1887

Abstract

Baculoviruses infect their lepidopteran hosts via the midgut epithelium through binding of occlusion-derived virus (ODV) and fusion between the virus envelope and microvillar membranes. To identify genes and sequences that are involved in this process, a random phage display library was screened for peptides that bound to brush border membrane vesicles (BBMV) derived from the midgut epithelium of . Seventeen peptides that bound to BBMV were recovered. Two of these, HV1 and HV2, had sequence similarity to the ODV envelope protein ODV-E66 that is found in five species of alphabaculoviruses. Chemically synthesized versions of HV1 and HV2, and two peptides (E66A and E66B) derived from similar sequences of multiple nucleopolyhedrovirus (MNPV) ODV-E66, bound to unfixed cryosections of whole midgut tissues. E66A, but not HV1, bound to gut BBMV proteins on a far-Western blot. Competition assays with HV1 and purified MNPV ODV resulted in decreased mortality of larvae at a dose of 1 LD, and a significant increase in survival time at higher virus concentrations. These results suggest a role for ODV-E66 in baculovirus infection of lepidopteran larval midgut epithelium.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.028118-0
2011-05-01
2020-01-26
Loading full text...

Full text loading...

/deliver/fulltext/jgv/92/5/1051.html?itemId=/content/journal/jgv/10.1099/vir.0.028118-0&mimeType=html&fmt=ahah

References

  1. Altschul S. F. , Madden T. L. , Schäffer 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 Res 25:, 3389–3402. [CrossRef] [PubMed]
    [Google Scholar]
  2. Bonnycastle L. L. , Mehroke J. S. , Rashed M. , Gong X. , Scott J. K. . ( 1996; ). Probing the basis of antibody reactivity with a panel of constrained peptide libraries displayed by filamentous phage. . J Mol Biol 258:, 747–762. [CrossRef] [PubMed]
    [Google Scholar]
  3. Boraston A. B. , Bolam D. N. , Gilbert H. J. , Davies G. J. . ( 2004; ). Carbohydrate-binding modules: fine-tuning polysaccharide recognition. . Biochem J 382:, 769–781. [CrossRef] [PubMed]
    [Google Scholar]
  4. Braunagel S. C. , Summers M. D. . ( 2007; ). Molecular biology of the baculovirus occlusion-derived virus envelope. . Curr Drug Targets 8:, 1084–1095. [CrossRef] [PubMed]
    [Google Scholar]
  5. Braunagel S. C. , Burks J. K. , Rosas-Acosta G. , Harrison R. L. , Ma H. , Summers M. D. . ( 1999; ). Mutations within the Autographa californica nucleopolyhedrovirus FP25K gene decrease the accumulation of ODV-E66 and alter its intranuclear transport. . J Virol 73:, 8559–8570.[PubMed]
    [Google Scholar]
  6. Braunagel S. C. , Russell W. K. , Rosas-Acosta G. , Russell D. H. , Summers M. D. . ( 2003; ). Determination of the protein composition of the occlusion-derived virus of Autographa californica nucleopolyhedrovirus. . Proc Natl Acad Sci U S A 100:, 9797–9802. [CrossRef] [PubMed]
    [Google Scholar]
  7. Cheng Y. M. , Hsieh F. C. , Meng M. . ( 2009; ). Functional analysis of conserved aromatic amino acids in the discoidin domain of Paenibacillus β-1,3-glucanase. . Microb Cell Fact 8:, 62. [CrossRef] [PubMed]
    [Google Scholar]
  8. Dinglasan R. R. , Jacobs-Lorena M. . ( 2005; ). Insight into a conserved lifestyle: protein–carbohydrate adhesion strategies of vector-borne pathogens. . Infect Immun 73:, 7797–7807. [CrossRef] [PubMed]
    [Google Scholar]
  9. Dinglasan R. R. , Alaganan A. , Ghosh A. K. , Saito A. , van Kuppevelt T. H. , Jacobs-Lorena M. . ( 2007; ). Plasmodium falciparum ookinetes require mosquito midgut chondroitin sulfate proteoglycans for cell invasion. . Proc Natl Acad Sci U S A 104:, 15882–15887. [CrossRef] [PubMed]
    [Google Scholar]
  10. Garcia-Maruniak A. , Abd-Alla A. M. , Salem T. Z. , Parker A. G. , Lietze V. U. , van Oers M. M. , Maruniak J. E. , Kim W. , Burand J. P. et al. ( 2009; ). Two viruses that cause salivary gland hypertrophy in Glossina pallidipes and Musca domestica are related and form a distinct phylogenetic clade. . J Gen Virol 90:, 334–346. [CrossRef] [PubMed]
    [Google Scholar]
  11. Ghosh A. K. , Ribolla P. E. , Jacobs-Lorena M. . ( 2001; ). Targeting Plasmodium ligands on mosquito salivary glands and midgut with a phage display peptide library. . Proc Natl Acad Sci U S A 98:, 13278–13281. [CrossRef] [PubMed]
    [Google Scholar]
  12. Ghosh A. K. , Devenport M. , Jethwaney D. , Kalume D. E. , Pandey A. , Anderson V. E. , Sultan A. A. , Kumar N. , Jacobs-Lorena M. . ( 2009; ). Malaria parasite invasion of the mosquito salivary gland requires interaction between the Plasmodium TRAP and the Anopheles saglin proteins. . PLoS Pathog 5:, e1000265. [CrossRef] [PubMed]
    [Google Scholar]
  13. Giordano R. J. , Cardó-Vila M. , Lahdenranta J. , Pasqualini R. , Arap W. . ( 2001; ). Biopanning and rapid analysis of selective interactive ligands. . Nat Med 7:, 1249–1253. [CrossRef] [PubMed]
    [Google Scholar]
  14. Hall T. A. . ( 1999; ). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. . Nucleic Acids Symp Ser 41:, 95–98.
    [Google Scholar]
  15. 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] [PubMed]
    [Google Scholar]
  16. Harrison R. L. , Sparks W. O. , Bonning B. C. . ( 2010; ). Autographa californica multiple nucleopolyhedrovirus ODV-E56 envelope protein is required for oral infectivity and can be substituted functionally by the Rachiplusia ou multiple nucleopolyhedrovirus ODV-E56. . J Gen Virol 91:, 1173–1182. [CrossRef] [PubMed]
    [Google Scholar]
  17. Herniou E. A. , Olszewski J. A. , Cory J. S. , O’Reilly D. R. . ( 2003; ). The genome sequence and evolution of baculoviruses. . Annu Rev Entomol 48:, 211–234. [CrossRef] [PubMed]
    [Google Scholar]
  18. 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.[PubMed]
    [Google Scholar]
  19. 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] [PubMed]
    [Google Scholar]
  20. Kariithi H. M. , Ince I. A. , Boeren S. , Vervoort J. , Bergoin M. , van Oers M. M. , Abd-Alla A. M. , Vlak J. M. . ( 2010; ). Proteomic analysis of Glossina pallidipes salivary gland hypertrophy virus virions for immune intervention in tsetse fly colonies. . J Gen Virol 91:, 3065–3074. [CrossRef] [PubMed]
    [Google Scholar]
  21. Lambrechts L. , Scott T. W. . ( 2009; ). Mode of transmission and the evolution of arbovirus virulence in mosquito vectors. . Proc Biol Sci 276:, 1369–1378. [CrossRef] [PubMed]
    [Google Scholar]
  22. Liu S. , Sivakumar S. , Sparks W. O. , Miller W. A. , Bonning B. C. . ( 2010; ). A peptide that binds the pea aphid gut impedes entry of Pea enation mosaic virus into the aphid hemocoel. . Virology 401:, 107–116. [CrossRef] [PubMed]
    [Google Scholar]
  23. O'Reilly D. R. , Miller L. K. , Luckow V. A. . ( 1992; ). Baculovirus Expression Vectors - A Laboratory Manual. New York:: W. H. Freeman & Company;.
    [Google Scholar]
  24. Peng K. , Wu M. , Deng F. , Song J. , Dong C. , Wang H. , Hu Z. . ( 2010; a). Identification of protein-protein interactions of the occlusion-derived virus-associated proteins of Helicoverpa armigera nucleopolyhedrovirus. . J Gen Virol 91:, 659–670. [CrossRef] [PubMed]
    [Google Scholar]
  25. Peng K. , van Oers M. M. , Hu Z. , van Lent J. W. M. , Vlak J. M. . ( 2010; b). Baculovirus per os infectivity factors form a complex on the surface of occlusion-derived virus. . J Virol 84:, 9497–9504. [CrossRef] [PubMed]
    [Google Scholar]
  26. Pfleiderer G. . ( 1970; ). Particle-bound aminopeptidate from pig kidney. . Methods Enzymol 19:, 514–521. [CrossRef]
    [Google Scholar]
  27. Pierro D. J. , Powers E. L. , Olson K. E. . ( 2008; ). Genetic determinants of Sindbis virus mosquito infection are associated with a highly conserved alphavirus and flavivirus envelope sequence. . J Virol 82:, 2966–2974. [CrossRef] [PubMed]
    [Google Scholar]
  28. Sambrook J. , Russell D. W. . ( 2001; ). Appendix 8: Commonly used Techniques in Molecular Cloning. Molecular Cloning: a Laboratory Manual, vol.3, pp. A8.1––A8.51. Cold Spring Harbor, NY:: Cold Spring Harbor Laboratory;.
    [Google Scholar]
  29. Slack J. , Arif B. M. . ( 2007; ). The baculoviruses occlusion-derived virus: virion structure and function. . Adv Virus Res 69:, 99–165. [CrossRef] [PubMed]
    [Google Scholar]
  30. Smith G. P. , Scott J. K. . ( 1993; ). Libraries of peptides and proteins displayed on filamentous phage. . Methods Enzymol 217:, 228–257. [CrossRef] [PubMed]
    [Google Scholar]
  31. Sparks W. O. , Harrison R. L. , Bonning B. C. . ( 2011; ). Autographa californica multiple nucleopolyhedrovirus ODV-E56 is a per os infectivity factor, but is not essential for binding and fusion of occlusion-derived virus to the host midgut. . Virology 409:, 69–76.[PubMed] [CrossRef]
    [Google Scholar]
  32. 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] [PubMed]
    [Google Scholar]
  33. van Hulten M. C. , Witteveldt J. , Peters S. , Kloosterboer N. , Tarchini R. , Fiers M. , Sandbrink H. , Lankhorst R. K. , Vlak J. M. . ( 2001; ). The white spot syndrome virus DNA genome sequence. . Virology 286:, 7–22. [CrossRef] [PubMed]
    [Google Scholar]
  34. van Oers M. M. , Vlak J. M. . ( 2007; ). Baculovirus genomics. . Curr Drug Targets 8:, 1051–1068. [CrossRef] [PubMed]
    [Google Scholar]
  35. Vigdorovich V. , Miller A. D. , Strong R. K. . ( 2007; ). Ability of hyaluronidase 2 to degrade extracellular hyaluronan is not required for its function as a receptor for jaagsiekte sheep retrovirus. . J Virol 81:, 3124–3129. [CrossRef] [PubMed]
    [Google Scholar]
  36. Vodovar N. , Vallenet D. , Cruveiller S. , Rouy Z. , Barbe V. , Acosta C. , Cattolico L. , Jubin C. , Lajus A. et al. ( 2006; ). Complete genome sequence of the entomopathogenic and metabolically versatile soil bacterium Pseudomonas entomophila . . Nat Biotechnol 24:, 673–679. [CrossRef] [PubMed]
    [Google Scholar]
  37. Wang Y. , Jehle J. A. . ( 2009; ). Nudiviruses and other large, double-stranded circular DNA viruses of invertebrates: new insights on an old topic. . J Invertebr Pathol 101:, 187–193. [CrossRef] [PubMed]
    [Google Scholar]
  38. Wolfersberger M. , Luethy P. , Maurer A. , Parenti P. , Sacchi F. V. , Giordana B. , Hanozet G. M. . ( 1987; ). Preparation and partial characterization of amino acid transporting brush border membrane vesicles from the larval midgut of the cabbage butterfly (Pieris brassicae). . Comp Biochem Physiol 86:, 301–308. [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.028118-0
Loading
/content/journal/jgv/10.1099/vir.0.028118-0
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