1887

Abstract

Recombinant fowl adenoviruses (FAdVs) have been successfully used as veterinary vaccine vectors. However, insufficient definitions of the protein-coding and non-coding regions and an incomplete understanding of virus–host interactions limit the progress of next-generation vectors. FAdVs are known to cause several diseases of poultry. Certain isolates of species FAdV-C are the aetiological agent of inclusion body hepatitis/hydropericardium syndrome (IBH/HPS). In this study, we report the complete 45667 bp genome sequence of FAdV-4 of species FAdV-C. Assessment of the protein-coding potential of FAdV-4 was carried out with the Bio-Dictionary-based Gene Finder together with an evaluation of sequence conservation among species FAdV-A and FAdV-D. On this basis, 46 potentially protein-coding ORFs were identified. Of these, 33 and 13 ORFs were assigned high and low protein-coding potential, respectively. Homologues of the ancestral adenoviral genes were, with few exceptions, assigned high protein-coding potential. ORFs that were unique to the FAdVs were differentiated into high and low protein-coding potential groups. Notable putative genes with high protein-coding capacity included the previously unreported fiber 1, hypothetical 10.3K and hypothetical 10.5K genes. Transcript analysis revealed that several of the small ORFs less than 300 nt in length that were assigned low coding potential contributed to upstream ORFs (uORFs) in important mRNAs, including the ORF22 mRNA. Subsequent analysis of the previously reported transcripts of FAdV-1, FAdV-9, human adenovirus 2 and bovine adenovirus 3 identified widespread uORFs in AdV mRNAs that have the potential to act as important translational regulatory elements.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.030064-0
2011-06-01
2024-10-06
Loading full text...

Full text loading...

/deliver/fulltext/jgv/92/6/1260.html?itemId=/content/journal/jgv/10.1099/vir.0.030064-0&mimeType=html&fmt=ahah

References

  1. Adair B., Fitzgerald S. 2008; Group I Adenovirus Infections. In Diseases of Poultry, 12th edn. pp. 252–266 Edited by Saif Y., Fadly A., Glisson J., McDougald L., Nolan L., Swayne D. Hoboken, NJ: Wiley-Blackwell;
    [Google Scholar]
  2. Alexander H. S., Huber P., Cao J., Krell P. J., Nagy E. 1998; Growth characteristics of fowl adenovirus type 8 in a chicken hepatoma cell line. J Virol Methods 74:9–14 [View Article][PubMed]
    [Google Scholar]
  3. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 [View Article][PubMed]
    [Google Scholar]
  4. Bangari D. S., Mittal S. K. 2006; Development of nonhuman adenoviruses as vaccine vectors. Vaccine 24:849–862 [View Article][PubMed]
    [Google Scholar]
  5. Barouch D. H. 2008; Challenges in the development of an HIV-1 vaccine. Nature 455:613–619 [View Article][PubMed]
    [Google Scholar]
  6. Benkö M., Harrach B., Both G., Russell W., Adair B., Ádam É., de Jong J., Hess M., Johnson M. et al. 2005; Family Adenoviridae . In Virus Taxonomy Eighth Report of the International Committee on the Taxonomy of Viruses pp. 213–228 Edited by Fauquet C., Mayo M., Maniloff J., Desselberger U., Ball L. San Diego, CA: Elsevier Academic Press;
    [Google Scholar]
  7. Benson G. 1999; Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580 [View Article][PubMed]
    [Google Scholar]
  8. Berk A. 2007; Adenoviridae: the viruses and their replication. In Fields Virology, 5th edn. pp. 2355–2394 Edited by Knipe D., Howley P., Griffin D., Lamb R., Martin M., Roizman B., Straus S. Philadelphia, PA: Lippincott Williams & Wilkins;
    [Google Scholar]
  9. Broker T. 1984; Animal Virus RNA Processing. In Processing of RNA pp. 181–212 Edited by Apirion D. Boca Raton, Florida: CRC Press;
    [Google Scholar]
  10. Brudno M., Do C. B., Cooper G. M., Kim M. F., Davydov E. NISC Comparative Sequencing Program Green E. D., Sidow A., Batzoglou S. 2003; lagan and Multi-lagan: efficient tools for large-scale multiple alignment of genomic DNA. Genome Res 13:721–731 [View Article][PubMed]
    [Google Scholar]
  11. Buchbinder S. P., Mehrotra D. V., Duerr A., Fitzgerald D. W., Mogg R., Li D., Gilbert P. B., Lama J. R., Marmor M., Delrio C. 2008; Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): a double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet 372:1881–1893 [View Article][PubMed]
    [Google Scholar]
  12. Calvo S. E., Pagliarini D. J., Mootha V. K. 2009; Upstream open reading frames cause widespread reduction of protein expression and are polymorphic among humans. Proc Natl Acad Sci U S A 106:7507–7512 [View Article][PubMed]
    [Google Scholar]
  13. Cao J. X., Krell P. J., Nagy E. 1998; Sequence and transcriptional analysis of terminal regions of the fowl adenovirus type 8 genome. J Gen Virol 79:2507–2516[PubMed]
    [Google Scholar]
  14. Chiocca S. 2007; Viral control of the SUMO pathway: Gam1, a model system. Biochem Soc Trans 35:1419–1421 [View Article][PubMed]
    [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[PubMed]
    [Google Scholar]
  16. Clamp M., Fry B., Kamal M., Xie X. H., Cuff J., Lin M. F., Kellis M., Lindblad-Toh K., Lander E. S. 2007; Distinguishing protein-coding and noncoding genes in the human genome. Proc Natl Acad Sci U S A 104:19428–19433 [View Article][PubMed]
    [Google Scholar]
  17. Cody J. J., Douglas J. T. 2009; Armed replicating adenoviruses for cancer virotherapy. Cancer Gene Ther 16:473–488 [View Article][PubMed]
    [Google Scholar]
  18. Corredor J. C., Nagy E. 2010; The non-essential left end region of the fowl adenovirus 9 genome is suitable for foreign gene insertion/replacement. Virus Res 149:167–174 [View Article][PubMed]
    [Google Scholar]
  19. Corredor J. C., Krell P. J., Nagy E. 2006; Sequence analysis of the left end of fowl adenovirus genomes. Virus Genes 33:95–106 [View Article][PubMed]
    [Google Scholar]
  20. Corredor J. C., Garceac A., Krell P. J., Nagy E. 2008; Sequence comparison of the right end of fowl adenovirus genomes. Virus Genes 36:331–344 [View Article][PubMed]
    [Google Scholar]
  21. Cuff J. A., Barton G. J. 2000; Application of multiple sequence alignment profiles to improve protein secondary structure prediction. Proteins 40:502–511 [View Article][PubMed]
    [Google Scholar]
  22. Cuff J. A., Clamp M. E., Siddiqui A. S., Finlay M., Barton G. J. 1998; JPred: a consensus secondary structure prediction server. Bioinformatics 14:892–893 [View Article][PubMed]
    [Google Scholar]
  23. Davison A. J., Benko M., Harrach B. 2003a). Genetic content and evolution of adenoviruses. J Gen Virol 84:2895–2908 [View Article][PubMed]
    [Google Scholar]
  24. Davison A. J., Dolan A., Akter P., Addison C., Dargan D. J., Alcendor D. J., McGeoch D. J., Hayward G. S. 2003b). The human cytomegalovirus genome revisited: comparison with the chimpanzee cytomegalovirus genome. J Gen Virol 84:17–28 [View Article][PubMed]
    [Google Scholar]
  25. El Bakkouri M., Seiradake E., Cusack S., Ruigrok R. W. H., Schoehn G. 2008; Structure of the C-terminal head domain of the fowl adenovirus type 1 short fibre. Virology 378:169–176 [View Article][PubMed]
    [Google Scholar]
  26. Favier A. L., Schoehn G., Jaquinod M., Harsi C., Chroboczek J. 2002; Structural studies of human enteric adenovirus type 41. Virology 293:75–85 [View Article][PubMed]
    [Google Scholar]
  27. Fernandez J., Yaman I., Huang C., Liu H. Y., Lopez A. B., Komar A. A., Caprara M. G., Merrick W. C., Snider M. D., Kaufman R. J. 2005; Ribosome stalling regulates IRES-mediated translation in eukaryotes, a parallel to prokaryotic attenuation. Mol Cell 17:405–416 [View Article][PubMed]
    [Google Scholar]
  28. Ferreira T. B., Alves P. M., Aunins J. G., Carrondo M. J. T. 2005; Use of adenoviral vectors as veterinary vaccines. Gene Ther 12:Suppl. 1S73–S83 [View Article][PubMed]
    [Google Scholar]
  29. François A., Eterradossi N., Delmas B., Payet V., Langlois P. 2001; Construction of avian adenovirus CELO recombinants in cosmids. J Virol 75:5288–5301 [View Article][PubMed]
    [Google Scholar]
  30. Francois A., Chevalier C., Delmas B., Eterradossi N., Toquin D., Rivallan G. H., Langlois P. 2004; Avian adenovirus CELO recombinants expressing VP2 of infectious bursal disease virus induce protection against bursal disease in chickens. Vaccine 22:2351–2360 [View Article][PubMed]
    [Google Scholar]
  31. Gallo P., Dharmapuri S., Cipriani B., Monaci P. 2005; Adenovirus as vehicle for anticancer genetic immunotherapy. Gene Ther 12:Suppl. 1S84–S91 [View Article][PubMed]
    [Google Scholar]
  32. Glotzer J. B., Saltik M., Chiocca S., Michou A. I., Moseley P., Cotten M. 2000; Activation of heat-shock response by an adenovirus is essential for virus replication. Nature 407:207–211 [View Article][PubMed]
    [Google Scholar]
  33. Guardado-Calvo P., Llamas-Saiz A. L., Fox G. C., Langlois P., van Raaij M. J. 2007; Structure of the C-terminal head domain of the fowl adenovirus type 1 long fiber. J Gen Virol 88:2407–2416 [View Article][PubMed]
    [Google Scholar]
  34. Holcik M., Sonenberg N. 2005; Translational control in stress and apoptosis. Nat Rev Mol Cell Biol 6:318–327 [View Article][PubMed]
    [Google Scholar]
  35. Huebner R. J., Rowe W. P., Schatten W. E., Smith R. R., Thomas L. B. 1956; Studies on the use of viruses in the treatment of carcinoma of the cervix. Cancer 9:1211–1218 [View Article][PubMed]
    [Google Scholar]
  36. Idamakanti N., Reddy P. S., Babiuk L. A., Tikoo S. K. 1999; Transcription mapping and characterization of 284R and 121R proteins produced from early region 3 of bovine adenovirus type 3. Virology 256:351–359 [View Article][PubMed]
    [Google Scholar]
  37. Jackson R. J., Hellen C. U. T., Pestova T. V. 2010; The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11:113–127 [View Article][PubMed]
    [Google Scholar]
  38. Johnson M. A., Pooley C., Ignjatovic J., Tyack S. G. 2003; A recombinant fowl adenovirus expressing the S1 gene of infectious bronchitis virus protects against challenge with infectious bronchitis virus. Vaccine 21:2730–2736 [View Article][PubMed]
    [Google Scholar]
  39. Kozak M. 1984; Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucleic Acids Res 12:857–872 [View Article][PubMed]
    [Google Scholar]
  40. Larkin M. A., Blackshields G., Brown N. P., Chenna R., McGettigan P. A., McWilliam H., Valentin F., Wallace I. M., Wilm A. et al. 2007; clustal w and clustal_x version 2.0. Bioinformatics 23:2947–2948 [View Article][PubMed]
    [Google Scholar]
  41. Lasaro M. O., Ertl H. C. J. 2009; New insights on adenovirus as vaccine vectors. Mol Ther 17:1333–1339 [View Article][PubMed]
    [Google Scholar]
  42. Lehrmann H., Cotten M. 1999; Characterization of CELO virus proteins that modulate the pRb/E2F pathway. J Virol 73:6517–6525[PubMed]
    [Google Scholar]
  43. McElrath M. J., De Rosa S. C., Moodie Z., Dubey S., Kierstead L., Janes H., Defawe O. D., Carter D. K., Hural J., Akondy R. 2008; HIV-1 vaccine-induced immunity in the test-of-concept Step Study: a case-cohort analysis. Lancet 372:1894–1905 [View Article][PubMed]
    [Google Scholar]
  44. Meijer H. A., Thomas A. A. M. 2002; Control of eukaryotic protein synthesis by upstream open reading frames in the 5′-untranslated region of an mRNA. Biochem J 367:1–11 [View Article][PubMed]
    [Google Scholar]
  45. Morley S. J., Coldwell M. J. 2008; A cunning stunt: an alternative mechanism of eukaryotic translation initiation. Sci Signal 1:pe32[PubMed]
    [Google Scholar]
  46. Morris D. R., Geballe A. P. 2000; Upstream open reading frames as regulators of mRNA translation. Mol Cell Biol 20:8635–8642 [View Article][PubMed]
    [Google Scholar]
  47. Murphy E., Rigoutsos I., Shibuya T., Shenk T. E. 2003; Reevaluation of human cytomegalovirus coding potential. Proc Natl Acad Sci U S A 100:13585–13590 [View Article][PubMed]
    [Google Scholar]
  48. Ojkic D., Nagy E. 2000; The complete nucleotide sequence of fowl adenovirus type 8. J Gen Virol 81:1833–1837[PubMed]
    [Google Scholar]
  49. Ojkic D., Nagy E. 2001; The long repeat region is dispensable for fowl adenovirus replication in vitro. Virology 283:197–206 [View Article][PubMed]
    [Google Scholar]
  50. Ojkic D., Nagy E. 2003; Antibody response and virus tissue distribution in chickens inoculated with wild-type and recombinant fowl adenoviruses. Vaccine 22:42–48 [View Article][PubMed]
    [Google Scholar]
  51. Ojkic D., Krell P. J., Nagy E. 2002; Unique features of fowl adenovirus 9 gene transcription. Virology 302:274–285 [View Article][PubMed]
    [Google Scholar]
  52. O’Shea C. C., Soria C., Bagus B., McCormick F. 2005; Heat shock phenocopies E1B-55K late functions and selectively sensitizes refractory tumor cells to ONYX-015 oncolytic viral therapy. Cancer Cell 8:61–74 [View Article][PubMed]
    [Google Scholar]
  53. Payet V., Arnauld C., Picault J. P., Jestin A., Langlois P. 1998; Transcriptional organization of the avian adenovirus CELO. J Virol 72:9278–9285[PubMed]
    [Google Scholar]
  54. Perricaudet M., Akusjärvi G., Virtanen A., Pettersson U. 1979; Structure of two spliced mRNAs from the transforming region of human subgroup C adenoviruses. Nature 281:694–696 [View Article][PubMed]
    [Google Scholar]
  55. Pooggin M. M., Hohn T., Fütterer J. 2000; Role of a short open reading frame in ribosome shunt on the cauliflower mosaic virus RNA leader. J Biol Chem 275:17288–17296 [View Article][PubMed]
    [Google Scholar]
  56. Qiao H., Lu N., Du E., Yao L., Xiao H., Lu S., Qi Y. 2011; Rare codons in uORFs of baculovirus p13 gene modulates downstream gene expression. Virus Res 155:249–253[PubMed] [CrossRef]
    [Google Scholar]
  57. Reddy P. S., Idamakanti N., Zakhartchouk A. N., Baxi M. K., Lee J. B., Pyne C., Babiuk L. A., Tikoo S. K. 1998; Nucleotide sequence, genome organization, and transcription map of bovine adenovirus type 3. J Virol 72:1394–1402[PubMed]
    [Google Scholar]
  58. Reddy P. S., Chen Y., Idamakanti N., Pyne C., Babiuk L. A., Tikoo S. K. 1999; Characterization of early region 1 and pIX of bovine adenovirus-3. Virology 253:299–308 [View Article][PubMed]
    [Google Scholar]
  59. Rigoutsos I., Novotny J., Huynh T., Chin-Bow S. T., Parida L., Platt D., Coleman D., Shenk T. 2003; In silico pattern-based analysis of the human cytomegalovirus genome. J Virol 77:4326–4344 [View Article][PubMed]
    [Google Scholar]
  60. Roelvink P. W., Lizonova A., Lee J. G. M., Li Y., Bergelson J. M., Finberg R. W., Brough D. E., Kovesdi I., Wickham T. J. 1998; The coxsackievirus-adenovirus receptor protein can function as a cellular attachment protein for adenovirus serotypes from subgroups A, C, D, E, and F. J Virol 72:7909–7915[PubMed]
    [Google Scholar]
  61. Schepetilnikov M., Schott G., Katsarou K., Thiébeauld O., Keller M., Ryabova L. A. 2009; Molecular dissection of the prototype foamy virus (PFV) RNA 5′-UTR identifies essential elements of a ribosomal shunt. Nucleic Acids Res 37:5838–5847 [View Article][PubMed]
    [Google Scholar]
  62. Sharma A., Tandon M., Ahi Y. S., Bangari D. S., Vemulapalli R., Mittal S. K. 2010; Evaluation of cross-reactive cell-mediated immune responses among human, bovine and porcine adenoviruses. Gene Ther 17:634–642 [CrossRef]
    [Google Scholar]
  63. Shashkova E. V., Cherenova L. V., Kazansky D. B., Doronin K. 2005; Avian adenovirus vector CELO-TK displays anticancer activity in human cancer cells and suppresses established murine melanoma tumors. Cancer Gene Ther 12:617–626 [View Article][PubMed]
    [Google Scholar]
  64. Sheppard M., Werner W., Tsatas E., McCoy R., Prowse S., Johnson M. 1998; Fowl adenovirus recombinant expressing VP2 of infectious bursal disease virus induces protective immunity against bursal disease. Arch Virol 143:915–930 [View Article][PubMed]
    [Google Scholar]
  65. Shibuya T., Rigoutsos I. 2002; Dictionary-driven prokaryotic gene finding. Nucleic Acids Res 30:2710–2725 [View Article][PubMed]
    [Google Scholar]
  66. Silke J. 1997; The majority of long non-stop reading frames on the antisense strand can be explained by biased codon usage. Gene 194:143–155 [View Article][PubMed]
    [Google Scholar]
  67. Sira S., Abouhaidar M. G., Liu Y. C., Campbell J. B. 1987; Multiple reiteration of a 40-bp nucleotide sequence in the inverted terminal repeat of the genome of a canine adenovirus. Virology 159:76–83 [View Article][PubMed]
    [Google Scholar]
  68. Tamura K., Dudley J., Nei M., Kumar S. 2007; mega4: Molecular Evolutionary Genetics Analysis (mega) software version 4.0. Mol Biol Evol 24:1596–1599 [View Article][PubMed]
    [Google Scholar]
  69. Tan P. K., Michou A. I., Bergelson J. M., Cotten M. 2001; Defining CAR as a cellular receptor for the avian adenovirus CELO using a genetic analysis of the two viral fibre proteins. J Gen Virol 82:1465–1472[PubMed]
    [Google Scholar]
  70. Virtanen A., Gilardi P., Näslund A., LeMoullec J. M., Pettersson U., Perricaudet M. 1984; mRNAs from human adenovirus 2 early region 4. J Virol 51:822–831[PubMed]
    [Google Scholar]
  71. Washietl S., Eisenhaber F. 2003; Reannotation of the CELO genome characterizes a set of previously unassigned open reading frames and points to novel modes of host interaction in avian adenoviruses. BMC Bioinformatics 4:55 [View Article][PubMed]
    [Google Scholar]
  72. Weiss R. S., Lee S. S., Prasad B. V. 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[PubMed]
    [Google Scholar]
  73. Wilson-Rawls J., Saha S. K., Krajcsi P., Tollefson A. E., Gooding L. R., Wold W. S. M. 1990; A 6700 MW membrane protein is encoded by region E3 of adenovirus type 2. Virology 178:204–212 [View Article][PubMed]
    [Google Scholar]
  74. Wold W. S. M., 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[PubMed]
    [Google Scholar]
  75. Xia X., Xie Z. 2001; dambe: software package for data analysis in molecular biology and evolution. J Hered 92:371–373 [View Article][PubMed]
    [Google Scholar]
  76. Yamamoto M., Curiel D. T. 2010; Current issues and future directions of oncolytic adenoviruses. Mol Ther 18:243–250 [View Article][PubMed]
    [Google Scholar]
  77. Yueh A., Schneider R. J. 1996; Selective translation initiation by ribosome jumping in adenovirus-infected and heat-shocked cells. Genes Dev 10:1557–1567 [View Article][PubMed]
    [Google Scholar]
  78. Zhao C., Datta S., Mandal P., Xu S., Hamilton T. 2010; Stress-sensitive regulation of IFRD1 mRNA decay is mediated by an upstream open reading frame. J Biol Chem 285:8552–8562 [View Article][PubMed]
    [Google Scholar]
  79. Zheng B. J., Graham F. L., Prevec L. 1999; Transcription units of E1a, E1b and pIX regions of bovine adenovirus type 3. J Gen Virol 80:1735–1742[PubMed]
    [Google Scholar]
/content/journal/jgv/10.1099/vir.0.030064-0
Loading
/content/journal/jgv/10.1099/vir.0.030064-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

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