1887

Abstract

Knowledge about biological diversity is the prerequisite to reliably reconstruct the evolution of pathogens such as papillomaviruses (PV). However, complete genomes of non-human PV have only been cloned and sequenced from 8 out of 18 orders within the Placentalia, although the host-specific variety of PV is considered much larger. We isolated and sequenced the complete genome of the first insectivoran PV type from hair follicle cells of the European hedgehog (), designated EHPV. We conducted phylogenetic analyses (maximum-likelihood criterion and Bayesian inference) with the genomic information of a systematically representative set of 67 PV types including EHPV. As inferred from amino acid sequence data of the separate genes E1, E2 and L1 as well as of the gene combination E6–E7–E1–E2–L1, EHPV clustered within the ----PV supertaxon and constituted the closest relative of genus infecting primates. Beside the typical organization of the PV genome, EHPV exhibited a 1172 bp, non-coding region between the E2 and the L2 open reading frames. This trait has been previously described for the only distantly related , but a common evolutionary origin of both non-coding regions is unlikely. Our results underscore the modular organization of the PV genome and the complex natural history of PV.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.008011-0
2009-03-01
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/jgv/90/3/626.html?itemId=/content/journal/jgv/10.1099/vir.0.008011-0&mimeType=html&fmt=ahah

References

  1. Ahola H., Bergman P., Ström A. C., Moreno-Lopéz J., Pettersson U. 1986; Organization and expression of the transforming region from the European elk papillomavirus (EEPV. Gene 50:195–205 [CrossRef]
    [Google Scholar]
  2. Antonsson A., Hansson B. G. 2002; Healthy skin of many animal species harbors papillomaviruses which are closely related to their human counterparts. J Virol 76:12537–12542 [CrossRef]
    [Google Scholar]
  3. Bernard H.-U., Calleja-Macias I. E., Dunn S. T. 2006; Genome variation of human papillomavirus types: phylogenetic and medical implications. Int J Cancer 118:1071–1076 [CrossRef]
    [Google Scholar]
  4. Bininda-Emonds O. R. P., Cardillo M., Jones K. E., MacPhee R. D. E., Beck R. M. D., Grenyer R., Price S. A., Vos R. A., Gittleman J. L., Purvis A. 2007; The delayed rise of present-day mammals. Nature 446:507–512 [CrossRef]
    [Google Scholar]
  5. Bravo I. G., Alonso Á. 2004; Mucosal human papillomaviruses encode four different E5 proteins whose chemistry and phylogeny correlate with malignant or benign growth. J Virol 78:13613–13626 [CrossRef]
    [Google Scholar]
  6. Bravo I. G., Müller M. 2005; Codon usage in papillomavirus genes. Papillomavirus Rep 16:63–72 [CrossRef]
    [Google Scholar]
  7. 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]
  8. 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]
  9. Dimmic M. W., Rest J. S., Mindell D. P., Goldstein R. A. 2002; rtREV: an amino acid substitution matrix for inference of retrovirus and reverse transcriptase phylogeny. J Mol Evol 55:65–73 [CrossRef]
    [Google Scholar]
  10. Doorbar J. 2005; The papillomavirus life cycle. J Clin Virol 32:Suppl. 1S7–S15
    [Google Scholar]
  11. Drummond A. J., Rambaut A. 2007; beast: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214 [CrossRef]
    [Google Scholar]
  12. Drummond D. A., Wilke C. O. 2008; Mistranslation-induced protein misfolding as a dominant constraint on coding-sequence evolution. Cell 134:341–352 [CrossRef]
    [Google Scholar]
  13. Forslund O., Antonsson A., Nordin P., Stenquist B., Hansson B. G. 1999; A broad range of human papillomavirus types detected with a general PCR method suitable for analysis of cutaneous tumours and normal skin. J Gen Virol 80:2437–2443
    [Google Scholar]
  14. Frith M. C., Hansen U., Weng Z. P. 2001; Detection of cis -element clusters in higher eukaryotic DNA. Bioinformatics 17:878–889 [CrossRef]
    [Google Scholar]
  15. García-Vallvé S., Alonso Á., Bravo I. G. 2005; Papillomaviruses: different genes have different histories. Trends Microbiol 13:514–521 [CrossRef]
    [Google Scholar]
  16. García-Vallvé S., Iglesias-Rozas J. R., Alonso Á., Bravo I. G. 2006; Different papillomaviruses have different repertoires of transcription factor binding sites: convergence and divergence in the upstream regulatory region. BMC Evol Biol 6:20 [CrossRef]
    [Google Scholar]
  17. Gasteiger E., Hoogland C., Gattiker A., Duvaud S., Wilkins M. R., Appel R. D., Bairoch A. 2005; Protein identification and analysis tools on the ExPASy server. In The Proteomics Protocols Handbook pp 571–607Edited by Walker J. M. Totowa, NJ: Humana Press;
    [Google Scholar]
  18. Gottschling M., Köhler A., Stockfleth E., Nindl I. 2007a; Phylogenetic analysis of beta-papillomaviruses as inferred from nucleotide and amino acid sequence data. Mol Phylogenet Evol 42:213–222 [CrossRef]
    [Google Scholar]
  19. Gottschling M., Stamatakis A., Nindl I., Stockfleth E., Alonso Á., Bravo I. G. 2007b; Multiple evolutionary mechanisms drive papillomavirus diversification. Mol Biol Evol 24:1242–1258 [CrossRef]
    [Google Scholar]
  20. Gottschling M., Wibbelt G., Wittstatt U., Stockfleth E., Nindl I. 2008; Novel papillomavirus isolates from Erinaceus europaeus (Erinaceidae, Insectivora) and the Cervidae (Artiodactyla), Cervus timorensis and Pudu puda , and phylogenetic analysis of partial sequence data. Virus Genes 36:281–287 [CrossRef]
    [Google Scholar]
  21. Hall T. A. 1999; BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98
    [Google Scholar]
  22. Hulo N., Bairoch A., Bulliard V., Cerutti L., Cuche B. A., de Castro E., Lachaize C., Langendijk-Genevaux P. S., Sigrist C. J. A. 2008; The 20 years of PROSITE. Nucleic Acids Res 36:D245–D249
    [Google Scholar]
  23. Jackson A. 2005; The effect of paralogous lineages on the application of reconciliation analysis by cophylogeny mapping. Syst Biol 54:127–145 [CrossRef]
    [Google Scholar]
  24. Katoh K., Kuma K., Toh H., Miyata T. 2005; mafft version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33:511–518 [CrossRef]
    [Google Scholar]
  25. Matys V., Fricke E., Geffers R., Gößling E., Haubrock M., Hehl R., Hornischer K., Karas D., Kel A. E. other authors 2003; transfac: transcriptional regulation, from patterns to profiles. Nucleic Acids Res 31:374–378 [CrossRef]
    [Google Scholar]
  26. Moreno-Lopéz J., Pettersson U., Dinter Z., Philipson L. 1981; Characterization of a papilloma virus from the European elk (EEPV). Virology 112:589–595 [CrossRef]
    [Google Scholar]
  27. Murphy W. J., Eizirik E., O'Brien S. J., Madsen O., Scally M., Douady C. J., Teeling E., Ryder O. A., Stanhope M. J. other authors 2001; Resolution of the early placental mammal radiation using Bayesian phylogenetics. Science 294:2348–2351 [CrossRef]
    [Google Scholar]
  28. Myers G., Lu H., Calef C., Leitner T. 1996; Heterogeneity of papillomaviruses. Semin Cancer Biol 7:349–358 [CrossRef]
    [Google Scholar]
  29. Nakai K., Horton P. 1999; psort: a program for detecting the sorting signals of proteins and predicting their subcellular localization. Trends Biochem Sci 24:34–35 [CrossRef]
    [Google Scholar]
  30. Narechania A., Chen Z., DeSalle R., Burk R. D. 2005; Phylogenetic incongruence among oncogenic genital alpha human papillomaviruses. J Virol 79:15503–15510 [CrossRef]
    [Google Scholar]
  31. Page R. D. M., Clayton D. H., Paterson A. M. 1996; Lice and cospeciation: a response to Barker. Int J Parasitol 26:213–218 [CrossRef]
    [Google Scholar]
  32. Puigbó P., Bravo I. G., Garcia-Vallvé S. 2008a; CAIcal: a combined set of tools to assess codon usage adaptation. Biol Direct 3:38 [CrossRef]
    [Google Scholar]
  33. Puigbó P., Bravo I. G., García-Vallvé S. 2008b; E-CAI: a novel server to estimate an expected value of Codon Adaptation Index (eCAI). BMC Bioinformatics 9:65 [CrossRef]
    [Google Scholar]
  34. Rector A., Van Doorslaer K., Bertelsen M., Barker I. K., Olberg R. A., Lemey P., Sundberg J. P., Van Ranst M. 2005; Isolation and cloning of the raccoon ( Procyon lotor ) papillomavirus type 1 by using degenerate papillomavirus-specific primers. J Gen Virol 86:2029–2033 [CrossRef]
    [Google Scholar]
  35. Rector A., Lemey P., Tachezy R., Mostmans S., Ghim S.-J., Van Doorslaer K., Roelke M., Bush M., Montali R. J. other authors 2007; Ancient papillomavirus-host co-speciation in Felidae. Genome Biol 8:R57 [CrossRef]
    [Google Scholar]
  36. Reyes A., Gissi C., Catzeflis F., Nevo E., Pesole G., Saccone C. 2004; Congruent mammalian trees from mitochondrial and nuclear genes using Bayesian methods. Mol Biol Evol 21:397–403
    [Google Scholar]
  37. Springer M. S., Stanhope M. J., Madsen O., de Jong W. W. 2004; Molecules consolidate the placental mammal tree. Trends Ecol Evol 19:430–438 [CrossRef]
    [Google Scholar]
  38. Stamatakis A. 2006; RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690 [CrossRef]
    [Google Scholar]
  39. Terai M., Burk R. D. 2002; Felis domesticus papillomavirus, isolated from a skin lesion, is related to canine oral papillomavirus and contains a 1.3 kb non-coding region between the E2 and L2 open reading frames. J Gen Virol 83:2303–2307
    [Google Scholar]
  40. Van Ranst M., Kaplan J. B., Sundberg J. P., Burk R. D. 1995; Molecular evolution of papillomaviruses. In Molecular Basis of Virus Evolution pp 455–476Edited by Gibbs A., Calisher C. H., García-Arenal F. Cambridge: Cambridge University Press;
    [Google Scholar]
  41. Varsani A., van der Walt E., Heath L., Rybicki E. P., Williamson A. L., Martin D. P. 2006; Evidence of ancient papillomavirus recombination. J Gen Virol 87:2527–2531 [CrossRef]
    [Google Scholar]
  42. Whelan S., Goldman N. 2001; A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18:691–699 [CrossRef]
    [Google Scholar]
  43. Zhao K. N., Liu W. J., Frazer I. H. 2003; Codon usage bias and A+T content variation in human papillomavirus genomes. Virus Res 98:95–104 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.008011-0
Loading
/content/journal/jgv/10.1099/vir.0.008011-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Supplementary material 2

PDF

Supplementary material 3

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error