1887

Abstract

In this study, four inhibitor of apoptosis genes () in the genome of nucleopolyhedrovirus (EppoMNPV) that are homologous to , , and genes of other baculoviruses have been identified. All four genes were sequenced and the and genes were shown to be functional inhibitors of apoptosis. The , and genes contain two baculovirus apoptosis inhibitor repeat motifs and a CHC RING finger-like motif. The activity of the genes was tested by transient expression in (Sf-21) cells treated with the apoptosis-inducing agents actinomycin D, cycloheximide, anisomycin, tumour necrosis factor-α and UV light. The gene prevented apoptosis induced by all agents tested, indicating activity towards a conserved component(s) of multiple apoptotic pathways. However, the gene was unable to function in the absence of a gene immediately upstream of that has homology to the gene of MNPV. The use of a CMV promoter rescued the apoptosis inhibition activity of the gene, indicating that the upstream homologue is associated with expression of . The gene was able to delay the onset of apoptosis caused by all of the induction agents tested but, unlike , was unable to prevent the development of an apoptotic response upon prolonged exposure of cells to the apoptosis induction agents. No anti-apoptotic activity was observed for the and genes of EppoMNPV.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-81-11-2803
2000-11-01
2020-01-22
Loading full text...

Full text loading...

/deliver/fulltext/jgv/81/11/0812803a.html?itemId=/content/journal/jgv/10.1099/0022-1317-81-11-2803&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.[CrossRef]
    [Google Scholar]
  2. Altschul, S. F., Madden, T. L., Schaffer, 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 Research 25, 3389-3402.[CrossRef]
    [Google Scholar]
  3. Barr, P. J. & Tomei, L. D. ( 1994; ). Apoptosis and its role in human disease. Bio/technology 12, 487-493.[CrossRef]
    [Google Scholar]
  4. 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]
  5. Bump, N. J., Hackett, M., Hugunin, M., Seshagiri, S., Brady, K., Chen, P., Ferenz, C. S., Franklin, C., Ghayur, T., Li, P., Licari, P., Mankovich, J., Shi, L., Greenberg, A. H., Miller, L. K. & Wong, W. W. ( 1995; ). Inhibition of ICE family proteases by baculovirus antiapoptotic protein P35. Science 269, 1885-1888.[CrossRef]
    [Google Scholar]
  6. Cartier, J. L., Hershberger, P. A. & Friesen, P. D. ( 1994; ). Suppression of apoptosis in insect cells stably transfected with baculovirus p35: dominant interference by N-terminal sequences p35 1–76. Journal of Virology 68, 7728-7737.
    [Google Scholar]
  7. Clem, R. J. & Miller, L. K. ( 1994; ). Control of programmed cell death by the baculovirus genes p35 and iap. Molecular and Cellular Biology 14, 5212-5222.
    [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, 1388-1390.[CrossRef]
    [Google Scholar]
  9. 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]
  10. Deveraux, Q. L., Takahashi, R., Salvesen, G. S. & Reed, J. C. ( 1997; ). X-linked IAP is a direct inhibitor of cell-death proteases. Nature 388, 300-304.[CrossRef]
    [Google Scholar]
  11. Du, Q., Lehavi, D., Faktor, O., Qi, Y. & Chejanovsky, N. ( 1999; ). Isolation of an apoptosis suppressor gene of the Spodoptera littoralis nucleopolyhedrovirus. Journal of Virology 73, 1278-1285.
    [Google Scholar]
  12. Duckett, C. S., Li, F., Wang, Y., Tomaselli, K. J., Thompson, C. B. & Armstrong, R. C. ( 1998; ). Human IAP-like protein regulates programmed cell death downstream of Bcl-xL and cytochrome c. Molecular and Cellular Biology 18, 608-615.
    [Google Scholar]
  13. Felsenstein, J. (1995). PHYLIP (Phylogeny Inference Package), version 3.5c. Distributed by the author. Department of Genetics, University of Washington, USA.
  14. Green, D. & Kroemer, G. ( 1998; ). The central executioners of apoptosis: caspases or mitochondria? Trends in Cell Biology 8, 267-271.[CrossRef]
    [Google Scholar]
  15. Hawkins, C. J., Uren, A. G., Hacker, G., Medcalf, R. L. & Vaux, D. L. ( 1996; ). Inhibition of interleukin 1β-converting enzyme-mediated apoptosis of mammalian cells by baculovirus IAP. Proceedings of the National Academy of Sciences, USA 93, 13786-13790.[CrossRef]
    [Google Scholar]
  16. Hay, B. A., Wasserman, D. A. & Rubin, G. M. ( 1995; ). Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell 83, 1253-1262.[CrossRef]
    [Google Scholar]
  17. Higgins, D. G. & Sharp, P. M. ( 1988; ). CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene 73, 237-244.[CrossRef]
    [Google Scholar]
  18. Hu, Z. H., Arif, B. M., Jin, F., Martens, J. W. M., Chen, X. W., Sun, J. S., Zuidema, D., Goldbach, R. W. & Vlak, J. M. ( 1998; ). Distinct gene arrangement in the Buzura suppressaria single-nucleocapsid nucleopolyhedrovirus genome. Journal of General Virology 79, 2841-2851.
    [Google Scholar]
  19. Huang, Q., Deveraux, Q. L., Maeda, S., Slavesan, G. S., Stennicke, H. R., Hammock, B. D. & Reed, J. C. ( 2000; ). Evolutionary conservation of apoptosis mechanisms: lepidopteran and baculoviral inhibitor of apoptosis proteins are inhibitors of mammalian caspase-9. Proceedings of the National Academy of Sciences, USA 97, 1427-1432.[CrossRef]
    [Google Scholar]
  20. Hyink, O., Graves, S., Fairbairn, F. M. & Ward, V. K. ( 1998; ). Mapping and polyhedrin gene analysis of the Epiphyas postvittana nucleopolyhedrovirus genome. Journal of General Virology 79, 2853-2862.
    [Google Scholar]
  21. Jiang, C., Baehrecke, E. H. & Thummel, C. S. ( 1997; ). Steroid regulated programmed cell death during Drosophila metamorphosis. Development 124, 4673-4683.
    [Google Scholar]
  22. Kamita, S. G., Majima, K. & Maeda, S. ( 1993; ). Identification and characterisation of the p35 gene of Bombyx mori nuclear polyhedrosis virus that prevents virus-induced apoptosis. Journal of Virology 67, 455-463.
    [Google Scholar]
  23. Li, P., Nijhawan, D., Budihardjo, I., Srinivasula, S. M., Ahmad, M., Alnemri, E. S. & Wang, X. ( 1997; ). Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91, 479-489.[CrossRef]
    [Google Scholar]
  24. Li, L., Harwood, S. H. & Rohrmann, G. F. ( 1999; ). Identification of additional genes that influence baculovirus late gene expression. Virology 255, 9-19.[CrossRef]
    [Google Scholar]
  25. Liston, P., Roy, N., Tamal, 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.[CrossRef]
    [Google Scholar]
  26. Liu, X., Kim, C. N., Yang, J., Jemmerson, R. & Wang, X. ( 1996; ). Induction of apoptotic program in cell free extracts: requirement for dATP and cytochrome c. Cell 86, 147-157.[CrossRef]
    [Google Scholar]
  27. Manji, G. A., Hozak, R. R., LaCount, D. J. & Friesen, P. D. ( 1997; ). Baculovirus inhibitor of apoptosis functions at or upstream of the apoptotic suppressor P35 to prevent programmed cell death. Journal of Virology 71, 4509-4516.
    [Google Scholar]
  28. Miller, L. K. ( 1997; ). Baculovirus interaction with host apoptotic pathways. Journal of Cellular Physiology 173, 178-182.[CrossRef]
    [Google Scholar]
  29. O’Brien, V. ( 1998; ). Viruses and apoptosis. Journal of General Virology 79, 1833-1845.
    [Google Scholar]
  30. Palli, S. R., Sohi, S. S., Cook, B. J., Brownwright, A. J., Caputo, G. F. & Retnakaran, A. ( 1996; ). RNA- and protein-synthesis inhibitors induce apoptosis in a midgut cell line from the spruce budworm Choristoneura fumiferana. Journal of Insect Physiology 42, 1061-1069.[CrossRef]
    [Google Scholar]
  31. 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.[CrossRef]
    [Google Scholar]
  32. Roy, N., Deveraux, Q. L., Takahashi, R., Salvesen, G. S. & Reed, J. C. ( 1997; ). The c-IAP-1 and c-IAP-2 proteins are direct inhibitors of specific caspases. EMBO Journal 16, 6914-6925.[CrossRef]
    [Google Scholar]
  33. Seshagiri, S. & Miller, L. K. ( 1997; ). Baculovirus inhibitors of apoptosis (IAPs) block activation of Sf-caspase-1. Proceedings of the National Academy of Sciences, USA 94, 13606-13611.[CrossRef]
    [Google Scholar]
  34. Seshagiri, S., Vucic, D., Lee, J. & Dixit, V. M. ( 1999; ). Baculovirus-based genetic screen for antiapoptotic genes identifies a novel IAP. Journal of Biological Chemistry 274, 36769-36773.[CrossRef]
    [Google Scholar]
  35. Steller, H. & Grether, M. E. ( 1994; ). Programmed cell death in Drosophila. Neuron 13, 1269-1274.[CrossRef]
    [Google Scholar]
  36. Thompson, C. B. ( 1995; ). Apoptosis in the pathogenesis and treatment of disease. Science 267, 1456-1462.[CrossRef]
    [Google Scholar]
  37. Tschopp, J., Thome, M., Hofmann, K. & Meinl, E. ( 1998; ). The fight of viruses against apoptosis. Current Opinion in Genetics & Development 8, 82-87.[CrossRef]
    [Google Scholar]
  38. Ucker, D. S. ( 1991; ). Death by suicide: one way to go in mammalian cellular development? New Biology 3, 103-109.
    [Google Scholar]
  39. Uren, A. G., Pakusch, M., Hawkins, C. J., Puls, C. J. & Vaux, D. L. ( 1996; ). Cloning and expression of apoptosis inhibitory protein homologs that function to inhibit apoptosis and/or bind tumor necrosis factor receptor-associated factors. Proceedings of the National Academy of Sciences, USA 93, 4974-4978.[CrossRef]
    [Google Scholar]
  40. Vaughn, J. L., Goodwin, R. H., Tompkins, G. J. & McCawley, P. ( 1977; ). The establishment of two cell lines from the insect Spodoptera frugiperda (Lepidoptera: Noctuidae). In Vitro 13, 213-217.[CrossRef]
    [Google Scholar]
  41. White, R. J. & Phillips, D. R. ( 1988; ). Transcriptional analysis of multisite drug–DNA dissociation kinetics: delayed termination of transcription by actinomycin D. Biochemistry 27, 9122-9132.[CrossRef]
    [Google Scholar]
  42. You, M. & Bose, H. R. J. ( 1998; ). Identification of v-Rel oncogene-induced inhibitor of apoptosis by differential display. Methods 16, 373-385.[CrossRef]
    [Google Scholar]
  43. Zandomeni, R., Bunick, D., Ackerman, S., Mittleman, B. & Weinmann, R. ( 1983; ). Mechanism of action of DRB. III. Effect on specific in vitro initiation of transcription. Journal of Molecular Biology 167, 561-574.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-81-11-2803
Loading
/content/journal/jgv/10.1099/0022-1317-81-11-2803
Loading

Data & Media loading...

Most cited articles

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