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.
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Rowe W.P., Huebner R.J., Gilmore L.K., Parrot R.H., Ward T.G., Proc Soc Exp Biol Med 84, 570-573, 1953.
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.
Barnett B.G., Crews C.J., and Douglas J.T., Biochim Biophys Acta 1575, 1-14, 2002.
Legrand V., Leissner P., Winter A., Mehtali M., and Lusky M., Curr Gene Ther 2, 323-239, 2002.
Mitani K. and Kubo S., Curr Gene Ther 2, 135-144, 2002.
Benkö M. and Harrach B., Arch Virol 43, 829-837, 1998.
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.
Davison A.J., Wright K.M., and Harrach B., J Gen Virol 81, 2431-2439, 2000.
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.
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.
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.
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.
Chiocca S., Kurzbauer R., Schaffner G., Baker A., Mautner V., and Cotten M., J Virol 70, 2939-2949, 1996.
Chroboczek J., Bieber F., and Jacrot B., Virology 186, 280-285, 1992.
Davison A.J., Telford E.A.R., Watson M.S., McBride K., and Mautner V., J Mol Biol 234, 1308-1316, 1993.
Hess M., Blocker H., and Brandt P., Virology 238, 145-156, 1997.
Khatri A. and Both G.W., Virology 245, 128-141, 1998.
Meissner J.D., Hirsch G.N., LaRue E.A., Fulcher R.A., and Spindler K.R., Virus Res 51, 53-64, 1997.
Morrison M.D., Onions D.E., and Nicolson L., J Gen Virol 78, 873-878, 1997.
Nagy M., Nagy E., and Tuboly T., J Gen Viro 82, 525-529, 2001.
Ojkic D. and Nagy E., J Gen Virol 81, 1833-1837, 2000.
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.
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.
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.
Roberts R.J., O'Neill K.E., and Yen C.T., J Biol Chem 259, 13968-13975, 1984.
Schöndorf E., Bahr U., Handermann M., and Darai G., J Virol 77, 4345-4356, 2003.
Sprengel J., Schmitz B., Heuss-Neitzel D., and Doerfler W., Curr Top Microbiol Immunol 199, 189-274, 1995.
Vrati S., Brookes D.E., Strike P., Khatri A., Boyle D.B., and Both G.W., Virology 220, 186-199, 1996.
Brinckmann U., Darai G., and Flügel R.M., EMBO J 2, 2185-2188, 1983a.
Brinckmann U., Darai G., and Flügel R.M., Gene 24, 131-135, 1983b.
Darai G., Matz B., Flügel R.M., Grafe A., Gelderblom H., and Delius H., Virology 104, 122-138, 1980.
Faissner A., Darai G., and Flügel R.M., Intervirology 14, 272-276, 1980.
Flügel R.M., Bannert H., Suhai S., and Darai G., Gene 34, 73-80, 1985.
Matz B., Delius H., Flügel R.M., and Darai G., J Gen Virol 51, 421-423, 1980.
Song B., Hu S.L., Darai G., Spindler K.R., and Young C.S., Virology 220, 390-401, 1996.
Van Kampen M., De Kloet E.R., Flugge G., and Fuchs E., Eur J Pharmacol 457, 207-216, 2002.
Bartolomucci A., de Biurrun G., Czeh B., van Kampen M., and Fuchs E., Eur Neurosci 15, 1863-1866, 2002.
Meyer U., van Kampen M., Isovich E., Flugge G., and Fuchs E., Hippocampus 11, 329-336, 2001.
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.
Fuchs E. and Flugge G., Z Psychosom Med Psychother 47, 80-97, 2001.
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.
Fuchs E., Flugge G., Ohl F., Lucassen P., Vollmann-Honsdorf G.K., and Michaelis T., Physiol Behav 73, 285-291, 2001.
Bosking W.H., Crowley J.C., and Fitzpatrick D., Nat Neurosci 5, 874-882, 2002.
Suss M., Washausen S., Kuhn H.J., and Knabe W., J Neurosci Methods 113, 147-158, 2002.
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.
Kock J., Nassal M., MacNelly S., Baumert T.F., Blum H.E., and von Weizsacker F., J Virol 75, 5084-5089, 2001.
Park U.S., Su J.J., Ban K.C., Qin L., Lee E.H., and Lee Y.I., Gene 251, 73-80, 2000.
Nishihara H., Terai Y., and Okada N., Mol Biol Evol 119, 1964-1972, 2002.
Flugge P., Fuchs E., Gunther E., and Walter L., Immunogenetics 53, 984-988, 2002.
Schmitz J., Ohme M., and Zischler H., Mol Biol Evol 17, 1334-1343, 2000.
Bahr U. and Darai G., J Virol 75, 4854-4870, 2001.
Tidona C.A., Kurz H.W., Gelderblom H.R., and Darai G., Virology 258, 425-434, 1999.
Kurz W., Gelderblom H., Flügel R.M., and Darai G., Intervirology 25, 88-96, 1986.
Okamoto H., Nishizawa T., Takahashi M., Tawara A., Peng Y., Kishimoto J., and Wang Y., J Gen Virol 82, 2041-2050, 2001.
Okamoto H., Takahashi M., Nishizawa T., Tawara A., Fukai K., Muramatsu U., Naito Y., and Yoshikawa A., J Gen Virol 83, 1291-1297, 2002.
Altschul S.F., Gish W., Miller W., Myers E.W., and Lipman D.J., J Mol Biol 215, 403-410, 1990.
Higgins D.G., and Sharp P.M., Gene 73, 237-244, 1988.
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.
Hofmann K., Bucher P., Falquet L., and Bairoch A., Nucleic Acids Res 27, 215-219, 1999.
Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G., Nucleic Acids Res 25, 4876-4882, 1997.
Larsen F., Gundersen G., Lopez R., and Prydz H., Genomics 13, 1095-1107, 1992.
Heller H., Kämmer C., Wilgenbus P., and Doerfler W., Proc Natl Acad Sci USA 92, 5515-5519, 1995.
Baldo A.M. and McClure M.A., J Virol 73, 7710-7721, 1999.
Pyles R.B., Sawtell N.M., and Thompson R.L., J Virol 66, 6706-6713, 1992.
Turelli P., Guiguen F., Mornex J.F., Vigne R., and Querat G., J Virol 71, 4522-4530, 1997.
Weiss R.S., Lee S.S., Prasad B.V., and Javier R.T., J Virol 71, 1857-1870, 1997.
Mol C.D., Harris J.M., McIntosh E.M., and Tainer J.A., Structure 4, 1077-1092, 1996.
van Breukelen B., Brenkman A.B., Holthuizen P.E., and van der Vliet P.C., J Virol 77, 915-922, 2003.
Brough D.E., Droguett G., Horwitz M.S., and Klessig D.F., Virology 196, 269-281, 1993.
Harfst E. and Leppard K.N., Virus Genes 18, 97-106, 1999.
Jones N. and Shenk T., Proc Natl Acad Sci USA 76, 3665-3669, 1979.
Bayley S.T. and Mymryk J.S., Int J Oncol 5, 425-444, 1994.
Houweling A., van den Elsen P.J., and van der Eb A.J., Virology 105, 537-550, 1980.
Mymryk J.S., Oncogene 13, 1581-1589, 1996.
Stephens C. and Harlow E., EMBO J 6, 2027-2035, 1987.
Ulfendahl P.J., Linder S., Kreivi J.P., Nordqvist K., Sevensson C., Hultberg H., and Akusjarvi G., EMBO J 6, 2037-2044, 1987.
Kimelman D., Miller J.S., Porter D., and Roberts B.E., J Virol 53, 399-409, 1985.
van Ormondt H., Maat J., and Dijkema R., Gene 12, 63-76, 1980.
Avvakumov N., Wheeler R., D'Halluin J.C., and Mymryk J.S., J Virol 76, 7968-7975, 2002.
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.
Webster L.C. and Ricciardi R.P., Mol Cell Biol 11, 4287-4296, 1991.
Whalen S.G., Marcellus R.C., Whalen A., Ahn N.G., Ricciardi R.P., and Branton P.E., J Virol 71, 3545-3553, 1997.
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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
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DOI: https://doi.org/10.1023/A:1025120418159