Skip to main content
SpringerLink
Log in

Bombyx mori nucleopolyhedrovirus ORF54, a viral desmoplakin gene, is associated with the infectivity of budded virions

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Bombyx mori nucleopolyhedrovirus (BmNPV) ORF54 (Bm54), a member of the viral desmoplakin N-terminus superfamily, is homologous to Autographa californica nucleopolyhedrovirus (AcMNPV) ORF66, which is required for the efficient egress of nucleocapsids from the nucleus and occlusion body formation. In this paper, we generated a bacmid with the Bm54 gene deleted via homologous recombination in Escherichia coli and characterized the mutant virus using a transfection-infection assay and transmission electron microscopy analysis. Our results demonstrated that the cells transfected with viral DNA lacking Bm54 produced non-infectious budded viruses (BVs). Electron microscopy showed that although the deletion of Bm54 did not affect assembly and release of nucleocapsids, it severely affected polyhedron formation. In conclusion, deletion of Bm54 resulted in non-infectious BV and defective polyhedra. Although the sequences of Bm54 and Ac66 are very similar, the two genes function quite differently in the regulation of viral life cycle.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Appel RD, Bairoch A, Hochstrasser DF (1994) A new generation of information retrieval tools for biologists: the example of the ExPASy WWW server. Trends Biochem Sci 19:258–260

    Article  PubMed  CAS  Google Scholar 

  2. Braunagel SC, Russell WK, Rosas-Acosta G, Russell DH, Summers MD (2003) Determination of the protein composition of the occlusion-derived virus of Autographa californica nucleopolyhedrovirus. Proc Natl Acad Sci USA 100:9797–9802

    Article  PubMed  CAS  Google Scholar 

  3. Fang M, Nie Y, Harris S, Erlandson MA, Theilmann DA (2009) Autographa californica multiple nucleopolyhedrovirus core gene ac96 encodes a per Os infectivity factor (PIF-4). J Virol 83:12569–12578

    Article  PubMed  CAS  Google Scholar 

  4. Fang MG, Nie YC, Theilmann DA (2009) Deletion of the AcMNPV core gene ac109 results in budded virions that are non-infectious. Virology 389:66–74

    Article  PubMed  CAS  Google Scholar 

  5. Garrod DR, Merritt AJ, Nie Z (2002) Desmosomal adhesion: structural basis, molecular mechanism and regulation (Review). Mol Membr Biol 19:81–94

    Article  PubMed  CAS  Google Scholar 

  6. Ge JQ, Yang ZN, Tang XD, Xu HJ, Hong J, Chen JG, Zhang CX (2008) Characterization of a nucleopolyhedrovirus with a deletion of the baculovirus core gene Bm67. J Gen Virol 89:766–774

    Article  PubMed  CAS  Google Scholar 

  7. Getsios S, Huen AC, Green KJ (2004) Working out the strength and flexibility of desmosomes. Nat Rev Mol Cell Biol 5:271–281

    Article  PubMed  CAS  Google Scholar 

  8. Gomi S, Majima K, Maeda S (1999) Sequence analysis of the genome of Bombyx mori nucleopolyhedrovirus. J Gen Virol 80(Pt 5):1323–1337

    PubMed  CAS  Google Scholar 

  9. Green KJ, Gaudry CA (2000) Are desmosomes more than tethers for intermediate filaments? Nat Rev Mol Cell Biol 1:208–216

    Article  PubMed  CAS  Google Scholar 

  10. Herniou EA, Jehle JA (2007) Baculovirus phylogeny and evolution. Curr Drug Targets 8:1043–1050

    Article  PubMed  CAS  Google Scholar 

  11. Jehle JA, Blissard GW, Bonning BC, Cory JS, Herniou EA, Rohrmann GF, Theilmann DA, Thiem SM, Vlak JM (2006) On the classification and nomenclature of baculoviruses: a proposal for revision. Arch Virol 151:1257–1266

    Article  PubMed  CAS  Google Scholar 

  12. Jiang SS, Chang IS, Huang LW, Chen PC, Wen CC, Liu SC, Chien LC, Lin CY, Hsiung CA, Juang JL (2006) Temporal transcription program of recombinant Autographa californica multiple nucleopolyhedrosis virus. J Virol 80:8989–8999

    Article  PubMed  CAS  Google Scholar 

  13. Ke JH, Wang JW, Deng RQ, Wang XZ (2008) Autographa californica multiple nucleopolyhedrovirus ac66 is required for the efficient egress of nucleocapsids from the nucleus, general synthesis of preoccluded virions and occlusion body formation. Virology 374:421–431

    Article  PubMed  CAS  Google Scholar 

  14. Li G, Wang J, Deng R, Wang X (2008) Characterization of AcMNPV with a deletion of ac68 gene. Virus Genes 37:119–127

    Article  PubMed  Google Scholar 

  15. Lin GY, Blissard GW (2002) Analysis of an Autographa californica multicapsid nucleopolyhedrovirus lef-6-null virus: LEF-6 is not essential for viral replication but appears to accelerate late gene transcription. J Virol 76:5503–5514

    Article  PubMed  CAS  Google Scholar 

  16. Lin GY, Blissard GW (2002) Analysis of an Autographa californica nucleopolyhedrovirus lef-11 knockout: LEF-11 is essential for viral DNA replication. J Virol 76:2770–2779

    Article  PubMed  CAS  Google Scholar 

  17. Liu X, Chen K, Cai K, Yao Q (2008) Determination of protein composition and host-derived proteins of Bombyx mori nucleopolyhedrovirus by 2-dimensional electrophoresis and mass spectrometry. Intervirology 51:369–376

    PubMed  CAS  Google Scholar 

  18. Maeda S (1989) Gene transfer vector of a baculovirus, Bombyx mori, and their use for expression of foreign genes in insect cells. In: Mitsuhashi J (ed) In invertebrate cell system applications. CRC Press, Boca Raton, pp 167–181

    Google Scholar 

  19. McMillan JR, Shimizu H (2001) Desmosomes: structure and function in normal and diseased epidermis. J Dermatol 28:291–298

    PubMed  CAS  Google Scholar 

  20. Meima R, Lidstrom ME (2000) Characterization of the minimal replicon of a cryptic Deinococcus radiodurans SARK plasmid and development of versatile Escherichia coli-D. radiodurans shuttle vectors. Appl Environ Microbiol 66:3856–3867

    Article  PubMed  CAS  Google Scholar 

  21. Miller LK (ed) (1997) The baculoviruses. Plenum Press, New York

    Google Scholar 

  22. Nicholas KB, Nicholas HJ, Deerfiels DW (1997) GeneDoc: analysis and visualization of genetic variation. EMBnet News 4:1–4

    Google Scholar 

  23. Nie Y, Theilmann DA (2010) Deletion of AcMNPV AC16 and AC17 results in delayed viral gene expression in budded virus infected cells but not transfected cells. Virology 404:168–179

    Article  PubMed  CAS  Google Scholar 

  24. O’Reilly DR, Miller LK, Luckow VA (1994) Baculovirus expression vectors : a laboratory manual. Oxford University Press, New York, Oxford

    Google Scholar 

  25. Shen H, Chen K, Yao Q, Zhou Y (2009) Characterization of the Bm61 of the Bombyx mori nucleopolyhedrovirus. Curr Microbiol 59:65–70

    Article  PubMed  CAS  Google Scholar 

  26. Sonnenberg A, Liem RK (2007) Plakins in development and disease. Exp Cell Res 313:2189–2203

    Article  PubMed  CAS  Google Scholar 

  27. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  28. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  Google Scholar 

  29. van Oers MM, Vlak JM (2007) Baculovirus genomics. Curr Drug Targets 8:1051–1068

    Article  PubMed  Google Scholar 

  30. Vasioukhin V, Bowers E, Bauer C, Degenstein L, Fuchs E (2001) Desmoplakin is essential in epidermal sheet formation. Nat Cell Biol 3:1076–1085

    Article  PubMed  CAS  Google Scholar 

  31. Wang RR, Deng F, Hou DH, Zhao Y, Guo L, Wang HL, Hu ZH (2010) Proteomics of the autographa Californica nucleopolyhedrovirus budded virions. J Virol 84:7233–7242

    Article  PubMed  CAS  Google Scholar 

  32. Xu HJ, Yang ZN, Wang F, Zhang CX (2006) Bombyx mori nucleopolyhedrovirus ORF79 encodes a 28-kDa structural protein of the ODV envelope. Arch Virol 151:681–695

    Article  PubMed  CAS  Google Scholar 

  33. Xu HJ, Yang ZN, Zhao JF, Tian CH, Ge JO, Tang XD, Bao YY, Zhang CX (2008) Bombyx mori nucleopolyhedrovirus ORF56 encodes an occlusion-derived virus protein and is not essential for budded virus production. J Gen Virol 89:1212–1219

    Article  PubMed  CAS  Google Scholar 

  34. Yang ZN, Xu HJ, Thiem SM, Xu YP, Ge JQ, Tang XD, Tian CH, Zhang CX (2009) Bombyx mori nucleopolyhedrovirus ORF9 is a gene involved in the budded virus production and infectivity. J Gen Virol 90:162–169

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (31070136, 30271008) and the National Basic Research Program of China (2010CB126205).

Author information

Authors and Affiliations

  1. Ministry of Agriculture Key Laboratory of Agricultural Entomology, Institute of Insect Science, Zhejiang University, Yuhangtang Road 866, Hangzhou, 310058, Zhejiang, China

    Min-Juan Zhang, Cai-Hong Tian, Xiao-Ying Fan, Yi-Han Lou, Ruo-Lin Cheng & Chuan-Xi Zhang

Authors
  1. Min-Juan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cai-Hong Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiao-Ying Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yi-Han Lou
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ruo-Lin Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chuan-Xi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chuan-Xi Zhang.

Additional information

M.-J. Zhang and C.-H. Tian contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhang, MJ., Tian, CH., Fan, XY. et al. Bombyx mori nucleopolyhedrovirus ORF54, a viral desmoplakin gene, is associated with the infectivity of budded virions. Arch Virol 157, 1241–1251 (2012). https://doi.org/10.1007/s00705-012-1276-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-012-1276-0

Keywords

Search

Navigation