1887

Abstract

Genome stability is a prerequisite for the production and use of adenoviruses for therapy of genetic diseases and cancer. To test the premise that the adenoviral genome is stable, the phylogenetic relationships of 16 adenovirus C (AdC) field isolates were studied in four genome regions: hexon, fiber, polymerase and E1A. The phylogenetic relationships in the fiber gene concurred with those in the hexon region. In contrast, the non-structural regions had marks of frequent recombination, to the point that an isolate of one serotype could contain non-structural proteins that were identical to the genes from a different serotype. Our results suggest that recombination among circulating adenoviruses is very frequent and plays an important role in shaping the phylogenetic relationships of adenovirus genomes. Analysis of the available complete genome sequences of AdB, AdC and AdD species showed that recombination shuffles genome fragments within a species, but not between species. One of the AdC field isolates possessed the fiber gene of AdC type 6, but a hexon gene that was distinct from all AdC serotypes. This strain could not be typed unambiguously in a neutralization test and might represent a novel serotype of AdC. Comparison of the right end (nt 18838–33452) of this isolate with that of the ATCC Ad6 strain showed clear evidence of multiple recombination events.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.83057-0
2008-02-01
2019-11-20
Loading full text...

Full text loading...

/deliver/fulltext/jgv/89/2/380.html?itemId=/content/journal/jgv/10.1099/vir.0.83057-0&mimeType=html&fmt=ahah

References

  1. Adhikary, A. K., Banik, U., Numaga, J., Suzuki, E., Inada, T. & Okabe, N. ( 2004; ). Heterogeneity of the fibre sequence in subgenus C adenoviruses. J Clin Pathol 57, 612–617.[CrossRef]
    [Google Scholar]
  2. Adrian, T., Schafer, G., Cooney, M. K., Fox, J. P. & Wigand, R. ( 1988; ). Persistent enteral infections with adenovirus types 1 and 2 in infants: no evidence of reinfection. Epidemiol Infect 101, 503–509.[CrossRef]
    [Google Scholar]
  3. Bailey, A. & Mautner, V. ( 1994; ). Phylogenetic relationships among adenovirus serotypes. Virology 205, 438–452.[CrossRef]
    [Google Scholar]
  4. Boursnell, M. E. & Mautner, V. ( 1981; ). Recombination in adenovirus: crossover sites in intertypic recombinants are located in regions of homology. Virology 112, 198–209.[CrossRef]
    [Google Scholar]
  5. Breyer, B., Jiang, W., Cheng, H., Zhou, L., Paul, R., Feng, T. & He, T. C. ( 2001; ). Adenoviral vector-mediated gene transfer for human gene therapy. Curr Gene Ther 1, 149–162.[CrossRef]
    [Google Scholar]
  6. Casas, I., Avellon, A., Mosquera, M., Jabado, O., Echevarria, J. E., Campos, R. H., Rewers, M., Perez-Brena, P., Lipkin, W. I. & Palacios, G. ( 2005; ). Molecular identification of adenoviruses in clinical samples by analyzing a partial hexon genomic region. J Clin Microbiol 43, 6176–6182.[CrossRef]
    [Google Scholar]
  7. Chroboczek, J., Bieber, F. & Jacrot, B. ( 1992; ). The sequence of the genome of adenovirus type 5 and its comparison with the genome of adenovirus type 2. Virology 186, 280–285.[CrossRef]
    [Google Scholar]
  8. Crawford-Miksza, L. K. & Schnurr, D. P. ( 1996; ). Adenovirus serotype evolution is driven by illegitimate recombination in the hypervariable regions of the hexon protein. Virology 224, 357–367.[CrossRef]
    [Google Scholar]
  9. Ebner, K., Pinsker, W. & Lion, T. ( 2005; ). Comparative sequence analysis of the hexon gene in the entire spectrum of human adenovirus serotypes: phylogenetic, taxonomic and clinical implications. J Virol 79, 12635–12642.[CrossRef]
    [Google Scholar]
  10. Fallaux, F. J., Kranenburg, O., Cramer, S. J., Houweling, A., Van Ormondt, H., Hoeben, R. C. & Van Der Eb, A. J. ( 1996; ). Characterization of 911: a new helper cell line for the titration and propagation of early region 1-deleted adenoviral vectors. Hum Gene Ther 7, 215–222.[CrossRef]
    [Google Scholar]
  11. Fallaux, F. J., Bout, A., van der Velde, I., van den Wollenberg, D. J., Hehir, K. M., Keegan, J., Auger, C., Cramer, S. J., van Ormondt, H. & other authors ( 1998; ). New helper cells and matched early region 1-deleted adenovirus vectors prevent generation of replication-competent adenoviruses. Hum Gene Ther 9, 1909–1917.[CrossRef]
    [Google Scholar]
  12. Felsenstein, J. ( 1989; ). phylip: phylogeny inference package (version 3.2). Cladistics 5, 164–166.
    [Google Scholar]
  13. Gagnebin, J., Brunori, M., Otter, M., Juillerat-Jeanneret, L., Monnier, P. & Iggo, R. ( 1999; ). A photosensitising adenovirus for photodynamic therapy. Gene Ther 6, 1742–1750.[CrossRef]
    [Google Scholar]
  14. Garnett, C. T., Erdman, D., Xu, W. & Gooding, L. R. ( 2002; ). Prevalence and quantitation of species C adenovirus DNA in human mucosal lymphocytes. J Virol 76, 10608–10616.[CrossRef]
    [Google Scholar]
  15. Grodzicker, T., Anderson, C., Sharp, P. A. & Sambrook, J. ( 1974; ). Conditional lethal mutants of adenovirus 2-simian virus 40 hybrids. I. Host range mutants of Ad2+ND1. J Virol 13, 1237–1244.
    [Google Scholar]
  16. 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]
  17. Hay, A. J., Gregory, V., Douglas, A. R. & Lin, Y. P. ( 2001; ). The evolution of human influenza viruses. Philos Trans R Soc Lond B Biol Sci 356, 1861–1870.[CrossRef]
    [Google Scholar]
  18. Hehir, K. M., Armentano, D., Cardoza, L. M., Choquette, T. L., Berthelette, P. B., White, G. A., Couture, L. A., Everton, M. B., Keegan, J. & other authors ( 1996; ). Molecular characterization of replication-competent variants of adenovirus vectors and genome modifications to prevent their occurrence. J Virol 70, 8459–8467.
    [Google Scholar]
  19. Horwitz, M. S. ( 2001; ). Adenoviruses. In Fields Virology, 4th edn, vol. 2, pp. 2301–2326. Edited by D. M. Knipe & P. M. Howley. Philadelphia, PA: Lippincott Williams & Wilkins.
  20. Kangasniemi, L., Kiviluoto, T., Kanerva, A., Raki, M., Ranki, T., Sarkioja, M., Wu, H., Marini, F., Hockerstedt, K. & other authors ( 2006; ). Infectivity-enhanced adenoviruses deliver efficacy in clinical samples and orthotopic models of disseminated gastric cancer. Clin Cancer Res 12, 3137–3144.[CrossRef]
    [Google Scholar]
  21. Lauer, K. P., Llorente, I., Blair, E., Seto, J., Krasnov, V., Purkayastha, A., Ditty, S. E., Hadfield, T. L., Buck, C. & other authors ( 2004; ). Natural variation among human adenoviruses: genome sequence and annotation of human adenovirus serotype 1. J Gen Virol 85, 2615–2625.[CrossRef]
    [Google Scholar]
  22. Lin, B., Wang, Z., Vora, G. J., Thornton, J. A., Schnur, J. M., Thach, D. C., Blaney, K. M., Ligler, A. G., Malanoski, A. P. & other authors ( 2006; ). Broad-spectrum respiratory tract pathogen identification using resequencing DNA microarrays. Genome Res 16, 527–535.[CrossRef]
    [Google Scholar]
  23. Lochmuller, H., Jani, A., Huard, J., Prescott, S., Simoneau, M., Massie, B., Karpati, G. & Acsadi, G. ( 1994; ). Emergence of early region 1-containing replication-competent adenovirus in stocks of replication-defective adenovirus recombinants (delta E1+delta E3) during multiple passages in 293 cells. Hum Gene Ther 5, 1485–1491.[CrossRef]
    [Google Scholar]
  24. Lukashev, A. N. ( 2005; ). Role of recombination in evolution of enteroviruses. Rev Med Virol 15, 157–167.[CrossRef]
    [Google Scholar]
  25. Lukashev, A. N., Lashkevich, V. A., Ivanova, O. E., Koroleva, G. A., Hinkkanen, A. E. & Ilonen, J. ( 2005; ). Recombination in circulating enterovirus B: independent evolution of structural and non-structural genome regions. J Gen Virol 86, 3281–3290.[CrossRef]
    [Google Scholar]
  26. Madisch, I., Harste, G., Pommer, H. & Heim, A. ( 2005; ). Phylogenetic analysis of the main neutralization and hemagglutination determinants of all human adenovirus prototypes as a basis for molecular classification and taxonomy. J Virol 79, 15265–15276.[CrossRef]
    [Google Scholar]
  27. Martin, D. P., Williamson, C. & Posada, D. ( 2005; ). rdp2: recombination detection and analysis from sequence alignments. Bioinformatics 21, 260–262.[CrossRef]
    [Google Scholar]
  28. Mautner, V. & Boursnell, M. E. ( 1983; ). Recombination in adenovirus: DNA sequence analysis of crossover sites in intertypic recombinants. Virology 131, 1–10.[CrossRef]
    [Google Scholar]
  29. Mautner, V., Williams, J., Sambrook, J., Sharp, P. A. & Grodzicker, T. ( 1975; ). The location of the genes coding for hexon and fiber proteins in adenovirus DNA. Cell 5, 93–99.[CrossRef]
    [Google Scholar]
  30. Ni, S., Bernt, K., Gaggar, A., Li, Z. Y., Kiem, H. P. & Lieber, A. ( 2005; ). Evaluation of biodistribution and safety of adenovirus vectors containing group B fibers after intravenous injection into baboons. Hum Gene Ther 16, 664–677.[CrossRef]
    [Google Scholar]
  31. Oberste, M. S., Maher, K. & Pallansch, M. A. ( 2004; ). Evidence for frequent recombination within species human enterovirus B based on complete genomic sequences of all thirty-seven serotypes. J Virol 78, 855–867.[CrossRef]
    [Google Scholar]
  32. Palmer, D. H., Mautner, V. & Kerr, D. J. ( 2002; ). Clinical experience with adenovirus in cancer therapy. Curr Opin Mol Ther 4, 423–434.
    [Google Scholar]
  33. Roberts, R. J., Akusjaervi, G., Alestroem, P., Gelinas, R. E., Gingeras, T. R., Sciaky, D. & Pettersson, U. ( 1986; ). A consensus sequence for the adenovirus-2 genome. In Adenovirus DNA, pp. 1–51. Edited by W. Doerfler. Boston: Martinus Nijhoff.
  34. Salminen, M. O., Carr, J. K., Burke, D. S. & McCutchan, F. E. ( 1995; ). Identification of breakpoints in intergenotypic recombinants of HIV type 1 by bootscanning. AIDS Res Hum Retroviruses 11, 1423–1425.[CrossRef]
    [Google Scholar]
  35. Segerman, A., Arnberg, N., Erikson, A., Lindman, K. & Wadell, G. ( 2003; ). There are two different species B adenovirus receptors: sBAR, common to species B1 and B2 adenoviruses, and sB2AR, exclusively used by species B2 adenoviruses. J Virol 77, 1157–1162.[CrossRef]
    [Google Scholar]
  36. Shenk, T. E. ( 2001; ). Adenoviridae: the viruses and their replication. In Fields Virology, 4th edn, vol. 2, pp. 2265–2300. Edited by D. M. Knipe & P. M. Howley. Philadelphia, PA: Lippincott Williams & Wilkins.
  37. Stoff-Khalili, M. A., Rivera, A. A., Glasgow, J. N., Le, L. P., Stoff, A., Everts, M., Tsuruta, Y., Kawakami, Y., Bauerschmitz, G. J. & other authors ( 2005; ). A human adenoviral vector with a chimeric fiber from canine adenovirus type 1 results in novel expanded tropism for cancer gene therapy. Gene Ther 12, 1696–1706.[CrossRef]
    [Google Scholar]
  38. Thompson, J. D., Higgins, D. G. & Gibson, T. J. ( 1994; ). clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673–4680.[CrossRef]
    [Google Scholar]
  39. Thompson, J. D., Gibson, T., Plewniak, F., Jeanmougin, F. & Higgins, D. ( 1997; ). The clustal_x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25, 4876–4882.[CrossRef]
    [Google Scholar]
  40. Wadell, G., Hammarskjold, M. L., Winberg, G., Varsanyi, T. M. & Sundell, G. ( 1980; ). Genetic variability of adenoviruses. Ann N Y Acad Sci 354, 16–42.[CrossRef]
    [Google Scholar]
  41. Williams, J., Grodzicker, T., Sharp, P. & Sambrook, J. ( 1975; ). Adenovirus recombination: physical mapping of crossover events. Cell 4, 113–119.[CrossRef]
    [Google Scholar]
  42. Young, L. S., Searle, P. F., Onion, D. & Mautner, V. ( 2006; ). Viral gene therapy strategies: from basic science to clinical application. J Pathol 208, 299–318.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.83057-0
Loading
/content/journal/jgv/10.1099/vir.0.83057-0
Loading

Data & Media loading...

Supplements

vol. , part 2, pp. 380 – 388

Oligonucleotides used to amplify AdC genome fragments [ PDF] (34 KB)



PDF

Most Cited This Month

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