Impact of a basement membrane-degrading protease on dissemination and secondary infection of multiple nucleopolyhedrovirus in (Fabricus) Free

Abstract

ScathL is a cathepsin L-like cysteine protease from the flesh fly, , that digests components of the basement membrane (BM) during insect metamorphosis. A recombinant baculovirus that expresses ScathL (AcMLF9.ScathL) kills larvae of the tobacco budworm, , significantly faster than the wild-type virus and triggers melanization and tissue fragmentation in infected larvae shortly before death. As BMs are a potential barrier to the spread of baculovirus secondary infection to other tissues in the host, this study tested the hypothesis that the rapid death of insects infected with AcMLF9.ScathL was caused by accelerated secondary infection resulting from the degradation of host BMs by ScathL. Viruses expressing catalytically active or inactive ScathL were used to examine the effects of ScathL activity on budded virus release into the haemocoel during infection, the production of polyhedra in infected larvae and the rate of infection of the gut, trachea, haemocytes, fat body and Malpighian tubules. It was concluded that the enhanced insecticidal efficacy of the recombinant baculovirus that expresses ScathL does not result from altered tissue tropism or accelerated systemic infection. Implications for the role of the BM as a barrier to baculovirus dissemination within the host insect are discussed.

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2007-04-01
2024-03-28
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References

  1. Bonning B. C. 2005; Baculoviruses: biology, biochemistry and molecular biology. In Comprehensive Molecular Insect Science . pp 233–270 Edited by Gilbert L. I., Iatrou K., Gill S. S. Oxford: Elsevier;
  2. Bradford M. M. 1976; A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254 [CrossRef]
    [Google Scholar]
  3. Carton Y., Nappi A. J. 1997; Drosophila cellular immunity against parasitoids. Parasitol Today 13:218–227 [CrossRef]
    [Google Scholar]
  4. Dai X., Willis L. G., Huijskens I., Palli S. R., Theilmann D. A. 2004; The acidic activation domains of the baculovirus transactivators IE1 and IE0 are functional for transcriptional activation in both insect and mammalian cells. J Gen Virol 85:573–582 [CrossRef]
    [Google Scholar]
  5. 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]
  6. Federici B. A. 1997; Baculovirus pathogenesis. In The Baculoviruses pp 33–60 Edited by Miller L. K. New York: Plenum Press;
    [Google Scholar]
  7. Fessler J. H., Fessler L. I. 1989; Drosophila extracellular matrix. Annu Rev Cell Biol 5:309–339 [CrossRef]
    [Google Scholar]
  8. Finney D. J. 1971 Probit Analysis London: Cambridge University Press;
    [Google Scholar]
  9. Granados R. R., Lawler K. A. 1981; In vivo pathway of Autographa californica baculovirus invasion and infection. Virology 108:297–308 [CrossRef]
    [Google Scholar]
  10. Harlow E., Lane D. 1988 Antibodies: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press;
    [Google Scholar]
  11. Harrison R. L., Bonning B. C. 2000; Use of scorpion neurotoxins to improve the insecticidal activity of Rachiplusia ou multicapsid nucleopolyhedrovirus. Biol Control 17:191–201 [CrossRef]
    [Google Scholar]
  12. Harrison R. L., Bonning B. C. 2001; Use of proteases to improve the insecticidal activity of baculoviruses. Biol Control 20:199–209 [CrossRef]
    [Google Scholar]
  13. Hess R. T., Falcon L. A. 1987; Temporal events in the invasion of the codling moth, Cydia pomonella , by a granulosis virus: an electron microscope study. J Invertebr Pathol 50:85–105 [CrossRef]
    [Google Scholar]
  14. Hill-Perkins M. S., Possee R. D. 1990; A baculovirus expression vector derived from the basic protein promoter of Autographa californica nuclear polyhedrosis virus. J Gen Virol 71:971–976 [CrossRef]
    [Google Scholar]
  15. Homma K., Natori S. 1996; Identification of substrate proteins for cathepsin L that are selectively hydrolyzed during the differentiation of imaginal discs of Sarcophaga peregrina . Eur J Biochem 240:443–447 [CrossRef]
    [Google Scholar]
  16. Hughes P. R., Wood H. A. 1981; A synchronous peroral technique for the bioassay of insect viruses. J Invertebr Pathol 37:154–159 [CrossRef]
    [Google Scholar]
  17. Jin H. 2002; Polyhedral envelope protein mutants in Rachiplusia ou multi-nucleocapsid nucleopolyhedrovirus. MSc thesis Iowa State University; Ames, IA, USA:
  18. Kalbfleisch J. D., Prentice R. L. 1980 The Statistical Analysis of Failure Time Data. New York: Wiley;
    [Google Scholar]
  19. Kamita S. G., Kang K.-D., Hammock B. D., Inceoglu A. B. 2005; Genetically modified baculoviruses for pest insect control. In Comprehensive Molecular Insect Science . pp 271–322 Edited by Gilbert L. I., Iatrou K., Gill S. S. Oxford: Elsevier;
  20. Keddie B. A., Aponte G. W., Volkman L. E. 1989; The pathway of infection of Autographa californica nuclear polyhedrosis virus in an insect host. Science 243:1728–1730 [CrossRef]
    [Google Scholar]
  21. Kitts P. A., Ayres M. D., Possee R. D. 1990; Linearization of baculovirus DNA enhances the recovery of recombinant virus expression vectors. Nucleic Acids Res 18:5667–5672 [CrossRef]
    [Google Scholar]
  22. Kunimi Y., Fuxa J. R., Hammock B. D. 1996; Comparison of wild type and genetically engineered nuclear polyhedrosis viruses of Autographa californica for mortality, virus replication and polyhedra production in Trichoplusia ni larvae. Entomol Exp Appl 81:251–257 [CrossRef]
    [Google Scholar]
  23. Lavine M. D., Strand M. R. 2002; Insect hemocytes and their role in immunity. Insect Biochem Mol Biol 32:1295–1309 [CrossRef]
    [Google Scholar]
  24. Moscardi F. 1999; Assessment of the application of baculoviruses for control of Lepidoptera. Annu Rev Entomol 44:257–289 [CrossRef]
    [Google Scholar]
  25. O'Reilly D. R., Miller L. K., Luckow V. A. 1992 Baculovirus Expression Vectors: a Laboratory Manual New York: Freeman;
    [Google Scholar]
  26. Reddy J. T., Locke M. 1990; The size limited penetration of gold particles through insect basal laminae. J Insect Physiol 36:397–407 [CrossRef]
    [Google Scholar]
  27. Robertson J. L., Preisler H. K. 1992 Pesticide Bioassays with Arthropods Baton Rouge, LA: CRC Press;
    [Google Scholar]
  28. Romoser W. S., Turell M. J., Lerdthusnee K., Neira M., Dohm D., Ludwig G., Wasieloski L. 2005; Pathogenesis of Rift Valley fever virus in mosquitoes – tracheal conduits and the basal lamina as an extra-cellular barrier. Arch Virol Suppl 89–100
    [Google Scholar]
  29. SAS Institute 1990 SAS User's Guide Version 6, 4th edn. Cary, NC: SAS Institute;
    [Google Scholar]
  30. Smith-Johannsen H., Witkiewicz H., Iatrou K. 1986; Infection of silkmoth follicular cells with Bombyx mori nuclear polyhedrosis virus. J Invertebr Pathol 48:74–84 [CrossRef]
    [Google Scholar]
  31. Summers M. D., Smith G. E. 1987; A Manual of Methods for Baculovirus Vectors and Insect Cell Culture Procedures . In Texas Agricultural Experiment Station Bulletin, No. 1555 pp 14–16 College Station, TX: Texas A & M University;
    [Google Scholar]
  32. Trudeau D., Washburn J. O., Volkman L. E. 2001; Central role of hemocytes in Autographa californica M nucleopolyhedrovirus pathogenesis in Heliothis virescens and Helicoverpa zea . J Virol 75:996–1003 [CrossRef]
    [Google Scholar]
  33. 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]
  34. Volkman L. E. 1997; Nucleopolyhedrovirus interactions with their insect hosts. Adv Virus Res 48:313–348
    [Google Scholar]
  35. Wang X. Z., Ooi B. G., Miller L. K. 1991; Baculovirus vectors for multiple gene expression and for occluded virus production. Gene 100:131–137 [CrossRef]
    [Google Scholar]
  36. Washburn J. O., Kirkpatrick B. A., Volkman L. E. 1995; Comparative pathogenesis of Autographa californica M nuclear polyhedrosis virus in larvae of Trichoplusia ni and Heliothis virescens . Virology 209:561–568 [CrossRef]
    [Google Scholar]
  37. 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]
  38. Wickham T. J., Davis T., Granados R. R., Shuler M. L., Wood H. A. 1992; Screening of insect cell lines for the production of recombinant proteins and infectious virus in the baculovirus system. Biotechnol Prog 8:391–396 [CrossRef]
    [Google Scholar]
  39. Yurchenco P. D., O'Rear J. 1993; Supramolecular organization of basement membranes. In Molecular and Cellular Aspects of Basement Membranes . pp 19–47 Edited by Rohrbach D. H., Timpl R. New York: Academic Press;
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