1887

Abstract

Activation of the innate immune response represents one of the most important cellular mechanisms to limit virus replication and spread in cell culture. Here, we examined the effect of adenoviral gene expression on the antiviral response in adenovirus-transformed cell lines; HEK293, HEK293SF and AGE1.HN. We demonstrate that the expression of the early region protein 1A in these cell lines impairs their ability to activate antiviral genes by the IFN pathway. This property may help in the isolation of newly emerging viruses and the propagation of interferon-sensitive virus strains.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000361
2016-02-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/jgv/97/2/293.html?itemId=/content/journal/jgv/10.1099/jgv.0.000361&mimeType=html&fmt=ahah

References

  1. Ackrill A. M., Foster G. R., Laxton C. D., Flavell D. M., Stark G. R., Kerr I. M. 1991; Inhibition of the cellular response to interferons by products of the adenovirus type 5 E1A oncogene. Nucleic Acids Res 19:4387–4393 [View Article][PubMed]
    [Google Scholar]
  2. Anderson K. P., Fennie E. H. 1987; Adenovirus early region 1A modulation of interferon antiviral activity. J Virol 61:787–795[PubMed]
    [Google Scholar]
  3. Barrett P. N., Mundt W., Kistner O., Howard M. K. 2009; Vero cell platform in vaccine production: moving towards cell culture-based viral vaccines. Expert Rev Vaccines 8:607–618 [View Article][PubMed]
    [Google Scholar]
  4. Basu M., Maitra R. K., Xiang Y., Meng X., Banerjee A. K., Bose S. 2006; Inhibition of vesicular stomatitis virus infection in epithelial cells by alpha interferon-induced soluble secreted proteins. J Gen Virol 87:2653–2662 [View Article][PubMed]
    [Google Scholar]
  5. Côté J., Garnier A., Massie B., Kamen A. 1998; Serum-free production of recombinant proteins and adenoviral vectors by 293SF-3F6 cells. Biotechnol Bioeng 59:567–575 [View Article][PubMed]
    [Google Scholar]
  6. Dumont J., Euwart D., Mei B., Estes S., Kshirsagar R. 2015; Human cell lines for biopharmaceutical manufacturing: history, status, and future perspectives. Crit Rev Biotechnol 18:1–13 [View Article][PubMed]
    [Google Scholar]
  7. Emeny J. M., Morgan M. J. 1979; Regulation of the interferon system: evidence that Vero cells have a genetic defect in interferon production. J Gen Virol 43:247–252 [View Article][PubMed]
    [Google Scholar]
  8. Endter C., Dobner T. 2004; Cell transformation by human adenoviruses. Curr Top Microbiol Immunol 273:163–214[PubMed]
    [Google Scholar]
  9. García-Sastre A. 2011; Induction and evasion of type I interferon responses by influenza viruses. Virus Res 162:12–18 [View Article][PubMed]
    [Google Scholar]
  10. García-Sastre A., Egorov A., Matassov D., Brandt S., Levy D. E., Durbin J. E., Palese P., Muster T. 1998; Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 252:324–330 [View Article][PubMed]
    [Google Scholar]
  11. Genzel Y., Reichl U. 2009; Continuous cell lines as a production system for influenza vaccines. Expert Rev Vaccines 8:1681–1692 [View Article][PubMed]
    [Google Scholar]
  12. Genzel Y., Behrendt I., Rodig J., Rapp E., Kueppers C., Kochanek S., Schiedner G., Reichl U. 2013; CAP, a new human suspension cell line for influenza virus production. Appl Microbiol Biotechnol 97:111–122[PubMed] [CrossRef]
    [Google Scholar]
  13. Giard D. J., Aaronson S. A., Todaro G. J., Arnstein P., Kersey J. H., Dosik H., Parks W. P. 1973; In vitro cultivation of human tumors: establishment of cell lines derived from a series of solid tumors. J Natl Cancer Inst 51:1417–1423[PubMed]
    [Google Scholar]
  14. Graham F. L., Smiley J., Russell W. C., Nairn R. 1977; Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J Gen Virol 36:59–74 [View Article][PubMed]
    [Google Scholar]
  15. Gutch M. J., Reich N. C. 1991; Repression of the interferon signal transduction pathway by the adenovirus E1A oncogene. Proc Natl Acad Sci U S A 88:7913–7917 [View Article][PubMed]
    [Google Scholar]
  16. Haller O., Staeheli P., Kochs G. 2009; Protective role of interferon-induced Mx GTPases against influenza viruses. Rev Sci Tech 28:219–231[PubMed]
    [Google Scholar]
  17. Jordan I., Horn D., Oehmke S., Leendertz F. H., Sandig V. 2009a; Cell lines from the Egyptian fruit bat are permissive for modified vaccinia Ankara. Virus Res 145:54–62 [View Article][PubMed]
    [Google Scholar]
  18. Jordan I., Vos A., Beilfuss S., Neubert A., Breul S., Sandig V. 2009b; An avian cell line designed for production of highly attenuated viruses. Vaccine 27:748–756 [View Article][PubMed]
    [Google Scholar]
  19. Kalbfuss B., Knöchlein A., Kröber T., Reichl U. 2008; Monitoring influenza virus content in vaccine production: precise assays for the quantitation of hemagglutination and neuraminidase activity. Biologicals 36:145–161 [View Article][PubMed]
    [Google Scholar]
  20. Koudstaal W., Hartgroves L., Havenga M., Legastelois I., Ophorst C., Sieuwerts M., Zuijdgeest D., Vogels R., Custers J., other authors. 2009; Suitability of PER.C6 cells to generate epidemic and pandemic influenza vaccine strains by reverse genetics. Vaccine 27:2588–2593 [View Article][PubMed]
    [Google Scholar]
  21. Lieber M., Smith B., Szakal A., Nelson-Rees W., Todaro G. 1976; A continuous tumor-cell line from a human lung carcinoma with properties of type II alveolar epithelial cells. Int J Cancer 17:62–70 [View Article][PubMed]
    [Google Scholar]
  22. Lohr V., Rath A., Genzel Y., Jordan I., Sandig V., Reichl U. 2009; New avian suspension cell lines provide production of influenza virus and MVA in serum-free media: studies on growth, metabolism and virus propagation. Vaccine 27:4975–4982 [View Article][PubMed]
    [Google Scholar]
  23. Lohr V., Genzel Y., Jordan I., Katinger D., Mahr S., Sandig V., Reichl U. 2012; Live attenuated influenza viruses produced in a suspension process with avian AGE1.CR.pIX cells. BMC Biotechnol 12:79 [View Article][PubMed]
    [Google Scholar]
  24. McSharry B. P., Forbes S. K., Avdic S., Randall R. E., Wilkinson G. W., Abendroth A., Slobedman B. 2015; Abrogation of the interferon response promotes more efficient human cytomegalovirus replication. J Virol 89:1479–1483 [View Article][PubMed]
    [Google Scholar]
  25. Mössler C., Groiss F., Wolzt M., Wolschek M., Seipelt J., Muster T. 2013; Phase I/II trial of a replication-deficient trivalent influenza virus vaccine lacking NS1. Vaccine 31:6194–6200 [View Article][PubMed]
    [Google Scholar]
  26. Niklas J., Schräder E., Sandig V., Noll T., Heinzle E. 2011; Quantitative characterization of metabolism and metabolic shifts during growth of the new human cell line AGE1.HN using time resolved metabolic flux analysis. Bioprocess Biosyst Eng 34:533–545 [View Article][PubMed]
    [Google Scholar]
  27. Pau M. G., Ophorst C., Koldijk M. H., Schouten G., Mehtali M., Uytdehaag F. 2001; The human cell line PER.C6 provides a new manufacturing system for the production of influenza vaccines. Vaccine 19:2716–2721 [View Article][PubMed]
    [Google Scholar]
  28. Reich N., Pine R., Levy D., Darnell J. E. Jr 1988; Transcription of interferon-stimulated genes is induced by adenovirus particles but is suppressed by E1A gene products. J Virol 62:114–119[PubMed]
    [Google Scholar]
  29. Richt J. A., García-Sastre A. 2009; Attenuated influenza virus vaccines with modified NS1 proteins. Curr Top Microbiol Immunol 333:177–195[PubMed]
    [Google Scholar]
  30. Samina I., Havenga M., Koudstaal W., Khinich Y., Koldijk M., Malkinson M., Simanov M., Perl S., Gijsbers L., other authors. 2007; Safety and efficacy in geese of a PER.C6-based inactivated West Nile virus vaccine. Vaccine 25:8338–8345 [View Article][PubMed]
    [Google Scholar]
  31. Sanders B. P., Oakes I. L., van Hoek V., Liu Y., Marissen W., Minor P. D., Wimmer E., Schuitemaker H., Custers J. H., other authors. 2015; Production of high titer attenuated poliovirus strains on the serum-free PER.C6(®) cell culture platform for the generation of safe and affordable next generation IPV. Vaccine 33:6611–6616 [View Article][PubMed]
    [Google Scholar]
  32. Schiedner G., Hertel S., Kochanek S. 2000; Efficient transformation of primary human amniocytes by E1 functions of Ad5: generation of new cell lines for adenoviral vector production. Hum Gene Ther 11:2105–2116 [View Article][PubMed]
    [Google Scholar]
  33. Schwarzer J., Rapp E., Hennig R., Genzel Y., Jordan I., Sandig V., Reichl U. 2009; Glycan analysis in cell culture-based influenza vaccine production: influence of host cell line and virus strain on the glycosylation pattern of viral hemagglutinin. Vaccine 27:4325–4336 [View Article][PubMed]
    [Google Scholar]
  34. Seitz C., Frensing T., Höper D., Kochs G., Reichl U. 2010; High yields of influenza A virus in Madin-Darby canine kidney cells are promoted by an insufficient interferon-induced antiviral state. J Gen Virol 91:1754–1763 [View Article][PubMed]
    [Google Scholar]
  35. Stewart C. E., Randall R. E., Adamson C. S. 2014; Inhibitors of the interferon response enhance virus replication in vitro. PLoS One 9:e112014 [View Article][PubMed]
    [Google Scholar]
  36. Subramanian S., Kim J. J., Harding F., Altaras G. M., Aunins J. G., Zhou W. 2007; Scaleable production of adenoviral vectors by transfection of adherent PER.C6 cells. Biotechnol Prog 23:1210–1217[PubMed]
    [Google Scholar]
  37. van Wielink R., Harmsen M. M., Martens D. E., Peeters B. P., Wijffels R. H., Moormann R. J. 2011; MDCK cell line with inducible allele B NS1 expression propagates delNS1 influenza virus to high titres. Vaccine 29:6976–6985 [View Article][PubMed]
    [Google Scholar]
  38. Wang L., Suarez D. L., Pantin-Jackwood M., Mibayashi M., García-Sastre A., Saif Y. M., Lee C. W. 2008; Characterization of influenza virus variants with different sizes of the non-structural (NS) genes and their potential as a live influenza vaccine in poultry. Vaccine 26:3580–3586 [View Article][PubMed]
    [Google Scholar]
  39. Wressnigg N., Voss D., Wolff T., Romanova J., Ruthsatz T., Mayerhofer I., Reiter M., Nakowitsch S., Humer J., other authors. 2009; Development of a live-attenuated influenza B deltaNS1 intranasal vaccine candidate. Vaccine 27:2851–2857 [View Article][PubMed]
    [Google Scholar]
  40. Young D. F., Andrejeva L., Livingstone A., Goodbourn S., Lamb R. A., Collins P. L., Elliott R. M., Randall R. E. 2003; Virus replication in engineered human cells that do not respond to interferons. J Virol 77:2174–2181 [View Article][PubMed]
    [Google Scholar]
  41. Zhu Z., Yang Y., Wei J., Shao D., Shi Z., Li B., Liu K., Qiu Y., Zheng H., Ma Z. 2014; Type I interferon-mediated immune response against influenza A virus is attenuated in the absence of p53. Biochem Biophys Res Commun 454:189–195 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000361
Loading
/content/journal/jgv/10.1099/jgv.0.000361
Loading

Data & Media loading...

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