1887

Abstract

We have examined the host range in different insect cell lines of Autographa californica nucleopolyhedrovirus (AcMNPV) recombinants lacking p35, iap1 or iap2. These genes encode, or are predicted to encode, anti-apoptotic proteins. Abrogation of p35 reduced the ability of AcMNPV to replicate in permissive cell lines derived from Spodoptera frugiperda insects by inducing apoptosis. In semi-permissive cell lines, such as Lymantria dispar and Spodoptera littoralis cells, we observed cytopathic effects after infection with AcMNPV but little virus production. Infection of these cells by AcMNPV lacking p35 resulted in apoptosis. However, p35-deficient viruses were still able to replicate normally in Trichoplusia ni, Mamestra brassicae and Panolis flammea cell lines. Disruption of AcMNPV iap1 and iap2 was found not to affect virus replication in any of the cell lines. It was also possible to disrupt both iap1 and iap2 in the same virus without loss of infectivity. A virus without iap1 and p35 demonstrated identical growth characteristics and host range to a virus lacking p35. We conclude that in cells which respond to AcMNPV infection by initiating programmed cell death, the p35 gene product alone is sufficient to inhibit apoptosis. Removal of iap1 or iap2 has no effect on virus replication, even in cell lines which do not undergo apoptosis in response to AcMNPV infection. Our results with two semi-permissive cell lines further indicate that whilst p35 is important in blocking block apoptosis, other factors are involved in restricting AcMNPV replication within these cells.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-80-4-1055
1999-04-01
2022-08-11
Loading full text...

Full text loading...

/deliver/fulltext/jgv/80/4/0801055a.html?itemId=/content/journal/jgv/10.1099/0022-1317-80-4-1055&mimeType=html&fmt=ahah

References

  1. Ahrens C. H., Russell R. L. Q., Funk C. J., Evans J. T., Harwood S. H., Rohrmann G. F. 1997; The sequence of the Orgyia pseudotsugata multinucleocapsid nuclear polyhedrosis virus genome. Virology 229:381–399
    [Google Scholar]
  2. Ayres M. D., Howard S. C., Kuzio J., Lopez-Ferber M., Possee R. D. 1994; The complete DNA sequence of Autographa californica nuclear polyhedrosis virus. Virology 202:586–605
    [Google Scholar]
  3. Birnbaum M. J., Clem R. J., Miller L. K. 1994; An apoptosis-inhibiting gene from a nuclear polyhedrosis virus encoding a polypeptide with Cys/His sequence motifs. Journal of Virology 68:2521–2528
    [Google Scholar]
  4. Braunagel S. C., Daniel K. D., Reilly L. M., Guarino L. A., Hong T., Summers M. D. 1993; Sequence, genomic organisation of the Eco RI-A fragment of Autographa californica nuclear polyhedrosis virus, and identification of a viral-encoded protein resembling the outer capsid protein VP8 of rotavirus. Virology 191:1003–1008
    [Google Scholar]
  5. Chejanovsky N., Gershburg E. 1995; The wild-type Autographa californica nuclear polyhedrosis virus induces apoptosis of Spodoptera littoralis cells. Virology 209:519–525
    [Google Scholar]
  6. Clem R. J., Miller L. K. 1994a; Control of programmed cell death by the baculovirus genes p35 and iap . Molecular and Cellular Biology 14:5212–5222
    [Google Scholar]
  7. Clem R. J., Miller L. K. 1994b; Induction and inhibition of apoptosis by insect viruses. In Apoptosis: The Molecular Basis of Apoptosis in Disease 2nd edn pp 89–110 Edited by Tomei L. D., Cope F. O. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  8. Clem R. J., Fechheimer M., Miller L. K. 1991; Prevention of apoptosis by a baculovirus gene during infection of insect cells. Science 254:388–1390
    [Google Scholar]
  9. Clem R. J., Hardwick J. M., Miller L. K. 1996; Anti-apoptotic genes of baculoviruses. Cell Death and Differentiation 3:9–16
    [Google Scholar]
  10. Crook N. E., Clem R. J., Miller L. K. 1993; An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. Journal of Virology 67:2168–2174
    [Google Scholar]
  11. Du X., Thiem S. M. 1997; Responses of insect cells to baculovirus infection: protein synthesis shutdown and apoptosis. Journal of Virology 71:7866–7872
    [Google Scholar]
  12. Duckett C. S., Nava V. E., Gedrich R. W., Clem R. J., Van Dongen J. L., Gilfillan M. C., Shiels H., Hardwick J. M., Thompson C. B. 1996; A conserved family of cellular genes related to the baculovirus iap gene and encoding apoptosis inhibitors. EMBO Journal 15:2685–2694
    [Google Scholar]
  13. Freemont P. S., Hanson I. M., Trowsdale J. 1991; A novel cysteine-rich sequence motif. Cell 64:483–484
    [Google Scholar]
  14. Gombart A. F., Blissard G. W., Rohrmann G. F. 1989; Characterisation of the genetic organization of the Hind III M region of the multicapsid nuclear polyhedrosis virus of Orgyia pseudotsugata reveals major differences among baculoviruses. Journal of General Virology 70:1815–1828
    [Google Scholar]
  15. Goodwin R. H., Thompkins G. J., McCawley P. 1978; Gypsy moth cell lines divergent in viral susceptibility. In vitro 14:485–494
    [Google Scholar]
  16. Guzo D., Rathburn H., Guthrie K., Dougherty E. 1992; Viral and host cellular transcription in Autographa californica nuclear polyhedrosis virus-infected gypsy moth cell lines. Journal of Virology 66:2966–2972
    [Google Scholar]
  17. Hay B. A., Wassarman D. A., Rubin G. M. 1995; Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell 83:1253–1262
    [Google Scholar]
  18. Hink W. F. 1970; Established insect cell line from the cabbage looper, Trichoplusia ni . Nature 226:266–467
    [Google Scholar]
  19. Kamita S. G., Majima K., Maeda S. 1993; Identification and characterization of the p35 gene of Bombyx mori nuclear polyhedrosis virus that prevents virus-induced apoptosis. Journal of Virology 67:455–463
    [Google Scholar]
  20. King L. A., Possee R. D. 1992 The Baculovirus Expression System. A Laboratory Guide London: Chapman and Hall;
    [Google Scholar]
  21. King L. A., Mann S. G., Lawrie A. M., Mulshaw S. H. 1991; Replication of wild-type and recombinant Autographa californica nuclear polyhedrosis virus in a cell line derived from Mamestra brassicae . Virus Research 19:93–104
    [Google Scholar]
  22. Kitts P. A., Possee R. D. 1993; A method for producing recombinant baculovirus expression vectors at high frequency. Bio/ Techniques 14:810–817
    [Google Scholar]
  23. Liston P., Roy N., Tamai K., Lefebvre C., Baird S., Cherton-Horvat G., Farahani R., McLean M., Ikeda J.-E., MacKenzie A., Korneluk R. G. 1996; Suppression of apoptosis in mammalian cells by NAIP and a related family of IAP genes. Nature 379:349–353
    [Google Scholar]
  24. McClintock J. T., Dougherty E. M. 1987; Superinfection of baculovirus-infected gypsy moth cells with the nuclear polyhedrosis viruses of Autographa californica and Lymantria dispar . Virus Research 7:197–204
    [Google Scholar]
  25. McClintock J. T., Dougherty E. M., Weiner R. M. 1986; Semipermissive replication of a nuclear polyhedrosis virus of Autographa californica in a gypsy moth cell line. Journal of Virology 57:197–204
    [Google Scholar]
  26. Palli S. R., Caputo G. F., Sohi S. S., Brownwright A. J., Ladd T. R., Cook B. J., Primavera M., Arif B. M., Retnakaran A. 1996; Cf MNPV blocks Ac MNPV-induced apoptosis in a continuous midgut cell line. Virology 222:201–213
    [Google Scholar]
  27. Possee R. D. 1986; Cell-surface expression of influenza virus haemagglutinin in insect cells using a baculovirus vector. Virus Research 5:43–59
    [Google Scholar]
  28. Possee R. D., Howard S. C. 1987; Analysis of the polyhedrin gene promoter of the Autographa californica nuclear polyhedrosis virus. Nucleic Acids Research 15:10233–10248
    [Google Scholar]
  29. Rothe M., Pan M.-G., Henzel W. J., Ayres T. M., Goeddel D. V. 1995; The TNFR2-TRAF signalling complex contains two novel proteins related to baculoviral inhibitor of apoptosis proteins. Cell 83:1243–1252
    [Google Scholar]
  30. Roy N., Mahadevan M. S., McLean M., Shutler G., Yaraghi Z., Farahani R., Baird S., Besner-Johnson A., Lefebvre C., Kang X., Salih M., Aubry H., Tamai K., Guan X., Ioannou P., Crawford T. O., de Jong P. J., Surh L., Ikeda J., Korneluk R. G., MacKenzie A. 1995; The gene for neuronal apoptosis inhibitory protein is partially deleted in individuals with spinal muscular atrophy. Cell 80:167–178
    [Google Scholar]
  31. Sugimoto A., Friesen P. D., Rothman J. H. 1994; Baculovirus p35 prevents developmentally programmed cell death and rescues a ced-9 mutant in the nematode Caenorhabditis elegans . EMBO Journal 13:2023–2028
    [Google Scholar]
  32. Thiem S. M., Du X., Quentin M. E., Berner M. M. 1996; Identification of a baculovirus gene that promotes Autographa californica nuclear polyhedrosis virus replication in a nonpermissive insect cell line. Journal of Virology 70:2221–2229
    [Google Scholar]
  33. Vaughn J. L., Goodwin R. H., Thompkins G. J., McCawley P. 1977; The establishment of two cell lines from the insect Spodoptera frugiperda (Lepidoptera: Noctuidae). In Vitro 13213–217
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-80-4-1055
Loading
/content/journal/jgv/10.1099/0022-1317-80-4-1055
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

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