
    [Google Scholar]
  20. Gardiol, D., Kühne, C., Glaunsinger, B., Lee, S. S., Javier, R. & Banks, L. ( 1999; ). Oncogenic human papillomavirus E6 proteins target the discs large tumour suppressor for proteasome-mediated degradation. Oncogene 18, 5487–5496.[CrossRef]
    [Google Scholar]
  21. Gerberding, J. L. ( 2004; ). Prevention of genital human papillomavirus infection. In Report to Congress. Atlanta, GA: Centers for Disease Control and Prevention. http://www.cdc.gov/std/HPV/2004HPV%20Report.pdf
  22. Gonzalez, S. L., Stremlau, M., He, X., Basile, J. R. & Münger, K. ( 2001; ). Degradation of the retinoblastoma tumor suppressor by the human papillomavirus type 16 E7 oncoprotein is important for functional inactivation and is separable from proteasomal degradation of E7. J Virol 75, 7583–7591.[CrossRef]
    [Google Scholar]
  23. Halbert, C. L., Demers, G. W. & Galloway, D. A. ( 1991; ). The E7 gene of human papillomavirus type 16 is sufficient for immortalization of human epithelial cells. J Virol 65, 473–478.
    [Google Scholar]
  24. Howley, P. M. & Lowy, D. R. ( 2001; ). Papillomaviruses and their replication. In Fields Virology, 4th edn, pp. 2197–2229. Edited by D. M. Knipe & P. M. Howley. Philadelphia, PA: Lippincott Williams & Wilkins.
  25. Iftner, T., Bierfelder, S., Csapo, Z. & Pfister, H. ( 1988; ). Involvement of human papillomavirus type 8 genes E6 and E7 in transformation and replication. J Virol 62, 3655–3661.
    [Google Scholar]
  26. Jackson, M. E., Pennie, W. D., McCaffery, R. E., Smith, K. T., Grindlay, G. J. & Campo, M. S. ( 1991; ). The B subgroup bovine papillomaviruses lack an identifiable E6 open reading frame. Mol Carcinog 4, 382–387.[CrossRef]
    [Google Scholar]
  27. Jones, D. L. & Münger, K. ( 1997; ). Analysis of the p53-mediated G1 growth arrest pathway in cells expressing the human papillomavirus type 16 E7 oncoprotein. J Virol 71, 2905–2912.
    [Google Scholar]
  28. Lambertsen, R. H., Kohn, B. A., Sundberg, J. P. & Buergelt, C. D. ( 1987; ). Genital papillomatosis in sperm whale bulls. J Wildl Dis 23, 361–367.[CrossRef]
    [Google Scholar]
  29. Lee, S. S., Glaunsinger, B., Mantovani, F., Banks, L. & Javier, R. T. ( 2000; ). Multi-PDZ domain protein MUPP1 is a cellular target for both adenovirus E4-ORF1 and high-risk papillomavirus type 18 E6 oncoproteins. J Virol 74, 9680–9693.[CrossRef]
    [Google Scholar]
  30. Münger, K., Basile, J. R., Duensing, S., Eichten, A., Gonzalez, S. L., Grace, M. & Zacny, V. L. ( 2001; ). Biological activities and molecular targets of the human papillomavirus E7 oncoprotein. Oncogene 20, 7888–7898.[CrossRef]
    [Google Scholar]
  31. Nguyen, M. L., Nguyen, M. M., Lee, D., Griep, A. E. & Lambert, P. F. ( 2003; ). The PDZ ligand domain of the human papillomavirus type 16 E6 protein is required for E6's induction of epithelial hyperplasia in vivo. J Virol 77, 6957–6964.[CrossRef]
    [Google Scholar]
  32. O'Connor, M. & Bernard, H.-U. ( 1995; ). Oct-1 activates the epithelial-specific enhancer of human papillomavirus type 16 via a synergistic interaction with NFI at a conserved composite regulatory element. Virology 207, 77–88.[CrossRef]
    [Google Scholar]
  33. O'Connor, M. J., Tan, S.-H., Tan, C.-H. & Bernard, H.-U. ( 1996; ). YY1 represses human papillomavirus type 16 transcription by quenching AP-1 activity. J Virol 70, 6529–6539.
    [Google Scholar]
  34. Patel, K. R., Smith, K. T. & Campo, M. S. ( 1987; ). The nucleotide sequence and genome organization of bovine papillomavirus type 4. J Gen Virol 68, 2117–2128.[CrossRef]
    [Google Scholar]
  35. Perrin, W. F., Würsig, B. & Thewissen, J. G. M. (editors) ( 2002; ). Interpretative summary of the phylogenetic relationships and geological ranges of important genera of cetaceans. In Encyclopedia of Marine Mammals, frontispiece. San Diego, CA: Academic Press.
  36. Phelps, W. C., Yee, C. L., Münger, K. & Howley, P. M. ( 1988; ). The human papillomavirus type 16 E7 gene encodes transactivation and transformation functions similar to those of adenovirus E1A. Cell 53, 539–547.[CrossRef]
    [Google Scholar]
  37. Rector, A., Bossart, G. D., Ghim, S. J., Sundberg, J. P., Jenson, A. B. & Van Ranst, M. ( 2004; ). Characterization of a novel close-to-root papillomavirus from a Florida manatee by using multiply primed rolling-circle amplification: Trichechus manatus latirostris papillomavirus type 1. J Virol 78, 12698–12702.[CrossRef]
    [Google Scholar]
  38. Rector, A., Lacave, G., Mostmans, S., Van Doorslaer, K., Rehtanz, M., Salbany, A., Ghim, S. J., Jenson, A. B. & Van Ranst, M. ( 2006; ). Genetic characterization of a novel close-to-root papillomavirus in a bottlenose dolphin: tursiops truncatus papillomavirus type 1 (TtPV-1). Abstract of the 34th European Association for Aquatic Mammals (EAAM) Conference, Riccione, Italy, 17–20 March 2006.
  39. Rehtanz, M. ( 1999; ). Identification of transcriptional control elements of the promoter P56 of human papillomavirus 18. Masters thesis, University of Cologne (in German).
  40. Scheffner, M., Werness, B. A., Huibregtse, J. M., Levine, A. J. & Howley, P. M. ( 1990; ). The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 63, 1129–1136.[CrossRef]
    [Google Scholar]
  41. Schmitt, A., Harry, J. B., Rapp, B., Wettstein, F. O. & Iftner, T. ( 1994; ). Comparison of the properties of the E6 and E7 genes of low- and high-risk cutaneous papillomaviruses reveals strongly transforming and high Rb-binding activity for the E7 protein of the low-risk human papillomavirus type 1. J Virol 68, 7051–7059.
    [Google Scholar]
  42. Sedman, J. & Stenlund, A. ( 1995; ). Co-operative interaction between the initiator E1 and the transcriptional activator E2 is required for replicator specific DNA replication of bovine papillomavirus in vivo and in vitro. EMBO J 14, 6218–6228.
    [Google Scholar]
  43. Sedman, S. A., Barbosa, M. S., Vass, W. C., Hubbert, N. L., Haas, J. A., Lowy, D. R. & Schiller, J. T. ( 1991; ). The full-length E6 protein of human papillomavirus type 16 has transforming and trans-activating activities and cooperates with E7 to immortalize keratinocytes in culture. J Virol 65, 4860–4866.
    [Google Scholar]
  44. Smola-Hess, S. & Pfister, H. ( 2002; ). Interaction of papillomaviral oncoproteins with cellular factors. In Structure-Function Relationships of Human Pathogenic Viruses, pp. 431–464. Edited by A. Holzenburg & E. Bogner. Dordrecht: Kluwer Academic.
  45. Stenlund, A. ( 2003; ). E1 initiator DNA binding specificity is unmasked by selective inhibition of non-specific DNA binding. EMBO J 22, 954–963.[CrossRef]
    [Google Scholar]
  46. Tan, S.-H., Leong, L. E.-C., Walker, P. A. & Bernard, H.-U. ( 1994; ). The human papillomavirus type 16 E2 transcription factor binds with low cooperativity to two flanking sites and represses the E6 promoter through displacement of Sp1 and TFIID. J Virol 68, 6411–6420.
    [Google Scholar]
  47. Taniguchi, A., Kikuchi, K., Nagata, K. & Yasumoto, S. ( 1993; ). A cell-type-specific transcription enhancer of type 16 human papillomavirus (HPV 16)-P97 promoter is defined with HPV-associated cellular events in human epithelial cell lines. Virology 195, 500–510.[CrossRef]
    [Google Scholar]
  48. Terai, M., DeSalle, R. & Burk, R. D. ( 2002; ). Lack of canonical E6 and E7 open reading frames in bird papillomaviruses: Fringilla coelebs papillomavirus and Psittacus erithacus timneh papillomavirus. J Virol 76, 10020–10023.[CrossRef]
    [Google Scholar]
  49. Thierry, F., Spyrou, G., Yaniv, M. & Howley, P. ( 1992; ). Two AP1 sites binding JunB are essential for human papillomavirus type 18 transcription in keratinocytes. J Virol 66, 3740–3748.
    [Google Scholar]
  50. Thomas, M., Laura, R., Hepner, K., Guccione, E., Sawyers, C., Lasky, L. & Banks, L. ( 2002; ). Oncogenic human papillomavirus E6 proteins target the MAGI-2 and MAGI-3 proteins for degradation. Oncogene 21, 5088–5096.[CrossRef]
    [Google Scholar]
  51. Titolo, S., Pelletier, A., Sauvé, F., Brault, K., Wardrop, E., White, P. W., Amin, A., Cordingley, M. G. & Archambault, J. ( 1999; ). Role of the ATP-binding domain of the human papillomavirus type 11 E1 helicase in E2-dependent binding to the origin. J Virol 73, 5282–5293.
    [Google Scholar]
  52. Van Bressem, M. F., Van Waerebeek, K. & Raga, J. A. ( 1999; ). A review of virus infections of cetaceans and the potential impact of morbilliviruses, poxviruses and papillomaviruses on host population dynamics. Dis Aquat Org 38, 53–65.[CrossRef]
    [Google Scholar]
  53. zur Hausen, H. & de Villiers, E.-M. ( 1994; ). Human papillomaviruses. Annu Rev Microbiol 48, 427–447.[CrossRef]
    [Google Scholar]
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vol. , part 12, pp. 3559 – 3565

Supplementary Methods.

GenBank accession numbers and hosts of animal and human PVs included in phylogenetic analysis.

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