Molecular characterization of novel mucosotropic papillomaviruses from a Florida manatee () Free

Abstract

We isolated two new manatee papillomavirus (PV) types, TmPV3 and TmPV4, from a Florida manatee (). Two PV types were previously isolated from this species. TmPV1 is widely dispersed amongst manatees and a close-to-root PV; not much is known about TmPV2. The genomes of TmPV3 and TmPV4 were 7622 and 7771 bp in size, respectively. Both PVs had a genomic organization characteristic of all PVs, with one non-coding region and seven ORFs, including the E7 ORF that is absent in other cetacean PVs. Although these PVs were isolated from separate genital lesions of the same manatee, an enlarged E2/E4 ORF was found only in the TmPV4 genome. The full genome and L1 sequence similarities between TmPV3 and TmPV4 were 63.2 and 70.3 %, respectively. These genomes shared only 49.1 and 50.2 % similarity with TmPV1. The pairwise alignment of L1 nucleotide sequences indicated that the two new PVs nested in a monophyletic group of the genus , together with the cutaneotropic TmPV1 and TmPV2.

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2015-12-01
2024-03-29
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References

  1. Bernard H. U., Burk R. D., Chen Z., van Doorslaer K., zur Hausen H., de Villiers E. M. 2010; Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 401:70–79 [View Article][PubMed]
    [Google Scholar]
  2. Bossart G. D., Cray C., Solorzano J. L., Decker S. J., Cornell L. H., Altman N. H. 1996; Cutaneous papovaviral-like papillomatosis in a killer whale (Orcinus orca). Mar Mamm Sci 12:274–281 [View Article]
    [Google Scholar]
  3. 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 [View Article][PubMed]
    [Google Scholar]
  4. Bossart G. D., Ghim S., Rehtanz M., Goldstein J., Varela R., Ewing R. Y., Fair P. A., Lenzi R., Joseph B., other authors. 2005; Orogenital neoplasia in Atlantic bottlenose dolphins (Tursiops truncatus). Aquat Mamm 31:473–480 [View Article]
    [Google Scholar]
  5. Bossart G. D., Romano T. A., Peden-Adams M. M., Rice C. D., Fair P. A., Goldstein J. D., Kilpatrick D., Cammen K., Reif J. S. 2008; Hematological, biochemical and immunological findings in Atlantic bottlenose dolphins (Tursiops truncatus) with orogenital papillomas. Aquat Mamm 34:166–177 [View Article]
    [Google Scholar]
  6. Burk R. D., Chen Z., van Doorslaer K. 2015; Creation of 21 new species and 10 new genera in the family Papillomaviridae (animal DNA viruses and retroviruses). http://talk.ictvonline.org/files/proposals/animal_dna_viruses_and_retroviruses/m/animal_dna_newly_submitted/5403.aspx
  7. Capone G., Calabrò M., Lucchese G., Fasano C., Girardi B., Polimeno L., Kanduc D. 2013; Peptide matching between Epstein-Barr virus and human proteins. Pathog Dis 69:205–212 [View Article][PubMed]
    [Google Scholar]
  8. Cuomo L., Cirone M., Di Gregorio A. O., Vitillo M., Cattivelli M., Magliocca V., Maiorano S., Meledandri M., Scagnolari C., other authors. 2015; Elevated antinuclear antibodies and altered anti-Epstein-Barr virus immune responses. Virus Res 195:95–99 [View Article][PubMed]
    [Google Scholar]
  9. de Villiers E. M., Fauquet C., Broker T. R., Bernard H. U., zur Hausen H. 2004; Classification of papillomaviruses. Virology 324:17–27 [View Article][PubMed]
    [Google Scholar]
  10. Dejucq N., Jégou B. 2001; Viruses in the mammalian male genital tract and their effects on the reproductive system. Microbiol Mol Biol Rev 65:208–231 [View Article][PubMed]
    [Google Scholar]
  11. Donà M. G., Rehtanz M., Adimey N. M., Bossart G. D., Jenson A. B., Bonde R. K., Ghim S. J. 2011; Seroepidemiology of TmPV1 infection in captive and wild Florida manatees (Trichechus manatus latirostris). J Wildl Dis 47:673–684 [View Article][PubMed]
    [Google Scholar]
  12. Doorbar J. 2013; The E4 protein; structure, function and patterns of expression. Virology 445:80–98 [View Article][PubMed]
    [Google Scholar]
  13. Fauquet C. M., Fargette D. 2005; International Committee on Taxonomy of Viruses and the 3,142 unassigned species. Virol J 2:64 [View Article][PubMed]
    [Google Scholar]
  14. Florida Fish and Wildlife Conservation Commission 2002; Final biological status review of the Florida manatee (Trichecus manatus latirostris). St. Petersburg: Florida Maritime Research Institute;
    [Google Scholar]
  15. Gauthier J. M., Dillner J., Yaniv M. 1991; Structural analysis of the human papillomavirus type 16-E2 transactivator with antipeptide antibodies reveals a high mobility region linking the transactivation and the DNA-binding domains. Nucleic Acids Res 19:7073–7079 [View Article][PubMed]
    [Google Scholar]
  16. Ghim S. J., Joh J., Mignucci-Giannoni A. A., Rivera-Guzmán A. L., Falcón-Matos L., Alsina-Guerrero M. M., Bossart G. D., other authors. 2014; Genital papillomatosis associated with two novel mucosotropic papillomaviruses from a Florida manatee (Trichechus manatus latirostris). Aquat Mamm 40:195–200 [View Article]
    [Google Scholar]
  17. Gottschling M., Bravo I. G., Schulz E., Bracho M. A., Deaville R., Jepson P. D., Van Bressem M. F., Stockfleth E., Nindl I. 2011; Modular organizations of novel cetacean papillomaviruses. Mol Phylogenet Evol 59:34–42 [View Article][PubMed]
    [Google Scholar]
  18. Hegde R. S. 2002; The papillomavirus E2 proteins: structure, function, and biology. Annu Rev Biophys Biomol Struct 31:343–360 [View Article][PubMed]
    [Google Scholar]
  19. Howley P. M., Lowy D. R. 2007 Papillomaviruses Philadelphia, PA: Lippincott Williams & Wilkins;
    [Google Scholar]
  20. Joh J., Hopper K., Van Doorslaer K., Sundberg J. P., Jenson A. B., Ghim S. J. 2009; Macaca fascicularis papillomavirus type 1: a non-human primate betapapillomavirus causing rapidly progressive hand and foot papillomatosis. J Gen Virol 90:987–994 [View Article][PubMed]
    [Google Scholar]
  21. Joh J., Jenson A. B., King W., Proctor M., Ingle A., Sundberg J. P., Ghim S. J. 2011; Genomic analysis of the first laboratory-mouse papillomavirus. J Gen Virol 92:692–698 [View Article][PubMed]
    [Google Scholar]
  22. Katoh K., Standley D. M. 2013; mafft multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780 [View Article][PubMed]
    [Google Scholar]
  23. Katoh K., Misawa K., Kuma K., Miyata T. 2002; mafft: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066 [View Article][PubMed]
    [Google Scholar]
  24. 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 [View Article][PubMed]
    [Google Scholar]
  25. Lockhart A. B., Thrall P. H., Antonovics J. 1996; Sexually transmitted diseases in animals: ecological and evolutionary implications. Biol Rev Camb Philos Soc 71:415–471 [View Article][PubMed]
    [Google Scholar]
  26. McBride A. A. 2013; The papillomavirus E2 proteins. Virology 445:57–79 [View Article][PubMed]
    [Google Scholar]
  27. Miller M. A., Pfeiffer W., Schwartz T. 2010; Creating the CIPRES Science Gateway for inference of large phylogenetic trees. Paper presented at the. Gateway Computing Environments Workshop New Orleans, LA:
    [Google Scholar]
  28. 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 [View Article][PubMed]
    [Google Scholar]
  29. Rector A., Stevens H., Lacave G., Lemey P., Mostmans S., Salbany A., Vos M., Van Doorslaer K., Ghim S. J., other authors. 2008; Genomic characterization of novel dolphin papillomaviruses provides indications for recombination within the Papillomaviridae . Virology 378:151–161 [View Article][PubMed]
    [Google Scholar]
  30. Rehtanz M., Bossart G. D., Fair P. A., Reif J. S., Ghim S. J., Jenson A. B. 2012; Papillomaviruses and herpesviruses: who is who in genital tumor development of free-ranging Atlantic bottlenose dolphins (Tursiops truncatus)?. Vet Microbiol 160:297–304 [View Article][PubMed]
    [Google Scholar]
  31. Rehtanz M., Ghim S. J., Rector A., Van Ranst M., Fair P. A., Bossart G. D., Jenson A. B. 2006; Isolation and characterization of the first American bottlenose dolphin papillomavirus: Tursiops truncatus papillomavirus type 2. J Gen Virol 87:3559–3565 [CrossRef]
    [Google Scholar]
  32. Robles-Sikisaka R., Rivera R., Nollens H. H., St Leger J., Durden W. N., Stolen M., Burchell J., Wellehan J. F. Jr 2012; Evidence of recombination and positive selection in cetacean papillomaviruses. Virology 427:189–197 [View Article][PubMed]
    [Google Scholar]
  33. Schuck S., Stenlund A. 2006; Surface mutagenesis of the bovine papillomavirus E1 DNA binding domain reveals residues required for multiple functions related to DNA replication. J Virol 80:7491–7499 [View Article][PubMed]
    [Google Scholar]
  34. Schulz E., Gottschling M., Ulrich R. G., Richter D., Stockfleth E., Nindl I. 2012; Isolation of three novel rat and mouse papillomaviruses and their genomic characterization. PLoS One 7:e47164 [View Article][PubMed]
    [Google Scholar]
  35. Stamatakis A. 2014; RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313 [View Article][PubMed]
    [Google Scholar]
  36. Van Bressem M. F., Cassonnet P., Rector A., Desaintes C., Van Waerebeek K., Alfaro-Shigueto J., Van Ranst M., Orth G. 2007; Genital warts in Burmeister's porpoises: characterization of Phocoena spinipinnis papillomavirus type 1 (PsPV-1) and evidence for a second, distantly related PsPV. J Gen Virol 88:1928–1933 [View Article][PubMed]
    [Google Scholar]
  37. Van Bressem M. F., Raga J. A., Di Guardo G., Jepson P. D., Duignan P. J., Siebert U., Barrett T., Santos M. C., Moreno I. B., other authors. 2009; Emerging infectious diseases in cetaceans worldwide and the possible role of environmental stressors. Dis Aquat Organ 86:143–157 [View Article][PubMed]
    [Google Scholar]
  38. Van Doorslaer K. 2013; Evolution of the Papillomaviridae . Virology 445:11–20 [View Article][PubMed]
    [Google Scholar]
  39. Zheng Z. M., Baker C. C. 2006; Papillomavirus genome structure, expression, and post-transcriptional regulation. Front Biosci 11:2286–2302 [View Article][PubMed]
    [Google Scholar]
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