1887

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Volume 85, Issue 3

DNA sequencing and analysis of the right-hand part of the genome of the unique bovine adenovirus type 10 Free

Abstract

The prototype strain of bovine adenovirus (BAdV) type 10 and four additional isolates that were indistinguishable in serum-neutralization tests have been shown to have remarkable variation in their genome size and restriction maps. In the present study, more than 40 % of the DNA sequence of the BAdV-10 isolate with the longest genome was determined. A biased base composition resulting in low (<41 %) GC content was noticed. Analysis of the genes of the DNA-binding protein, 100K, 33K, pVIII and fibre proteins, as well as early regions E3 and E4, which are encoded by the genome fragment examined, confirmed that BAdV-10 is different from the other known BAdV types regarding its phylogenetic distance and the organization of its exceptionally short E3 region, apparently containing only two genes. A comparative analysis of the E3 and E4 regions of BAdV-10 with various animal adenoviruses revealed interesting features accounting for the very short genome of BAdV-10. In the examined BAdV-10 isolate, duplicated sequences were localized in and around the fibre gene. Since BAdV-10 appears to be pathogenic to cattle and is genetically distant from the other BAdVs, we suggest that BAdV-10 is not a genuine bovine virus, but has recently switched host and is now undergoing an adaptation process in its new host. In accordance with this hypothesis, the remarkable predominance of AT-rich codons along with the variable fibre gene might be signs of adaptation.

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2004-03-01
2024-04-23
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References

  1. Adair B. M., McKillop E. R., Smyth J. A., Curran W. L., McNulty M. S. 1996; Bovine adenovirus type 10: properties of viruses isolated from cases of bovine haemorrhagic enterocolitis. Vet Rec 138:250–252
     [Google Scholar]
  2. Ambriovic-Ristov A., Mercier S., Eloit M. 2003; Shortening adenovirus type 5 fiber shaft decreases the efficiency of postbinding steps in CAR-expressing and nonexpressing cells. Virology 312:425–433
     [Google Scholar]
  3. Arnberg N., Kidd A. H., Edlund K., Nilsson J., Pring-Akerblom P., Wadell G. 2002; Adenovirus type 37 binds to cell surface sialic acid through a charge-dependent interaction. Virology 302:33–43
     [Google Scholar]
  4. Barbezange C., Benkő M., Dán Á., Harrach B. 2000; DNA sequencing and phylogenetic analysis of the protease gene of ovine adenovirus 3 suggest that adenoviruses of sheep belong to two different genera. Virus Res 66:79–85
     [Google Scholar]
  5. Bartha A. 1969; Proposal for subgrouping of bovine adenoviruses. Acta Vet Hung 19:319–321
     [Google Scholar]
  6. Benkő M. 2000; Comparison of the genome of ovine adenovirus types 1 through 5 by restriction enzyme analysis and DNA hybridisation. Acta Vet Hung 48:477–484
     [Google Scholar]
  7. Benkő M., Harrach B. 1998; A proposal for establishing a new (third) genus within the Adenoviridae family. Arch Virol 143:829–837
     [Google Scholar]
  8. Benkő M., Harrach B. 2003; Molecular evolution of adenoviruses. Curr Top Microbiol Immunol 272:3–35
     [Google Scholar]
  9. Benkő M., Bartha A., Wadell G. 1988; DNA restriction enzyme analysis of bovine adenoviruses. Intervirology 29:346–350
     [Google Scholar]
  10. Benkő M., Smyth J. A., Adair B. M., Harrach B. 1995; Genome typing of adenovirus isolates from fatal enterocolitis cases of cattle for the elaboration of a rapid diagnostic method. In Immunobiology of Viral Infections . Proceedings of the 3rd Congress of the European Society of Veterinary Virologists . pp  484–488 Edited by Schwyzer M., Ackermann M., Bertoni G., Kocherhans R., McCullough K., Engels M., Wittek R., Zanoni R. Zurich: European Society for Veterinary Virology;
  11. Benkő M., Harrach B., Russell W. C. 2000; Family Adenoviridae . In Virus Taxonomy . Seventh Report of the International Committee on Taxonomy of Viruses . pp  227–238 Edited by van Regenmortel M. H. V., Fauquet C. M., Bishop D. H. L., Carstens E. B., Estes M. K., Lemon S. M., Maniloff J., Mayo M. A., McGeoch D. J., Pringle C. R., Wickner R. B. San Diego: Academic Press;
  12. Benkő M., Élő P., Ursu K., Ahne W., LaPatra E. S., Thomson D., Harrach B. 2002; First molecular evidence for the existence of distinct fish and snake adenoviruses. J Virol 76:10056–10059
     [Google Scholar]
  13. Both G. W. 2002a; Atadenovirus . In The Springer Index of Viruses . pp  2–8 Edited by Tidona C. A., Darai G. Berlin: Springer;
  14. Both G. W. 2002b; Identification of a unique family of F-box proteins in atadenoviruses. Virology 20:425–433
     [Google Scholar]
  15. Chiocca S., Kurzbauer R., Schaffner G., Baker A., Mautner V., Cotten M. 1996; The complete DNA sequence and genomic organization of the avian adenovirus CELO. J Virol 70:2939–2949
     [Google Scholar]
  16. Chiocca S., Kurtev V., Colombo R., Boggio R., Sciurpi M. T., Brosch G., Seiser C., Draetta G. F., Cotten M. 2002; Histone deacetylase 1 inactivation by an adenovirus early gene product. Curr Biol 2:12594–12598
     [Google Scholar]
  17. Davison A. J., Telford E. A., Watson M. S., McBride K., Mautner V. 1993; The DNA sequence of adenovirus type 40. J Mol Biol 234:1308–1316
     [Google Scholar]
  18. Davison A. J., Wright K. M., Harrach B. 2000; DNA sequence of frog adenovirus. J Gen Virol 81:2431–2439
     [Google Scholar]
  19. Davison A. J., Akter P., Cunningham C. & 7 other authors (2003a). Homology between the human cytomegalovirus RL11 gene family and human adenovirus E3 genes. J Gen Virol 84:657–663
     [Google Scholar]
  20. Davison A. J., Benkő M., Harrach B. 2003b; Genetic content and evolution of adenoviruses. J Gen Virol 84:2895–2908
     [Google Scholar]
  21. Élő P. 2002; Comparative genome analysis of an atadenovirus isolate . PhD thesis University of Szeged; Szeged: (in Hungarian
  22. Élő P., Farkas L. S., Dán Á., Kovács G. 2003; The p32K structural protein of the atadenovirus might have bacterial relatives. J Mol Evol 56:175–180
     [Google Scholar]
  23. Farkas L. S., Benkő M., Élő P., Ursu K., Dán Á., Ahne W., Harrach B. 2002; Genomic and phylogenetic analyses of an adenovirus isolated from a corn snake ( Elaphe guttata ) imply common origin with the members of the proposed new genus Atadenovirus . J Gen Virol 83:2403–2410
     [Google Scholar]
  24. Ginsberg H. S., Prince G. A. 1994; The molecular basis of adenovirus pathogenesis. Infect Agents Dis 3:1–8
     [Google Scholar]
  25. Ginsberg H. S., Lundholm-Beauchamp U., Horswood R. L., Pernis B., Wold W. S., Chanock R. M., Prince G. A. 1989; Role of early region 3 (E3) in pathogenesis of adenovirus disease. Proc Natl Acad Sci U S A 86:3823–3827
     [Google Scholar]
  26. Gish W., States D. J. 1993; Identification of protein coding regions by database similarity search. Nat Genet 3:266–272
     [Google Scholar]
  27. Graham F. L., Prevec L. 1992; Adenovirus-based expression vectors and recombinant vaccines. Biotechnology 20:363–390
     [Google Scholar]
  28. Horner G. W., Hunter H., Thompson J. E. 1980; Isolation and characterisation of a new adenovirus serotype from a yearling heifer with systemic infection. N Z Vet J 28:165–167
     [Google Scholar]
  29. Horner G. W., Hunter R., Bartha A., Benkő M. 1989; A new subgroup 2 bovine adenovirus proposed as the prototype strain 10. Arch Virol 109:121–124
     [Google Scholar]
  30. Lehmkuhl H. D., Briggs R. E., Cutlip R. C. 1998; Survey for antibodies to bovine adenoviruses in six- to nine-month-old feedyard cattle. Am J Vet Res 59:1579–1580
     [Google Scholar]
  31. Lehmkuhl H. D., Cutlip R. C., DeBey B. M. 1999; Isolation of a bovine adenovirus serotype 10 from a calf in the United States. J Vet Diagn Invest 11:485–490
     [Google Scholar]
  32. Lehrmann H., Cotten M. 1999; Characterization of CELO virus proteins that modulate the pRb/E2F pathway. J Virol 73:6517–6525
     [Google Scholar]
  33. Mahr J. A., Gooding L. R. 1999; Immune evasion by adenoviruses. Immunol Rev 168:121–130
     [Google Scholar]
  34. Marschang R. E., Michling R., Benkő M., Papp T., Harrach B., Böhm R. 2003; Evidence for wide-spread atadenovirus infection among snakes. In Virus Persistence and Evolution . Proceedings of the 6th International Congress of Veterinary Virology p– 152 Edited by Jestin A., Clement G. Ploufragan: ZOOPOLE développement – ISPAIA;
     [Google Scholar]
  35. Matiz K., Benkő M., Zádori Z., Harrach B. 1996; Restriction site mapping of a bovine adenovirus type 10 strain. Acta Vet Hung 44:389–394
     [Google Scholar]
  36. Matiz K., Ursu K., Harrach B., Zádori Z., Benkő M. 1998; Sequencing and phylogenetic analysis of the protease gene, and genetic mapping of bovine adenovirus type 10 define its relatedness to other bovine adenoviruses. Virus Res 55:29–35
     [Google Scholar]
  37. Mayo M. A. 2002; ICTV at the Paris ICV: results of the plenary session and the binomial ballot. Arch Virol 147:2254–2260
     [Google Scholar]
  38. Meissner J. D., Hirsch G. N., LaRue E. A., Fulcher R. A., Spindler K. R. 1997; Completion of the DNA sequence of mouse adenovirus type 1: sequence of E2B, L1, and L2 (18–51 map units). Virus Res 51:53–64
     [Google Scholar]
  39. Michou A. I., Lehrmann H., Saltik M., Cotten M. 1999; Mutational analysis of the avian adenovirus CELO, which provides a basis for gene delivery vectors. J Virol 73:1399–1410
     [Google Scholar]
  40. Ojkic D., Krell P. J., Nagy E. 2002; Unique features of fowl adenovirus 9 gene transcription. Virology 302:274–285
     [Google Scholar]
  41. Pallister J., Wright P., Sheppard M. 1996; A single gene encoding the fiber is responsible for variations in virulence in the fowl adenoviruses. J Virol 70:5115–5122
     [Google Scholar]
  42. Raviprakash K. S., Grunhaus A., El Kholy M. A., Horwitz M. S. 1989; The mouse adenovirus type 1 contains an unusual E3 region. J Virol 63:5455–5458
     [Google Scholar]
  43. Ruigrok R. W. H., Barge A., Mittal S. K., Jacrot B. 1994; The fibre of bovine adenovirus type 3 is very long but bent. J Gen Virol 75:2069–2073
     [Google Scholar]
  44. Russell W. C. 2000; Update on adenovirus and its vectors. J Gen Virol 81:2573–2604
     [Google Scholar]
  45. Rusvai M., Harrach B., Bánrévi A., Evans P. S., Benkő M. 2000; Identification and sequence analysis of the core protein genes of bovine adenovirus 2. Virus Res 70:25–30
     [Google Scholar]
  46. Segerman A., Atkinson J. P., Marttila M., Dennerquist V., Wadell G., Arnberg N. 2003; Adenovirus type 11 uses CD46 as a cellular receptor. J Virol 77:9183–9191
     [Google Scholar]
  47. Shayakhmetov D. M., Lieber A. 2000; Dependence of adenovirus infectivity on length of the fiber shaft domain. J Virol 74:10274–10286
     [Google Scholar]
  48. Shenk T. E. 2001; Adenoviridae : the viruses and their replication. In Fields Virology , 4th edn. vol 2 pp  2265–2300 Edited by Knipe D. M., Howley P. M. Philadelphia: Lippincott Williams & Wilkins;
     [Google Scholar]
  49. Smyth J. A., Cush P. F., Adair B. M., Young J. A. 1986; Adenovirus associated enterocolitis in a bullock. Vet Rec 119:574–576
     [Google Scholar]
  50. Smyth J. A., Benkő M., Moffett D. A., Harrach B. 1996; Bovine adenovirus type 10 identified in fatal cases of adenovirus-associated enteric disease in cattle by in situ hybridization. J Clin Microbiol 34:1270–1274
     [Google Scholar]
  51. Smyth J. A., Moffett D. A., van Garderen E., Orr J. P. 1999; Examination of adenovirus-types in intestinal vascular endothelial inclusions in fatal cases of enteric disease in cattle, by in situ hybridisation. Vet Microbiol 70:1–6
     [Google Scholar]
  52. Sparer T. E., Tripp R. A., Dillehay D. L., Hermiston T. W., Wold W. S., Gooding L. R. 1996; The role of human adenovirus early region 3 proteins (gp19K, 10·4K, 14·5K, and 14·7K) in a murine pneumonia model. J Virol 70:2431–2439
     [Google Scholar]
  53. van Raaij M. J., Mitraki A., Lavigne G., Cusack S. 1999; A triple β -spiral in the adenovirus fibre shaft reveals a new structural motif for a fibrous protein. Nature 401:935–938
     [Google Scholar]
  54. Vrati S., Boyle D., Kocherhans R., Both G. W. 1995; Sequence of ovine adenovirus homologs for 100K hexon assembly, 33K, pVIII, and fiber genes: early region E3 is not in the expected location. Virology 209:400–408
     [Google Scholar]
  55. Vrati S., Brookes D. E., Strike P., Khatri A., Boyle D. B., Both G. W. 1996a; Unique genome arrangement of an ovine adenovirus: identification of new proteins and proteinase cleavage sites. Virology 220:186–199
     [Google Scholar]
  56. Vrati S., Macavoy E. S., Xu Z. Z., Smole C., Boyle D. B., Both G. W. 1996b; Construction and transfection of ovine adenovirus genomic clones to rescue modified viruses. Virology 220:200–203
     [Google Scholar]
  57. Weiss R. S., Lee S. S., Prasad B. V., Javier R. T. 1997; Human adenovirus early region 4 open reading frame 1 genes encode growth-transforming proteins that may be distantly related to dUTP pyrophosphatase enzymes. J Virol 71:1857–1870
     [Google Scholar]
  58. Wellehan J. F. X., Johnson A. J., Jacobson E. R., Tucker S. J., Johnson C. M., Harrach B., Benkő M. 2003; Nested PCR amplification and sequencing of reptile adenoviruses, including a novel gecko adenovirus associated with enteritis. In Annual Conference of the Association of Reptile and Amphibian Veterinarians 4–9 October, 2003 Minneapolis, Minnesota, USA:
     [Google Scholar]
  59. Wick N., Luedemann S., Vietor I., Cotten M., Wildpaner M., Schneider G., Eisenhaber F., Huber L. A. 2003; Induction of short interspersed nuclear repeat-containing transcripts in epithelial cells upon infection with a chicken adenovirus. J Mol Biol 328:779–790
     [Google Scholar]
  60. Wold W. S., Gooding L. R. 1991; Region E3 of adenovirus: a cassette of genes involved in host immunosurveillance and virus–cell interactions. Virology 184:1–8
     [Google Scholar]
  61. Wold W. S., Cladaras C., Magie S. C., Yacoub N. 1984; Mapping a new gene that encodes an 11,600-molecular-weight protein in the E3 transcription unit of adenovirus 2. J Virol 52:307–313
     [Google Scholar]
  62. Zakharchuk A. N., Kruglyak V. A., Akopian T. A., Naroditsky B. S., Tikchonenko T. I. 1993; Physical mapping and homology studies of egg drop syndrome (EDS-76) adenovirus DNA. Arch Virol 128:171–176
     [Google Scholar]
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DNA sequencing and analysis of the right-hand part of the genome of the unique bovine adenovirus type 10
J. Gen. Virol. 85, 593 (2004); https://doi.org/10.1099/vir.0.19697-0
/content/journal/jgv/10.1099/vir.0.19697-0
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