1887

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Volume 87, Issue 8

Response of immunocompetent and immunosuppressed larvae to baculovirus infection Free

Abstract

The Mediterranean lepidopteran pest is highly resistant to infection with the multiple nucleopolyhedrovirus (AcMNPV) via the oral route, but highly sensitive to infection with budded virus (BV) via the intrahaemocoelic route. To study the fate of AcMNPV infection in , vHSGFP, an AcMNPV recombinant that expresses the reporter green fluorescent protein gene under the control of the heat-shock promoter, and high-resolution fluorescence microscopy were utilized. fourth-instar larvae infected orally with vHSGFP showed melanization and encapsulation of virus-infected tracheoblast cells serving the midgut columnar cells. At 72 h post-infection, the viral foci were removed during the moult clearing the infection. Thus, oral infection was restricted by immune responses to the midgut and midgut-associated tracheal cells. By contrast, injection of BV into the haemocoel resulted in successful infection of tracheoblasts, followed by spread of the virus through the tracheal epidermis to other tissues. However, in contrast to fully permissive infections where tracheoblasts and haemocytes are equally susceptible to infection, a severe limitation to vHSGFP infection of haemocytes was observed. To investigate the resistance of haemocytes to BV infection with AcMNPV, the larval immune system was suppressed with the polydnavirus or a putatively immunosuppressive polydnavirus gene, . Both treatments increased the susceptibility of larvae to AcMNPV. It is concluded that the resistance of to AcMNPV infection involves both humoral and cellular immune responses that act at the gut and haemocyte levels. The results also support the hypothesis that tracheolar cells mediate establishment of systemic baculovirus infections in lepidopteran larvae. The finding that polydnaviruses and their encoded genes synergize baculovirus infection also provides an approach to dissecting the responses of the lepidopteran immune system to viruses by using specific polydnavirus immunosuppressive genes.

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2006-08-01
2024-04-27
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References

  1. 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 [CrossRef]
     [Google Scholar]
  2. Bishop D. H. L., Entwistle P. F., Cameron I. R., Allen C. J., Possee R. D. 1988; Field trials of genetically engineered baculovirus insecticides. In The Release of Genetically Engineered Micro-organisms pp  143–179 Edited by Sussman M., Collins C. H., Skinner F. A., Stewart-Tull D. E. New York: Academic Press;
     [Google Scholar]
  3. Chejanovsky N., Gershburg E. 1995; The wild-type Autographa californica nuclear polyhedrosis virus induces apoptosis of Spodoptera littoralis cells. Virology 209:519–525 [CrossRef]
     [Google Scholar]
  4. Chejanovsky N., Zilberberg N., Rivkin H., Zlotkin E., Gurevitz M. 1995; Functional expression of an alpha anti-insect scorpion neurotoxin in insect cells and lepidopterous larvae. FEBS Lett 376:181–184 [CrossRef]
     [Google Scholar]
  5. Clarke T. E., Clem R. J. 2002; Lack of involvement of haemocytes in the establishment and spread of infection in Spodoptera frugiperda larvae infected with the baculovirus Autographa californica M nucleopolyhedrovirus by intrahaemocoelic injection. J Gen Virol 83:1565–1572
     [Google Scholar]
  6. Du Q., Lehavi D., Faktor O., Qi Y., Chejanovsky N. 1999; Isolation of an apoptosis suppressor gene of the Spodoptera littoralis nucleopolyhedrovirus. J Virol 73:1278–1285
     [Google Scholar]
  7. Engelhard E. K., Kam-Morgan L. N. W., Washburn J. O., Volkman L. E. 1994; The insect tracheal system: a conduit for the systemic spread of Autographa californica M nuclear polyhedrosis virus. Proc Natl Acad Sci U S A 91:3224–3227 [CrossRef]
     [Google Scholar]
  8. Fleming J. A. G. W. 1992; Polydnaviruses: mutualists and pathogens. Annu Rev Entomol 37:401–425 [CrossRef]
     [Google Scholar]
  9. Gershburg E., Rivkin H., Chejanovsky N. 1997; Expression of the Autographa californica nuclear polyhedrosis virus apoptotic suppressor gene p35 in nonpermissive Spodoptera littoralis cells. J Virol 71:7593–7599
     [Google Scholar]
  10. Haas-Stapleton E. J., Washburn J. O., Volkman L. E. 2003; Pathogenesis of Autographa californica M nucleopolyhedrovirus in fifth instar Spodoptera frugiperda . J Gen Virol 84:2033–2040 [CrossRef]
     [Google Scholar]
  11. Kaeslin M., Pfister-Wilhelm R., Lanzrein B. 2005; Influence of the parasitoid Chelonus inanitus and its polydnavirus on host nutritional physiology and implications for parasitoid development. J Insect Physiol 51:1330–1339 [CrossRef]
     [Google Scholar]
  12. Kirkpatrick B. A., Washburn J. O., Engelhard E. K., Volkman L. E. 1994; Primary infection of insect tracheae by Autographa californica M nuclear polyhedrosis virus. Virology 203:184–186 [CrossRef]
     [Google Scholar]
  13. Kroemer J. A., Webb B. A. 2004; Polydnavirus genes and genomes: emerging gene families and new insights into polydnavirus replication. Annu Rev Entomol 49:431–456 [CrossRef]
     [Google Scholar]
  14. Kroemer J. A., Webb B. A. 2005; I κβ -related vankyrin genes in the Campoletis sonorensis ichnovirus: temporal and tissue-specific patterns of expression in parasitized Heliothis virescens lepidopteran hosts. J Virol 79:7617–7628 [CrossRef]
     [Google Scholar]
  15. Lange M., Wang H., Zhihong H., Jehle J. A. 2004; Towards a molecular identification and classification system of lepidopteran-specific baculoviruses. Virology 325:36–47 [CrossRef]
     [Google Scholar]
  16. Lu L., Du Q., Chejanovsky N. 2003; Reduced expression of the immediate-early protein IE0 enables efficient replication of Autographa californica multiple nucleopolyhedrovirus in poorly permissive Spodoptera littoralis cells. J Virol 77:535–545 [CrossRef]
     [Google Scholar]
  17. Lu L., Rivkin H., Chejanovsky N. 2005; The immediate-early protein IE0 of the Autographa californica nucleopolyhedrovirus is not essential for viral replication. J Virol 79:10077–10082 [CrossRef]
     [Google Scholar]
  18. Possee R. D. 1997; Baculoviruses as expression vectors. Curr Opin Biotechnol 8:569–572 [CrossRef]
     [Google Scholar]
  19. Smith G. E., Summers M. D. 1978; Analysis of baculovirus genomes with restriction endonucleases. Virology 89:517–527 [CrossRef]
     [Google Scholar]
  20. Statgraphics 2000 Statgraphics 5 Plus Manual Rockville, MD: Maugistics Inc;
     [Google Scholar]
  21. Stoltz D. B., Vinson S. B. 1979; Viruses and parasitism in insects. Adv Virus Res 24:125–171
     [Google Scholar]
  22. Strand M. R., Pech L. L. 1995; Microplitis demolitor polydnavirus induces apoptosis of a specific haemocyte morphotype in Pseudoplusia includens . J Gen Virol 76:283–291 [CrossRef]
     [Google Scholar]
  23. Summers M. D., Smith G. E. 1978; A Manual of Methods for Baculovirus Vectors and Insect Cell Culture Procedures (Texas Agriculture Experiment. Station Bulletin no: 1555 College Station, TX: Texas Agricultural Experiment Station;
     [Google Scholar]
  24. Thoetkiattikul H., Beck M. H., Strand M. R. 2005; Inhibitor κ B-like proteins from a polydnavirus inhibit NF- κ B activation and suppress the insect immune response. Proc Natl Acad Sci U S A 102:11426–11431 [CrossRef]
     [Google Scholar]
  25. Washburn J. O., Kirkpatrick B. A., Volkman L. E. 1996; Insect protection against viruses. Nature 383:767 [CrossRef]
     [Google Scholar]
  26. Washburn J. O., Haas-Stapleton E. J., Tan F. F., Beckage N. E., Volkman L. E. 2000; Co-infection of Manduca sexta larvae with polydnavirus from Cotesia congregata increases susceptibility to fatal infection by Autographa californica M nucleopolyhedrovirus. J Insect Physiol 46:179–190 [CrossRef]
     [Google Scholar]
  27. Wyder S., Blank F., Lanzrein B. 2003; Fate of polydnavirus DNA of the egg–larval parasitoid Chelonus inanitus in the host Spodoptera littoralis . J Insect Physiol 49:491–500 [CrossRef]
     [Google Scholar]
  28. Zhang P., Yang K., Dai X., Pang Y., Su D. 2002; Infection of wild-type Autographa californica multicapsid nucleopolyhedrovirus induces in vivo apoptosis of Spodoptera litura larvae. J Gen Virol 83:3003–3011
     [Google Scholar]
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Response of immunocompetent and immunosuppressed Spodoptera littoralis larvae to baculovirus infection
J. Gen. Virol. 87, 2217 (2006); https://doi.org/10.1099/vir.0.81918-0
/content/journal/jgv/10.1099/vir.0.81918-0
/content/journal/jgv/10.1099/vir.0.81918-0
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