1887

Abstract

Baculovirus occlusion-derived virions (ODVs) contain a number of infectivity factors essential for the initiation of infection in larval midgut cells. Deletion of any of these factors neutralizes infectivity by the route. We have observed that P74 of the group I alphabaculovirus multiple nucleopolyhedrovirus (AcMNPV) is N-terminally cleaved when a soluble form of the protein was incubated with insect midgut tissues under alkaline conditions and that cleavage was prevented by soybean trypsin inhibitor (SBTI). Presently, biological assays were carried out that suggest SBTI inhibits and trypsin enhances baculovirus infectivity. We developed a method to rescue infectivity of a P74 null virus involving co-transfection of viral DNA with a plasmid that transiently expresses . We used this plasmid rescue method to functionally characterize P74. A series of site-directed mutants were generated at the N terminus to evaluate if trypsin cleavage sites were necessary for function. Mutagenesis of R195, R196 and R199 compromised infectivity and rendered P74 resistant to midgut trypsin.

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2008-10-01
2024-04-19
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References

  1. Blissard G. W., Rohrmann G. F. 1991; Baculovirus gp64 gene expression: analysis of sequences modulating early transcription and transactivation by IE1. J Virol 65:5820–5827
    [Google Scholar]
  2. Blissard G. W., Wenz J. R. 1992; Baculovirus GP64 envelope glycoprotein is sufficient to mediate pH-dependent membrane fusion. J Virol 66:6829–6835
    [Google Scholar]
  3. Braunagel S. C., Summers M. D. 1994; Autographa californica nuclear polyhedrosis virus, PDV, and ECV viral envelopes and nucleocapsids: structural proteins, antigens, lipid and fatty acid profiles. Virology 202:315–328 [CrossRef]
    [Google Scholar]
  4. Bromme D., Okamoto K. 1995; The baculovirus cysteine protease has a cathepsin B-like S2-subsite specificity. Biol Chem Hoppe Seyler 376:611–615 [CrossRef]
    [Google Scholar]
  5. Brown M., Crawford A. M., Faulkner P. 1979; Genetic analysis of a baculovirus, Autographa californica nuclear polyhedrosis virus I. Isolation of temperature-sensitive mutants and assortment into complementation groups. J Virol 31:190–198
    [Google Scholar]
  6. Collins P. L., Chanock R. M., McIntosh K. 1995; Parainfluenza viruses. In Fields Virology pp 1215–1217Edited by Fields B. N., Knipe D. M., Howley P. M. Philadelphia: Lippincott-Raven Publishers;
    [Google Scholar]
  7. Duckert P., Brunak S., Blom N. 2004; Prediction of proprotein convertase cleavage sites. Protein Eng Des Sel 17:107–112 [CrossRef]
    [Google Scholar]
  8. Eppstein D. A., Thoma J. A. 1975; Alkaline protease associated with the matrix protein of a virus infecting the cabbage looper. Biochem Biophys Res Commun 62:478–484 [CrossRef]
    [Google Scholar]
  9. Eppstein D. A., Thoma J. A., Scott H. A., Young S. Y. 1975; Degradation of matrix protein from the nuclear-polyhedrosis virus of Trichoplusia ni by an endogenous protease. Virology 67:591–594 [CrossRef]
    [Google Scholar]
  10. Faulkner P., Kuzio J., Williams G. V., Wilson J. A. 1997; Analysis of p74, a PDV envelope protein of Autographa californica nucleopolyhedrovirus required for occlusion body infectivity in vivo . J Gen Virol 78:3091–3100
    [Google Scholar]
  11. Frana M. F., Behnke J. N., Sturman L. S., Holmes K. V. 1985; Proteolytic cleavage of the E2 glycoprotein of murine coronavirus: host-dependent differences in proteolytic cleavage and cell fusion. J Virol 56:912–920
    [Google Scholar]
  12. Granados R. R. 1978; Early events in the infection of Heliothis zea midgut cells by a baculovirus. Virology 90:170–174 [CrossRef]
    [Google Scholar]
  13. Haas-Stapleton E. J., Washburn J. O., Volkman L. E. 2004; P74 mediates specific binding of Autographa californica M nucleopolyhedrovirus occlusion-derived virus to primary cellular targets in the midgut epithelia of Heliothis virescens larvae. J Virol 78:6786–6791 [CrossRef]
    [Google Scholar]
  14. Hohmann A. W., Faulkner P. 1983; Monoclonal antibodies to baculovirus structural proteins: determination of specificities by Western blot analysis. Virology 125:432–444 [CrossRef]
    [Google Scholar]
  15. Horton H. M., Burand J. P. 1993; Saturable attachment sites for polyhedron-derived baculovirus on insect cells and evidence for entry via direct membrane fusion. J Virol 67:1860–1868
    [Google Scholar]
  16. Hughes P. R., Wood H. A. 1996; In vivo production, stabilization, and infectivity of baculovirus preoccluded virions. Appl Environ Microbiol 62:105–108
    [Google Scholar]
  17. Ichihashi Y., Oie M. 1982; Proteolytic activation of vaccinia virus for the penetration phase of infection. Virology 116:297–305 [CrossRef]
    [Google Scholar]
  18. Jehle J. A., Blissard G. W., Bonning B. C., Cory J. S., Herniou E. A., Rohrmann G. F., Theilmann D. A., Thiem S. M., Vlak J. M. 2006; On the classification and nomenclature of baculoviruses: a proposal for revision. Arch Virol 151:1257–1266 [CrossRef]
    [Google Scholar]
  19. Johnston K. A., Lee M. J., Gatehouse J. A., Anstee J. H. 1991; The partial purification and characterization of serine protease activity in Helicoverpa armigera . Insect Biochem 21:389–397 [CrossRef]
    [Google Scholar]
  20. Kawanishi C. Y., Summers M. D., Stoltz D. B., Arnott H. J. 1972; Entry of an insect virus in vivo by fusion of viral envelope and microvillus membrane. J Invertebr Pathol 20:104–108 [CrossRef]
    [Google Scholar]
  21. Kikhno I., Gutierrez S., Croizier L., Croizier G., Ferber M. L. 2002; Characterization of pif , a gene required for the per os infectivity of Spodoptera littoralis nucleopolyhedrovirus. J Gen Virol 83:3013–3022
    [Google Scholar]
  22. 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]
  23. Kozlov E. A., Levitina T. L., Gusak N. M. 1986; The primary structure of baculovirus inclusion body proteins. Evolution and structure-function aspects. Curr Top Microbiol Immunol 131:135–164
    [Google Scholar]
  24. Krogh A., Larsson B., von Heijne G., Sonnhammer E. L. 2001; Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305:567–580 [CrossRef]
    [Google Scholar]
  25. Kuzio J., Jaques R., Faulkner P. 1989; Identification of p74, a gene essential for virulence of baculovirus occlusion bodies. Virology 173:759–763 [CrossRef]
    [Google Scholar]
  26. Lamb R. A., Krug R. M. 1995; Orthomyxoviridae : the viruses and their replication. In Fields Virology pp 1359–1362Edited by Fields B. N., Knipe D. M., Howley P. M. Philadelphia: Lippincott-Raven Publishers;
    [Google Scholar]
  27. Langridge W. H. R., Balter K. 1981; Protease activity associated with the capsule protein of Estigmene acrea granulosis virus. Virology 114:595–600 [CrossRef]
    [Google Scholar]
  28. Leikina E., Onaran H. O., Zimmerberg J. 1992; Acidic pH induces fusion of cells infected with baculovirus to form syncytia. FEBS Lett 304:221–224 [CrossRef]
    [Google Scholar]
  29. Maeda S., Nagata M., Tanada Y. 1983; Ionic conditions affecting the release and absorption of an alkaline protease associated with the occlusion bodies of insect baculoviruses. J Invertebr Pathol 42:376–383 [CrossRef]
    [Google Scholar]
  30. Monsma S. A., Blissard G. W. 1995; Identification of a membrane fusion domain and an oligomerization domain in the baculovirus GP64 envelope fusion protein. J Virol 69:2583–2595
    [Google Scholar]
  31. Muramatsu M., Homma M. 1980; Trypsin action on the growth of Sendai virus in tissue culture cells. V. An activating enzyme for Sendai virus in the chorioallantoic fluid of the embryonated chicken egg. Microbiol Immunol 24:113–122 [CrossRef]
    [Google Scholar]
  32. Ogay I. D., Lihoradova O. A., Azimova S. S., Abdukarimov A. A., Slack J. M., Lynn D. E. 2006; Transfection of insect cell lines using polyethylenimine. Cytotechnology 51:89–98 [CrossRef]
    [Google Scholar]
  33. Ohkawa T., Majima K., Maeda S. 1994; A cysteine protease encoded by the baculovirus Bombyx mori nuclear polyhedrosis virus. J Virol 68:6619–6625
    [Google Scholar]
  34. Ohkawa T., Washburn J. O., Sitapara R., Sid E., Volkman L. E. 2005; Specific binding of Autographa californica M nucleopolyhedrovirus occlusion-derived virus to midgut cells of Heliothis virescens larvae is mediated by products of pif genes Ac119 and Ac022 but not by Ac115 . J Virol 79:15258–15264 [CrossRef]
    [Google Scholar]
  35. Oliveira M. G., De Simone S. G., Xavier L. P., Guedes R. N. 2005; Partial purification and characterization of digestive trypsin-like proteases from the velvet bean caterpillar, Anticarsia gemmatalis . Comp Biochem Physiol B Biochem Mol Biol 140:369–380 [CrossRef]
    [Google Scholar]
  36. O'Reilly D. R., Miller L. K., Luckow V. A. 1992 Baculovirus Expression Vectors: a Laboratory Manual: Oxford University Press; USA:
    [Google Scholar]
  37. Pearson M. N., Groten C., Rohrmann G. F. 2000; Identification of the Lymantria dispar nucleopolyhedrovirus envelope fusion protein provides evidence for a phylogenetic division of the Baculoviridae . J Virol 74:6126–6131 [CrossRef]
    [Google Scholar]
  38. Pereira M. E., Dorr F. A., Peixoto N. C., Lima-Garcia J. F., Dorr F., Brito G. G. 2005; Perspectives of digestive pest control with proteinase inhibitors that mainly affect the trypsin-like activity of Anticarsia gemmatalis Hubner. (Lepidoptera: Noctuidae; Braz J Med Biol Res 38, 1633–1641 [CrossRef]
  39. Pijlman G. P., Pruijssers A. J., Vlak J. M. 2003; Identification of pif-2 , a third conserved baculovirus gene required for per os infection of insects. J Gen Virol 84:2041–2049 [CrossRef]
    [Google Scholar]
  40. Rashidan K. K., Nassoury N., Giannopoulos P. N., Guertin C. 2005; Transcription, translation, and immunolocalization of ODVP-6E/ODV-E56 and p74 proteins: two highly conserved ODV-associated envelope proteins of Choristoneura fumiferana Granulovirus. J Biochem Mol Biol 38:65–70 [CrossRef]
    [Google Scholar]
  41. Rohrmann G. F. 1986; Polyhedrin structure. J Gen Virol 67:1499–1513 [CrossRef]
    [Google Scholar]
  42. Slack J. M., Lawrence S. D. 2002; Purification of DNA for the transfection of a Spodoptera frugiperda cell line. Methods Cell Sci 24:155–163 [CrossRef]
    [Google Scholar]
  43. Slack J. M., Lawrence S. D. 2005; Evidence for proteolytic cleavage of the baculovirus occlusion-derived virion envelope protein P74. J Gen Virol 86:1637–1643 [CrossRef]
    [Google Scholar]
  44. Slack J. M., Kuzio J., Faulkner P. 1995; Characterization of v-cath, a cathepsin L-like proteinase expressed by the baculovirus Autographa californica multiple nuclear polyhedrosis virus . J Gen Virol 76:1091–1098 [CrossRef]
    [Google Scholar]
  45. Slack J. M., Dougherty E. M., Lawrence S. D. 2001; A study of the Autographa californica multiple nucleopolyhedrovirus ODV envelope protein p74 using a GFP tag. J Gen Virol 82:2279–2287
    [Google Scholar]
  46. Tanada Y., Hess R. T., Omi E. M. 1975; Invasion of a nuclear polyhedrosis virus in midgut of the armyworm, Pseudaletia unipuncta , and the enhancement of a synergistic enzyme. J Invertebr Pathol 26:99–104 [CrossRef]
    [Google Scholar]
  47. Terra W. R., Ferreira C. 1994; Insect digestive enzymes: properties, compartmentalization and function. Comp Biochem Physiol 109:1–62 [CrossRef]
    [Google Scholar]
  48. Thompson J. D., Higgins D. G., Gibson T. J. 1994; clustal w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680 [CrossRef]
    [Google Scholar]
  49. Volkman L. E., Goldsmith P. A. 1985; Mechanism of neutralization of budded Autographa californica nuclear polyhedrosis virus by a monoclonal antibody: inhibition of entry by adsorptive endocytosis. Virology 143:185–195 [CrossRef]
    [Google Scholar]
  50. Vonderfecht S. L., Miskuff R. L., Wee S. B., Sato S., Tidwell R. R., Geratz J. D., Yolken R. H. 1988; Protease inhibitors suppress the in vitro and in vivo replication of rotavirus. J Clin Invest 82:2011–2016 [CrossRef]
    [Google Scholar]
  51. Westenberg M., Wang H., IJkel W. F., Goldbach R. W., Vlak J. M., Zuidema D. 2002; Furin is involved in baculovirus envelope fusion protein activation. J Virol 76:178–184 [CrossRef]
    [Google Scholar]
  52. Whitford M., Stewart S., Kuzio J., Faulkner P. 1989; Identification and sequence analysis of a gene encoding gp67, an abundant envelope glycoprotein of the baculovirus Autographa californica nuclear polyhedrosis virus. J Virol 63:1393–1399
    [Google Scholar]
  53. Wilson J. A. 1997; Strategies for the construction and safe release of recombinant baculovirus with enhanced insecticidal properties: intracellular complementation of P74, structural properties of P10 and functional analysis of GP41. Doctoral thesis Department of Microbiology and Immunology, Queen's University; Kingston, Canada:
  54. Yao L., Zhou W., Xu H., Zheng Y., Qi Y. 2004; The Heliothis armigera single nucleocapsid nucleopolyhedrovirus envelope protein P74 is required for infection of the host midgut. Virus Res 104:111–121 [CrossRef]
    [Google Scholar]
  55. Zanotto P. M., Kessing B. D., Maruniak J. E. 1993; Phylogenetic interrelationships among baculoviruses: evolutionary rates and host associations. J Invertebr Pathol 62:147–164 [CrossRef]
    [Google Scholar]
  56. Zhang G., Gurtu V., Kain S. R. 1996; An enhanced green fluorescent protein allows sensitive detection of gene transfer in mammalian cells. Biochem Biophys Res Commun 227:707–711 [CrossRef]
    [Google Scholar]
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