1887

Abstract

Members of the genus including bovine adenovirus 3 (BAdV-3) encode a genus-specific unique protein named pV. The pV encoded by BAdV-3 is a protein of 423 aa showing 40.9 % identity to pV of human adenovirus 2. Here, we report the construction and analysis of recombinant BAdV-3 (BAV.dV) containing deletion of pV. The BAV.dV could only be isolated in CRL.pV cells expressing pV, suggesting that pV appears essential for the infection of BAdV-3. Analysis of BAV.dV suggested that despite affecting some late gene expression in virus-infected cells, there was no significant difference in the incorporation of viral proteins in the mature virions. Moreover, analysis of mature virions revealed degraded capsids leading to change in morphology and infectivity of BAV.dV. Furthermore, analysis of the genome sequence of different clones of BAV.dV passaged in different cell lines revealed no mutations in core proteins pVII and pX\Mu suggesting that the replication defect may not be rescued. Our results suggest that pV is required for proper viral assembly of BAdV-3 as lack of pV produces aberrant capsids. Moreover, altered capsids lead to the production of non-infectious BAV.dV virions.

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2016-10-13
2024-12-02
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References

  1. Anand S. K., Gaba A., Singh J., Tikoo S. K. 2014; Bovine adenovirus 3 core protein precursor pVII localizes to mitochondria, and modulates ATP synthesis, mitochondrial Ca2+ and mitochondrial membrane potential. J Gen Virol 95:442–452 [View Article][PubMed]
    [Google Scholar]
  2. Anderson C. W., Baum P. R., Gesteland R. F. 1973; Processing of adenovirus 2-induced proteins. J Virol 12:241–252[PubMed]
    [Google Scholar]
  3. Ayalew L. E., Gaba A., Kumar P., Tikoo S. K. 2014; Conserved regions of bovine adenovirus-3 pVIII contain functional domains involved in nuclear localization and packaging in mature infectious virions. J Gen Virol 95:1743–1754 [View Article][PubMed]
    [Google Scholar]
  4. Benkó M., Elo P., Ursu K., Ahne W., LaPatra S. E., Thomson D., Harrach B. 2002; First molecular evidence for the existence of distinct fish and snake adenoviruses. J Virol 76:10056–10059 [View Article][PubMed]
    [Google Scholar]
  5. Chatterjee P. K., Vayda M. E., Flint S. J. 1985; Interactions among the three adenovirus core proteins. J Virol 55:379–386[PubMed]
    [Google Scholar]
  6. 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]
  7. Du E., Tikoo S. K. 2010; Efficient replication and generation of recombinant bovine adenovirus-3 in nonbovine cotton rat lung cells expressing I-SceI endonuclease. J Gene Med 12:840–847 [View Article][PubMed]
    [Google Scholar]
  8. Davison A. J., Wright K. M., Harrach B. 2000; DNA sequence of frog adenovirus. J Gen Virol 81:2431–2439 [View Article][PubMed]
    [Google Scholar]
  9. Davison A. J., Benko M., Harrach B. 2003; Genetic content and evolution of adenoviruses. J Gen Virol 84:2895–2908 [View Article][PubMed]
    [Google Scholar]
  10. Farina S. F., Gao G. P., Xiang Z. Q., Rux J. J., Burnett R. M., Alvira M. R., Marsh J., Ertl H. C., Wilson J. M. 2001; Replication-defective vector based on a chimpanzee adenovirus. J Virol 75:11603–11613 [View Article][PubMed]
    [Google Scholar]
  11. Horne R. W., Brenner S., Waterson A. P., Wildy P. 1959; The icosahedral form of an adenovirus. J Mol Biol 1:84-IN15 [View Article]
    [Google Scholar]
  12. Kovács G. M., LaPatra S. E., D'Halluin J. C., Benko M. 2003; Phylogenetic analysis of the hexon and protease genes of a fish adenovirus isolated from white sturgeon (Acipenser transmontanus) supports the proposal for a new adenovirus genus. Virus Res 98:27–34 [View Article][PubMed]
    [Google Scholar]
  13. Kulshreshtha V., Babiuk L. A., Tikoo S. K. 2004; Role of bovine adenovirus-3 33K protein in viral replication. Virology 323:59–69 [View Article][PubMed]
    [Google Scholar]
  14. Kulshreshtha V., Ayalew L. E., Islam A., Tikoo S. K. 2014; Conserved arginines of bovine adenovirus-3 33K protein are important for transportin-3 mediated transport and virus replication. PLoS One 9:e101216 [View Article][PubMed]
    [Google Scholar]
  15. Kulshreshtha V., Islam A., Ayalew L. E., Tikoo S. K. 2015; Leucine residues in conserved region of 33K protein of bovine adenovirus-3 are important for binding to major late promoter and activation of late gene expression. Virology 483:174–184 [View Article][PubMed]
    [Google Scholar]
  16. Le L. P., Le H. N., Nelson A. R., Matthews D. A., Yamamoto M., Curiel D. T. 2006; Core labeling of adenovirus with EGFP. Virology 351:291–302 [View Article][PubMed]
    [Google Scholar]
  17. Lehmberg E., Traina J. A., Chakel J. A., Chang R. J., Parkman M., McCaman M. T., Murakami P. K., Lahidji V., Nelson J. W. et al. 1999; Reversed-phase high-performance liquid chromatographic assay for the adenovirus type 5 proteome. J Chromatogr B Biomed Sci Appl 732:411–423 [View Article][PubMed]
    [Google Scholar]
  18. Leong K., Lee W., Berk A. J. 1990; High-level transcription from the adenovirus major late promoter requires downstream binding sites for late-phase-specific factors. J Virol 64:51–60[PubMed]
    [Google Scholar]
  19. Li X., Bangari D. S., Sharma A., Mittal S. K. 2009; Bovine adenovirus serotype 3 utilizes sialic acid as a cellular receptor for virus entry. Virology 392:162–168 [View Article][PubMed]
    [Google Scholar]
  20. Mangel W. F., San Martín C. 2014; Structure, function and dynamics in adenovirus maturation. Viruses 6:4536–4570 [View Article][PubMed]
    [Google Scholar]
  21. Matthews D. A., Russell W. C. 1998; Adenovirus core protein V interacts with p32 – a protein which is associated with both the mitochondria and the nucleus. J Gen Virol 79:1677–1685 [View Article][PubMed]
    [Google Scholar]
  22. Makadiya N., Gaba A., Tikoo S. K. 2015; Cleavage of bovine adenovirus type 3 non-structural 100K protein by protease is required for nuclear localization in infected cells but is not essential for virus replication. J Gen Virol 96:2749–2763 [View Article][PubMed]
    [Google Scholar]
  23. Paterson C. P. 2010 Molecular Characterization of 52k Protein of Bovine Adenovirus Type 3 PhD Thesis University of Saskatchewan, Saskatoon;
    [Google Scholar]
  24. Papp Z., Middleton D. M., Mittal S. K., Babiuk L. A., Baca-Estrada M. E. 1997; Mucosal immunization with recombinant adenoviruses: induction of immunity and protection of cotton rats against respiratory bovine herpesvirus type 1 infection. J Gen Virol 78:2933–2943 [View Article][PubMed]
    [Google Scholar]
  25. Paterson C. P., Ayalew L. E., Tikoo S. K. 2012; Mapping of nuclear import signal and importin α3 binding regions of 52K protein of bovine adenovirus-3. Virology 432:63–72 [View Article][PubMed]
    [Google Scholar]
  26. Puntener D., Engelke M. F., Ruzsics Z., Strunze S., Wilhelm C., Greber U. F. 2011; Stepwise loss of fluorescent core protein V from human adenovirus during entry into cells. J Virol 85:481–496 [View Article][PubMed]
    [Google Scholar]
  27. Pérez-Vargas J., Vaughan R. C., Houser C., Hastie K. M., Kao C. C., Nemerow G. R. 2014; Isolation and characterization of the DNA and protein binding activities of adenovirus core protein V. J Virol 88:9287–9296 [View Article][PubMed]
    [Google Scholar]
  28. Reddy V. S., Nemerow G. R. 2014; Structures and organization of adenovirus cement proteins provide insights into the role of capsid maturation in virus entry and infection. Proc Natl Acad Sci U S A 111:11715–11720 [View Article][PubMed]
    [Google Scholar]
  29. 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]
  30. Taylor L. A., Rose R. E. 1988; A correction in the nucleotide sequence of the Tn903 kanamycin resistance determinant in pUC4K. Nucleic Acids Res 16:7762 [View Article]
    [Google Scholar]
  31. Thanbichler M., Iniesta A. A., Shapiro L. 2007; A comprehensive set of plasmids for vanillate- and xylose-inducible gene expression in Caulobacter crescentus . Nucleic Acids Res 35:e137 [View Article][PubMed]
    [Google Scholar]
  32. Thompson K. G., Thomson G. W., Henry J. N. 1981; Alimentary tract manifestations of bovine adenovirus infections. Can Vet J 22:68–71[PubMed]
    [Google Scholar]
  33. Tollefson A. E., Hermiston T. W., Wold W. S. M. 1999; Preparation and titration of CsCl-banded adenovirus stock. In Adenovirus Methods & Protocols , pp. 1–9 Edited by Wold W. S. M. Totowa, NJ: Springer New York;
    [Google Scholar]
  34. Ugai H., Borovjagin A. V., Le L. P., Wang M., Curiel D. T. 2007; Thermostability/infectivity defect caused by deletion of the core protein V gene in human adenovirus type 5 is rescued by thermo-selectable mutations in the core protein X precursor. J Mol Biol 366:1142–1160 [View Article][PubMed]
    [Google Scholar]
  35. Ugai H., Dobbins G. C., Wang M., Le L. P., Matthews D. A., Curiel D. T. 2012; Adenoviral protein V promotes a process of viral assembly through nucleophosmin 1. Virology 432:283–295 [View Article][PubMed]
    [Google Scholar]
  36. Vayda M. E., Rogers A. E., Flint S. J. 1983; The structure of nucleoprotein cores released from adenovirions. Nucleic Acids Res 11:441–460 [View Article][PubMed]
    [Google Scholar]
  37. Wu Q., Tikoo S. K. 2004; Altered tropism of recombinant bovine adenovirus type-3 expressing chimeric fiber. Virus Res 99:9–15 [View Article][PubMed]
    [Google Scholar]
  38. Zhou Y., Reddy P. S., Babiuk L. A., Tikoo S. K. 2001; Bovine adenovirus type 3 E1B(small) protein is essential for growth in bovine fibroblast cells. Virology 288:264–274 [View Article][PubMed]
    [Google Scholar]
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