Skip to main content
Log in

Molecular Anatomy of Tupaia (Tree Shrew) adenovirus Genome; Evolution of Viral Genes and Viral Phylogeny

  • Published:
Virus Genes Aims and scope Submit manuscript

Abstract

Adenoviruses are globally spread and infect species in all five taxons of vertebrates. Outstanding attention is focused on adenoviruses because of their transformation potential, their possible usability as vectors in gene therapy and their applicability in studies dealing with, e.g. cell cycle control, DNA replication, transcription, splicing, virus–host interactions, apoptosis, and viral evolution. The accumulation of genetic data provides the basis for the increase of our knowledge about adenoviruses. The Tupaia adenovirus (TAV) infects members of the genus Tupaiidae that are frequently used as laboratory animals in behavior research dealing with questions about biological and molecular processes of stress in mammals, in neurobiological and physiological studies, and as model organisms for human hepatitis B and C virus infections. In the present study the TAV genome underwent an extensive analysis including determination of codon usage, CG depletion, gene content, gene arrangement, potential splice sites, and phylogeny. The TAV genome has a length of 33,501 bp with a G+C content of 49.96%. The genome termini show a strong CG depletion that could be due to methylation of these genome regions during the viral replication cycle. The analysis of the coding capacity of the complete TAV genome resulted in the identification of 109 open reading frames (ORFs), of which 38 were predicted to be real viral genes. TAV was classified within the genus Mastadenovirus characterized by typical gene content, arrangement, and homology values of 29 conserved ORFs. Phylogenetic trees show that TAV is part of a separate evolutionary lineage and no mastadenovirus species can be considered as the most related. In contrast to other mastadenoviruses a direct ancestor of TAV captured a DUT gene from its mammalian host, presumably controlling local dUTP levels during replication and enhance viral replication in non-dividing host tissues. Furthermore, TAV possesses a second DNA-binding protein gene, that is likely to play a role in the determination of the host range. In view of these data it is conceivable that TAV underwent evolutionary adaptations to its biological environment resulting in the formation of special genomic components that provided TAV with the ability to expand its host range during viral evolution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Rowe W.P., Huebner R.J., Gilmore L.K., Parrot R.H., Ward T.G., Proc Soc Exp Biol Med 84, 570-573, 1953.

    Google Scholar 

  2. Shenk T.E., Adenoviridae: The viruses and their replication, in Knipe D.M. and Howley P.M. (eds), Fields Virology, Volume2, Fourth Edition. Lippincott Williams & Wilkins, 2001, pp. 2265-2300.

  3. Barnett B.G., Crews C.J., and Douglas J.T., Biochim Biophys Acta 1575, 1-14, 2002.

    Google Scholar 

  4. Legrand V., Leissner P., Winter A., Mehtali M., and Lusky M., Curr Gene Ther 2, 323-239, 2002.

    Google Scholar 

  5. Mitani K. and Kubo S., Curr Gene Ther 2, 135-144, 2002.

    Google Scholar 

  6. Benkö M. and Harrach B., Arch Virol 43, 829-837, 1998.

    Google Scholar 

  7. Both G.W., Atadenovirus. Adenoviridae, in Tidona C.A. and Darai G. (eds), The Springer Index of Viruses, Springer-Verlag, Berlin Heidelberg New York, 2002, pp. 2-8.

    Google Scholar 

  8. Davison A.J., Wright K.M., and Harrach B., J Gen Virol 81, 2431-2439, 2000.

    Google Scholar 

  9. Harrach B., Aviadenovirus. Adenoviridae, in Tidona C.A. and Darai G. (eds), The Springer Index of Viruses, Springer-Verlag, Berlin Heidelberg New York, 2002, pp. 9-18.

    Google Scholar 

  10. Horwitz M.S., Adenoviruses, in Knipe D.M. and Howley P.M. (eds), Fields Virology, Volume 2, Fourth Edition. Lippincott Williams & Wilkins, 2000, pp. 2301-2326.

  11. van Regenmortel M.H.V., Fauquet C.M., and Bishop D.H.L. (eds), Virus Taxonomy. Seventh Report of the International Committee on Taxonomy of Viruses, Academic Press, San Diego, 2000.

    Google Scholar 

  12. Wadell G., Mastadenovirus. Adenoviridae, in Tidona C.A., and Darai G. (eds), The Springer Index of Viruses, Springer-Verlag, Berlin Heidelberg, New York, 2002, pp. 19-28.

    Google Scholar 

  13. Chiocca S., Kurzbauer R., Schaffner G., Baker A., Mautner V., and Cotten M., J Virol 70, 2939-2949, 1996.

    Google Scholar 

  14. Chroboczek J., Bieber F., and Jacrot B., Virology 186, 280-285, 1992.

    Google Scholar 

  15. Davison A.J., Telford E.A.R., Watson M.S., McBride K., and Mautner V., J Mol Biol 234, 1308-1316, 1993.

    Google Scholar 

  16. Hess M., Blocker H., and Brandt P., Virology 238, 145-156, 1997.

    Google Scholar 

  17. Khatri A. and Both G.W., Virology 245, 128-141, 1998.

    Google Scholar 

  18. Meissner J.D., Hirsch G.N., LaRue E.A., Fulcher R.A., and Spindler K.R., Virus Res 51, 53-64, 1997.

    Google Scholar 

  19. Morrison M.D., Onions D.E., and Nicolson L., J Gen Virol 78, 873-878, 1997.

    Google Scholar 

  20. Nagy M., Nagy E., and Tuboly T., J Gen Viro 82, 525-529, 2001.

    Google Scholar 

  21. Ojkic D. and Nagy E., J Gen Virol 81, 1833-1837, 2000.

    Google Scholar 

  22. Pitcovski J., Mualem M., Rei-Koren Z., Krispel S., Shmueli E., Peretz Y., Gutter B., Gallili G.E., Michael A., and Goldberg D., Virology 249, 307-315, 1998.

    Google Scholar 

  23. Reddy P.S., Idamakanti N., Song J.Y., Lee J.B., Hyun B.H., Park J.H., Cha S.H., Bae Y.T., Tikoo S.K., and Babiuk L.A., Virology 25, 414-426, 1998.

    Google Scholar 

  24. Reddy P.S., Idamakanti N., Zakhartchouk A.N., Baxi M.K., Lee J.B., Pyne C., Babiuk L.A., and Tikoo S.K., J Virol 72, 1394-1402, 1998.

    Google Scholar 

  25. Roberts R.J., O'Neill K.E., and Yen C.T., J Biol Chem 259, 13968-13975, 1984.

    Google Scholar 

  26. Schöndorf E., Bahr U., Handermann M., and Darai G., J Virol 77, 4345-4356, 2003.

    Google Scholar 

  27. Sprengel J., Schmitz B., Heuss-Neitzel D., and Doerfler W., Curr Top Microbiol Immunol 199, 189-274, 1995.

    Google Scholar 

  28. Vrati S., Brookes D.E., Strike P., Khatri A., Boyle D.B., and Both G.W., Virology 220, 186-199, 1996.

    Google Scholar 

  29. Brinckmann U., Darai G., and Flügel R.M., EMBO J 2, 2185-2188, 1983a.

    Google Scholar 

  30. Brinckmann U., Darai G., and Flügel R.M., Gene 24, 131-135, 1983b.

    Google Scholar 

  31. Darai G., Matz B., Flügel R.M., Grafe A., Gelderblom H., and Delius H., Virology 104, 122-138, 1980.

    Google Scholar 

  32. Faissner A., Darai G., and Flügel R.M., Intervirology 14, 272-276, 1980.

    Google Scholar 

  33. Flügel R.M., Bannert H., Suhai S., and Darai G., Gene 34, 73-80, 1985.

    Google Scholar 

  34. Matz B., Delius H., Flügel R.M., and Darai G., J Gen Virol 51, 421-423, 1980.

    Google Scholar 

  35. Song B., Hu S.L., Darai G., Spindler K.R., and Young C.S., Virology 220, 390-401, 1996.

    Google Scholar 

  36. Van Kampen M., De Kloet E.R., Flugge G., and Fuchs E., Eur J Pharmacol 457, 207-216, 2002.

    Google Scholar 

  37. Bartolomucci A., de Biurrun G., Czeh B., van Kampen M., and Fuchs E., Eur Neurosci 15, 1863-1866, 2002.

    Google Scholar 

  38. Meyer U., van Kampen M., Isovich E., Flugge G., and Fuchs E., Hippocampus 11, 329-336, 2001.

    Google Scholar 

  39. Czeh B., Michaelis T., Watanabe T., Frahm J., de Biurrun G., van Kampen M., Bartolomucci A., and Fuchs E., Proc Natl Acad Sci USA 98, 12796-12801, 2001.

    Google Scholar 

  40. Fuchs E. and Flugge G., Z Psychosom Med Psychother 47, 80-97, 2001.

    Google Scholar 

  41. Lucassen P.J., Vollmann-Honsdorf G.K., Gleisberg M., Czeh B., De Kloet E.R., and Fuchs E., Eur J Neurosci 14, 161-166, 2001.

    Google Scholar 

  42. Fuchs E., Flugge G., Ohl F., Lucassen P., Vollmann-Honsdorf G.K., and Michaelis T., Physiol Behav 73, 285-291, 2001.

    Google Scholar 

  43. Bosking W.H., Crowley J.C., and Fitzpatrick D., Nat Neurosci 5, 874-882, 2002.

    Google Scholar 

  44. Suss M., Washausen S., Kuhn H.J., and Knabe W., J Neurosci Methods 113, 147-158, 2002.

    Google Scholar 

  45. Zhao X., Tang Z.Y., Klumpp B., Wolff-Vorbeck G., Barth H., Levy S., von Weizsacker F., Blum H.E., and Baumert T.F., J Clin Invest 109, 221-232, 2002.

    Google Scholar 

  46. Kock J., Nassal M., MacNelly S., Baumert T.F., Blum H.E., and von Weizsacker F., J Virol 75, 5084-5089, 2001.

    Google Scholar 

  47. Park U.S., Su J.J., Ban K.C., Qin L., Lee E.H., and Lee Y.I., Gene 251, 73-80, 2000.

    Google Scholar 

  48. Nishihara H., Terai Y., and Okada N., Mol Biol Evol 119, 1964-1972, 2002.

    Google Scholar 

  49. Flugge P., Fuchs E., Gunther E., and Walter L., Immunogenetics 53, 984-988, 2002.

    Google Scholar 

  50. Schmitz J., Ohme M., and Zischler H., Mol Biol Evol 17, 1334-1343, 2000.

    Google Scholar 

  51. Bahr U. and Darai G., J Virol 75, 4854-4870, 2001.

    Google Scholar 

  52. Tidona C.A., Kurz H.W., Gelderblom H.R., and Darai G., Virology 258, 425-434, 1999.

    Google Scholar 

  53. Kurz W., Gelderblom H., Flügel R.M., and Darai G., Intervirology 25, 88-96, 1986.

    Google Scholar 

  54. Okamoto H., Nishizawa T., Takahashi M., Tawara A., Peng Y., Kishimoto J., and Wang Y., J Gen Virol 82, 2041-2050, 2001.

    Google Scholar 

  55. Okamoto H., Takahashi M., Nishizawa T., Tawara A., Fukai K., Muramatsu U., Naito Y., and Yoshikawa A., J Gen Virol 83, 1291-1297, 2002.

    Google Scholar 

  56. Altschul S.F., Gish W., Miller W., Myers E.W., and Lipman D.J., J Mol Biol 215, 403-410, 1990.

    Google Scholar 

  57. Higgins D.G., and Sharp P.M., Gene 73, 237-244, 1988.

    Google Scholar 

  58. Bucher P. and Bairoch A., in Altman R., Brutlag D., Karp P., Lathrop R., and Searls D. (eds), ISMB-94, Proceedings 2nd International Conference on Intelligent Systems for Molecular Biology. AAAIPress, Menlo Park, 1994, pp. 53-61.

    Google Scholar 

  59. Hofmann K., Bucher P., Falquet L., and Bairoch A., Nucleic Acids Res 27, 215-219, 1999.

    Google Scholar 

  60. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G., Nucleic Acids Res 25, 4876-4882, 1997.

    Google Scholar 

  61. Larsen F., Gundersen G., Lopez R., and Prydz H., Genomics 13, 1095-1107, 1992.

    Google Scholar 

  62. Heller H., Kämmer C., Wilgenbus P., and Doerfler W., Proc Natl Acad Sci USA 92, 5515-5519, 1995.

    Google Scholar 

  63. Baldo A.M. and McClure M.A., J Virol 73, 7710-7721, 1999.

    Google Scholar 

  64. Pyles R.B., Sawtell N.M., and Thompson R.L., J Virol 66, 6706-6713, 1992.

    Google Scholar 

  65. Turelli P., Guiguen F., Mornex J.F., Vigne R., and Querat G., J Virol 71, 4522-4530, 1997.

    Google Scholar 

  66. Weiss R.S., Lee S.S., Prasad B.V., and Javier R.T., J Virol 71, 1857-1870, 1997.

    Google Scholar 

  67. Mol C.D., Harris J.M., McIntosh E.M., and Tainer J.A., Structure 4, 1077-1092, 1996.

    Google Scholar 

  68. van Breukelen B., Brenkman A.B., Holthuizen P.E., and van der Vliet P.C., J Virol 77, 915-922, 2003.

    Google Scholar 

  69. Brough D.E., Droguett G., Horwitz M.S., and Klessig D.F., Virology 196, 269-281, 1993.

    Google Scholar 

  70. Harfst E. and Leppard K.N., Virus Genes 18, 97-106, 1999.

    Google Scholar 

  71. Jones N. and Shenk T., Proc Natl Acad Sci USA 76, 3665-3669, 1979.

    Google Scholar 

  72. Bayley S.T. and Mymryk J.S., Int J Oncol 5, 425-444, 1994.

    Google Scholar 

  73. Houweling A., van den Elsen P.J., and van der Eb A.J., Virology 105, 537-550, 1980.

    Google Scholar 

  74. Mymryk J.S., Oncogene 13, 1581-1589, 1996.

    Google Scholar 

  75. Stephens C. and Harlow E., EMBO J 6, 2027-2035, 1987.

    Google Scholar 

  76. Ulfendahl P.J., Linder S., Kreivi J.P., Nordqvist K., Sevensson C., Hultberg H., and Akusjarvi G., EMBO J 6, 2037-2044, 1987.

    Google Scholar 

  77. Kimelman D., Miller J.S., Porter D., and Roberts B.E., J Virol 53, 399-409, 1985.

    Google Scholar 

  78. van Ormondt H., Maat J., and Dijkema R., Gene 12, 63-76, 1980.

    Google Scholar 

  79. Avvakumov N., Wheeler R., D'Halluin J.C., and Mymryk J.S., J Virol 76, 7968-7975, 2002.

    Google Scholar 

  80. Culp J.S., Webster L.C., Friedman D.J., Smith C.L., Huang W.J., Wu F.Y., Rosenberg M., and Ricciardi R.P., Proc Natl Acad Sci USA 85, 6450-6454, 1988.

    Google Scholar 

  81. Webster L.C. and Ricciardi R.P., Mol Cell Biol 11, 4287-4296, 1991.

    Google Scholar 

  82. Whalen S.G., Marcellus R.C., Whalen A., Ahn N.G., Ricciardi R.P., and Branton P.E., J Virol 71, 3545-3553, 1997.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gholamreza Darai.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bahr, U., Schöndorf, E., Handermann, M. et al. Molecular Anatomy of Tupaia (Tree Shrew) adenovirus Genome; Evolution of Viral Genes and Viral Phylogeny. Virus Genes 27, 29–48 (2003). https://doi.org/10.1023/A:1025120418159

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1025120418159

Navigation