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Volume 76, Issue 2

polydnavirus induces apoptosis of a specific haemocyte morphotype in Free

Abstract

polydnavirus (MdPDV) is associated with , a parasitic wasp that attacks the larval stage of the lepidopteran . Previously, we observed that MdPDV induced several alterations in the granular cells and plasmatocytes of , the primary haemocytes involved in regulating the cellular immune response toward and other parasites. In examining the mechanisms underlying immunosuppression of this host, we found that MdPDV induced apoptosis of granular cells. Granular cells underwent apoptosis both when virus was injected into the haemocoel of larvae and after infection with MdPDV . Characteristics of MdPDV-induced apoptosis included condensation of chromatin, cell surface blebbing and fragmentation of DNA into a 200 bp ladder. Although MdPDV induced changes in the ability of plasmatocytes to adhere to foreign surfaces, apoptosis of this morphotype was not observed. Examples from the literature suggest that some viruses promote their own survival by suppressing apoptosis of host cells. However, since polydnaviruses are likely to be transmitted vertically, we suggest that MdPDV promotes its own survival by inducing apoptosis of host immune cells which would otherwise kill the developing egg.

  • Received:
  • Accepted:
  • Published Online:
© Journal of General Virology 1995
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1995-02-01
2024-04-19
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References

  1. Clem R. J., Miller L. K. 1993; Apoptosis reduces both the in vitro replication and the in vivo infectivity of a baculovirus. Journal of Virology 67:3730–3738
     [Google Scholar]
  2. Clem J. R., & 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]
  3. 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
     [Google Scholar]
  4. Cohen J. J. 1993; Apoptosis. Immunology Today 14:123–130
     [Google Scholar]
  5. Compton M. M. 1992; A biochemical hallmark of apoptosis: internucleosomal degradation of the genome. Cancer Metastasis Review 11:105–119
     [Google Scholar]
  6. Crook N. E., Clem R. J., Miller L. K. 1993; An apoptosis-inhibiting baculoviros gene with a zinc finger-like motif. Journal of Virology 67:2168–2174
     [Google Scholar]
  7. Davies D. H., Strand M. R., Vinson S. B. 1987; Changes in differential haemocyte count and in vitro behaviour of plasmatocytes from host Heliothis virescens caused by Campoletis sonorensis polydnavirus. Journal of Insect Physiology 33:143–153
     [Google Scholar]
  8. Edson K. M., Vinson S. B., Stoltz D. B., Summers M. D. 1981; Virus in a parasitoid wasp: suppression of the cellular immune response in the parasitoid’s host. Science 211:582–583
     [Google Scholar]
  9. Fleming J. G. W. 1992; Polydnaviruses: mutualists and pathogens. Annual Review of Entomology 37:401–425
     [Google Scholar]
  10. Fleming J. G. W., Summers M. D. 1991; Polydnavirus DNA is integrated in the DNA of its parasitoid wasp host. Proceedings of the National Academy of Sciences, USA 88:9770–9774
     [Google Scholar]
  11. Gorczyca W., Bigman K., Mittelman A., Ahmed T., Gong J., Melamed M. R., Darzynkiewicz Z. 1993; Induction of DNA strand breaks associated with apoptosis during treatment of leukemias. Leukemia 7:659–670
     [Google Scholar]
  12. Gougeon M., Montagnier L. 1993; Apoptosis and AIDS. Science 260:1269–1270
     [Google Scholar]
  13. Gregory C. D., Dive C., Henderson S., Smith C. A., Williams T., Gordon J., Rickinson A. B. 1991; Activation of Epstein–Barr virus latent genes protects human B cells from death by apoptosis. Nature 349:612–614
     [Google Scholar]
  14. Guzo D., Stoltz D. B. 1987; Observations on cellular immunity and parasitism in the tussock moth. Journal of Insect Physiology 33:19–31
     [Google Scholar]
  15. Henderson S., Rowe M., Gregory C., Croom-Carter D., Wang F., Longnecker R., Kieff E., Rickinson A. 1993; Epstein–Barr virus-coded BHRF1 protein, a viral homologue of Bcl-2, protects human B cells from programmed cell death. Proceedings of the National Academy of Sciences, USA 90:8479–8483
     [Google Scholar]
  16. Hershberger P. A., Dickson J. A., Friesen P. D. 1992; Site-specific mutagenesis of the 35-kilodalton protein gene encoded by Autographa californica nuclear polyhedrosis virus: cell line-specific effects on virus replication. Journal of Virology 66:5525–5533
     [Google Scholar]
  17. Hershberger P. A., LaCount D. J., Friesen P. D. 1994; The apoptotic suppressor p35 is required early during baculovirus replication and is targeted to the cytosol of infected cells. Journal of Virology 68:3467–3477
     [Google Scholar]
  18. Hinshaw V. S., Olsen C. W., Dybdahl-Sissoko N., Evans D. 1994; Apoptosis: a mechanism of cell killing by influenza A and B viruses. Journal of Virology 68:3667–3673
     [Google Scholar]
  19. Jeurissen S. H., Wagenaar M. F., Pol J. M. A., van der Eb A. J., Noteborn M. H. M. 1992; Chicken anemia virus causes apoptosis of thymocytes after in vivo infection and of cell lines after in vitro infection. Journal of Virology 66:7383–7388
     [Google Scholar]
  20. 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]
  21. Lackie A. M. 1988; Haemocyte behaviour. Advances in Insect Physiology 21:85–178
     [Google Scholar]
  22. Lerch R. A., Friesen P. D. 1993; The 35-kilodalton protein gene p 35) of Autographa californica nuclear polyhedrosis virus and the neomycin resistance gene provide dominant selection of recombinant baculoviruses. Nucleic Acids Research 21:1753–1760
     [Google Scholar]
  23. Levine B., Huang Q., Isaacs J. T., Reed J. C., Griffin D. E., Hardwick J. M. 1993; Conversion of lytic to persistent alphavirus infection by the bcl-2 cellular oncogene. Nature 361:739–742
     [Google Scholar]
  24. Martz E., Howell D. M. 1989; CTL: virus control cells first and cytolytic cells second?. Immunology Today 10:79–86
     [Google Scholar]
  25. Noteborn M. H. M., Todd D., Verschueren C. A. J., de Gauw W. F. M., Curran W. L., Veldkamp S., Douglas A. J., McNulty M. S., van der Eb A. J., Koch G. 1994; A single chicken anemia virus protein induces apoptosis. Journal of Virology 68:346–351
     [Google Scholar]
  26. Pech L. L., Trudeau D., Strand M. R. 1994; Separation and behavior in vitro of hemocytes from the moth, Pseudoplusia includens . Cell and Tissue Research 277:159–167
     [Google Scholar]
  27. Rao L., Debbas M., Sabbatini P., Hockenbery D., Korsmeyer S., White E. 1992; The adenovirus E1A proteins induce apoptosis, which is inhibited by the E1B 19-kda and Bcl-2 proteins. Proceedings of the National Academy of Sciences, USA 89:7742–7746
     [Google Scholar]
  28. Rizki R. M., Rizki T. M. 1990; Parasitoid virus-like particles destroy Drosophila cellular immunity. Proceedings of the National Academy of Sciences, USA 87:8388–8392
     [Google Scholar]
  29. Rojko J. L., Fulton R. M., Rezanka L. J., Williams L. L., Copelan E., Cheney C. M., Reichel G. S., Neil J. C., Mathes L. E., Fisher T. G., Cloyd M. W. 1992; Lymphocytotoxic strains of feline leukemia virus induce apoptosis in feline T4-thymic lymphoma cells. Journal of Clinical Investigation 66:418–426
     [Google Scholar]
  30. Rowley A. F., Ratcliffe N. A. 1981; Insects. In Invertebrate Blood Cells pp 471–490 Edited by Ratcliffe N. A., Rowley A. F. New York: Academic Press;
     [Google Scholar]
  31. Stoltz D. B. 1990; Evidence for chromosomal transmission of polydnavirus DNA. Journal of General Virology 71:1051–1056
     [Google Scholar]
  32. Stoltz D. B. 1993; The polydnavirus life cycle. In Parasites and Pathogens of Insects vol 1 pp 167–187 Edited by Beckage N. E., Thompson S. N., Federici B. A. New York: Academic Press;
     [Google Scholar]
  33. Stoltz D. B., Krell P., Summers M. D., Vinson S. B. 1984; Polydnaviridae – a proposed new family of insect viruses with segmented, double-stranded, circular DNA genomes. Intervirology 21:1–4
     [Google Scholar]
  34. Strand M. R. 1990; Characterization of larval development in Pseudoplusia includens (Walker) (Lepidoptera: Noctuidae). Annals of the Entomological Society of America 83:538–544
     [Google Scholar]
  35. Strand M. R. 1994; Microplitis demolitor polydnavirus infects and expresses in specific morphotypes of Pseudoplusia includens haemocytes. Journal of General Virology 75:3007–3020
     [Google Scholar]
  36. Strand M. R., Dover B. A. 1991; Developmental disruption of Pseudoplusia includens and Heliothis virescens larvae by the polydnavirus and venom of Microplitis demolitor . Archives of Insect Biochemistry and Physiology 18:131–145
     [Google Scholar]
  37. Strand M. R., Noda T. 1991; Alterations in the haemocytes of Pseudoplusia includens after parasitism by Microplitis demolitor . Journal of Insect Physiology 37:839–850
     [Google Scholar]
  38. Strand M. R., Wong E. A. 1991; The growth and role of Microplitis demolitor teratocytes in parasitism of Pseudoplusia includens . Journal of Insect Physiology 37:503–515
     [Google Scholar]
  39. Strand M. R., Pech L. L. 1995; Immunological basis for compatibility in parasitoid-host relationships. Annua! Review of Entomology 40:31–56
     [Google Scholar]
  40. Strand M. R., McKenzie D. I., Grassl V., Dover B. A., Aiken J. M. 1992; Persistence and expression of Microplitis demolitor polydnavirus in Pseudoplusia includens . Journal of General Virology 73:1627–1635
     [Google Scholar]
  41. Strand M. R., Johnson J. A., Noda T., Dover B. A. 1994; Development and partial characterization of monoclonal antibodies to venom of the parasitoid Microplitis demolitor . Archives of Insect Biochemistry and Physiology 26:123–136
     [Google Scholar]
  42. Tanaka T. 1987; Morphological changes in haemocytes of the host, Pseudaletia separata, parasitized by Microplitis mediator or Apanteles kariyai. Developmental and Comparative Immunology 11:57–67
     [Google Scholar]
  43. Upton C., Mossman K., McFadden G. 1992; Encoding of a homolog of the IFN-γ receptor by myxoma virus. Science 258:1369–1371
     [Google Scholar]
  44. Vaux D. L. 1993; Toward an understanding of the molecular mechanisms of physiological cell death. Proceedings of the National Academy of Sciences, USA 90:786–789
     [Google Scholar]
  45. Xu D., Stoltz D. 1991; Evidence for a chromosomal location of polydnavirus DNA in the ichnuemonid parasitoid Hyposoter fugitivus . Journal of Virology 65:6693–6704
     [Google Scholar]
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Microplitis demolitor polydnavirus induces apoptosis of a specific haemocyte morphotype in Pseudoplusia includens
J. Gen. Virol. 76, 283 (1995); https://doi.org/10.1099/0022-1317-76-2-283
/content/journal/jgv/10.1099/0022-1317-76-2-283
/content/journal/jgv/10.1099/0022-1317-76-2-283
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